Compendium of Grape Diseases, Disorders, and Pests, Second Edition

W. F. Wilcox, W. D. Gubler, and J. K. Uyemoto, eds.

Copyright © 2015 The American Phytopathological Society. All rights reserved.
ISBN: 978-0-89054-481-5

Part I. Diseases Caused by Biotic Factors

Diseases Caused by Fungi and Oomycetes
Anthracnose of the shoots (Fig. 18). Individual lesions may coalesce, caus-
ing affected shoots to blight. Infected areas may crack, causing
the shoots to become brittle. Affected shoots typically remain
Anthracnose, also known as black spot, bird’s-­eye rot, and stunted in growth. Small, pink masses of spores may appear
bird’s-­eye spot, is a disease of European origin that is now in the lesions during humid weather or following incubation
found in most grape-­growing regions of the world. When un- of suspect tissues under warm, humid conditions. Following
controlled, anthracnose can reduce fruit quality and yield, and severe attacks, the disease causes deterioration of older canes,
weaken the vine via significant destruction of new shoots and
leaves. It was probably introduced into other parts of the world
on vines imported from Europe, where it was among the most
serious disease problems before the introduction of powdery
and downy mildews. Most Vitis species are susceptible to an-
thracnose. It was first detected in the United States in the mid-­
1800s and quickly became a significant disease in the warm
and humid southeastern regions of the country, where weather
conditions during much of the growing season are conducive
for its development. In humid grape-­growing regions of South
and Southeast Asia, anthracnose is well established, making
some grape cultivars extremely difficult to grow. In the ab-
sence of adequate control programs, it can also cause damage
on highly susceptible cultivars following early-­season rains in
otherwise dry climates such as the grape-­growing regions of
southern Australia.
Once established in vineyards, anthracnose can be very de-
structive and difficult to manage. However, the overall inci-
dence and severity of anthracnose in European vineyards has
now been reduced to a negligible level, owing to the widespread
use of fungicides such as copper compounds, dithiocarbamates,
and phthalimides to control downy mildew and other diseases. Fig. 17. Early development of anthracnose on internodes, peti-
In addition to the regular use of such fungicides, the disease is oles, and leaves. (Cour­tesy M. White)
also limited by the general lack of rainfall throughout much
of the growing season in the Mediterranean to arid climates
where many of the world’s grapes are cultivated. In the humid
climate of eastern North America, anthracnose is sometimes
problematic on certain highly susceptible interspecific hybrid
cultivars, which typically receive only modest fungicide pro-
grams to control other diseases. Such outbreaks are most severe
in the warm southeastern and lower midwestern portions of the
United States, but also occur sporadically in more northerly re-
gions, especially in years with high rainfall.

Symptoms
Anthracnose, which literally means “like coal” in reference
to blackening of affected tissues, attacks the aerial, succulent
parts of the vine, including young shoots, leaves, petioles, ten-
drils, and clusters; however, lesions on shoots and berries are
most common and distinctive.
The first symptoms on young shoots appear as isolated,
small, reddish, circular spots that enlarge to become brownish,
sunken lesions with gray centers and dark, round or angular
margins (Fig. 17). A slightly raised area may form around the Fig. 18. Anthracnose lesions extending into the pith on a develop-
margins of the lesions, whose centers may extend to the pith ing shoot. (Cour­tesy W. F. Wilcox)

17
resulting in reduced yield. Anthracnose lesions on shoots may isolates of the anamorph G. ampelophagum. Perithecia con-
be confused with hail injury; however, unlike hail damage, taining asci and ascospores may also form on infected canes
the edges of the lesions caused by the anthracnose fungus are and berries left on the ground or in the trellis from the previous
raised and dark brown. In addition, hail damage usually ap- year. Asci (80–100 × 11–23 µm) are formed in pyriform locules
pears on only one side of the shoot, whereas anthracnose le- of ascostromata and each ascus contains eight brown to black,
sions are more generally distributed. Symptoms on petioles and four-­celled ascospores (29–35 × 4.5–7 µm).
tendrils develop similarly to those on shoots. Diseases caused by Colletotrichum spp. on many other crops
On leaves, numerous small (1–5 mm in diameter), circular, are given the common name “anthracnose.” This potentially am-
brown spots appear, which later turn gray in their centers and biguous situation has sometimes resulted in grapevine diseases
develop dark-­brown to black margins. Older lesions may have caused by Colletotrichum spp. being referenced as “anthracnose”
round or angular edges and the necrotic centers usually drop in the literature, especially in Asia, rather than as “ripe rot,” the
out, creating a “shot-­hole” and tattered appearance (Fig. 19). accepted common name of the disease caused by these patho-
Lesions may cover the entire blade or appear mainly along the gens. On grapevines in India and the Philippines, for example,
veins. In severe attacks, lesions may coalesce and cause distor- the C. gloeosporioides state of Glomerella cingulata (Stonem.)
tion of the leaf blade and eventually death of the entire leaf. Spauld. & Schrenk can cause light-­brown, irregularly scattered
Young leaves are more susceptible to infection than older leaves. spots with ashy gray centers, mostly on older leaves and weaker
When the veins are affected, especially on young leaves, the le- canes during the rainy season. In addition to being less virulent
sions prevent normal development and result in malformation than G. ampelophagum, C. gloeosporioides is also distinguished
or complete drying of the leaves; this is most obvious at the tips by the much larger conidia (12–21 × 3.5–6 µm) relative to those
of the shoots, giving them a burned appearance. of the former fungus, and the distinctly different symptoms that
Infection may also occur on clusters before flowering. The it causes on infected fruit (see Ripe Rot chapter).
rachis and pedicels develop lesions similar to those on shoots
and petioles. If the rachis is girdled, the distal portion of the Disease Cycle and Epidemiology
cluster shrivels and dries. On berries, small, reddish-­brown, Infected canes are the main source of pathogen survival be-
circular spots develop initially, which then enlarge to an av- tween seasons. Sclerotia or mycelium surviving in cane lesions
erage diameter of approximately 5–7 mm and may become become active in spring and produce abundant conidia when
slightly sunken. The centers of the spots turn whitish gray and they are wet with rain or dew for 24 h or more at temperatures
are surrounded by reddish-­brown to black margins, produc- above 2°C. These conidia are then splashed by rain (2 mm or
ing an appearance that sometimes resembles a bird’s eye (Fig. more) to new growing tissues, where they germinate and cause
20). During prolonged wet weather, a pinkish mass of fungal primary infection at temperatures from 2 to 32°C if tissues re-
spores oozes from the fruiting bodies (acervuli) that develop main wet for a sufficient length of time. Warm weather reduces
in these lesions. Lesions on berries may extend into the pulp, both the wetting time needed for initial infections to occur and
which induces cracking and facilitates infection by secondary the subsequent incubation period prior to symptom expression.
microorganisms, resulting in sour rot and poor juice quality. Optimum spore germination occurs at 25–30°C, with a mini-
Sometimes, the severely affected berries shrivel and dry into mum of 3–4 h of leaf wetness required for infection; the incuba-
mummies, retaining the outlines of the original spots. tion period is also shortest within this temperature range (3–4
days under ideally wet conditions). By contrast, after infection
Causal Organism at an incubation temperature of 10°C, disease symptoms do not
Grape anthracnose is caused by the ascomycete Elsinöe am- start developing until approximately 14 days. Conidia or asco-
pelina (de Bary) Shear (syn. E. viticola Raciborski). De Bary spores formed on infected berries that overwinter on the vine or
reported the disease for the first time in 1874 and named the vineyard floor also may cause primary infections.
causal fungus Sphaceloma ampelinum, giving the description
of its conidial form. Changes in the anamorphic name to Ram-
ularia ampelophaga Pass. and Gloeosporium ampelophagum
(Pass.) Sacc. were proposed 2 and 4 years later, respectively.
The fungus produces acervuli on the exterior of lesions.
Acervuli contain short, cylindrical, crowded conidiophores
bearing small, ovoid, hyaline conidia (3–7 × 2–4 µm) with mu-
cilaginous walls and one or two refringent spots. Morphologi-
cal and pathological variability has been found to exist among

Fig. 20. Anthracnose lesions on green

Fig. 19. Foliar anthracnose symptoms, including individual and berries exhibiting classical “birds-­eye” ap-
coalescing lesions and shot-­holing. (Cour­tesy W. F. Wilcox) pearance. (Cour­tesy M. White)

18
 Spores infect new leaves, shoots, tendrils, and young berries, Where disease pressure warrants it, foliar applications of fun-
producing lesions upon which acervuli form and produce abun- gicides are recommended at 7- to 14-­day intervals from the time
dant conidia during periods of humid weather. These conidia that shoots are 5–10 cm long until the berries are half grown,
serve as secondary inoculum and are responsible for further depending on the occurrence of potential infection events initi-
spread of the disease during the growing season. The mucilagi- ated by rainfall or sprinkler irrigation. Many of the fungicides
nous conidia are dislodged from the acervuli by raindrops and used in management programs for other diseases during this
are dispersed in the splashed droplets. Although most of these period also are effective in controlling anthracnose. Bordeaux
travel relatively short distances, conidia have been detected in mixture and copper oxychloride are the traditional fungicides
windborne droplets up to 7 m away from the source. The disease used to protect against anthracnose, but these have gradually
develops intensely as plant growth begins, but in the latter half been replaced by organic fungicides that provide good preven-
of summer, spread is often stopped by dry weather, depending tive action against E. ampelina, including mancozeb, chloro-
on region and year. On the Indian subcontinent, maximum dis- thalonil, dithianon, propineb, ziram, daconil, captan, folpet,
ease development and spread occurs during the monsoon sea- dichlofluanid, and fluazinam. Locally systemic fungicides,
son, when weather conditions become most conducive. such as carbendazim, thiophanate methyl, and some triazole
Epidemic development of anthracnose is governed by sus- compounds used against powdery mildew and other diseases,
ceptibility of the grapevine tissue, dispersal of conidia, and can control anthracnose more effectively than the contact fun-
prevailing weather conditions. The most important factor in gicides. However, following repeated use, the fungus can de-
determining the severity of epidemics is the frequency of rainy velop resistance to these materials because of their specificity
periods. Long dry intervals between rainy periods enable the in mode of action; therefore, applications of such materials
plant to escape infection, and once foliage and fruit attain ma- should be alternated with multisite, nonsystemic fungicides.
turity, they are less susceptible to the disease. Berries become
highly resistant about 50 days after anthesis, when soluble sol- Selected References
ids rise above 5–7%.
Brook, P. J. 1973. Epidemiology of grapevine anthracnose, caused by
Management Elsinoe ampelina. N. Z. J. Agric. Res. 16:332-­342.
Primary inoculum comes almost entirely from within the Kumar, S., Thind, T. S., and Mohan, C. 1995. Morphogenic and patho-
vineyard (infected canes and fallen mummified berries), so genic variations in Gloeosporium ampelophagum. Indian Phyto-
sanitation measures to reduce these sources are very important pathol. 48:331-­334.
and influential. Diseased canes should be pruned during the Magarey, R. D., Coffey, B. E., and Emmett, R. W. 1993. Anthracnose
dormant season and removed from the vineyard or destroyed. of grapevines, a review. Plant Prot. Q. 8:106-­110.
If numerous infected berries remain on the vineyard floor, the Magarey, R. D., Emmett, R. W., Magarey, P. A., and Franz, P. R. 1993.
spores originating from them can be largely negated by cov- Evaluation of control of grapevine anthracnose caused by Elsinoe
ampelina by pre-­ infection fungicides. Australas. Plant Pathol.
ering the berries with soil through cultivation or, if practical, 22:48-­52.
covering them with mulch. Quimio, T. H., and Quimio, A. J. 1975. Notes on Philippine grape and
Grape cultivars vary considerably in their susceptibility to an- guava anthracnose. Plant Dis. Rep. 59:221-­224.
thracnose, and the disease is a consistent threat or problem pri- Shear, C. L. 1929. The life history of Sphaceloma ampelinum de Bary.
marily on cultivars that show the greatest level of susceptibility, Phytopathology 19:673-­679.
including Thompson Seedless (Sultanina), Cardinal, Delicia, Sivanesan, A., and Critchett, C. 1974. Elsinöe ampelina. Descriptions
Italia, Citronella, and Queen of the Vineyards. In eastern North of Pathogenic Fungi and Bacteria, no. 439. C.A.B. International
America, the interspecific hybrid cultivar Vidal Blanc and sev- Mycological Institute, Kew, England.
eral minor seedless table grape varieties (especially Reliance) Sutton, B. C., and Pollack, F. G. 1973. Gloeosporium cercocarpi and
traditionally have been most affected. Several cold-­tolerant hy- Sphaceloma cercocarpi. Mycologia 65:1125-­1134.
brid cultivars derived from V.  riparia (especially Marquette)
also have been problematic. Highly susceptible cultivars should (Prepared by T. S. Thind)
be avoided in heavy soils with poor drainage, as such sites are
particularly conducive to the development of this disease.
As with most fungal diseases, canopy management also helps
in anthracnose control. Shoots likely to trail near the ground Armillaria Root Rot
should be removed and those remaining properly trained to fa-
cilitate air circulation and spray penetration. Because natural Armillaria root rot is a fatal disease of grapevines reported
dispersal of the pathogen is limited, exclusion should be the first from California, the southeastern United States, Europe, South
line of defense, and new vineyards (particularly those of highly America, and Australia. The common occurrence of Armil-
susceptible cultivars) should be established with vines from laria root rot on grapevines and orchard trees planted on sites
nurseries known to be free of anthracnose. Removal of wild previously inhabited by Quercus species (oaks) in California
grapes in hedgerows or wooded areas immediately adjacent to has been noted since the disease was first described in the
vineyards may also help in reducing sources of initial infection. 1880s, and has sometimes resulted in the common name “oak
Fungicide applications targeted against anthracnose are root rot.”
recommended where the disease is established in commercial
vineyards. Late-­ dormant-­season sprays (shortly before bud Symptoms
break) of DNOC preparations, lime sulfur, ferrous sulfate, or The pathogen infects grapevine roots and the root crown re-
copper-­containing products are applied in some viticultural gion, killing the cambium and decaying underlying xylem tis-
regions to inhibit sclerotial germination and the production of sue. The resulting symptoms include stunted shoots, dwarfed
primary conidial masses from the cankers of diseased canes leaves, wilting, premature defoliation, and shriveling of berries
retained after dormant pruning. In the lower midwestern region (Fig. 21). The most common course of symptom development
of the United States, such a “delayed dormant” application of is a gradual, multiyear reduction in pruning weight and yield
lime sulfur is considered a critical component of anthracnose caused by destruction of the root system’s vasculature. Less
management programs in vineyards where the disease has be- common is a rapid desiccation of leaves and berries followed by
come established. However, this material must be used with vine death, occurring between veraison and harvest on grape-
caution as it is caustic and can cause vine damage if applied vines previously exhibiting moderate symptoms. Grapevines
after bud break. with severely stunted shoots that do not succumb to Armillaria

19
root rot before harvest usually die during the dormant season ing mycelial fans and also may grow on the surface of infected
or soon after budbreak. The disease typically develops in local- roots.
ized, circular sections of the vineyard (disease centers). These Clusters of Armillaria basidiocarps (mushrooms) may form
disease centers appear to expand radially over time and typi- at or near the base of infected grapevines during the rainy sea-
cally include a combination of dead, symptomatic, and healthy son. However, the basidiocarps are not a reliable diagnostic
vines. feature as they may not form every year and they decompose
For diagnostic purposes, subterranean signs of the patho- within 2 weeks of emergence. Furthermore, basidiocarps of
gen are much more indicative of Armillaria root rot than are Armillaria spp. are not distinctive and, to the untrained eye,
aerial symptoms of the disease. Armillaria spp. form thick, resemble mushrooms of a number of other fungi.
white mats of vegetative fungal tissue (mycelial fans) beneath
the bark of infected roots (Fig. 22). Armillaria root rot may be Causal Organism
diagnosed in a vineyard by digging approximately 30 cm below Several Armillaria species are native to California and to
the soil line to expose the base of the vine trunk where the main other parts of western North America, but of these, only A. mel-
roots originate (the root collar). The bark is then removed with lea (Vahl:Fr.) P. Kumm. kills grapevines. The pathogen, which
a knife, and the inner surface of the bark pieces and subtending also is the cause of Armillaria root rot on grape in continen-
portion of the woody root collar are examined for the presence tal Europe, has a broad host range, infecting over 500 species
of mycelial fans. Wood beneath a mycelial fan may be rotted of woody plants. It produces mushroom fruiting bodies that
and, thus, very easy to cut through. It is most useful to examine are light yellowish brown, resulting in their common name of
the root collars of dead and severely symptomatic grapevines, “honey mushrooms” (Fig. 24). Caps are slightly darker in their
as the mycelial fans are closer to the soil surface than on grape-
vines with only slightly stunted shoots.
Armillaria spp. also form rhizomorphs, which are black,
shoestringlike structures containing mycelium (Fig. 23). Rhi-
zomorphs are occasionally found within the root bark cover-

Fig. 21. Foliar symptoms of Armillaria root rot. Shoots on the dis-
eased vine in the foreground are severely stunted, without fruit, and Fig. 23. Shoestring-­like rhizomorph of Armillaria
in a premature state of senescence. (Cour­tesy K. Baumgartner) mellea (arrows) beneath the bark of an infected
grapevine. (Cour­tesy K. Baumgartner)

Fig. 22. Mycelial fans of Armillaria mellea on the underside of the

bark (left and at center) and contacting surface of the wood (right), Fig. 24. A cluster of Armillaria mellea basidiocarps arising
from a segment of the trunk base (root collar) that was removed from the roots and root crown of an infected vine. (Cour­tesy
below the soil line. (Cour­tesy K. Baumgartner) K. Baumgartner)

20
centers, ranging broadly in size from approximately 3 to 28 cm the cambial tissue is destroyed, the fungi decay the underlying
in diameter. Scales are sometimes present on the cap. Gills are woody root tissue by decomposing cellulose and other cell wall
pale yellow to pink. Stipes are pale yellow to pink at the top components. Grapevines eventually succumb to the disease
and light yellowish brown at the base, usually have a fleshy, after the rot expands to girdle approximately 50% of the root
pale-­yellow to pink annulus, and range from 5 to 20 cm long collar and the remaining functional vascular tissue can no lon-
and 0.5 to 3 cm thick. Clusters of A. mellea may contain up to ger accommodate the demand for water from the shoots. Foliar
50 mushrooms, although this number can be highly variable. symptoms soon follow. The presence of a mycelial fan at the
The hyaline, cylindric basidiospores are white in mass and are root collar signifies that an Armillaria sp. has destroyed some
sometimes deposited by the tallest mushrooms onto the caps of of the underlying cambium and is in the process of girdling the
shorter ones beneath them. host’s trunk.
Reports of Armillaria root rot on grapevines outside western
North America and Europe include symptom descriptions iden- Management
tical to those caused by A. mellea, although different Armil- Once established in a planting, Armillaria root rot is relatively
laria species sometimes are identified as causal agents. In the unaffected by conventional pesticide applications, including
southeastern United States and the U.K., grapevine infections postplant soil fumigation and trunk injections with fungicides.
have been associated with A. tabescens (Scop.) Emel. In Aus- Because of the pathogens’ broad host range, replanting infected
tralia, the disease reportedly is caused by A. luteobubalina sites with another fruit crop is unlikely to eliminate an Armil-
Watling & Kile and, possibly, A. novae-­zealandiae (G. Stev.) laria root rot problem completely. Therefore, the best controls
Herink. Based on current knowledge of Armillaria species in are preventive measures. Rhizomorph growth and growth of
the Southern Hemisphere, A. novae-­zealandiae appears to be mycelium through living roots were once thought to be the two
the likely causal species in South America. However, the pres- main modes of infection and disease spread; however, such as-
ent unresolved taxonomy of Southern Hemisphere Armillaria sumptions originated from studies of Armillaria root rot in for-
species complicates interpretation of disease reports from these est stands, and newer research has shown them to be inaccurate
regions. in vineyards. Vineyard disease incidence is best minimized
The basidiocarps of the aforementioned species are very by removing residual roots before planting, not by preventing
similar in size, shape, and color to those of A. mellea, with the postplant dispersal of rhizomorphs. When clearing an orchard,
exception of A. tabescens, which has no annulus. Because dif- vineyard, or wooded site prior to planting a new vineyard, fo-
ferences in morphological features are relatively minor among liar symptoms (most obvious just before harvest) and disease
individual Armillaria species (e.g., basidiospore length), identi- centers should be looked for, and the root collars of dead and
fication to the species level is most accurate when the DNA se- dying plants should be examined for mycelial fans. Residual
quences of field collections are compared with those of known roots should be removed after clearing the site, with particular
species. However, regardless of the particular Armillaria spe- attention paid to any identified disease centers. General removal
cies involved, disease symptoms, development, epidemiology, of residual roots is recommended, especially for sites cleared
and control are the same. of forest trees, as mycelial fans on the root collars of forest
Armillaria spp. are cultured easily from mycelial fans, decayed versus fruit trees are more difficult to locate and more likely
wood, surface-­sterilized rhizomorphs, or the stipes of mush- to escape detection. Deep-­ripping the soil in several directions
rooms by the use of water agar amended with a benzimidazole brings large residual roots to the surface where they should be
fungicide and streptomycin. Armillaria mycelium cultured from collected and removed from the site. Although it is not possible
these sources is distinguished from other basidiomycete fungi by to remove all residual roots, simply moving them closer to the
the absence of clamp connections. In culture, Armillaria spp. do soil surface, where conditions are hotter and drier, lowers the
not produce spores or any other reproductive structures. probability of Armillaria spp. survival. In some regions, soil
solarization may achieve high soil temperatures quickly, but
Disease Cycle and Epidemiology its beneficial effects are restricted to small-­diameter roots at a
Armillaria species differ slightly in their host range and very shallow soil depth.
fruiting-­body morphology, but they share the same life cycle Preplant soil fumigation with materials such as methyl bro-
and infection cycle. The pathogen’s vegetative mycelium can mide and sodium tetrathiocarbonate may improve control of
survive for several years in the partially decayed, woody roots Armillaria root rot if the soil is properly prepared beforehand.
of a previously infected host that have remained in the soil after Preplant soil fumigation is effective when adequate fumigant
land clearing (residual roots). Following vineyard establish- reaches the majority of residual roots, but the soil depth to
ment, infection can occur when any woody part of a grapevine’s which the fumigant penetrates is significantly diminished by
root system comes into direct contact with Armillaria spp. my- soil moisture and various edaphic properties such as low po-
celium from residual roots. Once infected, woody grapevine rosity and high organic matter content. In desert and Mediter-
roots (whether still living or dead) serve as an additional source ranean climates, depth of penetration is improved significantly
of inoculum for replants and, to a lesser extent, for secondary by fumigating at the driest time of the season and by tarping
spread to neighboring vines. Disease centers appear to expand after application of the material. Soil moisture should be de-
radially over time, but the capacity for subterranean expansion pleted further by planting a vigorous cover crop such as Sor-
of A. mellea via rhizomorphs is extremely limited because of ghum vulgare Pers. (sudangrass) several months before the dry
their infrequent occurrence and limited length. Instead, the season begins. Injecting sodium tetrathiocarbonate into the soil
apparent expansion of disease centers is due to a succession is more effective than surface application, but neither approach
of primary infections. Vines planted within zones containing is as effective as applying methyl bromide followed by tarping.
the highest inoculum densities become infected first, followed The success of a curative treatment depends on the degree of
by adjacent vines in soil volumes with lower inoculum densi- damage already present in addition to the treatment’s ability to
ties. Although Armillaria spp. mushrooms release windblown decrease further colonization of healthy root tissue by Armil-
spores, they are not a significant source of disease spread laria spp. Therefore, curative treatments are recommended
among horticultural crops hosts. only for slightly to moderately symptomatic vines. One such
Once Armillaria spp. encounter a root, they secrete lytic en- treatment is root collar excavation, involving permanent re-
zymes that dissolve the root bark. Beneath the bark, Armillaria moval of soil from the base of the vine in an effort to protect
spp. colonize and kill a small section of vascular cambium, this critical portion of the plant from further pathogen coloni-
then form a mycelial fan. The mycelial fan expands beneath zation (Fig. 25). This causes the mycelial fan at the root collar
the root bark, colonizing and killing more cambial tissue. After to recede, thereby preventing further girdling of the trunk, and

21
 cluster, causing bunch rots. Some organisms cause storage and
transit rots that, although initiated primarily in the vineyard,
develop after harvest.
Annual losses to berry rots are typically 3–5% but in unfa-
vorable seasons may range from 15 to 80%. With few excep-
tions, rotting berries are not suitable for making wine or other
products such as vinegar because they impart odd and distaste-
ful flavors.
Various species of fungi, including yeasts, and some bacteria
contribute to the rotting of berries. Some 70 species of fungi in
30 genera and a few bacteria, including acetic acid-­producing
species (see Sour Rot), have been found on berries, and many of
these organisms are directly or indirectly involved in rot. Some
infect green berries, but infections do not necessarily advance
into rot. Others produce unsightly spots or scars on green ber-
ries, and still others become latent and later advance into rot
as berries mature. However, many of these 70 species of fungi
seem to be transient, occurring in abundance at specific times
Fig. 25. Root collar excavation for control of Armillaria root rot. but not necessarily building up and continuing to spread.
(Cour ­tesy K. Baumgartner) In general, the fruit-­rotting organisms may be divided into
two major groups: those that infect berries directly, or “pri-
mary invaders”; and those that enter berries through wounds
has improved yields on moderately symptomatic vines relative or follow a primary invader, known as “wound and secondary
to their untreated counterparts. invaders.” Wounds commonly found on berries are cracks in
Severity of Armillaria root rot is exacerbated by wet soil the skin caused by internal pressure associated with rain or by
conditions. Therefore, in vineyards where drip irrigation is diseases such as powdery mildew and black measles. Hail, bird
practiced, dripline emitters should be moved away from the pecks, and insect feeding also cause wounds that permit entry
base of the trunk as soon as possible following vineyard estab- of secondary invaders.
lishment. In Mediterranean climates, a relationship has been Evidence of rot problems in vineyards includes the odor of
documented between the imposition of frequent, shallow irri- vinegar, juice dripping over berries of a cluster, the presence of
gations during the dry season and development of Armillaria adults and larvae of the vinegar fly (Drosophila melanogaster
root rot on landscape and orchard trees. The mechanism under- Meigen), soft spots in the skin of berries (“slip-­skin”), and fun-
lying this relationship is not known, but possibilities include a gal fructifications on the surface of berries.
decreased defense response of root crown tissues in the water- Some specific rot diseases are described in the following sub-
logged portion of the soil and/or provision of a more favorable sections under the genus name of the causal organism, which is
environment for mycelial growth in this frequently wet region. commonly used to name a specific rot.
Grape rootstocks exhibit a range of tolerance to infection by Primary invaders. Alternaria rot caused by Alternaria al-
Armillaria spp. infection, and it is likely that resistant rootstocks ternata (Fr.) Keissl. (syn. A. tenuis Nees) often occurs near the
will be recommended for control of Armillaria root rot in the cap stem. The rot area is tan initially and becomes brown with
future. More research is needed to identify sources of resistance. age. Under humid conditions, fluffy gray tufts of mycelium and
conidiophores bearing conidia develop through cracks in the
Selected References brown skin over rot lesions. Infections may occur through the
skin in a small drop of water or at 98–100% relative humidity.
Baumgartner, K. 2004. Root collar excavation for postinfection control Rot at the cap stem may also develop from an infected pedicel.
of Armillaria root disease of grapevine. Plant Dis. 88:1235-­1240. Infections of pedicels occur during most seasons. The fungus
Baumgartner, K., and Rizzo, D. M. 2002. Spread of Armillaria root has been cultured from pedicels from the time of blossom shat-
disease in a California vineyard. Am. J. Enol. Vitic. 53:197-­203. ter to berry maturity.
Baumgartner, K., and Rizzo, D. M. 2006. Relative resistance of grape- Cladosporium rot caused by Cladosporium herbarum
vine rootstocks to Armillaria root disease. Am. J. Enol. Vitic. (Pers.:Fr.) Link is characterized by a well-­defined, black, soft,
57:408-­414. circular area ranging from 5–7 mm in diameter up to as much
Baumgartner, K., and Warnock, A. E. 2006. A soil inoculant inhibits as two-­thirds of a berry. At room temperature in a humid atmo-
Armillaria mellea in vitro and improves productivity of grapevines sphere, the surface of the rot area becomes a velvet olivaceous
with root disease. Plant Dis. 90:439-­444.
color due to the presence of conidiophores and conidia. Clado-
Baumgartner, K., Coetzee, M. P. A., and Hoffmeister, D. 2011. Secrets
of the subterranean pathosystem of Armillaria. Mol. Plant Pathol.
sporium rot is typically a storage disease that develops on fruit
12:515-­534. harvested late in the season after a rain, although it may also
Raabe, R. D. 1962. Host list of the root rot fungus Armillaria mellea. develop in the field under prolonged wet or humid conditions
Hilgardia 33:25-­88. before harvest. Infection takes place through the skin either in
the vineyard or in storage and may occur at temperatures from
(Prepared by K. Baumgartner and D. M. Rizzo) 4 to 30°C (optimum 24–26°C).
Other primary invaders include Botrytis cinerea Pers.; Col-
letotrichum gloeosporioides and C. acutatum J. H. Simmonds;
Diplodia natalensis Pole Evans; Elsinoë ampelina (de Bary)
Miscellaneous Berry Rots Shear; Guignardia bidwellii (Ellis) Viala & Ravaz; Greeneria
uvicola (Berk. & Curt.) Punithalingam; and Phomopsis viticola
and Raisin Molds (Sacc.) Sacc. They are covered elsewhere in this compendium.
Wound and secondary invaders. Aspergillus rot caused by
Berry rots and bunch rots are common viticultural problems Aspergillus niger van Tiegh. is common in warm to hot cli-
the world over. Many rot organisms infect individual berries mates. This rot is usually associated with a wound and is at first
and seldom spread to others in the cluster, whereas other rot tan to brown, but the area is soon covered with a dusty mass
organisms typically spread to many or most of the berries in the of brown or black spores. These rot areas are initially soft but

22
become firm and leathery. Under warm conditions (26–32°C) windblown, carried in dust, spread in rain, or transported on
and in the presence of free water, the fungus may infect mature the feet and mouthparts of insects. These fungi occur in vine-
fruit directly through the skin. yards on mummified berries, dead vine parts, the bark of canes
Blue mold or Penicillium rot caused by Penicillium spp. is and spurs, vineyard debris, and other decaying vegetation.
common in wounded berries (Fig. 26). The fungus produces Species of Alternaria, Cladosporium, and Stemphylium grow
large, dusty masses of blue spores. in bark of 1-­year-­old canes and sporulate there in the spring.
Rhizopus rot is a wet, juicy rot caused by Rhizopus arrhizus These three fungi, like Botrytis and Helminthosporium, grow
Tesher or R. stolonifer (Ehrenb.:Fr.) Lind in warm, humid cli- under humid conditions and sporulate on castoff flower parts
mates. Rotted areas on berries are soft and brown, drip juice, that remain in the cluster.
and under humid conditions may be covered with a cobwebby Berry rots and bunch rots are associated with wetness. They
mycelium. Numerous sporangiophores with small, spherical, are favored by high relative humidity, rain, and sprinkler irriga-
dark sporangia emerge through cracks in the skin of diseased tion during the time berries are maturing and approaching har-
berries or through the borders of a wound. In humid weather vest. In general, the degree of rot development is proportional
the fungus may spread to other berries in a cluster, causing a to the frequency and duration of wetting events. Rots become
bunch rot (Fig. 27). The disease is often abundant in vineyards increasingly abundant each year in a sequence of disease-­
near plum and peach trees with decaying fruit on the ground, conducive seasons but may stop abruptly during one dry sea-
and also near fields of sugar beets. son. Some cultivars are more susceptible to rot than others.
Fruit rots caused by Ascochyta sp., Fusarium moniliforme Control. Several viticultural practices may aid in reducing
Sheldon, Hormiscium sp., Stemphylium botryosum Walker, and rot. Prune to adjust the crop and prevent clumping of clusters.
Torula sp. are indiscrete rots or include a mix of organisms. Rot Thin if necessary to loosen clusters. Clean the vineyard and
caused by Helminthosporium sp. alone appears much like that surrounding area of debris, prunings, and unnecessary vegeta-
caused by Cladosporium herbarum. tion. Adjust time and duration of sprinkler irrigation so that
Alternaria geophila Deszew., Aspergillus niger, R. arrhizus, berries are not kept wet more than 18 h, and do not use sprin-
and R. stolonifer can become primary invaders when provided klers after fruit reach 15°Brix. Keep the vine canopy open so
free water or grape juice in the temperature range of 18–30°C. that fruit is well aerated. Control biological agents that injure
Water on the skin absorbs sugars and amino acids from the fruit, such as the powdery mildew fungus, birds, and insects.
berry and provides a good food base for the pathogens.
Other wound and secondary invaders include fungi such as Raisin Molds and Rots
Aspergillus aculeatus Iizuka, A. flavus Link, A. ochraceous Molds and rots of raisins occur periodically in association
Wilhelm, A. wentii Wehmer, Botryosphaeria dothidea (G. & with wet weather. The amount of mold and rot varies with
P.) Arx & Müller, Candida sp., Chaetomium elatum Kunze, the vineyard, the time of harvest, the district, and the season.
Cladosporium cladosporioides (Fres.) de Vries, C. oxysporium Losses range from 0 to 2% in a normal season and may be as
Berk. & Curt., Monilia sp., Penicillium brevicompactum high as 70% in a rainy season. These diseases reduce produc-
Diercks., P. cyclopium West., P. frequentaus West., P. stolon- tion, increase the cost of making and processing raisins, and re-
iferum Thom, Saccharomyces cerevisiae Kreger-­van Rij, and duce quality. The amount of preharvest berry rot in a vineyard
Sclerotinia sclerotiorum (Lib.) de Bary. grown for raisins is an indication of the potential for mold and
Sour bunch rots, which can vary significantly among geo- rot of raisins while drying.
graphical zones according to climate, are discussed in detail Symptoms. Molds are mostly contaminants. Mold fungi grow
elsewhere in this compendium. on the surface of the raisin, where they produce conidial spore
Disease cycle and epidemiology. Many fruit-­rotting organ- masses. They can be cleaned (brushed or washed) from the sur-
isms are fungi that produce large numbers of spores that are face. Rots are caused by fungi that colonize the inside of the

Fig. 26. Bluish sporulation of Penicillium

spp., the cause of blue mold. (Cour­tesy R. C. Fig. 27. Symptoms and signs of Rhizopus rot.
Pearson) (Cour­tesy R. C. Pearson)

23
berry before harvest or during drying. Fungi growing inside the Harvey, J. M., and Pentzer, W. T. 1960. Market diseases of grapes and
raisin form mats of mycelium and sporulation tufts on the sur- other small fruits. U. S. Dep. Agric. Handb. 189.
face. The internal mycelial mats can be observed after infected Hewitt, W. B. 1974. Rots and bunch rots of grapes. Calif. Agric. Exp.
raisins are soaked in a relatively large volume of warm water or Stn. Bull. 868.
are boiled in water until clear. Raisins with rot are a total loss Martini, L. P. 1966. The mold complex of Napa Valley grapes. Am. J.
because the rot cannot be removed by washing. Enol. Vitic. 17:87-­94.
Nelson, K.  E., and Ough, C.  S. 1966. Chemical and sensory effects
Causal organisms. The same fungi found normally in vine- of microorganisms on grape musts and wine. Am. J. Enol. Vitic.
yards are also found on berries when harvested and laid to dry 17:38-­47.
on trays in the vineyard or on racks or drying pads. Species of
Alternaria, Aspergillus, Botrytis, Chaetomium, Cladosporium, (Prepared by W. B. Hewitt)
Helminthosporiurn, Hormiscium, Hormodendrum, Penicillium,
Rhizopus, and Stemphylium are common raisin mold and rot
fungi.
Disease cycle and epidemiology. At harvest, berries have on Bitter Rot
their skin a representative sample of spores of fungi that occur
naturally in the vineyard. When berries are moistened by dew Bitter rot is a common disease in the southern two-­thirds of
or rain, sugars and amino acids of the berries move into surface the eastern United States, although it sometimes causes prob-
water. Conidia germinate and grow in this surface medium. lems as far north as Long Island and the New England states.
New colonies sporulate after a short period of time, and a new It appears to be relatively widespread internationally in regions
crop of conidia may be blown by wind or splashed by raindrops subject to warm rains during the fruiting season, and has been
to spread the organisms. reported from Australia, Brazil, China, Costa Rica, Greece,
Berries that have rot at the time of harvest and are laid on India, Japan, New Zealand, South Africa, and Taiwan. As rot-
trays to dry also support fungal sporulation. Conidia on these ten fruit begin to soften they have a distinct bitter taste, which
berries are also spread by wind or rain to other berries. Fur- is carried through the winemaking process to give the finished
thermore, when water remains on the surface of berries or on product an unpleasant, burnt or bitter flavor.
drying trays in contact with berries for 24–36 h or more, some
fungi, such as species of Alternaria, Aspergillus, Cladospo- Symptoms
rium, and Rhizopus, penetrate the skin and colonize the inte- The bitter rot pathogen infects all aboveground vegetative
riors of the berries or raisins and cause rot. These fungi may parts of the vine. Leaf infections are more common on musca-
also grow on the paper trays, causing the raisins to stick to the dine grapes (Muscadinia rotundifolia) than bunch grapes and
paper. Rains or showers that keep the fruit wet for periods of appear as tiny, sunken, reddish-­brown flecks with yellow halos.
24–30 h or longer at 15–23°C produce ideal conditions for the Lesions on stems and petioles are round to elliptical, reddish
development of molds and rots. brown to black, and may be slightly raised or sunken. The fun-
Control. Two approaches may be taken to control raisin gus has been reported to cause girdling of the shoots of several
molds and rots: prevention and chemical treatments. Although cultivars of V.  vinifera in Greece. Flecking of the sepals and
molds and rots on raisins generally occur after harvest while blighting of the flower buds can also occur (Fig. 28). Typically,
the fruit are on drying trays in the vineyard, preventive con- the bitter rot fungus first invades the berry from the pedicel
trol begins early in the season and continues through drying (berry stem) after veraison. Diseased regions of light-­skinned
and curing. Chemical control is a late choice and often a futile berries turn brown and form multiple, prominent fruiting bod-
effort. ies of the fungus (acervuli) after the berries have reached full
To prevent preharvest rot in the vineyard, suggested controls size (Fig. 29), causing the epidermises and cuticles to rupture.
for berry and bunch rots should be followed. The crop should Acervuli form in concentric rings as the rot expands through
be adjusted to obtain high levels of soluble solids early in the infected berries, but appear more uniformly distributed once
harvest and drying season to maximize quality and permit fruit are completely rotted (Fig. 30). These symptoms are less
flexibility in choice of harvesting time. Harvest dates should
be chosen in accordance with the best weather forecast for sat-
isfactory drying. Debris can be reduced by cultivating between
vine rows. A good tray base should be prepared by forming soil
to a firm slope faced to receive maximum sun exposure and
good drainage in case of rain. Care should be taken during har-
vest to minimize damage to fruit—that is, by cutting clusters
from the vine and placing them in only one layer on the drying
tray. The fruit should be turned over when they are partially dry
to shorten the drying time.
The effectiveness of a fungicide to prevent mold and rot of
raisins depends on the amount of inoculum, the amount and
degree of damage to berries at harvest, the fungicide used, the
timing and thoroughness of fungicide application, and the du-
ration of the wetting period. Fungicides have given reasonable
protection when applied to the fruit before harvest or to fruit on
drying trays soon after harvest but before rain.

Selected References
Barbe, G. D., and Hewitt, W. B. 1965. The principal fungus in the sum-
mer bunch rot of grapes. Phytopathology 55:815-­816.
Bisiach, M., Minervini, G., and Salomone, M. C. 1982. Recherches ex-
périmentales sur la pourriture acide de la grappe et sur ses rapports
avec la pourriture grise. Bull. OEPP/EPPO Bull. 12:15-­27. Fig. 28. Unopened flowers of muscadine grapes blighted by bitter
Delp, C. J., Hewitt, W. B., and Nelson, K. E. 1951. Cladosporium rot of rot (background leaf lesions are caused by black rot). (Cour­tesy
grapes in storage. (Abstr.) Phytopathology 41:937-­938. C. Fisk)

24
apparent on dark-­skinned berries, which appear roughened and of pink to salmon-­colored spores, whereas those with bitter rot
sometimes iridescent when acervuli develop (Fig. 31). Even- are not.
tually, infected grapes soften and begin to shrivel, becoming
completely covered with massive numbers of acervuli. Infected Causal Organism
berries may abscise, or may dry into mummies and remain Greeneria uvicola (Berk. & M. A. Curtis) Punith. (syn. Mel-
firmly attached to the pedicel. anconium fuligineum (Scribn. & Viala) Cav.), the cause of bitter
Bitter rot is often confused with ripe rot (caused by Colletot­ rot, forms acervuli (varying in diameter up to 250 µm) that are
richum spp.), as both are favored by the same weather condi- separate to confluent and subepidermal, with irregular dehis-
tions and symptoms on ripening fruit can be similar. Unlike cence (Fig. 32). Conidiophores (30 × 3 µm) are hyaline, septate,
ripe rot, fruit with bitter rot are characterized by their promi- and irregularly branched. Conidiogenous cells are enteroblas-
nent masses of acervuli and often leave hands black if they are tic, phialidic, discrete or more frequently integrated, determi-
handled when wet or shortly after damp weather has occurred. nate, cylindrical, tapered to the apexes, hyaline, and smooth;
In contrast, fruit with severe ripe rot infections are often cov- the collarette and channel are minute. Conidia (7.5–10 × 3–4
ered with a slimy mass during moist weather or a dried crust µm) are black, smooth, thin walled, nonseptate, cylindrical,
and fusiform to oval, with truncate base and obtuse apex (Fig.
33). A perfect stage of the organism has not been described.

Disease Cycle and Epidemiology

G. uvicola overwinters as a saprophyte on fallen fruit, cold-­
damaged shoot tips, and necrotic bark of the trunk and cor-
dons. In the spring, gelatinous masses of conidia are exuded

Fig. 29. Bitter rot on white-­skinned grapes. (Cour­

tesy T. B. Sutton) Fig. 31. Bitter rot on dark-­skinned grapes. (Cour­tesy T. B. Sutton)

Fig. 30. Density and distribution of Green­ Fig. 32. Acervuli of the bitter rot fungus (Greeneria
eria uvicola acervuli on grape berries af- uvicola) fruiting on the surface of a grape berry.
fected with bitter rot. (Cour­tesy M. A. Ellis) (Cour­tesy J. R. McGrew)

25
from acervuli and washed by rain to all green parts of the Selected References
vine, including the pedicels. Infection can occur during wet
periods across a temperature range of approximately 12–30°C, Critopolous, P. D. 1961. Girdling of grapevine canes by Melanconium
fuligineum. Phytopathology 51:524-­528.
although temperatures of 22.4–24.6°C and wetness durations
Kummuang, N., Smith, B. J., Diehl, S. V., and Graves, C. H., Jr. 1996.
of 6–12 h are optimal. The need for relatively long and warm Muscadine grape berry rot diseases in Mississippi: Disease identifi-
rains accounts for the predominant occurrence of the disease in cation and incidence. Plant Dis. 80:238-­243.
regions with warm, humid summers. Longland, J. M., and Sutton, T. B. 2008. Factors affecting the infec-
The pathogen invades the pedicels and becomes latent until tion of fruit of Vitis vinifera by the bitter rot pathogen Greeneria
fruit mature. Then, the pathogen resumes growth and moves uvicola. Phytopathology 98:580-­584.
from the infected pedicels into the ripening fruit, causing them Luttrell, E. S. 1953. Melanconium leaf and stem fleck of grapes. Phy-
to rot. Secondary infections occur when conidia from infected topathology 43:347-­348.
berries are rain splashed onto other ripening fruit. Berries Ridings, W. H., and Clayton, C. N. 1970. Melanconium fuligineum and
are susceptible to direct infection from conidia at all times the bitter rot disease of grape. Phytopathology 60:1203-­1211.
between bloom and harvest but are most susceptible near ve- Sutton, B. C., and Gibson, I. A. S. 1977. Greeneria uvicola. Descrip-
raison. Infections often occur in fruit that have been mechani- tions of Pathogenic Fungi and Bacteria, no. 538. Commonwealth
cally wounded by birds, insects, or hail, or is cracked owing Mycological Institute, Kew, Surrey, England.
to heavy rains.
(Prepared by T. B. Sutton)
Management
It is important to remove mummied fruit, pedicels, and
other dead tissues from the vines while pruning to reduce the
inoculum of G. uvicola for the next growing season. Training
Black Foot Disease
systems that minimize the retention of old wood also appear
to help to reduce disease incidence. Fungicide sprays applied First reported in France in 1961, black foot disease occurs
every 2 weeks from just after bloom until harvest are necessary in nearly all major viticulture regions throughout the world. It
to control the disease where it is a common problem, unless primarily affects young vines up to 8 years of age with incur-
rainfall is absent. If late-­season or preharvest sprays are omit- able and almost invariably fatal infections, although older vines
ted, the potential for bitter rot development is greatly increased. occasionally succumb as well. When the disease develops, it
Captan, mancozeb, benzimidazole, and QoI fungicides provide causes substantial economic losses resulting from reduced pro-
good control of bitter rot, whereas copper fungicides appear to ductivity and replanting costs. In California, black foot disease
be relatively ineffective. is most widespread in the North Coast region, perhaps owing to
Grape cultivars vary in susceptibility to this disease within its cooler climate relative to other production regions of the state.
and among species. Bronze muscadine cultivars tend to be more
susceptible than black ones. The V.  aestavalis cultivar Cyn- Symptoms
thiana (Norton) is highly resistant. French-­American hybrids Leaves of infected vines appear chlorotic and scorched as
are generally more resistant than most cultivars of V. vinifera. if by water stress, with the entire vine becoming stunted and
Within V. vinifera, Merlot, Riesling, and Sauvignon Blanc are often dying. In cross section, the base of the trunk appears
moderately resistant; Cabernet Sauvignon, Cabernet Franc, and necrotic and xylem vessels are plugged with black inclusions
Tempranillo are slightly susceptible; Chardonnay, Sangiovese, and tyloses, reminiscent of those associated with Petri Dis-
Syrah, and Viognier are moderately susceptible; and Mourvé- ease (Phaeomoniella chlamydospora, Phaeoacremonium spp.).
dre and Petit Verdot are highly susceptible. Roots of symptomatic vines show black, sunken, necrotic le-
sions (Fig. 34). Often, the root system appears normal, i.e., it

Fig. 33. Acervulus (top), conidia (bottom left), and conidiophores

(bottom right and center) of Greeneria uvicola. (Reproduced, by Fig. 34. Sunken root lesion associated with
permission, from Sutton and Gibson, 1977) black foot disease. (Cour­tesy E. Petit)

26
is well spread but frequently shallow, developing parallel to contain eight smooth and hyaline ellipsoidal ascospores, 8–16
the ground. Sometimes, an adventitious root system develops × 2.2–4.4 µm, each with a single septum.
from the rootstock portion of the trunk close to the soil surface, C. macrodidymum produces microconidia and mostly trisep-
and this can support the young plant for a while if the primary tate macroconidia (31–41 × 6–8 µm), predominantly straight
root system fails. When symptomatic vines are removed from and minutely widening toward the tip, with an apical cell
the ground, their root systems sometimes present a so-­called slightly bent to one side (Fig. 36). C. macrodidymum does not
“J-­root” configuration, typically the result of the bottom por- always produce chlamydospores. Its sexual stage, Neonec-
tion of the root system being bent upward at the time of plant- tria macrodidyma, is characterized by the presence of ovoid
ing and a failure of new roots to develop normally from these to obpyriform, dark-­red, smooth to finely warted perithecia
tissues thereafter (Fig. 35). (200–250 µm in diameter) without recognizable stroma. These
fructifications contain clavate to narrowly clavate asci, each
Causal Organisms bearing eight ellipsoid, uniseptate, smooth to finely warted,
Campylocarpon fasciculare Schroers, Halleen and Crous; hyaline ascospores measuring 12–18 × 3.5–4.5 µm.
Campylocarpon pseudofasciculare Halleen, Schroers and C. liriodendri is morphologically similar to C. destructans,
Crous; Cylindrocarpon obtusisporum (Cooke & Harness); Cyl- distinguishable from the latter primarily on the basis of conid-
indrocarpon destructans (Zinssm) Sholten; Cylindrocarpon ial shape (fusiform and gently curved) and by various molecu-
macrodidymum Halleen, Schroers and Crous; and Cylindro- lar characters. The sexual stage of C. liriodendri is not known.
carpon liriodendri (Cooke & Harness) Wollew. have all been Both Campylocarpon species produce brownish colonies on
described as causal agents of black foot disease. Since C. de- potato dextrose agar and brownish hyphal strands that form
structans was first reported in 1961 in France, it has been iso- in the aerial mycelium. C. fasciculare produces macroconidia
lated from diseased vines in Sicily, Portugal, Australia, New with three or four septa (38–44.5 × 6.5–8 µm or 47–51.5 × 7.5–
Zealand, South Africa, California, and southeastern Canada. 8.5 µm, respectively) on single or aggregated conidiophores. C.
C. macrodidymum has been reported recently in Australia, New pseudofasciculare produces macroconidia with three, four, or
Zealand, South Africa, California, and southeastern Canada. five septa (37.5–48.5 × 6.5–7.5 µm, 46.5–53.5 × 7–8.5 µm, or
C. obtusisporum was detected in Sicily in 1975. Campylocar- 51–59 × 7.5–8.9 µm, respectively). It also produces sparse chla-
pon fasciculare and Campylocarpon pseudofasciculare were mydospores (8–11 × 7–8.5 µm), whereas C. fasciculare does not
recently shown to cause black foot disease in South Africa. produce chlamydospores. Neither species forms microconidia,
The anamorph C. destructans produces microconidia and and no Campylocarpon species has a known sexual stage.
macroconidia that are mostly triseptate (22–31 × 4.5–6 µm),
hyaline, cylindrical with obtuse apices, straight (rarely curved), Disease Cycle and Epidemiology
and often having a distinct, protuberant, flat, basal abscission Cylindrocarpon species are ubiquitous soilborne fungi,
scar (Fig. 36). Distinctive mycelial chlamydospores, 8–25 µm causing root rot on a wide range of host plants. Based on what is
in diameter, either single or in chains or clusters with thick- known of their behavior on other hosts, it is assumed that they
ened, golden-­brown walls are profuse in older cultures (Fig. persist in a latent state in the soil and attack weakened plants
37). The teleomorph of C. destructans, Neonectria radicicola opportunistically under certain poorly defined conditions. For
(Gerlach & Nilsson) Mantiri & Samuels, is characterized by the example, black foot disease occurs most frequently in vine-
presence of red, globose to subglobose perithecia, 0.17–0.35 × yards or sections thereof with compacted, poorly drained soils.
0.15–0.32 mm, with a broadly conical papillum and a scarly to Although it has been linked to the planting of infected nursery
warted wall. These fructifications contain asci, which in turn stock, vineyard soils naturally infested with the pathogen are

Fig. 35. “J-­root” configuration on a Fig. 36. Conidia of Cylindrocarpon destructans at Fig. 37. Chlamydospores of Cylindrocarpon
young vine caused by the root sys- 400× magnification. (Cour­tesy E. Petit) destructans. (Cour­tesy E. Petit)
tem being bent upwards at the time
of planting, showing symptoms of
black foot disease that developed
subsequently. (Cour­tesy E. Petit)

27
believed to be a more important source of inoculum. The fun- though favored by warm weather, the disease is nevertheless a
gus infects through natural openings or wounds on the roots serious threat even in regions where relatively moderate tem-
or through the crown of the rootstock. Over time, it invades peratures accompany rainfall in the late spring and summer
lignified tissues of the plant, leading to the development of root (e.g., the Great Lakes region in North America, and Germany
lesions and plugging of the xylem by fungal tissue, gums, and and Switzerland in Europe). Although relatively easy to control
tyloses. The attendant reduction in mineral and water uptake with several groups of modern fungicides, black rot can cause
results in plant dieback. Diseased plants die very rapidly when virtually complete crop loss if not effectively managed. The
young, but as vines age, infection results in a steadier decline disease was one of the original impediments to the introduction
and death may not occur for more than 1 year after the initial of V. vinifera into North America, as noted in an 1888 USDA
onset of symptoms. Gelatinous masses of conidia are probably bulletin: “Black rot is the most serious and important disease of
spread through the soil by water. The production of chlamydo- the vine in the [eastern] United States ... there is no disease ...
spores allows the pathogen to survive in the soil for extended that causes in a few days such great losses ... after numerous
periods of time in the absence of suitable host tissue. The dis- trials the culture of European vines [V. vinifera] has been aban-
ease cycle of Campylocarpon spp. on grapevines is not known. doned  ...”. To this day, the disease remains one of the major
challenges to organic production of susceptible grape cultivars
Management in regions where it occurs regularly. Symptoms of black rot
No specific fungicide treatments against black foot disease were first recorded in a Kentucky vineyard in 1804 and the first
have been developed; therefore, host resistance, cultural prac- specimens were collected in Alabama in 1855. The pathogen
tices, and biological control are the primary tools available was introduced into Europe (France) in 1885, leading to the
to suppress pathogenesis. Uncontaminated nursery material first detailed account of the disease by Viala and Ravaz the
should be planted in soils having adequate drainage. In heavy following year. Although Guignardia bidwellii is indigenous
soils, drainage in the root zone can be facilitated by planting to eastern North America, it is also established now in some
on berms, installing tile drains, and moving drip irrigation regions of Europe, South America, and Asia. It is unknown in
emitters away from the vine, as appropriate. All phylloxera-­ Chile and is a quarantined pathogen in Australia.
resistant rootstocks show some level of susceptibility to black All cultivars of V.  vinifera appear to be highly susceptible
foot disease; greenhouse inoculations with C. macrodydimum to black rot. Most interspecific hybrid cultivars of primarily
and C. liriodendri showed 110R to be the most susceptible and V. labrusca origin are susceptible to highly susceptible; those
161-­49C the least susceptible of those examined. In additional primarily of V. aestavalis background are moderately resistant;
greenhouse studies, colonization of roots by the mycorrhizal and those of complex origin vary widely in susceptibility, de-
fungus Glomus intraradices prior to infection by the pathogen pending on their individual parentage and the criteria applied
provided good disease control. in selecting them for cultivation.

Selected References Symptoms

All new growth is susceptible to infection during the grow-
Alaniz, S., León, M., Vicent, A., García-­Jiménez, J., Abad-­Campos, P., ing season, although the most diagnostic symptoms occur on
and Armengol, J. 2007. Characterization of Cylindrocarpon spe- the leaves and fruit. Leaf lesions occur primarily on the adaxial
cies associated with black foot disease of grapevine in Spain. Plant surface, and are roughly circular to irregularly shaped, 2–10
Dis. 91:1187-­1193. mm in diameter, and characteristically delineated by a narrow,
Booth, C.  D. 1966. The genus Cylindrocarpon. Mycol. Pap. (CMI) dark-­brown band at the margin (Fig. 38). Lesions are initially
104:1-­56.
Gubler, W. D., Baumgartner, K., Browne, G. T., Eskalen, A., Latham,
cream colored, becoming tan and finally reddish brown as they
S.  R., Petit, E., and Bayramian, L.  A. 2004. Root diseases of mature. Pycnidia, which appear as small black pimples, de-
grapevines in California and their control. Australas. Plant Pathol. velop within the leaf lesions, often in a ring (Fig. 39). When the
33:157-­165.
Halleen, F., Schroers, H.-­J., Groenewald, J. Z., and Crous, P. W. 2004.
Novel species of Cylindrocarpon (Neonectria) and Campylocar-
pon gen. nov. associated with black foot disease of grapevines (Vitis
spp.). Stud. Mycol. 50:431-­455.
Petit, E., and Gubler, W. D. 2005. Characterization of Cylindrocarpon
species, the cause of black foot disease of grapevine in California.
Plant Dis. 89:1051-­1059.
Petit, E., and Gubler, W. D. 2006. Influence of Glomus intraradices
on black foot disease caused by Cylindrocarpon macrodidymum on
Vitis rupestris under controlled conditions. Plant Dis. 90:1481-­1484.
Petit, E., Barriault, E., Baumgartner, K., Wilcox, W. F., and Rolshau-
sen, P. E. 2011. Cylindrocarpon species associated with black-­foot
of grapevine in northeastern United States and southeastern Can-
ada. Am. J. Enol. Vitic. 62:177-­183.
Samuels, G. J., and Brayford, D. 1990. Variation in Nectria-­Radicicola
and its anamorph, Cylindrocarpon destructans. Mycol. Res.
94:433-­442.

(Prepared by E. Petit)

Black Rot
Black rot, caused by the pathogen Guignardia bidwellii
(Ellis) Viala and Ravaz (anamorph Phyllosticta ampelicida
[Engleman] Van der Aa) is an economically important disease Fig. 38. Leaf lesions caused by Guignardia bid­
in most viticultural regions with humid growing seasons. Al- wellii. (Cour­tesy M. Sosnowski)

28
 lesions fall on a main vein, the vein may turn black; blackened
veins may extend beyond the border of the lesion.
On berries, the first symptom is a small cream-­colored
dot, which very quickly becomes surrounded by a zone of
chocolate-­brown necrotic tissue (Fig. 40). This necrosis contin-
ues to expand until the entire berry becomes rotted, whereupon
it quickly turns dark and begins to shrivel into a hard, blue-­
black mummy that remains firmly attached to the pedicel (Fig.
41). Pycnidia first appear on the berry at the point of the initial
infection and quickly spread over the entire surface, sometimes
in concentric rings.
Lesions can also develop on the petioles, pedicels, shoots,
and tendrils. On the petioles and pedicels, they appear as small,
darkened depressions which soon turn black. Occasionally, le-
sions girdle the petiole and kill the entire leaf. Shoot infections
appear as elongated black cankers ranging in length from 1 mm
Fig. 39. Pycnidia of Guignardia bidwellii within a leaf lesion. to 2 cm (Fig. 42). Shoot and petiole lesions often contain abun-
(Photograph by W. McFadden-­Smith, Ontario Ministry of Agricul- dant pycnidia (Fig. 43).
ture and Food; Queen’s Printer of Ontario, © 2009. Re­produced Symptoms are different on the fruit of muscadine grapes
with permission.) (V.  rotundifolia). Lesions are small, black, superficial, and
scabby (Fig. 44). They do not cause the decay of the entire
berry as occurs on bunch grapes. Multiple infections on the
same berry may coalesce and form a brown to black crust on a

Fig. 42. Severe shoot and petiole infections caused by Guignar-

dia bidwellii. The small group of overwintered mummies attached
to the training wire served as the source of inoculum. (Cour­tesy
Fig. 40. Initial symptoms of black rot on an in- W. F. Wilcox)
fected berry. (Cour­tesy M. Sosnowski)

Fig. 41. Various stages of black rot development on berries. (Cour­ Fig. 43. Abundant formation of pycnidia in a petiole lesion caused
tesy W. F. Wilcox) by Guignardia bidwellii. (Cour­tesy M. Sosnowski)

29
portion of the berry surface, which may ultimately split. Pyc- the field, the vast majority have been recorded by the end of
nidia form in the surface of these scabby lesions. the bloom period. However, drought during the prebloom and
bloom period can delay ascospore depletion until rains resume.
Causal Organism In contrast, viable ascospores continue to be produced into late
G. bidwellii produces pseudothecia in a stroma on overwin- summer from mummies that are retained in the canopy. Once
tered mummies. Pseudothecia are separate, black, and spheri- discharged from pseudothecia, ascospores are dispersed by
cal (61–199 µm in diameter), with a flat or papillate ostiole at wind currents. Although their density is diluted with distance,
the apex. The centrum is pseudoparenchymatous and without trap plants 100 m or more from the nearest inoculum source
paraphyses. Asci (36–56 × 12–17 µm) are fasciculate, cylindri- (e.g., wild grapevines in adjacent woodlands) regularly become
cal to clavate, short stipitate, and eight spored. The ascus wall is infected. Similarly, black rot is becoming an increasing prob-
thick and bitunicate. Ascospores (10.6–18.4 × 4.8–8.9 µm) are lem in some densely planted regions of Europe where sporadic
hyaline, nonseptate, oval or oblong, rounded at the ends, and foci of abandoned vines serve as intense sources of primary
often present a characteristic footprint shape (Fig. 45). They inoculum for neighboring cultivated vineyards.
contain one to four nuclei and have finely granular cytoplasm Conidia from mummified berries and from overwintered
with two large refractive droplets at either end. cane lesions also can function as primary inoculum. Release
Spermagonia are also produced toward the end of the grow- of conidia from cane lesions peaks near bud break and declines
ing season on mummified berries in association with ascogo- progressively thereafter; release may be complete by bloom or
nial stromata. They are black, spherical (45–78 µm in diameter), continue through harvest, depending on the vineyard and year.
erumpent, and ostiolate at the apex. Bacilliform spermatia are Viable lesions capable of producing conidia can persist in wood
hyaline, nonseptate, and measure 2.5 × 1 µm. for at least 2 years; older lesions have not been investigated.
Black, erumpent pycnidia are produced from all infected tis- Conidia are splash-­dispersed short distances by raindrops, and
sues during the growing season. They are spherical (59–196 µm increased numbers of leaf infections have been recorded be-
in diameter), solitary, and ostiolate at the apex. Under wet or neath canes with overwintered black rot lesions. Conidia from
highly humid conditions, hyaline conidia exude from the neck mummies on the ground are probably of relatively minor im-
of the pycnidium in a white, mucilaginous cirrus. Conidia are portance, as (i) their production declines precipitously during
hyaline, nonseptate, ovoid to oblong, and rounded at the ends, the early growing season and is finished by bloom, and (ii)
measure 7.1–14.6 × 5.3–9.3 µm in diameter, and are either uni-­ splash dispersal from the vineyard floor to host tissue within
or binucleate, but occasionally trinucleate. the canopy is limited. In contrast, mummies retained within the
Three formae speciales of G. bidwellii were described by canopy between seasons pose an extreme risk, as they produce
Luttrell. G. bidwellii f. sp. euvitis is pathogenic to the Ameri- large numbers of conidia from bud break through veraison—
can bunch grape species of the section Vitis, and to V. vinifera. which includes the entire period of berry susceptibility—and
G. bidwellii f. sp. muscadinii is pathogenic to V. rotundifolia they are situated immediately adjacent to young berries and
and V. vinifera. A third forma specialis, G. bidwellii f. sp. par- other susceptible tissues, facilitating their dispersal to the host.
thenocissi, is pathogenic only to species of Parthenocissus, a
genus of climbing plants that belongs to the family Vitaceae.
Besides differing in pathogenicity, G. bidwellii muscadinii also
differs from G. bidwellii euvitis in appearance, growth rate of
colonies in culture, and the size of pseudothecia, ascospores,
and conidia.

Disease Cycle and Epidemiology

The disease cycle for black rot is presented diagrammatically
in Fig. 46. G. bidwellii overwinters in mummified berries either
retained on the vine or fallen to the ground, and in cane lesions.
Ascospores released from mummified berries serve as the most
common form of primary inoculum in commercial vineyards.
They are ejected from pseudothecia after approximately 0.3
mm or more of rain, and may be discharged for up to 8 h after
a rainfall. Ascospores from mummies on the ground can be
discharged from budbreak through mid summer, although in
both laboratory discharge tests and spore trapping studies in

Fig. 45. Fruiting bodies and spores of Guignardia bidwellii. A,

Cross section through a pseudothecium, with asci within a locule.
B, Ascus and ascospores. C, Cross section through a pycnidium.
Fig. 44. Scabby lesions of black rot on muscadine berries. (Cour­ D, Conidiogenous cells and conidia. (Modified and reproduced,
tesy P. Bertrand) by permission, from Sivanesan and Holliday, 1981)

30
Fig. 46. Disease cycle of black rot. (Drawing by R. Sticht and E. Gotham; reproduced by permission of Cornell University and the New York
State IPM Program)

Just a few mummies in the canopy can result in significant dis-

ease development in their vicinity (Fig. 42), with “hot spots” of
activity often observed beneath mummies that were inadver-
tently retained during dormant pruning.
Following the release of ascospores or conidia during rain
events, continued wetness of leaves, shoots, or berries is re-
quired for spore germination and subsequent infection. The
approximate wetness duration necessary for infection to occur
ranges from 24 h at a temperature of 10°C to only 6 or 7 h at
temperatures of 21–26.5°C (Table 2). These data can be used
to help determine the need for fungicide sprays in response to
putative or anticipated infection events.
Conidia produced from pycnidia that form in new infec-
tions can serve as secondary inoculum throughout the season.
Because of the copious number of conidia produced and their
proximity to other fruit in the cluster, just one or two infected
berries can serve as a source of inoculum to spread the dis-
ease throughout the entire bunch, particularly if they begin suggest a direct danger to berries from high levels of primary
sporulating while the remaining fruit are still young and highly inoculum within or near the vine.
susceptible. In contrast, the epidemiological role and economic Early researchers noted that only the young, tender portions
significance of leaf infections is not clear. The only detailed of the vine were susceptible to infection, but it was not until
study of parallel disease progress on leaves versus fruit sug- recently that this ontogenic, or age-­related, resistance in grape
gested that most foliar disease was caused by secondary in- leaves was described in detail. Conidia are able to germinate
oculum originating from recently infected berries, rather than and penetrate grape leaves of all ages, but subsequently are not
the converse. Nevertheless, if significant foliar infection oc- able to colonize or cause visible symptoms on those that have
curs prior to bloom, the pycnidia produced within these lesions become fully expanded. On such older leaves, germlings re-
could serve as an important source of secondary inoculum main quiescent but are able to resume growth saprobically if
threatening berries after they set. Such a scenario would also the tissue is killed.

31
 The phenomenon and practical importance of ontogenic and temperature. If more than a trace of disease develops on
resistance in fruit has also received new study. In the Finger young clusters, fungicidal protection should continue until fruit
Lakes region of New York, berries of Vitis × labruscana ‘Con- age to the point that they are no longer susceptible to infection.
cord’ exhibit a period of maximum susceptibility from bloom Several fungicide classes provide excellent control of black
until 2–4 weeks later, and do not become diseased when inocu- rot. Among the traditional protectants, the dithiocarbamates
lated after 5 weeks postbloom. Berries of V. vinifera cultivars (mancozeb, ferbam, and ziram) are very effective, whereas
exhibit a longer period of susceptibility: maximum levels of captan is only moderately so. A number of triazole fungicides
susceptibility persist until 3–5 weeks after bloom and a small (including difenoconazole, flusilazole, flutriafol, myclobutanil,
proportion of the berries remain susceptible until 6–7 weeks tebuconazole, tetraconazole, and triadimefon) are highly ef-
postbloom. These latter data agree with reports of black rot de- fective, providing moderate residual protective activity plus
velopment on V. vinifera vines in Switzerland. The incubation significant postinfection activity, thereby enabling their use
period also increases markedly as berries age and lose their in curative programs or as an emergency response following
susceptibility to colonization by the fungus. Whereas symp- unprotected infection events. In contrast, some other sterol
toms first appear 10–14 days after inoculation of young V. vi- demethylation inhibitor fungicides (e.g., fenarimol and tri-
nifera fruit (depending largely on temperature), the minimum flumizol) provide only modest control of this disease. The
incubation period is approximately 21 days on those inoculated strobilurin fungicides (azoxystrobin, kresoxim-­methyl, pyra-
6 weeks after bloom, with some berries in the same cluster not clostrobin, and trifloxystrobin) also provide excellent control
becoming symptomatic until a full month after inoculation. of black rot, primarily in a protectant mode but with modest
These extended incubation periods should be considered when curative activity as well. Copper provides the best control
trying to determine the infection event(s) leading to a disease among materials approved for organic production systems, al-
outbreak in the latter part of the summer. though it is only moderately effective and must be used at rela-
On muscadine grapes, G. bidwellii survives the winter as tively short spray intervals under significant disease pressure.
pseudothecia in senesced leaves and as pycnidia in infected Sulfur is poor. Because black rot spores require hydrophobic
canes. Asci mature in late winter and early spring, and asco- surfaces for germination, surfactants that improve the wetta-
spores are discharged for 4–5 weeks in April and May. Both bility of waxy leaf and berry surfaces may offer some promise
ascospores and conidia can serve as primary inoculum. Im- as alternative control materials; however, such materials have
mature leaves can be infected throughout the growing season, proven more effective in greenhouse settings than in limited
whereas berries may be infected from set until they reach full field tests. Lime sulfur applied shortly before bud break should
size. Conidia produced from primary infections can initiate reduce pycnidial inoculum from diseased canes retained dur-
secondary cycles of infection, as described above. ing pruning. This treatment may be useful where cane lesions
are important sources of primary inoculum, particularly in
Management circumstances where highly effective fungicides may not be
Management of black rot is most effective with an integration available.
of chemical and cultural components. Sanitation is the first line
of defense and can greatly impact the efficacy of a fungicide Selected References
program, depending on the extent to which it is implemented.
Becker, C. M., and Pearson, R. C. 1996. Black rot lesions on overwin-
When highly effective fungicides are not employed (e.g., or- tered canes of Euvitis supply conidia of Guignardia bidwellii for
ganic production systems), rigorous sanitation efforts are essen- primary inoculum in spring. Plant Dis. 80:24-­27.
tial for sustained control on susceptible cultivars in problematic Ferrin, D. M., and Ramsdell, D. C. 1977. Ascospore dispersal and in-
regions. Retention of mummies in the canopy, which is particu- fection of grapes by Guignardia bidwellii, the causal agent of grape
larly likely with mechanical pruning systems, provides greatly black rot disease. Phytopathology 67:1501-­1505.
increased disease pressure relative to the same number of mum- Ferrin, D. M., and Ramsdell, D. C. 1978. Influence of conidia disper-
mies on the ground, owing to the additional number of spores sal and environment on infection of grape by Guignardia bidwellii.
produced per mummy, the temporal shift in spore release to Phytopathology 68:892-­895.
coincide with the period of peak berry susceptibility, and the Hoffman, L. E., and Wilcox, W. F. 2003. Factors influencing the ef-
proximity of these inoculum sources to the new fruit. Thus, ficacy of myclobutanil and azoxystrobin for control of grape black
removal of mummies to the ground during dormant pruning is rot. Plant Dis. 87:273-­281.
a minimal sanitation practice, which typically is adequate in Hoffman, L.  E., Wilcox, W.  F., Gadoury, D.  M., and Seem, R.  C.
2002. Influence of grape berry age on susceptibility to Guignar-
vineyards where the disease is well controlled routinely. How-
dia bidwellii and its incubation period length. Phytophathology
ever, in vineyards where black rot control is problematic, addi- 92:1068-­1076.
tional procedures may be warranted. These include cultivating Hoffman, L.  E., Wilcox, W.  F., Gadoury, D.  M., Seem, R.  C., and
and/or mulching the vineyard floor to physically cover mum- Riegel, D. G. 2004. Integrated control of grape black rot: Influence
mies by or soon after bud break, and even physical removal of host phenology, inoculum availability, sanitation, and spray tim-
of mummies from the vineyard if practical. Diseased canes ing. Phytophathology 94:641-­650.
should be pruned from the vine and, ideally, removed from the Jermini, M., and Gessler, C. 1996. Epidemiology and control of grape
vineyard or destroyed. black rot in southern Switzerland. Plant Dis. 80:322-­325.
Traditionally, fungicide applications were recommended to Kuo, K., and Hoch, H. C. 1996. Germination of Phyllosticta ampeli-
begin when shoots were 10–15 cm in length and to continue cida pycnidiospores: Prerequisite of adhesion to the substratum
until the berries reached veraison. Recent research has shown and the relationship of substratum wettability. Fungal Genet. Biol.
the value of concentrating fungicidal protection during the 20:18-­29.
period of maximum berry susceptibility, from bloom until Kuo, K., and Hoch, H.  C. 1996. The parasitic relationship between
approximately 4–6 weeks later, depending on cultivar and Phyllosticta ampelicida and Vitis vinifera. Mycologia 88:626-­634.
Luttrell, E. S. 1946. Black rot of muscadine grapes. Phytopathology
weather. In vineyards where sanitation is good and the level of
36:905-­924.
overwintering inoculum is modest, a program of limited fun- Luttrell, E.  S. 1948. Physiologic specialization in Guignardia bid­
gicide applications extending from the immediate prebloom wellii, cause of black rot of Vitis and Parthenocissus species. Phy-
period through 4 weeks postbloom has provided excellent con- topathology 38:716-­723.
trol in several different regions where black rot is active. In Molitor, D., and Beyer, M. 2014. Epidemiology, identification and dis-
vineyards where disease historically has been difficult to con- ease management of grape black rot and potentially useful metabo-
trol and inoculum levels are higher, fungicide applications may lites of black rot pathogens for industrial applications—A review.
need to begin 2 or more weeks prebloom, depending on rainfall Ann. Appl. Biol. 165:305-­317.

32
Scribner, F.  L., and Viala, P. 1888. Black Rot (Laestadia bidwellii). multiple species within Botryosphaeriaceae that infect grape-
Dept. of Agric. Bot. Div. Bull. 7. vine wood.
Sivanesan, A., and Holliday, P. 1981. Guignardia bidwellii. Descrip- Botryosphaeriaceae spp. have been isolated from diseased
tions of Pathogenic Fungi and Bacteria, no. 710. Commonwealth grapevine wood in viticultural regions worldwide. Resultant
Mycological Institute, Kew, Surrey, England. yield losses of 25–30% have been reported in the susceptible
Spotts, R. A. 1977. Effect of leaf wetness duration and temperature on cultivars Cabernet Sauvignon, Cabernet Franc, and Sauvignon
the infectivity of Guignardia bidwellii on grape leaves. Phytopa-
thology 76:1378-­1381.
Blanc in France. An economic study of the California wine grape
Spotts, R. A. 1980. Infection of grape by Guignardia bidwellii—fac- industry conducted in the late 1990s estimated losses from
tors affecting lesion development, conidia dispersal and conidial canker diseases (shown subsequently to be primarily Eutypa
populations on leaves. Phytopathology 70:252-­255. dieback and Botryosphaeria dieback) to be over $260 million
per year at that time. Botryosphaeria dieback is currently rec-
(Prepared by W. F. Wilcox and L. E. Hoffman) ognized as one of the most prevalent diseases of grapevines
worldwide, limiting both vineyard longevity and productivity.
In Mexico and California, Botryosphaeria dieback is consid-
ered endemic in the arid and warmest grape-­growing regions.
Botryosphaeria Dieback Disease incidence up to 100% was reported in vineyards ≥10
years old in the southern California region of Coachella Valley,
Species in the family Botryosphaeriaceae Theiss. & P. Syd. with several cankers per vine.
1918 have a cosmopolitan distibution and are found as endo- Botryosphaeria dieback decreases vineyard longevity, re-
phytes, parasites, and/or saprophytes in and on a wide range of duces yields, and increases production costs through necessary
annual and perennial crops, ornamental plants, and forest trees. management programs, involving both prophylactic efforts
Several species are recognized as significant plant pathogens and the additional pruning and training practices required to
that cause a variety of symptoms in economically important replace lost fruiting wood. Although the disease usually affects
perennial crops, including leaf spots, fruit rots, shoot blight, matures vines (at least 6 years old), it sometimes causes decline
perennial cankers, and dieback syndromes that eventually cul- and eventual death of young vines as well. Native American
minate in host death. However, the association between species and interspecific hybrid cultivars are affected in addition to
within this family and dieback of grapevines has been over- those of Vitis vinifera.
looked for many years, as such organisms largely have been
considered saprophytes, secondary colonizers and/or weak Symptoms
parasites of this host. Recognition of grapevine diseases caused A wide range of vascular symptoms associated with Bot-
by Botryosphaeriaceae species also has remained problematic ryosphaeria dieback have been characterized, but foliar symp-
owing to misdiagnoses due to the similarity of these symptoms tomatology remains unclear. It now seems likely that some
to those of other trunk diseases, including esca, Eutypa die- symptoms previously described as caused by Botryosphaeri-
back, and Phomopsis cane and leaf spot. aceae spp. (e.g., chlorosis and colored spots on the leaf mar-
The pathogenicity of members of the Botryosphaeriaceae gins or blade that coalesce to form large necrotic areas) were
that parasitize grapevine and the epidemiology of their diseases confused with one of the many manifestations of esca, or that
also have been obscured by conflicting reports of virulence and they may have resulted from a complex combination of several
symptoms among cultivars and grape-­g rowing regions. Fur- fungi, including those causing esca, in a specific stage of vine
thermore, the taxonomy of species within the Botryosphaeri- development or decline. The most widely reported external
aceae has been subject to numerous revisions, complicating symptom associated with Botryosphaeria dieback has been the
efforts to accurately identify individual isolates or to compare total absence of spring growth from single or multiple spur po-
results among different reports, where different names may sitions of infected vines (Fig. 47), which has helped to differen-
have been ascribed to common taxa and vice versa. However, tiate this disease from the characteristic foliar symptomatology
research conducted in several countries since the late 1990s observed on grapevines affected by Eutypa dieback, esca, and/
has clarified the status of these fungi as important grapevine or Phomopsis cane and leaf spot. However, grapevines infected
trunk pathogens worldwide, resulting in advances in the under- by the fungi that cause Botryosphaeria dieback can also exhibit
standing of their epidemiology and control. normal and healthy shoot development so long as sufficient
Since a Botryosphaeriaceae species was first associated with healthy vascular tissue remains present to support it (Fig. 48).
grapevine dieback in the mid-­1960s, considerable controversy
and debate have ensued regarding the cause and name of trunk
diseases caused by fungi within this family. Until recently,
different common names, including black dead arm, Botryo­
sphaeria canker, and Diplodia cane dieback have been used
to refer to the same symptoms (e.g., wedge-­shaped cankers,
dark streaking, and/or light-­brown discoloration of the wood),
sometimes caused by a single organism. Furthermore, multiple
trunk diseases can occur within individual vineyards, and these
names have sometimes been applied erroneously in the diag-
nosis of symptoms attributable to accompanying diseases (e.g.,
esca) that are caused by unrelated pathogens, and this has con-
tributed significantly to the confusion regarding their etiology.
Recent studies have shown that various Botryosphaeriaceae
spp. can be isolated from grapevines exhibiting the same vas-
cular symptoms but diverse foliar symptomatology, either alone
or in combination with other trunk disease pathogens. Thus,
the use of multiple unique names to denote individual diseases
with well-­characterized symptoms and specific causal agents
does not appear to be appropriate. Consequently, the name Bot-
ryosphaeria dieback has been accepted recently by workers in Fig. 47. Absence of spring growth from spurs killed as a result of
this field to encompass the broad range of symptoms caused by Botryosphaeria dieback. (Cour­tesy J. R. Úrbez-­Torres)

33
 Vascular symptoms associated with Botryosphaeria dieback trunks for several years until only a small wedge of live tissue
include perennial cankers (Fig. 49); internal wood necrosis remains, culminating in death of the vine portions above the
(Fig. 50); dark-­and/or light-­brown streaking of the wood (Fig. canker once complete girdling occurs. Although typically ob-
51); and bud and pith necrosis. Additionally, several Botryo- served on mature vines, especially where large pruning wounds
sphaeriaceae spp. have been isolated from bleached canes, have been made while retraining them, wedge-­shaped cankers
pruning debris, asymptomatic wood, necrotic nursery material caused by Botryosphaeriaceae spp. also have been observed on
(scion and/or rootstock), and from necrotic areas of the graft young vines. Cankers have been shown to develop from cracks
union. Among all these symptoms, perennial cankers are the and natural openings on the framework of vines as well. Black,
most prevalent and widespread, as reflected by the former dis- ostiolate pycnidia can be found frequently beneath the bark on
ease name of Botryosphaeria canker. cankered areas in spurs, cordons and/or the vine trunk (Fig. 53).
The vascular symptoms associated with Botryosphaeria die-
back appear to initiate primarily from pruning wounds and to Causal Organisms
expand basipetally from that point of infection (Fig. 52). Peren- To date, the following 23 Botryosphaeriaceae spp. have been
nial cankers also expand laterally in the spurs, cordons, and identified on grapevines affected by Botryosphaeria dieback:
Botryosphaeria dothidea (Moug. : Fr.), Ces. & De Not.; Di-
plodia corticola A. J. L. Phillips, A. Alves & J. Luque; Diplo-
dia mutila (Fr. : Fr.) Fr.; Diplodia seriata De Not.; Dothiorella
americana J. R. Úrbez-­Torres, F. Peduto & W. D. Gubler; Do-
thiorella iberica A. J. L. Phillips, J. Luque & A. Alves; Dothio-

Fig. 50. Internal wood necrosis symptom of Botryosphaeria die-

Fig. 48. Dead wood infected by a Botryosphaeri- back. (Cour­tesy J. R. Úrbez-­Torres)
aceae species as revealed by removing the vine
bark, with the remaining live wood supporting
healthy shoot growth apical to it. (Cour­tesy G. M.
Leavitt)

Fig. 49. Cross-­sectional view through an expanding perennial Fig. 51. Internal wood streaking symptom
canker associated with Botryosphaeria dieback. (Cour­tesy J.  R. of Botryosphaeria dieback. (Cour­tesy J.  R.
Úrbez-­Torres) Úrbez-­Torres)

34
rella neclivorem W. M. Pitt & J. R. Úrbez-­Torres; Dothiorella W. M. Pitt, J. R. Úrbez-­Torres & F. P. Trouillas; and Sphaeropsis
vidmadera W.  M. Pitt, J.  R. Úrbez-­Torres & F.  P. Trouillas; porosa (Van Niekerk & Crous) A. J. L. Phillips & A. Alves.
Dothiorella vinea-­gemmas W.  M. Pitt & J.  R. Úrbez-­Torres; It is only in recent years that species definitions have been
Lasiodiplodia crassispora T. I. Burgess & Barber; Lasiodiplo- clarified and for this reason some earlier reports of “Botryos-
dia missouriana J. R. Úrbez-­Torres, F. Peduto & W. D. Gubler; phaeria” spp. on grapevines may not be entirely accurate. This
Lasiodiplodia theobromae (Pat.) Griff. & Maubl.; Lasiodiplo- is particularly true for species with Fusicoccum anamorphs,
dia viticola J. R. Úrbez-­Torres, F. Peduto & W. D. Gubler; Neo- where the name of B. dothidea (anam. Fusicoccum aesculi
fusicoccum australe (Slippers, Crous & M.  J. Wingf.) Crous, Corda) was often used in a broad sense that encompassed what
Slippers & A. J. L. Phillips; Neofusicoccum luteum (Pennycook are now considered to be several distinct species. On the basis
& Samuels) Crous, Slippers & A. J. L. Phillips; Neofusicoccum of several pathogenicity studies conducted during the last de-
macroclavatum T. I. Burgess, Barber & Hardy; Neofusicoccum cade, species of Botryosphaeriaceae infecting grapevines are
mediterraneum Crous, M.  J. Wingf. & A.  J.  L. Phillips; Neo- divided into three virulence rankings: those that are highly vir-
fusicoccum parvum (Pennycook & Samuels) Crous, Slippers ulent (Lasiodiplodia spp. and Neofusicoccum spp.); moderately
& A. J. L. Phillips; Neofusicoccum viticlavatum (Van Niekerk virulent (B. dothidea and Diplodia spp.); and slightly virulent
& Crous) Crous, Slippers & A.  J.  L. Phillips; Neofusicoccum (Dothiorella spp. and S. viticola).
vitifusiforme (Van Niekerk & Crous) Crous, Slippers & A. J. L. Among the 23 botryosphaeriaceous taxa listed above, B. do-
Phillips; Spencermartinsia viticola (A. J. L. Phillips & J. Luque) thidea, D. mutila, D. seriata, L. theobromae, and N. parvum
A. J. L. Phillips, A. Alves & Crous; Spencermartinsia westrale have been isolated most frequently from symptomatic wood.
Therefore, descriptions of these five species are provided below.
Ascomata of B. dothidea (200–500 µm in diameter) are
erumpent, brown to black, open through an ostiole, and form in
botryose aggregates of up to 100, although sometimes singly.
Asci are bitunicate with a thick endotunica, clavate, and stipi-
tate. Ascospores, (17–)19–24(–32) × (6–)7–8(–10) µm, are ellip-
soid to broadly fusoid, hyaline, smooth, thin walled, and one
celled. Pycnidia are morphologically indistinguishable from
the ascomata. Conidiophores are hyaline, cylindrical, and
smooth, 23–35 × 4–5 µm, and are formed from the cells lin-
ing the locule wall. Conidia, (17–)19.5–30(–34) × 4–6(7.5) µm,
are hyaline, thin walled, smooth, and narrowly or irregularly
fusiform, with a subtruncate to bluntly rounded base exhibiting
a minute marginal frill (Fig. 54). Colonies on potato dextrose
agar initially are white, becoming green to dark green after 3 or
4 days with copious aerial mycelium, ultimately becoming dark
gray (Fig. 55). Numerous conidiomata can be observed in cul-
tures after 1 week of incubation at room temperature. Optimum
colony growth occurs between 25 and 30ºC.
Ascomata of D. mutila are dark brown, immersed, and uni-
loculate with the wall composed of dark-­brown, thick-­walled
textura angularis. Asci are bitunicate with a thick inner wall,
clavate, and stipitate. Ascospores (25–36 × 9.5–13.6 µm) are
hyaline and aseptate, sometimes becoming translucent brown
and one or biseptate with age (Fig. 56). Pycnidia (130–195
µm in diameter) occur individually or in groups in dead corti-
Fig. 52. Vascular symptoms of Botryosphaeria
cal tissue. They are globose, dark brown to black, immersed,
dieback expanding basipetally from one or more thick walled, and with a central ostiole. Conidia, (21–)25–28 ×
pruning wounds, the apparent point(s) of infec- (10–)13–14.6 µm, are hyaline; one celled and cylindrical with
tion. (Cour­tesy J. R. Úrbez-­Torres) broadly rounded ends, some with a large central guttule; and

Fig. 53. Pycnidia of a Botryosphaeriaceae species beneath the Fig. 54. Conidia of Botryosphaeria dothidea. (Cour­tesy J.  R.
bark of an infected vine. (Cour­tesy J. R. Úrbez-­Torres) Úrbez-Torres)

35
smooth with a thick, glassy wall. Some conidia also become on water agar at room temperature. Optimum temperature for
pale, translucent brown, and develop a single septum after colony growth is 25°C.
discharge (Fig. 57). Colonies on potato dextrose agar are dark Ascomata of D. seriata are dark brown, immersed, and
green with moderate amounts of aerial mycelium (Fig. 58). uniloculate with the wall composed of dark-­brown and thick-­
Conidiomata, 1–2 mm in diameter, start to form after 1 week walled textura angularis. Asci are bitunicate with a thick inner
wall, clavate, and stipitate. Ascospores (23–38 × 7–3 µm) are
hyaline and one celled. Pycnidia are dark brown, unilocular
with a central ostiole, immersed in young tissue, and appear
individually or in groups under exfoliating bark of spurs, cor-
dons, and trunks. Cylindrical, one-­celled conidia, (15–)22.5–26
× (8)9.5–14 µm, are hyaline when immature, becoming light
brown when mature and before discharge from the pycnidia,
with both ends rounded or sometimes truncate at the base (Fig.
59). Colonies on potato dextrose agar are dark gray with mod-
erate aerial mycelium (Fig. 60) and start to form numerous
small (0.3–1.2 mm diameter) pycnidia after 5 days at room tem-
perature. The optimum temperature for colony growth is 27°C.
Ascomata of L. theobromae (250–399 µm) are dark brown
to black and aggregated. Asci (90–120 µm) are bitunicate, cla-
vate, and contain eight ascospores. Ascospores, (24–)30–35 ×
(7)11–14(–17) µm, are hyaline and aseptate. It should be noted

Fig. 55. Colony of Botryosphaeria dothidea on potato dextrose

agar. (Cour­tesy J. R. Úrbez-­Torres)

Fig. 58. Colony of Diplodia mutila on potato dextrose agar. (Cour­

tesy J. R. Úrbez-­Torres)

Fig. 56. Bitunicate asci of Diplodia mutila, containing eight asco-

spores. (Cour­tesy A. J. L. Phillips)

Fig. 57. Conidia of Diplodia mutila, representing pre-­ (hyaline)

and post-­ d ischarged (brown) morphologies. (Cour­ tesy J.  R. Fig. 59. Conidia of Diplodia seriata. (Cour­tesy A. J. L.
Úrbez-­Torres) Phillips)

36
that this teleomorph has not been unambiguously associated ostiole. Conidia are hyaline, smooth, and thin walled; unicel-
with L. theobromae. Pycnidia are single or grouped, black, glo- lular, (13.5–)15–22.5(–28.5) × 4–7.5 µm; and ellipsoid with a
bose, ostiolate, and subcutaneous to erumpent. Pycnidia vary subobtuse apex and truncate base (Fig. 63). Conidia frequently
from 93 to 625 µm in diameter, occur in or on a stroma, and become olivaceous or light brown with time, developing 1 or 2
may be hirsute or glabrous. Conidia are subovoid to ellipsoid-­ septa with a darker middle cell (Fig. 64). Microconidia, which
ovoid with a broadly rounded apex, (19.0–)21.0–31.0(–32.5) ×
(12.0–)13.0–15.5(–18.5) µm, taper to a truncate base, are thick
walled and widest in the middle to upper third, and have granu-
lar contents. They are hyaline and aseptate initially, becoming
dark brown with a single septum only long after discharge from
the pycnidia, with melanin deposits on the inner surface of the
wall arranged longitudinally to give a striate appearance (Fig.
61). Colonies on potato dextrose agar develop a mycelium ap-
pearing gray in white light, later turning dark gray with dense
aerial growth (Fig. 62). The optimum temperature for colony
growth is typically 30–35°C, with some strains showing opti-
mum growth up to 40°C.
Ascomata of N. parvum are virtually indistinguishable
from those of B. dothidea but are less frequently aggregated
into large clusters. Asci (75–145 × 17–20 µm) are bitunicate
with a thick endotunica, clavate, and stipitate. Smooth and
thin-­walled hyaline ascospores, (15–)18–27(–29.5) × (6–)8–11
µm, are broadly ellipsoid to fusoid and widest in the middle
to upper third. Pycnidia, externally indistinguishable from as-
comata, are uni-­or multilocular, occurring individually or in
the same stromata as the ascomata. Pycnidia are globose and Fig. 62. Colony of Lasiodiplodia theobromae on potato dextrose
nonpapillate to pyriform, opening through a nonperiphysate agar. (Cour­tesy J. R. Úrbez-­Torres)

Fig. 63. Young, hyaline, aseptate conidia of Neofusicoccum par-

Fig. 60. Colony of Diplodia seriata on potato dextrose agar. (Cour­ vum. (Cour­tesy A. J. L. Phillips)
tesy J. R. Úrbez-­Torres)

Fig. 61. Post-­discharged appearance of Lasiodiplodia theobro- Fig. 64. Older, darkened, multicellular conidia of Neofusicoccum
mae conidia. (Cour­tesy J. R. Úrbez-­Torres) parvum. (Cour­tesy A. J. L. Phillips)

37
are seen in some isolates, are hyaline, smooth, rod shaped, wood, which prolongs the life of grapevines infected by vari-
truncate at either end, and 3–5 × 1–1.5 µm. Colonies on potato ous canker-­forming fungi. When the disease has not progressed
dextrose agar appear similar to those of B. dothidea. The opti- throughout the vine, production can be at least partly restored
mum temperature for colony growth is 28°C. by pruning cankered portions a minimum of 15 cm below any
discolored wood. New fruiting wood is then developed on a re-
Disease Cycle and Epidemiology placement arm derived from a shoot arising from the remaining
The sexual stage of several Botryosphaeriaceae spp. has been healthy tissue. Application of wound protectants to large cuts
described, but teleomorphs are rarely found on grapevines or resulting from surgery or other retraining operations is highly
other substrates. Therefore, asexual pycnidia appear to be the recommended, particularly if these are made during periods of
principal source of primary inoculum. Pycnidia of the species high inoculum concentration.
responsible for Botryosphaeria dieback are commonly ob- Because species in the Botryosphaeriaceae infect grapevines
served embedded in the bark of diseased canes, spurs, cordons, primarily through wounds, prophylactic strategies to control
and trunks, and can be found on old prunings left in the vine- these pathogens are aimed at protecting pruning wounds. Sev-
yards. Pycnidia of B. dothidea, D. mutila, D. seriata, L. theo- eral active ingredients, including thiophanate-­methyl, pyraclos-
bromae, and N. parvum in particular have been reported from trobin, various triazole fungicides (including fenbuconazole,
a broad range of hosts, many of which are commonly found tebuconazole, and cyproconazole plus iodocarb), and a boron-­
surrounding vineyards. However, because dissemination of based paste have been shown to reduce the risk of infection
pycnidiospores occurs primarily via water splashing over rela- when applied as pruning wound protectants. Although large
tively short distances, it is generally accepted that most infec- wounds are at the greatest risk of infection by species in the
tions result from inoculum that is produced within an infested Botryosphaeriaceae, studies have shown that both 1-­ and
vineyard. However, the role that windblown rain might play in 2-­year-­old wounds also are susceptible. Ideally, protective
long-­distance dispersal of conidia into previously uninfested treatments should be applied to all pruning wounds. However,
vineyards is currently unknown. Several Botryosphaeriaceae the high cost of manually treating all pruning cuts, and the pos-
spp., especially D. seriata and N. parvum, have also been iso- sibility that repeat application(s) might be required to maintain
lated from necrotic wood of rootstocks, scions, and/or graft protection through the period of wound susceptibility, make
unions in young vines, suggesting that infected propagation such treatments economically viable only in high cash-­return
material also can play a role in the initiation and/or develop- vineyards. Pruning wound protection through tractor-­applied
ment of epidemics. Because some Botryosphaeriaceae species fungicide sprays can reduce cost significantly and facilitate
are known to act as latent pathogens, there is a potential for treatment of large vineyards, but such applications traditionally
asymptomatic material from infested vineyards to be used for have provided limited efficacy. However, recent research with
propagation material and ultimately infest new vineyards when several of the fungicides listed above, using spray application
they are planted. technology that maximizes deposition efficiency, has shown
Spore trapping studies conducted in both Northern and new promise for this approach.
Southern Hemisphere grape-­growing regions have somewhat Late pruning and/or double pruning, cultural practices used
elucidated the climatic conditions that promote spore release. widely in California to reduce disease caused by E. lata, also
Conidia of Botryosphaeriaceae spp. are primarily released from have been effective in reducing infections by Botryosphaeri-
pycnidia during rain events providing at least 0.2 mm of pre- aceae spp. there and in other regions with similar Mediter-
cipitation. It has also been confirmed that overhead sprinkler ranean climates. These techniques are designed to produce
irrigation can induce spore release. Seasonal spore dispersal final wounds near or after the end of the rainy season, when
patterns have been shown to vary among regions as a result of inoculum is limited and wounds may lose susceptibility more
their greatly variable climatic conditions. For example, in Cali- quickly as temperatures increase. Wound protection by fungi-
fornia most Botryosphaeriaceae spores were trapped following cide sprays may complement late pruning by reducing the like-
rain events during the winter months, whereas in France and lihood that the limited inoculum still present by that time is
New Zealand spores were trapped throughout the year and the able to colonize the host.
highest numbers were detected during summer months. Thus, Complete control of Botryosphaeria dieback and other
in Mediterranean climates such as California, the dormant grapevine trunk diseases is extremely difficult owing to the
pruning of grapevines takes place during the primary period high number of wounds made on individual vines each year,
of rainfall (and, consequently, spore release), thereby exposing the long time that wounds remain susceptible, the difficulty
highly susceptible infection sites to inoculum of the botryos- in controlling a wide spectrum of different pathogens with a
phaeriaceous fungi in these regions. For example, grapevine single fungicide active ingredient, and the technical and logisti-
pruning wounds in California are susceptible to infection by L. cal difficulties in delivering fungicide sprays to multiple targets
theobromae and N. parvum to varying extents throughout the efficiently and effectively.
entire dormant season, but susceptibility is greatest immedi-
ately after pruning and decreases significantly over time there- Selected References
after. Thus, the significance of high spore numbers detected
in some regions during the growing season, when pruning Díaz, G.  A., and Latorre, B.  A. 2013. Efficacy of paste and liquid
wounds appear to be much less susceptible to infection by these fungicide formulations to protect pruning wounds against patho-
fungi, is still not well understood. gens associated with grapevine trunk diseases in Chile. Crop Prot.
46:106-­112.
Management Kuntzmann, P., Villaume, S., and Bertsch, C. 2009. Conidia dispersal
Progress has been made in developing and implementing of Diplodia species in a French vineyard. Phytopathol. Mediterr.
novel control techniques against Botryosphaeria dieback but 48:150-­154.
Phillips, A.  J.  L. 2002. Botryosphaeria species associated with dis-
management is still extremely difficult, due in part to the wide eases of grapevines in Portugal. Phytopathol. Mediterr. 41:3-­18.
range of different species causing disease. Nevertheless, mini- Phillips, A.  J.  L., Alves, A., Abdollahzadeh, J., Slippers, B., Wing-
mizing inoculum in the vineyard by removing and destroying field, M. J., Groenewald, J. Z., and Crous, P. W. 2013. The Botryos-
all diseased wood at pruning time remains one of the most ef- phaeriaceae: Genera and species known from culture. Stud. Mycol.
fective means to reduce the risk of new infections, regardless of 76:51-­167.
the particular species involved. Pitt, W. M., Sosnowski, M. R., Huang, R., Qiu, Y., Steel, C. C., and
Management of Botryosphaeria dieback traditionally has Savocchia, S. 2012. Evaluation of fungicides for the management
been achieved by remedial surgery, i.e., the excision of diseased of Botryosphaeria canker of grapevines. Plant Dis. 96:1303-­1308.

38
Rolshausen, P. E., Úrbez-­Torres, J. R., Rooney-­Latham, S., Eskalen,  A., fruit storage and/or transit that may be imposed, and the ex-
Smith R. J., and Gubler, W. D. 2010. Evaluation of pruning wound tremely low tolerance for diseased fruit in the wholesale and
susceptibility and protection against fungi associated with grape- retail marketplace.
vine trunk diseases. Am. J. Enol. Vitic. 61:113-­119. In certain cultivars and under conducive preharvest weather
Úrbez-­Torres, J. R. 2011. The status of Botryosphaeriaceae spp. infect- conditions (ideally, foggy evenings and mornings, sunny af-
ing grapevines. Phytopathol. Mediterr. 50:S5-­S45. ternoons), Botrytis infections free of secondary contaminants
Úrbez-­Torres, J. R., and Gubler, W. D. 2009. Pathogenicity of Botryo-
sphaeriaceae species isolated from grapevine cankers in California.
can develop in the ripening clusters, giving rise to the so-­called
Plant Dis. 93:584-­592. “noble rot.” This form of the disease is desirable for some wine
Úrbez-­Torres, J. R., and Gubler, W. D. 2011. Susceptibility of grape- styles and is an important component of some exceptional and
vine pruning wounds to infection by Lasiodiplodia theobromae and highly priced sweet white wines.
Neofusicoccum parvum. Plant Pathol. 60:261-­270.
Úrbez-­Torres, J. R., Battany, M., Bettiga, L. J., Gispert, C., McGourty, Symptoms
G., Roncoroni, J., Smith, R.  J., Verdegaal, P., and Gubler, W.  D. Although rotting berries are the most frequent and problem-
2010. Botryosphaeriaceae species spore trapping studies in Cali- atic symptom of infection by B. cinerea, blights (sudden, severe
fornia vineyards. Plant Dis. 94:717-­724. necrosis of tissue) and rots (decomposition and putrefaction of
tissue) can occur on all herbaceous tissues of the vine. Early
(Prepared by J. R. Úrbez-­Torres, A. J. L. Phillips, in the growing season, infected buds and young shoots may
and W. D. Gubler) turn brown and desiccate (Fig. 65). Later in the preflowering
period, particularly following prolonged periods of rain, fog,
and/or dew, large irregular, necrotic patches appear on scat-
tered leaves, often localized at the leaf base or on the edge of
Botrytis Bunch Rot and Blight the lamina (Fig. 66) where water accumulates. Infection of
young clusters can occur that appear as brown to black spots
Botrytis bunch rot or gray mold occurs in vineyards through- on rachises (Fig. 67), calyptra (Fig. 68), and pedicels of inflo-
out the world, although it is most severe in regions experienc- rescences. Under humid or wet conditions, infections can blight
ing moderate temperatures and rainfall or extended periods the entire cluster, with infected tissues yielding the character-
of high humidity between veraison and harvest. The disease istic gray, cottony mycelia and conidia of the fungus (Fig. 69).
can cause serious economic losses by reducing both crop yield Young, immature berries may develop a soft brown rot with
and quality. Yield reductions may be associated with damaged characteristic sporulation if the early summer is extremely wet.
flower clusters early in the season or, more commonly, berry From approximately veraison onward, berries can begin exhib-
rot pre-­and/or postharvest. Economic losses also may accrue iting symptoms from previously quiescent infections that oc-
from the costs associated with manually sorting diseased clus- curred earlier in the season, typically near flowering. Small,
ters pre-­or postharvest, and from the lower prices received for water-­soaked lesions appear on the fruit, or a symptom known
diseased fruit or buyers rejecting it outright for failure to meet as “slip skin,” in which the berry skin appears shiny (Fig. 70)
quality standards. In wine production, quality losses result and is separated easily from the flesh by rubbing, can develop.
from the modified chemical composition of diseased berries. Tufts of gray, fungal mycelia and characteristic conidia appear
For example, B. cinerea converts simple sugars (glucose and on the surface of infected berries (Fig. 71). Often, rotted ber-
fructose) to glycerol and gluconic acid and secretes polysaccha- ries first develop near the center of the cluster (Fig. 72); such
rides such as β-­glucan, which hinder the clarification of wine. It infection loci can spread quickly from berry to berry in a pro-
also produces an enzyme (laccase) that catalyzes the oxidation cess known as “nesting” (Fig. 73), and infection may eventually
of phenolic compounds, resulting in a browning of white wines engulf the entire cluster (Fig. 74). Additionally, other fungi and
and color instability in red wines. In table grape production, the
most serious damage is the loss of fruit quality due to berry rot
in the field, during transit or in storage. Post­harvest losses are
highly problematic for producers and shippers of table grapes
owing to the pathogen’s propensity to remain quiescent and
undetected within clusters until tissues senesce, its ability to
grow at near-­freezing temperatures, the extended periods of

Fig. 66. Sporulating Botrytis cinerea on a

Fig. 65. Browning and desiccation of young shoots infected with leaf of cv. Müller-­Thurgau. (Cour­tesy R. C.
Botrytis cinerea. (Cour­tesy A. Wise) Pearson)

39
bacteria can invade the rotting berries, producing a variety of
colors, smells, and tastes (see Sour Rot). Infected table grapes
in cold storage often develop a wet rot of the rachis, laterals,
and pedicels, which can become covered by a mycelial mat,
sometimes with sporulation. Individual infected berries de-
velop circular, brown lesions that gradually cover the whole
fruit, culminating in the “slip-­skin” symptom. In severe cases,

Fig. 70. Shiny “slip skin” appearance of a ‘Pinot Noir’ berry in-
fected with Botrytis cinerea. (Cour­tesy W. Mahaffee)

Fig. 67. Dark lesion caused by Botrytis cinerea on young rachis.

(Cour­tesy W. D. Gubler)

Fig. 68. Necrosis of young florets due to infection by Botrytis Fig. 71. Characteristic tufts of gray conidia
cinerea. (Cour­tesy W. Mahaffee) of Botrytis cinerea arising from infected
grape berries. (Cour­tesy W. F. Wilcox)

Fig. 69. Blighting of young cluster by Botrytis cinerea, with char- Fig. 72. Initial disease locus of Botrytis cinerea established within
acteristic sporulation of the fungus. Infection has progressed into the center of a cv. Pinot Noir cluster, radiating outward. (Cour­tesy
the nodal region of the shoot. (Cour­tesy A. Wise) W. Mahaffee)

40
infections can spread among tightly packed berries and clusters moisture-­limiting conditions. Conidiophores develop directly
to cause extensive loss (Fig. 75). from hyphae and are generally long (1–5 mm), stout, dark
Late in the growing season, poorly hardened shoots may brown, irregularly branched near the apex, with enlarged apical
have patches of bleached bark where black sclerotia or gray- cells bearing clusters of conidia on short sterigmata (Fig. 77).
ish, sporulating mycelia frequently are present. The infected Conidia are unicellular (8–14 × 6–9 µm), generally multinucle-
part mostly surrounds a node (Fig. 76), suggesting entry of the ate, ovate, and individually hyaline but appearing grayish in
fungus through a diseased leaf or petiole or through a leaf scar. mass with a smooth surface.
Newly grafted grapevine cuttings incubated in callusing The mycelium can differentiate into two types of survival
boxes at temperatures near 30°C and at high humidity may be structures: chlamydospores and sclerotia. Chlamydospores are
infected and destroyed by rapid growth of the pathogen. The
fungus also can develop beneath the film of paraffin used to
seal the junction of grafted vines, thereby inhibiting develop-
ment of the union between rootstock and scion.

Causal Organism
The causal fungus is the ascomycete Botryotinia fuckeliana
(de Bary) Whetzel, although only the anamorph (asexual form),
Botrytis cinerea Pers., is commonly observed in vineyards. B.
cinerea will grow on most media suitable for the general cul-
tivation of fungi. Hyphae are branched, septate, and hyaline
but can appear tan to black when melonization occurs during

Fig. 75. Storage rot caused by Botrytis cinerea. (Cour­tesy R. C.

Pearson)

Fig. 73. “Nesting” pattern of spread of Botrytis cinerea through a

cv. Chardonnay cluster, resulting from physical contact of healthy
with diseased berries. (Cour­tesy W. F. Wilcox)

Fig. 76. Bleached nodal regions of 1-­year-­old cane infected with

Botrytis cinerea. (Cour­tesy W. D. Gubler)

Fig. 74. Culmination of berry-­ to-­

berry spread
of Botrytis cinerea throughout an infected cv. Fig. 77. Conidia on conidiophore of Botrytis cinerea. (Cour­tesy
Chardonnay cluster. (Cour­tesy R. C. Pearson) R. Wind)

41
hyaline cells of extremely variable shape and size, with termi- the free-­moving air currents above it, effecting longer-­range
nal or intercalary placement. Chlamydospores can germinate dispersal. In general, however, conidia produced from sources
to produce microconidia, hyphae, or macroconidia. Sclerotia on the ground and within the canopy are transported <1 m from
can be of both a macro-­and micro-­form. Macrosclerotia are their origin.
brown to black, irregularly shaped, up to 5 mm in diameter, Once deposited on a suitable substrate, conidia can germinate
and firmly attached to a substrate. They have a rind of thick-­ if conditions are favorable, but can otherwise remain dormant
walled cells and a medulla of filamentous hyphae loosely ar- for long periods of time. Germination and subsequent infection
ranged in a gelatinous matrix. Microsclerotia are individual or can occur at temperatures between 0 and 30°C, with 15–25°C
small groups of hyphal cells that have become thickened and being broadly optimal and 18–20°C being ideal. These pro-
are sometimes melonized. Microsclerotia germinate to pro- cesses are favored by the presence of free water (e.g., rain or
duce mycelia, whereas macrosclerotia produce either conidia dew), but also can occur in its absence when relative humid-
or, following sexual recombination, apothecia. Apothecia are ity is above 93% for an extended period. Conidial germination
cupulate, stalked, and brownish, with a stipe about 4–5 mm requires an exogenous nutrient source; thus, it and subsequent
long. Ascospores (7 × 5.5 µm) are hyaline, one-­celled, ovoid-­ infection are favored by the presence of damaged plant tissues.
ellipsoid, and smooth. At any time during the infection process, B. cinerea can enter
B. cinerea may also produce microconidia on phialides. The a state of quiescence, in which the pathogen remains alive but
phialides usually arise freely from single hyphal cells on old no longer grows. The cause of quiescence is poorly understood
aerial mycelium. They also can develop from germ tubes but appears to be plant mediated in response to changing envi-
produced by macroconidia, mature hyphae, or inside empty ronmental conditions. Such infections are increasingly likely to
hyphal cells, and from appressoria and sclerotia. The micro- become active again as tissues progressively senesce or should
conidia (2–3 µm in diameter) are hyaline and one celled, and they become moribund.
are formed in chains or in clusters enclosed within a protective Young leaves, clusters, and shoots can become infected in
covering (hülle). the spring when daytime temperatures regularly exceed 15°C
and moisture conditions are sufficient to induce formation of
Disease Cycle and Epidemiology spores from overwintering survival structures and their sub-
Botrytis bunch rot has a complex disease cycle, influenced sequent germination and penetration of host tissues. Young
by multiple pathogen-­host-­environment interactions, many of leaves may carry high levels of asymptomatic latent infections,
which are not well understood. This complexity and the myriad which can become active and sporulate if the leaves are killed
possible combinations of the factors involved likely underlie through natural causes or viticultural practices. Lesions on
the diversity of conclusions drawn from studies of the disease intact leaves and blighting of young, green shoots and inflo-
and its management in variable climates and production sys- rescences may become apparent after several days of rain or
tems around the world. fog if temperatures are favorable. It appears likely that disease
B. cinerea is a “weak” pathogen that requires an exogenous outbreaks following such long wet periods reflect an increase
nutrient source or a compromised host for successful infection in host susceptibility under these conditions, as conidia require
and colonization. Thus, highly succulent, necrotic, injured, or only 15 h of wetting to germinate and infect susceptible berries
senescing tissues are most susceptible. Old flower parts and at 15–20°C and B. cinerea preferentially colonizes numerous
ripe fruit are particularly important senescing tissues with re- host tissues when their water content is high. Although direct
spect to the epidemiology and economic impact of the pathogen losses from early infection of vegetative tissues are minimal,
on grapes. The fungus thrives under conditions of high humid- these can provide an important source of secondary inoculum
ity and still air. It has the capacity to remain quiescent, or la- adjacent to healthy inflorescences at the time of flowering.
tent, for extended periods in infected tissues, contributing to From bloom to the beginning of berry touch, inflorescences
the complexity and occasional unpredictability of the disease. and young clusters are highly susceptible to infection by B. ci-
All of these characteristics influence disease development and nerea. Furthermore, the structural parts of the clusters are
management. dusted with pollen then, which can serve as an exogenous food
B. cinerea is not specific to grapevines; it can infect almost source to support the pathogen’s growth. Berry infections that
all dicots, many monocots, and some Pteridophyta plant spe- occur during the period of bloom through early postbloom
cies under the proper conditions. It also can live as a normal typically remain quiescent, but sometimes become active as
resident in various dead plant tissues, providing the capacity fruit become ripe; such infections serve as sources for second-
to survive indefinitely as a saprophyte in climates to which it ary spread of bunch rot should activation occur preharvest, or
is adapted. In vineyards, it typically overwinters as sclerotia, they can initiate storage rot decay if they remain quiescent until
mycelia, or chlamydospores in infected grape tissues on the postharvest. Opinions and experiences differ with respect to
vine or vineyard floor. Old cluster components (rachides and the primacy of infections initiated during the bloom and early
mummified berries) and leaf tissues (petioles and blades) have postbloom period. Some authorities believe the period to be
been documented as particularly important sources of vineyard
inoculum in several regions. The pathogen also can over­winter
in asymptomatic weeds, becoming active and sporulating
once these plants senesce naturally the following season or are
killed by herbicide applications. In spring, conidia (or, rarely,
ascospores) are produced from these various sources (Fig. 78)
and function as primary inoculum. The production of conidia
is favored by successive interrupted periods of surface wet-
ness, moderate temperature, and changes in the atmospheric
humidity. Conidia are released largely by air movement, es-
pecially during periods of rapidly changing humidity, as well
as by splashing water, mechanical disturbances, or vertebrates
and insects. Although the latter animals can serve as vectors,
dispersal of conidia is primarily on wind currents, with con-
centrations in the air a function of the prevailing environment.
High wind velocities and accompanying turbulence facilitate Fig. 78. Conidia of Botrytis cinerea produced from sclerotia on
conidia escaping the canopy zone and becoming entrained in overwintered grape cane. (Cour­tesy W. D. Gubler)

42
the singlemost important stage in the progress of an epidemic, sus continued quiescence are poorly understood. Environmen-
whereas others contend its importance to be rivaled or even su- tal factors that have been shown to promote the development
perseded by events that occur during the preharvest period. To of rot from previously quiescent infections include persistently
some extent, such perspectives appear to be influenced by the high soil moisture during the postveraison period, high atmo-
specific contexts in which they are formed, including the likeli- spheric humidity during the immediate preharvest period, and
hood of significant preharvest rainfall occurring in the region. high levels of nitrogen in the berries. Various forms of stress,
Nevertheless, all workers agree that this is a potentially critical particularly wounding of the berries at the point of their attach-
phase in the disease cycle. ment to the pedicel, as may occur from high winds or cluster
Several infection pathways from the floral organs to the ber- compaction as the fruit swell before harvest, also have been
ries have been demonstrated. Early investigations of the phe- shown to activate quiescent infections. Injuries from compac-
nomenon suggested that B. cinerea first infects the style during tion and the resulting activation of quiescent infections are an-
bloom, and it grows from there into the ovule and remains qui- other likely reason that bunch rot often begins in the center of
escent until the berry ripens; however, subsequent investigators the cluster.
were largely unable to reproduce this finding. In contrast, sev- Berries that become symptomatic as a result of activated qui-
eral investigators have demonstrated infection of the receptacle escent infections are usually limited in number. Nevertheless,
area, both directly through wounds exposed as the calyptra are their economic impact can be vastly disproportionate to their
shed (“cap scars”) and via growth of fungal germlings through actual numbers in table grape production, where commercial
the stamens and into the receptacle at their point of attachment. tolerance for diseased fruit is virtually nonexistent and symp-
Dead floral tissues also function as important sources of berry toms may not appear until after bunches have been packed and
infection when they become infected during flowering (Fig. 79) shipped or placed into storage. In wine grape production, sig-
and then adhere to the cluster after they are shed, becoming nificant losses from Botrytis bunch rot are usually the result
trapped within as the bunches close. These food sources sup- of extensive secondary spread during the postveraison period,
port saprophytic growth of the fungus until it is able to move with activated quiescent infections serving an important role as
into the subtending berries as their resistance breaks down dur- primary disease foci that initiate the epidemic. Such spread is
ing ripening. Such infections via blossom debris likely contrib- by far most severe in tightly compressed bunches, which facili-
ute to the common phenomenon of bunch rot originating near tate rapid spread of the fungus from berry to berry through my-
the center of the cluster, as does similar saprophytic growth celial growth at the point of contact, resulting in the common
from unpollinated, aborted fruitlets that become infected near “nesting” pattern of spread. For example, it has been shown
flowering (Fig. 80) and remain trapped within the bunches after that preharvest disease can progress virtually throughout a
they close. compacted cluster from a single berry that develops rot post-
In addition to floral organs, B. cinerea also readily estab- veraison, with only minor spread developing in loose clusters
lishes quiescent infections within the structural cluster parts on the same vine. High berry nitrogen content and high soil
(rachises and pedicels) while they are young. Although these water content (presumably leading to elevated berry water con-
tissues develop moderate resistance as they age, conidia and tent) also have been shown to increase the rate of secondary
germlings can survive on their surfaces for extended periods of disease development in addition to increasing the activation of
time. In contrast, healthy grape skins are relatively resistant to quiescent, primary infections.
infection and colonization early in their development. However, Conidia produced on symptomatic berries also can be re-
damage to the berry skin by other pathogens (e.g., powdery sponsible for secondary disease spread. Infection may occur
mildew), insects, sun scald, or mechanical factors increases the via direct penetration of the skins as their resistance decreases
likelihood of its infection by B. cinerea and eventual rot of the near maturity or through wounds caused by various factors
entire berry as it ages. including rain cracking, bird claws and feeding, and insects.
Although young, green berries may become rotted by B. ci- Insects implicated as initiators of wounds subsequently colo-
nerea if the postbloom weather is extremely wet, the frequency nized by B. cinerea and/or as vectors of fungal spores to these
of diseased green berries typically is very low. Rather, in most wounds include the grape berry moth (Lobesia botrana), the
regions and years, berry rot symptoms are expressed from rip- New Zealand flower thrips (Thrips obscuratus), the Mediter-
ening onward, when the senescing fruit apparently are no lon- ranean fruit fly (Ceratitis capitata), the light-­brown apple moth
ger able to maintain quiescent infections in a latent state and (Epiphyas postvittana), and the vinegar fly (Drosophila me-
the newly active fungus colonizes the fruit. Studies have shown lanogaster). Following inoculation of fresh wounds, berries
that the majority of quiescent infections typically remain so
through harvest, but the factors that favor their activation ver-

Fig. 79. Grape floral tissue infected with sporulating Botrytis cine- Fig. 80. Aborted fruitlets infected with Botrytis cinerea and sporu-
rea. (Cour­tesy S. M. Zitter) lating during the preharvest period. (Cour­tesy S. M. Zitter)

43
typically become necrotic and sporulate within approximately have successfully reduced cluster compaction but have some-
1 week, providing further opportunity for epidemic spread times resulted in poor yield or reduced bloom the following year.
through vegetative and conidial inoculum. In regions where economic loss from Botrytis bunch rot is a
regular concern, effective fungicides must usually be applied in
Management addition to implementing appropriate cultural practices. Fun-
Perhaps more than for any other major fungal disease of the gicide efficacy is a function not only of the inherent product
grape fruit and foliage, control of Botrytis bunch rot is dependent efficacy and application timing but also of good spray cover-
upon a conscientious integration of feasible cultural practices age, which can be difficult to achieve late in the season without
with targeted chemical and/or biological treatments appropri- good canopy management. Most fungicides traditionally used
ate to climatic conditions and market demands. Although many to control other diseases have limited to no activity against
considerations go into the initial choice of cultivar, clone, and B. cinerea, at least at the standard rates employed. Therefore,
planting site, growers in regions prone to Botrytis should re- several classes of fungicides have been developed which are
member that such choices can have a profound effect on their active primarily against this fungus and a few related species,
ability to manage this disease for the lifetime of the vineyard. including the dicarboxamides, the anilinopyrmidines, and the
Cultivars vary considerably in their susceptibility to Botrytis hydroxyanilides. Some more recent QoI (strobilurin) and SDHI
bunch rot because of differences in berry chemistry, active re- (carboxin) fungicides also have shown good activity. B. cinerea
sponses to attempted infection, and cluster architecture. A fac- is a pathogen at high risk for fungicide resistance development,
tor sometimes as important as cultivar, but one whose choice owing to its high reproductive potential, the ready dispersal of
entails fewer commercial implications, is that of clone; loose-­ its conidia, and the multiple sprays sometimes applied for its
clustered clones of any given cultivar typically have fewer control; implementing basic resistance management practices
problems with Botrytis bunch rot than those with tight clusters, is critical for the sustainable use of these products.
and such differences can be pronounced. Planting sites, row On the basis of the disease epidemiology, potential fungi-
spacings, and row orientations that favor good air movement cide applications are traditionally focused on four phenological
through the canopy similarly aid in the overall management of growth stages: (i) mid-­bloom through the beginning of fruit set,
the disease. Rootstocks matched to the site to control vine vigor to prevent establishment of latent infections within the cluster
make necessary canopy management far easier. and limit the colonization of eventual blossom debris; (ii) just
In climates conducive to Botrytis development, canopy man- before berry touch, the last opportunity to fully cover all berry
agement is a critical component of a control program. Through surfaces; (iii) the beginning of veraison, to protect healthy ber-
canopy management, the microclimate around the berry clus- ries as they become susceptible to new infections and (as pro-
ters can be manipulated to reduce relative humidity and the du- vided by some systemic fungicides) to suppress the activation
ration of berry wetness by increasing airflow, light penetration, of existing latent infections; and (iv) one or more applications
and temperature. This alteration of the berry microclimate can beginning 2–4 weeks after the veraison application, to control
be done through the choice of training system and the subse- secondary spread. The importance of each timing varies among
quent imposition of shoot positioning, hedging, and leaf re- regions and years, depending largely on cultivar, cultural prac-
moval. Shoots should be positioned to develop an evenly spaced tices, and the weather conditions during that growth stage. In
canopy, which should be maintained throughout the season so regions with wet springs but dry summer and preharvest condi-
that light and air can continue to move through it. Leaf removal tions, the early applications are often considered most effec-
further increases light penetration and air flow, as well as the tive. In New York State, where rainfall throughout the growing
deposition upon clusters of spray materials applied to provide season varies greatly among years, a series of spray timing tri-
bunch rot control, and has proven to be a valuable practice in als conducted across three decades showed the critical num-
multiple regions where it has been implemented. For best re- ber and phenological timing of sprays to be inconsistent and
sults, leaf removal should be conducted as soon as possible weather dependent. Disease forecasting systems are currently
after fruit set. Earlier removal may result in poor set or return used in some regions to predict the occurrence or probability
bloom (although such is not always true and some studies have of infection events based upon environmental factors, although
indicated benefits from this practice), and later removal may di- the complex set of factors regulating bunch rot development has
minish some of the potential benefits in addition to making the restricted the utility of this approach in many others. In some
fruit more susceptible to subsequent sun scald. In regions and cases, models may be more useful for predicting the onset of
years where dry weather prevails throughout most of the sum- symptom expression than the potential severity of disease at
mer, particularly in the preharvest period, such cultural prac- harvest or following cold storage.
tices alone may provide adequate levels of bunch rot control. Applications of several registered biological control products
In arid regions, irrigation should be managed to balance can- based upon antagonistic microorganisms (e.g., species of the
opy vigor and avoid excessively succulent berries with tightly fungal genera Aureobasidium, Trichoderma, and Ulocladium,
compacted clusters. The judicious use of nitrogen fertilizers fermentation products of Bacillus spp. bacteria) have provided
will limit the potential for infection by reducing excessive can- a measure of control in some regions but have been ineffective
opy growth in addition to maintaining berry tissues in a physio- in others, particularly when disease pressure has been signifi-
logical state less conducive for fungal colonization. cant. For fresh market grapes, postharvest treatment or expo-
There are multiple reports of reducing disease severity sure to volatile compounds that inhibit growth of B. cinerea,
through the use of chemical growth regulators to loosen clus- such as sulfur dioxide, are typically necessary to insure against
ter compactness and thereby limit the spread of disease through decay in storage and extend shelf life.
berry-­to-­berry contact. Although common in some table grape
production systems, this technique has several potential pitfalls Selected References
on wine grape cultivars that must be addressed, including re-
Broome, J. C., English, J. T., Marois, J. J., Latorre, B. A., and Aviles,
duced fruit set and/or return bloom, in addition to local product J. C. 1995. Development of an infection model for Botrytis bunch
registration issues. Nevertheless, the technique offers significant rot of grapes based on wetness duration and temperature. Phyto­
opportunity when these pitfalls can be addressed successfully. pathology 85:97-­102.
Loosening clusters through a mechanical reduction of flower Coley-­Smith, J. R., Verhoeff, K., and Jarvis, W. R. 1980. The Biology
numbers during bloom, e.g., with a plastic brush as is practiced of Botrytis. Academic Press, London, UK.
in some table grape production regions, also has been shown to Elmer, P. A. G., and Michailides, T. J. 2004. Epidemiology of Botrytis
limit berry-­to-­berry spread but is labor intensive and costly. Ex- cinerea in orchard and vine crops. Pages 243-­272 in: Botrytis: Biol-
perimental programs utilizing leaf removal at or before bloom ogy, Pathology, and Control. Y. Elad, B. Williamson, P. Tudzynski,

44
 and N. Delen, eds. Kluwer Academic Publishers, Dordrecht, The Pieces of invaded roots or stems, when put in a moist cham-
Netherlands. ber, are rapidly covered with abundant growth of white hyphae.
Gubler, W. D., Marois, J. J., Bledsoe, A. M., and Bettiga, L. J. 1987. The fungus also may produce sclerotialike masses on the sur-
Control of Botrytis bunch rot of grape with canopy management. face of infected tissues.
Plant Dis. 71:599-­601.
Hill, G.  K., Stellwaag-­K ittler, F., Huth, G., and Schlösser, E. 1981. Causal Organism
Resistance of grapes in different developmental stages to Botrytis
cinerea. Phytopathol. Z. 102:328-­338.
The causal organism, Rosellinia necatrix Prill. (anamorph
Holz, G., Gütschow, M., Coertze, S., and Calitz, F. J. 2003. Occurrence Dematophora necatrix Hartig), produces nearly spherical,
of Botrytis cinerea and subsequent disease expression at different brown to black perithecia, aggregated and embedded in a brown
positions on leaves and bunches of grape. Plant Dis. 87:351-­358. web of hyphae on the host surface. Perithecia are about 1–2
Keller, M., Viret, O., and Cole, F. M. 2003. Botrytis cinerea infection mm in diameter. Young perithecia have a distinct protrusion
in grape flowers: Defense reaction, latency, and disease expression. around the ostiole that is visible with a dissecting microscope,
Phytopathology 93:316-­322.
Mlikota Gabler, F., Smilanick, J. L., Mansour, M., Ramming, D. W.,
and Mackey, B.  E. 2003. Correlations of morphological, ana-
tomical, and chemical features of grape berries with resistance to
Botrytis cinerea. Phytopathology 93:1263-­1273.
Nair, N. G., Guilbaud-­Oulton, S., Barchia, I., and Emmett, R. W. 1995.
Significance of carry over inoculum, flower infection and latency
on the incidence of Botrytis cinerea in berries of grapevines at har-
vest in New South Wales. Aust. J. Exp. Agric. 35:1177-­1180.
Thomas, A.  C., Matthee, F.  N., and Kotze, J.  M. 1981. Survival of
Botrytis cinerea from table grapevines in South Africa. Phytophy-
lactica 13:157-­160.
Vail, M. E., and Marois, J. J. 1991. Grape cluster architecture and the sus-
ceptibility of berries to Botrytis cinerea. Phytopathology 81:188-­191.

(Prepared by W. F. Wilcox, W. Mahaffee, and W D. Gubler)

Dematophora Root Rot

Dematophora root rot is a serious disease on many herba-
ceous and woody plants throughout much of the temperate
world. It is most common on deciduous fruit trees and grapes.
On grape it is commonly known as pourridié as well as auber-
nage, bianco, blanc, blanc des racines, blanquet, champignon
blanc, malbianco, mal nero, marciume radicale bianco, morbo
bianco, pourridié de la vigne, pourriture, Rosellinia root rot, Fig. 81. Hyphae of Dematophora necatrix
Weinstockfaule, white root rot, and Wurzelpilze. The disease growing from an infected plant under moist
has been reported mainly from European countries but also conditions. (Cour­tesy A. H. McCain)
on grape in North and South America, Africa, Australia, New
Zealand, India, the former Soviet Union, and Japan.

Symptoms
Symptoms of Dematophora root rot are not very diagnostic.
Diseased plants may die rapidly or slowly throughout one sea-
son, or may linger into a second year before succumbing. Vines
that linger frequently bear an excessively large crop the year
before they die. Diseased plants tend to be aggregated and to
occur in discrete areas of the vineyard.
The leaves remain attached on vines that die rapidly. On
vines that decline gradually, tendrils and leaves are weak and
stunted, wilting is common, and shoots may arise from the
base. Dead vines can be pulled easily from the soil because of
severe deterioration of the roots. Frequently, vines break off at
the soil line, where the fungus has weakened the wood. The
bark below the soil line is darkened and sloughs easily. At the
root crown, there may be a black, gummy ooze.
Under moist conditions, the fungus produces abundant hy-
phae on the surface of infected roots, giving them a white,
fluffy appearance (Fig. 81). The hyphae tend to grow along the
smaller roots and often form flattened strands in soil cavities
around the roots. As these fungal strands age, they darken and
may take on a tan or brown cast.
The fungus grows rapidly in the infected vine and produces
small, white plaques scattered throughout the wood (Fig. 82).
These plaques differ considerably from those of Amillaria mel- Fig. 82. Small, discontinuous plaques of
lea, which are confined to the area between the bark and the Dematophora necatrix on an infected root
wood (see Armillaria Root Rot). with bark removed. (Cour­tesy R. D. Raabe)

45
but ostioles on old perithecia are difficult to find. The perithecial warm and humid summers. When highly susceptible cultivars
stage takes several years to develop and is rarely found. are grown in such climates the potential exists for complete de-
Asci are cylindrical (8–12 × 250–380 µm), long-­stalked, and foliation and crop destruction in the absence of effective control
unitunicate. The eight ascospores are one celled, cymbiform, programs. The disease was first described in 1834 by Schwein-
straight or curved, and dark brown. They measure 5–8 × 3–50 itz on Vitis aestivalis in the southeastern United States, and was
µm and have a longitudinal slit running parallel to the long axis considered to be of minor importance on this and other mod-
of the spore for about one-­third of its length. erately to highly resistant North American grape species that
The conidial stage is composed of brown, rigid synnemata co-­evolved with the pathogen. However, downy mildew was a
up to 1–5 mm high. The stipe is 40–300 µm thick and is often principal reason (along with phylloxera) for the death of early
dichotomously branched toward the apex. Conidia (2.5 × 3–4.5 V. vinifera plantings established by colonists in eastern North
µm) are produced in large numbers. America. The pathogen was presumably introduced to Europe
Microscopic signs of the pathogen include distinct enlarge- via infected planting material and/or infested soil, as there
ments of the ends of hyphal cells next to the septa. This occurs were numerous introductions of New World vines to European
most frequently in older hyphae and is helpful in identifying farms and research institutions for at least 30 years prior to the
the fungus. discovery of the disease in the Bordeaux region in 1878. The
reproductive capacity of the pathogen, the near-­universal sus-
Disease Cycle and Epidemiology ceptibility of V. vinifera cultivars, and very conducive weather
The fungus grows through soil, using roots it has killed as a allowed downy mildew to spread rapidly across the continent,
food base. It is favored by the presence of moisture and organic and the disease was present in viticultural regions throughout
material, which also can serve as a food base, and is frequently Europe within a few years of its original discovery. Downy
found in soils high in clay content. The pathogen is spread by mildew is now a serious threat in virtually all viticultural re-
means of infested soil and infected planting material. Although gions worldwide where rainfall occurs regularly during the late
the Dematophora stage may produce many conidia, most re- spring and summer. Conversely, it is not a serious annual prob-
searchers have not been able to germinate them. Therefore, the lem in regions where low rainfall coupled with hot, dry weather
role of spores in the dissemination of the fungus is unclear. The in the spring and summer limits its spread (e.g., much of Argen-
fungus withstands drying and can remain viable in air-­dried tina, Australia, California and western North America, Chile,
pieces of wood in the laboratory for several years. It grows op- southern Peru, Spain, and much of the Mediterranean region).
timally at 22–28°C but does not grow at 31°C. However, serious losses can be experienced in some of these
areas when sporadic or atypical wet weather results in condi-
Management tions favorable for downy mildew.
Controlling Dematophora root rot is extremely difficult. Unlike in Vitis vinifera, there is a wide range of suscepti-
Many fumigants, such as allyl bromide, ammonium hydrosul- bility to downy mildew among Vitis interspecific hybrids.
fide, bromopicrin, carbon tetrachloride, chloroform, chloropic- Among North American grapevine species, V.  aestivalis and
rin, ethylene dibromide, and formalin pentachloroethane have V. labrusca are moderately susceptible, whereas V. cordifolia,
failed to control the disease in small-­scale experiments. In field V.  rupestris, and V.  rotundifolia are relatively resistant. Cer-
experiments, methyl bromide was ineffective in California but tain Vitis interspecific hybrid cultivars exhibit organ-­specific
was effective in Israel. Carbendazim and dazomet also have resistance: leaves may be moderately to highly susceptible
been reported as providing control. while fruit are highly resistant (e.g., Aurore and Delaware) or
The use of resistant rootstocks is a logical approach to con- leaves may exhibit moderate levels of resistance while clusters,
trol. Resistance has been reported in V.  cinerea, V.  vinfera tendrils, and shoot tips are highly susceptible (e.g., Chancel-
‘Carignane’, and in Solonis, a complex hybrid. In an experiment lor). Several new European cultivars (e.g., Regent) have been
established in an infested field in California, some survivors developed from progeny of crosses between V. vinifera and re-
included Iona, Red Malaga, Palomino, Dog Ridge, Salt Creek, sistant North American species in an effort to incorporate the
and St. George, V. arizonica, V. flexosa, and several hybrid se- most desirable qualities of both parental branches. These prog-
lections. Further testing of rootstocks is warranted. eny were selected for resistance to downy mildew, and resis-
tant clones were then repeatedly backcrossed to V. vinifera for
Selected References multiple generations, producing vines with the phenotype and
fruit quality characteristics of V.  vinifera while maintaining
Berlese, A.  N. 1892. Rapporti tra Dematophora e Rosellinia. Riv.
Patol. Veg. 1:1, 5-­17, 33-­46. downy mildew resistance introduced from the North American
Hansen, H.  N., Thomas, H.  E., and Thomas, H.  E. 1937. The con- species.
nection between Dematophora necatrix and Rosellinia necatrix.
Hilgardia 10:561-­565. Symptoms
Khan, A.  H. 1949. The root disease caused by Rosellinia necatrix The disease affects all green parts of the vine, particularly
(Hart.) Berl. Ph.D. thesis. University of California, Berkeley. leaves, inflorescences, and young berries. Lesions viewed from
Sivanesan, A., and Holliday, P. 1972. Rosellinia necatrix. Descriptions the upper leaf surface at first appear slightly darker and shiny,
of Pathogenic Fungi and Bacteria, no. 352. Commonwealth Myco- as if bruised. These spots rapidly become yellowish and circu-
logical Institute, Kew, England. lar, a symptom observed most commonly on young leaves and
Sztejnberg, A., Omary, N., and Pinkas, Y. 1983. Control of Rosellinia sometimes referred to as an “oil spot” (Fig. 83). Typically, the
necatrix by deep placement and hot treatment with methyl bromide. tissue within these lesions soon begins to turn necrotic (Fig.
Bull. OEPP/EPPO Bull. 13:483-­485. 84). Lesions become more angular and reddish brown as leaves
Viala, P. 1891. Monographie du Pourridié. Libraire de l’Académie de age and infected tissue eventually becomes completely necrotic
Médecine, Paris. C. Coulet, Montpellier, France.
(Fig. 85). Leaf lesions often are delimited by veins, particularly
when initiated late in the season, and late-­season lesions also
(Prepared by R. D. Raabe)
may be smaller than those initiated earlier (Fig. 86). Following
a damp night, sporulation is prominently visible on the lower
leaf surface immediately beneath these symptoms. Sporulation
Downy Mildew on young lesions appears as a dense, white, cottony mass (Fig.
87). With each repeated cycle of sporulation, the proportion of
Downy mildew, caused by Plasmopara viticola, is perhaps necrotic tissue increases until spore formation is limited to the
the most serious disease of grapevines in climates with relatively lesion’s margin (Fig. 88). Leaves with multiple lesions typically

46
abscise, and severe infection can result in defoliation (Fig. 89),
which limits the accumulation of sugars and flavors in fruit
and decreases the vine’s cold hardiness during the subsequent
winter. Infected shoot tips thicken, curl, and eventually become
brown and necrotic. Similar symptoms are seen on petioles,
tendrils, and young inflorescences, which may ultimately ab-
scise. Shoot tips and rachises that become infected as they are
rapidly elongating may show a severe epinasty or “shepherd’s
crook” appearance (Fig. 90). All of the preceding vine tissues

Fig. 86. Symptoms of downy mildew on a cv. Chardonnay leaf in

the late summer, with many lesions restricted in size and delim-
ited by leaf veins. (Cour­tesy W. F. Wilcox)

Fig. 83. “Oil spot” symptoms of downy mildew on young cv.

Delaware leaves. (Cour­tesy R. C. Pearson)

Fig. 87. Characteristic sporulation of Plasmopara viticola from

the underside of an infected cv. Ugni Blanc leaf. (Cour­tesy W. F.
Wilcox)

Fig. 84. Symptoms of downy mildew on the adaxial leaf surface

in early summer; necrosis within lesions becomes progressively
more severe with successive sporulation events. (Cour­tesy W. F.
Wilcox)

Fig. 88. Sporulation of Plasmopara viticola confined to the viable

Fig. 85. Old, necrotic downy mildew leaf lesions. (Cour­tesy W. F. margin of an otherwise necrotic lesion. (Cour­tesy D. M. Gadoury;
Wilcox) Reproduced, by permission, from Kennelly et al., 2007)

47
may support a white cottony coating of sporangiophores and Causal Organism
sporangia when conditions favor sporulation. The causal agent of grapevine downy mildew, Plasmopara
Young berries are highly susceptible, turning grayish when viticola (Berk. & M. A. Curt.) Berl. & De Toni, is an Oomy-
infected (gray rot). Under humid conditions, they too can be cete member of the family Peronosporales. Characteristics that
covered with a downy felt of sporulation (Fig. 91). Berries be- include heterokont flagella, cell walls containing glucans, and
come less susceptible as they mature, eventually becoming divergent molecular phylogeny place the Peronosporales within
impervious to direct infection as their stomata develop into len- the kingdom Chromista, taxonomically distinct from the true
ticels. However, the pedicels (berry stems) remain susceptible fungi (Mycota). However, ecologically and epidemiologically,
for some time after this, and older berries can become infected Oomycete plant pathogens share many similarities with the
if the pathogen expands into them from the pedicels, causing true fungi, and are treated as such in the practical aspects of
the so-­called brown rot or leather berry symptom. Berries so disease management.
infected usually will not support sporulation since they lack P. viticola is a biotrophic pathogen attacking members of the
the functional stomata through which sporangiophores must genus Vitis. It develops intercellularly within the parasitized
emerge, although sporulation may occur from the pedicels tissues of the vine in the form of tubular, coenocytic hyphae
or the berries themselves if a slight wound is made to permit 8–10 µm in diameter, bearing globular haustoria that are 4–10
egress of the sporangiophores. Infected older berries of white µm in diameter. Following penetration of the host cell wall,
cultivars may turn dull gray green (Fig. 92), while those of haustoria invaginate the host cell membrane.
black cultivars turn pinkish red (Fig. 93). Infected berries re-
main firm compared with healthy berries, which soften as they
ripen. These infected berries drop easily, leaving a dry stem
scar. Portions of the rachis or the entire cluster also may drop,
especially if prebloom infections cause girdling of the rachis.

Fig. 91. Characteristic sporulation of Plasmopara viticola on

young, infected berries following a humid night. (Cour­tesy R. C.
Fig. 89. Unsprayed vines severely defoliated by downy mildew, Pearson)
with adjacent fungicide-­
treated vines retaining healthy leaves.
(Photograph by W. McFadden-­Smith, Ontario Ministry of Agricul-
ture and Food; Queen’s Printer of Ontario, © 2014. Reproduced
with permission.)

Fig. 90. Necrosis and “shepherd’s crook” appearance (epinasty) Fig. 92. Dull gray-­green appearance of older white-­fruited ber-
of a rachis infected by Plasmopara viticola while expanding rap- ries infected by Plasmopara viticola. (Reproduced, by permission,
idly prior to bloom. (Cour­tesy W. F. Wilcox) from Kennelly et al., 2005)

48
 P. viticola is heterothallic; hence, sexual reproduction occurs Disease Cycle and Epidemiology
only when two isolates of opposite mating types are within The disease cycle is illustrated in Fig. 96. In temperate cli-
close proximity in the same tissue. For this reason, initiation mates, P. viticola overwinters as oospores in fallen leaves or,
of the sexual stage may be delayed until disease increases to a more commonly, in the surface layers of soil as infected leaves
level or persists for a duration that makes the chance pairing of are consumed and excreted by detritivores or otherwise decom-
sexually compatible isolates possible. Antheridia and oogonia pose. Epidemics can be initiated once suitable host tissue is
derive from hyphal tips wherein, following meiosis, the hap- present and these oospores are sufficiently warmed and moist-
loid nucleus of the antheridium migrates to and then fuses with ened to initiate germination. The precise conditions for oo-
that of the oogonium, forming a diploid oospore (20–120 µm spore germination have not been determined; however, based
in diameter). Oospores are most commonly recovered from in- on studies conducted with other Oomycetes, it is probable that
fected leaves, often near the periphery of distinct lesions, but soil moisture contents between field capacity and saturation
also throughout the lamina of leaves that exhibit numerous are most favorable. Upon production of primary sporangia
small colonies and abundant sporulation along the major and from the germinating oospores, zoospores are released dur-
minor veins. Oospores are robust survival structures resistant ing episodes of soil saturation and are dispersed to grapevines
to unfavorable temperatures and drought, and can survive more by splashing water droplets or in windblown aerosols derived
than one season in vineyard soil. The temporal limit of oospore from them. Zoospores that are deposited on green tissues swim
viability has not been determined for P. viticola, but it has been through water films to stomata on the lower leaf surfaces, shoot
shown to exceed 10 years for at least a fraction of the popula- tips, inflorescences, and young berries by means of flagellar
tion in some other Oomycete species. propulsion. Then, they shed their flagella and encyst, forming
Oospores germinate via production of one or occasionally a cell wall. An infection peg emerges from each cyst and pen-
two slender germ tubes (2–3 µm in diameter and of variable etrates the stoma. Under optimal conditions, the elapsed time
length), which terminate in a pyriform primary sporangium (28 between zoospore release and their penetration of the host can
× 36 µm). Primary sporangia remain attached to the germ tube be <90 min. Infections from oosporic sources are frequently
and, under saturated conditions, release approximately 30–60 associated with rain events of at least 2–3 mm coincident with
zoospores at least 3 h after oospore germination begins; some temperature ≥10°C during the rain event, beginning in the early
literature indicates that this process takes 10 h. Portions of the stages of vine growth (as little as 10 cm of shoot growth in
oospore population may continue to germinate as long as envi- some reports). Depending upon the primary inoculum load in
ronmental conditions remain favorable throughout the summer. the vineyard, the favorability of rain and temperature, and the
Asexual reproduction, responsible for secondary cycles of
the disease, results in the formation of ellipsoid and hyaline
sporangia (14 × 11 µm), which are borne upon sterigmata at
the tips of dendritic sporangiophores (140–250 µm) (Fig. 94)
that emerge through stomata (Fig. 95). This requirement for
stomatal emergence limits the tissues and locations from which
sporulation can be observed, e.g., only on the abaxial (under)
side of leaves and on young berries. Detached sporangia in a
water film quickly (20–30 min at optimal temperatures) cleave
four to 10 biflagellate zoospores (6–8 × 4–5 µm) that are im-
mediately released through a pore in the side of the sporangial
wall. Zoospores are generally uninucleate, rarely bi-­or multi-
nucleate. Zoospores as well the vegetative hyphae are diploid.

Fig. 94. Dendritic sporangiophore of Plasmopara viticola, bear-

ing mature sporangia upon terminal sterigmata. (Cour­tesy H.-­H.
Kassemeyer)

Fig. 93. Pinkish-­red berries of a black-­fruited

cultivar infected by Plasmopara viticola near
the end of their susceptible period. (Cour­tesy Fig. 95. Sporangiophores of Plasmopara viticola emerging through
W. F. Wilcox) stomata on the underside of a leaf. (Cour­tesy H.-­H. Kassemeyer)

49
Fig. 96. Disease cycle of downy mildew of grape. (Cour­tesy N. Schoepe)

innate susceptibility of the cultivar, the first infection event rents disseminate the sporangia to new host tissue where they
may rarely result in an incidence of leaf or cluster infection germinate by releasing zoospores, which initiate a new round
approaching 50%. However, when one or more of these factors of secondary infections as per the process described above.
is suboptimal, repeated secondary cycles are much more com- Infection typically requires a rain event to dislodge the spo-
monly required before disease becomes severe. rangia from their sporangiophores and provide the surface mois-
Upon penetration of the stoma by zoospores (originating from ture necessary for zoospore release and motility, although this
either oosporic or asexual secondary sporangia), the infection can also happen with heavy dew. Following release of the spo-
peg extends into the substomatal cavity, where it dilates into a rangia, the duration of wetting required for infection to occur
vesicle. From the substomatal vesicles, hyphae grow into the is relatively brief: approximately 1.5–2 h at 15–25°C, whereas
surrounding intercellular space and form numerous branches. 4, 6, and 8 h may be required at 10, 5, and 30°C, respectively.
Spread of the mycelium is limited by the veins, frequently re- Symptoms generally appear within 5–6 days when postinfec-
sulting in a mosaic pattern of sporulation and necrosis in older tion temperatures remain between 18 and 26°C, although the
leaves. Once colonization has developed to the extent that spor- incubation period can be as little as 4 days on highly suscep-
ulation is possible, the subsequent length of the latent period is tible tissues under optimal environmental conditions. Tempera-
dependent upon the occurrence of exacting environmental con- tures substantially lower or higher than the optimum persisting
ditions for this to occur: at least 4 h of darkness at temperatures for a prolonged period can extend the incubation period signifi-
>12.5°C and a relative humidity of 95–100%. Under vineyard cantly, e.g., 12 days at 12 or 34°C, with temperatures interme-
conditions, minor temperature fluctuations and radiant cool- diate to the optimum producing correspondingly intermediate
ing of plant tissues during night hours typically cause water incubation period durations. At the coldest temperatures inves-
to condense upon them once the ambient relative humidity ex- tigated (8–10°C), the incubation period may last 16–19 days.
ceeds 90%; thus, sporulation can usually be expected when the Leaves are most susceptible to infection when emergent or
ambient relative humidity is near 90% at night unless the air undergoing expansion, but on susceptible cultivars they never
temperature is rising. reach a high level of resistance and once infected generally
Upon induction of sporulation, a secondary substomatal ves- become severely diseased if conditions remain favorable. Ber-
icle forms, from which develop the hyphae that protrude from ries acquire ontogenic (age-­related) resistance to direct infec-
the stomata and differentiate to produce the dendritic sporan- tions coincident with the conversion of functional stomata to
giophores. Sporangia form on their tips and, once mature, are lenticels, approximately 2–3 weeks after bloom. However, such
detached from the sporangiophores following the dissolution berries may still become diseased via the growth of pathogen
of a callose cross wall in water. This entire process, from in- mycelium from infected rachises and pedicels, which remain
duction of sporulation to release of sporangia, occurs within as susceptible to new infections for one or more weeks beyond
little as 4 h at an optimal temperature of 18–22°C. Wind cur- this time.

50
 Lesion longevity and production of sporangia are dependent The duration of their effectiveness is limited by both the rate of
upon the number of cycles of sporulation. Sporangium produc- vine growth (tissues present at the time of application are the
tion is maximal through the first or second sporulation event most completely protected) and reductions of the initial deposit
but declines rapidly with each successive event until most of resulting from washing off by rain and weathering through
the lesion becomes necrotic and spore formation is restricted to hydrolysis and photolysis. The duration of protection provided
the periphery, generally once the lesion has sporulated four to by such fungicides can, therefore, vary greatly (e.g., from 3–14
five times. In the vineyard, ungerminated sporangia die within days, typically 7–10 days) depending upon vine growth, post­
8–10 h after sunrise under clear skies but remain viable for at application weather, the retentive properties of the fungicide,
least 48 h after formation if conditions are overcast. There are and its innate efficacy against downy mildew.
some reports of survival extending up to 5–7 days; this would Over the past 30–40 years, many groups of fungicides ac-
provide the potential for long-­distance dispersal, which could tive against downy mildews have been developed which exhibit
be meaningful in new viticultural districts if the pathogen was variable degrees of systemicity, i.e., absorption by and trans-
not yet established. location within the plant. These include cymoxanil, phenyl-
The complex interactions between temperature, daylight, amides, QoI (e.g., strobilurin) and QoO materials, carboxylic
rainfall, humidity, and host development have encouraged the acid amide (CAA) products such as dimethomorph and man-
creation of several models to forecast disease development dipropamid, iprovalicarb, ametoctradin, and phosphonates. In
based upon an integration of these various factors. Many, if addition to providing some residual protective activity of the
not most, are based upon the same foundational studies, as treated tissues, these also have the advantages of not being
amended by more recent work, and thus produce similar advi- washed off by rainfall and providing variable levels of postin-
sories when provided the same host and environmental inputs. fection (sometimes called “curative”) activity when applied be-
The most destructive epidemics occur in years with prolonged fore symptoms appear, i.e., during the incubation period. These
cloudy weather, frequent rain events coincident with tem- fungicides affect P. viticola most strongly within the early
peratures near the optimum of 25°C, high humidity resulting stages of colonization. At optimum temperatures for the patho-
in extended periods of evening leaf wetness, and the absence gen, the mycelium is well developed by 3 days after the start
of extended rain-­free periods with temperatures above 30°C. of infection, and most of the penetrating fungicides are un-
Regular, turbulent, evening thunderstorms particularly favor able to prevent the subsequent development of lesions when
the spread of the disease throughout a vineyard. applied beyond this stage. However, while still allowing lesion
development to proceed, applications of these materials during
Management the late incubation or initial-­symptom stages of infection often
Site selection and canopy management practices that pro- inhibit subsequent sporulation from such lesions, thereby re-
mote rapid drying of leaves, inflorescences, and clusters help ducing secondary spread of the disease from them. However,
to limit the potential for infection and disease spread. Mulches the penetrating fungicides typically act at a single or very lim-
that impede the movement of primary zoospores from the soil ited number of target sites in the metabolism of P. viticola, and
to the grapevines; early-­season elimination of low-­lying foliage there is a high risk of selecting strains of the pathogen resistant
most subject to infections derived from overwintering oospores to specific classes of these materials unless they are carefully
(e.g., shoots [“suckers”] arising from the basal trunk, or seed- managed. Once resistance begins to develop, the great repro-
lings from uncomposted pomace used for mulch [Fig. 97]); and ductive capacity of P. viticola (large numbers of spores widely
the destruction of nearby secondary inoculum sources (wild or dispersed in wind currents, a short incubation period promoting
feral grapevines, or abandoned vineyards) theoretically should multiple generations per year) allows a few resistant individuals
all aid in limiting disease development, to the extent that such to multiply to a level where the fungicide no longer provides
techniques are practical. However, because of the high suscepti- effective control, unless their reproduction is restricted some
bility of most cultivated grapevines, some degree of fungicidal other way. Therefore, it is often recommended that penetrating
control is almost always necessary in regions and years with fungicides with curative effects be applied in combination with
weather conditions conducive to downy mildew development. at least one other fungicide active against the local population
A number of surface-­acting fungicides (cupric salts, dithio- of P. viticola; this is typically, but not necessarily, a surface-­
carbamates, and phthalimides) are efficacious as preventive active protective fungicide at minimal risk for resistance
treatments. The risk of P. viticola developing resistance to development itself. Fungicide classes at risk of resistance devel-
them is low, as they are fungitoxic at multiple cellular sites. opment should be applied no more than two or three times per
season (all materials within a class), and applications during a
severe outbreak of the disease (large populations from which to
select resistant individuals) should be avoided.

Selected References
Blaeser, M., and Weltzien, H. C. 1978. Die Bedeutung von Sporangien­
bildung, ausbreitung und keimung fur die Epidemiebildung von
Plasmopara viticola. Z. Pflanzenkr. Pflanzenschutz 85:155-­161.
Hill, G. 1989. Effect of temperature on sporulation efficiency of oil­
spots caused by Plasmopara viticola (Berk & Curt. ex de Bary)
Berl. & de Toni in vineyards. Vit. Enol. Sci. 44:86-­90.
Kennelly, M. M., Gadoury, D. M., Wilcox, W. F., Magarey, P. A., and
Seem, R.  C. 2005. Seasonal development of ontogenic resistance
to downy mildew in grape berries and rachises. Phytopathology
95:1445-­1452.
Kennelly, M. M., Gadoury, D. M., Wilcox, W. F., Magarey, P. A., and
Seem, R. C. 2007. Primary infection, lesion productivity, and sur-
vival of sporangia in the grapevine downy mildew pathogen, Plas-
Fig. 97. Sporulation of Plasmopara viticola from the underleaf of mopara viticola. Phytopathology 97:512-­522.
an infected grape seedling growing on the vineyard floor; these Kiefer, B., Riemann, M., Büche, C., Kassemeyer, H. H. and Nick P.
plants originated from uncomposted seeds used for mulch. (Cour­ 2002. The host guides morphogenesis and stomatal targeting in the
tesy R. C. Pearson) grapevine pathogen Plasmopara viticola. Planta 215:387-­393.

51
Langcake, P., and Lovell, A. 1980. Light and electron microscopical An increased prevalence of the disease in California coincided
studies of the infection of Vitis spp. by Plasmopara viticola, the with a massive replanting of grapevines in Napa, Sonoma,
downy mildew pathogen. Vitis 19:321-­337. and Mendocino counties in the 1990s as a result of phylloxera
Mueller, K. 1936. Die biologischen Grundlagen für die Peronsopora- (Daktulosphaira vitifoliae [Fitch]) damage to the common and
bekämpfung nach der Inkubationskalender-­Methode. Z. Pflanzenkr. formerly resistant rootstock AXR1. Although the rootstocks of
Pflanzenschutz 46:104-­108. new vines had greater resistance to phylloxera, they were more
Rumbolz, J., Wirtz, S., Kassemeyer, H.  H., Guggenheim, R.,
Schäfer, E., and Büche, C. 2002. Sporulation of Plasmopara viti-
susceptible to the fungal causes of Petri disease. In the United
cola: Differentiation and light regulation. Plant Biol. 4:413-­422. States and other countries, the disease is reportedly linked to
Spencer-­Phillips, P.  T.  N., Gisi, U., Lebeda, A. 2002. Advances in water deficit or other stress factors, which favor symptom ex-
downy mildew research. Kluwer Academic Publisher, Dordrecht, pression in infected vines. Although widespread in occurrence,
Boston, London. vines showing decline due to Petri disease usually constitute a
Unger, S., Bueche, C., Boso, S., and Kassemeyer, H.-­H. The course of minor portion (1–5%) of a newly planted vineyard.
colonization of two different Vitis genotypes by Plasmopara viti- GLSD is an important disease of grapevine worldwide, both
cola indicates compatible and incompatible host-­pathogen interac- in the presence and absence of white rot. (Henceforth, the ac-
tions. Phytopathology 97:780-­786. ronym GLSD/EP is be used for simplicity, as most reports have
Wong, F. P., and Wilcox, W. F. 2001. Comparative physical modes of not distinguished between the single disease and the combina-
action of azoxystrobin, mancozeb, and metalaxyl against Plasmo- tion.) GLSD/EP can be found in California on wine, table, or
para viticola (grapevine downy mildew). Plant Dis. 85:649-­656. raisin grapes in years with high spring rainfall and high sum-
Wong, F. P., Burr, H. N., and Wilcox, W. F. 2001. Heterothallism in mer temperatures. The same disease is present across Europe
Plasmopara viticola. Plant Pathol. 50:427-­432.
in a wide range of climates, as well as in North Africa and,
(Prepared by H.-­H. Kassemeyer, D. M. Gadoury, G. Hill, more rarely, in Australia and South Africa. Like Petri disease,
and W. F. Wilcox) GLSD/EP has increased in significance in California in recent
years and in Europe since the end of the 1980s. Leaf symptoms
that once were uncommon on vines less than 10 years old are
now common on vines 1–6 years old.
Esca, Petri, and Grapevine Leaf The disease affects crop quality and yield, as well as the
Stripe Diseases productive life of the vineyard. Losses are normally underesti-
mated because the expression of symptoms fluctuates consider-
Esca is a name given in antiquity to a disease of grapevine ably; a vineyard may exhibit variable disease incidence among
that appeared as a sudden, lethal wilting of the entire vine. It seasons, as individual infected vines may show symptoms one
was first formally described on grapevine in France as folletage year but not the next. In California, losses are greatest on table
in 1865, and the cause of death was later attributed to wood grape varieties, especially older Thompson Seedless (Sultana)
decay (white rot) caused by basidiomycetous fungi, mainly vineyards in the San Joaquin Valley. Affected table grape clus-
Phellinus igniarius and Stereum hirsutum; the term apoplexy ters are unmarketable because of their disagreeable appearance
was substituted for that of folletage. In 1926, another symptom and the acrid taste that can occur; they are also more suscep-
was linked to the same syndrome: interveinal chlorosis and ne- tible to Botrytis bunch rot. In Europe, wine grapes are also
crosis on the leaf blades, later described as leaf stripes, and the heavily affected, with Cabernet Sauvignon, Ugni Blanc, Sau-
term esca was officially assigned to the disease. This was done vignon Blanc, Mourvèdre, and Sangiovese being only some of
after it was recognized that the names esca and iska had been the most susceptible cultivars. Affected wine grapes have less
used since ancient times in southern Italy and a Greek region sugar and greater acidity than those from healthy vines, and
(Smirne) of the modern Turkey, respectively, to identify apo- generally produce lower-­quality wine.
plectic grapevines showing rotted wood, albeit in the absence
of leaf stripe symptoms. More recent research has attributed Symptoms
the foliar symptoms to ascomycetous vascular (tracheomycotic) The first symptom of infection by the vascular fungi can be
pathogens distinct from the wood decay organisms originally noticed in nursery material as a brown to black streaking of
described as the causal agents of esca. These vascular patho- the wood. Longitudinal sections show dark streaks, single or
gens can produce different symptoms and syndromes at dif- in bundles, appearing in cross section as spots or groups of
ferent stages in the life of the vine, variously termed as black black vessels along the wood rings. A black, gumlike substance
wood streaking of rootstock, Petri disease in young vines, and exudes from these spots within a few minutes after cutting
leaf stripe disease (also known as “young esca”). through affected vessels (Fig. 98). The streaking often starts
Presently, it seems advisable to use the term esca in its
original meaning of apoplexy and decay, and to assign the name
“grapevine leaf stripe disease” (GLSD) to the vascular diseases
associated with foliar symptoms. As it is very common to have
wood rot and leaf stripe disease on the same vine, especially on
vines greater than 8–10 years old, the term esca proper (EP =
GLSD + white rot) has been suggested to indicate the syndrome
of vascular disease and wood rot and therefore to include fo-
liar symptoms, i.e., a complex of two different diseases. This
complex of diseases is also known in the United States as black
measles, because the most frequent and important symptom ap-
pears on berries in the form of small, gray to purple to brown
spots on the fruit surface, making table grapes unmarketable.
Petri disease, initially called by names such as young vine
decline or black goo, occurs in many of the world’s produc-
tion areas. It is a form of decline usually associated with vines
less than 7 years old, showing fungal infection of the rootstock.
It has become most common in California’s North Coast pro-
duction region, but also has been reported in eastern North Fig. 98. Gumlike exudate within vessels of a young grapevine in-
America, Europe, Australia, New Zealand, and South Africa. fected with Phaeomoniella chlamydospora. (Cour­tesy W. D. Gubler)

52
at the graft union in young vines or at the surface of a pruning
wound on mature vines. These internal symptoms of fungal in-
fection may be related to the decline of young vines once they
are planted in the field (Petri disease).
Symptoms of Petri disease include reduced trunk diameter,
shortened internodes, stunted shoot growth, shoot dieback, and
chlorotic and/or necrotic leaves (Fig. 99). The most prominent
internal symptom is the presence of brown to black streaks or
spots in the xylem vessels of the woody cylinder, as described
above (Fig. 100).
The most visible symptom of GLSD/EP in California is a
peculiar berry spotting, particularly noticeable on white varie-
ties. The skin is peppered with small, tan to purplish spots (Fig.
101). These spots may appear any time between fruit set and
ripening, most commonly as berries are just attaining their full
size, and may affect entire or only parts of clusters. In both se-
verely affected vines and those showing early symptom expres- Fig. 101. “Measles” symptom of GLSD/EP. (Cour­tesy W. F. Wilcox)
sion, berries often crack and dry on the vine.
Shoot tip dieback, tendril dieback, and leaf collapse may
occur in the spring (Fig. 102). Leaf symptoms usually develop
on canes with fruit symptoms, but also can develop on those
with normal fruit. Typically, affected leaves display small,
chlorotic, interveinal areas that enlarge, eventually desiccating
and becoming necrotic; in dark-­fruited varieties, the chlorotic
tissue may turn red before desiccating (Fig. 103) or red mar-
gins may surround the dead interveinal areas. A succession of

Fig. 102. Tendril and shoot tip dieback, the first

symptoms of GLSD/EP in the spring. (Cour­tesy
Fig. 99. Field symptoms of young vines affected with Petri dis-
J. R. Úrbez-­Torres)
ease. (Cour­tesy J. R. Úrbez-­Torres)

Fig. 100. Xylem necrosis and wood streaking of a young grape-

vine with Petri disease, as viewed in longitudinal section. (Cour­tesy Fig. 103. Interveinal leaf-­reddening symptom of GLSD/EP on cer-
J. R. Úrbez-­Torres) tain dark-­fruited varieties. (Cour­tesy J. R. Úrbez-­Torres)

53
chlorotic/pigmented and necrotic tissues that alternate between wounds. However, this canker development has not been attrib-
major veins bordered by a strip of unaffected tissue produces uted to the Phaeomoniella or Phaeoacremonium spp. that are
a so-­called “tiger stripe” pattern (Fig. 104). Severely affected known to cause GLSD.
leaves drop and the cane may die back from the tips. Foliar The peculiar discontinuity from year to year of the foliar
symptoms may appear at any time during the growing season, symptoms of GLSD has not yet been explained. In California,
but they are most prevalent during mid-­and late summer. En- there appears to be a close correlation between symptom ex-
tire vines or only portions of a vine may be affected, but occa- pression and current year infection, with symptomatic vines
sionally the symptoms appear so quickly and dramatically that sometimes appearing fully healthy the following year and
the entire vine collapses and dies (apoplexy) (Fig. 105). The lat- again showing symptoms in an unpredictable manner after one
ter symptom is most commonly seen in mid-­season in regions or more additional years have passed. Foliar symptoms are re-
with higher summer temperatures. Apoplexy occurs most com- portedly linked to toxic metabolites (certain polysaccharides
monly in the Mediterranean areas of Europe, and some workers and polypeptides, scytalone, and isosclerone) produced by the
have suggested that it may be a symptom of a distinct disease causal fungi Phaeomoniella chlamydospora and Phaeoacre-
that can occur in conjunction with GLSD/EP. monium aleophilum. It is possible that the involvement of toxic
Internal symptoms of GLSD include the same brown to black metabolites in foliar symptomatology contributes to the com-
longitudinal streaks (Fig. 106) or spots that appear in the rings plex and still-­unclarified interaction between the pathogens, the
of xylem vessels and often exude a black, sticky gum when cut host, and environmental factors with respect to variable symp-
in cross section (Fig. 107), as described above for Petri disease. tom development.
A brownish-­red necrosis may also develop primarily along the White heart rot was the first internal symptom to be de-
central part of the trunk, similar to the sectorial necrosis caused scribed as typical of esca. However, even though this concept
by species in the Botryosphaeriaceae, Eutypa lata, and Pho- stood for over six decades after the disease was named and
mopsis viticola following their infection of the wood through foliar symptoms attributed to it, all attempts to reproduce the
foliar and fruit symptoms described above failed when vines
were inoculated with several basidiomycete fungi that caused
such wood decay. Recent research indicates that white rot in

Fig. 104. Interveinal necrosis and “tiger-­striping”

symptom of GLSD/EP. (Cour­tesy W. F. Wilcox)

Fig. 106. Internal wood streaking in a mature grapevine affected

with GLSD/EP, viewed in longitudinal section. (Cour­tesy J.  R.
Úrbez-­Torres)

Fig. 107. Internal wood symptoms in a mature grapevine af-

Fig. 105. Apoplexy (sudden collapse) symptom fected with GLSD/EP, viewed in cross section. (Cour­tesy J.  R.
of GLSD/EP. (Cour­tesy P. Lecomte) Úrbez-­Torres)

54
wood does not affect vine performance except for longevity. der phialides bearing a typically hyaline conidiogenous cell
Extensive decay in older vines has been associated with apo- that produces straight, 3–4 × 1–3 µm conidia. The mycelium
plectic symptoms, but apoplexy has not been reproduced by of Pm. aleophilum is honey brown, frequently producing a
inoculation with any pathogen. yellow pigment on oatmeal or potato dextrose agar (Fig. 109),
and supports phialides that produce ellipsoid to allantoid, 4–6
Causal Organisms × 1–3 µm conidia. Pa. chlamydospora produces tiny, Phoma-­
In California, the primary pathogen consistently associated like pycnidia on the exposed vascular tissue of grapevine cor-
with vines showing symptoms of Petri disease has been Pha- dons and spurs, which serve as sources of inoculum in infested
eomoniella chlamydospora (W. Gams, Crous, M. J. Wingf. & vineyards. Pa. chlamydospora has been isolated as a pathogen
Mugnai) Crous & W. Gams. The pathogen more closely associ- only on grapevine, with the exception of a single isolation from
ated with GLSD/EP of older vines in California vineyards is Convolvulus arvensis, which suggest a possible, albeit rare, risk
Phaeoacremonium aleophilum W. Gams, Crous, M. J. Wing- of infection from weeds.
field & L. Mugnai, although both pathogens occur together Togninia minima (Tul. & C. Tul.) Berl. (Diaporthales, Tog­
in many wood samples of cordons and spurs. However, Pa. niniaceae), the teleomorph of Pm. aleophilum, spreads via
chlamydospora is always the more prevalent of the two species ascospores produced by perithecia on infected vines. Though
associated with both Petri disease and GLSD/EP in Europe, Pm. aleophilum occurs in different host species including
Australia, and South Africa. Twenty-­five different Phaeoacre- stone fruits, olive trees, and kiwifruit vines, no perithecia
monium spp. have been isolated from grapevines to date, but have been found on these crops. Perithecia of T. minima have
Pm. aleophilum is the most prevalent worldwide and the only been found on grapevines exhibiting leaf stripe and black
one consistently associated with foliar symptoms. The internal measles symptoms in vineyards located throughout Califor-
wood, foliar, and fruit symptoms described for these diseases nia and South Africa; the perithecia are mostly aggregated,
above have been reproduced following inoculation with both (160–)250–285(–420) µm in diameter at their basal part and
Pa. chlamydospora and Pm. aleophilum. (200–)285–325(–400) µm tall, with a long, sometimes double
Both Pa. chlamydospora (Chaetothyriales, Herpotrichiel- neck. Perithecia of four other Togninia species have been asso-
laceae) and Pm. aleophilum produce conidia on phialidic co- ciated with GLSD on grapevines and have been found on trees
nidiophores. The initially yeastlike, whitish mycelium of Pa. such as ash (Fraxinus spp.) in riparian and forest ec­osystems
chlamydospora soon becomes dark green (Fig. 108), with slen- near vineyards. All have been shown to be pathogenic on
grapevine; however, T. minima is the most prevalent of these
species in vineyards.
The vascular disease caused by Pa. chlamydospora and Pm.
aleophilum is, especially in older vines, typically the result of in-
fection through pruning wounds. Later, this tissue is sometimes
colonized by basidiomycetous decay fungi, resulting in wood
rot. Species of the genus Fomitiporia appear to be among the
more common of such organisms involved, including F. medi-
terranea (=F. punctata) in Europe, where the white wood decay
symptom has been reproduced by inoculating grapevines with
this species. Fomitiporia mediterranea forms resupinate basid-
iocarps of a cinnamon color on grapevine trunks and various
woody host plants. Other common colonizers include F. poly-
morpha in California, F. australiensis in Australia, and vari-
ous Fomitiporia and Phellinus species in South Africa. Some
workers hypothesize that the succession of such decay organ-
isms following attack by the vascular fungi contributes to the
complexity of the symptomatology of EP/GLSD, although this
has never been demonstrated experimentally.

Fig. 108. Young, whitish (top) and older, dark-­

green (bottom) colonies of Phaemoniella
chlamydospora growing on malt agar. (Cour­ Fig. 109. Colony of Phaeoacremonium aleophilum produc-
tesy L.  Mugnai; Reproduced, by permission, ing a yellow pigment on potato dextrose agar. (Cour­tesy J.  R.
from Mugnai et al., 1999) Úrbez-­Torres)

55
Disease Cycle and Epidemiology be effective, so sprays must be applied in high water volumes
Phaeomoniella chlamydospora overwinters as pycnidia re- to thoroughly wet the cordons and spurs, such that the mate-
siding on the grapevine, most commonly in 3-­to 5-­year-­old rial is forced through exfoliating bark and down onto the dis-
pruning wounds. Mycelium formed on exposed infected wood eased tissues. Pruning grapevines before such applications is
can also produce conidia via its phialides. Spores are released recommended to improve coverage and to reduce the amount
throughout the year, but the number of spores released is very of chemical needed.
low during the coldest winter months (below 10°C) and during Infections of new pruning wounds can potentially be reduced
hot periods. The greatest numbers of spores are usually trapped by protecting them through wound sealants containing fungi-
in early to late autumn and in spring to early summer, and are cides or biological control agents specifically selected for such
always linked to rainfall. New infections occur through pruning use. Research to identify the materials most suitable for this
wounds, which have been shown to remain susceptible for up purpose is ongoing in several regions.
to 16 weeks, although their susceptibility decreases over time. As with nearly all diseases, appropriate cultural practices are
Togninia minima perithecia reside inside dead, decaying an important component of an integrated control program. Dis-
vascular tissue, e.g., old pruning wounds or vine injuries. As- eased wood should always be removed from the vineyard and
cospores are released during fall and winter rainfall events, burned if possible, as this reduces inoculum potential within
corresponding to the period of dormant pruning in many re- the vineyard. Although infection can occur through pruning
gions. Spores are forcibly ejected from the asci to a height of wounds of any size, the probability of infective spores being
approximately 10 cm, whereupon they are transported by wind deposited upon a susceptible pruning wound is directly propor-
currents or are dispersed to pruning wounds by water droplets. tional to its exposed area; therefore, utilizing pruning and train-
When spores of one (or both) of these fungi reach injured ing systems that minimize large wounds is desirable in terms
wood tissue, they germinate and growth occurs in the xylem of disease management. When the disease is already present in
vessels, causing plugging of the vessels through the produc- the vineyard, trunk renewal or retraining cordons when symp-
tion of gums and tyloses. The end result of this infection is toms first appear provides an immediate, though often tempo-
internal discoloration of the wood, which in association with rary, reduction in the incidence of symptomatic vines. Theory
other poorly understood factors can lead to the development of does not suggest nor does experience indicate that the vascular
typical leaf stripe symptoms in summer. In a California study, pathogens can spread on pruning implements; therefore, it is
spur positions inoculated in February showed severe stunting not necessary to prune healthy and diseased vines separately.
of shoots (approximately 50%) in early summer and both leaf In regions such as California, where spore release is concen-
and fruit symptoms developed by August. The pathogens were trated in winter and early spring, the practice of double prun-
able to colonize the vascular tissue of a 1-­year-­old spur and ing or late pruning has been shown to reduce the establishment
move into the basal bud tissue within 7 months of inoculation. of new infections for various wood diseases, including GLSD/
In addition to field spread via aerial inoculum, Pa. chlamydo- EP. Initially, all canes are pruned to five to seven buds in the
spora and Pm. aleophilum also are distributed via infected early winter, a step that can easily be mechanized (e.g., with
nursery plants. As vascular pathogens, these fungi can move in a tractor-­mounted rotary saw), leaving the entire vineyard with
infected mother plants, resulting in asymptomatic but infected spur positions in which new infections resulting from winter
propagating material. Perhaps relatedly, routine isolations from rains progress slowly under ambient seasonal temperatures. The
symptomatic younger vines (less than 7–8 years old) in Califor- second cut, designed to remove any such new infections before
nia yielded the pathogens primarily from the rootstock portion they reach the lower bud positions to be retained, is made in late
of the plant, suggesting an infection court other than pruning winter or early spring after most spores have been released and
wounds for such vines. new pruning wounds are less susceptible to infection. Ideally,
Phaeomoniella chlamydospora and Pm. aleophilum appear this second cut should be followed by application of an effective
to be ubiquitous fungi. Both have been shown to exhibit en- fungicide, delivered with a sprayer with directed nozzles.
dophytic behavior in grapevines and are able to reside in the Unfortunately, this approach is not considered to be applica-
trunk xylem undetected, sporadically causing symptoms under ble in Europe, where the greatest number of spores is collected
the influence of various stress factors such as low water and in late spring (May–June), and where there is no evidence of
high temperature conditions. reduced susceptibility to infection in early spring versus winter.
In these regions, choosing a careful pruning technique, select-
Management ing trellising systems that avoid large wounds, and applying a
Control of the various syndromes associated with esca, Petri suitable and effective wound dressing continue to comprise the
disease, and GLSD requires a broad and integrated approach. traditional preventive program.
The first step in control of the tracheomycotic fungi is preven-
tion of infection in the nurseries, accomplished through the Selected References
identification, maintenance, and use of clean scion and root-
stock material. For control of Petri disease, it is also preferable Di Marco, S., Mazzullo, A., Calzarano, F., and Cesari, A. 2000. The
to plant into sites where existing infected vines are not present. control of esca: Status and perspectives. Phytopathol. Mediterr.
Avoiding or ameliorating vine stress is also highly advisable, 39:232-­240.
e.g., planting new vineyards in a manner not to promote “J” Edwards, J., and Pascoe, I.  G. 2004. Occurrence of Phaeomoniella
rooting, limiting yields during the initial establishment years chlamydospora and Phaeoacremonium aleophilum associated with
thereafter, and providing timely irrigation as necessary. Petri disease and esca in Australian grapevines. Australas. Plant
Reduction of surface inoculum can be obtained with dor- Pathol. 33:273-­279.
mant sprays designed to kill spores produced on the outer vine Eskalen, A., Feliciano, A. J., and Gubler, W. D. 2007. Susceptibility of
surface before their discharge. In Europe and California, thor- grapevine pruning wounds and symptom development in response
to infection by Phaeoacremonium aleophilum and Phaeomoniella
ough spraying with sodium arsenite during the dormant season
chlamydospora. Plant Dis. 91:1100-­1104.
was long practiced as a means of controlling GLSD/EP, and Ferreira, J. H. S., van Wyk, P. S., and Calitz, F. J. 1999. Slow dieback
the syndrome appeared to become significantly more com- of grapevine in South Africa: Stress-­related predisposition of young
mon after this material was banned from use. Late dormant vines for infection by Phaeoacremonium chlamydosporum. S. Afr.
sprays of calcium polysulfide (lime sulfur), a general oxidant J. Enol. Vitic. 20:43-­46.
that reduces surface inoculum prior to its dispersal to pruning Fischer, M. 2002. A new wood-­decaying basidiomycete species asso-
wounds, has provided positive results in some trials. However, ciated with esca of grapevine: Fomitiporia mediterranea (Hymeno-
this product must physically contact the inoculum in order to chaetales). Mycol. Prog. 1:315-­324.

56
Fourie, P. H., and Halleen, F. 2004. Proactive control of Petri disease as the canopy continues to develop (Fig. 112). However, as fo-
of grapevine through treatment of propagation material. Plant Dis. liar symptoms on diseased arms become increasingly severe
88:1241-­1245. in succeeding years, eventually only extremely dwarfed shoots
Gramaje, D., and Armengol, J. 2011. Fungal trunk pathogens in the remain (Fig. 113). Finally, all of the arms fail to produce new
grapevine propagation process: Potential inoculum sources, de- shoots in the spring and the vine dies.
tection, identification, and management strategies. Plant Dis. Close examination of a cordon or trunk with vascular connec-
95:1040-­1055.
Larignon, P., and Dubos, B. 1997. Fungi associated with esca disease
tions to symptomatic shoots usually reveals a canker surround-
in grapevine. Eur. J. Plant Pathol. 103:147-­157. ing a pruning wound that was made several years previously.
Mostert, L., Halleen, F., Fourie, P., and Crous, P. W. 2006. A review Removal of bark is necessary to reveal the extent of the canker
of Phaeoacremonium species involved in Petri disease and esca of emanating from the point of origin (Fig. 114). In cross section,
grapevines. Phytopathol. Mediterr. 45:S12-­29. a zone of brown, necrotic sapwood typically is found, expand-
Mugnai, L., Graniti, A. and Surico, G. 1999. Esca (black measles) and ing from an initial small, wedge-­shaped sector of symptomatic
brown wood-­streaking: Two old and elusive diseases of grapevines. tissue to include a progressively greater area over time (Fig.
Plant Dis. 83:404-­418. 115). However, this symptom can also be produced by other
Rooney-­Latham, S., Eskalen, A., and Gubler, W. D. 2005. Occurrence canker-­forming fungi and is not diagnostic for Eutypa dieback.
of Togninia minima perithecia in esca-­affected vineyards in Cali- The fungus does not infect and colonize green current-­
fornia. Plant Dis. 89:867-­871. season shoots, and therefore it cannot be isolated from these tis-
Surico, G., Marchi, G., Braccini, P., and Mugnai, L. 2000. Epidemi- sues. Rather, the foliar symptoms are believed to be induced by
ology of esca in some vineyards in Tuscany (Italy). Phytopathol.
Mediterr. 39:190-­205.
Surico, G., Mugnai, L., and Marchi, G. 2008. The Esca Disease Com-
plex. Pages 119-­136 in: Integrated Management of Diseases Caused
by Fungi, Phytoplasma and Bacteria. A. Ciancio and K. G. Mukerji,
eds. Springer, Heidelberg, Germany.
Weber, E. A., Trouillas, F. P., and Gubler, W. D. 2007. Double pruning
of grapevines: A cultural practice to reduce infections by Eutypa
lata. Am. J. Enol. Vitic. 58:61-­66.

(Prepared by W. D. Gubler, L. Mugnai, and G. Surico)

Eutypa Dieback
Eutypa dieback, known also as “dying arm” and formerly as
“dead arm,” is one of the most destructive diseases of the trunk
and other woody tissues of grapevines. It is found in most coun-
tries of both hemispheres, with the frequency in any one region
seemingly limited only by the incidence of rainfall. The dis-
ease occurs chronically and affects productivity, berry quality,
and the lifespan of infected vines. A California study con-
ducted in the late 1990s estimated that the loss of net income to
wine grape growers attributed to this disease (an estimate now
known to have included losses from Botryosphaeria dieback)
was $260 million dollars per annum at that time, or 14% of the
gross farm gate value of California wine grapes. Fig. 110. Characteristic symptoms of Eutypa
Eutypa lata, the primary causal organism, has a wide host dieback on affected young leaves, including
size reduction, chlorosis, cupping, and necrosis.
range that includes approximately 80 species distributed across (Cour­tesy M. Sosnowski)
at least 27 vascular plant families. Most hosts are tree species,
including some that are components of natural forests. The
most severely affected horticultural hosts are grapevine, apri-
cot, cherry, kiwifruit, and blueberry.

Symptoms
The first symptoms of Eutypa dieback usually are not seen
until grapevines are at least 10 years old, with symptomatic
vines typically becoming more numerous each year thereaf-
ter. Symptoms initially appear in the spring when healthy new
shoots are approximately 25–50 cm long. The most readily rec-
ognized and diagnostic symptoms involve reduced vigor and
deformation of the affected shoots, with young leaves appear-
ing chlorotic, reduced in size, and cupped; these often develop
small, necrotic spots and tattered margins, sometimes with
larger areas of necrosis, as they age (Fig. 110). A marked dwarf-
ing of the internodes accompanies the development of the leaf
symptoms, contributing to a stunting of the shoot. Decreases
in shoot length and leaf size become progressively greater over
succeeding years. Clusters on affected shoots may have a mix-
ture of large and small berries (Fig. 111).
At disease onset, mildly affected shoots are readily visible Fig. 111. Clusters from shoots exhibiting symptoms of Eutypa die-
until late spring but then become obscured by healthy growth back. (Cour­tesy M. Sosnowski)

57
translocated toxins, such as eutypine, generated by mycelium grapevine cuttings in greenhouse bioassays. However, the fo-
of the fungus in the wood cankers. However, recent studies liar symptoms of Eutypa dieback have only been reproduced
were unable to detect any of the known toxins in symptom- by inoculation with E. lata and a newly recognized Eutypa
atic green tissues, nor were any detected in the sap of infected sp., which should be considered the only causal agents of this
grapevines. Thus, the mechanisms leading to disease expres- disease.
sion are more complex than initially thought, and remain at best Eutypa lata is the primary causal organism. It is found
only partially understood. worldwide, but is most common and problematic in regions
with Mediterranean climates. Asci, produced within perithe-
Causal Organisms cia, are borne on pedicels 60–130 µm long and measure 30–60
Eutypa lata (Pers.:Fr.) Tul. & C. Tul. (syn. E. armeniacae × 5–7.5 µm, with an apical pore. The eight ascospores are pale
Hansf. & Carter, anamorph Libertella blepharis A. L. Smith
[syn. Cytosporina sp.]) was long believed to be the sole causal
agent of Eutypa dieback. More recently, extensive disease
surveys in nascent and established viticultural regions and
improved molecular tools have associated multiple other spe-
cies in the Diatrypaceae with wedge-­shaped cankers, fruiting
bodies of these fungi have been identified on diseased wood,
and several of these species have produced necrotic lesions on

Fig. 114. Large canker of Eutypa dieback

emanating from an old pruning wound, re-
vealed by removing the rough outer bark.
(Reproduced, by permission, from Moller and
Kasimatis, 1981)

Fig. 112. Stunted shoot exhibiting symptoms of

Eutypa dieback (center), becoming obscured by
growth of healthy shoots in late spring. (Cour­tesy
M. Sosnowski)

Fig. 115. Zone of necrotic sapwood exposed in

cross section through a cankered grapevine
arm, revealing the extent of colonization by
Fig. 113. Later-­stage symptom of Eutypa dieback, with all shoots an expanding Eutypa lata infection. (Cour­
tesy
on an affected arm stunted and deformed. (Cour­tesy W. F. Wilcox) M. Sosnowski)

58
 Fig. 116. Vertical section of perithecial stroma (left) and asci and ascospores (right) of Eutypa lata. (Reproduced, by permis-
sion, from Carter and Talbot, 1974)

Fig. 117. Perithecia of Eutypa lata embedded in a stroma on in- Fig. 118. Cavities of perithecia of Eutypa lata revealed in a
fected grapevine wood. (Cour­tesy M. Sosnowski) shallow slice cut from the stroma with a sharp blade. (Cour­tesy
M. Sosnowski)

yellow and allantoid, measuring 6.5–11 × 1.8–2 µm (Fig. 116).

On grapevines, perithecia (300–700 µm wide) are produced
within stromata on diseased wood several years after the ini-
tial infection, at first in small patches surrounding the infection
site, or sometimes on the wound stub that formed the original
point of entry. Later, as the vine becomes more extensively
invaded, larger areas of stromatic tissue may form within the
outer bands of the dead wood of the trunk or cordon (Fig. 117).
Stromata, visible after the loose bark has exfoliated, are black
and continuous; perithecia are revealed when a shallow slice is
cut from their surface with a sharp blade (Fig. 118).
The newly recognized Eutypa sp. has been identified only in
the colder, humid climates of eastern North America. It shares
several morphological features with E. lata, but is distinguished
from the latter morphologically by its smaller perithecia width
(200–400 µm) and ascospore length (5.5–9 µm). Fig. 119. Conidiogenous cells and conidiophores (left) and co-
nidia (right) from a culture of Libertella blepharis. (Drawings by
Both Eutypa species may be isolated readily from small
B. C. Sutton; reproduced by permission)
chips excised aseptically from the margin of discolored sap-
wood in diseased arms or trunks, using common laboratory
growth media such as potato dextrose or malt agar. White my- are similar in size. Exposing culture plates to an alternating
celium grows from infected wood chips after 3–4 days at 20– 12-­h light/dark regime or to near-­ultraviolet radiation promotes
25°C. Perithecia are not produced in culture, but conidiomata sporulation.
may develop after 6–8 weeks, often exuding the characteristic Positive identification of the causal agents of Eutypa die-
single-­celled conidia that measure 18–45 × 0.8–1.5 µm (Fig. back is confounded by an unresolved species concept within
119) in white to beige cirri. Conidia of Eutypa sp. and E. lata the family Diatrypaceae owing to the discordance between

59
morphological descriptions of fungal type specimens and their seasons after infection. By the third or fourth season, a canker
phylogenetic analyses. The lack of sexual fruiting bodies pro- is usually visible, often accompanied by the foliar symptoms
duced in culture also has hindered the delimitation of species described above. Several more years may elapse before the af-
boundaries within this group. The presence in grapevine wood fected arm or trunk is killed. Because of the slow progress of
cankers of Eutypa species in addition to E. lata and Eutypa the disease, its full economic impact is not likely to be felt until
sp., including E. laevata and E. leptoplaca, and other closely after a vineyard reaches maturity. One of the greatest threats to
related diatrypaceous fungi, such as species of Diatrypella, Di- vine productivity posed by Eutypa dieback is the possibility of
atrype, Cryptovalsa, Cryptosphaeria, and Eutypella, has fur- infection of the many large wounds made when mature vines
ther complicated disease diagnosis. Specimens of these various are reworked to change the pruning and trellising system, adapt
fungi look alike in culture, and the paucity and plasticity of the growth habit for mechanical harvesting, or change scion
associated morphological characters make them unreliable for cultivars in the field.
use in identification to the species level. Molecular tools are
currently being utilized to clarify the identity and role of poten- Management
tial etiological agents other than E. lata and the newly recog- In regions where inoculum is produced abundantly on mul-
nized Eutypa sp. In most diseased vineyards, the incidence of tiple hosts, Eutypa dieback cannot be effectively managed with
these other organisms is not as significant as that of E. lata, and sanitation methods alone, although such methods are a mean-
it is possible that some or many have a restricted geographical ingful component of an integrated management program. In
distribution and/or a lesser ability to produce virulence factors regions with vast plantings of grapes and few alternate hosts
(e.g., cell-­wall degrading enzymes and phytotoxins) to colonize nearby, the regular excision and destruction of cankered wood
the plant hosts. to limit inoculum production may be highly beneficial in and
of itself. Because early-­stage infections are most apparent in
Disease Cycle and Epidemiology spring prior to extensive canopy development, vineyards should
Little is known about the biology of Eutypa sp., hence this be scouted for the presence of characteristic foliar symptoms
discussion focuses on E. lata, a cosmopolitan organism that is when healthy shoots are 25–50 cm long, marking affected cor-
restricted to geographical locations with at least 350 mm of an- dons for removal during the next dormant pruning cycle.
nual rainfall. Although the fungus produces both conidia and In some production regions, surgical removal of diseased
ascospores in nature, only its ascospores are infectious. Asco- cordons has been an effective method to control Eutypa dieback
spores are discharged with rainfalls of approximately 2 mm or on affected vines. Usually, during the season prior to removal,
greater. They are disseminated in wind currents and can travel a shoot arising from tissue scheduled for retention is trained
long distances (more than 50 km), although the likelihood of to the wire to replace the cordon scheduled for removal. The
infection is increased when an inoculum source is nearby. As- following year, the diseased cordon is removed by cutting at
cospore discharge begins within 2 h of the onset of rainfall least 10 cm below any visible canker symptoms. This remedial
and continues for approximately 36 h, after which perithecia treatment allows individual vines to continue producing and
become depleted. At least 12 days are required for discharged potentially recover, although it addresses neither the prevention
asci to be replenished with new, mature ascospores. In regions of new infections nor undetected nascent infections.
where winters are temperate, ascospores are released and dis- No grape cultivars are known to be immune, but where dif-
persed primarily in fall and spring. In regions where winter ferences in cultivar tolerance are recognized, it is advisable to
temperatures below 0°C prevail, dissemination of ascospores prune the least tolerant cultivars last. For example, Cabernet
is greatest as temperatures begin to rise in late winter and early Sauvignon and Chardonnay are more susceptible than Merlot
spring. In the US states of New York and Michigan, a winter or Zinfandel. In California, delaying pruning until the end of
snow blanket can prevent ascospore dispersal, although dis- the dormant season, by which time pruning wounds are healing
charge can occur when snow is melting even in the absence faster, has effectively limited the spread of the disease. In large
of rainfall. Perithecia of E. lata are produced on a wide range vineyards, however, this technique may not allow pruning to be
of woody hosts, including cultivated fruit and nuts crops, or- completed before bud break. Therefore, a “double pruning” sys-
namentals, and native trees. In California for example, apricot tem was developed, whereby vine growth above the top wire is
(Prunus armeniaca), cherry (P. avium), almond (P. dulcis), ole- first cut in early winter (December or January) with a tractor-­
ander (Nerium oleander), willow (Salix spp.), big leaf maple mounted saw, allowing a second cut to be made quickly by hand
(Acer macrophyllum), and California buckeye (Aesculus cali- in the late dormant season (March), finally leaving two-­bud
fornica) can serve as inoculum reservoirs for this pathogen. spurs. Any new infections initiated after the first pruning will
The host range for Eutypa sp. has not been established. not have expanded to the position of the second cut by the time
Infection is initiated when ascospores enter into the open it is made, leaving the retained spur tissue free of the pathogen.
ends of xylem vessels exposed by freshly made pruning In many parts of eastern North America, growers of V. vi-
wounds. Pruning-­wound susceptibility is affected by the age of nifera and other cold-­sensitive cultivars routinely utilize a
the wound and the time of pruning. Generally, the susceptibil- multiple-­trunk training system and practice a regular program
ity of wounds diminishes markedly during the first 2 weeks of “trunk renewal,” periodically replacing older individual
following pruning, and after 5–6 weeks they are unlikely to trunks with new ones derived from shoots that arise from basal
become infected. Wound susceptibility declines more rapidly latent buds. This practice significantly limits the severity of Eu-
with high degree-­day accumulation after pruning. In Califor- typa dieback associated with the trunks, owing to the very slow
nia, wounds made in December and January remain susceptible development of the disease after infection.
longer than wounds made in February and March. Wounds are the main entrance port for the causal agents of
Ascospores germinate within 24 h at the optimal tempera- Eutypa dieback. Although the fungus can invade 1-­year-­old
tures of 20–25°C. Germination occurs within the vessels, usu- canes after pruning, large wounds are more likely to be-
ally 2 mm or more beneath the wound surface. The mycelia come infected, owing to their greater surface area and atten-
proliferate slowly, at first within the vessels and later through dant probability of being impacted by ascospores, and should
associated elements of the functional wood. Eutypa lata pro- be both minimized and protected where possible. Treat-
duces cell wall-­degrading enzymes and phytotoxic secondary ment of fresh pruning wounds with a concentrated slurry of
metabolites that contribute to the deterioration of the integrity thiophanate-­methyl provides good protection against Eutypa
and function of the vessel elements and in the subsequent devel- dieback and several other important trunk diseases (e.g., Bot-
opment of the wood dieback. Cankers develop slowly on grapes, ryosphaeria dieback and esca). However, several applications
and no symptoms are seen during the first one or two growing may be required because the activity of a single fungicide ap-

60
plication may not persist throughout the remaining period of Rolshausen, P.  E., Baumgartner, K., Travadon, R., Fujiyoshi, P.  T.,
host susceptibility. Similarly, a 5% (w/w) concentration of boric Pouzoulet, P., and Wilcox, W. F. 2014. Identification of Eutypa spp.
acid in commercial grafting or wound-­protection paste also causing Eutypa dieback of grapevine in eastern North America.
has provided a highly effective barrier against the invasion of Plant Dis. 98:483-­491.
pruning wounds by E. lata, as boron inhibits both ascospore Sosnowski, M.  R., Shtienberg, D., Creaser, M.  L., Wicks, T.  J.,
germination and subsequent mycelial growth. The advantage Lardner, R., and Scott, E. S. 2007. The influence of climate on fo-
liar symptoms of Eutypa dieback in grapevines. Phytopathology
of this paste is that it provides a physical barrier that is not 97:1284-­1289.
washed off with rainfall, and therefore only one postpruning Sosnowski, M. R., Wicks, T. J., and Scott, E. S. 2011. Control of Eu-
application is necessary. However, boron has limited activity typa dieback in grapevines using remedial surgery. Phytopathol.
against other trunk diseases (e.g., Botryosphaeria dieback) and Mediterr. 50:S277-­S284.
cases of phytotoxicity have been reported in which the bud(s) Sosnowski, M. R., Loschiavo, A. P., Wicks, T. J., and Scott, E. S. 2013.
below the treated wound fail to grow in the spring. Both treat- Evaluating treatments and spray application for the protection of
ments should be applied by hand as a wound dressing to opti- grapevine pruning wounds from infection by Eutypa lata. Plant
mize coverage of the infection court and subsequent disease Dis. 97:1599-­1604.
control. Various international studies have reported the efficacy Travadon, R., Baumgartner, K., Rolshausen, P.  E., Gubler, W.  D.,
of other fungicides for control of E. lata, including members of Sosnowski, M. R, Lecomte, P., Halleen, F., and Péros, J-­P. 2012.
the DMI (tebuconazole, flusilazole, and myclobutanil) and QoI Genetic structure of the fungal grapevine pathogen Eutypa lata
(pyraclostrobin) classes. Research has also revealed the effi- from four continents. Plant Path. 61:85-­95.
cacy of some members of these groups against other pathogenic Travadon, R., Rolshausen, P. E., Gubler, W. D., Cadle-­Davidson, L.,
and Baumgartner, K. 2013. Susceptibility of cultivated and wild
species of Diatrypaceae and Botryosphaeriaceae. Postpruning
Vitis spp. to wood infection by fungal trunk pathogens. Plant Dis.
application of fungicides by conventional spray equipment can 12:1529-­1536.
also be successful if good wound coverage is achieved, and Trese, A. T., Burton, C. L., and Ramsdell, D. C. 1980. Eutypa arme-
ongoing research to increase spray deposition efficiency is im- niacae in Michigan vineyards: Ascospore production and survival,
proving the efficacy of this technique. host infection, and fungal growth at low temperatures. Phytopathol-
ogy 70:788-­793.
Selected References Trouillas, F. P., and Gubler, W. D. 2010. Host range, biological varia-
tion, and phylogenetic diversity of Eutypa lata in California. Phyto-
Carter, M. V. 1991. The status of Eutypa lata as a pathogen. Phyto- pathology 100:1048-­1056.
pathological Paper 32. International Mycological Institute, Surrey, Trouillas, F. P., Pitt, W. M., Sosnowski, M. R., Huang, R. J., Peduto, F.,
UK. Loschiavo, A., Savocchia, S., Scott, E. S., and Gubler, W. D. 2011.
Carter, M.  V., and Talbot, P. H. B. 1974. Eutypa armeniaceae. De- Taxonomy and DNA phylogeny of Diatrypaceae associated with
scriptions of Pathogenic Fungi and Bacteria, no. 436. Common- Vitis vinifera and other woody plants in Australia. Fungal Diversity
wealth Mycological Institute, Kew, Surrey, England. 49:203-­223.
Carter, M.  V., Bolay, A., and Rappaz, F. 1983. An annotated host Weber, E. A., Trouillas, F. P., and Gubler, W. D. 2007. Double pruning
list and bibliography of Eutypa armeniacae. Rev. Plant Pathol. of grapevines: A cultural practice to reduce infections by Eutypa
62:251-­258. lata. Am. J. Enol. Vit. 58:61-­66.
Gramaje, D., Ayres, M. R., Trouillas, F. P., and Sosnowski, M. R. 2012.
Efficacy of fungicides on mycelial growth of diatrypaceous fungi (Prepared by P. Rolshausen, M. Sosnowski, F. P. Trouillas,
associated with grapevine trunk disease. Australas. Plant Pathol. and W. D. Gubler)
41:295-­300.
Moller, W. J., and Kasimatis, A. N. 1981. Eutypa dieback of grape-
vines. Pages 57-61 in: Grape Pest Management. D. L. Flaherty,
F. L. Jensen, A. N. Kasimatis, H. Kido, and W. J. Moller, eds. Publ.
4105. Division of Agricultural Sciences, University of California,
Grapevine Leaf Rust
Berkeley.
Munkvold, G. P., Duthie, J. A., and Marois, J. J. 1994. Reductions in Grapevine leaf rust occurs throughout eastern Asia, extend-
yield and vegetative growth of grapevines due to Eutypa dieback. ing from East Timor and Indonesia northward to Korea and
Phytopathology 84:186-­192. Japan. The disease also has long been established in some warm
Munkvold, G. P., and Marois, J. J. 1995. Factors associated with varia- and humid regions of the Americas from Colombia, Venezu-
tion in susceptibility of grapevine pruning wounds to infection by ela, and Central America through the West Indies and into the
Eutypa lata. Phytopathology 85:249-­265. southeastern United States, occasionally extending as far north
Pearson, R. C. 1980. Discharge of ascospores of Eutypa armeniacae as North Carolina, although it is seldom a commercial prob-
in New York. Plant Dis. 64:171-­174.
lem in the United States. It was first detected in Brazil in 2001,
Pitt, W.  M., Trouillas, F.  P., Gubler, W.  D., Savocchia, S., and
Sosnowski, M.  R. 2013. Pathogenicity of diatrypaceous fungi on
and has now become endemic in some tropical and subtropi-
grapevines in Australia. Plant Dis. 97:749-­756. cal regions of that country. In 2001, it also was detected in the
Ramos, D.  E., Moller, W.  J., and English, H. 1975. Production and far north of Australia (Darwin); the National Grapevine Leaf
dispersal of ascospores of Eutypa armeniacae in California. Phyto- Rust Eradication Program began two years later, and involved
pathology 65:1364-­1371. the implementation of a quarantine zone, extensive surveys, re-
Rolshausen, P. E., and Gubler, W. D. 2005. Use of boron for the control moval of diseased vines, and monitoring of healthy plants. The
of Eutypa dieback of grapevines. Plant Dis. 89:734-­738. disease was declared eradicated from Australia in July 2007,
Rolshausen, P.  E., Mahoney, N.  E., Molyneux, R.  J., and Gubler, and this was considered to be the first successful eradication of
W. D. 2006. A reassessment of the species concept in Eutypa lata, an established rust disease in the world. Grapevine leaf rust is
the causal agent of Eutypa dieback of grapevine. Phytopathology not known to occur in Europe.
96:369-­377.
Rolshausen, P.  E., Greve, L.  C., Labavitch, J.  M., Mahoney, N.  E., Symptoms
Molyneux, R. J., and Gubler, W. D. 2008. Pathogenesis of Eutypa
lata in grapevine: Identification of virulence factors and biochemi- Small, yellow-­orange pustules of uredinia, either scattered or
cal characterization of cordon dieback. Phytopathology 98:222-­229. densely distributed, appear on the lower leaf surface (Fig. 120),
Rolshausen, P. E., Urbez-­Torres, J. R., Rooney-­Latham, S., Eskalen, A., usually with corresponding chlorosis on the upper leaf surface.
Smith, R. J., and Gubler, W. D. 2010. Evaluation of pruning wound On severely affected leaves, the chlorosis becomes necrotic,
susceptibility and protection against fungi associated with grape- forming small, black lesions (Fig. 121). Toward the end of the
vine trunk diseases. Am. J. Enol. Vitic. 61:113-­119. growing season, dark-­brown telia develop among the uredinia

61
(Fig. 122). Severe infection causes leaf yellowing, premature and are densely packed in three to five layers, with the top-­layer
defoliation, and reduced fruit quality and yield. spores being pale brown. They are oblong to oblong-­ellipsoid
and 13–32 × 7–13 µm. Basidiospores are kidney shaped and
Causal Organism 8–11 × 5–8 µm.
Until 2000, the causal agent of grapevine leaf rust was con- Other rust fungi have been recorded on Vitis species. Phakop­
sidered to be a member of Phakopsora ampelopsidis, a spe- sora uva Buriticá & Hennen is reported on unidentified Vitis
cies complex. In that year, the taxonomy of these fungi on species in Colombia and Mexico, but has not been found else-
vitaceous hosts was revised, dividing the pathogens among where. Additional reported species include Phakopsora cron-
three species on the basis of morphology and host specificity. artiiformis (Barcl.) Dietel; Catenulopsora vitis (Butler) Mund.
The species pathogenic on Ampelopsis and Parthenocissus & Thirum.; and Uredo caucensis Mayor.
spp. were designated as Phakopsora ampelopsidis and P.
vitis, respectively, and that on Vitis spp. was described as a Disease Cycle and Epidemiology
new species, P. euvitis Y. Ono. P. euvitis was believed to be P. euvitis is a heteroecious, macrocyclic rust fungus (Fig.
restricted to Vitis spp. until 2004, when it was shown to be 123), the basidiospores of which infect Meliosma myriantha,
capable of infecting two Australian native vitaceous species, a tree native to Japanese forests. Spermogonia and aecia are
Ampelocissus acetosa and A. frutescens, under experimen- produced in sequence on infected leaves, and have only been
tal conditions. P. euvitis is a macrocyclic rust that produces reported in Japan. Aeciospores infect the alternate host, Vitis,
spermogonia and aecia on Meliosma myriantha, a deciduous on which uredinia and telia are produced. Outside Japan, only
tree native to Japan, and uredinia and telia on Vitis species. uredinia and telia are found.
The aecial anamorph is known as Aecidium meliosmae-­ In tropical and subtropical regions, uredinia are produced
myrianthae P. Hennings & Shirai. throughout the year on green leaf tissue of Vitis species. In
Uredinia of P. euvitis appear as minute yellow-­orange pus- temperate regions where Vitis spp. are dormant in winter, telia
tules, 0.1–0.5 mm in diameter, primarily on the lower leaf sur- develop in autumn as the temperatures fall and host leaves
face but occasionally on the upper leaf surface if infection is senesce. Teliospores germinate at temperatures between 10–
severe. The uredinium is surrounded by cylindrical to weakly 30°C, with 15–25°C representing optimum temperatures for
incurved paraphyses, 30–75 µm high, with moderately thick- both teliospore germination and basidiospore formation. Ure-
ened dorsal walls (1.5–4.0 µm). Urediniospores are obovoid, diniospore germination can occur from 8–32°C, with an opti-
obovoid-­ ellipsoid, or oblong-­ellipsoid, 15–29 × 10–18 µm, mum of 24°C. High humidity enhances germination but light
with pale-­yellow walls 1.5 µm thick, echinulate with 6 scat- is detrimental. Appressoria can be observed 6 h after inocula-
tered or rarely 4 equatorial germ pores. Telia appear as brown tion with urediniospores and penetrate through stomata after
to blackish-­brown minute pustules, 0.1–0.2 µm in diameter, 12 h. Uredinial pustules appear 5–6 days after inoculation at
subepidermal, and crustose. Teliospores are formed in chains 16–30°C and after 15–20 days at 12°C. Temperatures >35°C
limit disease development. Fully expanded leaves are more
susceptible to infection than young leaves, which is thought to
be related to stomatal development. High humidity at night is
necessary for development of epidemics.

Management
The tropical Vitis species V.  tiliaefolia, V.  simpsoni, and
V. coriacea have been documented to be nearly immune. Over
400 grapevine genotypes representing 14 different Vitis spp.
(principally V.  vinifera) were screened for resistance in Aus-
tralia and the majority were found to be moderately to highly
susceptible. None were classified as immune.
Twenty-­one fungicide products were tested for their control
of P. euvitis infection. Fungicides effective against rust dis-
eases on other crops, such as dithiocarbamates and triazoles,
control this disease as well. Copper is also reported to be effec-
Fig. 120. Small, yellow-­orange uredial pustules of the grape- tive. Anecdotal evidence suggests that typical fungicide pro-
vine leaf rust fungus, Phakopsora euvitis. (Cour­tesy L. S. grams used in countries such as the United States and Japan to
Leu) manage other fungal diseases also suppress grapevine leaf rust.

Fig. 121. Small, black lesions on the upper side of a grape- Fig. 122. Dark-­brown telia mixed with yellow-­orange ure-
vine leaf severely infected by Phakopsora euvitis. (Cour ­tesy dinia of the grapevine leaf rust fungus, Phakopsora euvitis.
A. M. Daly) (Cour­tesy L. S. Leu)

62
 Fig. 123. Disease cycle of grapevine leaf rust, caused by Phakopsora euvitis. (Cour­tesy A. Kudo)

Selected References Macrophoma Rot

Chatasiri, S., and Ono, Y. 2008. Phylogeny and taxonomy of the Asian
grapevine leaf rust fungus, Phakopsora euvitis, and its allies (Ure- Macrophoma rot affects both bunch and muscadine (V. ro-
dinales). Mycoscience 49:66-­74. tundifolia) grapes; however, the disease is most prevalent and
Daly, A. M., Hennessy, C. R., and Schultz, G. C. 2005. New host re- destructive on muscadines grown in the southeastern United
cord for the grapevine leaf rust fungus, Phakopsora euvitis. Austra- States. In susceptible muscadine cultivars such as Higgins and
las. Plant Pathol. 34:415-­416. Fry, 20–30% of the ripening berries can be lost as a result of
Hennessy, C. R., Daly, A. M., and Hearnden, M. N. 2007. Assessment this disease. In addition to causing fruit rot on several tem-
of grapevine cultivars for resistance to Phakopsora euvitis. Austra- perate and subtropical species, the causal fungus also causes
las. Plant Pathol. 36:313-­317. stem blighting and wood cankers on numerous hosts, including
Leu, L. S., and Wu, H. G. 1983. Uredospore germination, infection and grapes (see Botryosphaeria Dieback).
colonization of the grape rust fungus, Phakopsora ampelopsidis. Muscadine cultivars vary in their susceptibility to the disease.
Plant Prot. Bull. (Taiwan) 25:167-­175.
Black-­skin cultivars such as Noble and Nesbitt are resistant, as
Naruzawa, E. S., Celoto, M. I. B., and Papa, M. F. S. 2006. Estudos
epidemiologicos e controle quimico de Phakopsora euvitis [Epi- is the bronze cultivar Scuppernong. However, most bronze culti-
demiological studies and chemical control of Phakopsora euvitis]. vars are susceptible, with Triumph and Fry being the most sus-
Fitopatol. Brasiliera 31:41-­45. ceptible and Carlos being intermediate in susceptibility. There
Ono, Y. 2000. Taxonomy of the Phakopsora ampelopsidis species is no information on the relative susceptibility of cultivars of
complex on vitaceous hosts in Asia including a new species, P. eu- V. vinifera and other bunch grapes to Macrophoma rot.
vitis. Mycologia 92:154-­173.
Weinert, M. P., Shivas, R. G., Pitkethley, R. N., and Daly, A. M. 2003. Symptoms
First record of grapevine leaf rust in the Northern Territory, Austra- In early stages, the rachis becomes soft and develops latitu-
lia. Australas. Plant Pathol. 32:117-­118. dinal dark lesions that are difficult to differentiate from those
caused by Phomopsis viticola. Berry symptoms usually are not
(Prepared by J. Edwards) visible until fruit begin to mature, but may develop suddenly,

63
sometimes in association with rachis blight. On muscadine ber- Causal Organism
ries, initial symptoms consist of circular, flat or slightly sunken Botryosphaeria dothidea (Moug. ex Fr.) Ces. & de Not. (syn.
lesions, 1–4 mm in diameter (Fig. 124); young lesions are black B. ribis Grossenbacher & Duggar), anamorph: Fusicoccum
with small, tan or buff-­colored centers in which pycnidia are aesculi = Macrophoma sp., has been reported as the causal
embedded. On V. vinifera, initial symptoms are not distinct. On organism of Macrophoma rot. B. dothidea causes cankers in
both muscadine and bunch grapes, a tan to brown, soft rot ex- grapevine spurs, trunks, and arms, but only the pycnidial stage
pands from the initial infection site to eventually envelop the has been found on blighted shoots and diseased fruit. Pycnidia
entire fruit of susceptible cultivars (Fig. 125). Affected fruit are spherical and range from 153 to 197 µm in diameter. Co-
drop from the vine, shrivel, and are finally reduced to dry, hol- nidia (14–25 × 5–8 µm) are hyaline, unicellular, narrowly el-
low shells with pycnidia scattered over the entire surface. liptical to ovoid, and rounded at either end.
As described elsewhere in this volume, B. dothidea is a taxon
that for many years was applied broadly to a variety of similar
organisms, some of which are now assigned to different taxa.
Thus, the identity of the species causing Macrophoma rot may
benefit from a reassessment in light of current concepts of the
genus Botryosphaeria.

Disease Cycle and Epidemiology

Very little information is available concerning the disease
cycle and epidemiology of Macrophoma rot of grape. The
fungus is known to overwinter as pycnidia on infected ber-
ries and stems. Pycnidia, spermagonia, and ascocarp initials
are produced in stromata on stems during late fall and winter.
Conidia are released during rainy periods throughout the grow-
ing season and are splashed or blown onto fruit. The optimal
temperature for growth and sporulation of the causal organism
is approximately 28°C.

Management
Sanitation practices that aid in the management of other fruit
Fig. 124. Initial symptoms of Macrophoma rot on muscadine rot diseases by reducing primary inoculum (e.g., removal of
grapes. (Cour­tesy P. Bertrand) overwintered mummies, rachis tissues, and diseased or dead
wood during pruning) are important for management of Mac-
rophoma rot as well. As with all fungal fruit rots, maintenance
of an open canopy that dries rapidly, limits humidity, and fa-
cilitates spray coverage is very beneficial. Where the disease
is a problem, it is necessary to apply protectant fungicides on
a biweekly schedule from just after bloom until harvest except
during periods of drought.

Selected References
Clayton, C. N. 1975. Diseases of muscadine and bunch grapes in North
Carolina and their control. N. C. Agric. Exp. Stn. Bull. 451.
Jenkins, W. A. 1941. Diseases of muscadine grapes. Pages 19-­29 in:
Further Studies with Muscadine Grapes. L. Ascham, T. L. Bissell,
W. L. Brown, T. A. Pickett, E. F. Savage, M. M. Murphy, Jr., and
J. G. Woodroof, eds. Ga. Agric. Exp. Stn. Bull. 217.
Kummuang, N., Smith, B. J., Diehl, S. V., and Graves, C. H., Jr. 1996.
Muscadine grape berry rot diseases in Mississippi: Disease identifi-
cation and incidence. Plant Dis. 80:238-­243.
Luttrell, E. S. 1948. Botryosphaeria ribis, perfect stage of the Macro­
phoma causing ripe rot of muscadine grapes. Phytopathology
Fig. 125. Muscadine grapes enveloped by light-­brown soft rot due 38:261-­263.
to infection by Botryosphaeria dothidea sensu lato, the causal
agent of Macrophoma rot. (Cour­tesy T. B. Sutton) (Prepared by T. B. Sutton)

Minor Foliage Diseases synonyms. Minor foliage diseases typically are not a problem in
commercial vineyards that receive general disease-­control prac-
tices, but some may occasionally bridge the gap between wild
The literature contains numerous reports of fungi described hosts and cultivated vines when conditions particularly favor
on grape foliage. Most of these were collected from vines of the their growth, such as unusually wet growing seasons. They are
many wild species of Vitis in diverse climates. Many are local- reported disproportionately from nontraditional growing dis-
ized or limited to a few host species, some have a wide host range tricts, often by newer growers who cannot identify them as one
that happens to include Vitis, and all appear under a multitude of of the usual diseases described in reference manuals.

64
 Leaf Blight Causal Organism
Pseudocercospora vitis (Lév) Speg. (syn. Isariopsis clavis-
In the United States, leaf blight or Pseudocercospora leaf pora (Berk. & Curt.) Sacc.), the imperfect stage of Mycosphae-
blight, also called Isariopsis leaf spot, occurs primarily in the rella personata Higgins, is the causal agent of leaf blight. The
Southeast and westward into Texas, where it has been par- fruiting structures are slender, black, bristlelike synnemata
ticularly problematic on Cabernet Sauvignon. It has not been (200–500 µm long) bearing olive-­brown, elongate conidia (25–
reported on muscadine grapes. It also occurs in Massachu- 99 × 4–8 µm) with 3–17 septa.
setts, Connecticut, Kansas, Illinois, and California on vines The teleomorph may develop on dead leaves late in the sea-
of wild species. It has been reported throughout the warmer son. Perithecia are round (60–90 µm in diameter), black, em-
grape-­growing areas of the world under various synonyms. The bedded, and warty above. Asci are club shaped (30–40 × 6–10
disease tends to appear after harvest when spraying is discon- µm), and ascospores (10–20 × 2.5–3.6 µm) may be forcibly
tinued (Fig. 126) and may cause considerable defoliation in a discharged.
wet year if not controlled.
Selected References
Symptoms
Spots are irregular to angular, often numerous, 2–20 mm in Deighton, F.  C. 1976. Studies on Cercospora and allied genera. VI.
diameter, and initially chlorotic. Lesions soon turn brown to Pseudocercospora Speg., Pantospora Cif. and Cercoseptoria Petr.
black and become necrotic, and may coalesce (Fig. 127). They Mycological Paper 140. Commonwealth Mycological Institute,
have clearly defined borders on the upper leaf surface and dif- Kew, England.
fuse margins on the lower leaf surface. Lesions typically ap- Higgins, B. B. 1929. Morphology and life history of some ascomycetes
with special reference to the presence and function of spermatia. II.
pear first on the lower, shaded leaves.
Ga. Agric. Exp. Stn. J. Ser. Pap. 28:287-­296.
Rhodes, A. S. 1926. Diseases of grapes in Florida. Fla. Agric. Exp.
Stn. Bull. 178.

(Prepared by J. R. McGrew and F. G. Pollack)

Leaf Blotch
The fungus that causes leaf blotch is widespread throughout
the eastern United States (New York to Wisconsin and south
to Texas and North Carolina) and has been reported from Italy
and northern Portugal as well. Lesions are most often found on
the foliage of rootstock cultivars derived from native Ameri-
can Vitis spp. but sometimes appear on V. labrusca, V. vinif-
era, and Vitis interspecific hybrid cultivars. The fungus also
has been found fruiting on berries that were left on the vine
past normal harvest. Only fruit infection has been reported
Fig. 126. Numerous late-­season leaf infections caused by Pseudo­ from Italy.
cercospora vitis. (Cour­tesy J. Kamas) The leaf blotch fungus has been found in association with
the larvae of the grape leaffolder, Desmia funeralis (Hübner),
fruiting on frass inside the rolled-­up portion of the leaf blade
and sometimes producing a leaf lesion with synnemata in the
immediate area of the infested frass.
Inoculation trials in Portugal indicate that rootstock clones
are more susceptible than V.  vinifera and interspecific hybrid
fruiting cultivars. When rootstocks were grown in Maryland
without fungicide applications and leaf blotch was obviously
present, the overall reduction in effective leaf area was minor.

Symptoms
Leaf lesions generally appear after midseason and range in
size from 5 mm in diameter to as much as one-­third of a leaf.
Smaller lesions may have distinct, dark margins, while larger
ones show distinct, light-­colored, zonate rings or arcs (Fig.
128). Synnemata are produced within 3 or 4 days of the appear-
ance of a lesion.

Causal Organism
Briosia ampelophaga Cav., the cause of leaf blotch, forms
scattered and conspicuous synnemata, more frequently on
lesions on the lower leaf surface but sometimes on both sur-
faces. Synnemata have relatively thick, white stipes consisting
of parallel, hyaline hyphae that are massed, anastomosed, and
interwoven to form rigid, upright structures as long as 1 mm.
Fig. 127. Initial chlorotic lesions and subse- The stipe is capped with a dark, spherical mass, which may
quent necrotic, coalesced lesions caused be 1 mm in diameter, consisting of chains of dry, dark-­brown
by Pseudocercospora vitis. (Cour­tesy conidia. Individual conidia are globose and measure 3–5 µm
J. Kamas) in diameter.

65
Fig. 128. Leaf blotch, caused by Briosia ampelophaga, on a leaf
of the interspecific hybrid cv. Rougeon. (Cour­tesy J. R. McGrew)
Fig. 129. Zonate leaf spot, caused by Cristulariella moricola. (Cour­
tesy J. R. McGrew)
Selected References

Cavara, F. 1888. lntorno al dissecamento dei grappoli della vite. Atti

Ist. Bot. Univ. Pavia 1:293-­324.
Doutel Serafim, D. J. 1955. Coremium luteolum S. Camara: Causa de
uma doença das folhas algumas videiras. Agron. Lusit. 17:297-­334.

(Prepared by J. R. McGrew and F. G. Pollack)

Zonate Leaf Spot

Zonate leaf spot, also called target spot, has been reported
infrequently on wild and cultivated grapes. The fungus that
causes this disease has a wide host range of both herbaceous
and deciduous plants and is known to be present from Florida
to Massachusetts and north into Canada as well as in Japan,
China, and India. It has been reported to produce severe defo-
liation on several other crop species.
The disease appears very sporadically on grapes, and may be
extensive in a vineyard one year yet not appear the following
season. Differential susceptibility among cultivars has not been
noted. Inoculum responsible for a severe outbreak in a vineyard
may originate from any of several species of nearby infected
trees or shrubs. Field studies have shown that the fungus moves
only a limited distance (less than 50 m).
Fig. 130. Fruiting structure of Cristulariella
Symptoms moricola. (Cour­tesy A. J. Latham)
The generally circular lesions of zonate leaf spot may ap-
pear at any time during the growing season following several
consecutive days of high humidity and accompanying rainfall, affixed horizontally to a leaf surface at the center of a newly
fog, or dew. They resemble lesions of leaf blotch except that formed lesion. The fruiting structures are formed only during
the larger lesions tend to have a more concentric zonation (Fig. periods when the relative humidity is above 96%. Lesions may
129). The central portion of older lesions tends to disintegrate, resume production of these structures even after dry periods
leaving a hole in the leaf. Under some conditions, lesions can be of 60 days. In culture, the conical structures produce minute
numerous and probably affect vine growth. phialides and globose phialospores (2.4–3.5 µm in diameter)
from the globular cells.
Causal Organism
Cristulariella moricola (Hino) Redhead (syn. C. pyrami- Selected References
dalis Waterman & Marshall) is the causal organism of zonate
leaf spot. A sclerotial stage produced by this fungus, known as French, W. J. 1972. Cristulariella pyramidalis in Florida: An exten-
sion of range and new hosts. Plant Dis. Rep. 56:135-­138.
Sclerotium cinnamomi Sawada, may serve as an overwintering
Pollack, F.  G., and Waterworth, H.  E. 1969. A leafspot disease of
stage. The entire fungal fruiting structure, which resembles a Kenaf in Maryland associated with Cristulariella pyramidalis.
miniature conifer, serves as a functional conidium (Fig. 130). It Plant Dis. Rep. 53:810-­812.
is pale, conical, up to 0.5 mm in length, and borne on a slender Redhead, S. A. 1979. Mycological observations: 1. On Cristulariella;
stalk that is one cell thick and four to many cells long. The stalk 2. on Valdensinia; 3. on Neolecta. Mycologia 71:1248-­1253.
produces globose or lobed cells that proliferate by budding, fi- Trolinger, J.  C., Elliott, E.  S., and Young, R.  J. 1978. Host range of
nally forming a dense mass of cells. These cells are not freed Cristulariella pyramidalis. Plant Dis. Rep. 62:710-­714.
individually as conidia. The entire structure, which can break
away from the stalk, may be carried by wind. It can be found (Prepared by J. R. McGrew and F. G. Pollack)

66
 Septoria Leaf Spot
Septoria leaf spot, also called mélanose, occurs infrequently
in the eastern United States and has been reported from New
York to Florida and westward, from Wisconsin to Texas. It was
presumably introduced into Europe during the phylloxera cri-
sis, and has now been documented in France, Germany, Spain,
Switzerland, European portions of the former Soviet Union,
and Algeria. The disease is known to affect American Vitis
spp., muscadine grapes, and some V. labrusca cultivars. V. vi-
nifera cultivars are reported to be immune.

Symptoms
Few to many reddish-­brown to black spots appear generally
after midseason. They are interveinal, angular, and generally
1–2 mm in diameter, but can extend up to 2 cm in diameter on
muscadine foliage. The margins of lesions are often thickened. Fig. 131. Moderate symptoms of the physiological disorder
Later, if there are several spots on a leaf, the surrounding area Rupestris speckle on the interspecific hybrid cv. Chambour-
may become yellow. cin. (Cour­tesy T. E. Martinson)

Causal Organism
Leaf spot is caused by Septoria ampelina Berk. & Curt. Pyc-
nidia are 50–60 µm in diameter and have a large, open ostiole.
Conidia (40–60 × 2 µm) are hyaline and undulating, with three
to six septa.

Selected Reference
Boubals, D., and Mur, G. 1983. Une autre maladie de la vigne sevit
dans le Penedes (Espagne). Prog. Agric. Vitic. 100:453.

(Prepared by J. R. McGrew and F. G. Pollack)

Other Minor Foliage Diseases

Brulure Fig. 132. Severe symptoms of the physiological disorder
Brulure, which is caused by the fungus Anthostomella pul- Ru­pestris speckle on a cv. Chambourcin vine. (Cour­tesy
lulans (de Bary) Bennett, occurs on all parts of the vine. The T. E. Martinson)
incitant is distributed worldwide and is generally a saprophyte.

Cladosporium Leaf Spot Rupestris Speckle

Cladosporium viticola Cesati causes a leaf spot disease on Rupestris speckle appears to be a physiological disorder as-
older foliage of both wild and cultivated vines. The disease has sociated only with V. rupestris. It may appear in a milder form
been reported in Europe and in the eastern United States. on interspecific hybrids derived from this species, such as Vil-
lard Blanc and Chambourcin. Symptoms are similar to those of
Cercospora Leaf Spot Septoria leaf spot or oxidant stipple but tend to be on older and
Cercospora leaf spot (cercosporiose), caused by Phaeoramu- shaded leaves. The necrotic areas vary from circular to angular,
laria dissiliens (Duby) Deighton, produces variable yellowish are generally less than 2 mm in diameter, and tend to show a
to dark spots. It has been reported from Pakistan through Asia yellow halo (Fig. 131). Spotting is more pronounced on weak or
Minor, Europe, and North Africa. stressed vines (Fig. 132), and a range of severities may be found
in the same vineyard. No control measures have been prescribed,
Tar Spot and the effect on vine growth is thought to be insignificant.
Tar spot, caused by Rhytisma vitis Schw., produces a black
spot 2–4 mm in diameter, with or without a circular, brown Selected References
halo up to 1 cm in diameter. It is common on wild vines in the
southeastern United States. Bennett, F. T. 1928. On Dematium pullulans de B. and its ascigerous
stage. Ann. Appl. Biol. 15:371-­391.
Miscellaneous Leaf Spots Deighton, F. C. 1976. Three fungi on leaves of Vitis. Trans. Br. Mycol.
A leaf spot caused by Asperisporium minutulum (Sacc.) Soc. 67:223-­232.
Griffiths, D. A. 1974. The origin, structure and function of chlamydo-
Deighton produces lesions with indefinite margins. It has been spores in fungi. Nova Hedwigia 25:503-­547.
reported only on V. californica in California and Oregon. Viala, P. 1893. Les Maladies de la Vigne. 3rd ed. Coulet, Montpellier,
Another leaf spot, caused by Phaeoramularia heterospora France.
(Ell. & Gall.) Deighton, has been reported on V. californica and
V. girdiana in California and on V. vinifera in Israel. (Prepared by J. R. McGrew and F. G. Pollack)

67
 Phomopsis Cane and Leaf Spot winds before shoots become attached to the trellis wires (Fig.
134). During the dormant season, infected canes may become
bleached or grayish in appearance, and numerous tiny, black
Phomopsis cane and leaf spot is widely distributed through- fungal fruiting bodies (pycnidia) erupt through the surface to
out the viticultural regions of the world, and has been reported produce a speckled appearance.
from every continent on which grapes are grown. The disease Elongated, black lesions similar to those on young shoots
is especially problematic in regions or years where the climate develop on infected petioles (Fig. 133) and may cause affected
following bud break may keep grapevines wet for extended pe- leaves to turn yellow and drop if severe. On infected leaf blades,
riods of time. Although the common name of the disease is small, light-­green lesions with irregular margins develop early
Phomopsis cane and leaf spot, economic losses in regions with in the season. As the disease progresses, these spots turn dark
humid growing seasons are more often the result of infections brown to black with surrounding yellow halos (Fig. 135). The
of the fruit and rachises (cluster stems). Fruit and rachis in- infected tissue may drop out, causing a “pin-­pricked” appear-
fections typically are sporadic but can be severe under heavy ance. Heavily infected leaf blades are often misshapen and
disease pressure, with yield losses up to 30% documented in crinkled. The economic impact of foliar infections is question-
vineyards with abundant inoculum if prolonged rains occur in able and does not appear to be great.
the spring and early summer and control programs are limited. Lesions on rachises are typically sunken and black (Fig.
Such infections are uncommon in drier regions such as those 136) and cause rachises to become brittle; clusters may break
with Mediterranean climates, where losses are generally lim-
ited to the occasional weakening and breaking of green shoots
at infection sites on the basal internodes.
Information on relative susceptibility among Vitis species
and the cultivars within them is limited. Most V. vinifera culti-
vars appear to be susceptible, although the disease is particu-
larly common on spur-­pruned varieties. Limited inoculation
studies suggest that accessions of V. aestivalis and V. amuren-
sis are relatively resistant; those of V. riparia and V. yensha-
nensis are highly susceptible; and interspecific hybrids vary
widely in susceptibility, depending on their parentage. Most
common V.  labrusca cultivars and cultigens are susceptible,
and cv. Niagara appears to be highly susceptible. In the Great
Lakes region of North America, Phomopsis rachis and fruit
infections cause greater consistent losses on these cultivars
than does any other infectious disease, likely owing to (i) the
cultivars’ pendulous growth habit, which causes new, suscep-
tible tissues to develop beneath sources of splash-­dispersed
inoculum; (ii) their susceptibility to this disease relative to
others more problematic on V. vinifera (e.g., powdery mildew);
and (iii) the less intensive disease management programs that
they typically receive relative to V. vinifera and interspecific
hybrid cultivars.

Symptoms
Lesions on shoots and leaves are the most common symptom
of the disease. Shoot infections result in black, elongated le- Fig. 134. Wind breakage of a young shoot
sions that are most numerous on the first three to six basal in- at the site of an internode lesion caused by
ternodes (Fig. 133). Cracks or fissures may develop within these Phomopsis viticola. (Cour­tesy W. F. Wilcox)
lesions, and eventually crust over to produce a rough, black
appearance by the end of the season. The stem is weakened
around these infection sites, which may cause it to break in high

Fig. 135. Numerous small, dark leaf lesions surrounded by a yel-

Fig. 133. Black, elongated lesions caused by Phomopsis viticola low halo, characteristic foliar symptoms of Phomopsis cane and
on the basal internodes and leaf petioles of cv. Concord, with a leaf spot. (Photograph by W.  McFadden-­Smith, Ontario Ministry
dead pruning stub (the likely inoculum source) directly above. of Agriculture and Food; Queen’s Printer of Ontario, © 2009.
(Cour­tesy W. F. Wilcox) Reproduced with permission.)

68
at these points under the weight of the maturing crop or dur- Causal Organism
ing harvest operations, leading to a reduction in yield. Rachis Phomopsis viticola (Sacc.) Sacc. (syn. Fusicoccum viticola
infection during the early stages of cluster development may Reddick) is the causal agent of Phomopsis cane and leaf spot.
lead to the loss of the “wing” (lateral branch of the cluster) (Fig. There has been a great deal of confusion as to whether an as-
137). On highly susceptible cultivars, the fungus may advance cogenous stage of the fungus exists; if so, it is rarely encoun-
from rachis and pedicel infections into individual berries (Fig. tered. A number of other species of Phomopsis are associated
138), or the entire cluster may be girdled and lost (Fig. 139). with grape plants, but only P. viticola is known to be strongly
After infected berries become completely necrotic, multiple pathogenic.
black fruiting bodies (pycnidia) of the fungus erupt through the Phomopsis viticola produces black pycnidia ranging in di-
skin, giving them a rough texture (Fig. 140). Eventually, dis- ameter from 0.2 to 0.4 mm. Each pycnidium has one or more
eased berries may shrivel into black raisin-­like mummies very locules, depending on the substrate. Pycnidia are globose, but
similar to those caused by black rot or bitter rot, but they more
frequently fall to the ground beforehand.
Fruit rot caused by Phomopsis is sometimes confused with
black rot and bitter rot, as the same regional weather patterns
are conducive to the development of all three. In general, Pho-
mopsis fruit rot is distinguished by its late appearance (typi-
cally, just before harvest); the fact that diseased berries are
easily detached from their pedicels; and the coincidence of fruit
rot with the above-­described symptoms on basal internodes,
petioles, leaf blades, and/or rachises.

Fig. 138. Expansion of Phomopsis viticola

from infected rachis and pedicel tissues into
ripening berries of cv. Niagara. (Cour ­tesy
W. F. Wilcox)

Fig. 136. Sunken, black lesions on basal internodes and cluster

rachis of cv. Concord caused by Phomopsis viticola. (Cour­tesy
R. C. Pearson)

Fig. 137. Loss of the “wing” (lateral branch) on a cluster of cv. Fig. 139. Girdling of cv. Niagara rachis with
Concord (arrow) resulting from infection by Phomopsis viticola resulting loss of the cluster following infec-
during the early stage of cluster development (left) compared with tion by Phomopsis viticola. (Cour­tesy W. F.
a healthy cluster with wing intact (right). (Cour­tesy W. F. Wilcox) Wilcox)

69
may be conical at maturity. An ostiole opens at the peak of a several layers of pseudoparenchymatic cells arise from these
short neck. The opening on a pycnidium is usually round and areas and provide the conidia that serve as inoculum for new
smooth but may be irregular and sometimes ragged. infections. In culture, the branched mycelium of P. viticola is
Pycnidiospores often ooze through the ostiole, either in a ge- hyaline, septate, and forms a slightly raised, dense mat, often in
latinous matrix or in long, curled, yellowish to cream-­colored concentric rings under alternating light-­dark regimes. Portions
cirri (Fig. 141). The inner surface of a pycnidium is typically of the mat or the margins of concentric rings turn dark gray to
lined with straight pycnidiophores of two types. One type is black as the culture ages. Pycnidia form irregularly in the dark
elongate with a pointed apex, measures 12–20 × 2 µm, and parts of the mycelial mat, either singly or in clumps.
bears nonseptate, hyaline, elliptical-­fusoid pycnidiospores (or
alpha conidia, 7–10 × 2–4 µm) that are acute on one or both Disease Cycle and Epidemiology
ends and multiguttulate; guttules are sometimes grouped at In the late winter and early spring, spores are produced
the polar ends. The other type of pycnidiophore is short (5–8 within pycnidia that formed in previously infected woody tis-
× 1.5 µm) and produces scolecospores or beta conidia. Beta sues. (Although the exact time of pycnidia production in woody
conidia, which are much less abundant than alpha conidia, are tissues is not clear, and may vary among climates, they gener-
long and curved or threadlike, nonseptate spores measuring ally are not observed in newly infected shoots until some time
18–30 × 0.5–1 µm (Fig. 142). Both alpha-­and beta-­conidia can after these have lignified into canes and become dormant). Be-
be formed in the same pycnidium, although beta conidia rarely cause shoot infections are most frequent on basal internodes,
germinate and their function has not been determined. It has inoculum production is particularly favored by spur-­pruning
been reported that beta conidia are infrequently observed when systems in which only basal cane segments are retained during
cultures are incubated at 20°C, but are produced abundantly dormant pruning, thereby maximizing the retention of infected
when cultures are incubated at 30°C. Spore-­ trapping stud- wood. Infected pruning stubs, which once originated as basal
ies from vineyards in the northcentral (Michigan) and north- internode segments, are similarly important as potential in-
eastern (New York) United States have yielded primarily beta oculum sources (Fig. 133). Mechanical hedging systems, which
conidia in the mid-­summer but far larger quantities of almost retain large numbers of basal cane segments, can be especially
exclusively alpha conidia earlier in the season. problematic for management of this disease. The fungus can
In green shoots, the mycelium invades mostly cortical pa- continue to produce pycnidia and spores for an indeterminate
renchyma tissue. The mycelium is hyaline and forms pseudo-­ number of years after infection first occurs, even after infected
parenchymatous mats among host cells. In addition to causing wood dies. Therefore, a serious disease outbreak in one sea-
necrosis of infected cells, the mats may turn black, giving spots son may provide inoculum for new infections for multiple years
and lesions this color. Eventually, black pycnidia comprising afterward.
Spores ooze out of the pycnidia in a sticky mass during humid
or wet weather and are then splashed by rain onto newly devel-

Fig. 140. Pycnidia on necrotic berry of cv. Niagara infected with

Phomopsis viticola. (Cour­tesy W. F. Wilcox)

Fig. 142. Conidiogenous cells and co-

nidia of Phomopsis viticola, with alpha
(a) and beta (β) spores. (Reproduced,
Fig. 141. Pycnidia of Phomopsis viticola exuding spores in cirri on by permission, from Punithalingam,
the surface of a 1-­year-­old cane. (Cour­tesy W. Gärtel) 1979)

70
oping tissues. Splash dispersal results in significant numbers rating it into the soil, or by burning. Owing to the extremely
of spores moving only a short distance, and it is not unusual local dispersal of infective spores and the monocyclic nature
to see the disease localized in “hot spots” within individual of this disease, serious Phomopsis outbreaks are almost always
vines where inoculum is plentiful. Infection can occur dur- the result of high inoculum levels within a vineyard in addition
ing wet periods at temperatures ranging from approximately to very wet weather conditions. When used with recommended
5 to 35.5°C (optimum 16 to 20°C), with the resulting disease sanitation practices, even a modest fungicide program (which
severity a function of both temperature and wetness duration. not only protects against current losses but also limits estab-
Significant infection frequently occurs during extended spring lishment of the fungus in subsequently retained wood) typi-
rains at temperatures well below the optimum. cally provides adequate control of the disease.
In the north-­central and northeastern regions of the United Broad-­spectrum protectant fungicides such as mancozeb,
States, most inoculum is dispersed between bud break and captan, folpet, ziram, chlorothalonil, and dithianon are very ef-
bloom, and few infectious alpha spores are available beyond the fective against Phomopsis and are commonly used for its control
pea-­sized berry stage. With the exception of diseased berries, throughout the world. More modern fungicide groups, such as
which sporulate shortly after these organs become necrotic the DMI and QoI materials, have provided control in some re-
during the preharvest period, conidia are seldom produced gions but not in others. Sulfur is recommended in some regions
from new infections during the current growing season. Con- but has provided little to no control under heavy disease pressure
sequently, secondary spread of the disease is rare, even when in New York trials. Copper also is relatively ineffective; thus,
summer rainfall is not limiting. Thus, the period during which growers using organic production practices should focus strongly
new infections are possible and fungicidal protection may be on sanitation programs, particularly in regions where this dis-
necessary is restricted by both the onset of dry weather (in some ease can be problematic. Fungicides targeted against Phomopsis
regions and/or seasons) and the depletion of primary inoculum. should be applied during the very early part of the growing sea-
Shoot and leaf lesions usually appear 3–4 weeks after in- son as influenced by the occurrence of favorable weather condi-
fection. Rachis infections may appear within a month after tions, inoculum levels in the vineyard, varietal susceptibility, and
infection, although they typically are most pronounced dur- local experience. Controlling early-­season infections of shoots
ing the preharvest period. Fruit infections usually are not ap- is very important for reducing sources of primary inoculum for
parent until after veraison and typically become most visible subsequent growing seasons. The first few weeks after cluster
during the last 1–3 weeks before harvest. Although pycnidia emergence is the most important portion of the season for con-
can develop within newly diseased berries, the potential for trolling rachis and fruit infections in regions where they occur.
secondary disease spread from these sources is limited by the Continued protection against fruit infections may be necessary
timing of their appearance and the requirement for a postinfec- through the early postbloom period if the weather remains wet
tion incubation period, whose length usually exceeds the time in high-­risk sites where they are a potential problem.
remaining until harvest. A “delayed dormant” (immediately before bud break) ap-
On shoots, the young growing tip is most susceptible and tis- plication of materials such as lime sulfur (calcium polysulfide)
sue becomes relatively resistant as it matures. Although shoot and fluazinam has often been effective in reducing, but not
tissues two or three internode positions back from the growing eliminating, disease development during the subsequent grow-
tips are highly resistant, susceptible tissue is continually pro- ing season, presumably by reducing the production of primary
duced as the shoot keeps growing, and the timing of infection inoculum from pycnidia on the vines. However, the potential
is restricted only by the availability of inoculum and favorable benefit of this approach must be considered with respect to its
weather. Leaves become resistant to infection once they are fully cost. A predictive model has been developed to forecast specific
expanded. Rachises are highly susceptible as nascent clusters infection events for this disease; however, the current lack of
first become exposed, when shoots are about 8–10 cm long (E-­L fungicides with significant curative activity against P. viticola
stage 12). Infections during the very early period of cluster devel- limits the application of such a predictive system within com-
opment are the most damaging and may cause serious girdling mercial disease management programs.
as the uninfected portions of the inflorescence expand around
them, with subsequent berry loss. Rachis susceptibility declines Selected References
a few weeks after bloom, coinciding with the depletion of in- Cucuzza, J. D., and Sall, M. A. 1982. Phomopsis cane and leaf spot
oculum. Berry infection apparently can occur via expansion of disease of grapevine: Effects of chemical treatments on inoculum
infections initiated in the pedicel (berry stem), beginning soon level, disease severity, and yield. Plant Dis. 66:794-­797.
after the time that small clusters first emerge, or directly through Erincik, O., Madden, L. V., Ferree, D. C., and Ellis, M. A. 2001. Effect
the fruit epidermis after set. Berry infections typically remain of growth stage on susceptibility of grape berry and rachis tissues to
latent (inactive) until the preharvest period, when they colonize infection by Phomopsis viticola. Plant Dis. 85:517-­520.
and rot the fruit. Some studies indicate that berries become re- Erincik, O., Madden, L. V., Ferree, D. C., and Ellis, M. A. 2003. Tem-
sistant to the initial establishment of infection after the pea-­sized perature and wetness-­duration requirements for grape leaf and cane
stage of development (E-­L stage 31), whereas others show them infection by Phomopsis viticola. Plant Dis. 87:832-­840.
to remain susceptible to new infections throughout the season. Mostert, L., Crous, P. W., Kang, J.-­C., and Phillips, A. J. L. 2001. Spe-
However, because few infective P. viticola spores are available cies of Phomopsis and a Libertella sp. occurring on grapevines with
beyond mid-­summer, it appears likely that in regions where they specific reference to South Africa: Morphological, cultural, molec-
ular and pathological characterization. Mycologia 93:146-­167.
occur, fruit infections are initiated primarily between the time of
Phillips, A.  L. 2000. Excoriose, cane blight and related diseases of
cluster emergence and the early postbloom period. grapevines: A taxonomic review of the pathogens. Phytopathol.
Mediterr. 39:341-­356.
Management Pscheidt, J. W., and Pearson, R. C. 1989. Effect of grapevine training
Phomopsis cane and leaf spot can be managed through an systems and pruning practices on occurrence of Phomopsis cane
integrated program of sanitation and fungicide application. and leaf spot. Plant Dis. 73:825-­828.
Sanitation should be the first line of defense. To whatever extent Pscheidt, J. W., and Pearson, R. C. 1989. Time of infection and control
possible, the introduction of P. viticola into the vineyard should of Phomopsis fruit rot of grape. Plant Dis. 73:829-­833.
be avoided by use of pathogen-­free propagation materials when Punithalingam, E. 1979. Phomopsis viticola. Descriptions of Patho-
genic Fungi and Bacteria, no. 635. Commonwealth Mycological
establishing a new vineyard. Once the disease has appeared, as
Institute, Kew, Surrey, England.
much diseased and dead wood as practical should be removed
during pruning. To reduce a major source of inoculum, debris (Prepared by W. F. Wilcox, M. A. Ellis, B. Rawnsley,
from pruning should be destroyed by shredding and incorpo- A. Rossman, and J. Pscheidt)

71
 Phymatotrichopsis Root Rot Much of the grapevine root system is rotted by the time
the first foliar symptoms are observed. Thick or thin mycelial
strands of the pathogen are usually observed on the surfaces of
Phymatotrichopsis root rot (formerly Phymatotrichum root infected roots (Fig. 144). Often, the root cortex is easily sepa-
rot), commonly called Texas root rot or cotton root rot, also has rated from the woody cylinder.
been reported in mango and avocado orchards in the semitropi-
cal states of Veracruz, Michoacan, and Sinaloa in Mexico. Causal Organism
The causal fungus, Phymatotrichopsis omnivora (Duggar)
Symptoms
Hennebert (syns. Phymatotrichum omnivorum (Shear) Dug-
Phymatotrichopsis root rot usually appears as patches in the gar, Ozonium omnivorum Shear), produces large, sparingly
vineyard. Natural spread of the pathogen is slow and it appears to branched, leader hyphal cells. White mycelial strands, which
be restricted to certain areas of the vineyard, although the reason become brown with age, are formed by the parallel growth of
for this is not understood. Affected vines may suddenly wilt and hyphae and lateral branching of short hyphal cells. The fungus
die during the early or midsummer, with their leaves becoming can be easily identified with a microscope by observing these
brown and brittle and remaining rigidly attached to the dead vine strands, which have numerous acicular and characteristically
(Fig. 143). Before wilting, leaves on some infected vines may cruciform hyphae (Fig. 145).
gradually turn yellow or red, with interveinal yellow spots and Globose to irregularly shaped, brown sclerotia, 1–2 mm
irregular necrotic areas on the leaf blade and margins. Some dis- in diameter, are produced singly or in clusters from infected
eased vines may show discoloration and necrosis of a few leaves roots in soil. Spore mats, which consist of numerous hyphae
in early summer, with no further progression of symptoms for with globose to elongated conidiophores bearing single-­celled,
the remainder of the season. Shoot growth is reduced and leaves spherical to ovate conidia (4.8–5.5 µm in diameter), are some-
are dull green on such vines the following year. times produced on the surface of the soil after several days of
Vines showing complete foliar discoloration or necrosis in irrigation or rain (Fig. 145).
early summer become partly or totally defoliated by midsum-
mer, and their clusters become exposed and sunburned (raisin- Disease Cycle and Epidemiology
ing). Occasionally, these vines appear to recover during late Sclerotia are produced in soil following infection, usually
summer and produce new shoots. Such vines may die during 15–75 cm deep in the profile although they can be found to a
the winter or decline the following year. depth of 2 m. They are the survival structures of the fungus, ca-
pable of persisting to serve as the source of primary inoculum

Fig. 143. Sudden midsummer collapse of a vine affected with

Phymatotrichopsis root rot, with characteristic adherence of brit-
tle, brown foliage. (Cour­tesy J. Kamas)

Fig. 145. Morphology of Phymatotrichopsis omnivora. A, Single

hypha. B, Strand formed by branching hyphae surrounding a
large central hypha. C, Mature strand with cruciform hyphae.
Fig. 144. Mycelial strands of Phymatotrichopsis omnivora on D, Cruciform hypha with acicular points. E, Conidia on conidio-
the surface of dead infected roots, a reliable diagnostic indica- phores from a sporemat. F, Conidia freed from conidiophore. G,
tor of Phymatotrichopsis root rot. (Cour­tesy Department of Plant Conidiophores before conidiation. H, Cross section of a sclero-
Pathology, CAE La Laguna CIAN-­INIA-­SARH, Matamoros, Coah., tium, with thick-­walled rind cells and parenchyma. (Reproduced,
Mexico) by permission, from Streets and Bloss, 1973)

72
for at least 12 years. Sclerotia germinate by producing myce- sis, premature development of fall leaf colors, wilting, defolia-
lial strands, which colonize root surfaces and form infection tion, and vine death. Affected vines may survive in an unthrifty
cushions at natural openings such as lenticels and cracks where state for several years or be killed within one growing season,
lateral roots emerge. depending on the rate and extent of disease progression.
The fungus infects the root cortex and then invades the vas- Crown and root rot do not always occur together. Portions
cular elements, impeding water translocation. Sudden wilt of of the root system and/or lower trunk infected by the pathogen
the vine occurs as a result of either extensive rotting of the root become necrotic. The stelar and cortical areas of rotted roots
system or occlusion of the vascular tissue of the main roots. become dark brown to black, whereas infected bark and sub-
The fungus moves from diseased to adjacent healthy vines by tending vascular tissues of the root crown and trunk become
colonizing their overlapping root systems, which are typically reddish brown to black. Removal of the outer bark with a sharp
distributed along the trellis where drip irrigation exists. knife reveals zones of healthy and diseased tissues that are de-
The optimum temperature for growth of P. omnivora is 28– lineated by a distinct margin (Fig. 147) until the vine dies and
30°C, which occurs in soil only during the summer months. In desiccates. Crown rot lesions may extend up the trunk above
cotton, the disease is less severe in soils with a pH of 6 or lower, the soil surface, or the necrosis may be limited to subterra-
and is most serious where soil is slightly acid to alkaline (pH nean portions of the trunk or root crown. Unlike root crown
6.5–8.5) and calcareous. infections caused by Armillaria, those caused by species of

Management
In regions where Phymatotrichum root rot occurs, planting
in infested soil can be avoided by mapping the areas where
susceptible crop plants such as alfalfa and cotton show symp-
toms. When purchasing property intended for new vineyards,
any history of cultivating cotton or alfalfa on the site should be
determined. Only healthy propagation material should be used
when planting in pathogen-­free soil. Roots with partially rotted
tissue may carry hyphal strands on their surface and mycelium
in their vascular tissue, thereby introducing the pathogen.
Vines grafted onto Dog Ridge rootstock are a good option
in sites to be replanted. This rootstock has good vigor and root
regeneration characteristics that appear to enhance its survival
compared with own-­rooted V. vinifera cultivars. However, ex-
cess vigor and low fruitfulness may be a problem with some
cultivars on this rootstock in fertile soils.

Selected References
Herrera, P. T. 1984. Investigación sobre portainjertos y su resistencia a Fig. 146. Poor spring growth of several contiguous vines afflicted
pudrición de la raíz por Phymatotrichum omnivorum. Pages 83-­93 with Phytophthora crown and root rot (center) compared with
in: En Memorias ler. Simposia International sobre Pudrición Tex- healthy neighboring vines. (Cour­tesy B. A. Latorre)
ana, Biologia, y Control de Phymatotrichum omnivorum (Shear)
Duggar. Escuela de Agricultura y Ganadeyia, Hermosillo, Son.
México-­Dic.
Lyda, S.  D. 1978. Ecology of Phymatotrichum omnivorum. Annu.
Rev. Phytopathol. 16:193-­209.
Mortensen, E. 1938. Nursery tests with grape rootstock. Proc. Am.
Soc. Hortic. Sci. 36:153-­157.
Mortensen, E. 1952. Grape rootstock for southwest Texas. Tex. Agric.
Exp. Stn. Prog. Rep. 1475.
Perry, R. L. 1980. Anatomy and morphology of Vitis roots in relation
to pathogenesis caused by Phymatotrichum omnivorum. Ph.D. diss.
Texas A&M University, College Station.
Streets, R. B., and Bloss, H. E. 1973. Phymatotrichum root rot. Mono-
graph 8. American Phytopathological Society, St. Paul, MN.

(Prepared by S. McBride and D. Appel)

Phytophthora Crown and Root Rot

Phytophthora crown and root rots have been reported on
grapevines in Australia, Chile, India, New Zealand, Spain,
and the United States (California). Many vineyards and grape
nurseries in South Africa have suffered serious economic loss
due to the disease, but in most grape-­growing regions it tends
to be localized and associated with susceptible rootstocks and
particularly wet sites and/or years.

Symptoms Fig. 147. Reddish-­brown root crown lesion characteristic of Phy-

Aboveground symptoms are similar to those of Armillaria tophthora crown and root rot, exposed by cutting through the bark
root rot and include poor shoot growth (Fig. 146), leaf chloro- after removing soil surrounding the trunk. (Cour­tesy B. A. Latorre)

73
Phytophthora do not exhibit plaques of mycelium in or under 33–48 µm); ellipsoid to ovoid or obpyriform for P. cinnamomi
the bark. (typically 75 × 40 µm); and ovoid to obpyriform with a rounded
Grapevines of any age can be affected by Phytophthora spp., base for P. cryptogea versus ovoid, obpyriform, or ellipsoid
but the rate of disease progression and frequency of mortality with a tapered base for P. drechsleri (typically about 37–40 ×
are greatest in young, small vines. In affected vineyards, dis- 23 µm for both). Hyphae of P. cinnamomi are uniquely coral-
ease occurrence is often associated with areas that have poor loid. On cornmeal agar, colonies of P. cinnamomi have a rosette
water drainage for a variety of reasons, e.g., disease frequency appearance whereas those of P. cryptogea and P. drechsleri are
may be greater in hillside areas with shallow soil overlying a radiate.
water-­impermeable layer than in lower areas with deep soil. P. parasitica Dastur produces sporangia in liquid and on
The distribution of diseased vines may also reflect a distribu- solid media. Sporangia are broadly ovoid or pyriform to spheri-
tion of inoculum related to both edaphic and external factors, cal, variable in size, papillate, sometimes intercalary, and non-
e.g., the distribution of infested planting stock. caducous. Chlamydospores form on solid media. As cultures
age, some isolates produce sex organs in single culture; oogonia
Causal Organisms vary widely in size, and antheridia are amphigynous. On corn-
Species of Phytophthora confirmed as primary causes of meal agar, most cultures exhibit a characteristic “bushy” and
the disease in pathogenicity tests include P. cactorum (Leb. & irregular rosette pattern.
Cohn) Schroet., P. cinnamomi Rands, P. cryptogea Pethyb. &
Laff., P. drechsleri Tucker, and P. parasitica Dastur. Phytoph- Disease Cycle and Epidemiology
thora megasperma Drechs. has been isolated from diseased Species of Phytophthora can be introduced into vineyards
grapevines in South Africa and California, and P. cambivora via infected plant material or infested soil and water; irrigation
(Petri) Buisman was isolated from diseased vines in California, water from rivers, canals, and ponds is frequently contaminated
but neither species has caused measurable disease consistently with them. Although species of Phytophthora generally are not
in pathogenicity tests. Phytophthora citricola Sawada was as- competitive as saprophytes in decaying tissues, they can typi-
sociated with declining grapevines in New Zealand, but its cally persist for many years once introduced into agricultural
pathogenicity was not confirmed. soils, presumably as thick-­walled oospores and chlamydospores
Worldwide, P. cinnamomi is the most prevalent and virulent that facilitate survival under adverse conditions. Evidence sug-
species of Phytophthora on grape; it is an important pathogen gests that zoospores, produced from sporangia that arise either
of the crop in Australia, California, Chile, India, New Zealand, from these resting spores or as secondary inoculum from re-
Spain, and South Africa. In South Africa, P. cinnamomi was cently infected tissues, are the principal agents of infection.
more virulent and more frequently isolated than the other spe- Episodes of soil saturation with water stimulate the production,
cies causing root and crown rot in that country, which included release, and motility of zoospores, thereby facilitating crown
P. cactorum, P. cryptogea, and P. parasitica. Phytophthora and root infection. Conversely, drainage to field capacity or
parasitica also was isolated from diseased grapevines in Cali- drier states suppresses the release and motility of zoospores,
fornia, whereas P. drechsleri has only been isolated from dis- thereby greatly limiting or preventing new infections while dry
eased vines in Chile, where P. cryptogea also has been found. soil conditions prevail. Chlamydospores and oopspores pro-
Isolations of Phytophthora spp. from tissue recently infected duced within infected tissues are liberated into the soil as the
by the pathogen are more successful than those from older ne- tissues decay, thereby completing the disease cycle.
crotic lesions well colonized by secondary decay organisms, Phytophthora-­induced diseases generally are favored by cool
and are greatly facilitated by the use of semi-­selective media. to moderate temperatures, which in Mediterranean climates
Some workers have incorporated the fungicide hymexazol such as those from which this disease is most commonly re-
to suppress closely related and commonly isolated Pythium ported occur largely from late winter through early summer
spp., which otherwise grow on these media and typically out-­ and again in the fall. However, responses to temperature differ
compete Phytophthora spp., although hymexazol can also in- among individual Phytophthora spp., e.g., infections by P. cin-
hibit growth of some Phytophthora spp. namomi are skewed toward warmer conditions than are those
Phytophthora spp. can be isolated from infested soil or water by P. cactorum. Temperature ranges for sporulation, zoospore
by using parts of plants (e.g., fruits, cotyledons, and leaf disks) release, and zoospore motility (all being components of the
as bait for swimming zoospores. Soil samples must be flooded infection process) are more restrictive than are temperatures
(typically for 48 h) to facilitate the production and dispersal of for mycelial growth and survival. Local climates and viticul-
zoospores to the baits. Many workers have used firm, green, tural practices, especially as they relate to edaphic conditions,
unblemished pear fruits as bait for Phytophthora spp., includ- can have large influences on the seasonal risk of Phytophthora
ing those that infect grape. The Phytophthora spp. can then be crown and root rot development.
isolated from the necrotic bait tissue onto a semi-­selective me- Genetic susceptibility to Phytophthora spp. varies signifi-
dium for further identification or study. cantly among grape rootstocks, and susceptible rootstocks have
Some key morphological characteristics of individual Phy- been shown to support higher population densities of P.  cin-
tophthora spp. that affect grapevines are as follows: namomi in the soil. It is not known whether environmental or
Phytophthora cactorum produces both sporangia and sex seasonal factors have important effects on the physiological
organs abundantly in single culture on solid media. Sporangia susceptibility of grapevines to Phytophthora spp., but such ef-
are broad and ellipsoidal, ovoid, or obpyriform (26–36 × 22–30 fects have been shown for other hosts.
µm); conspicuously papillate; sympodial and nonproliferous;
and caducous with a short pedicel (up to 4 µm long). Oogonia Management
are smooth-­walled and spherical (18–40 µm), tapering at the Integrating cultural and genetic approaches provides the
base. Antheridia are attached paragynously. Some isolates form most economical strategy for managing disease caused by
chlamydospores. On cornmeal agar, cultures are slightly radi- Phytophthora spp., although chemical approaches can provide
ate to uniform, with very little aerial mycelium. valuable augmentation for high-­risk areas. To minimize disease
Phytophthora cambivora, P. cinnamomi, P. cryptogea, and risk, vineyards should be established on well-­drained soils. In
P. drechsleri are heterothallic and produce nonpapillate, non- some problem areas, soil water drainage can be improved by
caducous sporangia in soil extract solution. On solid media, installing surface or subsurface drainage conduits. Planting
P. cryptogea and P. drechsleri may form a few sporangia as vines on berms helps to avoid water accumulation around root
cultures age, but P. cambivora and P. cinnamomi form none. crowns. On irrigated sites, it is advisable to minimize periods
Sporangia are usually broadly ovoid for P. cambivora (44–69 × of soil saturation, avoiding those that last longer than 24 h or

74
techniques that result in applications of excessive water near the discovery that sulfur could be used to combat the disease
the root crown. Research has shown that foliar treatments with and the development of methods for its large-­scale application
phosphonate can reduce the incidence of Phytophthora diseases brought the disease under control in France and much of Eu-
on several crops, including root rot caused by P. cinnamomi rope. Although O. tuckeri was widely presumed in Europe to
on grape. Soil treatment with mefenoxam and metalaxyl also be the same fungus described by Schweinitz in North America,
suppressed P. cinnamomi on grape. Pre-­plant soil fumigation this was not proven until the discovery of fruiting bodies of
can improve the subsequent growth of young vines, but only the sexual stage (chasmothecia, syn. cleistothecia) in France by
provides short-­term reductions in soilborne populations of Phy- Couderc in 1892. The disease was first reported in California
tophthora spp. within infested sites. vineyards in 1859.
Careful rootstock selection can reduce the incidence and se-
verity of Phytophthora crown and root rot. Under field condi- Symptoms
tions in South Africa, cultivars of own-­rooted V. vinifera were Erysiphe necator is, with the exception of the haustoria,
less susceptible to P. cinnamomi than several rootstocks that are wholly external to the host tissues, and grows upon the surface
hybrids between V.  vinifera and other Vitis spp. Furthermore, of the plant epidermis (Fig. 148). Thus, it is the actual pres-
rootstock cultivars of V. rupestris (St. George and Rupestris du ence of the pathogen’s mycelium and conidia, i.e., the whit-
Lot), V. berlandieri × rupestris (1045 Paulsen, 99 Richter, 110 ish, powdery-­appearing growth from which the disease gets
Richter, and 1103 Paulsen), and V. riparia × rupestris (3306 C) it name that is the most conspicuous feature of powdery mil-
were highly susceptible to P. cinnamomi, compared with sev- dew. Although these fungal structures are technically a sign of
eral rootstocks with V. vinifera in their parentage (i.e., Jacquez, the disease, for the sake of convenience we shall use the term
3-­5 USVIT, 3-­6 USVIT, and 2-­1 USVIT). Of the many root- symptoms to refer to the visual manifestations of the pathogen
stocks used for grape in California, only vines on Rupestris St. itself in addition to the appearance of infected host tissues.
George have been known to suffer widespread loss due to in- All green tissues of the vine may be infected. On leaves,
fection by P. cinnamomi, and only this rootstock among more symptoms vary with the source of inoculum, tissue age at the
than 20 others was consistently susceptible to P. cinnamomi in time of infection, and the age of the mildew colony. When as-
replicated greenhouse tests. cospores are the principal or sole source of primary inoculum,
colonies on the lower leaf surface are the predominant symp-
Selected References tom during the earliest stages of the epidemic. They are often
inconspicuous and are most frequently found on the first-­
Agnihothrudu, V. 1968. A root rot of grapes in Andhra Pradesh. Curr. formed leaves closest to the trunk or arms of the vine, where
Sci. 37:292-­294.
the ascospore-­bearing chasmothecia are most likely to have
Erwin, D. C., and Ribeiro, O. K. 1996. Phytophthora Diseases World-
wide. American Phytopathological Society, St. Paul, MN. overwintered (Fig. 149). Infection of the lower leaf surface
Latorre, B. A., Wilcox, W. F., and Muñoz, R. 1997. Crown and root often produces chlorotic spots on the upper surface (Fig. 150),
rot of table grapes caused by Phytophthora spp. in Chile. Vitis which may sometimes be confused with the “oil spot” symp-
36:195-­197. tom of downy mildew. On cultivars with dense leaf hairs on
Marais, P. G. 1980. Fungi associated with decline and death of nursery the lower leaf surfaces, the pathogen may not be visible to the
grapevines in the Western Cape. Phytophylactica 12:9-­13. naked eye, but with care can be resolved by a 15–20× hand lens.
Marais, P. G. 1988. Grapevine roots and soil-­borne fungi. Pages 106-­ On leaves with smooth lower surfaces, mildew colonies are at
137 in: The Grapevine Root and its Environment. J. L. Van Zyl, ed. first white with a silver-­gray or very light-­brown tinge. On the
Tech. Comm. 215. Republic of South Africa, Department of Agri- upper leaf surfaces, young colonies appear whitish and show
culture and Water Supply, Pretoria. a somewhat metallic sheen. They may only be visible at a low
Marais, P. G., and Hattingh, M. J. 1986. Reduction of root rot caused viewing angle, by looking across the leaf; this is especially true
by Phytophthora cinnamomi in grapevines by chemical treatments. for colonies that have not yet sporulated. Colonies are roughly
Plant Dis. 70:109-­111. circular, occur singly or in groups, and range in size from a few
Zentmyer, G. A. 1980. Phytophthora cinnamomi and The Diseases It
Causes. Monogr. 10. American Phytopathological Society, St. Paul,
millimeters to a centimeter or more in diameter. Older and pro-
MN. fusely sporulating colonies are most conspicuous, and are stark
white (Fig. 151). Senescent colonies eventually turn grayish,
(Prepared by G. T. Browne and B. A. Latorre) and by mid-­to late season may bear large numbers of yellow
(immature) or black (mature) chasmothecia, the sexual fruiting

Powdery Mildew
Perhaps because of its lack of dependence on rainfall for
secondary spread, high reproductive potential, and the general
susceptibility of Vitis vinifera, powdery mildew is the most
consistently troublesome disease of grapevines worldwide.
Powdery mildew, also called Oïdium, Mehltau, Echter Mehl-
tau, Schimmel, Äscherich, Oidio, mal bianco, and cenicilla,
is caused by Erysiphe necator Schw. The fungus was first de-
scribed in eastern North America, the region to which it ap-
pears to be native, in 1834 by Schweinitz as Erysiphe necator,
and this taxonomic assignation has recently been readopted,
although Uncinula necator (Schw.) Burr. is encountered more
commonly in literature published between 1900 and 2005. The
organism was exclusively a minor pathogen of native Vitis spe-
cies in North America until 1845, when it was first observed in
a glasshouse in Margate, England by Tucker, for whom Berke-
ley named the anamorph Oidium tuckeri in 1847. By 1850,
the pathogen had spread throughout Europe and caused stag- Fig. 148. Hyphae of Erysiphe necator growing on the surface of
gering losses that often approached 100%. By 1858, however, an infected grape leaf. (Cour­tesy D. M. Gadoury)

75
bodies of the pathogen (Fig. 152). Dead epidermal cells may ing those of the nascent inflorescence during bud formation the
be observed throughout the colonized area, as natural mor- previous season) or infection of berries within one week after
tality in the mildew colony, use of fungicides, mycoparasites, their formation result in the most severe manifestation of the
or resistance responses in the leaf result in the deaths of seg- disease, and such tissues may be completely coated with whit-
ments of the mildew colony and the infected epidermal cells ish mildew colonies. The epidermis of such berries ceases to
(Fig. 153). Severely affected leaves usually senesce, develop grow during berry expansion, often causing the skin to split
necrotic blotches, and fall prematurely (Fig. 154). Infection of
stems initially produces symptoms similar to those on leaves,
with affected areas turning black as the disease progresses and
epidermal cells are killed. Eventually, the mildew colonies are
killed as periderm forms in maturing canes, resulting in a dark,
weblike scarring of the affected area (Fig. 155).
Berries may be infected directly by windborne conidia or
ascospores, or by spread of a colony originating on the rachis
or pedicel (Fig. 156). Prebloom infections of the cluster (includ-

Fig. 151. Characteristic foliar symptom of powdery mildew, con-

sisting of white sporulating colonies of Erysiphe necator. (Cour ­tesy
W. F. Wilcox)

Fig. 149. Inconspicuous powdery mildew colony on the abaxial

(lower) surface of a young leaf near the vine trunk, resulting from
primary, ascosporic infection by Erysiphe necator. (Cour­tesy D. M.
Gadoury)

Fig. 152. Immature (yellow) and mature (black) chasmothecia of

Erysiphe necator on the surface of a grape leaf with powdery mil-
dew. (Cour­tesy D. M. Gadoury)

Fig. 153. Patches of necrotic epidermal leaf cells resulting from

Fig. 150. Chlorotic spots on the adaxial (upper) surface of powdery mildew development, surrounded by senescing (gray)
a leaf that has been colonized by Erysiphe necator on the and young (white) colonies of Erysiphe necator. (Cour­tesy W. F.
abaxial surface directly opposite. (Cour­tesy R. C. Pearson) Wilcox)

76
(Fig. 157), and the berry eventually desiccates and mummifies and flag shoots are generally less vigorous than those arising
(Fig. 154) or becomes rotted by other fungi and bacteria. Ber- from healthy buds (Fig. 161). Accordingly, their discovery in
ries become highly resistant to new infections as they age, but the vineyard may be delayed, and made more difficult by the
those in a transitional stage between susceptible and resistant obscuring growth of the healthy shoots. Leaves on flag shoots
(typically, about 3–4 weeks after anthesis, or cap fall) may may be cupped, dwarfed, or distorted, even before conspicuous
develop diffuse infections characterized by a loose colony of mildew colonies are seen (Fig. 162). Copious sporulation on flag
nonsporulating hyphae. These are generally not visible to the
naked eye, but can be resolved with low-­power magnification.
Diffuse colonies die as berries continue to mature, leaving be-
hind a network of necrotic epidermal cells (Fig. 158).
In viticultural regions where low winter temperatures do not
preclude it, overwinter survival of infected buds results in a
distinctive foliar symptom when these buds give rise to shoots
the following spring. In the most severe cases, such shoots are
systemically infected and so heavily coated with fungal growth
that they appear stark white and stand out like white flags in
the vine, resulting in the term flag shoots (Fig. 159). More
commonly, colonization of a flag shoot is less extensive and
infection of a single leaf, or of leaves on one side of the shoot
only, is observed (Fig. 160). The degree of colonization of the
bud prophylls and leaf primordia within lateral buds may de-
termine the macroscopic appearance of flag shoots the follow-
ing season; incomplete colonization leads to the appearance of
colonies on only one or two leaves and/or parts of the petioles
and stem, whereas heavy colonization of the bud interior may
Fig. 156. Expansion of an Erysiphe necator colony to a young
lead to stark white, heavily colonized shoots that die soon after
‘Concord’ berry following prebloom infection of the rachis. (Cour­
sporulation occurs. Breaking of infected buds is often delayed, tesy D.  M. Gadoury; Reproduced, by permission, from Gadoury
et al., 2001)

Fig. 154. Symptoms of severe powdery mildew development on

an unsprayed ‘Chardonnay’ vine, including leaf necrosis, prema- Fig. 157. ‘Chardonnay’ berries infected by Erysiphe necator soon
ture defoliation, and berry desiccation. Healthy, treated vines are after their formation, coated with white mildew colonies and split-
in the background. (Cour­tesy W. F. Wilcox) ting due to poor epidermal expansion. (Cour­tesy C. N. Austin)

Fig. 158. Nonsporulating hyphae of Erysiphe necator within a dif-

fuse powdery mildew colony on a berry inoculated approximately
3 weeks after the end of bloom, and subtending patches of ne-
Fig. 155. Blackened tissue on shoots infected with Erysiphe ne- crotic epidermal cells. (Cour­tesy D. M. Gadoury; Reproduced, by
cator. (Cour­tesy R. C. Pearson) permission, from Gadoury et al., 2007)

77
shoots depends upon occurrence of favorable air temperatures
and may be observed as early as 2 weeks after shoot growth
begins. Even where they occur, flag shoots are usually present
in low frequency. However, they provide intense point sources
of inoculum early in the growing season, and this feature often
pinpoints their presence in the canopy retrospectively, as nu-
merous colonies resulting from secondary disease spread are
eventually observed on the surrounding shoots and vines.

Causal Organism
Erysiphe necator Schw. (syns. Uncinula necator (Schw.) Burr.,
E. tuckeri Berk., U. americana Howe, U. spiralis Berk. & Curt;
anamorph Oidium tuckeri Berk.) is obligately parasitic upon gen-
era within the Vitaceae, including Vitis, Cissus, Parthenocissus,
and Ampelopsis. Hyaline hyphae (4–5 µm in diameter) are super-
ficial upon epidermal cells, with the exception of globose hausto-
ria formed at regular intervals along the hyphal strands beneath
lateral, multilobed appressoria. Haustoria, the feeding organs of
the fungus, penetrate the epidermal cell walls and associate with
the outer surface of the subsequently invaginating epidermal cell
membrane, through which they absorb nutrients. Segments of
semipersistent hyphae frequently die in response to temperature Fig. 161. Flag shoot with inconspicuous powdery mildew colonies
extremes, ultraviolet radiation, fungicide applications, or devel- (far left), exhibiting reduced and deformed growth relative to adja-
opment of resistance in host tissues, which may lead to the death cent healthy shoots. (Cour­tesy M. Sosnowski)
of many of the epidermal cells harboring haustoria.
Conidiophores are multiseptate (10–400 µm in height) and
form perpendicular to the prostrate hyphae, densely in rapidly

Fig. 159. Heavily colonized “flag shoot” resulting from springtime

growth of a bud infected by Erysiphe necator the previous grow-
ing season. (Cour­tesy R. C. Pearson)
Fig. 162. Dwarfed, cupped leaves in a close-
u p of a powdery mildew flag shoot, with few
­
signs of fungal growth yet developed. (Cour­tesy
M. Sosnowski)

Fig. 160. Young shoot only partially colonized by Erysiphe ne-

cator following perennation of the pathogen within the bud from Fig. 163. Chains of hyaline conidia of Erysiphe necator. (Cour ­tesy
which it arose. (Cour­tesy W. D. Gubler) M. J. Welser)

78
growing colonies on susceptible tissue but less so on more re- wall eventually darken, as do the basal cells of the appendages
sistant tissues. Conidia are hyaline, cylindro-­ovoid, with one that form the characteristic uncinate tips during the final phase
to two large water-­containing vacuoles. They measure 27–47 of development, about 4 weeks after the ascocarp is initiated;
× 14–21 µm, although their dimensions in various mountants by this time, the ascocarp wall is heavily melanized and dark
are strongly affected by the osmotic potential of the spore cy- brown. Anchorage hyphae and the parent hyphae die after 4 to
toplasm relative to the mountant employed, and the presence 5 weeks under typical field temperatures during the mid-­to late
of a highly elastic conidial cell wall. Individual conidiophores summer, and the chasmothecium develops a basal concavity,
generally produce only one conidium per day, although under effectively disconnecting it from the mildew colony.
still-­air conditions, conidia may accumulate in chains over a Chasmothecia contain four to six asci at maturity, each of
period of several days (Fig. 163), the oldest conidium at the dis- which contains usually four and as many as seven hyaline,
tal end. Long conidial chains are rarely seen under field condi- ovate to subglobose ascospores, 15–25 µm × 10–14 µm; how-
tions, as the conidia are easily dislodged and dispersed by even ever, as with conidia, exact spore dimensions are sensitive to
low-­velocity wind. Conidia germinate via a single germ tube, the osmotic potential of the mountant used in their examina-
which terminates in a lobed appressorium. tion. Although ascocarps may reach morphological maturity in
Populations are bipolar-­heterothallic, and ascocarps are ini- 4 weeks, physiological maturity may not be reached for several
tiated within 24 h of contact between hyphae of compatible months, particularly in colder climates. Physiologically mature
mating types. Nearly all literature published before 2010 re- chasmothecia dehisce circumscissally when in contact with free
ferred to the ascocarps as cleistothecia, but this term has been water. No longer under restriction of the ascocarp wall, the asci
superseded by chasmothecia in more recent literature. Within expand greatly, push back the upper half of the chasmothecium,
72 h, the hyaline ascocarp initial increases to 40 µm in diam- and discharge ascospores forcefully through a slitlike rupture of
eter. Anchorage hyphae form as short outgrowths of cells of the the ascus tip. Like conidia, ascospores germinate with a single
outer ascocarp wall and become intertwined in the subtending germ tube, which terminates in a lobed appressorium.
mildew colony, but form no functional connections or appres-
soria. Ascocarps turn yellow after about 7 days as a yellow lipid Disease Cycle and Epidemiology
accumulates in the centrum and wall cells. The upright and The general disease cycle for powdery mildew is shown in
bristlelike appendages are initiated after about 3 weeks of age, Fig. 164. In areas with relatively mild winters, mycelium with
and are arranged equatorially. The cells of the outer ascocarp haustoria and conidia can survive the dormant period within

Fig. 164. Disease cycle of powdery mildew. (Drawing by E. Gotham from R. Sticht)

79
infected lateral buds, which give rise to conidia-­bearing flag ing types upon the same tissue becomes possible. On heavily
shoots the following spring. Buds that subsequently give rise diseased vines, they may be found by mid-­summer; however,
to flag shoots can form soon after shoot growth begins in the under effective control programs, significant numbers usually
spring. Surface tissues of basal bud positions are very suscep- do not form until the end of the season, after spray programs
tible to infection from budbreak until shoots have elongated have eased. In areas where chasmothecia do occur by mid-­
to contain six true leaves (BBCH stages 9–16), and coloniza- summer, e.g., the central coast of California and South Austra-
tion of their surface during this period promotes ingress of the lia, there can be late-­season ascospore release with subsequent
colony to the interior of the bud, as bud scales and leaf pro- new infections from these sources in addition to conidia. Chas-
phyls develop. With the exception of the meristem, all tissues mothecia also may be found on other severely infected tissues,
of the dormant bud may be colonized subsequently. Suscep- such as berries (Fig. 165), rachises, or shoots late in the grow-
tibility of lateral buds near the base of shoots decreases rela- ing season. Given sufficient time to mature morphologically
tively quickly as they age—i.e., by BBCH stage 19 (nine true (i.e., approximately 4–6 weeks after initiation, depending on
leaves present)—owing to the progressive suberization of the temperature), chasmothecia become detached from the anchor-
bud surface. However, as shoots continue to extend, new lat- age hyphae. In areas with sufficient rainfall, nearly all mature
eral buds in susceptible stages continue to be formed near the ascocarps are dispersed by rain to either the bark of the vine,
apex of the growing shoot. Whereas on spur-­pruned vines the where some survive the winter, or to the soil. They may also
exclusive retention of basal buds necessarily restricts the origin be dispersed by very high winds. Naked chasmothecia appar-
of flag shoots to buds infected very early in the growing sea- ently do not survive on or in soil. However, in climates with
son, on cane-­pruned vines flag shoots may be found emerging relatively low rainfall and mild winter temperatures (e.g., Cali-
from nearly any position (hence, from infections initiated at fornia, South Australia, or Italy), they do not completely dis-
any time during the previous season). It is presumed that infec- perse from the leaves and some survive within leaf litter on the
tions of lateral buds reduce their winter hardiness, accounting vineyard floor.
for the relative lack to complete absence of flag shoots follow- In spring, ascospores are discharged when the ascocarps are
ing the occurrence of winter temperatures well below freezing wet from rain or irrigation (Fig. 166). Fog and heavy dew may
in colder viticultural regions (e.g., interior regions of Europe, also release ascospores if chasmothecia become sufficiently
and eastern Washington and New York in the United States). wet. The period of ascospore release in New York begins near
However, it is also possible that the pathogen itself is incapable bud break and continues until the bloom or early postbloom
of surviving these low temperatures as nascent infections. For period. Similar periods of spring ascospore release have been
example, debilitation of active E. necator colonies and transient reported in several other regions. In both California and South
resistance to new infections have been demonstrated following Australia, some chasmothecia may also release ascospores
brief (e.g., 2 h) exposure of leaves to temperatures between 2 during fall or winter rains. In general, ascosporic infection is
and 8°C, and such overnight low temperatures have been docu- favored by precipitation in excess of 2–3 mm coincident with
mented to occur commonly before bloom in many viticultural temperatures above 10°C, although infection becomes increas-
regions. ingly likely as temperatures increase to an optimum value of
The pathogen also overwinters in nearly all viticultural approximately 25°C. Although free water is necessary to initi-
regions as chasmothecia, providing an additional source of ate discharge of the ascospores from chasmothecia, continued
primary inoculum where flag shoots are common, and the wetness is not required for subsequent spore germination and
principal to sole source where flag shoots are rare to absent. infection.
Chasmothecia are formed primarily on foliage once disease se- Where ascospores are the only propagules of primary in-
verity has increased to a level where pairing of compatible mat- oculum, new leaves may be infected as they form, but foliar
disease severity typically does not increase markedly until after
bloom. Therefore, although disease incidence may increase
rapidly beforehand, low severity usually makes it inconspicu-
ous to the casual observer. However, without effective fungi-

Fig. 165. Small, black chasmothecia of

Erysiphe necator forming on severely
infected cv. Chardonnay berries in late sum- Fig. 166. Rupturing chasmothecium of Erysiphe necator with asci
mer. (Cour­tesy W. F. Wilcox) containing ascospores (× 400). (Cour­tesy R. C. Pearson)

80
cide treatment, foliar severity increases rapidly toward bloom in the shade, e.g., temperature increases ranging from 2 to 13°C
because temperatures optimal for mildew development persist have been measured for exposed versus shaded leaves in cli-
for increasing portions of the day. It is usually during this phase mates as diverse as New York and South Australia, depend-
that observers first notice an outbreak of the disease. ing on the intensity of the sunlight and the water status of the
Where flag shoots serve as sources of primary inoculum, vines at the time of measurement. Furthermore, the detrimental
an additional level of complexity may be introduced into the effects of UV radiation are more pronounced at 28°C than at
development of the epidemic. Coincident with the random 20 or 25°C, indicating the synergistic effects of UV and heat
distribution of ascosporic inoculum, a variable density of flag at supraoptimal temperatures. Thus, disease severity is often
shoots may occur throughout the vineyard. A focus of disease several times greater on shaded tissues than on those afforded
develops early in the growing season around each flag shoot, good sunlight exposure.
as intense conidial production spreads the disease to nearby Free water is detrimental to E. necator mycelium and co-
shoots and vines. Usually, these disease foci persist until after nidia; however, in the field, this effect may be more than offset
bloom, but may become less obvious as they coalesce and gen- by the favorable impacts of moderate temperatures, limited di-
eral disease levels increase throughout the vineyard. On varie- rect sunlight, and high humidity that are all likely to precede
ties highly susceptible to bud infection (e.g., Carignane), flag and follow rain events. Thus, the most severe mildew epidem-
shoots may be observed on the same vines year after year, thus ics often accompany atypically rainy growing seasons, despite
making prior flag shoot location a key component of disease the deleterious impact upon the pathogen of discrete periods of
monitoring for advisory programs. free water.
Temperature is the principal environmental factor that regu- Leaves are most susceptible to infection when half expanded,
lates growth and secondary spread of the pathogen. Mildew and susceptibility is reduced significantly after they have fully
colonies grow and sporulate most rapidly from 23 to 30°C, and expanded and begun to age. However, leaves never become
the latent period (time from the start of infection to produc- immune to infection, and older ones can support substantial
tion of new conidia from the resulting colony) can be as short quantities of powdery mildew. Additionally, in some environ-
as 5–6 days if temperatures are constantly within this range. ments and management systems, the indeterminate growth
However, the pathogen is considerably less robust and the latent of shoots and forcing of laterals by summer hedging insures
period increases significantly under cooler conditions, i.e., to a continual supply of highly susceptible young leaves, and an
11, 18, and 25 days at constant temperatures of 15, 12, and 9°C, ever-­increasing supply of older, less susceptible ones.
respectively. Recent studies conducted under the fluctuating In contrast to that of leaves, the period of fruit susceptibility
temperature conditions of the field suggest that latent periods is relatively brief. Individual berries of V. vinifera cultivars are
can be approximately 30% longer than would be expected on highly susceptible to infection for the first 1–2 weeks after they
the basis of daily average temperatures if nighttime lows drop have set, and infection during this period can lead to complete
below 8°C, particularly during the first 4–6 weeks of the grow- destruction of the fruit. Although older references usually asso-
ing season. The lower and upper temperature limits for disease ciate sugar accumulations of 8% or more with berry resistance,
development are 6 and 32°C, respectively. Germination of co- a high level of ontogenic (age-­related) resistance is widely ob-
nidia is inhibited at 35°C and conidia can be killed after ex- served at 3–4 weeks after the completion of bloom, at which
posure to higher temperatures, with the lethal exposure time a time the concentration of soluble solids (°Brix) is still basal,
function of temperature, e.g., 12, <5, and 0.5 h at temperatures fluctuating between 4 and 5%. The inconspicuous, diffuse in-
of 38, 40, and 44°C, respectively, in laboratory studies. Simi- fections that develop on berries that become infected as they
larly, many of the hyphae within mildew colonies may be killed transition to a resistant state at this time may result in a deg-
by high temperatures that persist for a critical duration, e.g., 20, radation of wine quality by both exacerbating the severity of
6, and 1 h at 36, 40, and 44°C, respectively. However, mortality Botrytis bunch rot and elevating populations of other microor-
resulting from high temperatures is commonly incomplete in ganisms that lead to spoilage during fermentation. Diffuse in-
the field, especially within the shaded interior of the canopy, fections also have been associated with increased wounding by
and surviving portions of colonies may resume activity if tem- fruit-­feeding insects, particularly wasps (Vespula spp.), which
peratures again become favorable. appear to be attracted by increased levels of volatile compounds
Other environmental factors influencing disease develop- emitted by these berries even before visible symptoms of decay
ment include atmospheric humidity and sunlight exposure. are seen. Berries of less susceptible Vitis species and interspe-
Although E. necator is unique among the fruit and foliar patho- cific hybrids appear to develop ontogenic resistance earlier than
gens of grapevines in its ability to thrive in both arid and humid those of V.  vinifera, e.g., berries of Vitis × labruscana ‘Con-
climates, powdery mildew develops optimally at a relative hu- cord’ are virtually immune within 2 weeks after fruit set.
midity of approximately 85%, and both incidence and sever-
ity decrease moderately but progressively as the air becomes Management
drier. For example, under controlled conditions at an optimum All cultivars of V.  vinifera, a species that evolved in the
temperature of 25°C, disease severity at 40% relative humidity absence of the pathogen, are susceptible to powdery mildew,
was approximately one-­half that at 85%, with a linear response some especially so. A number of cultivars of native North
to the humidity level occurring over that range. Germination American species and interspecific hybrids show considerably
of conidia responds similarly, but unlike mycelial growth and more resistance, but demand for them is limited outside a few
sporulation, germination frequency is severely inhibited at rela- specific regions and markets. Therefore, commercial control of
tive humidity values above approximately 87%. powdery mildew generally requires a significant use of fungi-
Ultraviolet (UV) light also is detrimental to the fungus, cides, although cultural practices are important components of
which resides primarily on the surface of infected grape tis- an integrated management program and can greatly impact the
sues and is without protective pigmentation. Exposure to UV success and requisite number of fungicide applications. Prun-
radiation reduces both the frequency and rate of conidium ing and training of the grapevine canopy should provide good
germination, appressorium formation, and subsequent colony ventilation and promote sunlight exposure in the cluster zone
expansion, prolonging the latent period and reducing disease to whatever extent is possible without causing sunburn. This
severity relative to tissues protected from UV radiation. These not only creates a microclimate around bunches that is less fa-
effects appear to be cumulative, i.e., the latent period is simi- vorable to the pathogen (by reducing humidity and exposing
larly increased by four daily 6-­h exposures or a single 24-­h them to solar radiation), but also greatly facilitates their effec-
exposure. Furthermore, surface temperatures of grapevine tis- tive coverage by the applied fungicides. Selective removal of
sues in direct sunlight often are substantially higher than those leaves around the clusters immediately after fruit set, while

81
the berries are still highly susceptible to infection, has been Good season-­long control of foliar (and bud) infections is also
shown to aid in control of powdery mildew as well as Botrytis the best means of minimizing the level of primary inoculum
bunch rot. Biological control by species of the soilborne bacte- available to initiate disease the following season. To maintain
rium Bacillus, the mycoparasite Ampelomyces quisqualis, and such control, postharvest fungicide applications may be neces-
the mycophageous mite Orthotydeus lambi, has met with lim- sary in regions where conditions are conducive to disease de-
ited commercial and/or experimental success, although these velopment for prolonged periods after the crop has been taken.
organisms may augment the level of suppression provided by In general, from 4 to 6 weeks of frost-­free weather are required
fungicides in plantings where they can be introduced success- for late-­season infections to form mature chasmothecia before
fully or occur naturally. the leaves sustaining their development are killed.
Fungicide applications typically commence early in the Sulfur is the fungicide used most widely against powdery
growing season. In regions where chasmothecia are the major mildew worldwide. Its efficacy, relatively low cost, and lack of
or sole source of primary inoculum, infections can occur once pathogen resistance have made it a central component of man-
an adequate rain (2–3 mm) has fallen and temperatures reach at agement programs for over 160 years. Sulfur provides control
least 10°C; thus, fungicide programs may need to begin shortly through a combination of protective, curative (postinfection),
after bud break if such conditions occur, but may be delayed and eradicative activities, although its value for eradication
by one to several weeks thereafter if cool conditions or a lack is limited against dense, well-­ developed colonies. Activity
of rainfall delays the development of primary infections. In appears to accrue through both direct contact of the applied
California, an application of wettable sulfur near completion of material (especially when applied in aqueous suspensions) and
budbreak yields enhanced suppression of powdery mildew, pre- redistribution through the vapor phase. Due to the latter mecha-
sumably by acting against the earliest ascosporic inoculum. In nism, activity has often been stated to decline at temperatures
areas with regular occurrences of flag shoots, these sites of pri- below 18°C, although controlled studies have shown little to
mary infection are present within 1–2 weeks after bud break, no loss of efficacy at lower temperatures. Conversely, phyto-
and fungicide coverage should commence as early as BBCH toxicity may occur with applications made above 30°C, and is
stage 13 (three unfolded leaves) to limit secondary spread and progressively more likely as temperatures increase beyond this
colonization of young lateral buds at the base of the new shoots. limit. Studies in South Australia have indicated that sulfur phy-
Several systems for determining the most efficient timing of totoxicity is dependent upon both temperature and relative hu-
fungicide applications throughout the remaining season have midity, with little to no injury at temperatures as high as 45°C
been utilized in different parts of the world. In California, a if relative humidity remains below 70%, whereas phytotoxic-
disease risk assessment index has been developed based largely ity occurs at temperatures above 35°C when relative humidity
upon the rapid reproduction of E. necator at temperatures be- exceeds 70%. Phytotoxicity is also genotype-­dependent, being
tween 21 and 30°C, the relatively slow development of disease more likely on some V.  vinifera cultivars than others. Severe
under cooler conditions, and the deleterious effect of tempera- phytotoxicity, regardless of temperature, precludes the use of
tures >35°C. In Germany, a different system has been devel- sulfur on some cultivars of Vitis spp. native to North America
oped, initially utilizing a combination of the previous season’s and their interspecific hybrids, particularly red-­or purple-­
disease severity and lowest winter temperature (i.e., the proba- fruited types. The utility of sulfur also is compromised in vari-
bility of bud perennation and subsequent flag shoot formation) ous regions by its being washed off treated vines during rains,
plus current temperature and relative humidity conditions, as- although this limitation can be addressed to some extent by
suming a minimum of 65% relative humidity for robust disease utilizing sprayable formulations with very small particle sizes,
development. Recently, this system has been adapted also to increasing the application rate, and/or adding an appropriate
account for the heightened sensitivity of clusters to infection surfactant to the spray solution.
in the prebloom through early postbloom period as discussed A number of different classes of modern organic fungicides
below. In some warmer regions of Australia, an empirical sys- provide excellent control of powdery mildew, including the
tem has been developed in which sprays are restricted to the benzimidazoles; the DMI and morpholine subgroups of the er-
period of 2–6 weeks following bud break, after which condi- gosterol biosynthesis inhibitors; the strobilurin members of the
tions are typically too hot and sunny for significant disease de- QoI class; various SDHI materials; and several newer powdery
velopment. Although all such systems are based upon certain mildew-­specific compounds that include quinoxyfen and the re-
fundamentals of pathogen biology, each tends to emphasize the lated the related proquinazid, metrafenone, and cyflufenamid.
influence of specific factors that are particularly determinative Relative to sulfur, these materials offer the advantages of main-
under local conditions. taining efficacy with lower use rates and longer application in-
The timing of fungicide applications and choice of materials tervals; being much less subject to removal by rainfall; and in
may be influenced by the stage of crop development. Because some cases, providing a broader spectrum of activity against
individual berries of V. vinifera cultivars are most susceptible to additional fungal pathogens. However, the high reproductive
infection from the immediate prebloom period until 1–2 weeks rate of E. necator, its ability to infect under a wide range of
after their caps fall and retain significant susceptibility for ap- climatic conditions, and its ready dispersal by air currents col-
proximately 2 additional weeks, management efforts should be lectively promote the rapid development of pathogen popula-
at their peak during this critical period, placing particular em- tions resistant to specific fungicides if these materials are used
phasis on factors such as fungicide quality and rate, appropriate in a manner that selects for resistant biotypes. The speed with
intervals between sprays, and quality of the spray application which control failures have occurred in specific commercial
technique. However, the protracted, asynchronous opening of vineyards illustrates the need for implementing resistance man-
grapevine flowers that occurs in viticultural regions with rela- agement practices whenever utilizing modern synthetic fungi-
tively warm winters (e.g., California, South Australia, Chile, cides, virtually all of which should be considered at risk for
etc.) may extend this critical period for the youngest berries in resistance development.
a cluster until approximately 6 weeks after the general onset of Erysiphe necator is unique in that, unlike all other fungal
flowering. Applications after berries have become resistant to pathogens of grapes, its “body” (thallus) resides almost en-
infection are generally designed to prevent infection of clus- tirely on the surface of infected tissues. This feature renders it
ter rachises and the foliage. Although the necessary degree of susceptible to topical applications of an assortment of materi-
foliar control may vary among cultivar and intended market als that have little, if any, direct activity against other fungal
for the fruit, healthy foliage is generally required to ripen the pathogens, the thalli of which are protected from such treat-
crop and provide storage carbohydrates to the vine, which may ments inside the tissues that they infect. Examples of effective
be critical to survival in regions with low winter temperatures. topical materials include botanical and petroleum-­based oils,

82
inorganic salts (e.g., potassium bicarbonate, monopotassium Kast, W. K., and Bleyer, K. 2011. Efficacy of sprays applied against
[dihydrogen potassium] phosphate), and hydrogen peroxide (di- powdery mildew (Erysiphe necator) during a critical period for in-
hydrogen oxide). Such materials, which are effective primarily to fections of clusters of grapevines (Vitis vinifera). J. Plant Pathol.
exclusively when used in a curative or eradicative mode, rely on 93:S1.29-­S1.32.
direct contact with the fungal thallus and, therefore, are highly Moyer, M. M., Gadoury, D. M., Cadle-­Davidson, L., Dry, I. B., Wilcox,
dependent upon complete spray coverage for their activity. How- W. F., and Seem, R. C. 2010. Development of an advisory system
for grapevine powdery mildew in eastern North America: A reas-
ever, residues of many such materials have little or no effect upon sessment of epidemic progress. Plant Health Progress doi:10.1094/
spore germination and penetration processes, so they provide PHP-­2010-­0526-­02-­SY.
limited to no protective activity following an application. Cop- Moyer, M.  M., Gadoury, D.  M., Cadle-­ Davidson, L., Dry, I.  B.,
per, captan, dithiocarbamates, and several other traditional pro- Magarey, P.  A., Wilcox, W.  F., and Seem, R.  C. 2010. Effects of
tectant fungicides provide moderate suppression of the disease, acute low temperature events on development of Erysiphe necator
but their activity is generally inadequate on highly susceptible and susceptibility of Vitis vinifera. Phytopathology 100:1240-­1249.
varieties, particularly under high disease-­pressure conditions. Pearson, R. C., and Gadoury, D. M. 1987. Cleistothecia, the source of
primary inoculum for grape powdery mildew in New York. Phyto-
Selected References pathology 77:1509-­1514.
Peduto, F., Backup, P., Hand, E. K., Janousek, C. N., and Gubler, W. D.
Austin, C. N., Meyers, J., Grove, G. G., and Wilcox, W. F. 2011. Quan- 2013. Effect of high temperature and exposure time on Erysiphe ne-
tification of powdery mildew severity as a function of canopy vari- cator growth and reproduction: Revisions to the UC Davis powdery
ability and associated impacts on sunlight penetration and spray mildew model risk index. Plant Dis. 97:1438-­1447.
coverage within the fruit zone. Am. J. Enol. Vitic. 62:23-­31. Rumbolz, J., and Gubler, W. D., 2004. Susceptibility of grapevine buds
Austin, C. N., and Wilcox, W. F. 2011. Effects of fruit zone leaf re- to infection by the grapevine powdery mildew fungus Uncinula ne-
moval, training system, and variable irrigation on powdery mildew cator (Schw.) Burr. Plant Pathol. 54:535-­548.
development on Vitis vinifera L. Chardonnay. Am. J. Enol. Vitic.
62:193-­198. (Prepared by D. M. Gadoury, W. F. Wilcox, J. Rumbolz,
Austin, C.  N., and Wilcox, W.  F. 2012. Effects of sunlight expo­ and W. D. Gubler)
sure on grapevine powdery mildew development. Phyto­pathology
102:857-­866.
Bulit, J., and Lafon, R. 1978. Powdery mildew of the vine. Pages 525-­
548 in: The Powdery Mildews. D. M. Spencer, ed. Academic Press, Ripe Rot
New York.
Carroll, J. E., and Wilcox, W. F. 2003. Effects of humidity on the devel- As its name implies, ripe rot develops on grapes as they mature
opment of grapevine powdery mildew. Phytopathology 93:1137-­1144. and near harvest. This disease was first reported in the United
Delp, C.  J. 1954. Effects of temperature and humidity on the grape States in 1891 and has since been found in most warm and moist
powdery mildew fungus. Phytopathology 44:615-­626.
regions where bunch and muscadine grapes are grown. Losses
Doster, M. A., and Schnathorst, W. C. 1985. Effects of leaf maturity
and cultivar resistance on development of the powdery mildew fun-
from the disease are greatest during warm, wet seasons.
gus of grapevines. Phytopathology 75:318-­321.
Gadoury, D. M., and Pearson, R. C. 1988. Initiation, development, dis- Symptoms
persal, and survival of cleistothecia of Uncinula necator in New The primary symptom of this disease is rotting of the ripe
York vineyards. Phytopathology 78:1413-­1421. fruit. Affected berries initially develop circular, reddish-­brown
Gadoury, D.  M., and Pearson, R.  C. 1990. Ascocarp dehiscence spots of decay on their skins (Fig. 167). The spots subsequently
and ascospore discharge in Uncinula necator. Phytopathology enlarge to include entire berries, which characteristically be-
80:393-­401. come covered with salmon-­colored masses of conidia as they
Gadoury, D. M., Seem, R. C., Ficke, A., and Wilcox, W. F. 2001. The decay (Fig. 168). Eventually, diseased berries shrivel and su-
epidemiology of powdery mildew on Concord grapes. Phytopathol- perficially resemble those in the terminal stages of several
ogy 91:948-955. other rot diseases (black rot, bitter rot, Phomopsis), although
Gadoury, D. M., Seem, R. C., Ficke, A., and Wilcox, W. F. 2003. Onto- the presence of the characteristic conidia is diagnostic for ripe
genic resistance to powdery mildew in grape berries. Phytopathol- rot (Fig. 169). Rotted fruit of most grapes typically remain at-
ogy 93:547-­555.
Gadoury, D.  M., Seem, R.  C., Wilcox, W.  F., Henick-­K ling, T.,
tached to the rachis, although those of Vitis rotundifolia may
Conterno, L., Day, A., and Ficke, A. 2007. Effects of diffuse coloni- drop when the rot is complete. Symptoms are not common on
zation of grape berries by Uncinula necator on bunch rots, berry mi- leaves or shoots.
croflora, and juice and wine quality. Phytopathology 97:1356-­1365.
Gadoury, D. M., Cadle-­Davidson, L., Wilcox, W. F., Dry, I. B., Seem,
R.  C., and Milgroom, M.  G. 2012. Grapevine powdery mildew
(Erysiphe necator): A fascinating system for the study of the biol-
ogy, ecology and epidemiology of an obligate biotroph. Mol. Plant
Pathol. 13:1-­16.
Gubler, W. D., Rademacher, M. R., Vasquez, S. J., and Thomas, C. S.
1999. Control of powdery mildew using the UC Davis powdery mil-
dew risk index. APS Feature, American Phytopathological Society,
St. Paul, MN. doi:10.1094/APSnetFeature-­1999-­0199.
Hill, G. K. 1990. The influence of annual weather patterns on epidemics
of Uncinula necator in Rheinhessen. Wein-­Wissenschaft 45:43-­46.
Jarvis, W. R., Gubler, W. D., and Grove, G. G. 2002. Epidemiology of
powdery mildews in agricultural pathosystems. Pages 169-­199 in:
The Powdery Mildews: A Comprehensive Treatise. R. R. Bélanger,
W. R. Bushnell, A. J. Dik, and T. L. W. Carver, eds. American Phy-
topathological Society, St. Paul, MN.
Kast, W. K., and Bleyer, K. 2010. The expert system OiDiag-­2.2 -­a
useful tool for the precise scheduling of sprays against the pow-
dery mildew of vine (Erysiphe necator Schwein.). Pages 151-­153 in:
Proc. 6th Int. Workshop on Grapevine Downy and Powdery Mil- Fig. 167. Initial symptom of ripe rot, consisting of a circular red-­
dew. INRA-­INITA, Bordeaux, France. brown spot of decay on the skin. (Cour­tesy T. B. Sutton)

83
Causal Organisms nose on grapes is the accepted name for the disease caused by
Ripe rot is caused by homothallic and heterothallic strains of Elsinoë ampelina, an unrelated organism. Unfortunately, this
Colletotrichum gloeosporioides (Penz.) Penz. & Sacc. (teleo- potentially ambiguous situation has resulted in Colletotrichum
morph Glomerella cingulata (Stonem.) Spauld. & Schrenk) and spp. being ascribed as the causal agents of “anthracnose” on
C. acutatum J. H. Simmonds (teleomorph G. acutata Guerber grapes in some literature and nontechnical publications, par-
& Correll). Colletotrichum spp. produce subepidermal acer- ticularly from Asia. Accounts that utilize this common name
vuli which are arranged in circles on the surface of the fruit. A should be read carefully to determine the true etiology of the
mass of sticky, salmon-­colored conidia is discharged from the disease.
acervuli. Conidia of C. gloeosporioides are hyaline and gut-
tulate, 12–21 × 3.5–6 µm, rounded at the ends, and are often Disease Cycle and Epidemiology
slightly curved. Conidia of C. acutatum are hyaline, straight, Colletotrichum spp. and G. cingulata survive from one sea-
mostly fusiform, 8–16 × 2.5–4 µm, and frequently pointed at son to another on the vine as dormant mycelium in mummified
one or both ends. Perithecia are subspherical and more or less fruit and infected pedicels, and in dead bark and other tissues
grouped. Asci are subclavate and measure 42–60 × 10–12 µm; on the cordons that have been colonized. Ascospores, dispersed
ascospores measure 12–24 × 4–6 µm. from these structures by wind during rainy periods in the
Diseases caused by Colletotrichum spp. on many other crops spring, and conidia spread short distances by splashing rain,
are given the common name “anthracnose,” whereas anthrac- serve as primary inoculum. Production of conidia from mum-
mies and pedicels is greatest in early spring and decreases dur-
ing the summer months; few or no primary spores are produced
by mid-­to late summer. Sporulation on ripe fruit near harvest
provides an abundant source of secondary inoculum immedi-
ately adjacent to healthy berries, and frequent rains during this
period can result in severe crop loss in the absence of adequate
control measures.
Fruit are susceptible to infection by Colletotrichum spp. and
G. cingulata from bloom until harvest, but do not show symp-
toms until they begin to ripen. Disease development is favored
by warm (25–30°C), wet weather. Spores germinate in a film
of water and can penetrate the cuticle within a matter of hours
under favorable conditions, but the fungus remains quiescent
until the fruit mature.

Management
Cultural practices, such as pruning out dead spurs, remov-
ing overwintered mummies, and removing weak or dead cor-
dons, are important to help reduce inoculum of both ripe rot
and bitter rot (Greeneria uvicola) in the vineyard. Converting
Fig. 168. Characteristic salmon-­c olored spore masses of a to a cane pruning system rather than spur pruning has reduced
Colletotrichum sp. on muscadine berries with ripe rot. (Cour­tesy disease development in some cases, presumably by removing
T. B. Sutton) certain perennial sources of inoculum. It is necessary to apply
protectant fungicides on a 2-­week schedule from bloom until
harvest where the disease is a problem, except during peri-
ods of drought. Captan, EBDC fungicides, and the strobilurin
members of the QoI group have good activity against ripe rot,
whereas the DMI fungicides are not effective.
Cultivars within various grapevine species and interspe-
cific hybrids differ in their susceptibility to ripe rot. Within
V. vinif­era, Barbera, Chardonnay, Merlot, and Syrah are mod-
erately resistant; Cabernet Franc, Tempranillo, and Sauvignon
Blanc are slightly susceptible to moderately susceptible; and
Cabernet Sauvignon and Petit Verdot are highly susceptible.
Dark-­skinned muscadine cultivars are resistant, whereas most
bronze cultivars are susceptible. Among French-­A merican
hybrids, Traminette is moderately resistant; Chambourcin
and Seyval Blanc are slightly susceptible; and Vidal Blanc is
highly susceptible. The V.  aestavalis cv. Cynthiana (Norton)
is resistant.

Selected References
Clayton, C. N. 1975. Diseases of muscadine and bunch grapes in North
Carolina and their control. N.C. Agric. Exp. Stn. Bull. 451.
Daykin, M.  E., and Milholland, R.  D. 1984. Ripe rot of muscadine
grape caused by Colletotrichum gloeosporioides and its control.
Phytopathology 74:710-­714.
Daykin, M.  E., and Milholland, R.  D. 1984. Histopathology of ripe
Fig. 169. Advanced symptoms and signs of ripe rot caused by Colletotrichum gloeosporioides on muscadine grape.
rot on a V.  vinifera cluster, including decay and Phytopathology 74:1339-­1341.
shriveling of affected berries, some with pinkish Kummuang, N., Smith, B. J., Diehl, S. V., and Graves, C. H. Jr. 1996.
spore masses of a Colletotrichum sp. (Cour­tesy Muscadine grape berry rot diseases in Mississippi: Disease identifi-
W. F. Wilcox) cation and incidence. Plant Dis. 80:238-­243.

84
Quimio, T. H., and Quimio, A. J. 1975. Notes of Philippine grape and not seem to invade the cluster rachis. In severe cases, the ber-
guava anthracnose. Plant Dis. Rep. 59:221-­224. ries are destroyed, leaving the rachis bearing only a few indi-
vidual berries or none at all. High levels of infection during
(Prepared by T. B. Sutton) bloom can result in 80–90% crop loss.
Lesions of angular leaf scorch are similarly constricted by
the major veins and laminar margin, giving rise to the disease
name. Lesions usually retain a yellow margin (Fig. 172), al-
Rotbrenner and Angular Leaf Scorch though it may be red on some red-­fruited cultivars of V. vinifera
or absent on some native American cultivars such as Concord.
Symptoms of rotbrenner were well known in Europe during Most of the leaf blade may be killed in the case of severe infec-
the nineteenth century. Before Müller-­Thurgau first described tion (Fig. 173). Infections of the inflorescences are rare.
the causal agent in 1903, the disease was thought to be caused
by unfavorable weather conditions, water deficiency, or exces- Causal Organisms
sive soil moisture. Although rotbrenner has been identified in Pseudopezicula tracheiphila (Müll.-­Thurg.) Korf & Zhuang
most European countries, it is most problematic in cool viticul- (syn. Pseudopeziza tracheiphila Müll.-­Thurg, anamorph Phialo­
tural regions (e.g., Austria, the Champagne and Alsace regions phora tracheiphila (Sacc. & Sacc.) Korf [syn. Botrytis tracheiph-
of France, Germany, Hungary, Luxembourg, and Switzerland) ila Sacco & Sacc.]), the cause of rotbrenner, is a discomycete
and is generally confined to certain locally restricted areas. In with minute (up to 0.6 mm diameter), sessile, gelatinous, whit-
some of these areas the disease results in severe losses annu- ish to faintly colored, gregarious apothecia. The fungus appears
ally, whereas in others it occurs only sporadically. The disease to be composed of two mating types, which exhibit a bipolar
also has been observed to develop during several succeeding heterothallic mating system. The apothecia rise from the leaf
years in some locations, then not to reappear for several more. tissue and are often associated with the veins. The inopercu-
Rotbrenner affects the cultivated European grape, V.  vinif- late, broadly clavate, eight-­spored asci (115–145 × 18–28 µm)
era, as well as other Vitis species and interspecific hybrids. It show a blue pore in iodine only after pretreatment in aqueous
may also occur on Virginia creeper (Parthenocissus quinque-
folia) and Boston ivy (P. tricuspidata). In the 1980s, a simi-
lar disease was noted to occur sporadically on the foliage of
grapevines in the state of New York, particularly those of in-
terspecific hybrid cultivars. Subsequent research showed that
this disease was caused by a unique species within the same
genus as the fungus that causes rotbrenner, and the disease was
named angular leaf scorch.

Symptoms
Rotbrenner leaf lesions initially are yellow on white-­fruited
cultivars and bright red to reddish brown on red-­and black-­
fruited cultivars. With time, a reddish-­brown necrosis develops
in the center of the lesion, leaving only a thin margin of yellow
or red tissue between the necrotic and green areas of the leaf
(Fig. 170). The lesions are typically confined by the major veins
and the leaf margin, and may be several centimeters wide.
Atypical symptoms, such as freckled spots or discoloration
scattered over the leaf surface, often occur late in the season. Fig. 171. Dried inflorescence affected with rotbrenner. (Cour­tesy
Early infections may occur on the first to the sixth leaf of young A. Bolay)
shoots, resulting in minor losses. Later infections may attack
leaves up to the 10th or 12th position on the shoot and can result
in severe defoliation.
The fungus also may attack inflorescences before or dur-
ing bloom, causing them to rot and dry out (Fig. 171). Unlike
Botrytis blight, only the pedicels are attacked; the fungus does

Fig. 172. Lesion of angular leaf scorch on the

Fig. 170. Symptoms of rotbrenner on leaves of a white V. vinifera white-­fruited interspecific cultivar Aurore. (Cour­
cultivar. (Cour­tesy W. Gärtel) tesy R. C. Pearson)

85
potassium hydroxide. The ellipsoid, hyaline ascospores (19–26 species is distinguished from P. tracheiphila by its smaller apo-
× 9–14 µm) are flattened on one side and produce a sporelike thecia (0.1–0.3 mm in diameter) and its broadly clavate asci
vesicle upon germination, which gives rise to one or more germ (80–100 × 20–22 µm) that contain only four binucleate asco-
tubes or conidiophores. Paraphyses are branched and curved spores, in contrast to the eight-­spored European species. Apo-
or slightly deformed at the apex, filiform, septate, and hyaline. thecia form readily on dead, infected leaf tissue after several
The anamorph may form on malt agar, producing hyaline, days incubation in a moist chamber.
septate, short conidiophores that are coarser than the vegeta-
tive hyphae. Conidiogenous cells are monophialidic and lageni- Disease Cycle and Epidemiology
form, with well-­defined but thin-­walled collarettes. Conidia The incidence and severity of rotbrenner are influenced
(2–3 × 1.5–2 µm) are ellipsoid, hyaline, and unicellular. The strongly by the abundance of apothecia on fallen leaves and
hyphae grow in a characteristic sin-­wave pattern (Fig. 174) the quantity of released ascospores. Apothecia are formed pri-
that, when observed in the vessel elements of diseased tissue, is marily on overwintered leaves in the spring, although they may
often considered diagnostic. develop on current-­season infections in late summer or fall if
Angular leaf scorch is caused by the species P. tetraspora provided sufficient wetness of the leaf substrate. Apothecial pri-
Korf, Pearson, & Zhuang (anamorph Phialophora-­type). This mordia mature as soon as temperatures rise at the end of the
winter and ascospores may be released even before bud burst
under wet and warm conditions, although infection appears to
occur most commonly after shoots have elongated to the six-­leaf
stage. Heavy rainfall and prolonged wetting periods favor infec-
tion and can lead to severe disease, but little is known regarding
the precise temperature and moisture conditions necessary for
ascospore maturation, release, or germination and infection.
After an incubation period of 2–4 weeks, the fungus may
invade the vascular elements of infected leaves, causing symp-
tom development. If unable to invade the vessel elements, the
fungus remains quiescent and can be isolated from green leaves
showing no symptoms. Conditions required for the pathogen to
invade the vascular system are not well understood; however,
soil conditions and a water supply that place the vine under
temporary stress appear to be important factors.
The epidemiology of angular leaf scorch is poorly under-
stood, but is assumed to be similar to that of rotbrenner. The
first infections can occur soon after bud break given suitable
temperatures and rain, with a 3-­to 4-­week incubation period
before the appearance of symptoms. Although secondary
spread is uncommon, apothecia may form on the dead portions
of diseased leaves still attached to the vine following several
Fig. 173. Severely diseased leaf of the red-­ consecutive days of persistent rain, leading to additional infec-
fruited interspecific cultivar Rougeon infected tions when weather conditions favor their development.
with Pseudopezicula tetraspora. (Cour­tesy R. C.
Pearson) Management
Although rotbrenner infections can occur when the first leaf
reaches a width of approximately 5 cm, the most critical pe-
riod for disease development is from the six-­leaf stage through
the end of the bloom. In locations where severe symptoms
occur annually, fungicide control programs should be imple-
mented routinely. In vineyards in which the disease occurs spo-
radically, fungicide treatments should be implemented in wet
springs that favor the maturation of apothecia. Sprays should
be applied at 7-­to 10-­day intervals between the six-­and 12-­
leaf stage, depending on rainfall forecasts, the rate of plant de-
velopment, and the material used. Later in the season, sprays
targeting rotbrenner can be integrated with those sprays against
downy mildew. Dithiocarbamates are the traditional materials
used for control of this disease, although some newer fungi-
cides also are effective, including some triazole and strobilurin
products. Monitoring ascospore release by means of spore traps
may provide additional information to aid in the forecasting of
disease pressure.
Angular leaf scorch is seldom serious enough to warrant tar-
geted control programs. It appears to be controlled primarily by
fungicides targeted at a complex of other diseases active during
the early part of the growing season. Mancozeb is known to be
effective; it is assumed that other fungicides effective against
rotbrenner are likely to be effective against angular leaf scorch
as well, although this has not been proved.
Fig. 174. Hyphae (arrows) of Pseudo­ Selected References
pezicula tracheiphila growing in a sine-­
wave pattern inside a vessel of an infected Korf, R. P., Pearson, R. C., Zhuang, W., and Dubos, B. 1986. Pseudo-
leaf. (Cour­tesy H. Schüepp) pezicula (Helotiales, Peziculoideae), a new discomycete genus for

86
 pathogens causing an angular leaf scorch disease of grapes (“Rot- tial proportion of the cluster. Clusters with significant levels of
brenner”). Mycotaxon 26:457-­471. sour rot can seriously reduce the quality of wines made from
Levadoux, M. L. 1944. Le brenner (Pseudopeziza tracheiphila Müll.-­ them. Thus, entire clusters supporting diseased berries may be
Thurg.). Bull. Off. Int. Vin. 17:43-­54. excluded from harvest or discarded between harvest and crush
Müller-­Thurgau, H. 1903. Der rote Brenner des Weinstockes. Cen- even though many healthy berries remain, resulting in a degree
tralbl. Bakteriol. Parasitenkd. Infektionskr. Abt. 2 10:1-­38. of economic loss that exceeds the losses due only to rotten fruit.
Pearson, R. C., Smith, F. D., and Dubos, B. 1988. Angular leaf scorch,
a new disease of grapevines in North America caused by Pseudope-
Economic losses also accrue when rapidly spreading disease
zicula tetraspora. Plant Dis. 72:796-­800. forces growers to harvest the remaining crop prematurely in
Pearson, R.  C., Siegfried, W., Bodmer, M., and Schüepp, H. 1991. order to avoid further damage, resulting in a loss of crop quality
Ascospore discharge and survival in Pseudopezicula tracheiphila, beyond that directly attributable to decay.
causal agent of Rotbrenner of grape. J. Phytopathol. 132:177-­185.
Reiss, K., and Zinkernagel, V. 1994. Heterothallie bei Pseudopezicula Symptoms
tracheiphila (Müll.-­ Thurg.) Korf & Zhuang (syn. Pseudopeziza Sour rot develops during the late stages of ripening when the
tracheiphila Müll.-­ Thurg.). Z. Pflanzenkrankh. Pflanzenschutz berries have high sugar content. In humid climates, infected
101:212-­214. berries of white varieties turn light chestnut brown (Fig. 175),
Reiss, K., and Zinkernagel, V. 1997. Epidemiologische Untersuchun- whereas those of red varieties become brick or purplish red
gen zur Ascosporenfreisetzung von Pseudopezicula tracheiphila (Fig. 176). The color change usually begins at the point of pedi-
(Müll.-­Thurg.) Korf & Zhuang, dem Erreger des Roten Brenners cel attachment in berries without obvious injuries. The flesh is
am Wein. Z. Pflanzenkrankh. Pflanzenschutz 104:113-­112. rapidly and completely degraded, becoming soft and watery,
Reiss, K., Gutmann, M., Bartscherer, H.-­Ch., and Zinkernagel, V.
typically with strong acetic acid (and sometimes ethyl acetate)
1997. Pseudopezicula tracheiphila on Vitis vinifera: Microscopical
studies of the infection mechanism. Z. Pflanzenkrankh. Pflanzen-
odors. The skin becomes thin and fragile and breaks down, re-
schutz 104:483-­491. leasing juice that attracts drosophilids (fruit/vinegar flies) and
Schüepp, H. 1976. Verstärktes Auftreten des Rotbrenners der Rebe. other insects that can vector the causal organisms to uninfected
Schweiz. Z. Obst Weinbau 112:379-­381. berries. Signs of Botrytis, Aspergillus, Penicillium, and other
Siegfried, W., and Schüepp, H. 1983. Der Rotbrenner der Rebe, eine filamentous fungi may be common on other parts of the same
unberechenbare Krankheit. Schweiz. Z. Obst Weinbau 119:235-­239.

(Prepared by H.-­H. Kassemeyer and W. F. Wilcox)

Sour Rot
Sour rot (pourriture acide, pudrición ácida), also known in
parts of the western United States as summer rot, is a poorly
defined condition characterized by the rapid decomposition of
ripening grape berries. The term sometimes is used to define
a general decay syndrome that may involve various bacteria,
yeasts, and/or filamentous fungi other than species known to
be primary decay pathogens (e.g., Botrytis cinerea, Greeneria
uvicola, etc.). However, berries affected with “true” sour rot
characteristically exude the vinegarlike odor of acetic acid,
from which the condition gets its name, and often that of ethyl
acetate (nail polish remover). Berries with sour rot can contain
acetic acid concentrations of 0.3–12.4 grams per liter, resulting
from the oxidation of ethanol, which can be produced by as-
Fig. 175. Symptoms of sour rot on cv. Riesling. (Photograph by
sociated yeasts; they also typically contain high concentrations W.  McFadden-­Smith, Ontario Ministry of Agriculture and Food;
of gluconic acid, a result of the metabolism of glucose by ace- Queen’s Printer of Ontario, © 2014. Reproduced with permission.)
tic acid bacteria, and dihydroxyacetone, produced when acetic
acid bacteria oxidize glycerol formed by yeasts. Dihydroxy-
acetone persists through fermentation into the wine, affect-
ing its sensory quality and sulfur dioxide binding properties.
Additionally, infected berries have elevated concentrations of
glycerol and tartaric acid relative to healthy berries, and higher
levels of titratable acidity.
Complexes of different but overlapping groups of organisms
appear to be associated with the disease in different climates.
Sour rot typically develops in berries injured by primary patho-
gens, insects, or birds or in berries subjected to abiotic forms
of physical damage such as cracking due to rain or compres-
sion within expanding bunches. Thus, tight-­clustered and thin-­
skinned varieties or clones tend to be particularly susceptible
to sour rot development. Botrytis bunch rot and sour rot are
often conflated, so that sour rot is sometimes thought to be the
final and most destructive stage of bunch rot. However, the two
rots are caused by distinctly different etiological agents and, al-
though they often occur together in regions or seasons with wet
Fig. 176. Purplish-­red discoloration of ‘Pinot Noir’ berries symp-
preharvest conditions, the occurrence of one does not always tomatic of sour rot, with a drosophilid fly on a healthy berry within
imply the occurrence of the other. Crop damage due to sour rot the cluster. (Photograph by W. McFadden-­Smith, Ontario Ministry
can be extensive because infections that begin in a single berry of Agriculture and Food; Queen’s Printer of Ontario, © 2014.
can spread rapidly to adjacent berries and destroy a substan- Reproduced with permission.)

87
clusters or others nearby (Fig. 177). There is no “slip skin” the disease in some locales. Hanseniaspora uvarum (Niehaus)
symptom as found with Botrytis bunch rot. In the final stages Shehata et al. (anamorph Kloeckera apiculata (Reess) Janke)
of decay, the berries frequently become hollow as a result of is the yeast most frequently identified as a causal organism of
insect feeding and consist only of empty shells of dry skin. Nu- sour rot. Cells are apiculate, spheroidal to ovoidal, 1.5–5.0 ×
merous vinegar flies often emerge from infected clusters and 2.5–11.5 µm, and occur singly or in pairs, with reproduction
their larvae are commonly observed on and in infected berries. by bipolar budding. On glucose-­yeast extract-­peptone agar it
Wasps are also attracted to the leaking juice. produces white to creamy, smooth, glossy colonies that are
slightly raised in the middle. On Wallerstein Laboratory nutri-
Causal Organisms ent agar it produces intense green, flat, smooth, opaque colo-
The acetic acid bacteria, Acetobacter spp. and/or Glucono- nies. H. uvarum ferments only glucose and can produce acetic
bacter spp., are always associated with “true” sour rot and can acid and its esters, including ethyl acetate, and grows in the
cause its decay symptoms on inoculated fruit in the absence of presence of cycloheximide.
other organisms. They are obligately aerobic, Gram-­negative, Several Candida species have been cited as capable of
catalase positive, oxidase-­negative, and well adapted to grow causing sour rot. The Candida spp. associated with sour rot
in sugar-­rich environments. They can typically oxidize ethanol have ovoid to elongated cells and undergo multilateral bud-
to acetic acid. ding. Some species produce simple to elaborate pseudohy-
Gluconobacter spp. are ovoid or rod-­shaped cells, 0.5–1.0 × phae. They assimilate glucose, glycerol, and ethanol. C. krusei
2.6–4.2 µm, occurring singly or in pairs, and rarely in chains. (Castellani) Berkhout (teleomorph Issatchenkia orientalis)
They may be motile or nonmotile; if motile, cells have three to produces white to cream butryous colonies. It assimilates glu-
eight polar flagella. Colonies are white, yellow, or even brown to- cose, N-­acetyl-­d -­glucosamine, ethanol, glycerol, dl-­lactate,
ward the middle; circular, raised or convex; and regularly edged. and succinate. Candida zemplinina (Kroemer & Krumbholz)
Growth is optimum at 25–30°C and pH 5–6, although most Meyer & Yarrow (previously C. stellata) is acidogenic, highly
strains can grow at pH as low as 3.5. They are negative for nitrate osmotolerant, and grows well in the presence of ethanol and at
reduction, gelatin liquefaction, indole production, and H2S pro- low temperatures.
duction. They do not oxidize lactate or acetate to CO2 and H2O Pichia membranaefaciens Hansen is a film-­forming yeast
and do not cause a color change when incubated on Dextrose sor- that causes off aroma and flavor in table wine. Its cells are ovoi-
bitol mannitol agar. All strains produce 2-­ketogluconic acid from dal to elongate, (1.8–4.5) × (2.5–17) µm, and occur singly or in
d-­glucose. G. oxydans (previously Acetobacter suboxydans) is pairs, chains or clusters. Colonies are yellowish tan, dull, and
most frequently identified in the literature as the species causing smooth or wrinkled. Asci may be unconjugated or show conju-
sour rot. It is the most common acetic acid bacterium on the sur- gation between independent cells or between a parent cell and a
face of the healthy grapes, likely owing to its superior ability to bud. One to four spheroidal or hemispheroidal ascospores with
metabolize sugars. G. cerinus, G. albidus, and G. frateurii have or without a ledge are produced per ascus in culture. It produces
also been cited as causal agents of sour rot. acetaldehyde, ethyl acetate, and isoamyl acetate.
Acetobacter spp. are ellipsoid to rod-­shaped cells, straight Pichia kluyveri (Bedford) forms white to cream butryous
or slightly curved, 0.6–0.9 × 1.0–4.0 µm, occurring singly, in colonies, undergoes vegetative reproduction by budding, pro-
pairs, or chains. They can be motile or nonmotile; if motile, fla- duces simple pseudohyphae, and produces evanescent asci con-
gella are peritrichous. They form pale colonies and most strains taining up to four hat-­shaped ascospores.
produce no pigments. Their optimal temperature for growth is Metschnikowia pulcherrima Miller and van Uden produces
30°C, with an optimal pH of 4.0–6.0. They are negative for ni- a red diffusing pigment, pulcherin. Its colonies are smooth and
trate reduction, gelatin liquefaction, indole production, and H2S cream colored with an entire margin. It produces pseudohy-
production. The Acetobacter species reported to cause sour rot phae and buds multilaterally. One to two needlelike ascospores
are A. aceti and A. pasteurianus. per ascus are produced in culture, sometimes only after mixing
Although many yeast species have been isolated from ber- sexually compatible strains.
ries with sour rot, only a few are able to cause the fruit disin- Saccharomycopsis crataegensis Kurtzman and Wickerham
tegration and characteristic ethyl acetate odor associated with (syn. S. vini, Endomycopsis vini) does not cause sour rot on
its own; however, when co-­inoculated with M. pulcherrima, it
can cause sour rot symptoms. In nutrient broth, cells are ovoid;
elongate to cylindrical; 2.4–3.2 × 4.0–8.0 µm; and occur singly,
in pairs, in short chains, or as multilateral buddings. Aerobic
growth on agar is white to cream, butyrous, rough, glisten-
ing, and flat with filamentous margin. After 7 days at 25°C,
growth on corn meal agar under a coverglass shows abundant
true hyphae with conidia. Pseudohyphae are formed and the
species appears heterothallic. Chains of two to four ellipsoidal
asci, containing two ascospores, are borne directly on hyphae
or supported by short stalks.

Disease Cycle and Epidemiology

Inoculations with bacteria or yeasts isolated from diseased
berries have replicated the symptoms of berry decomposition
accompanied by odor of acetic acid or ethyl acetate, respec-
tively, although some investigators report that acetic acid pro-
duction requires co-­ inoculation of ethanol-­producing yeasts
Fig. 177. Riesling clusters with (i) sour rot, characterized by with the acetic acid bacteria. These microorganisms occur on
chestnut-­brown color and lack of sporulation on berries in the the surface of healthy grape berries, although in significantly
mid-­and lower portion of the rightmost cluster; contrasting with
lower numbers than on diseased ones. They are not aggressive
(ii) Botrytis bunch rot, characterized by the fuzzy, gray sporulation
on infected berries above those with sour rot and in the adjacent pathogens and appear to require mechanical injury or predis-
cluster. (Photograph by W.  McFadden-­ Smith, Ontario Ministry posing infections by other microorganisms to gain entry into
of Agriculture and Food; Queen’s Printer of Ontario, © 2014. Re­ the berries. It is likely that the additional organisms involved
produced with permission.) vary among different regions and habitats.

88
 The volatile compounds in the juice that leaks from injured maturity. Heavy rains provide numerous infection courts by
berries, especially those with sour rot, attracts vinegar flies causing berries to swell rapidly and split, and by facilitating
(Drosophila spp.). Adult flies can vector yeasts and bacteria to pathogen development and dispersal to infection sites. Simi-
uninfected clusters and into neighboring, subsequently matur- larly, sour rot is exacerbated in arid regions by use of over-­the-­
ing cultivars. Adults typically lay eggs near the juncture of the canopy sprinklers as berries mature. The disease frequently
berry and the pedicel. It is hypothesized that when berries swell develops from the interior of the cluster, where berries become
and pull away from the pedicel in the final stages of ripening, crushed as they and their neighbors swell, then progresses out-
as is particularly likely in tightly compressed clusters, hatching ward. Wounding from hail, birds, insects, and fungal diseases
larvae can enter the berries and carry yeasts and bacteria with may also allow entry of sour rot causal organisms. For example,
them to the infection court. sour rot is sometimes found as a secondary infection following
In wetter climates, severe sour rot development is usually as- botrytis bunch rot, and diffuse powdery mildew infections also
sociated with high daytime temperatures (optimum being 25– can cause minute wounds in the skin that allow the prolifera-
28°C), high humidity, and heavy precipitation during the final tion of contaminating yeasts and bacteria, some of which can
2–3 weeks before harvest. In Ontario, Canada, sour rot does cause sour rot under favorable conditions. In the vineyard, there
not occur in the field until berries reach a minimum of 15°Brix, is likely a succession of organisms causing sour rot. For ex-
nor do inoculated berries become diseased before this stage of ample, apiculate yeasts (Hanseniaspora, anamorph Kloeckera)

Fig. 178. Inverted stroma of Aspergillus niger, C, after drying in soil or, E, freshly recovered from within a decaying
grape berry. A, B, D, and F, cross-­sectional views of conidiophores and conidia produced from such a stroma. (Cour­
tesy C. Pisani)

89
initially colonize many fruit surfaces and are dominant at early Guerzoni, M. E., and Marchetti, R. 1987. Analysis of yeast flora as-
stages of ripeness. As the fruit deteriorates, yeasts capable of sociated with grape sour rot and of the chemical disease markers.
utilizing a broader spectrum of carbon sources become appar- Appl. Environ. Microbiol. 53:571-­576.
ent on the surface. Pichia spp. and Candida spp. are in this Marchetti, R., Guerzoni, M. E., and Gentile, M. 1984. Recherche sur
latter category. l’étiologie d’une nouvelle maladie de la grappe: la pourriture acide.
Vitis 23:55-­65.
In Mediterranean climates, Aspergillus niger Tiegh. and As-
Nisiotou, A. A., and Nychas, G.-­J. E. 2007. Yeast populations residing
pergillus carbonarius (Bainier) Thom are usually the first fungi on healthy or Botrytis-­infected grapes from a vineyard in Attica,
to colonize berries that have been injured after veraison, often Greece. Appl. Environ. Microbiol. 73:2765-­2768
by insects and birds. Aspergillus spp. colonize berry pulp rap- Pisani, C. 2011. Identification of a novel fungal fruiting structure
idly, causing leakage onto berries below the rot. Although the formed by Aspergillus niger and Aspergillus carbonarius in sour
Aspergillus fungi do not cause true sour rot, they are soon rot infected grape berries under artificial and field conditions. M.S.
followed by other fungi and the acetic acid bacteria that pro- thesis, University of California, Davis.
duce the vinegar smell. Both species of Aspergillus have been Sholberg, P. L., Lowery, T., Bowen, P., Haag, P., and Walker, M. 2008.
shown to produce a previously undescribed fruiting body in Effect of early leaf stripping on bunch rot, powdery mildew and
rotted berries, characterized as a polymorphic, inverted stroma sour rot of wine grapes. Pages 199-­211 in: Crop Protection Research
from which conidia of the pathogen are produced (Fig. 178). Advances. E. N. Burton and P. V. Williams, eds. Nova Science Pub-
These stromata fall to the ground in late summer and become lishers, New York.
leathery. It is hypothesized that these serve as overwintering Zoecklein, B. W., Wolf, T. K., Duncan, N. W., Judge, J. M., and Cook,
structures that survive in the soil and provide spores for the M. K. 1992. Effects of fruit zone leaf removal on yield, fruit com-
position, and fruit rot incidence of Chardonnay and White Riesling
following year’s infections.
(Vitis vinifera L.) grapes. Am. J. Enol. Vitic. 43:139-­148.
Non-­Botrytis slip skin is a related postharvest disease of Zoecklein, B. W., Williams, J. M., and Duncan, S. E. 2000. Effect of
table grapes and occurs mostly on thin-­skinned varieties such sour rot on the composition of White Riesling (Vitis vinifera L.)
as Red Globe. The disease occurs only on clusters from which grapes. Small Fruits Rev. 1:63-­77.
other berries with sour rot have been trimmed before pack-
ing. It is caused in storage (0°C, 94% relative humidity) by an (Prepared by W. McFadden-­Smith and W. D. Gubler)
SO2-­resistant Hanseniospora uvarum biotype able to ferment
the sugar residues on healthy fruit that resulted from leakage
by neighboring fruit with sour rot, eventually resulting in a
berry decay similar to Botrytis box rot. This storage rot can Verticillium Wilt
be avoided by not harvesting clusters with sour rot symptoms.
Verticillium wilt is a serious vascular disease of hundreds of
Management woody and herbaceous plant species throughout the temperate
The primary strategy for managing sour rot is to minimize areas of world, including some common dicot weeds and fruit
various forms of berry injury to the greatest extent practical. and vegetable crops such as strawberries, raspberries, potatoes,
Standard programs for managing fungal diseases, especially and tomatoes. It occurs sporadically on grapes in several coun-
powdery mildew and botrytis, should be implemented and ad- tries in North and South America, Europe, Asia, and Ocea-
justed as necessary for the particular location and year. Insects nia. Because affected vines exhibit symptoms similar to those
that wound berries, such as wasps and grape berry moth, should caused by other stresses, it is likely that the disease is present
be controlled; the use of bird netting, where appropriate, should but has been misdiagnosed or unrecognized in some additional
also reduce injuries subject to sour rot initiation. Canopy man- locations. Although first described on grapes in the 1950s in
agement and removal of leaves to improve cluster exposure and Germany, the disease is most destructive in warmer, irrigated
promote drying have been shown to reduce sour rot develop- regions. During the rapid expansion of the grape industry in
ment, sometimes dramatically. Berry damage caused by cluster California in the 1970s, the disease developed in many new
compaction may be reduced by loosening clusters through vi- vineyards planted at sites where crop plants susceptible to the
ticultural practices and/or the use of chemical growth regula- causal pathogen had been grown previously. Following another
tors, as appropriate for the cultivar and region. Broad-­spectrum major round of new planting in California in the 1990s, there
fungicides applied during the postveraison period sometimes was another resurgence of the disease. Typically, Verticillium
provide modest control of the secondary decay fungi often as- wilt only affects grapevines less than 6–7 years old.
sociated with sour rot, but have little effect on sour rot per se
beyond their control of botrytis. Over-­the-­canopy irrigation Symptoms
should be limited when sour rot or predisposing injuries are Symptom expression is the result of vascular occlusion and
present. root death. Infected vines do not show symptoms in the early
part of the growing season, but as transpirational demand in-
Selected References creases as a result of rising temperatures (and declining soil
moisture in some cases), a few shoots start to die and the vas-
Barata, A., Santos, S.  C., Malfaeto-­Ferreira, M., and Loureiro, V. cular elements in the wood of these shoots become discolored
2012. New insights into the ecological interaction between grape (Fig. 179). New shoot growth from the base of such vines is
berry microorganisms and Drosophila flies during the development often vigorous.
of sour rot. Microb. Ecol. 64:416-­430. By early summer, the leaves on declining shoots wilt and
Bisiach, M., Minervini, G., and Zerbetto, F. 1986. Possible integrated show marginal burning. By midsummer, many shoots that had
control of grapevine sour rot. Vitis 25:118-­128. developed normally during the early season collapse com-
Duncan, R. A., Stapleton, J. J., and Leavitt, G. M. 1995. Population dy- pletely. The leaves on these shoots become desiccated, and
namics of epiphytic mycoflora and occurrence of bunch rots of wine
some may drop from the vine (Fig. 180). Fruit clusters at the
grapes as influenced by leaf removal. Plant Pathol. 44:956-­965.
Gadoury, D.  M., Seem, R.  C., Wilcox, W.  F., Henick-­K ling, T., base of these affected shoots dry up, and the individual berries
Conterno, L., Day, A., and Ficke, A. 2007. Effects of diffuse coloni- remain attached to the pedicels as shriveled mummies, a re-
zation of grape berries by Uncinula necator on bunch rots, berry mi- sult of their rapid desiccation before formation of an abscission
croflora, and juice and wine quality. Phytopathology 97:1356-­1364. zone. Symptoms typically are confined to one side of the vine,
Gravot, E., Blancard, D., Fermaud, M., Lonvaud, A., Joyeux, A., 2001. with leaves and shoots on a single cordon showing wilting. Oc-
La pourriture acide. I. Étiologie: Recherché de causes de cette pour- casionally, all shoots on a vine may collapse, whereas only a
riture dans le vignoble bordelaise. Phytoma 543:36-­39. few shoots may show symptoms on others.

90
 Fig. 180. Wilted leaves and dying shoots on one side of a cv.
Semillon vine infected with Verticillium dahliae. (Cour­tesy A. C.
Goheen)

apparently spontaneous recovery is one reason it took many

years of investigation before it was demonstrated that Verticil-
lium infects grapes.
Full production is delayed in vineyards that show early
wilting, but yields do not seem to be adversely affected once
Fig. 179. Discolored xylem in the trunk of a vines reach an age when they become asymptomatic. Unless
young cv. Chenin Blanc vine infected with Verti- young vines are killed by the initial attack, after 8–10 years
cillium dahliae. (Cour­tesy R. C. Pearson) it is difficult to find the areas in the vineyard where disease
occurred.
Verticillium wilt of grapes is uncommon in the southern San
Causal Organism Joaquin Valley of the California, even though it appears to be
Verticillium dahliae Kleb., the causal fungus, grows rap- caused by the mild (SS-­4) strain of the fungus that affects cot-
idly on potato-­dextrose agar at 24°C. Mycelium is hyaline to ton in that area. For unknown reasons, it is more common in the
whitish at first but later turns black with the formation of mi- northern San Joaquin Valley and in the Salinas Valley, where
crosclerotia. Microsclerotia arise from individual hyphae by previous hosts, such as strawberries, apricots, and tomatoes,
repeated budding. They are dark brown to black and torulose have favored the increase of the mildly virulent strain of the
or botryoidal. They consist of swollen, almost globular cells fungus.
that vary in shape and size (generally 15–50 µm in diameter,
and 100 µm maximum). Chlamydospores are absent, and dark-­ Management
brown resting mycelium is formed only in association with Sites in the few locations where the fungus has been known
microsclerotia. to kill grapevines, or where the immediate cropping history
Conidiophores are erect, hyaline, and verticillately branched, suggests high levels of soilborne inoculum, should be avoided.
with three to four phialides arising at each node. Phialides More specific control measures for Verticillium wilt usually are
(16–35 × 1–2.5 µm) are secondarily branched on occasion. unnecessary, although fumigation may be warranted if micro-
Conidia (2.5–8 × 1.4–3.2 µm) arise singly at phialide apices sclerotia populations are very high (e.g., as a result of the previ-
and are ellipsoidal to subcylindrical and single-­celled, rarely ous cropping history).
uniseptate.
V. dahliae is distinguished from the closely related species Selected References
V. albo-­atrum Reinke & Berth. primarily by the presence of its
true microsclerotia and ability to grow at 30°C. In late spring, Braun, A. J. 1953. Ills of the American bunch grapes. Pages 754-­760
it is difficult to isolate the fungus from shoots that are start- in: Plant Diseases: The Yearbook of Agriculture, 1953. U.S. Depart-
ing to show symptoms, but isolation from leaves, petioles, and ment of Agriculture, Washington, DC.
discolored wood in the canes becomes easier as the season Canter-­Visscher, T. W. 1970. Verticillium wilt of grapevine, a new re-
progresses. cord in New Zealand. N. Z. J. Agric. Res. 13:359-­361.
Gubler, W. D., Baumgartner, K., Browne, G. T., Eskalen, A., Latham,
Disease Cycle and Epidemiology S.  R., Petit, E., and Bayramian, L.  A. 2004. Root diseases of
Infection apparently takes place through the roots of young grapevines in California and their control. Austral. Plant Pathol.
vines. This leads to vascular plugging by gums and tyloses that 33:157-­165.
are produced by the plant in response to occlusion of the ves- Hawksworth, D. L., and Talboys, P. W. 1970. Verticillium dahliae. De-
scriptions of Pathogenic Fungi and Bacteria, no. 256. C.A.B. Inter-
sels by spores and mycelium of the fungus. Disease foci usually
national Mycological Institute, Kew, England.
occur at locations where susceptible crops or weeds grew previ- Mace, E. M., Bell, A. A., and Beckman, C. H. 1981. Fungal Wilt Dis-
ously, causing inoculum to build up in the soil. The distribution eases of Plants. Academic Press, New York.
of affected vines at such sites is erratic. Schnathorst, W. C., and Goheen, A. C. 1977. A wilt disease of grape-
Vines that are planted in infested soil usually do not show vines (Vitis vinifera) in California caused by Verticillium dahliae.
disease symptoms during the first year. Some vines show Plant Dis. Rep. 61:909-­913.
symptoms during the second year, and new infections continue Thate, R. 1961. Die Apoplexie der Rebe: Eine Verticilliose. Mitt. Biol.
to appear for several subsequent seasons. By the fifth or sixth Bundesanst. Land Forstwirtsch. Berlin-­Dahlem 104:100-­103.
season, symptomatic vines that have not died typically recover,
and the disease is no longer noticeable in the vineyards. This (Prepared by A. Eskalen)

91
 White Rot (Fig. 183). A result of the infection and colonization is the rais-
ing of the cuticle from the epidermal layer, thus conferring a
whitish appearance to the berries. At maturity, pycnidia turn
White rot was first reported in Italy and the pathogen was grayish white, hence the name white rot. Warm temperatures
described by Spegazzini in 1878. The disease can be found in and persistently high relative humidity promote internal growth
most of the world’s viticultural regions that have warm, humid of mycelia from infected berries into the pedicel and then the
summers. The white rot fungus can infect all green tissues of rachis, thereby girdling the cluster and causing it to desiccate
the grapevine, although clusters are the most susceptible. Unin- and die (Fig. 184).
jured berries are resistant to infection, whereas injured berries, Directly infected pedicels show a small, pale-­brown, elon-
pedicels, or rachises are susceptible. Severe epidemics and the gated depression. Under high relative humidity, the fungus ex-
greatest damage to clusters occur in areas particularly prone to pands throughout the entire pedicel and into uninjured berries.
hailstorms, where losses may reach 20–80% of the yield. For Pycnidia cover the wrinkled, withering surface of the berry
this reason, white rot is sometimes known as “hail disease,” within a few days, whereas under dry conditions they develop
although hailstorms are not essential for its development. Vitis inside the berry on the surface of the seeds.
species differ greatly in their susceptibility to white rot. The Fungal infection of nonlignified shoots can cause cankers.
Asiatic species are resistant to highly resistant (V. amurensis, This symptom rarely occurs on V. vinifera cultivars, but it is fre-
V.  davidii, and V.  qinlingensis belong to the latter category), quently observed in nurseries producing American or interspe-
whereas V.  vinifera and American species are susceptible to cific hybrid rootstock selections, where shoots develop freely on
highly susceptible. For example, the rootstock Kober 5 BB is the soil surface. Infections on green shoots are often localized
considered highly susceptible, as are the V.  vinifera cultivars around the nodes. Colonized tissue becomes necrotic, appearing
Chardonnay, Chasselas, and Rhine Riesling. brown, elongated, and depressed. The bark covering necrotic
tissue splits, with the fibrous material conferring a characteristic
Symptoms
frayed appearance to the canker. Cankers on canes in a nursery
Symptoms of white rot vary among different plant organs. cause a significant loss of grafting wood and reduce the percent-
Rachis infections appear initially as brown pin-­point spots, age of successful grafts. The fungus rarely infects leaves.
which later become elongated and depressed. Persistently high
relative humidity favors girdling of the rachis, resulting in a
sudden desiccation and death of the distal portion of the cluster
(Fig. 181). Immature infected berries become pale green and
shrivelled, later turning pinkish and then brown (Fig. 182).
Early desiccation of infected berries prevents complete fungal
colonization, whereupon pycnidia can be found only around the
infection point. These symptoms can mistakenly be diagnosed
as physiological drying, also known as stem necrosis, attrib-
uted to nutritional imbalances (improper Ca and Mg/K ratios)
or water deficit problems.
Before veraison, berries on hailstorm-­injured clusters turn
beige within a few days of infection, then become pinkish blue
and shrivelled. Erumpent pycnidia develop densely from the in-
fected tissue, appearing brownish violet in hue while im­mature

Fig. 182. Immature berries of cv. Rhine Riesling infected through

the pedicels by Pilidiella diplodiella. (Cour­tesy M. Bisiach)

Fig. 181. Infection on the rachis of cv. Rhine Fig. 183. Brownish-­violet, immature pycnidia of Pilidiella diplodi-
Riesling by Pilidiella diplodiella, causing desicca- ella erupting across the surface of an infected berry. (Cour­tesy
tion and death of the cluster. (Cour­tesy M. Bisiach) M. Bisiach)

92
Causal Organism at the optimal temperatures of 22–27°C, and is triggered by the
White rot is caused by the fungus Pilidiella diplodiella (Speg.) presence of juice or berry exudates. Infection of unwounded
Crous & Van Niekerk [syns. Coniella diplodiella (Speg.) Petrak rachises and pedicels requires longer durations of wetness. Se-
& Sidow, Coniothyrium diplodiella (Speg.) Sacc., Phoma dip­ vere disease development can follow hailstorms when tempera-
lodiella Speg.]. Intercellular, dichotomously branched, hyaline tures are near the optimum, whereas negligible incidence has
to yellowish septate hyphae (12–16 µm in diameter) give rise to been recorded if the temperature drops below 15°C for 24–48
appressoria and haustoria. Hyphal anastomoses are abundant h after a hailstorm. Mycelium grows rapidly and the fungus
and chlamydospores form. Subglobose pycnidia, 100–200 µm produces abundant pycnidia at optimal temperatures, whereas
wide and with a central ostiole, arise from subcuticular stro- growth is slower and no pycnidia are formed at temperatures
mata, turning dark brown at maturity (Fig. 185, top). Conidio- <15°C or >34°C. The incubation period typically varies from
phores (10–20 × 3–4 µm) are simple or branched at the base, 3–8 days in the field, depending on the type of tissue infected,
hyaline, with 0–3 septa. Smooth, single-­celled, multiguttulate cultivar susceptibility, and weather conditions. Conidia re-
conidia (8–16 × 5–7 µm) are hyaline when immature but be- leased from newly formed pycnidia may cause secondary in-
come pale to medium brown with time, and are elliptical or fections, thereby creating the potential for epidemic disease
ovate with an obtuse apex and truncate base (Fig. 185, bottom). development should favorable conditions persist or recur.

Disease Cycle and Epidemiology Management

The fungus overwinters as mycelium and pycnidia in infected Control of white rot in commercial vineyards is generally
canes and rachises, and in mummified berries that fall to the based on the use of fungicides, although some degree of control
soil or are retained on the vines. Inoculum remains viable for can also be provided by cultural practices, such as minimiz-
months and accumulates in vineyards affected by the disease, ing wounds, planting tolerant varieties, utilizing a high trellis
where soil may contain 300–2,000 conidia per gram. Under system, and employing sanitation to reduce primary inoculum
humid or wet conditions, thousands of conidia are extruded in sources within the canopy and on the soil. Numerous traditional
a mucilaginous matrix through the ostiole of a pycnidium, and protective fungicides, including pthalimides, dichlofluanid, and
individual conidia are then separated and dispersed primarily chlorothalonil, are effective against white rot; dicarboximides
by rainfall. Soilborne inoculum can also be distributed on con- and the DMI fungicide difenoconazole also are efficacious.
taminated soil particles dispersed by rain, hailstones, or farm Captan or folpet applied within 12–18 h after a hailstorm pro-
equipment. The pathogen infects berries through wounds, most vides about 75% control of new infections, but efficacy falls to
often caused by hail; wounds caused by insects or other fungal 50% if treatment is delayed for 21 h and is generally ineffective
diseases such as powdery mildew can also afford the pathogen after 24 h, especially at temperatures >20°C. The dicarboxi-
entry but are epidemiologically less important. In contrast, ra- mides also provide good control if applied within 12–18 h after
chises and pedicels can be infected via direct penetration by the a hailstorm at temperatures <20°C. Efficacious systemic mate-
fungus. Berries may also be colonized by mycelial expansion rials such as difenoconazole should provide a longer period of
of the fungus from infected pedicels. Cluster susceptibility is postinfection control than the traditional protective materials.
highest during flowering, decreasing after.
Conidia germinate in free water at temperatures of 11–30°C.
Infection of injured berries occurs within about 6 h of wetness

Fig. 184. White rot on a cv. Barbera cluster, girdled

by expansion of Pilidiella diplodiella from infected
berries into the rachis; air introduced between the
epidermis and raised cuticle has caused some Fig. 185. Reproductive structures of Pilidiella diplodiella: (top) cross
berries to appear white. (Cour­tesy M. Bisiach) section of a pycnidium; (bottom) conidia. (Cour­tesy P. Cortesi)

93
 Selected References Locci, R., and Quaroni, S. 1972. Studies on Coniothyrium diploidella.
I. Isolation, cultivation and identification of the fungus. Riv. Patol.
Bisiach, M., and Battino-­Viterbo, A. 1973. Attività in vitro di alcuni Veg. 8:59-­82.
composti chimici contro Coniothyrium diploidella. Not. Mal. Pi- Van Niekerk, J.  M., Groenewald, J.  Z., Verkley, G.  J.  M., Fourie,
ante 88-­89(III S., N. 14-­15):73-­79. P.  H., Wingfield, M.  J., and Crous, P.  W. 2004. Systematic reap-
Bisiach, M., and Battino-­ Viterbo, A. 1973. Further researches on praisal of Coniella and Pilidiella, with specific reference to species
grapevine cluster drying-­off caused by Coniothyrium diploidella. occurring on Eucalyptus and Vitis in South Africa. Mycol. Res.
Meded. Fac. Landbouwwet. Rijksuniv. Gent 38:1561-­1571. 108:283-­303.
Bolay, A. 1977. Le point actuelle sur le traitement des vignes par les
fongicides après la grele. Prog. Agric. Vitic. 94:233-­234. (Prepared by P. Cortesi, in memory of M. Bisiach)
Li, D., Wan, Y., Wang, Y., and He, P. 2008. Relatedness of resis-
tance to anthracnose and to white rot in Chinese wild grapes. Vitis
47:213-­215.

Diseases Caused by Bacteria

Bacterial Blight growth of these developing shoots is stunted. Buds and shoots
from other spurs on the same vine may develop normally. The
Bacterial blight of grapevine is a destructive disease that was first symptoms on young shoots become visible when they are
first reported in the late nineteenth century in Italy and France. 2–3 weeks old. Initially, linear reddish-­brown streaks appear,
After almost a century of confusion regarding the nature of grape- extending from the base to the shoot tip; then, longitudinal
vine decline, the causal agent was isolated and identified in Greece cracks develop surrounded by brown to black necrotic tissue,
as the bacterium Xanthomonas ampelina and later renamed Xy- and cankers form as these deepen and extend to the pith (Fig.
lophilus ampelinus on the basis of DNA and RNA studies. 186). Shoots subsequently wilt, droop, and may eventually die.
Bacterial blight is a chronic, systemic disease that causes Longitudinal-­and cross-­sections through stems show a one-­
significant economic loss due to decreases in yield (up to 80% sided reddish or brown discoloration of the xylem vessels.
reduction from infected vines) and the shortened life spans Leaves on infected shoots may exhibit sectorial or marginal
of affected vineyards. Serious damage has been reported on necrosis of the blades (Fig. 187) and one-­sided cracking of
highly susceptible cultivars such as Thompson Seedless, Ugni their petioles (Fig. 188). When leaves are penetrated directly
Blanc, Grenache, and Macabeu. To date, the disease has been via the stomata, angular, reddish-­brown spots about 1–2 mm in
observed across Southern Europe, where it is also known as mal diameter can be observed, usually surrounded by a yellow halo
nero (Italy), maladie d’Oléron (France), tsilik marasi (Greece), (Fig. 187); a pale yellow bacterial ooze may be seen emanating
necrosis bacteriana (Spain), mal negro (Portugal); bacterial from them when humidity is high. Cracks and cankers may
blight has also been observed in South Africa, where it is also also appear on the peduncle and rachis of the clusters (Fig.
known as vlamsiekte. X. ampelinus is a quarantine pest for the 188).
EU and many other countries, including the United States. Symptoms may vary considerably depending on the cultivar
and possibly environmental conditions. In several cultivars,
Symptoms cracks and cankers do not develop on the shoots and canes or
Symptoms can appear on all aerial parts of the plant. In early do so only occasionally. It is not unusual for chronically in-
spring, budbreak on affected spurs either fails or is delayed, and fected vines that show little sign of disease to suddenly develop

Fig. 186. Symptoms of bacterial blight Fig. 187. Spots and marginal necrosis on Fig. 188. Shoot canker and necrosis and
at the base of a young shoot, including a a leaf infected by Xylophilus ampelinus. cracking of petioles and rachis due to bac-
deep canker. (Cour­tesy W. Gärtel) (Cour­tesy C. G. Panagopoulos) terial blight. (Cour­tesy A. Bolay)

94
acute symptoms and become debilitated. Affected vines may tained from disease-­free areas. New vines should be inspected
be scattered throughout the vineyard but more often occur in before planting and quarantine restrictions strictly followed.
pockets. In contaminated vineyards, disease spread can be minimized
Although the symptoms described above are typical of bac- by removing and burning all symptomatic vine parts, or, in
terial blight, they are not specific to it and can be confused with cases of severe infections, removing and burning the entire vine.
those of several other diseases. For example, bacterial blight’s Pruning tools should be disinfested before moving from one
shoot cankers and leaf spots are somewhat similar to those of plant to the next. Sprays of copper fungicides are recommended
anthracnose (Elsinöe ampelina), although the latter does not immediately after pruning and periodically up to the stage of
cause brown discoloration of the xylem vessels, and of Phomp- half-­expanded leaves and appear to be especially helpful in
sis cane and leaf spot (P. viticola), although this disease pro- rainy areas. Overhead sprinkler irrigation should be avoided.
duces leaf lesions that are more discrete and shoot cankers less
sunken than found with bacterial blight. Spur failure and the Selected References
development of dead branches could also be caused by various
wood canker and vascular pathogens. Laboratory identifica- Botha, W. J., Serfontein, S., Greyling, M. M., and Berger, D. K. 2001.
tion of the causal agent by means of techniques such as direct Detection of Xylophilus ampelinus in grapevine cuttings using a
isolation on nonselective media, serological tests (immunofluo- nested polymerase chain reaction. Plant Pathol. 50:515-­526.
rescence, ELISA), or molecular tests (e.g., PCR) is therefore Dreo, T., Gruden, K., Manceau, C., Janse, J.  D., and Ravnikar, M.
necessary for definitive diagnosis. 2007. Development of a real-­time PCR-­based method for detection
of Xylophilus ampelinus. Plant Pathol. 56:9-­16.
EPPO/OEPP. 2009. PM 7/96(1): Xylophilus ampelinus. Bulletin
Causal Organism 39:403-­412.
X. ampelinus is a gram-­negative, aerobic, nonspore-­forming, Grall, S., Roulland, C., Guillaumes, J., and Manceau, C. 2005. Bleed-
rod-­shaped bacterium, motile by a single polar flagellum. In ing sap and old wood are the two main sources of contamina-
vitro growth is generally very slow on most media. On nutrient tion of emerging organs of vine plants by Xylophilus ampelinus,
agar, colonies are round with entire margins, semitranslucent, the causal agent of Bacterial Necrosis. Appl. Environ. Microbiol.
slightly raised, glistening and pale yellow; colony diameters 71:8292-­8300.
are 0.2–0.3 mm after 6 days incubation and 0.6–0.8 mm after Panagopoulos, G. C. 1969. The disease “Tsilik marasi” of grapevine:
15 days. Best growth is reported on yeast extract-­galactose-­ Its description and identification of the causal agent (Xanthomonas
calcium carbonate (YGC) medium. Minimum, maximum, and ampelina sp. nov.) Ann. Inst. Phytopathol. Benaki 9:59-­81.
optimal growth temperatures are 6, 30, and 24°C, respectively. Willems, A., and Gillis, M. 2005. Genus Incertae Sedis XIX. Xylophi-
X. ampelinus strains are oxidase negative and catalase posi- lus Willems, Gillis, Kersters, Van Den Broecke and De Ley 1987,
tive and use only a limited number of carbohydrates, organic 428VP. Pages 759-­763 in: Bergey’s Manual of Systematic Bacteri-
ology, 2nd ed. D. J. Brenner, N. R. Krieg, J. T. Staley, and G. M.
acids and amino acids for growth. All strains of Xylophilus are
Garrity, eds. Williams & Wilkins, Baltimore, MD.
sensitive to phage P X. a.15. Willems, A., Gillis, M., Kersters, K., Van Den Broecke, L., and De
Ley, J. 1987. Transfer of Xanthomonas ampelina Panagopoulos
Disease Cycle and Epidemiology 1969 to a new genus, Xylophilus gen. nov., as Xylophilus ampelinus
Grapevine is the only known host of X. ampelinus. The (Panagopoulos 1969) comb. nov. Int. J. Syst. Bacteriol. 37:422-­430.
pathogen survives and multiplies in the vascular tissues of in-
fected plants and cuttings. It moves through the xylem vessels (Prepared by F. Peduto Hand)
in late winter, thereby spreading to healthy canes and spurs
and the shoots and clusters that later arise from them. It also
can be moved from external sources to healthy plants by rain
or overhead irrigation, infecting them through multiple types Crown Gall
of wounds or leaf stomata. Wind and rain not only facilitate
the spread of bacteria, but heavy winds and storms may cause Crown gall is a disease of numerous plant species, character-
wounds that provide additional entry points for the pathogen. It ized by the development of fleshy tumors that can affect plant
also can be transmitted through human activity, both locally via vigor. Grapevines are affected by crown gall wherever they
the use of contaminated pruning tools and over long distances are cultivated, but the problem is most serious in areas with
through the distribution of infected vines or grafting material, low winter temperatures. The primary crown gall disease of
which may be asymptomatic. Up to 50% of apparently healthy grapes is caused by the bacterium Agrobacterium vitis. This
canes obtained from diseased vineyards have been found to be disease is similar in many ways to crown gall caused by the
infected. related species Agrobacterium tumefaciens, which affects over
Sap bleeding from infected vines in the spring provides an 600 dicotyledonous plants worldwide (including grapes) and is
important source of inoculum. Young green shoots that develop particularly important on fruit, nut, and ornamental crops such
from overwintering buds are easily injured and very suscep- as almonds, cherries, peaches, raspberries, and roses. In 1990,
tible to infection, and can be contaminated and subsequently the predominant grapevine crown gall pathogen, previously
infected by bacteria contained in sap dripping from nearby considered “biovar 3” of A. tumefaciens, was reclassified as a
pruning wounds. Cankers developing on new growth provide separate species, A. vitis.
additional inoculum, although contaminated sap is considered Infected vines may grow poorly or die, depending on the
a more important source. Bacteria oozing from infected leaves extent of infection. Crop yield may be reduced, new trunks
during humid periods constitute another source of inoculum. may need to be established, or entire vines may have to be re-
Disease severity in the vineyard may vary considerably from placed. The appearance of galls can be particularly significant
year to year. Some cases of complete recovery were observed in grapevine nursery operations, where diseased plants are usu-
in Greece, probably the result of environmental conditions un- ally discarded, resulting in significant economic loss.
favorable to the pathogen and modified agricultural practices.
Symptoms
Management The major symptom of crown gall is the fleshy galls that are
Control efforts should be directed toward preventing the produced in response to infection. Galls are composed of dis-
spread of the pathogen into unaffected grape-­growing regions organized primary and secondary phloem tissues. Irregularly
and into newly established vineyards in regions where it is al- shaped parenchyma cells and disorganized vascular bundles
ready present. All planting and grafting material should be ob- can also be found in the gall tissue. Because galls are initiated

95
in the cambium, normal nutrient flow is disrupted, compromis- extending up the trunk also are common (Fig. 190), with galls
ing grapevine health. Galls on grapevines are mostly found on sometimes forming on woody tissues extending more than 2
the lower trunk (Fig. 189), often at graft unions and near the m up into the trellis. Galled vines frequently produce inferior
soil line. Small, localized galls or masses of small, pimply galls shoot growth, and portions of the vine above the galls may de-
cline and die.
A high incidence of galling may occur in nurseries at the
graft unions and above (Fig. 191), and at the below-­ground dis-
budded nodes of some cultivars and rootstocks. Galls on lateral
roots, however, are uncommon. Large galls may develop rap-
idly and completely girdle young vines in one season.
Gall expression is determined by the extent of the wound
that initiated infection, the grape cultivar, and the strain of the
pathogen. Current-­season galls are first apparent in early to
mid-­summer as white, fleshy callus growths developing near
injury sites, often near the periphery of old galls. The new
galls turn brown by late summer and in the fall become dry
and corky. After one or two years, the dead galls may flake off
the vine. In some cases, galling that occurs at graft unions may
not be possible to distinguish from abundant callus formation,
and the pathogen must be isolated and identified for diagnosis.
Galls at graft unions have been attributed to inoculum spread
on grafting tools, but inoculum may also come from systemi-
cally contaminated propagation material.
Both tumorigenic and nontumorigenic strains of A. vitis have
been shown to incite necrotic lesions in grape roots, a symptom
not seen with A. tumefaciens. In the field, these lesions appear
on current-­season roots as dark, sunken areas about 3–4 mm in
diameter (Fig. 192).

Fig. 189. Crown gall, which is most apparent

on the basal portions of trunks, developing
upward. (Cour­tesy T. J. Burr)

Fig. 191. Crown gall at the graft unions of young grapevines in a

commercial nursery. (Cour­tesy T. J. Burr)

Fig. 190. Small, pimplelike galls resulting from

infection by Agrobacterium vitis, extending up a Fig. 192. Dark, sunken necrosis in a current-­season grape root
trunk. (Cour­tesy T. J. Burr) caused by Agrobacterium vitis. (Cour­tesy T. J. Burr)

96
Causal Organisms tomato, sunflower, and tobacco (particularly Nicotiana glauca).
Agrobacterium vitis (Ophel and Kerr 1990), the primary For A. vitis, grape plants must be used to test virulence for some
cause of crown gall of grapevines, belongs to the family Rhizo- host-­specific strains, although most strains produce galls on
biaceae. This family includes bacteria such as A. tumefaciens common A. tumefaciens hosts. Recently, a method employing
(Smith and Townsend 1907) Conn 1942 and Rhizobium spp., magnetic capture hybridization (MCH) technology in conjunc-
the symbionts that cause nodules on leguminous plants asso- tion with real-­time PCR was developed, which allows sensitive
ciated with atmospheric nitrogen fixation. Colonies of A. vitis detection of tumorigenic strains of A. vitis from grapevine tis-
and A. tumefaciens growing on nonspecific culture media are sues. This method will further the understanding of the patho-
white, convex, circular, glistening, and translucent; the bacteria gen in grapevines as well as in other potential sources in the
are gram negative, motile, and rod shaped. The two species are environment.
morphologically indistinguishable
The pathogenicity of both A. vitis and A. tumefaciens is as- Disease Cycle and Epidemiology
sociated with the presence of a tumor-­inducing (Ti) plasmid, Tumorigenic A. vitis is associated exclusively with cultivated
an extrachromosomal fragment of DNA. For A. vitis, a sec- grapevines and vineyard soils. It has not been found to cause
ond plasmid encoding tartrate utilization is also involved in crown gall on other plants under natural conditions, although
the host-­pathogen interaction. The genetic makeup of A. vitis there is one report of infection of chrysanthemum. Nontumori-
strains is diverse; they are generally categorized by the pres- genic strains have also been isolated from roots of wild grape-
ence and makeup of their Ti plasmid. A. vitis and A. tumefa- vines growing in locations far removed from vineyards. The
ciens have been shown to form a biofilm on tomato roots and bacterium is routinely disseminated in symptomless grapevine
on abiotic surfaces, abilities that may be associated with both propagation material in which it is endophytically established,
survival and host infection. Nonpathogenic strains of A. vitis and it is probably present in most grape plantings as an endo-
and A. tumefaciens are also found in nature. They may be de- phyte. However, A. vitis does not cause crown gall until it in-
tected as cohabitants with pathogenic strains in soil, in appar- fects plant cells.
ently healthy plant tissue, and in galls. The disease cycle is shown in Figure 193. Infection is initiated
Selective culture media make it possible to isolate Agrobac- in the cambium. Like other Agrobacterium spp., A. vitis infects
terium spp. from soil and plant tissues. Some of the media are by transferring into the plant cell a group of genes (the T-­DNA)
selective for A. vitis, and others allow growth of both A. tu- that reside on its Ti plasmid. These genes are incorporated into
mefaciens and A. vitis. Because colonies of tumorigenic and the DNA of one of the plant’s chromosomes, and when tran-
nontumorigenic isolates of both species look identical and grow scribed by the plant their expression causes it to produce in-
equally well on selective media, inoculation tests are necessary creased levels of hormones (cytokinin and auxin). This results
to confirm their pathogenicity following recovery from grape- in rapid and uncontrolled growth of the cambial cells, leading
vine tissue or the environment. Indicator plants commonly used to the development of the fleshy, unorganized gall tissue char-
in greenhouse pathogenicity tests for A. tumefaciens include acteristic of the disease. The process of how Agrobacterium

Fig. 193. Crown gall disease cycle. (Drawing by D. Boyce)

97
species infect plant cells has been studied extensively for many Burr, T. J., and Reid, C. L. 1993. Biological Control of grape crown
years, and excellent reviews on how they transfer their T-­DNA gall with nontumorigenic Agrobacterium vitis strain F2/5. Am.
to plants have been written. J. Enol. Vitic. 45:213-­219.
Johnson, K. L., Zheng, D., Kaewnum, S., Reid, C., and Burr, T. J. 2013.
Management Development of a magnetic capture hybridization real-­time PCR
Grape crown gall generally develops following attachment of assay for detection of tumorigenic Agrobacterium vitis in grape-
vines. Phytopathology 103:633-­640.
the bacteria to plant cells at sites where wounding has occurred. Kerr, A. 1972. Biological control of crown gall: Seed inoculation.
Wounds may play several functions, including the release of J. Appl. Bacteriol. 35:493-­497.
chemical signals that attract the bacterium and promote infection. Lowe, N., Gan, H. M., Chakravartty, V., Scott, R., Szegedi, E., Burr,
Wounds also stimulate cell division in the plant cambium, thereby T. J., and Savka, M. A. 2011. Quorum-­sensing signal production by
generating cells that are susceptible to infection. Internationally, Agrobacterium vitis strains and their tumor-­inducing and tartrate-­
the most common form of wounds leading to the development catabolic plasmids. FEMS Microbiol Lett. 296:102-­109.
of crown gall are those initiated by freeze injuries on trunks, Ophel, K., and Kerr, A. 1990. Agrobacterium vitis sp. nov. for strains
although mechanical injuries such as those associated with till- of Agrobacterium biovar 3 from grapevines. Int. J. Syst. Bacteriol.
age equipment or grafting are sometimes involved. Therefore, 40:236-­241.
all practices that help to prevent trunk injury are important in Zhu, J., Oger, P.  M., Shrammeijer, B., Hooykaas, P.  J.  J., Farrand,
the management of crown gall. These include selecting planting S. K., and Winans, S. C. 2000. The basis of crown gall tumorigen-
sites with good air and water drainage to reduce the chance of esis. J. Bact. 182:3885-­3895.
freeze injuries, selecting an appropriate cultivar for planting in Zupan, J., Muth, T. R., Draper, O., and Zambryski, P. 2000. The trans-
fer of DNA from Agrobacterium tumefaciens into plants: A feast of
sites where winter injury is a potential threat, and using cultural
fundamental insights. Plant J. 23:11-­28.
practices that are less likely to result in trunk injuries.
When possible, vineyards should be established in soil not (Prepared by T. J. Burr)
previously planted to grapevines, using planting stock derived
from pathogen-­free sources if available. Training vines with
multiple trunks (3–5 per vine) allows the removal of individual
galled trunks while maintaining productivity from the retained Pierce’s Disease
healthy trunks and training suckers as new replacement trunks
for those removed. Hilling above the union on grafted vines in Pierce’s disease, caused by the xylem-­limited bacterium Xy-
late autumn protects basal latent buds from freezing and en- lella fastidiosa, is a lethal disease of European (Vitis vinifera),
sures the development of new scion shoots that may be needed some American (V. labrusca), and French-­American interspe-
for trunk renewal the following season. cific hybrid grapevines. The disease is found throughout areas
Grape varieties differ in their susceptibility to crown gall de- of North and Central American with mild winter temperatures;
velopment, with winter hardiness being a key trait governing it has also been reported in northwestern South America. It is
this response. In climates with cold winters, crown gall is a not found in other viticultural regions of the world, where X.
significantly greater problem on V.  vinifera cultivars than on fastidiosa is usually rated as a pathogen of quarantine signifi-
cultivars derived primarily from native American species such cance. Pierce’s disease is not found in North American viti-
as V. labrusca or interspecific hybrid cultivars. Although Agro- cultural regions that experience low winter temperatures, such
bacterium is sensitive to antibiotics such as streptomycin, treat- as inland portions of the Pacific Northwest, the Upper Mid-
ing plants with bactericides has not provided effective control, west, and the Northeast. Research has shown that grapevines
possibly because the bacteria reside within plant tissues and do experimentally infected with X. fastidiosa and displaying
not come into direct contact with topically applied compounds. symptoms of Pierce’s disease emerge pathogen-­and disease
Similarly, soil fumigation has not been effective for eradicating free following exposure to low winter temperatures that typi-
Agrobacterium from soils, probably because bacteria within cally include many hours below 0°C. Although the “cold curing
infected root fragments are protected from exposure to the fu- phenomenon” has been clearly documented, the physiological/
migants. Treatment of dormant cuttings by submersion in water biochemical basis for it has not been elucidated.
at 50°C for 30 minutes reduces internal levels of A. vitis but Pierce’s disease, named after USDA scientist Newton B.
cannot be relied on for eradication. Pierce who demonstrated the disease to be graft transmissible,
The K-­84 strain of A. radiobacter has been used successfully was first described in 1897 in the Anaheim region of Orange
for control of crown gall caused by A. tumefaciens in other crop County, California. Within a matter of years, the disease had
systems, but this biocontrol is not effective against A. vitis on killed approximately 50,000 acres (20,000 ha) of vineyards,
grapevines. Some nonpathogenic strains of A. vitis are now which led to the closure of more than 50 wineries in this region.
being tested for their utility as biocontrol agents. Transgenic Decades later, the disease was reported in Florida and other
grapevine rootstocks that show reduced susceptibility to crown southeastern states. However, this was likely a result of the ex-
gall disease also have been produced. panded planting of susceptible grapevine genotypes into the
The treatment of established galls with eradicant chemicals region, as many scientists believe that X. fastidiosa is endemic
has produced varying results. In regions where freeze injury to to the southeastern United States and was introduced into Cali-
vines occurs only occasionally, such treatments may be use- fornia on rootstocks or cultivars imported from there. Today,
ful in the very early stage of the disease to minimize further Pierce’s disease is a limiting factor in the cultivation of sus-
gall development, although these vines do remain infected. ceptible grapevine species and hybrids throughout the south-
Some eradicants are effective in killing existing gall tissues, eastern United States, and it is believed to have prevented the
but new galls frequently develop at treated sites the following culture of V. vinifera in Florida beginning with the early Span-
year. Effective treatments for preventing infection within exist- ish settlement in the sixteenth century. The disease continues
ing, infested vineyards have yet to be developed, so every effort to cause significant economic losses throughout California’s
should be made to obtain pathogen-­free planting material for coastal and northern viticultural regions, including Napa and
establishing new vineyard sites. Sonoma valleys. It caused epidemic losses in California’s cen-
tral San Joaquin valley in the 1940s, but losses have remained
Selected References low since then in this large viticultural region.
Bini, F., Kuczmog, A., Putnoky, P., Otten, L., Bazzi, C., Burr, T. J., and Pierce’s disease is spread by sucking insects that specialize in
Szegedi, E. 2008. Novel pathogen-­specific primers for the detection of feeding on xylem sap. Leafhoppers (Hemiptera: Cicadellidae)
Agrobacterium vitis and Agrobacterium tumefaciens. Vitis 47:181-­189. commonly referred to as sharpshooters (subfamily Cicadelli-

98
nae) are the principal vectors, but other families in the order cells and biofilms as well as by host reactions to the pathogen
Hemiptera, such as spittle bugs (Cercopidae) and cicadas (Ci- such as the formation of tyloses and gums (Fig. 194), and are
cadidae), also can transmit the causal bacterium. In the south- more severe in hotter climates and in vines with moisture stress.
eastern United States, there are at least 40 species of xylem Small spots or sections of the leaf margin initially develop chlo-
feeding insects thought to be capable of infecting grapevines. rosis; as the season progresses, this chlorosis extends further
The most important vectors vary with region and immediate into the leaf blade and the margin of the leaf turns brown and
habitat near the vineyard. The introduction of the glassy wing necrotic (Fig. 195). Eventually, the entire leaf may become chlo-
sharpshooter (Homalodisca vitripennis) into southern Califor- rotic and necrotic, and late in the season, the leaf blade detaches
nia in the late 1980s resulted by the early 2000s in epidemic from the end of the petiole and the petiole remains attached to
losses from Pierce’s disease in such regions as Temecula, and the cane (Fig. 196). This late-­season “match stick” symptom is
this insect vector of X. fastidiosa continues to cause significant very diagnostic for Pierce’s disease when observed in conjunc-
disease losses in several southern California counties. Major tion with other foliar symptoms. In red varieties, there is often a
investments have funded research to find a cure for Pierce’s dark-­red band of pigmentation near the margin of the chlorotic
disease. Some of the most promising methods include geneti- zone (Fig. 197), whereas white varieties typically produce only
cally engineering grapevines for resistance to the pathogen, al- the chlorotic band. Infections initiated in early summer often
though consumer acceptance of any resulting products remains produce only yellowed or reddened leaves without distinctive
a concern. marginal discoloration. Fruit on diseased portions of the vine
typically shrivel and can become “raisined” at any time follow-
Symptoms ing veraison (Fig. 198); such fruit is economically worthless.
Symptoms of Pierce’s disease are most severe in the Euro- Infected canes may fail to uniformly lignify late in the sum-
pean grapevine species, V. vinifera. All varieties of V. vinifera mer, resulting in “green islands” of nonlignified tissue that often
are susceptible to the disease and most infected vines eventu- form at the bases of leaf petitoles or fruit rachises attached to the
ally die, although there are some differences among cultivars in canes (Fig. 199). There is a direct correlation between the sever-
the severity of symptom expression and frequency of mortality. ity of symptoms and the concentration of X. fastidiosa bacteria
Chardonnay and Pinot Noir wine grapes and Red Globe table in the tissue. The presence of the bacteria in symptomatic tis-
grapes are examples of cultivars that express severe symptoms sues is easily confirmed by culture, ELISA, and PCR. However,
and die more rapidly than Cabernet Sauvignon, Chenin Blanc, bacteria are very hard to detect in the new growth of infected but
and Merlot, cultivars that typically take up to 5 years to die. asymptomatic vines early in the season, before overwintering
In contrast, muscadine (Vitis rotundifolia Michx. cultivars and bacteria can move to them from overwintering sites in woody
some hybrids between V. vinifera and other bunch-­grape Vitis tissues and begin multiplying.
species native to the southeastern United States become sys-
temically infected with X. fastidiosa but bear quality fruit and
show few symptoms beyond mild leaf scorching.
Following inoculation with X. fastidiosa by infectious insect
vectors, symptoms of Pierce’s disease typically appear during
the same year in the inoculated shoot and may appear in other
shoots, depending on varietal susceptibility, date of infection,
and temperatures favorable for pathogen growth. The bacterium
then moves systemically into older wood and throughout the
entire vine within 2–5 years, depending upon varietal suscep-
tibility. Foliar symptoms typically occur in mid-­to late sum-
mer in most North American viticulture regions, although they
may appear earlier near the Gulf of Mexico. In California, foliar
symptoms begin to develop in the warmer southern counties in
early to mid-­July but not until late July or early August in north-
ern production counties. Overall, symptoms of Pierce’s disease
are associated with the plugging of xylem elements by bacterial

Fig. 195. Marginal leaf chlorosis developing into necrosis on a

grapevine with Pierce’s disease. (Cour­tesy J. S. Kamas)

Fig. 194. Electron micrograph of a cross-­sectional view through

the vascular system of a grapevine infected with Xylella fastidi-
osa, with two xylem vessels plugged by tyloses (upper left, left) Fig. 196. Retained petioles following abscission of affected leaf
and another plugged by a mass of bacterial cells (right). (Cour­tesy blades late in the season, resulting in the “matchstick” symptom
H. C. Hoch) characteristic of Pierce’s disease. (Cour­tesy J. S. Kamas)

99
 In the years following initial infection, the vine continues the observation of significant foliar chlorosis in May or June is
to produce symptomatic leaves, fruit, and canes but permanent unlikely to be caused by Pierce’s disease. The stunted, chlo-
woody cordons begin to die back as the disease progresses. rotic shoots produced as a result of Eutypa dieback also can
Canes that develop on infected cordons often push out later in be confused with the stunted canes associated with Pierce’s
the spring and their growth is very stunted early in the season disease. However, distinctive pruning wound-­associated can-
compared with healthy vines. Spring growth on vines that were kers can usually be found on the cordon basal to shoots stunted
severely infected the year before may be stunted and distorted, by Eutypa infection, whereas cankers are not a symptom of
with interveinal chlorosis resembling zinc deficiency. New Pierce’s disease (although unrelated co-­infection by canker
canes can have shortened internodes with a zigzag pattern of fungi and X. fastidiosa is possible). Vines with Armillaria
growth. However, retarded cane growth can be caused by abi- root rot (Armillaria spp.) or cotton root rot (Phymatotrichop-
otic factors as well as other grapevine pathogens, and this par- sis omnivora) may also exhibit foliar symptoms and dieback
ticular symptom occurring by itself should not be considered that can resemble Pierce’s disease, although such vines often
diagnostic for Pierce’s disease. The dieback of permanent wood show diagnostic signs of those causal pathogens as described
continues until the entire vine fails to leaf out in the spring, within their respective sections of this book. Severe drought
although most growers remove vines affected long before they stress can also mimic the foliar symptoms of Pierce’s disease,
die since they fail to set viable fruit once the entire vine shows although an examination of climatic data and/or any irrigation
these symptoms. regime can usually confirm or eliminate this as a possibility.
Symptoms of Pierce’s disease can be confused with only a Ultimately, however, X. fastidiosa is readily detected in symp-
few other conditions or diseases. Similar chlorotic leaves are tomatic leaves by a number of conventional laboratory tests,
produced by esca-­affected vines, but there are important dif- thereby conclusively confirming the presence of the pathogen.
ferences. Unlike that of Pierce’s disease, foliar chlorosis due to Suspensions of cultured X. fastidiosa can be efficiently inocu-
ecsa usually occurs throughout the leaf blade and in its initial lated into plants by means of a pin-­prick method to confirm
stages is not necessarily confined to the leaf margins. In addi- their pathogenicity.
tion, esca foliar symptoms tend to occur earlier in the growing
season than is typical for Pierce’s disease. Thus, in California Causal Organism
Studies in the late nineteenth century established that Pierce’s
disease was caused by a graft-­transmissible pathogen. Bacteria
were later found in the xylem of affected vines by electron mi-
croscopy, but not until 1978 was a bacterium successfully cul-
tured and shown conclusively to be the causal agent of Pierce’s
disease. This organism, Xylella fastidiosa, is a gram negative,
rod-­shaped bacterium with a rippled cell wall. In addition to
the strain that causes Pierce’s disease, several additional ge-
netically and pathologically distinct strains of X. fastidiosa also
cause diseases of citrus (citrus variegated chlorosis), almond
(almond leaf scorch), and oleander (oleander leaf scorch).
In plants, the bacterium colonizes xylem vessels exclusively;
in its insect vectors, it also colonizes the lining of the foregut.
X.  fastidiosa strains are nutritionally fastidious and typically
are grown on complex, undefined media such as Periwinkle wilt
(PW) or PD3, although some strains have been grown recently

Fig. 197. Band of dark-­red pigmentation near the margin of the

chlorotic and necrotic zone on a leaf of a red-­fruited grapevine
cultivar with Pierce’s disease. (Cour­tesy H. C. Hoch)

Fig. 199. “Green islands” of stem tissue fail-

Fig. 198. Shriveled fruit on a vine infected with Xylella fastidiosa. ing to form periderm on a vine infected with
(Cour­tesy J. S. Kamas) Xylella fastidiosa. (Cour­tesy J. S. Kamas)

100
on chemically defined media. X. fastidiosa grows very slowly also a preferred feeding and reproductive host of an X. fastidi-
on all types of culture media, with Pierce’s disease strains typi- osa vector, the nymphs that emerge on an infected plant have
cally producing small, opalescent colonies within 7–10 days. a much greater probability of acquiring and transmitting the
The complete genomes of X. fastidiosa strains that cause pathogen to healthy plants.
disease in citrus, grapevine, almond, and oleander have been Infected V. vinifera and tolerant native Vitis spp. are consid-
sequenced, allowing researchers to study numerous specific in- ered to be important pathogen reservoirs in the southeastern
teractions between the bacterium, its host, and its vector. For United States and Southern California. This is largely because
example, studies found that X. fastidiosa polygalacturonase glassy-­winged sharpshooter is the most important Pierce’s dis-
is necessary for the pathogen to systemically colonize grape- ease vector in these areas. In California, it has been shown to
vines. Its Type I secretion system was shown to be necessary feed on and acquire X. fastidiosa from woody canes as well to
for the bacterium to survive in grapevine xylem, and mutants transmit the pathogen into new woody canes, although feeding
unable to synthesize a “diffusible signal factor” mediating the on woody tissues is rarely observed in the southeastern United
expression of a number of X. fastidiosa genes were hyperviru- States. Because X. fastidiosa overwinters in woody grapevine
lent in grapevines and no longer transmissible by sharpshooter tissues, glassy-­winged sharpshooter likely can acquire bac-
vectors. Similarly, mutations in the bacterium’s hemagglutinin terium from an infected vine much earlier in the season than
genes, which play a role in cell-­cell attachment and biofilm for- other vectors. Experiments have shown that glassy-­ winged
mation, were likewise hypervirulent and somewhat impaired sharpshooter can transmit the pathogen to dormant vines in the
in insect transmissibility. The question of how the bacterium is southern San Joaquin Valley of California, although the same
able to systemically move throughout plants against the xylem experiments failed to show acquisition from diseased dormant
transpirational stream without a flagellum was answered by the vines. If an infectious glassy-­winged sharpshooter feeds on a
discovery that the bacterium exhibits a “twitching” motility pruned woody spur, the bacterium has only a short distance
that is mediated by Type IV pili. A recent discovery found that to travel in order to become systemically established within
a breakdown product of pectin triggers gene expression needed the permanent framework of that vine. In contrast, many other
for the bacterium to attach to vector mouthparts, which is the sharpshooter vectors can only acquire and transmit X. fastidi-
crucial step of the vector transmission process. osa from green leaves and shoots. If an infectious vector such
These discoveries and others have greatly increased our as the blue-­green sharpshooter feeds on the succulent ends of
understanding of how X. fastidiosa causes disease and how it is a 2-­m-­long shoot, the bacterium has a much greater distance
transmitted by insect vectors. This basic information has sug- to travel before it can cause systemic infection in woody tis-
gested strategies for developing Pierce’s disease-­resistant trans- sues. Indeed, research has shown that X. fastidiosa only causes
genic grapevines as well as other nontransgenic approaches for systemic infection if vines are inoculated very early in the
managing the disease, which are being evaluated. season by vectors such as blue-­green sharpshooter or green-­
and red-­headed sharpshooters, Draeculacephala minerva and
Disease Cycle and Epidemiology Carneocephala fulgida, respectively, which feed exclusively on
In nature, Xylella fastidiosa is transmitted from infected host succulent tissues. The latter three sharpshooters are the most
plants to healthy plants by xylem sap-­feeding insects and root important vectors of Pierce’s disease in the North Coast and
grafts. After acquiring X. fastidiosa, a vector can immediately Central Valley regions of California.
transmit the bacterium to a healthy plant, without a transmis- The epidemiology of Pierce’s disease in California is driven
sion latent period. However, the longer an insect feeds on an by the feeding behavior, preferences, and prevalence of its vec-
infected host plant, the greater the probability of it acquiring tors. The glassy-­winged sharpshooter is a very dispersive and
the bacterium. (Similarly, the more often a grapevine is chal- polyphagous insect. As such, it can acquire X. fastidiosa from
lenged by vectors that have acquired the bacterium, the greater a variety of monocot and dicot hosts. In mixed plantings and
the probability of it becoming infected). Once acquired, the natural vegetation, a glassy-­winged sharpshooter shifts plant
vector inoculates a healthy plant by egesting X. fastidiosa into hosts during the course of the day. In contrast, other Pierce’s
its xylem. Nearly all xylem-­feeding insects that have been disease vectors often remain on single plant hosts for days at
tested can acquire and transmit X. fastidiosa with some effi- a time. Because the glassy-­winged sharpshooter can acquire
ciency, although a vector-­specific strain of the bacterium was and transmit the pathogen to woody grapevine tissues, it can
reported recently. Some vectors, such as the blue-­green sharp- inoculate healthy vines during most of the growing season.
shooter (Graphocephala atropunctata) are extremely efficient Its ability to acquire X. fastidiosa from an infected vine and
at acquiring and transmitting X. fastidiosa to grape, whereas then migrate to and infect adjacent healthy vines results in ef-
others, such as the glassy-­winged sharpshooter, are consider- ficient spread within a vineyard. If glassy-­winged sharpshooter
ably less efficient. However, even an inefficient vector such populations are high, this can result in epidemic Pierce’s dis-
as glassy-­winged sharpshooter can cause extensive spread of ease losses such as those documented in Temecula, California
Pierce’s disease if it is abundant and moves extensively within in the early 2000s. Vineyards inoculated by the glassy-­winged
vineyards. Nymphal stages of the insect vectors can transmit sharpshooter ultimately suffer widespread vine loss throughout
the bacterium, but the pathogen is shed when the insect molts the planting, although it is common to see a clumped distribu-
to its next nymphal or adult stage. X. fastidiosa is not transmit- tion characteristic of localized vine-­to-­vine spread early in the
ted transovarially from an infested female to its offspring, nor course of an epidemic.
is it seedborne. In contrast to the glassy-­winged sharpshooter, the blue-­green
Grapevine strains of X. fastidiosa can infect a large num- sharpshooter, which is the primary vector of X. fastidiosa in
ber of plant species. Most of these are not systemic hosts of the coastal and North Coast regions of California, prefers to
X. fastidiosa but rather nonsystemic, “microsite” hosts where feed on select dicot hosts that live in riparian areas near vine-
the bacteria are restricted to a few xylem vessels at the feeding yards. Adults of the blue-­green sharpshooter overwinter in
site of the vector. Vectors can acquire X. fastidiosa from such the riparian areas where they may acquire X. fastidiosa from
plants, but they are less important as pathogen reservoirs than various plant hosts. Adult sharpshooters that acquire the bacte-
systemically infected hosts. In California, some of the most rium from infected V. vinifera vines in the fall remain infective
epidemiologically significant X. fastidiosa reservoirs are wild through the winter. As temperatures increase in the spring and
grapevines (Vitis californica and feral V.  californica/V.  vinif- vines begin new growth, infectious blue-­green sharpshooter
era hybrids), ground periwinkle (Vinca minor), and Himalayan migrate out of the riparian zone and into adjacent vineyards.
blackberry (Rubus armeniacus) growing in riparian habitats The early-­season distribution pattern of blue-­green sharpshoot-
adjacent to vineyards. If a systemic host of X. fastidiosa is ers resembles that of Pierce’s disease in these vineyards: the

101
highest incidence near the riparian source area of overwinter- before they transmit X. fastidiosa to healthy vines. In areas
ing vectors and diminishing with distance, with most Pierce’s with reasonably cold winters, there is the possibility that vines
disease-­affected vines found within 100 m of the riparian areas. showing limited, first-­year infections may emerge pathogen
This spatial disease pattern occurs very stably over time (80-­to and disease free the following spring owing to the cold-­curing
100-­year-­old vineyards show this same pattern), regardless of phenomenon discussed above in Disease Cycle and Epidemiol-
whether blue-­green sharpshooter populations are found in the ogy. Vines showing a few symptomatic canes should be identi-
vineyard during the summer or if the planting is treated with fied and marked in mid-­to late August and pruned as normal
insecticides to eliminate detectable populations of the insect. the following fall or winter. Growers should inspect these vines
Thus, vector populations in vineyards after late spring seem for poor shoot growth in the spring and for typical foliar symp-
unimportant for systemic Pierce’s disease spread. toms in August. If it is apparent that the vine did not recover
When, during the season, an infection is initiated determines over the winter and additional symptomatic canes are observed
the likelihood of its persistence through the following winter. the following season, the vine should be considered systemi-
In California, vines that were experimentally exposed to in- cally infected and removed to eliminate it as a pathogen res-
fested vectors every month from April through August became ervoir. Severe pruning of affected cordons, and even removing
infected with X. fastidiosa at similar rates throughout that pe- the entire trunk close to the graft unions, has not eliminated
riod. However, almost all vines inoculated in April were still the pathogen in research trials. Although severely pruned vines
diseased the next year, whereas Pierce’s disease persisted in may produce disease-­free, vigorous growth the year after prun-
far fewer vines inoculated in May and only a few that were ing, nearly all develop Pierce’s disease symptoms throughout
inoculated in July. Thus, infections that occur during the initial the vine in the second year.
period of growth in the spring appear to be those most likely No potential bactericides (e.g., antibiotics, copper, and zinc)
to persist as chronic Pierce’s disease. Populations of X. fastidi- or compounds that induce systemic acquired resistance in other
osa become sufficiently high in the new growth of chronically plants have successfully cured or prevented new infections in
diseased vines to be detected by late June or July, when in- evaluation trials, regardless of the mode of delivery employed.
sect vectors most readily acquire the bacterium. However, the Likewise, attempts to find bacterial endophytes antagonistic to
nonchronic nature of new infections established during sum- X. fastidiosa for deployment as biological control agents have
mer months explains why vector control within vineyards after been unsuccessful. However, research in Florida identified a
spring has not slowed Pierce’s disease spread in coastal and strain of X. fastidiosa from elderberry that can systemically
Northern California vineyards and why removing diseased infect V. vinifera vines but not cause disease in them. Further-
vines from vineyards has had no detectable effect in slowing more, vines that were prophylactically inoculated with this non-
the spread of Pierce’s disease in these regions. pathogenic strain did not develop Pierce’s disease when grown
Climatic variables are important factors in both the rate of in Florida, where X. fastidiosa is endemic and Pierce’s disease
Pierce’s disease development and overwinter recovery from pressure is high, whereas unprotected control vines died from
the disease. Summer temperatures of 22–32°C are ideal for the disease within a few years. Additional evaluations of this
the continuous growth of X. fastidiosa, which may explain the X. fastidiosa-­biocontrol strain are currently underway in the
faster appearance of symptoms of Pierce’s disease in Florida southeastern United States and California.
and Texas than in regions of California with cooler night tem- In Southern California, where glassy-­winged sharpshooter
peratures. Within the United States, the geographic areas in is an important vector, applications of systemic and topi-
which Pierce’s disease transitions from a regular to a sporadic cal insecticides have greatly reduced populations relative to
problem and then to a rarity generally reflect the geographic those that first developed after it was introduced into the state.
transitions in measures of winter severity. In general, Pierce’s Vineyards are typically treated with systemic neonicotenoids
disease severity decreases in the Appalachian Mountains with through irrigation water once a year, whereas contact insecti-
increases in altitude and northern latitude as well as distance cides are applied on an as-­needed basis. Insecticides are also
from the moderating influence of the Atlantic Ocean. Both al- applied to citrus, a preferred feeding and reproductive host
titude and latitude correlate broadly with winter cold, but there for glassy-­winged sharpshooter, as well as to other perennial
are no quantitative measures of the precise climatic conditions vector hosts near vineyards. Because the glassy-­winged sharp-
most likely to deter Pierce’s disease development or favor its shooter congregates and breeds in habitats outside vineyards,
spread. Disease severity has increased following mild winters an area-­wide program is necessary to manage Pierce’s disease
in the Texas Hill Country west of Austin and in mountain vine- where this insect is the primary vector. Removal of chronically
yards in Georgia. infected vines may also be important to reduce inoculum where
Both the red-­headed and green sharpshooters that are the glassy-­winged sharpshooter is the primary vector, since citrus
main vectors of Pierce’s disease in California’s Central Valley and other crops traditionally grown near grapes are not alterna-
prefer to feed and reproduce on monocot plant hosts. They then tive host plants of X. fastidiosa. Although some vine losses still
move into adjacent vineyards when their annual weed hosts occur in treated vineyards, these are minimal compared to the
dry up in the summer or are physically removed and can cause heavy losses sustained in the early 2000s. In California, state
noticeable Pierce’s disease problems if populations are suffi- and federal governments in cooperation with ornamental nurs-
ciently high. Alfalfa fields are good breeding habitats for both ery and grape-­grower organizations fund an extensive nursery
red-­headed and green sharpshooters if their grass host plants plant inspection system, the goal of which is to prevent the
occur as weeds there. Alfalfa also serves as a systemic, propa- spread of glassy-­winged sharpshooter into noninfested coun-
gative host of X. fastidiosa, as do some grass and sedge species. ties. This effort has been very successful to date, with only a
The typical vineyard infected by these vectors is adjacent to few localized detections of glassy-­winged sharpshooter outside
weedy alfalfa fields or irrigation ditches, and the distribution of the infested southern counties. In such cases, local infestations
infected vines typically reveals a gradient from the weed habi- have been eradicated by aggressive insecticide applications.
tat. Like the blue-­green sharpshooter, red-­headed and green Control of Pierce’s disease in coastal and Northern Cali-
sharpshooters prefer to feed only on succulent green tissues of fornia, where the blue-­green sharpshooter is the primary vec-
the grapevine. tor, has focused on managing riparian plant composition and
timely springtime insecticide applications in riparian areas.
Management Work is ongoing with various federal and state regulatory
To date, there is no therapeutic cure for Pierce’s disease-­ agencies to develop a riparian plant management program that
affected V. vinifera grapevines, but much can be done to pre- selectively removes the breeding hosts of the vector while si-
vent disease spread if vectors can be excluded or controlled multaneously providing environmental benefits to the riparian

102
habitats. Growers can apply for permits to remove vector plant Chatterjee, S., Almeida, R. P. P., and Lindow, S. E. 2008. Living in two
hosts while replanting the area with native vegetation that is worlds: The plant and insect lifestyles of Xylella fastidiosa. Ann.
not attractive to the blue-­green sharpshooter. This program has Rev. Phytopathol. 46:243-­271.
been very effective at reducing blue-­green sharpshooter popu- Davis, M. J., Purcell, A. H., and Thomson, S. V. 1978. Pierce’s disease
lations and lowering the incidence of Pierce’s disease in ad- of grapevines: Isolation of the causal bacterium. Science 199:75-­77.
jacent vineyards; unfortunately, it also is very labor intensive Feil, H., and Purcell, A. H. 2001. Temperature-­dependent growth and
survival of Xylella fastidiosa in vitro and in potted grapevines.
and expensive. Additionally, implementing the program is not Plant Dis. 85:1230-­1234.
feasible unless the vegetation can be managed on both sides of Feil, H., Feil, W.  S., and Purcell, A.  H. 2003. Effects of date of in-
the waterway, which sometimes requires the cooperation of a oculation on the within-­plant movement of Xylella fastidiosa and
neighboring landowner. persistence of Pierce’s disease within field grapevines. Phytopathol-
Management of weeds in adjacent fields, especially those ogy 93:244-­251.
of alfalfa, and along irrigation ditches is the primary means Guilhabert, M. R., and Kirkpatrick, B. C. 2005 Identification of Xylella
of reducing populations of the red-­headed and green sharp- fastidiosa avirulence genes: Hemagglutinin adhesions contribute to
shooter. If undertaken, weed control significantly reduces the Xylella fastidiosa biofilm maturation and colonization and attenu-
incidence of Pierce’s disease in California’s Central Valley and ate virulence. Mol. Plant-­Microbe Interact. 18:856-­868.
other viticultural regions where these insects are its primary Hopkins, D. L. 2005. Biological control of Pierce’s disease in the vine-
vectors. yard with strains of Xylella fastidiosa benign to grapevine. Plant
In the southeastern United States where the disease is clearly Dis. 89:1348-­1352.
polycyclic, rouging of infected vines inhibits within-­vineyard Hopkins, D.  L., and Purcell, A.  H. 2002. Xylella fastidiosa: Cause
of Pierce’s disease of grapevine and other emergent diseases. Plant
spread of the pathogen and is an integral part of disease
Dis. 86:1056-­1066.
management. Kamas, J., Appel, D., Black, M., Labay, A., Lewis, J., and Morano, L.
Currently, the only satisfactory control of Pierce’s disease 2012. Pierce’s Disease Overview and Management Guide: A Re-
in areas where the disease is endemic and chronic is to plant source for Grape Growers in Texas and other Eastern U. S. Growing
grapevines that are genetically resistant to X. fastidiosa. Cur- Regions. Texas A&M AgriLife Ext. Serv., College Station.
rently available resistant genotypes do not produce fruit that is Killiny, N., and Almeida, R. P. P. 2009. Host structural carbohydrate
comparable to that from V.  vinifera cultivars, and the market induces vector transmission of a bacterial plant pathogen. Proc.
for it is limited to affected regions. Whereas all V. vinifera va- Natl. Acad. Sci. U. S. A. 109:22416-­22420.
rieties are susceptible and eventually die from Pierce’s disease Meng, Y., Li, Y., Galvani, C.  D., Hao, G., Turner, J.  N., Burr, T.  J.,
once infected, some are much more susceptible and die sooner and Hoch, H. C. 2005. Upstream migration of Xylella fastidiosa via
than others. Where commercially feasible, growers should plant pilus-­driven twitching motility. J. Bacteriol. 187:5560-­5570.
less-­susceptible cultivars near known sources of the pathogen Newman, K. L., Almeida, R. P. P., Purcell, A. H., and Lindow, S. E.
and insect vectors, such as riparian areas. The discovery that 2004. Cell-­ cell signaling controls Xylella fastidiosa interac-
genes for Pierce’s disease resistance reside in a single locus in tions with both insects and plants. Proc. Natl. Acad. Sci. U. S. A.
101:1737-­1742.
V. arizonica has facilitated the utilization of traditional breed- Purcell, A. H., and Sanders, S. R. 1999. Fate of Pierce’s disease strains
ing methodologies to develop resistant hybrids with V. vinifera of Xylella fastidiosa in common riparian plants in California. Plant
that maintain fruit qualities of the latter. Field testing of these Dis. 83:825-­830.
selections is currently underway. A number of strategies to de- Redak, R. A., Purcell, A. H., Lopes, J. R. S., Blua, M. J., Mizell, R. F.,
velop Pierce’s disease-­resistant transgenic V. vinifera cultivars and Andersen, P. C. 2004. The biology of xylem fluid–feeding in-
or rootstocks are being evaluated nationwide. Development and sect vectors of Xylella fastidiosa and their relation to disease epide-
use of transgenic rootstocks that could deliver anti-­X. fastidiosa miology. Annu. Rev. Entomol. 49:243-­270.
compounds into nontransgenic fruiting varieties are seen by Reddy, J. D., Reddy, S. L., Hopkins, D. L., and Gabriel, D. W. 2007.
some as the most desirable and likely approach to be accepted TolC is Required for Pathogenicity of Xylella fastidiosa in Vitis vi-
by growers, wineries, and consumers. nifera Grapevines. Mol. Plant-­Microbe Interact. 20:403-­410.
Roper, M.  C., Greve, L.  C., Warren, J.  G., Labavitch, J.  M., and
Selected References Kirkpatrick, B. C. 2007. Xyella fastidiosa requires polygalacturo-
nase for colonization and pathogenicity in Vitis vinifera grapevines.
Almeida, R.  P.  P., and Purcell, A.  H. 2003. Transmission of Xylella Mol. Plant-­Microbe Interact. 20:411-­419.
fastidiosa to grapevines by Homalodisca coagulata (Hemiptera: Walker, A. 2008. Breeding Pierce’s disease resistant winegrapes.
Cicadellidae). J. Econ. Entomol. 96:264-­271. Pages 248-­253 in: Proc. Pierce’s Dis. Res. Symp. Calif. Dep. Food
Almeida, R. P. P., Wistrom, C., Hill, B. L., Hashim, J., and Purcell, Agric., Sacramento.
A.  H. 2005. Vector transmission of Xylella fastidiosa to dormant
grape. Plant Dis. 89:419-­424. (Prepared by B. C. Kirkpatrick)

Diseases Caused by Phytoplasmas

Grapevine Yellows Diseases phloem of plants and are transmitted only by specific, phloem-­
feeding insect vectors (leafhoppers, planthoppers, and psyllids)
or through vegetative propagation techniques. Because phyto-
Grapevine yellows are a group of diseases reported in several plasmas can be transmitted within infected cuttings and bud-
countries and continents. All varieties of grapevines are sus- wood, grapevine yellows diseases may become epidemic when
ceptible to grapevine yellows, but some may be more affected infected mother plants are used as sources of propagating mate-
than others. Symptoms of all grapevine yellows diseases are rial and the resulting progeny are established in vineyard sites
similar: canes, shoots, leaves, and berries are damaged, result- inhabited by vector species.
ing in a decline of the affected vines and significant loss in crop The history of grapevine yellows diseases dates back to the
yield and quality. All grapevine yellows diseases are associated 1950s, when flavescence dorée was first reported in south-
with phytoplasmas, obligate intracellular parasites similar to west France. At that time flavescence dorée was regarded as a
bacteria but lacking a true cell wall. They are restricted to the physiological disorder, with symptoms of bright golden leaves

103
on the interspecific hybrid cultivar Baco 22A. Later, after aerial Grapevine yellows diseases have been identified in all
spread and graft transmission were demonstrated, the causal grapevine-­growing countries of Europe, in Israel and Leba-
agent was assumed to be a virus. In 1967, however, a different non, in Asia Minor, in several states along the eastern seaboard
class of pathogens was ascribed to the so-­called yellows group of the United States, and in Australia. The reason for the ap-
of plant diseases. First called mycoplasmalike organisms and parent absence of grapevine yellows diseases in California is
now renamed phytoplasmas, these microbes were subsequently unknown. In the eastern United States, North American grape-
identified in affected grapevines and in vector insects, allowing vine yellows is most destructive in Virginia, where nearly 30%
flavescence dorée to be compared with Bois noir and Vergil- of the vines have been lost in some Chardonnay plantings over
bungskrankheit diseases occurring in northern France, Italy, a 5-­to 10-­year period, but becomes less severe moving both
and Germany, and to yellows diseases of grapevines reported in northward and southward; e.g., the disease is observed only
other countries around the world. The generic name of grape- sporadically and with little general consequence in New York.
vine yellows was recommended for application to these indi- Phytoplasmas are acquired by vector insects while feeding
vidual diseases in 1994 by the Steering Committee of ICVG in the phloem sieve tubes of infected host plants. After acquisi-
(International Council for the Study of Virus and Virus-­like tion, the phytoplasmas move, multiply, and persist in the body
Diseases of the Grapevine). of infected vectors, which transmit them to other susceptible
With the development of molecular tools to detect and char- plants while feeding. Phytoplasmas occupy only the phloem
acterize phytoplasmas in plants and insects, the causal organ- sieve tubes of the vascular system but are distributed through-
isms of each disease can now be characterized and vector species out the grapevine in this tissue, including roots, trunk, canes,
identified. Because phytoplasmas are presently unculturable, shoots, leaf petioles and veins, and bunch rachises. However,
they cannot be classified according to formally recognized spe- their distribution within infected plants is uneven and their
cies with Latin binomials, which requires a description of the movement and multiplication are not fully understood. Affected
organism grown in pure culture. They therefore have been classi- current-­year shoots do not lignify (become woody) and they
fied mainly on the basis of the sequence homology of their ribo- therefore die in the winter. Phytoplasmas, nevertheless, persist
somal DNA (16S rDNA and 16S-­23S intergenic spacer region), over the winter in cordons, trunks, roots, and in (asymptomatic)
and the convention of ‘Candidatus Phytoplasma’ species has dormant, lignified canes, and therefore may be propagated by
been adopted as one means of referring to distinct phytoplasma grafting or rooting dormant wood, providing a mechanism for
lineages and putative species. Biological traits, when available, long-­distance spread of the pathogens. Although phytoplasmas
are also taken into account to differentiate closely related organ- are persistent in vector insects once acquired, they generally
isms grouped in the same cluster. To date, nine different phyto- are not passed on to their progeny transovarially. Hence, the
plasmas belonging to five different groups have been associated role of reservoir plants in maintaining inoculum is considered
with the various grapevine yellows diseases. Table 3 lists some to be critical.
characteristics of these phytoplasmas. The most outstanding fea- Natural spread of each grapevine yellows diseases depends
ture of the classification of grapevine yellows phytoplasmas is on the presence and abundance of its vector species in addi-
their great diversity. The association of phytoplasmas within the tion to specific aspects of vector biology, behavior, and feeding
same ribosomal group with different vectors, for example, those activity. Disease transmission is also dependent on the distri-
causing flavescence dorée and Palatinate grapevine yellows, fur- bution of infected vines within the vineyard, and the presence
ther accentuates grapevine phytoplasmas diversity. outside the vineyard of reservoir plants from which insect vec-

104
tors may acquire inoculum and subsequently become infective. Magarey, P.  A., and Wachtel, M.  F. 1986. Australian grapevine yel-
Hence, epidemiological features of the various grapevine yel- lows. Int. J. Trop. Plant Dis. 4:1-­14.
lows diseases do differ. In general, two modes of spread have Maixner, M., Daire, X., Boudon-­Padieu, E., Laviña, A., Batlle, A., and
been recognized, i.e., clustered and random, depending on the Reinert, W. 1997. Phytoplasmas. Pages 183-­195 in: Sanitary Selec-
preferred-­or occasional-­feeding status of specific vectors on tion of the Grapevine: Protocols for Detection of Viruses and Virus-­
grapevines. Individual diseases have exhibited contrasting epi- like Diseases. Les Colloques 86, INRA Editions, Paris, France.
Seemüller, E., Marcone, C., Lauer, U., Ragozzino, A., and Göschl, M.
demiological traits among different vineyards subject to vari- 1998. Current status of molecular classification of the phytoplas-
able environments and viticultural practices. mas. J. Plant. Pathol. 80:3-­26.
Uyemoto, J.  K., Cummins, J.  R., and Abawi, G.  S. 1977. Virus and
Management virus-­like diseases affecting grapevines in New York vineyards.
Although spontaneous remissions have occurred, in general American J. Enol. Vitic. 28:131-­136.
grapevine yellows-­ affected grapevines cannot be purposely Wolf, T. K., Prince, J. P., and Davis, R. E. 1994. Occurrence of a grape-
cured. Therefore, disease management is largely predicated vine yellows in Virginia vineyards. Plant Dis. 78:208.
on preventative measures based upon knowledge of the vector
identity, biology, and behavior, and of phytoplasma host reser- (Prepared by E. Boudon-­Padieu)
voirs. For example, in some portions of western Europe, flaves-
cence dorée has been managed with a well-­timed application
of an insecticide targeting a single leafhopper vector, which
has only one generation per year and lives only on grapevines. Australian Grapevine Yellows
In contrast, North American grapevine yellows is vectored by
multiple leafhopper species with most having multiple genera- Symptoms of grapevine yellows were first reported in Aus-
tions per year; thus, effective insecticidal control would require tralia in 1976. The disease was originally named the “Rhine
repeated treatments throughout the year, which is both eco- Riesling problem” in South Australia and “Chardonnay de-
nomically and environmentally impractical. For this disease, cline” in Victoria, but was later renamed Australian grapevine
management recommendations include the avoidance of highly yellows because of its similarity to other grapevine yellows
susceptible cultivars, removal of wild reservoir hosts, and early diseases. The disease is now found in most viticultural re-
roguing of symptomatic vines gions of Australia. A high incidence occurs in the hotter inland
New vineyards should be established from propagation grape-­growing districts of Sunraysia in New South Wales and
sources that are free of grapevine yellows phytoplasmas, and Victoria, the Riverina in New South Wales, and the Riverland
movement of phytoplasma-­infected and/or vector-­infested ma- in South Australia, with cvs. Chardonnay and Riesling most
terials to areas not already harboring them must be avoided. commonly affected. However, disease symptoms have been
The flavescence dorée phytoplasma is a quarantine organism in observed and phytoplasmas detected in other cultivars as well.
the European Community and importation of infected planting
material is prohibited. Soaking dormant planting material in Symptoms
hot water (50°C for 45 min) can be used to eradicate phytoplas- During spring and summer, disease symptoms on white-­
mas and destroy insect eggs deposited in the bark. fruited cultivars include one or more shoots with an irregular
chlorosis of the leaves (Fig. 200). Later, the chlorotic areas of
Selected References the leaves often turn necrotic. In red-­fruit cultivars, affected
leaves can show an irregular pattern of reddening, but they can
Batlle, A., Martínez, M. A., and Laviña, A. 2000. Occurrence, dis- also be solid red in color (Fig. 201). In both red-­and white-­
tribution and epidemiology of Grapevine Yellows in Spain. Eur. J. fruited cultivars, the leaf margins tend to curl downward and
Plant Pathol. 106:811-­816. overlay one another. Leaf blade abscission occurs with the peti-
Bianco, P. A., Davis, R. E., Casati, P., and Fortusini, A. 1996. Preva- oles initially remaining attached to the shoots, although they
lence of aster yellows (AY) and elm yellows (EY) group phytoplas- eventually abscise as well. Shoots with Australian grapevine
mas in symptomatic grapevines in three areas of northern Italy. yellows symptoms may produce aborted fruit clusters early in
Vitis 35:195-­199. the season or berry shrivel later in the season. A dieback begins
Boudon-­Padieu, E., and Grenan, S. 2002. Hot water treatment. Meth- at the shoot tips and progresses downward node by node. Af-
ods page of website of International Council for the Study of Virus
fected canes develop a blue, waxy appearance, lignify unevenly
and Virus-­ like Diseases of the Grapevine (ICVG). http://web.
pppmb.cals.cornell.edu/fuchs/icvg/data/icvghotw.pdf or not at all, and become rubbery in strength. Often only a few
Bovey, R., and Martelli, G.  P. 1992. Directory of Major Virus and
Virus-­like Diseases of Grapevines: Description, Historical Re-
view and Bibliography. Mediterr. Fruit Crop Improv. Counc. and
Int. Coun. for the Study of Viruses and Virus-­like Diseases of the
Grapevine. Imprimerie Finzi, Tunis, Tunisia.
Carraro, L., Loi, N., Kuszala, C., Clair, D., Boudon-­Padieu, E., and
Refatti, E. 1994. On the ability-­inability of Scaphoideus titanus Ball
to transmit different grapevine yellows agents. Vitis 33:231-­234.
Daire, X., Clair, D., Larrue, J., and Boudon-­Padieu, E. 1997. Survey
for grapevine yellows phytoplasmas in diverse European countries
and Israel. Vitis 36:53-­54.
Davis, R.  E., Dally, E.  L., Tanne, E., and Rumbos, I.  C. 1997. Phy-
toplasma associated with grapevine yellows in Israel and Greece
belong to the stolbur phytoplasma subgroup, 16SrXII-­A.  J. Plant
Pathol. 79:181-­187.
Gibb, K. S., Constable, F. E., Moran, J. R., and Padovan, A. C. 1999.
Phytoplasmas in Australian grapevines—detection, differentiation
and associated diseases. Vitis 38:107-­114.
Lee, I.-­M., Gundersen-­R indal, D.  E., Davis, R.  E., and Bartoszyk,
I.  M. 1998. Revised classification scheme of Phytoplasmas based Fig. 200. Irregular chlorosis and downward curling of leaves on a
on RFLP analyses of 16S rRNA and ribosomal protein gene se- white-­fruited cultivar affected with Australian grapevine yellows.
quences. Int. J. Syst. Bacteriol. 48:1153-­1169. (Cour­tesy F. E. Constable)

105
canes are affected on a grapevine, but occasionally all may be vineyards. However, strains of ‘Ca. Phytoplasma australiense’
symptomatic. Significant yield reductions have been reported (genetically similar to the Australian grapevine yellows phy-
in some Australian grapevine yellows-­ affected vineyards. toplasma) were detected in papaya and strawberry in northern
Symptoms mimicking those of the disease may be confused Australia and in flax (Phormium tenax) in New Zealand. Insect
with certain abiotic causes of vascular disruption, such as stran- vectors have not been identified for any strains of ‘Ca. Phyto-
gulation by tendrils, mechanical breakage, or insect feeding. plasma australiense’ in Australia; however, in New Zealand, the
However, symptomatic leaves are always distal to the point of vector of the Phormium yellow leaf strain of ‘Ca. Phytoplasma
injury in these examples. australiense’ is the planthopper Oliarus atkinsonii (Myers) of
the family Ciixidae.
Causal Organisms In contrast, the tomato big bud phytoplasma has a broad
Three distinct phytoplasmas have been associated with Aus- plant host range and is vectored by Orosius argentatus
tralian grapevine yellows on the basis of electron microscopy (Evans). Studies have demonstrated acquisition of tomato big
studies, antibiotic treatments, and polymerase chain reaction bud phytoplasma by O. argentatus when the insects are ex-
(PCR) assays: the Australian grapevine yellows phytoplasma posed to diseased grapevines, and successful retransmission
of the stolbur (16SrXII) group; the Australian tomato big bud to faba bean test plants. Vineyard surveys using PCR assays
phytoplasma of the faba bean phyllody (16SrII) group; and for detection of the tomato big bud phytoplasma have detected
the Buckland Valley grapevine yellows phytoplasma, which low numbers of potentially inoculative O. argentatus. No in-
is closely related to the stolbur and the aster yellows (16SrI) sect vector of the Buckland Valley grapevine yellows phy-
groups. The Australian grapevine yellows phytoplasma was toplasma has been identified. The propagation of Australian
further assigned the Candidatus (Ca.) species name ‘Ca. Phy- grapevine yellows and tomato big bud phytoplasmas through
toplasma australiense’ because analysis of its 16S rRNA gene green cuttings has been demonstrated, albeit at a frequency of
sequence showed it to be distinct from other members of the less than 1%.
stolbur group, which includes the grapevine phytoplasma as-
sociated with the Bois noir/Vergilbungskrankheit disease. In Management
addition, ‘Ca. Phytoplasma australasia’ is the designated Can- Because the existence of aerial vectors for any Australian
didatus species name for the tomato big bud phytoplasma. A grapevine phytoplasma has not been proven, insecticide sprays
Candidatus species name has not been proposed for the Buck- are not recommended as a general management strategy to
land Valley grapevine yellows phytoplasma. The Australian prevent the spread of Australian grapevine yellows disease.
grapevine yellows phytoplasma occurs more frequently than However, there is a risk of spreading the phytoplasmas through
the tomato big bud or Buckland Valley grapevine yellows phy- conventional propagation practices, so only clean sources
toplasmas; the latter is currently limited to two vineyards in the should be used. On the basis of research done elsewhere with
Buckland Valley of Victoria. None of the other phytoplasmas other grapevine yellows diseases, hot water treatment of 50°C
known to infect grapevines in other parts of the world have for 30 min may be tried.
been found in Australia.
Selected References
Disease Cycle and Epidemiology
The incidence of Australian grapevine yellows disease in Bonfiglioli, R. G., Guerrini, S., and Symons, R. H. 1996. Cooperative
individual vineyards can fluctuate from year to year. Chronic Research Centre for Viticulture: Sampling program for grapevine
symptoms can persist over several years in some grapevines yellows diseases. Aust. Grapegrower and Winemaker 394:22-­24.
while the disease goes into remission in others. The reason Constable, F.  E. 2002. The biology and epidemiology of Australian
grapevine phytoplasmas. Ph.D. thesis. University of Adelaide,
for the apparent recovery of some symptomatic grapevines is
Australia.
not known. Both Australian grapevine yellows and tomato big Constable, F. E., Whiting, J. R., Gibb, K. S., and Symon, R. H. 2002.
bud phytoplasmas have been detected throughout the year in A new grapevine yellows phytoplasma from the Buckland Valley of
shoot, cordon, trunk, and root tissues by means of PCR assays, Victoria, Australia. Vitis 41:147-­154.
indicating that they can persistently infect grapevines. Phyto- Constable, F. E., Gibb, K. S., and Symons, R. H. 2003. Seasonal dis-
plasmas also have been detected in symptomless Australian tribution of phytoplasmas in Australian grapevines. Plant Pathol.
grapevines, albeit less frequently than in symptomatic vines. 52:267-­276.
Alternative hosts for the Australian grapevine yellows phyto- Constable, F. E., Whiting, J. R., Jones, J., Gibb, K. S., and Symons,
plasma have not been found consistently in or around diseased R. H. 2003. The distribution of grapevine yellows disease associ-
ated with the Buckland Valley grapevine yellows phytoplasma. J.
Phytopathol. 151:65-­73.
Constable, F. E., Jones, J., Gibb, K. S., Chalmers, Y. M., and Symons,
R.  H. 2004. The incidence, distribution and expression of Aus-
tralian grapevine yellows, restricted growth and late season leaf
curl diseases in selected Australian vineyards. Ann. Appl. Biol.
144:205-­218.
Davis, R. E., Dally, E. L., Gundersen, D. E., Lee, I-­M., and Habili, N.
1997. “Candidatus Phytoplasma australiense,” a new phytoplasma
taxon associated with Australian grapevine yellows. Int. J. Syst.
Bacteriol. 47:262-­269.
Gibb, K. S., Constable, F. E., Moran, J. R., and Padovan, A. C. 1999.
Phytoplasmas in Australian grapevines—detection, differentiation
and associated diseases. Vitis 38:107-­114.
Liefting, L. W., Beever, R. E., Winks, C. J., Pearson, M. N., and For-
ster, R. L. S. 1997. Planthopper transmission of Phormium yellow
leaf phytoplasma. Aust. Plant Pathol. 26:148-­154.
Magarey, P.  A., and Wachtel, M.  F. 1986. Australian grapevine yel-
lows. Int. J. Trop. Plant Dis. 4:1-­14.
Osmelak, J.  A., Emmett, R.  W., and Pywell, M. 1989. Monitoring
Fig. 201. Solid red discoloration and downward curling of leaves for potential leafhopper vectors (Hemiptera: Cicadelloidea and
on a red-­fruited cultivar affected with Australian grapevine yel- Fulgoroidea) of the causal agent of Australian grapevine yellows.
lows. (Cour­tesy F. E. Constable) Plant Prot. Q. 4:8-­10.

106
Schneider, B., Padovan, A., De la Rue, S., Eichner, R., Davis, R., Ber- and 208), Chardonnay, Scheurebe, and Kerner, but are less dis-
nuetz, A., and Gibb, K. 1999. Detection and differentiation of phy- tinctive in cv. Müller-­Thurgau.
toplasmas in Australia: An update. Aust. J. Agric. Res. 50:333-­342. Generally, symptoms on infected grapevines are either re-
White, D. T., Blackall, L. L., Scott, P. T., and Walsh, K. B. 1998. Phy- stricted to a few shoots on an otherwise normal cane or involve
logenetic positions of phytoplasmas associated with dieback, yellow entire canes. Symptoms usually develop throughout the vine if
crinkle and mosaic diseases of papaya, and their proposed inclusion it is infected while young. As with flavescence dorée, infected
in ‘Candidatus Phytoplasma australiense’ and a new taxon, ‘Can-
didatus Phytoplasma australasia’. Int. J. Syst. Bacteriol. 48:941-­951.
grapevines may be in symptom remission one year and develop
symptoms the next. Whether grapevines recover completely,
(Prepared by F. E. Constable)

Bois noir or Vergilbungskrankheit

Bois noir was first described in northeastern France and later
in the Moselle and Rhine river valleys of Germany as Ver­
gilbungskrankheit. The two terms are synonyms, describing
the same disease. Bois noir/Vergilbungskrankheit is the most
widespread grapevine yellows disease in Europe and southern
Mediterranean countries and continues to spread in Germany.
It has occurred in conjunction with flavescence dorée in vine-
yards in southern France and Italy and with other grapevine
yellows diseases in Italy, Germany, Greece and Israel.

Symptoms
The overall symptoms of Bois noir/Vergilbungskrankheit
diseases are essentially similar to those of other grapevine yel- Fig. 203. Cluster symptoms of Bois noir/Vergilbungskrankheit,
including partial abortion of set berries on cv. White Riesling.
lows diseases. All involve leaf discoloration, even if restricted (Cour­tesy M. Maixner)
to secondary shoots (Fig. 202), accompanied by flower abor-
tion, cluster collapse (Fig. 203), or berry shrivel (Fig. 204), and
delayed lignification of shoots and canes. However, symptoms
of Bois noir/Vergilbungskrankheit may differ slightly among
grape cultivars. It causes black pustules arranged in longitu-
dinal rows along the stems of V. vinifera cvs. White Riesling
and Scheurebe (Fig. 205), a symptom that is absent on cvs.
Pinot Noir, Pinot Blanc, and Pinot Gris. Leaf symptoms are
pronounced in Pinot Noir (Fig. 206), White Riesling (Figs. 207

Fig. 204. Cluster symptoms of Bois noir/Vergilbungskrankheit, in-

cluding berry shrivel in cv. Pinot Noir. (Cour­tesy M. Maixner)

Fig. 202. Leaf symptoms of Bois noir/Vergilbungs­ Fig. 205. An unlignified shoot of cv. White Riesling affected by
krankheit on cv. White Riesling, confined to Bois noir/Vergilbungskrankheit, with rows of black pustules ar-
random shoots developing on otherwise normal ranged longitudinally and a bluish layer of wax (largely removed
appearing canes. (Cour­tesy M. Maixner) from the middle internode). (Cour­tesy M. Maixner)

107
remain in a state of latency for one or more years, or are rein- of pronounced symptoms. Symptom intensity is reduced when
oculated via infective leafhoppers is uncertain. As a rule, Bois grapevines are deficient in nitrogen or coinfected by nepoviruses.
noir/Vergilbungskrankheit is not lethal.
Symptom severity is influenced by ambient weather condi- Causal Organism
tions. Cool, wet weather leads to delayed symptom development Bois noir and Vergilbungskrankheit are associated with the
whereas hot and dry conditions favor an early, rapid development same phytoplasma of the stolbur (16SrXII-­A) group, which is
found in Austria, Croatia, France, Germany, Greece, Hungary,
Italy, Slovenia, Spain, Switzerland, Israel, and Lebanon. Al-
though stolbur phytoplasmas are widespread and infect a wide
variety of plants, the group is quite homogenous with little
genomic variation between isolates; however, a molecularly
distinct isolate of Vergilbungskrankheit was detected in one vi-
ticulture area in Germany.

Disease Cycle and Epidemiology

The cixiid planthopper, Hyalesthes obsoletus Signoret, re-
portedly vectors Bois noir/Vergilbungskrankheit, although
it is possible that alternative vectors might be involved in at
least some locations. H. obsoletus is a circum-­Mediterranean
species whose distribution extends from North Africa and the
Middle East to Central Europe and is a known vector of the stol-
bur phytoplasma to solanaceous plants. Among the additional
herbaceous host species susceptible to this phytoplasma is the
bindweed (Convolvulus arvensis L.), upon which H. obsoletus
Fig. 206. Early leaf symptoms on cv. Pinot Noir affected by Bois completes its entire life cycle as this insect’s preferred breeding
noir/Vergilbungskrankheit; dark sectors will eventually expand host. Eggs are deposited on the root collar; after hatching, all
across the entire leaf surface. (Cour­tesy M. Maixner) larval instars remain on the roots and acquire the phytoplasma
from infected plants. Consequently, emerging adults may al-
ready be infective. H. obsoletus has a single generation in cen-
tral Europe and Turkey, two in Israel.
Although H. obsoletus feed on a wide range of plant spe-
cies, feedings on grapevines are regarded as accidental events.
Nevertheless, incidental probes are sufficient to transmit the
pathogen and cause infections. Overall, infected grapevines
are regarded as a “dead-­end” host for this phytoplasma from
which no additional transmission occurs, and these vines serve
no significant function in the disease epidemiology. Regard-
less, disease incidence can be high in some areas and years,
albeit with considerable annual fluctuation. The extent of dis-
ease development is strongly influenced by abiotic and biotic
factors that affect the vector species and breeding host. For ex-
ample, vineyards in Germany on steep slopes are characterized
by stony soils with high average soil temperatures, supporting
high densities of bindweed plants and thereby contributing to
large populations of potentially infectious vectors. In some
Fig. 207. Early leaf symptoms of Bois noir/Vergilbungskrankheit regions, large vector populations attributed to above-­normal
on cv. White Riesling. Yellow discoloration and necrosis begins summer temperatures have also been associated with Bois noir/
along the main veins and extends across the leaf blade. (Cour­tesy
M. Maixner) Vergilbungskrankheit outbreaks.

Management
Currently, no satisfactory disease management strategy has
been identified. Applications of insecticides directed at the vec-
tor H. obsoletus are not recommended owing to its subterranean
behavior and the low affinity of the adults to grapevines. How-
ever, the use of sticky traps to monitor adults emerging from the
soil may provide some estimate of potential infection pressure.
As bindweed plants are considered the principal host for the
pathogen and vector species, control of this weed may provide
benefit. A combination of different strategies, including but
not limited to herbicide treatments and planting of competi-
tive cover crops, should be considered in vineyards. Manage-
ment of this weed should be extended to neighboring fallowed
fields to whatever extent possible, especially where disease
spread is chronic. In northern Europe, infected grapevines play
an insignificant role in the disease epidemiology and removal
of diseased vines from affected vineyards is not warranted.
Fig. 208. Advanced leaf symptoms of Bois noir/Vergilbungs­ Thorough inspection of propagation sources and/or hot water
krankheit on cv. White Riesling, with tissue chlorosis and necrosis treatment to eradicate phytoplasmas from propagating wood
extending over substantial portions of the leaf blade and leaf mar- should be practiced to limit disease spread to new vineyards
gins rolled downwards. (Cour­tesy M. Maixner) and disease-­free regions.

108
 Selected References grapevine diseases in Europe. All V. vinifera scions are suscep-
tible and losses from the disease have caused vineyards to be
Batlle, A., Martínez, M.  A., and Laviña, A. 2000. Occurrence, dis- abandoned in some regions. Even in regions where flavescence
tribution and epidemiology of Grapevine Yellows in Spain. Eur. J. dorée is absent, the presence of S. titanus should be regarded as
Plant Pathol. 106:811-­816. posing a threat of a disease outbreak.
Carraro, L., Loi, N., Kuszala, C., Clair, D., Boudon-­Padieu, E., and Re-
fatti, E. 1994. On the ability-­inability of Scaphoideus titanus Ball to Symptoms
transmit different grapevine yellows agents. Vitis 33:231-­234.
Caudwell, A., Larrue, J., Kuszala, C., and Bachelier, J. C. 1971. Plu-
All Vitis vinifera cultivars are susceptible to flavescence
ralité des jaunisses de la vigne. Ann. Phytopathol. 3:95-­105. dorée, albeit to different degrees. Highly susceptible cultivars
Daire, X., Clair, D., Larrue, J., and Boudon-­Padieu, E. 1997. Survey may die after 2–3 years or may display a crisis-­recovery-­relapse
for grapevine yellows phytoplasmas in diverse European countries cycle, whereas more resistant cultivars can recover completely
and Israel. Vitis 36:53-­54. the year after symptoms appear. Symptom expression is prob-
Daire, X., Clair, D., Reinert, W., and Boudon-­Padieu, E. 1997. De- ably dependent also on the response of the rootstock partner.
tection and differentiation of grapevine yellows phytoplasmas be- Bud burst in the spring is typically delayed or even absent on
longing to the elm yellow group and to the stolbur subgroup by infected vines and entire inflorescences may dry up before or
PCR amplification of non-­ribosomal DNA. Eur. J. Plant Pathol. during bloom. The most characteristic symptoms occur in the
103:507-­514. summer and include discoloration and downward rolling of the
Klein, M., Weintraub, P.  G., Davidovich, M., Kuznetsova, L., leaves, shriveling of berries on developing clusters, and poor lig-
Zahavi, T., Ashanova, A., Orenstein, S., and Tanne, E. 2001. Moni- nification of shoots and canes that results in flexuous wood and
toring phytoplasma-­bearing leafhoppers/planthoppers in vineyards a “weeping” posture of conspicuously symptomatic vines in au-
in the Golan Heights, Israel. J. Appl. Entomol. 125:19-­23.
tumn. On black-­fruited cultivars, all parts of the leaf (both lamina
Maixner, M., Ahrens, U., and Seemüller, E. 1995. Detection of the
German grapevine yellows (Vergilbungskrankheit) MLO in grape-
and veins) most exposed to the sun turn red (Fig. 209), whereas
vine, alternative hosts and a vector by a specific PCR procedure. affected leaves become golden yellow on white-­fruited cultivars
Eur. J. Plant Pathol. 101:241-­250. (Fig. 210). Because the vector leafhopper S. titanus completes its
Reinert, W., and Maixner, M. 2000. Distribution and differentiation of life cycle on grapevine, symptomatic vines commonly occur in
grapevine phytoplasmas in Germany. 13th ICVG Conference, Inter- clusters that progressively expand in area over time.
national Council for the Study of Virus and Virus-­like Diseases of Leaf symptoms of flavescence dorée may be confused with
the Grapevine (ICVG). http://web.pppmb.cals.cornell.edu/fuchs/ those caused by certain virus diseases (leafroll disease, corky
icvg/data/abstrb.pdf
Sforza, R., Clair, D., Daire, X., Larrue, J., and Boudon-­Padieu, E.
1998. The role of Hyalesthes obsoletus (Hemiptera: Cixiidae) in
the occurrence of Bois noir of grapevines in France. J. Phytopathol.
146:549-­556.
Weber, A., and Maixner, M. 1998. Survey of populations of the pl-
anthopper Hyalesthes obsoletus Sign. (Auchenorrhyncha, Cixiidae)
for infection with the phytoplasma causing grapevine yellows in
Germany. J. Appl. Entomol. 122:375-­381.

(Prepared by M. Maixner)

Flavescence dorée
Flavescence dorée was the first grapevine yellows disease to
be recognized, in 1955 in southwestern France. Its leafhopper
vector, Scaphoideus titanus Ball (= S. littoralis Ball), a nearctic Fig. 209. Red, downward-­c urled leaves and “weeping” growth
species that in Europe lives only on grapevine, was identified habit symptomatic of flavescence dorée, on red-­ fruited cv.
in 1961. A native of eastern North America, it was introduced Grenache Noir in September. (Cour­tesy E. Boudon-­Padieu)
to Europe after World War II. The associated flavescence dorée
phytoplasma was visualized in 1971. Although some other
grapevine yellows diseases were originally described as “fla-
vescence dorée-­like,” molecular characterization of phytoplas-
mas now permits their differentiation.
In Europe, the vector, S. titanus, occurs in the northern parts
of Portugal, Spain, and Italy; in the southern half of France;
and in a portion of Switzerland and western Slovenia. Dis-
tribution of the disease in France is confined to all southern
and southwestern viticulture regions and a few localities in the
east. Although large populations of S. titanus are found in the
viticultural regions to the north (i.e., the Rhone Valley, Beau-
jolais, Bourgogne, Franche-­Comté, and Pays de Loire), these
currently are not affected by flavescence dorée. In Northern
Italy, flavescence dorée extends to the provinces of Piemonte,
Lombardia, Trentino-­Alto Adige, Veneto, Friuli-­Venezia Gi-
ulia, Liguria, and some sites in Emilia-­Romagna. In Spain, fla-
vescence dorée has been identified in a limited number of sites
in northeastern Catalonia. Fig. 210. Golden-­yellow, downward-­curled leaves symptomatic
Flavescence dorée is a quarantine disease in the European of flavescence dorée, on white-­fruited cv. Sémillon in September.
Community and is considered to be among the most dangerous (Cour­tesy E. Boudon-­Padieu)

109
bark, and the yellow mosaic syndrome of fanleaf degenera- Management
tion); magnesium deficiency; or mechanical injury. However, As long-­distance spread of flavescence dorée is associated
with leafroll disease, veins remain green and lignification of with infected planting materials, care must be taken in select-
the stems is not affected; with leafroll or corky bark, berries ing sources for vine propagation. Only clean sources should be
do not shrivel; and with the yellow mosaic strain of Grapevine used and propagations should be avoided in affected viticul-
fanleaf virus or magnesium deficiency, leaves do not roll down- tural regions. Alternatively, a hot water treatment (50°C for 45
ward. Also, flavescence dorée-­like symptoms associated with min) may be employed to destroy the flavescence dorée phyto-
mechanical injury are limited to the part of the cane or shoot plasma in dormant canes.
beyond the point of injury. Infected mother plants used in root- Consideration must also be given to the long distance trans-
stock production either develop weak symptoms (delayed bud port of the vector species on infested canes and plants, where up
burst and/or irregular lignification) or remain asymptomatic. to 1,000 viable eggs per kilogram of cane have been reported.
However, rootstocks derived from such asymptomatic vines Once the disease is established in a region, insecticides may
can serve as a source of inoculum to infect and cause typical be applied during the egg hatching period to control the single
disease symptoms in otherwise-­healthy scion varieties that are generation of the vector. Because the insect is not infectious
budded or grafted onto them. during its incubation period, insecticide treatments do not need
to begin until 3 weeks after the first hatch and can discontinue
Causal Organism once the hatch is completed.
The flavescence dorée phytoplasma belongs to the elm yel-
lows or 16SrV group, which also includes phytoplasmas of Selected References
forest trees and other woody plants in North America, Europe,
and China. The genome size is about 700 Kb. The flavescence Angelini, E., Clair, D., Borgo, M., Bertaccini, A., and Boudon-­
dorée phytoplasma is specifically acquired from and transmit- Padieu, E. 2001. Flavescence doree in France and Italy -­Occur­rence
ted to grapevines by the vector leafhopper S. titanus. It has of closely related phytoplasma isolates and their near relationships
been transmitted experimentally to the herbaceous broadbean to Palatinate grapevine yellows and an alder yellows phytoplasma.
Vitis 40:79-­86.
plant (Vicia faba L.) by means of S. titanus collected in flaves- Angelini, E., Bianchi, G. L., Filippin, L., Morassutti, C., and Borgo, M.
cence dorée-­affected vineyards, and from infected broadbean 2007. A new TaqMan method for the identification of phytoplas-
to grape seedlings by means of S. titanus reared in an insectary. mas associated with grapevine yellows by real-­time PCR assay.
The flavescence dorée phytoplasma also has been transmitted J. Micro­biol. Meth. 68:613-­622.
from broadbean to broadbean with another leafhopper, Eus- Batlle, A., Laviña, A., Kuszala, C., Clair, D., Larrue, J., and Boudon-­
celidius variegatus Kirschbaum. Padieu, E. 1997. Detection of Flavescence dorée phytoplasma in
Although belonging to the same group of phytoplasmas as grapevine in northern Spain. Vitis 36:211-­212.
those associated with Palatinate grapevine yellows, the flaves- Borgo, M., and Angelini, E. 2002. Diffuzione della Flavescenza do-
cence dorée phytoplasma and these latter organisms are clearly rata della vite in Italia e relazioni con vitigni, pratiche agronomiche
distinguished in terms of their vectors, molecular assays, and et materiali di propagazione. ATTI Giornate Fitopatologiche 2002.
specific antibodies formed against them. A single isolate of the 1:35-­50.
flavescence dorée phytoplasma appears to be widespread and Boudon-­Padieu, E., Larrue, J., and Caudwell, A. 1989. ELISA and dot-­
commonplace in all affected provinces in France, Italy, and blot detection of Flavescence dorée MLO in individual leafhop-
per vectors during latency and inoculative state. Curr. Microbiol.
Spain.
19:357-­364.
Boudon-­Padieu, E. 2002. Flavescence dorée of the grapevine: Knowl-
Disease Cycle and Epidemiology edge and new developments in epidemiology, etiology and diagno-
Cultivated and wild grapevines are the sole source of flaves- sis. ATTI Giornate Fitopatologiche 2002 1:15-­34.
cence dorée inoculum. In Europe, the vector species S. titanus Caudwell, A., Larrue, J., Boudon-­Padieu, E., and McLean, G. D. 1997.
lives exclusively on Vitis spp. Eggs are laid in summer, over- Flavescence dorée elimination from dormant wood of grapevines
winter beneath bark and between bud scales, and begin hatch- by hot-­water treatment. Aust. J. Grape Wine Res. 3:21-­25.
ing around the second week of May in southern France. The Daire, X., Boudon-­ Padieu, E., Bervillé, A., Schneider, B., and
length of the hatching period depends on the degree of winter Caudwell, A. 1992. Cloned DNA probes for detection of grapevine
chilling, which is necessary for terminating egg diapause, typi- Flavescence dorée mycoplasma-­like organism (MLO). Ann. Appl.
cally ranging from 5 weeks in southern France to 12 weeks in Biol. 121:95-­103.
Lefol, C., Lherminier, J., Boudon-­Padieu, E., Larrue, J., Louis, C., and
Corsica. After five larval instar stages at moulting intervals of Caudwell, A. 1994. Propagation of the Flavescence dorée MLO
approximately 10 days, the adults emerge in mid-­July, mate, lay (Mycoplama-­like organism) in the leafhopper vector Euscelidius
eggs, and perish in September, providing just one generation variegatus Kbm. J. Invertebr. Pathol. 63:285-­293.
per year. Meignoz, R., Boudon-­Padieu, E., Larrue, J., and Caudwell, A. 1992.
The flavescence dorée phytoplasma overwinters within in- Flavescence dorée de la vigne. Présence de MLO et effets cyto-
fected canes in an incubation phase. It is acquired through feed- pathogènes associés, dans le liber de la vigne. J. Phytopathol.
ing of S. titanus nymphs in the spring or by adults once they 134:1-­9.
have developed in the summer, a process that usually takes 7–8 Quartau, J. A., Guimarães, J. M., and André, G. 2001. On the occur-
(but as few as 4) days, after which the pathogen multiplies and rence in Portugal of the nearctic Scaphoideus titanus Ball (Homop-
circulates inside the insect, which becomes infective after ap- tera, Cicadellidae), the natural vector of the grapevine “Flavescence
proximately 4 additional weeks of incubation. The S. titanus dorée” (FD). IOBC/wprs Bulletin 24:273-­276.
adults are very mobile and, since they transmit the flavescence Schvester, D., Carle, P., and Moutous, G. 1961. Sur la transmission
dorée phytoplasma from vine to vine and feed only on grapes, de la Flavescence dorée des vignes par une cicadelle. C. R. Acad.
Agric. Fr. 47:1021-­1024.
can spread the disease rapidly within a viticultural district.
Steffek, R., Reisenzein, H., and Zeisner, N. 2007. Analysis of the pest
Symptoms generally appear the year after infection. risk from grapevine Flavescence dorée phytoplasmas to Austrian
Flavescence dorée can also be transmitted through the use viticulture. EPPO Bull. 37:191-­203.
of dormant wood for grafting, although only from canes that Vidano, C. 1964. Scoperta in Italia dello Scaphoideus littoralis Ball
were inoculated the previous growing season and, thus, still in Cicalina americana collegata all “Flavescence dorée” della Vite.
a state of incubation. Because such canes are asymptomatic, Ital. Agric. 101:1031-­1049.
they pose a danger of inadvertent spread of the disease if used
for propagation. (Prepared by E. Boudon-­Padieu)

110
 North American Grapevine Yellows In cases where disease symptoms appear early in the season,
they often advance to affect other shoots on the grapevine as
The presence of a North American grapevine yellows was the season progresses. In the first season of expression, overt
first suggested in 1974 on the basis of similarities between symptoms can appear anytime after bloom, and are often first
flavescence dorée and expression of a previously undescribed apparent as a destruction of fruit clusters. Cluster abortion is
disease of the Vitis interspecific hybrid cv. DeChaunac in the noticed initially as a loss of berry turgor, followed by rapid
Finger Lakes region of New York State. Later termed leaf curl desiccation of the entire cluster, including the rachis. Shriveled
and berry shrivel, the DeChaunac disease affected a relatively berries adhere to the rachis, but the entire cluster may eventu-
low percentage of grapevines in several vineyards. However, ally abscise from the shoot. Fruit clusters and tendrils on af-
the causal pathogen of leaf curl and berry shrivel was not deter- fected shoots are subject to abortion any time from fruit set
mined. Flavescence dorée-­like symptoms were also observed (Fig. 211) through berry maturity. Additional symptoms on
on V.  vinifera cv. Riesling in the same region, where the in- Chardonnay can include significant shoot dieback and the ac-
digenous leafhopper, Scaphoideus titanus Ball, was proposed quisition of a blue-­gray cast to the shoot stems, rather than the
as a possible vector. North American grapevine yellows was shades of green with red highlights that stems normally express
first reported in 1993 in Virginia, where flavescence dorée-­like in mid-­summer. Shoot stems fail to develop brown periderm,
symptoms had been observed since 1987, initially on the highly or develop periderm in irregular islands or patches (Fig. 212).
susceptible V. vinifera cultivars Chardonnay and Riesling and, Dark pustules less than 2 mm in diameter may appear on the
in time, on other vinifera cultivars and rarely on interspecific base of the stems, particularly with cv. Riesling. North Ameri-
hybrids. Symptomatic vines have more recently been observed can grapevine yellows-­affected shoots are pliable and often
and found positive for the causal pathogen in Maryland, south- droop, a condition thought to be related to the failure of af-
east Pennsylvania, the Finger Lakes region of New York, and fected shoots to form lignified secondary phloem fibers. Inter-
the midwestern states of Ohio and Missouri. In Virginia, the nodes are often shortened, leading to an overlapped pattern of
highest incidence of North American grapevine yellows has leaves on a shoot.
been observed in the western piedmont and Blue Ridge Moun- Leaf symptoms are variable, but commonly include abaxial
tain region of the state. leaf rolling; the acquisition of a crisp, hardened, or brittle tex-
ture; and discoloration. Discoloration is variable and a func-
Symptoms tion of cultivar, leaf age, and stage of symptom development.
The symptoms originally observed with North American Foliar symptoms on Chardonnay initiate on the older, more
grapevine yellows in DeChaunac grapevines included yellow- basal leaves of the shoot, and the discoloration is first appar-
ing, hardening, and downward rolling of leaves, and a late-­ ent as an expanding chlorosis, starting at the leaf margins. As
summer shriveling of berries that easily dislodged from the the season progresses, symptoms extend to younger primary
cluster rachis. Shoots remained green or exhibited delayed leaves, as well as to the leaves of lateral shoots. The chlorosis
periderm development in late summer, when healthy shoots may appear as a diffuse yellowing of the normal dark-­green
matured into woody canes. Diseased grapevines in the vine- interveinal region of the leaf (Fig. 213), or it may involve the
yards had expressed chronic infections. However, when indi- development of discrete chlorotic zones either confined to in-
vidual grapevines were transplanted and established in large terveinal regions or including veinal tissue. Chlorotic tissue
containers, or when diseased canes were rooted and grown can become necrotic before leaves abscise. The appearance of
in a greenhouse, all recovered and developed into apparently
healthy plants that failed to reexpress leaf curl and berry shrivel
symptoms within the two years they were observed.
Symptoms of North American grapevine yellows on V. vinif-
era cultivars are essentially similar to those of other grapevine
yellows diseases, and bear many similarities to the symptoms
described for leaf curl and berry shrivel on DeChaunac. Symp-
toms initially involve one to several shoots of an otherwise ap-
parently healthy grapevine, although all shoots of an affected
cordon or grapevine may simultaneously express symptoms,
particularly in highly susceptible varieties such as Chardonnay.

Fig. 212. Lack of late-­season periderm devel-

opment and aborted fruit cluster on the shoot
of a NAGY-­affected cv. Chardonnay vine (right)
Fig. 211. Aborted clusters on Chardonnay grapevine affected compared with healthy shoot (left) that has
with North American grapevine yellows (NAGY), approximately 2 well-­d eveloped periderm and a fully developed
weeks post bloom. (Cour­tesy T. K. Wolf) fruit cluster. (Cour­tesy T. K. Wolf)

111
 growth is stunted and systemic spread is evident throughout
the canopy. Symptomatic grapevines often fail to survive into
a third season, and rarely survive into a fourth. Symptom ex-
pression sometimes varies among locations, which may be the
result of environmental factors that affect the titer or spatial
distribution of phytoplasmas within the host vine. There is no
evidence to date that the two phytoplasmas present in Virginia
vineyards elicit different symptoms.
The epidemiological aspects of North American grapevine
yellows diseases are incompletely understood, but some com-
ponents are known and some can be inferred from knowledge
of other grapevine yellows diseases. Wild grapevines have
tested positive for the presence of phytoplasmas in New York
State and Virginia, and, hence, may serve as phytoplasma res-
ervoirs. The highest incidence of North American grapevine
yellows diseases in Virginia has been observed in vineyards
Fig. 213. Chlorotic cv. Chardonnay leaf symptomatic of NAGY
closely bounded by deciduous woods, especially those harbor-
(left) compared with healthy leaf (right). (Cour­tesy T. K. Wolf) ing Prunus and Vitis species. Specific vectors of North Ameri-
can grapevine yellows phytoplasmas have not been conclusively
identified; however, there is mounting evidence of one or more
discrete zones of chlorotic tissue is more commonly observed insect vectors.
on cv. Riesling, where leaves may also develop a coppery or Scaphoideus titanus, vector of the flavescence dorée phyto-
metallic sheen. Symptoms in red-­fruited cultivars are similar, plasma in Europe, is abundant in the vicinity of North Ameri-
except the leaf discoloration causes leaves to turn red rather can grapevine yellows-­affected vineyards in the Finger Lakes
than yellow. Leaf abscission occurs as the symptoms intensify region of New York State. This leafhopper acquires phytoplas-
and the season progresses. mas from cultivated and wild grapevines in New York State and
transmits them to Vicia faba plants, which develope grapevine
Causal Organisms yellows-­like symptoms. S. titanus and a closely related species,
Early studies of North American grapevine yellows-­like dis- S. minor, are also found in and around vineyards in Virginia.
eases in New York State implicated phytoplasmas as the causal In addition, several other leafhopper species known to vector
agent, first on the basis of the similarity of the disease’s symp- other phytoplasmas to different hosts occur abundantly in Vir-
toms to those described for flavescence dorée in Europe, and ginia vineyards, and currently these are being investigated as
later owing to enzyme-­linked immunosorbent assay (ELISA) potential vectors of North American grapevine yellows phyto-
tests of S. titanus leafhoppers collected from symptomatic plasmas. Preliminary laboratory transmission studies in Vir-
vines and wild V. riparia grapevines growing in the vicinity, ginia have implicated several leafhopper species as potential
in which up to 20% reacted positively to antibodies produced vectors.
from flavescence dorée-­infected plants. As with other grapevine yellows diseases, Chardonnay, Mal-
Additional evidence of phytoplasma involvement was ob- bec, and Pinot Noir are particularly sensitive to North Ameri-
tained in the 1990s when phytoplasmas genetically similar can grapevine yellows symptom expression. Multiyear survey
to those that cause X-­disease of stone-­fruit trees (including data in Virginia found an incidence of recently-­infected Char-
peach) were detected in North American grapevine yellows-­ donnay grapevines as high as 6% and cumulatively exceeding
symptomatic Chardonnay grapevines in Virginia by means of 25% over a 6-­year period. In Virginia vineyards that exhibit up
a polymerase chain reaction (PCR) test. Shortly thereafter, a to 3% annual loss of Chardonnay grapevines to North Ameri-
second phytoplasma was also detected and described from af- can grapevine yellows, infections and plant losses have also
fected Virginia vineyards and other hosts in the vicinity of the occurred in V.  vinifera cvs. Cabernet Franc, Cabernet Sauvi-
affected vineyards. The second phytoplasma was closely asso- gnon, Sauvignon Blanc, Petit Manseng, and Viognier, but at a
ciated with the rRNA group 16SrI phytoplasmas, or aster yel- far lower (< 0.5%) annual incidence.
lows group (‘Candidatus Phytoplasma asteris’-­related strains)
and was related to subgroup A (tomato big bud). Both this Management
16SrI-­group phytoplasma and the previously detected 16SrIII The most effective means of North American grapevine yel-
phytoplasma (a ‘Candidatus Phytoplasma pruni’-­related strain) lows management is to avoid planting highly susceptible culti-
occurred alone or in mixed infections in Chardonnay grape- vars such as Chardonnay, Malbec, and Riesling in or near the
vines in Virginia. Both phytoplasmas also were detected fre- vicinity of diseased vineyards. Efforts to prune out affected
quently in wild V.  vulpina (syn. V.  cordifolia) grapevines cordons or entire trunks in the first season of symptom expres-
outside the affected vineyards, while the 16SrI phytoplasma sion has failed thus far to limit the systemic movement of the
also was detected in black cherry (Prunus serotina Ehrh.) trees. causal organism in grapevines. Prophylactic insecticide treat-
Neither V. vulpina nor P. serotina expressed disease symptoms. ments might be warranted if specific insect vectors and their
The 16SrI North American grapevine yellows phytoplasma is seasonal biology are resolved.
known to have a wide host range, including wild and cultivated
Vitis species, whereas the 16SrIII phytoplasma has been de- Selected References
tected only in V. vinifera. To date, neither of the specific North
American grapevine yellows phytoplasmas has been detected Beanland, L., Noble, R., and Wolf, T. K. 2006. Spatial and temporal
distribution of North American grapevine yellows disease and of
outside North America. potential vectors of the causal phytoplasmas in Virginia. Environ.
Entomol. 35:332-­344.
Disease Cycle and Epidemiology Davis, R., Dally, E. L., Zhao, Y., Lee, I., Wei, W., Wolf, T. K., Beanland,
The North American grapevine yellows diseases observed L., LeDoux, D. G., Johnson, D. A., Fiola, J. A., Walter-­Peterson, H.,
in eastern North America share common symptoms and may Dami, I., and Chien, M. L. 2015. Unraveling the etiology of North
share one or more causal agents. Regardless of cultivar, the ap- American Grapevine Yellows (NAGY): Novel NAGY phytoplasma
pearance of initial symptoms in the first year is followed by a sequevars related to ‘Candidatus Phytoplasma pruni’. Plant Dis.
more severe expression the next growing season, where shoot doi: http://dx.doi.org/10.1094/PDIS-­11-­14-­1185-­R E

112
Davis, R. E., Jomantiene, R., Dally, E. L., and Wolf, T. K. 1998. Phy- infecting grapevine and other plants in Europe. These molec-
toplasmas associated with grapevine yellows in Virginia belong to ular differences also are important to differentiate Palatinate
group 16SrI, subgroup A (tomato big bud phytoplasma subgroup), grapevine yellows from flavescence dorée, which have yet to
and group 16SrIII, new subgroup I. Vitis 37:131-­137. be found together in the same region. Furthermore, Palatinate
Maixner, M., Pearson, R.  C., Boudon-­Padieu, E., and Caudwell, A. grapevine yellows is vectored by the alder leafhopper Oncopsis
1993. Scaphoideus titanus, a possible vector of grapevine yellows alni Schrank, and the vector of flavescence dorée, S. titanus,
in New York. Plant Dis. 77:408-­413.
Pearson, R.  C., Pool, R.  M., Gonsalves, D., and Goffinet, M.  C.
does not occur in the Palatinate region.
1985. Occurrence of flavescence dorée-­like symptoms on ‘White
Riesling’ grapevines in New York, USA. Phytopathol. Mediterr. Disease Cycle and Epidemiology
24:82-­87. Palatinate grapevine yellows is typically restricted to old
Prince, J. P., Davis, R. E., Wolf, T. K., Lee, I.-­M., Mogen, B. D., Dally, vineyards of cv. Scheurebe planted on the valley floor along-
E. L., Bertaccini, A., Credi, R, and Barba, M. 1993. Molecular de- side creeks and rivers populated with black elder trees. The
tection of diverse mycoplasmalike organisms (MLOs) associated incidence of infected vines usually remains below 1%. In con-
with grapevine yellows and their classification with aster yellows, trast, Vergilbungskrankheit naturally infects several cultivars
X-­disease, and elm yellows MLOs. Phytopathology 83:1130-­1137. and grapevines of all ages and is more commonly found in
Prince, J.  P., Davis, R.  E., Wolf, T.  K., Lee, I.  M., and Dally, E.  L. vineyards situated on steep slopes. Occasionally, both disease
1994. Genomic diversity and possible wild plant sources of myco- agents may occur in the same vineyard.
plasmalike organisms (MLOs) infecting grapevines: Implications
for epidemiology. IOM Letters 3:288 (Abstr).
Stoepler, T.  M., and Wolf, T.  K. 2013. North American grapevine
yellows disease: Current knowledge and management recommen-
dations for wine growers. Virginia Coop. Ext. Publ. AREC-­48P.
http://pubs.ext.vt.edu/AREC/AREC- ­48/AREC- ­48.html
Uyemoto, J. K. 1975. A new disease affecting the grapevine variety de
Chaunac. Proc. Am. Phytopathol. Soc. 1:146 (Abstr.).
Uyemoto, J.  K., Cummins, J.  R., and Abawi, G.  S. 1977. Virus and
virus-­like diseases affecting grapevines in New York vineyards.
Am. J. Enol. Vitic. 28:131-­136.
Wolf, T. K., Prince, J. P. and Davis, R. E. 1994. Occurrence of grape-
vine yellows in Virginia vineyards. Plant Dis. 78:208.

(Prepared by T. K. Wolf)

Palatinate Grapevine Yellows

Currently, Palatinate grapevine yellows occurs only in four
viticultural areas of Germany, where it was first detected in the
Palatinate (Pfalz) region. This disease is closely related to other
European grapevine yellows of the elm yellows group such as
flavescence dorée, but its epidemiology differs significantly
from that of the latter.

Symptoms
Symptoms of Palatinate grapevine yellows resemble those Fig. 214. Grapevine cv. Scheurebe affected
typical of all grapevine yellows diseases, such as leaf discolor- by PGY exhibiting a stunted, non­lignified sec-
ation and rolling, lack of shoot lignification, and cluster abortion ondary shoot with downward-rolled yellow
or shriveling of berries. Therefore, when Palatinate grapevine leaves on a primary shoot in an advanced
yellows and Bois noir/Vergilbungskrankheit occur in the same stage of lignification. (Cour­tesy M. Maixner)
vineyard, their symptoms are indistinguishable. However, Pa-
latinate grapevine yellows is almost completely restricted in the
field to cv. Scheurebe, although other cultivars have produced
typical symptoms when inoculated experimentally.
Most grapevines infected by Palatinate grapevine yellows
develop systemic symptoms with severe downward rolling of
uniformly discolored leaves (Fig. 214). Symptoms develop late
in the season, which might explain the nearly complete ligni-
fication of primary shoots (Fig. 215) and attendant difficulty
in identifying infected wood during dormancy. Although the
vigor of infected grapevines is reduced considerably, they usu-
ally survive dormancy.

Causal Organism
An elm yellows (16SrV) group phytoplasma has been associ-
ated with Palatinate grapevine yellows, representing four dif-
ferent types designated as PGY-­A, -­B, -­C, and -­D. Black alder
(Alnus glutinosa (L.) Gaertn.) trees appear to be the natural host
of the PGY phytoplasma, as they are commonly infected, albeit
in latent fashion. PGY phytoplasmas may be distinguished by Fig. 215. A grapevine of cv. Scheurebe with systemic symptoms
molecular traits from other elm yellows group phytoplasmas of PGY, adjacent to healthy vines. (Cour­tesy M. Maixner)

113
 The phytoplasma associated with alder yellows in Germany of closely related phytoplasma isolates and their near relationships
resembles the one associated with Palatinate grapevine yellows to Palatinate grapevine yellows and an alder yellows phytoplasma.
from grapevine. It is transmitted by the leafhopper Oncopsis Vitis 40:79-­86.
alni Schrank, a strictly monophagous species that preferen- Daire, X., Clair, D., Reinert, W., and Boudon-­Padieu, E. 1997. De-
tially feeds on different species of Alnus. Exposing healthy tection and differentiation of grapevine yellows phytoplasmas be-
grapevines to O. alni collected from symptomatic alder trees longing to the elm yellow group and to the stolbur subgroup by
PCR amplification of non-­ribosomal DNA. Eur. J. Plant Pathol.
produced characteristic Palatinate grapevine yellows symp- 103:507-­514.
toms, and field surveys have confirmed the occasional presence Maixner, M., and Reinert, W. 1999. Oncopsis alni (Schrank) (Auche-
of O. alni in vineyards adjacent to alder trees despite the strict norrhyncha: Cicadellidae) as a vector of the alder yellows phy-
host preference of the leafhopper. Nevertheless, transmission toplasma of Alnus glutinosa (L.) Gaertn. Eur. J. Plant Pathol.
efficiency of the phytoplasma to grapevines is very low because 105:87-­94.
the vector ceases to feed on them after just a few probes, per- Maixner, M., Rüdel, M., Daire, X., and Boudon-­Padieu, E. 1995. Di-
haps explaining in part the low incidence of Palatinate grape- versity of grapevine yellows in Germany. Vitis 34:235-­236.
vine yellows in vineyards. Maixner, M., Reinert, W., and Darimont, H. 2000. Transmission of
grapevine yellows by Oncopsis alni (Schrank) (Auchenorrhyncha:
Management Macropsinae). Vitis 39:83-­84.
No specific control measures are required because the in- Reinert, W., and Maixner, M. 2000. Distribution and differentiation of
cidence and economic impact of this disease have been insig- grapevine phytoplasmas in Germany. 13th ICVG Conference, Inter-
nificant. Infected grapevines are typically retained in vineyards national Council for the Study of Virus and Virus-­like Diseases of
the Grapevine (ICVG). http://web.pppmb.cals.cornell.edu/fuchs/
because further spread between them does not occur.
icvg/data/abstrb.pdf
Selected References
(Prepared by M. Maxiner)
Angelini, E., Clair, D., Borgo, M., Bertaccini, A., and Boudon-­
Padieu, E. 2001. Flavescence dorée in France and Italy -­Occur­rence

Diseases Caused by Viruses and Viruslike Agents

Grapevine Virus Diseases V. rupestris), leading to the replanting of vines on alternative,
phylloxera-­resistant rootstocks typically derived from virus-­
indexed mother blocks. However, unlike AXR#1, which toler-
Until the mid-­ 1800s, the traditional viticultural regions ated latent viruses, bud-­grafts of diseased scion sources onto
throughout Europe enjoyed relative freedom from widespread several of these rootstocks declined rapidly, sometimes even
problems with virus diseases. This envious scenario from vi- when elite foundation material was used. Subsequent investiga-
ticulture’s premodern era was likely due to limited trade of tions led to the discovery and characterization of Grapevine
grapevine cultivars among countries and to plantings pre- leafroll-­associated virus 2 (GLRaV-­2) isolates that are involved
dominately of own-­rooted scions; both served to minimize in graft-­incompatibility disorders and decline of young grape-
wholesale spread of viruses and vectors. Later, however, a vines grafted onto susceptible rootstocks. For more informa-
sundry array of virus and viruslike diseases began to plague tion, see “Grapevine leafroll-­ associated virus 2 and Graft
the well-­ established viticultural regions. This change was Incompatibility.” Furthermore, based on the differential re-
brought about by the introduction of the phylloxera root aphid, sponses in two rootstock trials, other sources were determined
Daktulosphaira vitifoliae (Fitch) (Homoptera: Phylloxeridae), to contain additional, yet unidentified, graft-­ transmissible
from North America to Europe in the 1860s, and the destruc- agents (GTAs) associated with decline/death of bud-­inoculated
tion of essentially all vineyards in France in the ensuing 20 test plants grown on specific rootstocks.
years. Thus began an intensive effort to combat this exotic pest. Currently, more than 70 viruses, viroids, and graft-­
Breeders made interspecific crosses with the aim of producing transmissible agents are known to infect grapevines. Some
resistant fruiting scions and rootstocks. The subsequent prac- have restricted distribution, such as Peach rosette mosaic virus,
tice of establishing (or re-­establishing) vineyards in Europe which is restricted to Michigan and southwestern Ontario in the
and elsewhere with grafted vines utilizing phylloxera-­resistant Great Lakes region of North America, whereas others such as
rootstocks, many of them symptomlessly or latently infected grapevine leafroll associated viruses occur worldwide.
with different viruses, proved to be a significant factor in the
eventual global dissemination of virus diseases. (Prepared by J. K Uyemoto and G. P. Martelli)
In 1953, the International Council for the Study of Viruses
and Virus Diseases of Grapevine (ICVG) was organized to
promote communication and collaboration among scientists
studying grapevine virus diseases. The first formal meeting Enation Disease
was held in Switzerland in 1964 and the ICVG met regularly
thereafter. Over the years, council members helped to establish First identified in California in the 1950s as a disorder pos-
standards and procedures for implementing virus disease con- sibly caused by a viruslike agent, enation disease was known to
trol measures and assist in promulgating rules for certification occur in Germany as early as the turn of the nineteenth century.
programs. Adoption of a clean stock program was critical be- It was later reported from most European countries, Venezuela,
cause all viral agents may be increased and disseminated long South Africa, Tunisia, New Zealand, and Australia.
distances in propagating materials and planting stocks.
In the 1980s and 1990s, a new biotype of phylloxera arose Symptoms
in California and destroyed numerous vineyards planted to Affected vines of sensitive cultivars (e.g., Italia, Panse pre-
the previously resistant rootstock AXR#1 (Vitis  vinifera × coce, Primus) show delayed bud burst, slow growth of the

114
shoots, and produce a bushy appearance. As the season pro- Disease Cycle and Epidemiology
gresses, the shoots resume a more normal growth pattern. Ena- Enation disease is not known to spread naturally in the field.
tions, the foliar alterations for which the disease is named, are Its dissemination apparently depends entirely on the use of in-
cuplike in outline and develop along main veins as linear out- fected propagative material.
growths of variable length (up to 4–5 cm) and height (2–3 mm).
Enations occur primarily on the undersides of basal leaves (Fig. Management
216). However, in certain V.  vinifera cultivars and American Disease-­free propagative material obtained through selec-
rootstocks, enations have developed on the upper leaf surfaces tion and indexing should be used. There is no information on
(Fig. 217). Symptomatic leaves are misshapen, fanlike in out- whether the disease can be eliminated by heat treatment or
line with deep lacination, prominent veins, and a thickened meristem tip culture.
lamina. Severely affected leaves drop prematurely, whereas
leaves developed late in the season are asymptomatic and re- Selected References
main attached. The basal internodes of affected shoots are
short, irregular and misshapen with longitudinal bark cracks. Credi, R. 1995. Epidemiological observations on grapevine ena-
Expression of leaf enations can vary greatly from year to year, tion disease in Emilia-­ Romagna (Italy). Phytopathol. Mediterr.
and chronically infected grapevines may be in remission 2 or 3 34:88-­92.
years following the appearance of severe symptoms. Fruit from Hewitt, W. B. 1954. Some virus and virus-­like diseases of grapevines.
infected vines is poor in quality and yields may be reduced by Bull. Calif. Dep. Agric. 43:47-­64.
up to 50%. Prota, U., Garau, R., and Cugusi, M. 1982. Quantitative aspects of
yield of grapevine affected by enation disease in Sardinia. Pages
Causal Agent 41-­48 in: Proc. 7th Meeting ICVG, Niagara Falls 1980, Canada
Agriculture.
The causal agent is unknown but successful graft transmis-
sion suggests that it may be a virus. Transmission by grafting is
(Prepared by U. Prota and R. Garau)
erratic, presumably owing to uneven distribution of the causal
agent within infected vines. The hybrid LN33 is the best indi-
cator currently available. Symptoms appear between 2 and 6
years after grafting, with the greatest frequency in the third and The Fleck Complex
fourth years. Transmission has not been obtained using bud-
wood from infected asymptomatic plants. The fleck complex consists of the diseases fleck proper, as-
teroid mosaic, Rupestris necrosis, Rupestris vein feathering,
Grapevine redglobe virus (GRGV), and viruses that cause la-
tent or semilatent infections in Vitis vinifera and most Ameri-
can Vitis species and rootstock interspecific hybrids. Fleck and
asteroid mosaic diseases were first described in California, but
whereas fleck occurs worldwide, asteroid mosaic is known only
in California. Rupestris necrosis has been reported from Japan
and Rupestris vein feathering from Greece and Italy. GRGV
has been reported from Italy and California.

Symptoms
All diseases in the fleck complex except GRGV are detected
in the indicator host, Vitis rupestris ‘St. George’. Symptoms
of fleck disease include localized translucent spots along the
tertiary leaf veins (Fig. 218). Leaves with intense flecking are
wrinkled, twisted, and may curl upward. Severe forms of the
disease also cause stunting, reduced rooting ability, and poor
Fig. 216. Severe deformation and enations (outgrowths) on under-
graft take. The disease is latent in V. vinifera cultivars and in
sides of basal leaves, symptomatic of grapevine enation disease. most American rootstocks.
(Cour ­tesy U. Prota)

Fig. 217. Symptoms of enation disease appearing on the upper Fig. 218. Translucent spots along tertiary veins of a V. rupestris
side of affected leaves. (Cour­tesy U. Prota) leaf with fleck disease. (Cour­tesy G. P. Martelli)

115
 Symptoms of asteroid mosaic in V. vinifera consist of star-­ morphological, chemico-­ physical, and molecular properties
shaped chlorotic spots with occasional necrotic centers, irregu- similar to GFkV, and all are phylogenetically related. How-
larly distributed on leaf blades. Affected grapevines may be ever, whereas GRGV is in the genus Maculavirus, GAMaV and
stunted and produce little or no fruit. Symptoms in V. rupestris GRVFV are in the genus Marafivirus. Both genera are in the
appear as creamy-­yellow bands along the main leaf veins, and family Tymoviridae.
affected leaves are twisted and asymmetric. GFkV-­infected grapevine cells contain multivesiculated bod-
Rupestris necrosis is characterized by localized necrosis of ies, i.e. cytopathic structures derived from deranged mitochon-
leaf petioles and veinlets (Fig. 219). In contrast, symptoms of dria that undergo peripheral vesiculation following invagination
Rupestris vein feathering consist of transient, mildly chlorotic of both lamellae of the organelle’s limiting membrane. Identi-
discolorations of the primary and secondary leaf veins (Fig. cal structures and particles of an unidentified isometric virus
220). were observed in the phloem of V.  rupestris displaying leaf
vein necrosis. Also, vesiculated chloroplasts and mitochondria
Causal Agents are observed in the phloem elements of grapevines infected by
The agent of fleck is Grapevine fleck virus (GFkV), the type GRVFV and GAMaV, respectively. Vesicles in mitochondria
species of genus Maculavirus in the family Tymoviridae. GFkV and chloroplasts are likely sites of viral RNA replication.
has isometric particles approximately 30 nm in diameter with Polyclonal antisera and monoclonal antibodies raised to
rounded contour and a prominent surface structure, provided GFkV are widely used for diagnosis, and virus-­specific prim-
by clusters of coat protein subunits (molecular mass of approxi- ers have been designed for the molecular detection of GFkV,
mately 25 kDa) arranged as pentamers and hexamers. Virions GAMaV, GRGV. and GRVFV.
contain a single molecule of capped, positive-­sense, single-­
stranded RNA of 7564 nt, four open reading frames, and high Disease Cycle and Epidemiology
cytosine content (about 50%). In density gradient centrifuga- All recognized or putative disease agents of the fleck com-
tion, virus preparations sediment as two components: T, empty plex are phloem-­limited, nonmechanically transmitted viruses
protein shells; and B, virions containing 35% RNA. that persist in infected propagative material and are dissemi-
GRGV, Grapevine asteroid mosaic-­associated virus (GAMaV), nated with it. GFkV is not seedborne. Vectors are unknown,
and Grapevine rupestris vein feathering virus (GRVFV) have but natural spread of fleck has been reported in South Africa
and Italy.

Management
GFkV can be eliminated by heat therapy and meristem tip
culture. Control depends on the production and distribution of
healthy nursery material. Symptomless infections make sani-
tary selection based on symptoms of V. vinifera cultivars and
most American rootstock hybrids unreliable. Hence, all sources
must be indexed onto V. rupestris St. George and/or assayed by
means of antisera or primer sets. Only pathogen-­free materials
should be used for propagations.

Selected References

Abou Ghanem-­ Sabanadzovic, N., Sabanadzovic, S., and Martelli,

G. P. 2003. Sequence analysis of the 3′ end of three grapevine fleck
virus-­like viruses from grapevine. Virus Genes 27:11-­16.
Boscia, D., Martelli, G. P., Savino, V., and Castellano, M. A. 1991. Iden-
tification of the agent of grapevine fleck disease. Vitis 30:97-­105.
Boscia, D., Sabanadzovic, S., Savino, V., Kyriakopoulou, P. E., Mar-
Fig. 219. Localized necrosis of the veins in V. rupestris, symptom- telli, G.  P., and Lafortezza, R. 1994. A non-­mechanically trans-
atic of Rupestris necrosis. (Cour­tesy S. T. Ohki) missible isometric virus associated with asteroid mosaic of the
grapevine. Vitis 33:101-­102.
El Beaino, T., Sabanadzovic, S., Digiaro, M., Abou-­ Ghanem-­
Sabanadzovic, N., Rowhani, A., Kyriakopoulou, P. E., and Martelli,
G.  P. 2001. Molecular detection of Grapevine fleck virus-­like vi-
ruses. Vitis 40:65-­68.
Martelli, G.  P., Sabanadzovic, S., Abou Ghanem-­Sabanadzovic, N.,
Edwards, M.  C., and Dreher, T. 2002. The family Tymoviridae.
Arch. Virol. 147:1837-­1846.
Martelli, G.  P., Sabanadzovic, S., Abou Ghanem-­Sabanadzovic, N.,
and Saldarelli, P. 2002. Maculavirus, a new genus of plant viruses.
Arch. Virol. 147:1847-­1853.
Matsumoto, T., and Ohki, S.  T. 1998. A possible new necrotic dis-
eases of grapevine associated with small isometric particles and
novel membrane-­bound large particles. Ann. Phytopath. Soc. Japan
64:560-­564.
Sabanadzovic, S., Abou Ghanem, N., Castellano, M. A., Digiaro, M.,
and Martelli, G. P. 2000. Grapevine fleck virus-­like viruses in Vitis.
Arch. Virol. 145:553-­565.
Sabanadzovic, S., Abou Ghanem-­Sabanadzovic, N., Saldarelli, P., and
Martelli, G.  P. 1998. Complete nucleotide sequence and genome
organization of grapevine fleck virus. J. Gen. Virol. 82:2009-­2015.
Fig. 220. Vitis rupestris leaf with symptoms of Rupestris vein
feathering, consisting of mild chlorotic discolorations of the pri- (Prepared by G. P. Martelli, A. Rowhani,
mary and secondary leaf veins. (Cour­tesy G. P. Martelli) and S. Sabanadzovic)

116
Fig. 221. Chlorotic, deformed leaf blades of a Kyoho grapevine
infected with Grapevine berry inner necrosis virus. (Cour­tesy
Y. Terai)

Grapevine Berry Inner Necrosis

Originally named grapevine mosaic, the disease was first Fig. 222. Dark-­ green spots developing on the
recognized in the table grape cultivar Kyoho (V.  vinifera L.) surface of fruit from a Kyoho grapevine infected
in 1984. In 1992, concomitant with identification of the causal with Grapevine berry inner necrosis virus. (Cour­
agent, the disease was renamed grapevine berry inner necrosis tesy Y. Terai)
(GBIN) disease and the causal agent Grapevine berry inner ne-
crosis virus (GBINV). The disease is economically important
in the table grape cultivars Kyoho and Pione but is unknown
outside of Japan.

Symptoms
Diseased grapevines exhibit delayed bud break and reduced
vegetative vigor. With chronic infection, the canopy volume is
limited in part as a result of shortening of internodes and vas-
cular necrosis in young shoots. Also, affected leaves develop
chlorotic rings and line patterns beginning in early spring that
remain visible thereafter, and leaves become malformed (Fig.
221). Grape clusters and berries are small with dark-­green spots
developing on the skin surface (Fig. 222) and an internal ne-
crosis of the flesh tissue (Fig. 223). Berries mature late and the
flesh is hard.
Graft inoculations to other grape cultivars produce strong
symptoms in cultivar Campbell Early; the related cultivars
Takao, Kyoho, and Pione; and the rootstock V. riparia Gloire. Fig. 223. Internal view of Kyoho grapes expressing symptoms of
All are useful indicators for GBINV. Latent infections occur in grapevine berry inner necrosis disease. (Cour­tesy Y. Terai)
cultivars Delaware (V. × labrusca L.), Koshu, Kaiji, Semillon,
Merlot, Cabernet Sauvignon, Cabernet Franc, and Pinot Noir
(all V. vinifera). mite (Colomerus vitis), acquired GBINV from diseased grape-
vines and transmitted it to healthy ones. The virus-­vector rela-
Causal Agent tionship and transmission mode are not known. GBINV is the
GBINV (genus Trichovirus) is a flexuous filamentous par- first miteborne virus reported in grapes.
ticle, ca. 740 nm in length by 12 nm in width, containing a
polyadenylated, single-­stranded RNA, mol. wt. 2.5 × 10 6 Da; a Management
genome organization with three open reading frames (encoding Only grapevines propagated from certified sources should be
for replication-­associated protein, movement protein, and coat planted. Applications of lime sulfur during the dormant season
protein); and a coat protein size of 22 kDa. The virus can be may be used to reduce populations of the vector species.
sap-­transmitted to Chenopodium quinoa Willd. and Nicotiana
occidentalis L. and is readily detected in extracts of young Selected References
grape leaves by ELISA or RT-­PCR.
Kunugi, Y., Asari, S., Terai, Y., and Shinkai, A. 2000. Studies on the
grapevine berry inner necrosis virus disease: 2. Transmission of
Disease Cycle and Epidemiology grapevine berry inner necrosis virus by the grape erineum mite,
Natural virus spread was demonstrated when healthy plants Colomerus vitis in Yamanashi. Bull. Yamanashi Fruit Tree Exp.
of cultivars Kyoho and Pione were transplanted into a diseased Stn. 10:57-­64.
vineyard site and exposed for a year. In Yamanashi Prefecture, Nishijima, T., Terai, Y., and Kunugi, Y. 2000. Studies on the grapevine
disease incidences of 9.1 and 73.1% were correlated with low berry inner necrosis virus disease: 1. Symptoms on vines, varietal
and high vector mite populations in their respective vineyard susceptibility and natural spread. Bull. Yamanashi Fruit Tree Exp.
sites. In transmission experiments, the vector, grape erineum Stn. 10:47-­56.

117
Yoshikawa, N., Iida, H., Goto, S., Magome, H., Takahashi, T., and soil, and cultural practices. Under certain conditions, includ-
Terai, Y. 1997. Grapevine berry inner necrosis, a new trichovirus: ing the use of rootstocks susceptible to graft-­incompatibility
Comparative studies with several known trichoviruses. Arch. Virol. disorders and young vine decline, certain isolates of Grapevine
142:1351-­1363. leafroll-­associated virus 2 (GLRaV-­2) can cause plant death.
Although long recognized as a graft-­transmissible disease, the
(Prepared by Y. Terai) etiology of grapevine leafroll disease has only recently been
elucidated after several Grapevine leafroll-­associated viruses
(GLRaVs) were purified and antisera produced. Further ad-
Grapevine Leafroll Disease vances in virus strain characterization and detection have been
accomplished utilizing molecular techniques. Once considered
to be a disease transmitted only through propagative materials,
Grapevine leafroll disease was first recognized as rougeau mealybugs (Hemiptera: Pseudococcidae) and soft-­scale insects
in France (ca. 1853). In Germany, typical disease symptoms (Hemiptera: Coccidae) have now been shown to vector some
were observed as early as 1910, and the viral nature of the dis- GLRaVs.
ease was demonstrated in 1936. Today, grapevine leafroll is a
major virus disease occurring in every grape-­growing region Symptoms
worldwide. This status was reached by disseminating, albeit Grapevine leafroll disease involves a degeneration of primary
unknowingly, infected grape cuttings and propagating scions phloem tissue in young shoots, leaves, and fruit pedicels. In-
on infected but symptomless rootstocks. In California, the dis- fected vines often show delayed bud break and shoot develop-
order was originally known as White Emperor disease. ment, slightly smaller leaves, and reduced shoot length with an
Grapevine leafroll may have originated in the Near East and overall attendant loss of vigor and yield of fruit. Fruit clusters
co-­evolved with Vitis vinifera. Disease severity and yield losses borne on diseased grapevines are smaller than normal, and both
are dependent on a combination of factors, including but not sugar accumulation and pigmentation (in dark-­fruited cultivars)
limited to virus strain, scion cutltivar and rootstock, climate, are often greatly reduced. Leaf symptoms are most striking on
dark-­fruited cultivars, and consist of reddening of the inter-
veinal regions contrasting with green veins. The intensity of this
symptom expression can range from scattered blotches of red
virtually indistinguishable from symptoms of red blotch disease
(Fig. 224) to progressively greater areas of the lamina being dis-
colored (Figs. 225 and 226) to the entire leaf turning bright red
with the exception of the green veins (Figs. 227 and 228). Leaf
symptoms on light-­fruited cultivars are much less pronounced,
consisting of chlorotic interveinal tissue and normal green veins
(Fig. 229). Foliar symptoms typically begin to develop mid-­
season, initially on the more basal-­positioned leaves. However,
their onset and intensity are dependent on virus strain, scion
cultivar, and growing conditions. Mixed virus infections are
common and may act additively or synergistically, thereby in-
creasing disease severity. In addition to showing discoloration,
affected leaves may roll downward, giving rise to the disease
name; the extent of this reaction is dependent on the virus strain
and scion/rootstock combination.
The damage to infected grapevines is chronic. Even so, the
Fig. 224. Blotchy interveinal reddening on a Cab-
ernet Sauvignon vine testing positive for Grape-
severity of leafroll disease may vary from one growing season
vine leafroll-associated virus 3 but negative for to the next. Most American rootstocks with GLRaV infections
Grapevine red blotch-associated virus. (Cour­tesy
M. Fuchs)

Fig. 226. Pronounced interveinal reddening, con-

Fig. 225. Incomplete reddening of the interveinal trasting green veins, and downward rolling on a
regions of a leaf from a cv. Pinot Noir vine with cv. Cabernet Franc leaf exhibiting symptoms of
grapevine leafroll disease. (Cour­tesy M. Fuchs) grapevine leafroll disease. (Cour­tesy M. Fuchs)

118
 Fig. 228. Severe foliar symptoms of grapevine leafroll disease on
a cv. Cabernet Franc vine. (Cour­tesy M. Fuchs)
Fig. 227. Severe foliar symptoms of grapevine leaf­
roll disease on a cv. Pinot Noir vine. (Cour­ tesy
M. Fuchs)

are symptomless. Limited surveys have shown leafroll infec-

tion to be common in juice grapes (e.g., Vitis × labruscana
‘Concord’ and V. labrusca ‘Niagara’), although typical symp-
toms generally are not present. The consequence of such infec-
tions in these cultivars remains unclear.

Causal Agents
Although conclusive scientific proof of their individual eti-
ologies is still lacking, there are five recognized, serologically
distinct viruses associated with grapevine leafroll disease. The
association of disease and virus strain has been corroborated for
GLRaV-­1 and GLRaV-­3 through large-­scale serological testing Fig. 229. Interveinal chlorosis and downward rolling of leaves on a
of diseased grapevines worldwide. This strict association has cv. Chardonnay vine exhibiting symptoms of grapevine leafroll dis-
been further affirmed by transmission experiments using graft ease characteristic for white-­fruited cultivars. (Cour­tesy M. Fuchs)
inoculations, vector transmissions, and heat therapy sanitation.
Taxonomically, all five GLRaVs are classified in the family
Closteroviridae, characterized by large, flexuous rod-­shaped with the exception of some genetic variants of GLRaV-­2, can
particles with lengths ranging from 1250 to 2200 nm; a genome be detected in a 2-­year field and/or a 2-­to 3-­month greenhouse
size ranging from 13,696 nucleotides (nt) encoding seven open indexing of candidate sources through the use of V.  vinifera
reading frames to one of 18,498 nt encoding 13 open reading cvs. Cabernet Franc or Pinot Noir as indicators. Alternatively,
frames; and coat protein size classes of either 26 or 35 to 39 laboratory-­based tests such as enzyme-­linked immunoassay
kDa. Phylogenetically, GLRaVs-­1, 3, and, 4 are classified in the and reverse-­transcription polymerase chain reaction assay are
genus Ampelovirus (vectored by mealybug); GLRaV-­2 in the available with results in 1–2 days.
genus Closterovirus (vectored by aphids); and GLRaV-­7 in the If spread of the viruses transmitted by vectors within or be-
genus Velarivirus (no known vector). GLRaV-­8 is now consid- tween plantings is problematic, roguing, mealybug control, and
ered an erroneously established or invalid virus species. On the sanitation measures can reduce new infections. Removal of
basis of sequence information available to date, the formerly whole blocks should also be considered to control the disease
recognized GLRaV-­5, -­6, -­9, -­Pr, -­De, and -­Car are now re- when disease incidence exceeds a certain threshold, followed
garded as more or less widely divergent variants of GLRaV-­4. by a 2-­year fallow period to manage remnant roots on which
some vector species can be present. Economic thresholds can
Disease Cycle and Epidemiology be developed to help identify the best control options for indi-
GLRaVs have been widely disseminated through the propa- vidual vineyard blocks and devise optimal profit-­maximizing
gation of infected plant material. However, in some viticulture management strategies.
regions, natural spread also is evident locally. Experimentally,
transmissions have been demonstrated with scale insects (GL- Selected References
RaV-­1 by Pulvinaria innumnerabilis, P. vitis, and Parthenole-
canium corni; and GLRaV-­3 by P. innumnerabilis and P. vitis) Almeida, R. P. P., Daane, K. M., Bell, V. A., Blaisdell, G. K., Cooper,
and mealybugs (GLRaV-­1 by Heliococcus adenostomae and M. L., Herrbach, E., and Pietersen, G. 2013. Ecology and manage-
ment of grapevine leafroll disease. Front. Microbiol. 4:94.
Phenacoccus aceris; GLRaV-­3 by H. adenostomae, P. aceris,
Al Rwahnih, M., Dolja, W.  V., Daubert, S., Koonin, E.  V., and
Planococcus citri, Pl. ficus, Pseudococcus calceolariae, Ps. Rowhani, A. 2012. Genomic and biological analysis of Grapevine
comstocki, Ps. longispinus, Ps. maritimus, and Ps. viburni; and leafroll-­associated virus 7 reveals a possible new genus within the
GLRaV-­4 by Pl. ficus and Ps. longispinus). family Closteroviridae. Virus Res. 163:302-­309.
Atallah, S. S., Gomez, M. I., Fuchs, M. F., and Martinson, T. E. 2012.
Management Economic impact of grapevine leafroll disease on Vitis vinifera
The best control option is to propagate planting materials cv. Cabernet franc in Finger Lakes vineyards of New York. Am. J.
using only sources testing negative for GLRaVs. All GLRaVs, Enol. Vitic. 63:73-­79.

119
Belli, G., Fortusini, A., Casati, P., Belli, L., Bianco, P. A., and Prati, S.
1994. Transmission of a grapevine leafroll associated closterovirus
Grapevine leafroll-­associated virus 2
by the scale insect Pulvinaria vitis L. Riv. Patol. Veg. 4:105-­108.
Bertazzon, N., Borgo, M., Vanin, S., and Angelini, E. 2010. Genetic
and Graft Incompatibility
variability and pathological properties of Grapevine leafroll-­
associated virus 2 isolates. Eur. J. Plant Pathol. 127:185-­197. The involvement of a viral agent or agents, including Grape-
Daane, K. M., Almeida, R. P. P., Bell, V. A., Walker, J. T. S., Botton, M., vine leafroll-­associated virus 2 (GLRaV-­2), in graft incompat-
Fallahzadeh, M., Mani, M., Miano, J. L., Sforza, R., Walton, V. M., ibility and young vine decline was suspected in France and
and Zaviezo, T. 2012. Biology and management of mealybugs in Italy in the early 1990s. In California, failure of the AXR#1
vineyards. Pages 271-­307 in: Arthropod Management in Vine- rootstock to control a new strain of the grape phylloxera (Dak­
yards: Pests, Approaches, and Future Directions. N. J. Bostanian, tulosphaira vitifoliae), first recognized in the mid-­1980s, led
C. Vincent, and R. Isaacs, eds. Springer Science, Berlin, Germany. to wide-­scale replantings in winegrape vineyards where it
Fazeli, C. F., and Rezanian, M. A. 2000. Nucleotide sequence and or- had formerly predominated, employing alternative rootstocks
ganization of ten open reading frames in the genome of grapevine with higher levels of phylloxera resistance. However, whereas
leafroll-­associated virus 1 and identification of three subgenomic AXR#1 tolerated latent viruses, infected scions grafted onto
RNAs. J. Gen. Virol. 81:605-­615.
certain phylloxera-­ resistant rootstocks declined soon after
Gambino, G., and Gribaudo, I. 2006. Simultaneous detection of nine
grapevine viruses by multiplex reverse transcription-­polymerase
transplanting. One graft-­ incompatible-­
associated agent was
chain reaction with coamplification of a plant RNA as internal con- later characterized. Initially called Grapevine rootstock stem
trol. Phytopathology 96:1223-­1229. lesion-­associated virus, it is now referred to as GLRaV-­2 strain
Ghanem-­Sabanadzovic, N.  A., Sabanadzovic, S., Gugerli, P., and Red Globe (GLRaV-­2 RG). In parallel, additional distinct, ge-
Rowhani, A. 2012. Genome organization, serology and phylogeny netically related GLRaV-­2 variants associated with graft in-
of Grapevine leafroll-­associated viruses 4 and 6: Taxonomic impli- compatibility also were described.
cations. Virus Res. 163:120-­128.
Goheen, A. C., Harmon, F. N., and Weinberger, J. H. 1958. Leafroll Symptoms
(white Emperor disease) of grapes in California. Phytopathology In bench grafts of GLRaV2 RG-­infected scions onto sensitive
48:51-­54. rootstocks, disease symptoms consist of weak plant growth,
Golino, G. A., Sim, S., Gill, R., and Rowhani, A. 2002. California stunted shoots, and leaves with early fall color. The unions are
mealybugs can spread grapevine leafroll disease. Calif. Agric. enlarged and the majority of affected plants succumb during
56:196-­201. the growing season. On virus-­insensitive rootstocks such as
Gugerli, P., Brugger, J.-­J., and Bovey, R. 1984. L’enroulement de la
Freedom and 101-­14 Mtg, where the infections are latent, in-
vigne: Mise en évidence de particules virales et développement
d’une méthode immuno-­enzymatique pour le diagnostic rapide. fected plants develop normal unions (Fig. 230) and canopies.
Rev. Suisse Vitic. Arboric. Hortic. 16:299-­304. In 2-­year-­old test plants of Cabernet Sauvignon propa-
Harmon, F. N., and Snyder, E. 1946. Investigations on the occurrence, gated on different phylloxera-­resistant rootstocks and graft-­
transmission, spread, and effect of “white” fruit color in the Em- inoculated with GLRaV-­2 RG, the canopies developed a similar
peror grape. Proc. Am. Soc. Hortic. Sci. 47:190-­194. reddish color a year later (Fig. 231), and in dormancy several
Jarugula, S., Alabi, O. J., Martin, R. R., and Naidu, R. A. 2010. Ge- symptomatic plants died. A few surviving plants produced
netic variability of natural populations of Grapevine leafroll-­ weak shoot growth and reddish, small leaves in the next grow-
associated virus 2 in Pacific Northwest vineyards. Phytopathology ing season (Fig. 232). Survivor plants on rootstock Kober 5BB
100:698-­707. developed small, discrete necrotic lesions on the rootstock por-
Jelkmann, W., Mikona, C., Turturo, C., Navarro, B., Rott, M. E., Men- tion, whereas survivors on rootstock 3309C developed more
zel, W., Saldarelli, P., Minafra, A. and Martelli, G. P. 2012. Molecu- extensive lesions. Lesion development required two growing
lar characterization and taxonomy of grapevine leafroll-­associated seasons.
virus 7. Arch. Virol. 157:359-­362.
The mechanistic interaction between GLRaV-­2 RG and the
Maree, H. J., Almeida, R. P. P., Bester, R., Chooi, K-­M., Cohen, D.,
Dolja, V. V., Fuchs, M. F., Golino, D. A., Jooste, A. E. C., Martelli,
sensitive rootstocks resembles a girdling effect at the scion/
G. P., Rayapati, N., Rohawni, A. K., Saldarelli, P., and Burger, J. T.
2013. Grapevine leafroll-­associated virus 3. Front. Microbiol. 4:82.
Martelli, G.  P., Agranovsky, A.  A., Bar-­Joseph, M., Boscia, D.,
Candresse, T., Coutts, R.  H.  A., Dolja, V.  V., Falk, B.  W.,
Gonsalves,  D., Jelkmann, W., Karasev, A.  V., Minafra, A.,
Namba, S., Vetten, H. J., Wisler, G. C., and Yoshikawa, N. 2002.
The family Closteroviridae revised. Arch. Virol. 147:2039-­2044.
Martelli, G. P., Abou Ghanem-­Sabanadzovic, N., Agranovsky, A. A.,
Al Rwahnih, M., Dolja, V. V., Dovas, C. I., Fuchs, M., Gugerli, P.,
Hu, J. S., Jelkmann, W., Katis, N. I., Maliogka, V. I., Melzer, M. J.,
Menzel, W., Minafra, A., Rott, M. E., Rowhani, A., Sabanadzovic, S.,
and Sladarelli, P. 2012. Taxonomic revision of the family Clostero-
viridae with special reference to the Grapevine leafroll-­associated
members of the genus Ameplovirus and the putative species unas-
signed in the family. J. Plant Pathol. 94:7-­19.
Sforza, R., Boudon-­Padieu, E., and Greif, C. 2003. New mealybug
species vectoring Grapevine leafroll-­associated viruses-­1 and -­3
(GLRaV-­1 and -­3). Eur. J. Plant Pathol. 109:975-­981.
Thompson, J.  R., Fuchs, M., and Perry, K. 2012. Genomic analysis
of Grapevine leafroll-­associated virus-­5 and related viruses. Virus
Res. 163:19-­27.
Fig. 230. Specimens of Red Globe scions infected with GLRaV-­2
Tsai, C-­W., Rowhani, A., Golino, D. A., Daane, K. M., and Almeida, RG bench-­grafted onto two acutely sensitive and two insensitive
R.  P.  P. 2010. Mealybug transmission of grapevine leafroll vi- rootstocks. Rootstocks 5BB (far left) and 3309C (second from
ruses: An analysis of virus–vector specificity. Phytopathology left) with enlarged unions and necrotic fissures (rootstock 3309C
100:830-­834. also with severe stem necrosis); rootstocks Freedom (second
from right) and 101-­14 Mgt (far right) with normal woody cylinders.
(Prepared by A. Rowhani and P. Gugerli) (Cour­tesy J. K. Uyemoto)

120
rootstock junction, owing in part to completely reddened leaves GLRaV-­2 RG causes latent infections in the standard virus dis-
throughout the canopy. Cabernet Sauvignon scions die when ease indicators used in grapevine certification programs, e.g.,
bench-­grafted on the acutely sensitive rootstocks 5C, 1103P, it infected but failed to induce observable symptoms in own-­
1616C, 3309C, and Kober 5BB. In contrast, GLRaV-­ 2 RG rooted indicator plants V. vinifera ‘Cabernet Franc’, LN33, and
causes latent infections in the rootstocks O39-­16, 101-­14Mtg, V. rupestris St. George, and on test plants of Cabernet Sauvi-
110R, 140R, 420A, Boerner, Freedom, Harmony, Ramsey, gnon grafted to GLRaV-­2 RG-­insensitive rootstocks.
Schwarzmann, Vitis riparia Gloire, and Vitis rupestris St.
George. Some of these virus-­insensitive test plants, e.g., root- Management
stocks O39-­16, 101-­14Mtg, Freedom, Harmony, and Ramsey, Propagation material should be derived only from pretested,
are devoid of stem lesions. clean sources. GLRaV-­2 RG likely causes latent infections in
In two trials, a common strain of GLRaV-­2 induced typical
leafroll symptoms on the various test plants. All symptomatic
test plants in these trials survived in an apparently robust fash-
ion throughout the 5–8 year duration of the trials.

Causal Agent
GLRaV-­2 RG was first isolated and characterized from an
infected Red Globe grapevine. Molecularly, it shares 74% se-
quence homology with other GLRaV-­2 strains classified in the
genus Closterovirus, family Closteroviridae. Members in this
virus family have a genome organization consisting of 9 open
reading frames and a coat protein subunit size of 22 to 25 kDa.
Furthermore, the coat protein of GLRaV-­2 RG cross-­reacts
with GLRaV-­2 antiserum in western blot assays, confirming
the virus relationship and demonstrating it as a molecular and
biological variant.
Four GTAs in addition to GLRaV-­2 RG have been found to
cause stem lesions on selective grapevine rootstocks. Source
GTA-­1 induced red foliage 1 year post-­inoculation in test plants
of Cabernet Sauvignon propagated on the rootstocks 101-­14
Mtg, 3309C, and Freedom. Only test plants on 101-­14 Mtg sur-
vived dormancy; when these were later sacrificed and bark re-
moved, the rootstock stems contained scattered, discrete small
necrotic lesions (Fig. 233). Bud grafts on other test plants devel-
oped typical leafroll symptoms and did not decline. Test plants
developed stem lesions or were killed when on rootstock 5C
inoculated with source GTA-­2; on Harmony, 5BB and 1616C
rootstocks inoculated with source GTA-­3; and on rootstock
5BB inoculated with GTA-­4. Attempts are underway to char- Fig. 232. Reddish mottled leaves and weak
acterize the unknown GTAs. spring growth of cv. Cabernet Sauvignon sci-
ons on 3309C rootstocks 2 years after chip-­bud
Disease Cycle and Epidemiology inoculation with GLRaV-­2 RG. (Cour­tesy J.  K.
Uyemoto)
Although first discovered in the table grape cv. Red Globe,
about 20% of samples collected from diseased wine grape
cultivars in various California viticulture regions also tested
positive for GLRaV-­2 RG. Propagation with infected source
material is likely the principal method of virus dissemination.

Fig. 233. Discrete stem lesions produced on rootstock 101-­14 Mtg

Fig. 231. Test plants of cv. Cabernet Sauvignon scions on 3309C (right) graft inoculated with an unknown transmissible agent ca-
rootstocks 1 year after chip-­bud inoculation with GLRaV-­2 RG; pable of inducing graft-­incompatibility symptoms similar to those
two of these plants did not survive through the following dormant on sensitive rootstocks inoculated with GLRaV-­ 2 RG; healthy
season. (Cour­tesy J. K. Uyemoto) plant is on the left. (Cour­tesy J. K. Uyemoto)

121
most scions and rootstocks, and therefore virus contamination Sonoma counties, diseased vineyards have also been found in
is difficult to assess visually. Source plants may be assayed by the central coast and San Joaquin Valley regions of California;
RT-­PCR or graft-­indexed using indicator plants of Cabernet in the states of Arizona, Arkansas, Georgia, Maryland, New
Sauvignon propagated on virus-­sensitive rootstocks 5BB, 5C, York, North Carolina, Oregon, Pennsylvania, Texas, Virginia,
1103P, 1616C, or 3309C. and Washington; and in the provinces of British Columbia and
Ontario, Canada. This widespread distribution of the virus was
Selected References determined through surveys in North America during the 2012
and 2013 growing seasons, and it seems likely that the disease
Bertazzon, N., Borgo, M., Vanin, S., and Angelini, E. 2010. Genetic will be confirmed in many additional locations as further in-
variability and pathological properties of Grapevine leafroll-­
vestigations continue. The occurrence of red blotch outside of
associated virus 2 isolates. Eur. J. Plant Pathol. 127:185-­197.
Bertazzon, N., Borgo, M. and Angelini, E. 2010. The complete ge- North America has not yet been reported, although plant mate-
nome sequence of the BD variant of grapevine leafroll-­associated rial introduced to the United States from abroad was found to
virus 2. Arch. Virol. 155:1717-­1719. be infected.
Greif, C., Garau, R., Boscia, D., Prota, V.  A., Fiori, M., Bass, P.,
Walter, B., and Prota, U. 1995. The relationship of grapevine Symptoms
leafroll-­associated closterovirus 2 with a graft incompatible condi- Grapevines of various ages (2–25 years old) have been found
tion of grapevines. Phytopathol. Mediterr. 34:167-­173. exhibiting red blotch symptoms. Disease symptoms generally
Martelli, G.  P., Agranovsky, A.  A., Bar-­ Joseph, M., Boscia, D., start appearing in late August through September as irregular
Candresse, T., Coutts, R. H. A., Dolja, V. V., Falk, B. W., Gonsalves, D., red blotches on leaf blades located on basal portions of shoots,
Jelkmann, W., Karasev, A. V., Minafra, A., Namba, S., Vetten, H. J., either between secondary or tertiary veins (Fig. 234) or extend-
Wisler, G. C., and Yoshikawa, N. 2002. The family Closteroviridae ing from the leaf margin (Fig. 235). The veins of affected leaves
revised. Arch. Virol. 147:2039-­2044. can turn partly or fully red (Fig. 236). Occasionally, reddening
Meng, B., Li, C., Goszczynski, D., and Gonsalves, D. 2005. Ge- of the leaf blade in the interveinal zones between secondary
nome sequence and structure of two biologically distinct strains of
Grapevine leafroll-­associated 2 and sequence analysis. Virus Genes
31:31-­41.
Uyemoto, J. K., Rowhani, A., Luvisi, D., and Krag, C. R. 2001. New
closterovius in ‘Redglobe’ grape causes decline of grafted plants.
Calif. Agric. 55(4):28-­31.
Uyemoto, J.  K., and Rowhani, A. 2003. Discovery of different
grapevine sources with graft-­transmissible agents causing union-­
incompatibility on sensitive rootstocks. Pages 139-­140 in: Proc. 14
Meeting, International Council for the Study of Virus and Virus-­like
Diseases of the Grapevine (ICVG). http://web.pppmb.cals.cornell.
edu/fuchs/icvg/data/2003Session45.pdf

(Prepared by J. K. Uyemoto and A. Rowhani)

Grapevine Red Blotch

Grapevine red blotch disease was first recognized in 2008 in
vineyards in Napa County, California. The name “red blotch”
was given to distinguish disease symptoms from those caused Fig. 235. Symptoms of red blotch extending in-
by leafroll viruses and other graft-­ transmissible agents in- ward from the margins on a leaf of cv. Carignane.
volved in graft union disorders on red-­fruited V. vinifera cul- (Cour ­tesy M. Fuchs)
tivars, as well as those caused by various injuries to trunks
and shoots. In addition to north coast vineyards in Napa and

Fig. 236. Symptoms of red blotch on the under-

side of a cv. Cabernet Sauvignon leaf, including
Fig. 234. Symptoms of red blotch on a leaf of cv. reddening of primary and secondary veins and
Cabernet Franc. (Cour­tesy M. Fuchs) the petiole. (Cour­tesy M. Fuchs)

122
Fig. 237. Interveinal reddening on the leaf blade of a cv. Pinot Noir
vine infected with Grapevine red blotch-­associated virus, similar
to certain symptoms caused by leafroll-­associated viruses. (Cour­
Fig. 238. Symptoms on the leaf blade of a cv.
tesy M. Fuchs)
Cabernet Franc vine infected with a leafroll-­
associated virus, easily confused with red blotch
symptoms. (Cour­tesy M. Fuchs)

veins (Fig. 237) may resemble certain symptoms of grapevine

leafroll disease (Fig. 238), with which red blotch has sometimes Disease Cycle and Epidemiology
been confused. However, in contrast with leafroll disease, the The primary source of inoculum appears to be infected
margins of red blotch-­affected leaves do not roll downward. planting material. Disease incidence has exceeded 90% in
To date, disease symptoms have been observed in vineyards of several vineyards surveyed and secondary spread is suspected
V. vinifera cultivars Cabernet Franc, Cabernet Sauvignon, Mal- in some situations. The Virginia creeper leafhopper (Erythro-
bec, Merlot, Mourvèdre, Petite Sirah, Petit Verdot, Pinot Noir, neura ziczac Walsh) is reported to transmit GRBaV from vine
and Zinfandel. Infections of white V. vinifera cultivars such as to vine in the greenhouse. The role of this and other potential
Chardonnay, Riesling, Semillon, and Viognier also have been insect vectors in transmitting GRBaV in vineyards has yet to be
detected, but disease symptoms on them are less conspicuous. determined. GRBaV is graft transmissible but is not likely to be
Red blotch symptoms may appear earlier (mid-­to late June) in seedborne, as there is no evidence for seed transmission of any
the season in some cultivars (e.g., Cabernet Franc and Merlot) other members of the family Geminiviridae.
than others (e.g., Cabernet Sauvignon). Severity of red blotch
symptoms may also vary from year to year. Management
The most significant impact of red blotch is on the accumu- The occurrence of red blotch disease may be difficult to as-
lation of total soluble solids (°Brix), which can be as much as sess visually owing to symptomatic similarities with grapevine
4–5 units lower in fruit from diseased vines than in fruit from leafroll disease and deficiencies of certain nutrients, such as po-
healthy vines. Also, fruit from affected grapevines exhibit in- tassium. Therefore, vines should be assayed by PCR. Diseased
creased acidity. It is not yet established whether red blotch dis- grapevines should be replaced with healthy vines derived from
ease has any effect on vine vigor or fruit yield. clean, certified virus-­tested stocks.
Causal Agent Selected References
Although red blotch symptoms have sometimes been con-
fused with those caused by nutritional deficiencies, stress, or Al Rwahnih, M., Dave, A., Anderson, M. M., Rowhani, A., Uyemoto,
other infectious agents such as viruses associated with leafroll J.  K., and Sudarshana, M.  R. 2013. Association of a DNA virus
disease, independent studies using rolling circle amplification with grapevines affected by red blotch disease in California. Phyto­
and deep sequencing have identified a previously unknown pathology 103:1069-­1076.
virus, now named Grapevine red blotch-­ associated virus Krenz, B., Thompson, J. R., Fuchs, M., and Perry, K. L. 2012. Com-
(GRBaV), in vines exhibiting red blotch symptoms. (This virus plete genome sequence of a new circular DNA virus from grape-
was initially reported as Grapevine cabernet franc-­associated vine. J. Virol. 86:7715.
virus). GRBaV has a circular, single-­stranded DNA genome Poojari, S., Alabi, O.  J., Fofanov, V.  Y., and Naidu, R.  A. 2013. A
leafhopper-­transmissible DNA virus with novel evolutionary lin-
and is proposed to be a member of the family Geminiviridae.
eage in the family Geminiviridae implicated in grapevine redleaf
Based on the GRBaV genome sequence information, a PCR test disease by next-­generation sequencing. PLoS ONE 8:e64194.
was developed for accurate diagnosis, and by means of this test, Sudarshana, M.  R., and Wolpert, J.  A. 2012. Grapevine red blotch
the virus has been detected consistently in grapevines exhibit- disease. UC Cooperative Ext. Fact Sheet. http://ucanr. edu/sites/
ing red blotch symptoms. Recently, GRBaV was proven to be viticulture-­fresno/files/157139.pdf
the cause of this disease through inoculation studies utilizing
Agrobacterium tumefaciens. (Prepared by M. Sudarshana and M. Fuchs)

123
 Nematode-­transmitted GFLV and several of the other grapevine-­infecting European
nepoviruses have distorting and chromogenic strains and may
Virus Diseases occur in mixed infections. Their economic impact varies with
the tolerance of the cultivar to the viruses. Tolerant cultivars
produce moderately good crops. In contrast, sensitive culti-
vars are severely affected, showing progressive vine decline,
European Nepoviruses and low yields (up to 80% losses) with poor fruit quality, shortened
Strawberry latent ringspot virus productive life of the vineyard, a low proportion of graft take,
reduced rooting ability of propagation material, and decreased
tolerance of adverse climatic factors.
Several nepoviruses and Strawberry latent ringspot virus
(SLRSV) infect grapevines in Europe, causing degenerative Symptoms
diseases (collectively termed infectious degeneration) whose Infectious degeneration is characterized by two distinct syn-
symptoms are similar to or indistinguishable from those dromes, infectious malformation and yellow mosaic, caused
of fanleaf degeneration induced by Grapevine fanleaf virus by different strains of the causal agents. Infectious malforma-
(GFLV). Fanleaf is the oldest known virus disease of V. vinif- tion is a syndrome induced by distortion-­causing strains of the
era. Its name comes from the peculiar malformation of in- virus. Affected leaves are variously and severely distorted, and
fected leaves, which exhibit widely open petiolar sinuses and may be asymmetrically shaped, puckered, and/or exhibit open
abnormally gathered primary veins that produce an appear- petiolar sinuses, deep lobes, and acute denticulations (Figs. 239
ance resembling that of an open fan (Fig. 239). In European and 240). Chlorotic mottling may accompany these deforma-
literature, records of this disease date back some 200 years, tions (Figs. 241, 242, and 243). Foliar symptoms develop early
and grapevine leaves with typical symptoms were found in in the spring and persist throughout the vegetative season, be-
herbaria established before the introduction of American root- coming less distinct in summer. Shoots also are malformed,
stock hybrids. The consensus is that fanleaf degeneration may showing abnormal branching, double nodes, short internodes,
have existed in the Mediterranean Basin and the Near East fasciations, and zigzag growth. Fruit clusters are smaller and
since the earliest time of grape cultivation. Now the disease is fewer in number, and berries ripen irregularly and are small
known to occur worldwide. and set poorly (Fig. 244).
Yellow mosaic is induced by chromogenic virus strains.
Leaves of infected grapevines develop bright chrome-­yellow

Fig. 239. Fan-­shaped and denticulated leaves of a cv. Montepul-

ciano vine infected with Grapevine fanleaf virus. (Cour­tesy G. P.
Fig. 241. Mottled leaf infected by Grapevine fanleaf virus. (Cour­
Martelli)
tesy G. P. Martelli)

Fig. 240. Fan-­shaped leaf of a cv. Sylvaner vine infected by Straw- Fig. 242. Mottling and malformations induced by Arabis mosaic
berry latent ringspot virus. (Cour­tesy M. Fuchs) virus in a leaf of cv. Zirock. (Cour­tesy M. Fuchs)

124
discolorations early in the spring that may also affect stems,
tendrils, and inflorescences. Chromatic alterations of the leaves
vary from a few scattered, yellow spots that sometimes appear
as rings or lines, to extensive mottling of the veins and/or in-
terveinal areas, to a typical yellowing of most or all of the leaf
blade (Fig. 245). Often, infected grapevines occur in patches
(Fig. 246) that are easily seen from a distance. The foliage
and shoots show little if any malformation, but fruit clusters
and berries are small and few. With increased ambient tem-
peratures during summer, the chlorosis fades rapidly and the
canopy develops a normal green color.
“Vein banding” is a disease characterized by chrome-­
yellow flecks first localized along the main veins of mature
leaves and progressing into the interveinal areas (Fig. 247).
The discolorations appear in mid-­to late summer in a lim-
ited number of leaves, which show little malformation. Fruit
set is poor, clusters are straggly, and the yield may be virtu-
ally zero. This disorder was first reported from California as
a syndrome ascribed to a specific strain of GFLV. More re-
cently, however, vein banding symptoms were demonstrated
to be induced by a co-­infection by Grapevine yellow speckle
viroid and GFLV.
Trabeculae, or endocellular cordons, are diagnostic of grape-
vines infected by GFLV. These are radial bars crossing the
lumen of epidermal, parenchyma, phloem, and xylem cells,
and they are made up of pectic cores surrounded by cellulose Fig. 245. Typical yellow mosaic symptoms in-
sheaths encrusted with lignin, suberin, or cutin, depending duced by a chromogenic strain of Grapevine
on the tissue in which they form. These structures are readily fanleaf virus. (Cour­tesy G. P. Martelli)

Fig. 246. Patchy distribution of grapevines infected with a chromo-

Fig. 243. Mottled leaf of cv. Chardonnay infected by the grape-
genic strain of Grapevine fanleaf virus. (Cour­tesy G. P. Martelli)
vine strain of Raspberry ringspot virus. (Cour­tesy M. Fuchs)

Fig. 244. Healthy fruit of Cabernet Sauvignon (left) compared Fig. 247. Vein-­banding symptoms in a leaf of cv. Sultanina dou-
with fruit from a vine infected with Grapevine fanleaf virus (right). bly infected with Grapevine fanleaf virus and Grapevine yellow
(Reproduced from Raski et al., 1983) speckle viroid 1. (Cour­tesy G. P. Martelli)

125
visible by light microscopy in lignified shoots, especially in the Nepoviruses of subgroup B. TBRV is distantly related se-
basal internodes. rologically to GCMV. RNA-­1 has 7356 nt and RNA-­2 4662 nt.
TBRV supports the replication of a satellite RNA with 1327
Causal Agents nt. Joannes Seyve virus, known to cause a severe disease of
With one proposed exception, all recognized causal agents cv. Joannes Seyve in Ontario, Canada, is a strain of this virus.
of degenerative diseases are members of the genus Nepovirus TBRV was first recorded from grapevines in Germany, and
belonging to one of three subgroups, discussed below. They are then occasionally in former Yugoslavia, Greece, Israel, Turkey,
subgroup A (GFLV, Arabis mosaic virus [ArMV], Raspberry and Ontario.
ringspot virus [RpRSV], and the newly described Grapevine GCMV is serologically distantly related to TBRV. RNA-­1
deformation virus [GDefV]); subgroup B (Tomato black ring has 7212 nt and RNA-­2 4441 nt. GCMV was first found in Hun-
virus [TBRV], Grapevine chrome mosaic virus [GCMV], and gary, near Lake Balaton, and was originally called Hungarian
a newly described virus from Turkey denoted Grapevine Ana- chrome mosaic virus. It occurs also in former Czechoslovakia,
tolian ringspot virus [GARSV]); and subgroup C [Cherry lea- Croatia, and Austria.
froll virus (CLRV)]. Strawberry latent ringspot virus (SLRSV), GARSV is not serologically related to any of the known
also discussed below, is an unassigned species in the family grapevine nepoviruses but is phylogenetically related to TBRV
Secoviridae. These viruses have polyhedral particles about 30 and GCMV. RNA-­1 has 7286 nt and RNA-­2 has 4607 nt.
nm in diameter with a positive-­sense, single-­stranded RNA ge- GARSV has no recognized vector, is not seedborne, and has
nome existing as two functional species (RNA-­1 and RNA-­2), been reported from southeastern Turkey and Iran.
both being required for infectivity and separately encapsidated. Nepovirus of subgroup C. CLRV is not serologically re-
Virus preparations sediment as three centrifugal components: lated to any of the other known nepoviruses. RNA-­1 has 7918
component T, made up of empty protein shells; component nt and RNA-­2 has 6360 nt. The virus is transmitted through
M, containing 27–31% RNA-­2; and component B, containing seeds and pollen in walnut, but whether these types of trans-
38–43% RNA-­1. Except for SLRSV, which has capsid protein mission operate in grapevines is unknown. Grapevine infection
subunits of two sizes (27 and 43 kDa, respectively), all other by CLRV has been reported in Chile, Poland, and Germany.
viruses have subunits of a single size, 52–57 kDa. Strawberry latent ringspot virus. SLRSV, a virus serologi-
Individual viruses can be identified by biological assays (dif- cally unrelated to all known nepoviruses, was recently clas-
ferential reactions on an herbaceous host range) and labora- sified as an unassigned species in the family Secoviridae. Its
tory tests. ELISA using polyclonal antisera and/or monoclonal RNA-­1 has 7496 nt and RNA-­2 has 3824 nt. SLRSV supports
antibodies, when available, is rapid, inexpensive, and reliable. the replication of a satellite RNA with 1118 nt. SLRSV has been
The best antigen sources for serological diagnosis are leaves recovered from grapevines in the Palatinate (Germany) and in
collected in spring or cortical shavings from mature dormant northern Italy and was also detected occasionally in other Eu-
canes. Molecular assays using radioactive or digoxigenin-­ ropean countries and Turkey.
labelled probes, reverse transcription-­polymerase chain reac-
tion (RT-­PCR), and immunocapture RT-­PCR are becoming Disease Cycle and Epidemiology
increasingly popular. RT-­PCR is estimated to be four-­to sixfold Most of the grapevine-­infecting European nepoviruses are
more sensitive than ELISA. transmitted from grapevine to grapevine by nematodes be-
Nepoviruses of subgroup A. GFLV was the first grapevine longing to the Longidoridae family. GFLV is transmitted by
virus to be recovered by mechanical inoculation and to be Xiphinema index. A single brief feeding on an infected plant
thoroughly characterized physico-­chemically and molecularly. is sufficient for virus acquisition. In nature, X. index acquires
RNA-­1 has 7342 nt and RNA-­2 has 3774 nt. Virus populations GFLV only from roots of infected grapevines (Fig. 248), and
are antigenically uniform and occur as families with minor retains it for up to 4 years in the absence of host plants or up
molecular variants. A satellite RNA with 1114 nt is associated to 3 months when the nematode feeds on virus-­immune host
with some isolates. GFLV has been disseminated extensively plants. The virus is retained in the cuticular lining of the
via infected grapevines and now occurs worldwide. esophageal lumen of the vector. Adults and juvenile stages of
ArMV is serologically related to GFLV. Its RNA-­1 is 7334 nt X. index can transmit the virus experimentally. Specific trans-
in size and there are two types of RNA-­2 molecules differing mission by X. index is determined by the viral coat protein. The
slightly in size (3711 and 3852 nt). ArMV supports the replica- sequence determining viral transmission consists of a stretch of
tion of two satellite RNAs, a linear form 1104 nt and a circular 11 conserved amino acids located in an exposed region of the
model about 350 nt in size. Although cross-­protection between coat protein.
ArMV and GFLV has been reported, these viruses often occur
in mixed infections in certain areas of central Europe and
with other nepoviruses in western Germany. ArMV was also
recorded from grapevines in Switzerland, Bulgaria, former
Yugoslavia, Hungary, Romania, Turkey, Israel, Canada, USA
(California and Missouri), France, and Japan.
Serologically, the grapevine strain of RpRSV is very dis-
tantly related to the two main serotypes, Scottish and English,
and it differs from the type strain because it sediments as a
single centrifugal component. These differences suggest that
grapevine-­infecting RpRSV may be a different virus species.
RNA-­1 has 7935 nt and RNA-­2 has 3928 nt. RpRSV occurs
as two different strains of different virulence in the Palatinate
(western Germany), where harvests of infected grapevines can
be reduced by more than 30%.
GDefV is distantly related serologically to ArMV but not
to GFLV, the two viral species from whose recombination it
originated. RNA-­1 contains 7386 nt and RNA-­2 contains 3753
nt. GDefV has no recognized vector, is not seedborne, and has Fig. 248. Xiphinema index nematodes feeding on a grapevine root.
been reported only from southeastern Turkey. (Cour­tesy G. P. Martelli)

126
 ArMV and SLRSV are transmitted by Xiphinema diver- Host resistance to GFLV and to X. index has been identified
sicaudatum. As with GFLV, both viruses are retained in the in some eastern V. vinifera cultivars and in Muscadinia or Vitis
esophageal lumen of the vectors. Their particles apparently species other than V. vinifera. Work is under way in different
attach to a discontinuous layer of carbohydrates that lines the laboratories to create resistant rootstocks or cultivars through
nematode’s odontophore (the posterior portion of the stylet) and traditional breeding methods or genetic transformation tech-
esophagus, from which they dissociate when secretions of the nology. Various rootstocks have been successfully transformed
esophageal glands are regurgitated during the first phases of with the coat protein gene of GFLV, ArMV, and GCMV for
feeding on plant roots. induction of resistance and are currently under evaluation.
The grapevine strain of RpRSV is transmitted by Paralongi- Combining a careful selection of planting materials with vine-
dorus maximus, whereas the vectors of TBRV to grapevine are yard sanitation practices provides a powerful tool for reducing
Longidorus attenuatus in Germany and L. elongatus in Can- or altogether avoiding the introduction of degenerative diseases
ada. Although field association between GCMV and Xiphinema into new vineyards. Healthy stocks planted in nematode-­free
vuittenezi has been reported and virus particles were detected soil or soil with populations of nonviruliferous vectors remain
by immunosorbent electron microscopy in X. index that had fed healthy for the productive life of the vineyard. Relative to those
on infected hosts, experimental evidence for transmissions of planted with infected stock, vineyards established with GFLV-­
GCMV by either nematode species has not been obtained. free stocks are very homogeneous in morphology and produc-
Short-­distance spread of all grapevine-­infecting nepoviruses is tivity, grape yields are improved by 40–70%, berries contain
dependent on their vectors. For instance, the yellow mosaic strain more sugar, and the wine is of better quality. Virus elimination
of GFLV may be spread in the field to a distance of 1.3–1.5 m per is readily achieved from vegetative shoot tips by heat treatment
year by nematodes. Although pollenborne, GFLV is rarely trans- (38–40°C for 4 weeks), in vitro meristem tip culture, micro-
mitted through grape seeds. It has been recorded from naturally grafting, or somatic embryogenesis, providing healthy source
infected weeds (Aristolochia clematis, Lagenaria siceraria var. material for subsequent multiplication and propagation.
turbinata, and more recently, Cynodon dactylon and Polygonum
aviculare), but the importance of such infections in the epide- Selected References
miology of disease on grapevines is not known. GCMV is seed-
borne, though at a very low rate, and ArMV, SLRSV, TBRV, and Andret-­Link, P., Schmitt-­Keichinger, C., Demangeat, G., Komar, G.,
RpRSV have alternative hosts, which may facilitate virus sur- and Fuchs, M. 2004. The specific transmission of Grapevine fan-
vival, representing a factor to consider in disease epidemiology. leaf virus by its nematode vector Xiphinema index is solely deter-
However, the primary source of GFLV and nematode acquisition mined by the viral coat protein. Virology 320:12-­22.
is root tissue of infected grapevines. Infected grapevine roots can Demangeat, G., Voisin, R., Minot, J. C., Bosselut, N., Fuchs, M., and
remain undegraded in the soil for many years after removal of Esmenjaud, D. 2005. Survival of Xiphinema index in vineyard soil
and retention of Grapevine fanleaf virus over extended time in the
the mother plants, supporting the reproduction and survival of absence of host plants. Phytopathology 95:1151-­1156.
viruliferous X. index populations during that period. Hewitt, W. B., Goheen, A. C., Raski, D. J., and Gooding, G. V. 1962.
Although none of the grapevine-­ infecting nepoviruses is Studies on virus diseases of grapevine in California. Vitis 3:57-­83.
disseminated over long distances by natural means because of Komar, V., Vigne, E., Demangeat, G., Lemaire, O., and Fuchs, M.
the limited range of vector movement, long-­distance spread is 2008. Cross-­protection as control strategy against Grapevine fan-
achieved through transport of infected propagation material. leaf virus in naturally infected vineyards. Plant Dis. 92:1689-­1694.
Anecdotal evidence suggests that GFLV had long been local- Martelli, G. P. 1978. Nematode-­borne viruses of grapevine, their epi-
ized along with its vector in scattered enclaves in the traditional demiology and control. Nematol. Mediterr. 6:1-­27.
European grape-­growing regions during the era when all vine- Martelli, G. P., ed. 1993. Graft-­transmissible Diseases of Grapevines.
yards were established with own-­rooted plants. The disastrous Handbook for Detection and Diagnosis. FAO Publ. Div., Rome,
dissemination of GFLV in Europe and throughout the world Italy.
began in the late 1800s, a period during which the practice of Mayo, M.  A., Fritsch, C., Leibowitz, M.  J., Palukaitis, P., Scholthof,
grafting scions onto rootstocks to combat the grape phyllox- K. B., Simons, G., and Taliansky, M. 2000. Satellite nucleic acids.
Pages 1028-­1032 in: Virus Taxonomy: 7th Report of the International
era (Daktulosphaira vitifoliae) became commonplace. Many
Committee on Taxonomy of Viruses. M.  H.  V. van Regenmortel,
phylloxera-­ resistant rootstocks were largely asymptomatic C. M. Fauquet, D. H. L. Bishop, E. B. Carstens, M. K. Estes, S. M.
when infected with GFLV and other deleterious viruses, and Lemon, J. Maniloff, M. A. Mayo, D. J. McGeoch, C. R. Pringle and
were unwittingly used to propagate finished plants. R. B. Wichner, eds. Academic Press, San Diego, CA.
Raski, D. J., Goheen, A. C., Lider, L. A., and Meredith, C. P. 1983.
Management Strategies against grapevine fanleaf virus and its nematode vector.
It is virtually impossible to eradicate an established popula- Plant Dis. 67:335-­339.
tion of nematode vectors in vineyard sites. Therefore, several Sanfaçon, H., Wellink, J., LeGall, O., Karasev, A., van der Vlugt, R.,
steps must be taken in the preplanting stages to break the eco- and Wetzel, T. 2009. Secoviridae: A proposed family of plant vi-
logical cycle of the nematode-­virus-­grapevine complex. In re- ruses within the order Picornavirales that combines the families
plant situations, the thorough removal of grapevine roots should Sequiviridae and Comoviridae, the unassigned genera Cheravirus
be attempted in conjunction with prolonged fallow and weed and Sadwavirus, and the proposed genus Torradovirus. Arch. Virol.
control. To reduce nematode vector populations, high rates of 154:889-­907.
soil fumigants have been used. However, fumigants only slow Sanfaçon, H., Iwanami, T., Karasev, A.  V., van der Vlugt, R.,
Wellink, J., Wetzel, T., and Yoshikawa, N. 2012. Secoviridae.
the virus transmission rate in shallow soils, and have largely
Page 881 in: Virus Taxonomy: Classification and Nomenclature of
been ineffective at deep soil sites, especially in clay soils. Thus, Viruses. A.  M.  Q. King, M.  J. Adams, E.  B. Carstens, and E.  J.
in some contaminated sites, soil fumigants offer at best tem- Lefkowitz, eds. Academic Press, San Diego, CA.
porary disease control. Furthermore, the future availability of Szychowski, J.  A., McKenry, M.  V., Walker, M.  A., Wolpert, J.  A.,
fumigants is questionable in many locations as a result of in- Credi, R., and Semancik, J. S. 1995. The vein-­banding disease syn-
creased regulatory control of their use. drome: A synergistic reaction between grapevine viroids and fan-
In France, use of GFLV-­infected grapevines to offer protec- leaf virus. Vitis 34:229-­232.
tion against subsequent infections by ArMV via nematode vec- Taylor, C.  A., and Brown, D.  J.  F. 1997. Nematode Vectors of Plant
tors and vice versa has shown some promise. However, cross Viruses. CAB International, Wallingford, UK.
protection has many limitations and is not applicable against
other unrelated nepoviruses. (Prepared by G. P. Martelli, M. Fuchs, and V. Savino)

127
 North American Grapevine Symptoms
In northeastern North America, ToRSV and TRSV cause
Nepoviruses a disease known as virus-­induced grapevine decline, which
involves extensive damage in own-­rooted vines of V. vinifera
To date, seven nepoviruses have been described in North cultivars (Chardonnay, Mission, and Riesling) and interspecific
American vineyards: Arabis mosaic virus (ArMV); Blueberry hybrids (Baco Noir, Cascade, Chelois, DeChaunac, Dutchess,
leaf mottle virus (BLMoV) [syn. Grapevine Bulgarian latent Ventura, Siegfriedrebe, Vidal Blanc, and Vincent). Although
virus (GBLV)]; Grapevine fanleaf virus (GFLV); Peach ro- cultivars vary in susceptibility, both viruses induce similar dis-
sette mosaic virus (PRMV); Tobacco ringspot virus (TRSV); ease symptoms. The first symptom of infection on an other-
Tomato black ring virus (TBRV); and Tomato ringspot virus wise healthy appearing grapevine consists of leaves on isolated
(ToRSV). However, only ToRSV, TRSV, and PRMV are re- shoots that have chlorotic mottling, oak leaf pattern, and/or ring
garded as North American in origin, whereas the others were spots (Fig. 249). Thereafter, in chronically infected grapevines,
reported previously in Europe and presumably introduced into buds can be killed or injured by low winter temperatures and
North America via infected imports. These viruses cause simi- surviving buds produce characteristically stunted, weak shoot
lar symptoms, i.e., delayed bud burst in the spring accompa- growth (Fig. 250) and small, distorted leaves. Yields are nil or
nied by slow development of shoots and leaves, which may be greatly reduced as fruit clusters are few and berries set poorly
mottled and malformed. With chronic infections, grapevines and ripen unevenly (Fig. 251).
degenerate, decline, and suffer severe yield loss. In North ToRSV also incites diseases known as grapevine yellow vein
American vineyards, GFLV is the predominant nepovirus, fol- in California and grapevine little berry in Maryland, where the
lowed by ToRSV and to a lesser extent TRSV. The occurrence overall symptoms differ markedly from those produced in the
of BLMoV and TBRV has not been described in commercial colder viticultural regions of New York State, Pennsylvania,
vineyards in the past 25 years, PRMV only rarely, and ArMV, and Ontario, Canada. With grapevine yellow vein, symptoms
although present occasionally in California, Missouri, and appear as a general chlorosis on portions of the leaf blade and
Canada, causes limited economic damage. yellow flecks concentrated along leaf veins. In Maryland, in-
fected grapevines do not develop leaf symptoms, although both
diseases reduce fruit set. Furthermore, in conjunction with this
fruit thinning effect and in the absence of severe low tempera-
tures damaging buds during dormancy (e.g., in California), dis-
eased grapevines show increased vegetative vigor, producing
“bull canes” and appearing more robust than healthy ones.
Peach rosette mosaic virus is restricted to Michigan and to
southwestern Ontario, Canada. Other names for disease in-
cited by this virus include grapevine degeneration, grapevine
decline, berry shelling, and delayed budding. PRMV was first
described infecting peach trees, where it causes leaf mosaic
and rosetting of shoots. In infected Concord grapevines (V. ×
labruscana), bud burst is delayed, leaves are malformed and
mottled, shoots are stunted, fruit set is poor, and ripening un-
even (Fig. 252). Affected grapevines generally decline slowly
over a period of several years.
Blueberry leaf mottle virus typically remains latent in cul-
tivars of V. vinifera. When present, symptoms are subtle, con-
sisting of canes with reduced growth and leaves with widened
sinuses. In V. × labruscana cv. Concord, infected vines exhibit
Fig. 249. Foliar symptoms of ToRSV infection in the interspecific
hybrid cv. Cascade. (Cour­tesy J. K. Uyemoto)
delayed bud burst, erratic shoot growth, and fan-­like leaves
(Fig. 253), although these symptoms are largely absent by late
summer and diseased vines do not decline appreciably. Never-
theless, fruit clusters are few, small and poorly set. Seed trans-

Fig. 250. Symptoms of infection by ToRSV in grapevine cv.

Cascade, consisting of a stunted, weak cane and lack of fruit Fig. 251. Berry cluster of the interspecific hybrid
production (right), compared with cane from a healthy plant (left). Le Commandant (Bertille Seyve 2862) infected
(Cour­tesy J. K. Uyemoto) with TRSV. (Cour­tesy M. Fuchs)

128
mission of BLMoV occurs in cv. Concord, producing seedlings Causal Agents
that show leaves with flattened sinuses. All abovementioned viruses belong to the genus Nepovirus
An isolate of Tomato black ring virus was reported from in the family Secoviridae and most have nematode vectors. In
Ontario, Canada, in the interspecific hybrid cv. Chambourcin addition to those already discussed under European nepovi-
(Joannes-­Seyve 26-­205). Infected grapevines exhibited leaf de- ruses, ToRSV is vectored by the dagger nematodes Xiphinema
formity, severe stunting and had few, if any, fruit clusters. In an americanum, X. californicum, and X. rivesi; TRSV by X. amer-
extensive graft-­inoculation trial, chronic symptoms developed icanum; and PRMV by X. americanum and Longidorus diadec-
in V.  labrusca cvs. Dutchess, Elvira, Fredonia, and Vinered; turus. No nematode vector is known for BLMoV.
in the interspecific hybrids Baco 22A, Chambourcin, and LN These nepoviruses are transmissible by mechanical inocula-
33; V. vinifera cv. Mission; and rootstocks 4453, 110R, and V. tion of grapevine leaf extracts to herbaceous host plants, e.g.,
rupestris St. George. Other cultivars and rootstocks developed Chenopodium quinoa. They can also be seedborne in a variety
latent infections or were resistant to the virus. Overall, eight of weed hosts. With the exception of GFLV and ArMV, which
of 10 rootstocks, 11 of 16 V. labrusca cultivars, eight of 10 in- are serologically related, the others are antigenically distinct,
terspecific hybrids, and one of five V.  vinifera cultivars were readily detected and identified by serological assays of extracts
successfully infected. prepared from succulent leaf tissues of grapevines and herba-
Grapevine fanleaf virus is widespread in California and has ceous host plants.
been found in Washington State and Missouri. Arabis mosaic
virus is documented in California, Missouri, and the Canadian Disease Cycle and Epidemiology
provinces of British Columbia, Ontario, and Quebec. For more These viruses are easily disseminated through propagation
information on GFLV and ArMV, see “European Nepoviruses of infected source material, a particular concern with BLMoV,
and Strawberry latent ringspot virus.” TBRV, GFLV, and ArMV, for which latent infections are com-
mon and visual inspections unreliable for detecting contami-
nated candidates. Also, with the possible exception of BLMoV,
various weed hosts can serve as reservoirs for each of the in-
dividual nepoviruses, providing a reservoir source from which
the nematode vector species can acquire and later transmit
them to grapevines. These viruses are commonly seed trans-
mitted and are easily perpetuated in their weed hosts. Weed
hosts of primary concern with ToRSV and PRMV are dande-
lion (Taraxacum officinale); with TRSV, broadleaf plantain
(Plantago major); with TBRV, 24 species in 15 plant families;
and with ArMV, 15 species in 12 plant families.
BLMoV is seedborne in grapevine and C. quinoa. However,
lacking a nematode vector, the epidemiological importance of
such infections in grapevine seedlings is uncertain. The seem-
ingly extensive occurrence of the serologically related GBLV in
Bulgarian vineyards is assumed to be due to vine propagation
from infected, asymptomatic sources.
Although GFLV is the causal agent of a production-­limiting
disease in various vineyard sites in California, it has not yet
posed a worrisome problem in other regions of the United States
or in Canada. Although the virus can be distributed occasion-
ally through infected propagation material, it does not spread
in areas where the nematode vector species, X. index, does not
occur or fails to survive extreme winter temperatures.

Management
Only certified, clean planting stocks should be used when
Fig. 252. Uneven ripening on a vine of cv. Con- establishing new vineyards or replacing missing vines. Some
cord infected with PRMV. (Cour­tesy A. Schilder) resistant scion cultivars and/or rootstocks also are available.
For example, all cultivars of V. labrusca are resistant to ToRSV
and TRSV and certain ones are also resistant to the grapevine
isolate of TBRV. Although several interspecific hybrids are
highly susceptible to ToRSV and TRSV, Aurore (Siebel 5279),
Seyval Blanc, and Vidal 256 appear to be resistant to ToRSV.
Furthermore, susceptible scions may be propagated on the
ToRSV-­resistant rootstocks 5A, 5C, 18-­815, 41B Millardet et de
Grasset, 44-­53 Malegue, 110 Richter, 1616C, Clinton, Sanona,
Shakoka, V. riparia Gloire, and V. rupestris St. George. Host
resistance to GFLV has been identified, albeit not in commer-
cially available cultivars and rootstocks. However, the use of
X. index-­tolerant rootstocks can substantially delay GFLV in-
fection of scions
Assuming the use of clean or resistant planting stock, the
most effective control tactic for these diseases is careful pre-
plant preparation of known infested sites. Large grape roots
should be thoroughly destroyed when replanting previous vine-
Fig. 253. Two diseased leaves with flat sinuses (leaf lobes near yard ground, as they are capable of surviving for several years
petiole) from a BLMoV-­infected cv. Concord grapevine, compared after vine removal and can sustain residual populations of
with a healthy leaf (right). (Cour­tesy J. K. Uyemoto). viruliferous vector nematodes. Nematicides are generally not

129
efficient for disease control due to their inability to reach nema- McKenzie, D. J., Johnson, R. C., and Warner, C. 1996. Incidence of
todes present in deeper layers of the soil. Fallowing for up to a four important viral pathogens in Canadian vineyards. Plant Dis.
10-­year period is recommended for eradication of X. index and, 80:955-­958.
therefore, control of GFLV. However, this practice is difficult to Mekuria, T. A., Gutha, L. R., Martin, R. R., and Naidu, R. A. 2009.
implement for economic reasons. Thorough control of potential Genome diversity and intra-­and interspecies recombination events
virus-­reservoir weed hosts is a necessity. in Grapevine fanleaf virus. Phytopathology 99:1394-­1402.
Milkus, B. N. 2001. Incidence of four NEPO viruses in Missouri vine-
yards. Am. J. Enol. Vitic. 52:56-­57.
Selected References Mountain, W. L., Powell, C. A., Forer, L. B., and Stouffer, R. F. 1983.
Transmission of Tomato ring spot virus from dandelion via seed
Allen, W. R., Van Schagen, J. G., and Eveleigh, E. S. 1982. Transmis- and dagger nematodes. Plant Dis. 67:867-­868.
sion of peach rosette mosaic virus to peach, grape and cucumber by Murant, A.  F. 1970. Arabis mosaic virus. Descriptions of Plant Vi-
Longidorus diadecturus obtained from diseased orchards in On- ruses, no. 16. Commonwealth Mycological Institute and Associa-
tario. Can. J. Plant Pathol. 4:16-­18. tion of Applied Biologist, Kew, England.
Dias, H.  F. 1975. Peach rosette mosaic virus. Descriptions of Plant Murant, A.  F. 1970. Tomato black ring virus. Descriptions of Plant
Viruses, no. 150. Commonwealth Mycological Institute and Asso- Viruses, no. 38. Commonwealth Mycological Institute and Associa-
ciation of Applied Biologist, Kew, England. tion of Applied Biologist, Kew, England.
Gonsalves, D. 1982. Reaction of grape varieties to Tomato ring spot Ramsdell, D. C., and Stace-­Smith, R. 1983. Blueberry leaf mottle virus.
virus. Dev. Ind. Microbiol. 23:91-­97. Descriptions of Plant Viruses, no. 267. Commonwealth Mycological
Lunden, S., Meng, B., Avery, J., and Qiu, W. 2010. Association of Institute and Association of Applied Biologist, Kew, England.
Grapevine fanleaf virus, Tomato ringspot virus and Grapevine ru­ Stobbs, L.  W., and Van Schagen, J.  G. 1985. Relationship between
pestris stem pitting-­associated virus with a grapevine vein-­clearing Grapevine Joannes-­Seyve virus and Tomato blackring virus. Can
complex on var. Chardonnay. Eur. J. Plant Pathol. 126:135-­144. J. Plant Pathol. 7:37-­40.
Martelli, G.  P., Gallitelli, D., Abracheva, P., Savino, V., and Uyemoto, J. K., Cummins, J. R., and Abawi, G. S. 1977. Virus and vi-
Quacquarelli, A. 1977. Some properties of Grapevine Bulgarian ruslike diseases affecting grapevines in New York vineyards. Am.
latent virus. Ann. Appl. Biol. 85:51-­58. J. Enol. Vitic. 28:131-­136.
Martelli, G.  P., Quacquarelli, A., and Gallitelli, D. 1978. Grapevine Uyemoto, J. K., Taschenberg, E. F., and Hummer, D. K. 1977. Isolation
Bulgarian latent virus. Descriptions of Plant Viruses, no. 186. Com- and identification of a strain of Grapevine Bulgarian latent virus in
monwealth Mycological Institute and Association of Applied Biolo- Concord grapevines in New York State. Plant Dis. Rep. 61:949-­953.
gist, Kew, England. (Prepared by J. K. Uyemoto)

The Rugose Wood Complex are much reduced or not expressed under cool and wet condi-
tions) and possibly in relation to the scion/rootstock combina-
Descriptions of woody cylinder alterations on grapevines tion as well. For example, grapevine shoot necrosis reported to
resembling rugose wood symptoms are found in the French affect cv. Corniola in the Apulia region of Italy may represent a
literature of the early 1900s, with no indication of their pos- cultivar reaction to a rugose wood component.
sible infectious nature. As a graft-­transmissible disease, rugose Rugose wood is a complex consisting of four different dis-
wood was first identified and described from southern Italy eases recognized by the differential reactions induced in the
in the early 1960s. It is now known to occur worldwide, with indicators Vitis rupestris St. George, LN33, and Kober 5BB.
records existing from Europe, the Mediterranean basin, Near Rupestris stem pitting disease. Symptoms on the woody
and Far East, Australia, South Africa, and North and South cylinder appear as a distinct band of basipetal pitting extend-
America. ing downward from the point of inoculation in V.  rupestris
St. George (Fig. 256), whereas LN33 and Kober 5BB remain
Symptoms symptomless.
Affected grapevines appear less vigorous than normal and
show delayed bud opening in spring; some decline and die
within a few years from planting. Grafted grapevines often
show swollen scions at the bud union and a marked difference
in the relative diameters of their scion and rootstock (Fig. 254).
With certain cultivars, the bark above the graft union is ex-
ceedingly thick and corky, spongy in texture, and has a rough
appearance, a condition aptly named “corky rugose wood.” The
woody cylinder is typically marked by pits and grooves, which
correspond to peg-­and ridgelike protrusions originating from
the cambial surface of the bark (Fig. 255). These alterations
may occur on scions, rootstocks, or both. In most cases, no
specific foliage symptom develops, although certain cultivars
show leaf rolling, yellowing, or reddening. Bunches may be few
and small, and the crop reduced by 20–30%. Highly susceptible
cultivars can be unfruitful. Most, if not all, Vitis vinifera cul-
tivars and American rootstocks are susceptible. Infections are
latent in ungrafted scions and rootstocks; symptoms develop
after grafts are complete, although some infected grafted plants Fig. 254. Rugose wood symptoms at the graft union of an infected
remain asymptomatic. The severity of pitting and grooving in grapevine with a swollen scion portion with thick, rough bark.
symptomatic wood varies according to climate (e.g., symptoms (Cour­tesy G. P. Martelli)

130
 Corky bark disease. Symptoms occur as grooves and pits × 12 nm, with distinct transverse cross banding and contain-
over the entire stem surface of V. rupestris and LN33. More- ing a single species of linear positive-­sense, single-­stranded
over, LN33 is severely stunted with rolled, reddish leaves and RNA that accounts for 5% of the total particle weight. Coat
internodal swelling of the canes (Fig. 257). No disease symp- protein subunits have a molecular weight of 22–28 kDa. Viti-
toms develop in Kober 5BB. viruses, but not foveaviruses, are mechanically transmissible
Kober stem grooving disease. Symptoms of marked groov- to a restricted range of herbaceous hosts, albeit with difficulty.
ing develop on Kober 5BB (Fig. 258), whereas wood markings Individual viruses can be identified through ELISA tests with
are absent on V. rupestris and LN33. polyclonal antisera and/or monoclonal antibodies. The best
LN33 stem grooving disease. The grooves formed on LN33 antigen sources for serological diagnosis are cortical shavings
are indistinguishable from those of corky bark, but are not ac- from mature dormant canes. Alternative assays include single-­
companied by the foliar discolorations or internodal swellings step or nested reverse transcription-­polymerase chain reaction
associated with corky bark. No diagnostic symptoms are in- (RT-­PCR), immunocapture RT-­PCR, and spot-­RT-­PCR using
duced in V. rupestris or Kober 5BB. degenerate or virus-­specific primers. Immunocapture RT-­PCR
is 1000-­fold more sensitive than ELISA for virus detection in
Causal Agents grapevines.
Viruses in the genera Vitivirus or Foveavirus are recognized Grapevine rupestris stem pitting-­associated virus (GRSPaV),
as putative agents of the individual diseases of the rugose wood a definitive member of the genus Foveavirus, is the associated
complex. All have flexuous filamentous particles of about 800

Fig. 257. Symptoms of corky bark disease on LN33, including

Fig. 255. Prominent peglike protrusions originating from the cam- swelling and cracking of shoot basal internodes on plants inocu-
bial surface of the bark of a rugose wood-­affected grapevine, with lated with Grapevine virus B (healthy cane on right). (Cour­tesy
corresponding pits and grooves in the underlying wood cylinder. G. P. Martelli)
(Cour­tesy G. P. Martelli)

Fig. 256. Symptoms of rupestris stem pitting

disease on V. rupestris ‘St. George’, including
a line of small pits developing basipetally from Fig. 258. Symptoms of Kober stem grooving
the point of inoculation with Grapevine rupes- disease in Kober 5BB rootstock, associated
tris stem pitting-associated virus. (Cour ­tesy with infections by Grapevine virus A. (Cour­
G. P. Martelli) tesy G. P. Martelli)

131
agent of rupestris stem pitting disease. Virus particles are not No information is available regarding the utility of control-
readily observed with the electron microscope. GRSPaV occurs ling mealybug vectors. However, these insects are not easy to
in nature as a family of molecular variants, with a viral RNA control by pesticides as they overwinter under the bark of grape-
genome of 8726 nt. vines and possess an unwettable waxy covering. Scale insects
Grapevine virus A (GVA), the type species of the genus Viti- are also difficult to control with pesticides. No natural sources
virus, has been associated with Kober stem grooving. Its viral of resistance to any rugose wood agent are known but the possi-
RNA has a genome of 7349 nt. Biological, serological, and mo- bility of using pathogen-­derived resistance in transformed Vitis
lecular variants of the virus are known. Some of these variants constructs has shown potential and is being explored.
are thought to be implicated in the etiology of Shiraz disease in
South Africa and Australia. Selected References
Grapevine virus B (GVB) is a vitivirus distantly related se-
rologically to GVA and one of the etiological agents associated Abou Ghanem, N., Saldarelli, P., Minafra, A., Buzkan, N., Castellano
M. A., and Martelli, G. P. 1997. Properties of grapevine virus D, a
with corky bark. GVB is also involved in young grapevine de-
novel putative trichovirus. J. Plant Pathol. 79:15-­25.
cline, a graft incompatibility condition recorded from Califor- Alabi, O. J., Martin, R. R., and Naidu, R. A. 2010. Sequence diversity,
nia. GVB has a genome of 7599 nt and occurs in nature as a population genetics and potential recombination events in Grape-
family of molecular variants. vine rupestris stem pitting-­associated virus in Pacific North-­West
Grapevine virus D (GVD) is a vitivirus distantly related sero- vineyards. J. Gen. Virol. 91:265-­276.
logically to GVA and GVB. An association with corky rugose Boscia, D., Savino, V., Minafra, A., Namba, S., Elicio, V., Castellano,
wood has been reported, but there is no experimental evidence M. A., Gonsalves, D., and Martelli G. P. 1993. Properties of a fila-
of its implication in the genesis of this disease. mentous virus isolated from grapevines affected by corky bark.
Grapevine virus E (GVE) is a newly described vitivirus. Al- Arch. Virol. 130:109-­120.
though identified from a table grape cultivar with stem pitting Boscia, D., Minafra, A., and Martelli, G. P. 1997. Filamentous viruses
symptoms, its implication in the rugose wood complex is un- of the grapevine: Putative trichoviruses and capilloviruses. Pages
certain. GVE has also been detected in Alaska in domesticated 19-­28 in: Filamentous Viruses of Woody Plants. P. L. Monette, ed.
Ribes spp. exhibiting a vein-­clearing symptom, but not in native Research Signpost, Trivandrum, India.
Ribes spp. GVE has a genome of 7568 nt. The Ribes isolate Chevalier, S., Greif, C., Clauzel, J. M., Walter, B., and Fritsch, C. 1995.
Use of an immunocapture-­polymerase chain reaction procedure for
of GVE contains a 322 intergenic region that is absent in the
the detection of grapevine virus A in Kober stem grooving-­infected
grapevine isolates. grapevines. J. Phytopathol. 143:369-­373.
Grapevine virus F (GVF) is a novel member of the genus Coetzee, B., Maree, H. J., Stephan, D., Freeborough, M-­J., and Burger,
Vitivirus found in California. Its genome is 7551 nt in size. It in- J.  T. 2010. The first complete nucleotide sequence of a grapevine
duces graft incompatibility in cv. Cabernet Sauvignon grafted virus E variant. Arch. Virol. 155:1357-­1360.
on different rootstocks. Conti, M., Milne, R. G., Luisoni, E., and Boccardo, G. 1980. A clo-
sterovirus from a stem-­pitting-­diseased grapevine. Phytopathology
Disease Cycle and Epidemiology 70:394-­399.
GVA and GVB are transmitted among grapevines by pseu- Du Preez, J., Stephan, D., Mawassi, M., and Burger, J. T. 2011. The
dococcid mealybugs and/or scale insects in a semipersistent grapevine infecting vitiviruses with particular reference to grape-
manner. Specific GVA vectors are the mealybugs Planococcus vine virus A. Arch. Virol. 156:1495-­1503.
Goszczynski, D.  E., du Preez, J., and Burger J.  T., 2008. Molecular
citri, Pl. ficus, Pseudococcus longispinus, Ps. viburni, Helio-
divergence of Grapevine virus A (GVA) variants associated with
coccus bohemicus, Phenacoccus aceris, and the scale insect Shiraz disease in South Africa. Virus Res. 138:105-­110.
Neopulvinaria innumerabilis. The virus was consistently de- Hewitt, W.  B., Goheen, A.  C., Raski, D.  J., and Gooding, G.  V. Jr.
tected in over 70% of mealybug populations collected in rugose 1962. Studies on virus diseases of the grapevine in California. Vitis
wood-­infected vineyards from different European and Medi- 3:57-­83.
terranean countries. GVB is transmitted by Ps. longispinus, Ps. La Notte, P., Buzkan, N., Choueiri, E., Minafra, A., and Martelli, G. P.
viburni, Ps affinis, Ph. aceris, and Pl. ficus. GVE is transmitted 1997. Acquisition and transmission of Grapevine virus A by the
by Pseudococcus comstocki. GRSPaV has no known vectors, mealybug Pseudococcus longispinus. J. Plant. Pathol. 79:79-­85.
but is suspected to be borne by pollen. Martelli, G. P., ed. 1993. Graft-­transmissible Diseases of Grapevine.
All putative disease agents of the rugose wood complex are Handbook for Detection and Diagnosis. FAO Publication Division,
phloem-­limited viruses that persist in infected stocks and gen- Rome, Italy.
erally are mechanically transmittable with difficulty. No alter- Martelli, G. P., and Jelkmann, W. 1998. Foveavirus, a new plant virus
native hosts in nature are known, and natural dissemination is genus. Arch. Virol. 142:1245-­1249.
limited owing to the relatively limited range of vector move- Martelli, G. P., Minafra, A., and Saldarelli, P. 1997. Vitivirus, a new
genus of plant viruses. Arch. Virol. 42:1929-­1932.
ment. Long-­ distance spread is, therefore, achieved through Martelli, G.  P., Adams, M.  J., Kreuze, J.  F., and Dolja, V.  V. 2007.
transport of infected propagative material. The presence of Family Flexiviridae: A case study in virion and genome plasticity.
rugose wood and its causal agents in phylloxera-­free countries Annu. Rev. Phytopathol. 45:73-­100.
with a millennial history of own-­rooted grapevine cultivation Meng, B., Pang, S. Z., Forsline, P. L., McFerson, J. R., and Gonsalves, D.
suggests that the disease complex originated in the Old World 1998. Nucleotide sequence and genome structure of grapevine rup-
and was distributed worldwide in infected plants. estris stem pitting-­associated virus-­1 reveal similarities to apple
stem pitting virus. J. Gen. Virol. 79:2059-­2069.
Management Meng, B., Johnson, R., Peressini, S., Forsline, P. L., and Gonsalves D.
Sanitary selection of propagating material can efficiently re- 1999. Rupestris stem pitting associated virus-­1 is consistently de-
duce or minimize the introduction of rugose wood into vine- tected in grapevines that are infected with rupestris stem pitting.
yards. However, symptomless infections limit the reliability of Eur. J. Plant Pathol. 105:191-­199.
Minafra, A., Saldarelli, P., and Martelli, G. P. 1997. Grapevine virus
sanitary selection; hence, all sources must be indexed on three A: Nucleotide sequence, genome organization, and relationships in
indicators (V. rupestris, Kober 5BB, and LN33) and/or assayed the Trichovirus genus. Arch. Virol. 142:417-­423.
using antisera or PCR primer sets. Rugose wood agents can be Nakaune, R., Toda, S., Mochizuki, M., and Nakano, M. 2008. Identifi-
eliminated with high efficiency (up to 85%) by heat therapy, cation and characterization of a new vitivirus from grapevine. Arch
meristem tip culture, or a combination of the two. Other effi- Virol. 153:1827-­1832.
cient methods are somatic embryogenesis (GRSaV, GVA), cryo- Saldarelli, P., Minafra, A., and Martelli, G.  P. 1996. The nucleotide
therapy, and electrotherapy (GVA). Only clean material should sequence and genomic organization of Grapevine virus B. J. Gen.
be used for propagation. Virol. 77:2645-­2652.

132
Zhang, Y.-­P., Uyemoto, J. K., Golino, D. A., and Rowhani, A. 1998. ies of symptomatic leaf tissues have depicted modifications in
Nucleotide sequence and RT-­PCR detection of a virus associated the shape and outward appearance of chloroplasts.
with grapevine rupestris stem pitting disease. Phytopathology
88:1231-­1237. Causal Agent
Vein mosaic is caused by an unidentified graft-­transmissible
(Prepared by G. P. Martelli, D. Boscia, A. Minafra, agent. Transmission to Vitis riparia Gloire de Montpellier, the
and P. Saldarelli) specific indicator, is readily achieved by chip budding in the
field and by green grafting. Under greenhouse conditions at
26°C, symptoms may appear within 3 weeks after inoculation
Vein Mosaic (Fig. 260). In field indexing experiments, symptoms develop
much more slowly, requiring incubation of up to 1 year.
Vein mosaic is a semi-­latent disease first described from Disease Cycle and Epidemiology
France, and reported to occur in other European countries with Vein mosaic is spread through propagation of infected ma-
incidence of up to 50–60%. It also has been reported from Cali- terials. Although seed transmission is suspected, there is no
fornia, Brazil, and Australia. evidence of natural spread.
Symptoms Management
In sensitive V. vinifera cultivars, disease symptoms include Propagation should be done using only clean sources. The
pale green discoloration of the leaf tissues, primarily along the disease agent can be eliminated from contaminated sources by
main veins (Fig. 259). The veins themselves produce a feath- heat therapy.
ering or banding, which is not necessarily restricted to these
zones. Grapevine size and vigor may be adversely affected. Selected References
Symptom severity can vary with cultivar and year, although
specific climatic influences have not been determined. Infected Kassemeyer, H.-­H., Grenan, S., and Greif, C. 1997. Use of green
V. rupestris St. George vines are reduced in vegetative growth grafting for the biological indexing of grapevine virus and virus-­
and basal leaves develop chlorosis. However, infections are like diseases. Pages 119-­127 in: Sanitary Selection of the Grape-
commonly symptomless in most cultivars. Ultrastructural stud- vine. Protocols for Detection of Viruses and Virus-­l ike Diseases.
B. Walter, ed. Les Colloques 86. INRA-­I NITA, Bordeaux, France.
Krake, L.  R., Steele Scott, N., Rezaian, M.  A., and Taylor, R.  H.
1999. Graft-­transmitted diseases of grapevines. CSIRO Publishing,
Collingwood, Victoria, Australia.
Legin, R., and Vuittenez, A. 1973. Comparaison des symptomes et
transmission par greffage d’une mosaique nervaire de Vitis vinif-
era, de la marbrure de V. rupestris et d’une affection necrotique des
nervures de l’hybride Rup.-­Berl. 110 R. Riv. Patol. Veg. Ser. IV, 9
(Suppl.):57-­63.
Legin, R., and Walter, B. 1986. Regenerierung von Virosen befallener
Reben durch Thermotherapie oder Wärmebehandlung und Schnell-
vermehrung del Rebe. Wein-­Wiss. 41:14-­25.

(Prepared by U. Prota and R. Garau)

Vein Necrosis
Vein necrosis was first found in France. It also occurs in
other European countries, California, Brazil, and Australia.
Fig. 259. Symptoms of vein mosaic disease with Disease incidence exceeding 70% has been observed in com-
pale green discoloration along the veins of a mercial vineyards.
V. vinifera leaf. (Cour­tesy U. Prota)
Symptoms
The disease is latent in all V.  vinifera cultivars and most
American rootstocks. On the indicator host for vein necrosis,
V.  rupestris × V.  berlandieri 110R, symptoms include veinlet
necrosis (Fig. 261) appearing first on the basal leaves and pro-
gressing to other leaves toward the shoot tip. Necrotic symp-
toms are best seen on the lower leaf surfaces but are visible on
the upper leaf surfaces also. Severe forms of the disease may
induce necrosis of tendrils, dieback of green shoots, stunting,
and occasionally plant death. Symptoms persist and are readily
observed throughout the vegetative season.

Causal Agent
Vein necrosis is caused by a graft-­transmissible agent whose
identity has not been determined, although some genetic vari-
ants of Grapevine rupestris stem pitting-­associated virus are
associated with the disease. Transmissions to the 110R indica-
tor host is accomplished by chip bud grafts and by green grafts.
Fig. 260. Typical vein mosaic symptoms on the indicator Vitis Symptoms appear 4 weeks after inoculation under greenhouse
riparia ‘Gloire de Montpellier’. (Cour­tesy U. Prota) conditions at 26°C or 8–10 weeks in the field. Mild disease

133
Fig. 261. Necrotic veins and veinlets symptomatic of vein necro-
sis disease on the indicator host V. rupestris x V. berlandieri 110R.
(Cour ­tesy U. Prota)

forms may require incubation of up to 1 year before symptoms

develop.

Disease Cycle and Epidemiology

Vein necrosis spreads only through propagation of infected Fig. 262. Bright yellow foliar discolorations
materials. symptomatic of grapevine yellow mottle dis-
ease. (Cour­tesy G. P. Martelli)
Management
Propagation only from healthy sources is recommended. Grapevine yellow mottle. This disease is characterized
Detection is accomplished by grafting on 110R; RT-­PCR with by different patterns of chrome-­yellow discolorations of the
virus-­specific primers and western blot with an antiserum to foliage. The spring growth shows more or less extensive yel-
recombinant coat protein of GRSPaV allow sensitive and reli- lowing of leaf blades that usually does not extend to the veins
able detection in symptomatic 110R plants. The disease agent (Fig. 262), whereas typical summer responses are faint yellow
can be eliminated from contaminated sources by heat therapy. speckling and ring and line patterns. The putative causal agent
is Alfalfa mosaic virus (AMV), a mechanically-­transmissible
Selected References virus with differently shaped particles (from quasi-­isometric to
bacilliform, 30–57 nm in size) and a tripartite RNA genome
Alliaume. A., Spilmont. A.  S., Beuve. M., and Lemaire. O. 2012.
consisting of 3644, 2593, and 2037 nt for RNA-­1, -­2, and 3,
Grapevine vein necrosis is not exclusively associated to GRSPaV
group 2. Pages 84-­85 in: Proc. 17th Congress, International Council
respectively. AMV is aphidborne but new infections in grape-
for the Study of Virus and Virus-­like Diseases of the Grapevine vines are very rare, suggesting that spread is primarily through
(ICVG). http://web.pppmb.cals.cornell.edu/fuchs/icvg/data/ICVG-­ the use of infected propagating materials. Yellow mottle has
2012-­Proceedings.pdf been reported from Bulgaria, former Czechoslovakia, France,
Bouyahia, H., Boscia, D., Savino, V., La Notte, P., Pirolo, C., Germany, Hungary, Switzerland, and Turkey.
Castellano, M. A., Minafra, A., and Martelli, G. P. 2005. Grapevine Grapevine line pattern. Symptoms are bright yellow discol-
rupestris stem pitting-­associated virus is linked with grapevine vein orations of the leaves forming marginal rings, scattered spots,
necrosis. Vitis 44:133-­137. blotches, or maple leaf patterns that typically are confined to the
Kassemeyer, H.  H., Grenan, S., and Greif, C. 1997. Use of green petiolar areas or upper part of the leaf blade, roughly following
grafting for the biological indexing of grapevine virus and virus-­ its contour (Fig. 263). Grapevine line pattern virus (GLPV),
like diseases. Pages 119-­127 in: Sanitary Selection of the Grape- the presumed causal agent of the disease, is a poorly charac-
vine. Protocols for Detection of Viruses and Virus-­like Diseases. terized putative Ilarvirus with differently shaped particles,
B. Walter, ed. Les Colloques 86. INRA-­INITA, Bordeaux, France. quasi-­spherical 25–30 nm in diameter and bacilliform 40–75
Legin, R., and Vuittenez, A. 1973. Comparaison des symptomes et
nm in length. GLPV has no known vector, is seed-­transmitted
transmission par greffage d’une mosaique nervaire de Vitis vinif-
era, de la marbrure de V. rupestris et d’une affection necrotique des and spread by propagating diseased materials. This disease has
nervures de l’hybride Rup.-­Berl. 110 R. Riv. Patol. Veg. Ser. IV, 9 been reported only from Hungary.
(Suppl.):57-­63. Grapevine Roditis leaf discoloration. Symptoms of this
Savino, V., Boscia, D., and Martelli, G.  P. 1985. Incidence of some disease are prominent in late summer and consist of yellow
graft-­transmissible viruslike diseases of grapevine in visually se- and/or reddish discolorations of the tissues along the veins,
lected and heat-­treated stocks from southern Italy. Phytopathol. in the interveinal areas, or across variously extended and de-
Mediterr. 24:204-­207. formed sectors of the leaf blade, especially near the petiole
(Fig. 264). Bunches are reduced in number and size and ber-
(Prepared by U. Prota and R. Garau) ries have low sugar content. Symptomatic grapevines were re-
ported to be doubly infected with GFLV and Carnation mottle
virus (CarMV), an isometric virus 30 nm in diameter with a
monopartite RNA genome of 4003 nt. More recent findings in-
Minor Virus Diseases dicate, however, that GFLV is not involved in the etiology of the
disease. Instead, Grapevine virus B (GVB), one of the putative
Several graft-­transmissible diseases of minor economic im- agents of corky bark (rugose wood complex) has a very high
portance have been recorded from Europe. association with diseased grapevines. Roditis leaf discoloration

134
 Fig. 265. Leaf symptoms of grapevine angular mosaic in a self-­
cross of V. vinifera cv. Baresana. (Cour­tesy S. M. Girgis)

RBDV is widespread in Rubus spp. It was recently isolated

from grapevines cv. Laski Rizling in Slovenia that showed
yellow line pattern symptoms resembling those reported for
GLPV.

Fig. 263. Marginal yellow line pattern pre-

Selected References
sumed to be elicited by Grapevine line pattern
virus infection. (Cour­tesy G. P. Martelli) Bovey, R., and Brugger, J. J. 1975. Le virus de la mosaïque de la lu-
zerne sur la vigne. Rev. Suisse Vitic., Arboric., Hortic. 7:63-­65.
Girgis, S. M., Bem, F. P., Kyriakopoulou, P. E., Dovas, C. I., Avgelis, A.,
and Katis, N. I. 2003. The etiology of a new virus disease: Grape-
vine angular mosaic. Page 19 in: Extended Abstracts 14th Meeting,
International Council for the Study of Virus and Virus-­like Dis-
eases of the Grapevine (ICVG). http://web.pppmb.cals.cornell.edu/
fuchs/icvg/data/2003Session12.pdf
Mavrič Pleško, I., Viršček Marn, M., Širca, S., and Urek, G. 2009.
Biological, serological and molecular characterisation of Raspberry
bushy dwarf virus from grapevine and its detection in the nematode
Longidorus juvenilis. Eur. J. Plant Pathol. 123:261-­268.
Rumbos, I. C., and Avgelis, A. D. 1989. Roditis leaf discoloration: A
new virus diseases of grapevine: Symptomatology and transmission
to indicator plants. J. Phytopathol. 125:274-­278.

(Prepared by G. P. Martelli and A. D. Avgelis)

Other Viruses and Viruslike Agents

Fig. 264. Symptoms of grapevine Roditis leaf discoloration in cv.
Roditis. (Cour­tesy A. D. Avgelis)
The most significant viruses and viruslike diseases of grape-
vines have been described elsewhere in this compendium.
is graft-­transmissible and spreads with infected propagative However, other pathogens and diseases that are less known or
material. It has been recorded only from Greece. limited in distribution have been reported in grapevines over
Grapevine angular mosaic. The symptoms of this disease the years (Table 4). One disease found in South America, Elqui
include chlorotic angular spots on leaf blades, discoloration yellows, might be caused by a phytoplasma. The distribution
of tissues bordering the veins, and crinkling and deformation and horticultural significance of these viruses and diseases
of the leaves (Fig. 265). Infected grapevines are stunted, de- vary considerably. Whereas a few are mentioned in isolated
cline gradually, and some die. Fruit bunches are poorly devel- reports, others have occurred in one or more cultivars in a spe-
oped because of floral abortion. Berries when present remain cific region or were found in several viticultural areas. Some
small, wrinkled, and bear nonviable seeds. The disease agent agents were latent and produced no obvious or measurable
is Grapevine angular mosaic virus (GAMV), a virus with a effect, whereas others caused significant symptoms and yield
tripartite RNA genome molecularly related to a number of il- losses in specific geographic areas. The causal agents for 11
arviruses, the closest being Tobacco streak virus. GAMV is of these diseases are unknown; their detection was based on
pollenborne in herbaceous hosts, but whether this mechanism symptoms displayed or transmissions to healthy grape plants or
operates in grapevines is not known. The disease has been re- herbaceous indicators.
ported only from Greece. Grapevine viruses have being characterized in significant
Raspberry bushy dwarf virus (RBDV), the type species of numbers in recent years, and new diseases caused by unknown
the genus Idaeovirus, is a pollen-­and seedborne virus with pathogens have been reported. Modern diagnostic and mo-
quasi-­spherical particles about 30 nm in diameter and a bipar- lecular technologies have assisted in detecting both known
tite single-­stranded RNA genome consisting of two functional viruses newly associated with grapes and newly described vi-
RNA species with 5449 nt (RNA-­1) and 2214 nt (RNA-­2). ruses associated with symptoms of formerly unknown etiology.

135
Innovations in viticultural practices have contributed in the Bovey, R., and Martelli, G. P. 1992. Directory of Major Virus and Vi-
recognition of some new diseases. Changes in cultivars and ruslike Diseases of Grapevines. Imprimerie Finzi, Tunis.
rootstocks have led to the emergence of latent infections into Frison, E.  A., and Ikin, R., eds. 1991. Technical Guidelines for the
newly recognized diseases, often with serious economic conse- Safe Movement of Grapevine Germplasm. Food and Agriculture
quences for specific scion/rootstock combinations. New trans- Organization of the United Nations (FAO) and International Board
mission opportunities and, sometimes, economic damage may for Plant Genetic Resources (IBPGR), Rome, Italy.
Koklu, G., Digiaro, M., Sabanadzovic, S., and Savino, V. 1999. Natural
result when a pathogen is introduced into an environment with infections by cucumber mosaic virus in Turkish grapevines. Phyto-
different populations of potential insect or nematode vectors. pathol. Medit. 38:33-­36
Plant damage and yield losses may also result when grapevines Smith, I.  M., Dunez, J., Lelliot, R.  A., Phillips, D.  H., and Archer,
or formerly exotic Vitis species are introduced into a region and S. A., eds. 1988. European Handbook of Plant Diseases. Blackwell
exposed to endemic pathogens and vectors for the first time. Scientific, Oxford, UK.
The primary means of virus spread over long distances is by
movement of infected propagative material. In today’s market, (Prepared by R. Johnson and J. A. Foster)
international transport of plants for commercial and research
purposes is significant and increasing. Viticulturists and grow-
ers alike are interested in importing and evaluating new culti-
vars and rootstocks. Viruses and viruslike graft-­transmissible Grapevine Viroids
agents are difficult to detect in dormant plants or propagative
materials without diagnostic testing. Once established, these Viroids are small, circular RNA molecules that are a fraction
agents are often difficult to control. Infected plants cannot be of the size of viruses. The first viroid reported in grapevines
therapeutically cured. was Hop stunt viroid (HSVd-­g) in Japan. Subsequent research
revealed multiple viroid infections in grapevines worldwide.
Selected References Although viroids can cause severe diseases in other plant hosts,
e.g., potato spindle tuber and citrus exocortis, there is no con-
Bovey, R., Gärtel, W., Hewitt, W. B., Martelli, G. P., and Vuittenez, A. sistent evidence that they cause adverse effects in grapevines
1980. Virus and Virus-­like Diseases of Grapevines. Payot Laus- in and of themselves. However, two related viroids serve as
anne, Switzerland. components of the deleterious grapevine leaf banding disease.

136
Grapevine yellow speckle disease is the name given to the only characterized grapevine viroid probes. AGVd also is found in
syndrome attributed solely to infection by viroids. California.
The remaining two viroids also are presumed to be latent in
Symptoms grapevines. As early as 1952, stunted hop plants were observed
Foliar symptoms of grapevine yellow speckle disease are in Japan. A biological assay using cucumber was developed
often absent or difficult to diagnose when only a few yellow- and the causal agent was identified and named Hop stunt vi-
ish spots or flecks develop along major or minor leaf veins. roid (HSVd). In grapevine, the same infectious low-­molecular-­
In some years in Australia, the symptoms can be spectacular, weight RNA (designated HSVd-­g) was detected by molecular
consisting of bright yellow blotches (Fig. 266, A and D); vein-­ hybridization assays with HSVd probe, and on cucumber plants
banding patterns (Fig. 266, E) are a variant resulting from co-­ it caused symptoms indistinguishable from those incited by the
infections with Grapevine fanleaf virus (GFLV). Occasionally, hop isolate. HSVd-­g has been detected in nearly all grapevines
the symptoms may develop during mid-­spring, but more often tested in Japan and Australia, and is reported from the United
during late summer to autumn. When symptoms occur early, States and Europe. Its significance in grapevines may be as a
the speckles appear bleached and by late summer turn white. reservoir to infect hop plants.
Speckle symptoms that develop mid-­season are pale yellow Symptoms of citrus exocortis were first described on that
and those developed during late summer light green. Yellow host in 1948. The causal agent, Citrus exocortis viroid (CEVd),
speckle symptoms are most likely to develop on exposed basal was transmitted to herbaceous plants and Gynura aurantiaca
leaves. as an indicator host. In Spain, a viroid with 89–92% sequence
homology with CEVd was isolated from a symptomless grape-
Causal Agents vine and designated CEVd-­g. It was also detected in symptom-
To date, five different viroids have been identified in grape- less grapevines in Australia.
vines (Table 5). Two of these, Grapevine yellow speckle
viroids 1 and 2 (GYSVd-­1 and -­2), are the causal agents of yel- Disease Cycle and Epidemiology
low speckle disease and are only known to infect grapevines. Long-­distance spread of viroids is largely attributed to the
Grapevine vein banding disease, common in Europe and Cali- propagation and distribution of infected plant material. The ap-
fornia and previously attributed to GFLV as the sole incitant, is parent ubiquitous presence of viroids within individual vine-
now known to require the presence of GFLV plus GYSVd-­1 or yards is likely attributable to mechanical transmissions with
-­2, with its symptoms the product of a synergistic interaction contaminated pruning tools.
between GYSVds and GFLV.
Australian grapevine viroid (AGVd) also is unique to grape- Management
vines, in which it is latent. It was originally recovered from Propagation should be done using only clean source material.
grapevines in Australia co-­infected with the other four viroids Although grape seedlings were once regarded as viroid-­free
from this host but was distinguished from them by differences germplasm, the grapevine viroids GYSVd-­1, -­2, AGVd, and
in electrophoretic properties, ability to replicate in cucumber GEVd have been detected in seedlings by means of molecu-
and tomato, and in failed hybridization assays using previously lar diagnostic techniques, which also have provided additional
evidence of seed to seedling transmissions of GYSVd-­1 and
HSVd-­g in multiple grape cultivars.

Selected References

García-­A renal, F., Pallas, V., and Flores, R. 1987. The sequence of
a viroid from grapevine closely related to severe isolates of citrus
exocortis viroid. Nucleic Acids Res. 15:4203-­4210.
Koltunow, A. M., and Ali Rezaian, M. 1988. Grapevine yellow speckle
viroid: Structural features of a new viroid group. Nucleic Acids Res.
16:849-­864.
Koltunow, A. M., and Rezaian, M. 1989. Grapevine viroid 1B, a new
member of the apple scar skin viroid group contains the left termi-
nal region of tomato planto macho viroid. Virology 170:575-­578.
Krake, L. R., and Woodham, R. C. 1983. Grapevine yellow speckle
agent implicated in the aetiology of vein banding disease. Vitis
22:40-­50.
Little, A., and Rezaian, M.  A. 2003. Grapevine viroids. Pages 195-­
Fig. 266. Variations in grapevine yellow speckle symptoms in 206 in: Viroids: Properties, Detection, Diseases and their Control.
inoculated cv. Cabernet Franc leaves (A–D). A, Severe symp- A. Hadidi, R. Flores, J. Randles, and J. Semancik, eds. CSIRO Pub-
toms resulting from seedling inoculation with plus-­sense dimeric lishing, Australia.
GYSVd-­1 transcript; B, scattered speckles from seedling inocu- Rezaian, M.  A. 1990. Australian grapevine viroid—evidence for
lation with GYSVd-­2; C, moderate symptoms from co-­inoculation extensive recombination between viroids. Nucleic Acids Res.
of a seedling with GYSVd-­1 and -­2; and D, severe leaf symptoms 18:1813-­1818.
from a field-­grown grapevine. E, Leaf of cv. Sultana with vein-­ Sano, T., Uyeda, I., Shikata, E., Meshi, T., Ohno, T., and Okada, Y.
banding symptoms, resulting from co-­ infection by GYSVd and 1985. A viroid-­like RNA isolated from grapevine has high sequence
GFLV. (Cour­tesy L. R. Krake) homology with hop stunt viroid. J. Gen. Virol. 66:333-­338.

137
Szychowski, J.  A., McKenry, M.  V., Walker, M.  A., Wolpert, J.  A., Wolpert, J. A., Szychowski, J. A., and Semancik, J. S. 1996. Effect of
Credi, R., and Semancik, J. S. 1995. The vein-­banding disease syn- viroids on growth, yield, and maturity indices of Cabernet Sauvi-
drome: A synergistic reaction between grapevine viroids and fan- gnon grapevines. Am. J. Enol. Vitic. 47:21-­24.
leaf virus. Vitis 34:229-­232.
(Prepared by M. A. Rezaian and A. Little)

Nematode Parasites of Grapevines

Nematode diseases of grape were first reported in the mid-­ host range primarily consisting of woody perennial species:
1880s. These initial reports were concerned exclusively with citrus, olive, persimmon, and grape. The citrus nematode is
root-­k not nematodes, primarily owing to the visible galls they highly pathogenic to grapevines, particularly in finer-­textured
produced on affected roots. Scarcely more than a handful of ad- soils where root-­k not nematodes are less competitive. Vine
ditional reports were published until the mid-­1950s. The impe- vigor is markedly reduced, and affected plants do not have the
tus for the study of nematodes was the discovery of chemicals resilience to withstand stressful conditions. Yields gradually
in the 1940s and 1950s that reduced nematode numbers while and inevitably decline, and vineyards become uneconomical.
increasing plant growth. Since 1954, research has shown that
grapes are afflicted by a wide array of root-­parasitic nematode Symptoms
species. Many of the species occur worldwide wherever grapes No specific symptoms diagnostic for the citrus nematode are
are grown, as they have been transported with rooted planting apparent on aboveground parts of the vine. The main effect be-
material. Although some nematode species cause characteris- lowground is the death of feeder roots, although some rootlets
tic galls on the root system, aboveground symptoms are gen- may remain alive and support large populations of nematodes
erally nonspecific and may be manifested as unthrifty vines, (Fig. 267). The bodies of adult females protrude from the root,
poor growth, reduced yields, nutrient deficiency, and greater often with many individuals in close proximity to each other
sensitivity to stress. These effects of damage to the root system and probably feeding from the same nurse cell system. Females
are often misdiagnosed as water stress or nutrient deficiency. produce a gelatinous matrix in which they deposit the eggs, and
Indeed, in some cases the effect of the root damage may be this covers the mass of female nematodes when they are located
partially compensated by increased water or nutrient supply, close together. Soil particles adhere to the matrix and are not
but that is usually a short-­term solution. The types of plant-­ easily dislodged when soil is shaken from the roots, giving in-
feeding nematodes that become established in a vineyard are fested rootlets a dirty appearance.
determined by the nematode assemblage present in the soil at
planting, sanitation and cleanliness of nursery stock, suscepti- Causal Organism
bility of the selected rootstock, the nematode host status of ro- The citrus nematode is Tylenchulus semipenetrans Cobb,
tation and cover crops, water source and irrigation method, and the specific epithet reflecting that in the adult female stage the
movement of soil by vehicles and tillage. The damage caused anterior of the body is embedded in the root and the posterior
by nematodes may be exacerbated by climatic conditions, geo- remains exposed on the root surface.
graphic region, moisture and nutrient stress, and viticultural
practices. Life Cycle and Epidemiology
Juvenile citrus nematodes hatch from the egg in the second
developmental stage. Those individuals destined to become
males develop quite differently from those that will become fe-
Citrus Nematode males. Male juveniles have a degenerate stylet and esophagus
and do not feed, and therefore do not cause damage to plants.
The citrus nematode was first found on citrus roots in 1913 They pass through three molts, with the intestine developing
and first reported on grape in 1956, in both California and Aus- a progressively starved appearance with some residual bands
tralia; since that time, it has been reported from all continents of food reserves and clear areas where reserves have been de-
where grapes are grown. This nematode has a relatively narrow pleted. Males are not necessary for reproduction; females pro-
duce viable eggs without being fertilized.
Juveniles destined to become adult females do feed, as ecto-
parasites on root epidermal or outer cortical cells and in areas
where lateral rootlets are emerging, as they pass through three
more stages after hatching before becoming adult; therefore,
they do not have the starved appearance of males. When they
reach the young female stage, the nematodes penetrate the root
so that the head is in the inner cortical region, near the endo-
dermis. There, the nematode stimulates formation of a system
of somewhat enlarged, metabolically active nurse cells. As the
females feed, their bodies enlarge; this occurs primarily on that
portion of the body outside the root, as enlargement of the an-
terior portion embedded in the root tissue is restricted by the
walls of root cells. Since the enlarged nematodes are partially
inside the root and no longer able to move, these nematodes
in the adult female stage are described as sedentary semi-­
endoparasites. The females, either in groups or as individuals,
deposit several hundred eggs into the gelatinous matrix sur-
Fig. 267. Roots damaged by citrus nematodes (right) versus rounding them. The life cycle from egg to egg requires 4–8
healthy roots (left). (Cour­tesy D. J. Raski) weeks to complete.

138
 Selected References root tip. Parasitism by L. africanus causes root growth to stop
soon after feeding begins.
Anwar, S.  A., and Van Gundy, S.  D. 1989. Influence of four nema-
todes on root and shoot growth parameters in grape. J. Nematol. Causal Organisms
21:276-­283.
Rahman, L., Creecy, H., and Orchard, B. 2008. Impact of citrus nema- The species of dagger nematodes that have been associated
tode (Tylenchulus semipenetrans) densities in soil on yield of grape- with grape are: Xiphinema index Thorne & Allen; X. italiae
vines (Vitis vinifera ‘Shiraz’) in south-­eastern New South Wales. Meyl; X. diversicaudatum (Micoletzky) Thorne; X. mediter-
Vitis 47:175-­180. raneum Martelli & Lamberti; X. pachtaicum (Tulagonov)
Siddiqi, M.  R. 1974. Tylenchulus semipenetrans. Descriptions of Kirjanova; X. algeriense Luc & Kostadinov; X.  vuittenezi
Plant-­Parasitic Nematodes. Set 3. No. 34. Commonwealth Institute Luc, Lima, Weischer & Flegg; X. turcicum Luc & Dalmasso;
of Helminthology, St. Albans, Hertfordshire, England. and X. americanum Cobb. Within the X. americanum species
Van Gundy, S.  D. 1958. The life history of the citrus nematode complex the following species have been reported: X. rivesi
Tylenchulus semipenetrans Cobb. Nematologica 3:283-­294. Dalmasso; X. californicum Lamberti & Bleve-­Zacheo; and
X. brevicolle Lordello & da Costa.
(Preparted by I. A. Zasada, H. Ferris, and M. V. McKenry) The species of needle nematodes that have been associated
with grape are: Longidorus attenuatus Hooper; L. africanus
Merny; L. carniolensis Sirca; L. elongatus (de Man) Thorne
& Swanger; L. juvenilis Micoletzky; L. leptocephalus Hooper;
Dagger and Needle Nematodes L. sylphus Thorne; L. diadecturus Eveleigh & Allen; L. irani-
cus Sturhan & Barooti; L. macrosoma Hooper; L. poessnecken-
Dagger nematodes, Xiphinema spp., are present in all major
sis Altherr; L. protae Lamberti & Bleve-­Zacheo; and L. raskii
grape-­growing areas of the world. This is a diverse group of
Lamberti & Agostinelli. In addition, Paralongidorus maximus
nematodes with over 50 described species. Whereas many dif-
has been reported from Europe.
ferent species of Xiphinema have been reported from vineyards
There are several Nepoviruses that are vectored by dagger
during surveys, the pathogenicity of many of these species to
and/or needle nematodes. Specific virus/vector associations in-
grapevines has not been determined. Xiphinema index Thorne
clude: Grapevine fanleaf virus (X. index, X. italiae, and X. vuit-
& Allen, the most thoroughly studied of the dagger nematodes,
tenzi); Tomato ringspot virus (X. californicum, X. americanum,
is worldwide in distribution and can be a devastating pathogen
and X.  revesi); Tobacco ringspot virus (X.  americanum and
of grapevines. Affected vines within highly porous soils de-
X. rivesi); Peach rosette mosaic virus (X. americanum, X. revesi,
cline markedly, producing fewer shoots until ultimately vines
and L. diadecturus); Arabis mosaic virus (X. diversicaudatum);
are totally unproductive. Besides its direct damage to plant
Raspberry ringspot virus (L.  elongatus, L. macrosoma, and
roots, this nematode is also a vector of Grapevine fanleaf virus
P.  maximus); Tomato black ring virus (L.  attenuates and
(GFLV), and infestations of X. index that are viruliferous have
L. elongatus), and Artichoke Italian latent virus (L. attenuatus).
even more devastating effects on vineyards. Xiphinema vuit-
In addition, the sadwavirus Strawberry latent ringspot virus is
tenezi Luc, Lima, Weischer & Flegg is most common in Eu-
vectored by X. diversicaudatum.
rope, although it also is reported from other locations; direct
damage associated with the species plus its ability to vector Life Cycle and Epidemiology
Nepoviruses make it a serious pest. Xiphinema diversicau-
Dagger and needle nematodes hatch from eggs as first-­stage
datum (Micoletzky) Thorne also is most common in Europe
juveniles and most molt four times in the soil to become adults
but found elsewhere as well. Xiphinema americanum Cobb is
(Fig. 269). Those within the X. americanum species complex
considered a complex of morphologically similar species and
are reported to have only three juvenile stages. Adults resemble
relationships within the group will no doubt become clearer
the young, remaining vermiform without swellings or modi-
with application of molecular technologies. Xiphinema ameri-
fications such as cysts. The duration of the cycle from egg to
canum sensu lato is widespread in the United States but less
adult female in X. index varies by region. It has been reported
so in European vineyards. Although not a strong pathogen of
as 22–27 days in California, a very short time for a nematode
grapevines unless present at very high population densities, it
with such a large body size, and as 7–9 months in Israel; rea-
also can cause damage as a vector of Tomato ringspot virus
sons for such a difference are not known. Xiphinema index has
(ToRSV, a serious problem on some interspecific hybrid cul-
been reported to survive in soil for up to 4 years; its survival
tivars in eastern North America) and Tobacco ringspot virus
in vineyard soils following vine removal is extended when
(TRSV).
At least 15 species of needle nematodes, Longidorus spp., are
reported from vineyard soils worldwide. Of these, L. africanus
has been described as causing necrosis and malformations of
grape roots. The remaining species have not been studied and
are known only as part of recorded collections.
Both dagger and needle nematodes cause slow, gradual de-
cline, seldom killing the vines outright. Once decline caused
by these nematodes begins, little can be done to restore the
affected vines’ vigor and productivity. When these species
also transmit plant viruses, their effects are significantly more
devastating.

Symptoms
The root system of a vine attacked by X. index, X. vuittenzi,
or X. diversicaudatum exhibits terminal root galls and many
dead feeder roots if population levels are high (Fig. 268). Most
feeding takes place near root tips, where proliferation and en-
largement of affected cells often causes a bending of the root
accompanied by slight swelling. Multiple prolonged attacks can Fig. 268. Roots damaged by dagger nematodes (left and center)
result in darkened, necrotic spots that spread over the entire compared with healthy roots (right). (Cour­tesy D. J. Raski)

139
 Fig. 269. Life cycle of the dagger nematode. (Cour­tesy D. J. Raski; drawing revised by R. Sticht)

residual grape roots remain alive. The longevity of X. ameri- site during or between molts, virus particles are readily reac-
canum individuals is 3–5 years, with only one generation pro- quired when feeding commences again. Xiphenema index is
duced per year. able to retain GFLV for at least 4 years in the absence of host
Dagger and needle nematodes are strictly ectoparasitic. They plants, revealing an extremely long survival and viral retention
feed by means of a very long stylet that they use to penetrate period within that nematode.
the root tip cells. Their feeding alters cells in the meristematic Vectoring of plant viruses by dagger nematodes has been
region, leading to hypertrophy and hyperplasia, and commonly most thoroughly studied in the X. index/GFLV system. Ac-
the nematode feeds from several enlarged nurse cells. Each ju- quisition of the virus by the nematode occurs passively as the
venile stage must feed before it can molt and continue growth. nematode withdraws plant cell contents through the stylet. The
Reproduction in most species is parthenogenic and males often virus particles selectively adhere to the cuticular lining of the
are rare or unknown, although they are present in about the esophageal lumen and are lost when that cuticle is molted. Par-
same numbers as females in a few species. These nematodes ticles are thought to be released from the esophageal cuticle
spread to new fields primarily by transport of infected planting when nematode enzymes are secreted into the plant cell. The
material or as a result of cultural practices that move infested virus does not seem to directly harm the nematode beyond
soil, sometimes in contaminated irrigation water. its effects on debilitating or killing the host plant. The virus
Upon acquisition of appropriate Nepoviruses, needle nema- particles do not replicate in the nematode and are not passed
todes retain the virus particle on the inner surface of the stylet, through the egg stage to the juveniles.
whereas virus particles bind to the esophageal lining of dagger
nematodes. Those cuticular portions of the nematode digestive Selected References
system are shed during the molts between developmental stages
so that the adhering virus is also lost and must be reacquired Cohn, E., and Mordechai, M. 1969. Investigations on the life cycles
by the nematode during subsequent feeding events. Since the and host preference of some species of Xiphinema and Longidorus
nematodes probably do not move far from the root-­tip feeding under controlled conditions. Nematologica 15:295-­302.

140
Decraemer, W., and Robbins, R. T. 2007. The who, what and where of vines. Other species from this family also may occur in the
Longidoridae and Trichodoridae. J. Nematol. 39:295-­297. vineyard feeding on roots of weeds or ground cover. The
Demangeat, G., Voisin, R., Minot, J. C., Bosselut, N., Fuchs, M., and common name of the ring nematode is derived from its thick,
Esmenjaud, D. 2005. Survival of Xiphinema index in vineyard soil deeply striated cuticle, which gives the nematode the appear-
and retention of Grapevine fanleaf virus over extended time in the ance of being surrounded by a sequence of collocated rings. In
absence of host plants. Phytopathology 95:1151-­1156. some areas additional nematodes in the same family, includ-
Ferris, H., and McKenry, M. V. 1974. Seasonal fluctuations in the spa-
tial distribution of nematode populations in a California vineyard.
ing the sheathoid nematode Hemicriconemoides californianus
J. Nematol. 6:203-­210. Pinochet & Raski and other Hemicriconemoides species have
Ferris, H., and McKenry, M. V. 1975. Relationship of grapevine yield been reported from vineyards. These nematodes have the pro-
and growth to nematode densities. J. Nematol. 7:295-­304. tection of a double cuticle and appear to have similar parasitic
Halbrendt, J. M., and Brown, D. J. F. 1992. Morphometric evidence habits as M. xenoplax.
for three juvenile stages in some species of Xiphinema americanum
sensu lato. J. Nematol. 24:305-­309. Life Cycle and Epidemiology
Martelli, G. P. 1978. Nematode-­borne viruses of grapevine, their epi- Adult stages of M. xenoplax are sedentary ectoparasites
demiology and control. Nematol. Mediterr. 6:1-­27. with a life cycle of 30–60 days. It is likely that roots encoun-
Pinochet, J., Raski, D.  J., and Goheen, A.  C. 1976. Effects of Prat- ter ring nematode adults as they grow, rather than the nema-
ylenchus vulnus and Xiphinema index singly and combined invine todes actively migrating toward roots. However, juvenile stages
growth of Vitis vinifera. J. Nematol. 8:330-­335. are more active and are likely involved in moving toward host
Robbins, R. T. 1993. Distribution of Xiphinema americanum and re- roots. Once the stylet has been inserted into plant tissue, the
lated species in North America. J. Nematol. 25:344-­348.
nematodes remain at that location, somewhat protected from
Taylor, C.  E., and Brown, D.  J.  F. 1997. Nematode vectors of plant
viruses. CAB International, Oxford, UK.
other rhizosphere organisms by their thick cuticle. In a time
frame similar to that of root-­k not nematodes, ring nematodes
(Prepared by I. A. Zasada, H. Ferris, and M. V. McKenry) can develop to very high population levels in porous soils. Ring
nematodes population densities are highest in areas where
grape roots are most abundant, usually within the top 45 cm
of soil.
Ring Nematode
Selected References
The ring nematode, Mesocriconema xenoplax, was first re-
Brzeski, M., Loof, P. A. A., and Choi, Y. E. 2002. Compendium of the
ported from California in 1952, and has been subject to sev- genus Criconemoides Taylor, 1936 (Nematoda: Criconematidae).
eral taxonomic reclassifications since then. This status remains Nematology 4:325-­339.
unsettled, and both the names Mesocriconema xenoplax and Brzeski, M., Loof, P.  A.  A., and Choi, Y.  E. 2002. Compendium of
Criconemoides xenoplax appear in current literature. Herein, the genus Mesocriconema Andrássy, 1965 (Nematoda: Criconema-
we use Mesocriconema for the generic reference. tidae). Nematology 4:341-­360.
The ring nematode is a migratory ectoparasite of plant roots. Decraemer, W., and Hunt, D. 2006. Structure and classification. Pages
It does not enter the root but feeds deep into root tissues using 3-­32 in: Plant Nematology. R. N. Perry and M. Moens, eds. CAB
a long, stout stylet. Since the nematodes are relatively inactive, International, Oxford, UK.
they do not readily pass through the tissue barrier of the Baer- Ferris, H., Zheng, L., and Walker, M. A. 2013. Soil temperature effects
mann funnel commonly used for extracting most other nema- on the interaction of grape rootstocks and plant-­parasitic nema-
tode species. Consequently, they are not readily detected by that todes. J. Nematol. 45:49-­57.
method and must be extracted by alternative methods that float Klingler, J. 1975. Observations on the parasitic activity of the nema-
the nematodes from soil rather than rely on their active move- tode Macroposthonia xenoplax on grape vine roots. Z. Pflanzen-
krankh. Pflanzenschutz 82:722-­728.
ment. Because of this inefficiency of detection by means of
Pinkerton, J. N., Schreiner, R. P., Ivors, K. L., and Vasconcelos, M. C.
common methodology, it is highly likely that the importance of 2004. Effects of Mesocriconema xenoplax on Vitis vinifera and as-
the ring nematode in grape vineyards has been underestimated. sociated mycorrhizal fungi. J. Nematol. 36:193-­201.
Pinochet, J., and Raski, D.  J. 1975. Four new species of the genus
Symptoms Hemicriconemoides (Nematoda: Criconematidae). J. Nematol.
Porous soils such as sands, coarse sandy loams, or well-­ 7:263-­270.
aggregated clay loams appear necessary for the development of Santo, G.  S., and Bolander, W.  J. 1977. Effects of Macroposthonia
the ring nematode at the high population levels associated with xenoplax on the growth of Concord grape. J. Nematol. 9:215-­217.
symptom expression on vines. Damage by ring nematodes often
results in reduction of small feeder roots, and there may be a (Prepared by I. A. Zasada, H. Ferris, and M. V. McKenry)
“witches’-broom” appearance of small roots emanating from
larger roots below the tillage zone. Almost all grapevine cultivars
and rootstocks are susceptible to the ring nematode; vines exhib-
iting the greatest aboveground damage appear to be those with Root-­knot Nematodes
the least inherent vigor, including such cultivars as Chardonnay
and Pinot Noir. In severe cases, more than half the buds along a Root-­k not nematodes were first found and described on spe-
cordon or spur may fail to develop. Current season growth that cies of Vitis in Florida in 1911. Since then, at least seven species
develops from an apparently healthy spur can appear as a mass of Meloidogyne have been reported from vineyards worldwide
of worthless twigs. In a few vineyards, leaves on affected plants and this number is likely to increase as molecular identification
have been observed to exhibit interveinal necrosis by early sum- methods are employed to distinguish between morphologically
mer. Ring nematode may also negatively impact vine associa- similar forms currently assigned to a single taxon. Currently,
tions with arbuscular mycorrhizal fungi, suppressing arbuscule the species reported most frequently and considered the most
frequency and leading to symptoms of phosphorus deficiency. damaging are M. hapla, which is dominant in cooler regions
of the world, and M. incognita, M. arenaria, and M. javanica,
Causal Organisms which are common in warmer regions. Specific rootstocks once
Within the Criconematidae family, Mesocriconema xeno- considered as resistant to Meloidogyne spp. can become highly
plax (Raski) Loof & de Grisse (= Criconemoides xenoplax susceptible to certain Meloidogyne populations or pathotypes
Raski) is the primary species associated with damage to grape- over time.

141
Symptoms Chile; and M. chitwoodi Golden, O’Bannon, Santo & Finley
The distinctive response of grape roots to root-­knot nematodes from California. Biotypes within the nematode species differ
is the production of small swellings or galls on young feeder in their virulence to grapevine cultivars and rootstocks. As
roots or secondary rootlets (Fig. 270). Larger galls may result resistant rootstocks are deployed, the diversity of virulence
from multiple infections. The galling response varies across among root-­k not nematode species gradually becomes appar-
cultivars and rootstocks. For example, galls are barely visible ent through the selection of virulent pathotypes.
on Teleki 5C, Schwarzmann, or RS-­3 rootstocks and nematode
feeding sites and galls are restricted to new roots. Other root- Life Cycle and Epidemiology
stocks, including 99R and 110R do not exhibit galls but wash- Root-­k not nematode females do not retain their eggs; they
ing of the roots can reveal the presence of numerous glistening, deposit them outside their bodies, typically in a mass of 400–
reproductive adult females along root surfaces. Root-­knot resis- 500 (occasionally up to 1,500) eggs within a gelatinous matrix
tant rootstocks, like the UCD-­GRN series and others, do not that is secreted by glands in the posterior region of the body.
gall and do not support nematode development and reproduc- The matrix is usually located on the outside of the root but may
tion. The galling response also differs with nematode species; be inside and completely surrounded by root tissue. The em-
for example, penetration of susceptible roots by M. hapla or bryo within the egg develops into a juvenile nematode, molts
M.  chitwoodi may result in very small galls or indiscernible once, and emerges from the egg as a second-­stage juvenile, the
swellings. Among other root-­knot species, gall size can be larger migratory and infective stage. Their root penetration capabili-
or smaller depending on the specific host genotype attacked. ties are restricted to a zone just behind the growing root tip;
When the galls are broken apart, the tiny, glistening, white bod- however, some also appear to successfully reinvade maternal
ies of mature females can be detected with the aid of a hand feeding sites, thus perpetuating a survival of galls on the roots
lens. Gelatinous egg masses are often attached to the female that may last a decade. Following penetration, the juveniles
bodies. Second-­stage juveniles and males can be found only by quickly migrate toward the root cap, then reverse direction and
microscopic examination after extracting nematodes from soil. migrate toward developing vascular tissues where they estab-
Usually, the size of root systems of grapevines damaged by root-­ lish a feeding site and complete their life cycle as sedentary
knot nematodes is severely limited, with few feeder roots. endoparasites. The plant response to their feeding is the pro-
Root-­k not nematodes cause their greatest damage in newly duction of undifferentiated, multinucleate, thick-­walled “giant
replanted vineyards with high populations of nematodes asso- cells” within the vascular region. Typically, a gall becomes
ciated with the previous vines. Young vines, which may already visible within 15 days after nematode entry, although there are
be weakened owing to other replant factors, fail to establish exceptions with different rootstocks. Galls are barely visible on
an effective root system under the nematode pressure. Vines Teleki 5C, Schwarzmann, or RS-­3 rootstocks and their feed-
that do become established may be weak and fail to grow suf- ing sites and galls are restricted to new roots. Rootstocks such
ficiently to permit training onto trellises. Root-­k not nematodes as 99R and 110R do not exhibit galls but washing of the roots
seldom kill vines; more often, plants decline in vigor and be- can reveal the presence of numerous glistening, reproductive
come more susceptible to other stress factors. On occasion, adult females along root surfaces. Penetration by M. hapla or
scorching of leaves, cordons, and even the berries may occur M. chitwoodi does not yield readily visible galls. Among other
on devigorated, nematode-­infected vines. Yields of infested root-­k not species, gall size can be larger or smaller depending
blocks may be less than half those of healthy vineyards in the on the specific host genotype attacked.
same region. Greatest damage by root-­k not nematodes usually Second-­stage infective juveniles emerging from eggs have
occurs in vineyards planted in sandy soils in areas where higher sufficient energy reserves at 25°C to persist for about 2 weeks,
soil temperatures are experienced. during which time they must penetrate the roots and establish
feeding sites. Once established, the juveniles commence to
Causal Organisms feed, become enlarged, pass through two more developmental
Root-­k not nematodes are members of the genus Meloidogyne stages without further feeding, and become adult, pear-­shaped
Goeldi. The four species currently considered to have greatest females. The life cycle from egg to egg takes about 25 days at
impact on grape production are M. incognita (Kofoid & White) 25°C, and at this temperature adult females may survive ap-
Chitwood, M. javanica (Treub) Chitwood, M. arenaria (Neal) proximately 60 days. Meloidogyne incognita, M. javanica, and
Chitwood, and M. hapla Chitwood. Other root-­k not nematode M. arenaria can complete five to six generations while temper-
species reported on grapevines include: M. nataliei Golden, ature and other conditions are favorable for nematode and plant
Rose & Bird from Michigan; M. ethiopica Whitehead from physiological activity. With approximately 500 eggs produced
per female within each generation, the potential for population
increase during a single growing season is enormous. When
vines enter dormancy, root-­k not nematodes overwinter princi-
pally as developing juveniles inside eggs within the gelatinous
matrix of the egg mass.
Root-­k not nematodes are mostly parthenogenic, i.e., females
produce viable eggs without fertilization by a male. Males are
rare or absent from the soil but may become apparent when
roots become overcrowded or in response to other conditions
unfavorable to the nematodes. The life cycle of a male is similar
to that of a female up to the third juvenile stage. At that point,
a metamorphosis takes place and the enlarged body is reor-
ganized into a coiled-­worm shape, which emerges as an adult
male from the cuticle of the fourth stage juvenile.
In deep vineyard soils, root-­k not nematodes can be found
wherever roots occur, but they are most prevalent at a depth of
15–90 cm. Even after the removal of a vineyard, old grapevine
roots can remain alive and support root-­k not nematode popu-
Fig. 270. Roots of cv. Cabernet Sauvignon vine damaged by root-­ lations for 8 years or more. Additionally, root-­k not nematode
knot nematodes, with galls and swellings on secondary rootlets. species have wide host ranges and are sustained and increased
(Cour­tesy D. J. Raski) on both weed and crop hosts that follow the vineyard.

142
 Selected References tensis (de Man) Filipjev; P. zeae Graham; P. hexincisus Taylor
& Jenkins; P. coffeae Zimmermann; P. crenatus Loof; and
Anwar, S. A., and McKenry, M. V. 2002. Development response of a P. thornei Sher & Allen.
resistance-­breaking population of Meloidogyne arenaria on Vitis
The genus Zygotylenchus Siddiqi belongs to the same nema-
spp. J. Nematol. 34:28-­33.
Anwar, S.  A., McKenry, M.  V., and Faddoul, J. 2001. Reproductive
tode family as Pratylenchus. A few records of Zygotylenchus
variability of field populations of Meloidogyne spp. on grape root- spp. have been published in surveys of vineyard soils, but noth-
stock. J. Nematol. 32:265-­270. ing more is known about their abundance, general incidence, or
Cain, D. W., McKenry, M. V., and Taralio, R. E. 1984. A new patho­ significance in grape production.
type of root-­ k not nematode on grape rootstocks. J. Nematol.
16:207-­208. Life Cycle and Epidemiology
Carneiro, R. M. D. G., Almeida, M. R. A., Cofcewicz, E. T., Magu- Root-­lesion nematodes are migratory and endoparasitic in
nacelaya, J.  C., and Aballay, E. 2007. Meloidogyne ethiopica, a life habit, spending a portion of their lives in the soil and a por-
major root-­ k not nematode parasitizing Vitis vinifera and other tion in root tissues. The female deposits eggs singly in the soil
crops in Chile. Nematology 9:633-­639. or in root tissues. The young develop and elongate in the egg,
Ferris, H., and McKenry, M. V. 1974. Seasonal fluctuations in the spa- molt once, and emerge as second-­stage juveniles. The nematode
tial distribution of nematode populations in a California vineyard. invades host roots and moves through the cortex, penetrating,
J. Nematol. 6:203-­210. feeding on, and killing cells. All juvenile stages and adults are
Ferris, H. 1976. Observations on the distribution of Meloidogyne spp.
capable of invading roots and feeding. Most Pratylenchus spp.
in a vineyard soil. J. Nematol. 8:183-­184.
Ferris, H., Schneider, S. M., and Stuth, M. C. 1982. Probability of pen- are parthenogenic; however, in some species, such as P. vulnus,
etration and infection by Meloidogyne arenaria in grape cultivars. males are common and sexual reproduction occurs.
Am. J. Enol. Vitic. 33:31-­55.
Ferris, H., Zheng, L., and Walker, M.  A. 2012. Resistance of grape Selected References
rootstocks to plant-­parasitic nematodes. J. Nematol. 44:377-­386.
Allen, M. W., and Jensen, H. J. 1951. Pratylenchus vulnus, new spe-
McKenry, M.  V. 1984. Grape root phenology relative to control of
cies (Nematoda: Pratylenchinae), a parasite of trees and vines in
parasitic nematodes. Am. J. Enol. Vitic. 35:206-­211.
California. Proc. Helminthol. Soc. Wash. 18:47-­50.
Pinochet, J., and Raski, D. J. 1977. Observations on the host-­parasite
(Prepared by I. A. Zasada, H. Ferris, and M. V. McKenry) relationship of PratyIenchus vulnus on grapevine, Vitis vinifera.
J. Nematol. 9:87-­88.
Pinochet, J., Raski, D.  J., and Goheen, A.  C. 1976. Effects of Prat-
ylenchus vulnus and Xiphinema index singly and combined invine
Root-­lesion Nematodes growth of Vitis vinifera. J. Nematol. 8:330-­335.
Puerari, H. H., Dias-­Arieira, C. R., Moura, M. F., Biela, F., Chiamolera,
Root lesion nematodes (Pratylenchus spp.) are commonly en- F.  M., and da Cunha, T.  P.  L. 2012. Reaction of grapevine root-
countered in vineyard soils, although in many cases there has stocks to Pratylenchus brachyurus and Pratylenchus zeae. Trop.
been no attempt to identify these nematodes to species. Ten spe- Plant Pathol. 37:220-­222.
cies have been identified but only a few have been tested for Sauer, M.  R. 1962. Distribution of plant-­parasitic nematodes in ir-
their pathogenicity to grapevines. Pratylenchus vulnus is re- rigated vineyards at Merbein and Robinvale. Aust. J. Exp. Agric.
ported from California, Spain, and Australia and has received Anim. Husb. 2:8-­11.
Walker, G., and Morey, B. 2000. Effects of lesion nematodes associ-
the most research attention. The presence of P. zeae in Australia
ated with cereals on grapevine growth. Aust. Grapegr. Winemaker
and Brazil and P. brachyurus in Brazil may also warrant con- 438:130-­132.
cern. The remaining species have limited distribution or are as-
sociated primarily with ground covers present in the vineyard. (Prepared by I. A. Zasada, H. Ferris, and M. V. McKenry)
Damage caused by root-­lesion nematodes can be severe, but
almost exclusively in settings where vines are planted following
removal of an orchard crop upon which they develop far more
readily and have achieved high population levels. An early at- Miscellaneous Ectoparasitic
tack by root-­lesion nematodes particularly inhibits growth of
the main root system. Vineyard plantings that have not grown Nematodes
well for their first decade for this reason often can be invigo-
rated by a series of nematicide treatments. Upon receiving ade- Surveys in several countries have revealed a wide array of ec-
quate protection, the vine can develop a new root system that toparasitic species in vineyard soils, including: pin nematodes,
outgrows subsequent increases in the nematode population. Paratylenchus spp., especially P. hamatus; reniform nema-
todes, Rotylenchulus spp.; spiral nematodes, Helicotylenchus
Symptoms spp.; lance nematodes, Hoplolaimus spp. and Rotylenchus spp.;
There are no specific symptoms on grapevines that are di- stubby-­root nematode, Paratrichodorus minor (Allen) Siddiqi;
agnostic for root-­lesion nematode damage. Root systems ex- and stunt nematodes, Tylenchorhynchus (syn. Telotylenchus)
hibit poor development, including an absence of major roots spp. The importance of these nematodes to grape production is
and many dead feeder roots. Occasionally, rootlets are killed poorly understood.
shortly after they are produced. In some hosts, certain phenolic
compounds are oxidized, causing necrosis and lesion formation Selected References
at feeding sites, but these symptoms are rare on grapevines.
The two best indications of the presence of these nematodes are Ferris, H., and McKenry, M. V. 1975. Relationship of grapevine yield
and growth to nematode densities. J. Nematol. 7:295-­304.
the cropping history of the soil and appropriate soil sampling.
Ferris, H., and McKenry, M. V. 1976. Nematode community structure
in a vineyard soil. J. Nematol. 8:131-­137.
Causal Organisms Ferris, H., and McKenry, M.  V. 1976. A survey of nematode dis-
Root-­lesion nematodes are members of the genus Pralylenchus tribution in California vineyard soils. J. Am. Soc. Hortic. Sci.
Filipjev. Species that have been reported from vineyards world- 101:332-­336.
wide are: P. vulnus Allen & Jensen; P. brachyurus (Godfrey) Mohamed, R. M. S. 2009. Plant parasitic nematodes associated with
Filipjev & Schuurmans Stekhoven; P. scribneri Steiner; P. ne- grapevine in Sana’a and Sadah Governorates of Yemen. Mansoura
glectus (Rensch) Filipjev & Schuurmans Stekhoven; P. pra- J. Agric. Sci. 34:1339-­1345.

143
Raski, D. J. 1955. Additional observations on the nematodes attacking in soil that is not known to be free of pest nematode species.
grapevines and their control. Am. J. Enol. Vitic. 6:29-­31. Nematodes are easily moved and introduced on soil adhering
Raski, D. J., and Radewald, J. D. 1958. Reproduction and symptom- to vehicles, implements, and animals; ensure that such poten-
atology of certain ectoparasitic nematodes on roots of Thompson tial sources are eliminated by appropriate sanitation practices.
seedless grape. Plant Dis. Rep. 42:941-­943. Nematodes are also moved and introduced by water, either
Sulan, L., Puchao, H., and Dongting, Z. 2003. Investigation on para- through flooding or runoff or through irrigation with water
sitic nematodes associated with the wild grapes native to China.
Acta Hortic. Sin. 30:127-­130.
drained from neighboring fields or drawn from rivers that
have passed through infested areas. Several tactics of varied
(Prepared by I. A. Zasada, H. Ferris, and M. V. McKenry) effectiveness have been tested and implemented for reducing
infestation levels of irrigation water, including redesign of the
supply system, settling ponds, use of water from deep wells,
and ozone treatment.
Vineyard establishment. Soil preparation. Several prepara-
Nematode Management tory measures and decisions must be made prior to planting.
Deep tillage may be necessary to disrupt restrictive layers that
Effective nematode management programs for grape vine- may be naturally occurring or that have resulted from previous
yards rely on a suite of practices. If an area is free of damaging cultural practices. Some nematodes are susceptible to soil dis-
species of plant-­parasitic nematodes, every precaution should turbance. For example, population levels of large-­bodied dag-
be taken to exclude them, as nematode infestations are perma- ger nematodes, Xiphinema spp., can be reduced by repeated
nent once established. Since the 1950s, control programs in tillage of fallow soil. However, this practice can be detrimental
vineyards have been centered on nematicidal chemicals. How- to soil structure and does not affect nematodes below the tilled
ever, as the availability of such chemicals becomes progres- profile.
sively more regulated, strategies based on nematode ecology Population levels of potentially harmful nematode species
and hostplant resistance or tolerance become increasingly im- may be reduced by rotation with appropriate nonhost or resis-
portant alternatives. In essence, current and evolving nematode tant crop species. Cover crops and organic amendments may be
management strategies are increasingly information-­based and used to build soil carbon levels and to provide resources for the
require consideration of the host ranges, life cycles, survival beneficial organisms of the soil food web.
strategies, and longevity of the plant-­parasitic nematode spe- Soil fumigation. Application of fumigant nematicides can
cies present in a vineyard. Knowledge of the ability of resident be an effective way to reduce plant-­parasitic nematode popula-
nematode species to feed upon the grape rootstock and cover tions prior to planting; the availability of soil fumigants varies
crops present, and an appreciation for the importance and stew- depending upon location. Soil fumigants that have been widely
ardship of natural regulators of pest species populations, are used in vineyards include 1,3-­dichloropropene, metam sodium,
required. Important decisions must be made, and practices im- and chloropicrin. Proper planning to ensure adequate soil prep-
plemented, prior to vineyard establishment. Continued moni- aration and conditions at the time of treatment are the keys to
toring and management of soil health are necessary throughout successful fumigation.
the development and productive cycle of the vineyard. Damage Rootstocks. One of the most important decisions prior to
from plant-­parasitic nematodes is much less common in soils planting is the selection of a cultivar or rootstock that is resis-
with physical, chemical, and biological characteristics that sus- tant to, or tolerant of, the plant-­parasitic nematodes present in
tain plant growth while maintaining biological homeostasis the specific site or that are known to exist in the general area.
and providing beneficial ecosystem services such as organic Rootstocks available for grapevines differ in their susceptibil-
matter decomposition, nutrient cycling, and water purification. ity to nematodes, and various selections have been developed
and released in recent years that have resistance to several
Preplant Management species of plant-­parasitic nematodes. Besides their nematode-­
Field assessment. Fields should be sampled to determine the resistance characteristics, it is important to select rootstocks
diversity and abundance of plant-­parasitic nematodes prior to that have appropriate vigor and horticultural characteristics for
planting a vineyard. Nematode population densities are high- the local conditions. A summary of available data on the sus-
est in the fall, and assessments at this time are most indicative ceptibility of various rootstocks to individual nematode species
of the damage potential. Both soil and root samples must be is provided in Table 6.
collected; root samples provide a better diagnostic measure of Vineyard renovation. Replanting a vineyard that has de-
population densities of root lesion nematode. The distribution clined in productivity provides special challenges because the
of plant-­parasitic nematodes in a field tends to be patchy and is biological, chemical, and physical causes of the decline may
determined by soil conditions and previous management his- still be present in the soil. Old vines must be extracted with
tory. Therefore, samples for nematode analysis should consist equipment that removes the greatest possible root mass from
of composites of soil cores or subsamples representing each the soil profile. There may be advantages in applying an appro-
area of the field that appears reasonably uniform in terms of priate herbicide to vine stumps before their removal so that root
soil texture and previous crop vigor. One such composite sam- fragments remaining in the soil are killed and do not provide a
ple of about 20 cores or subsamples should be collected per 2–5 resource for pest nematode survival. Following vine removal,
hectares of the field. Sample depth may vary with the root pro- cultural practices such as fallow, crop rotation, or cover crop-
file of the previous crop, but generally samples taken to a depth ping may be implemented to reduce survival and reproduction
of 30 cm are appropriate. If the previous crop is still in the field, of resident nematode populations.
samples should be taken from the root zone of these plants in When a vineyard is removed, a crop-­rotation period should
areas where active root growth has been favored, e.g., within be allowed before replanting in order to limit nematode pressure
zones of irrigation when used. Samples should be clearly la- on the new planting. Rotations may include nonhosts, resistant
beled and kept cool until processed by a diagnostic laboratory. hosts, allelopathic plants, fallow, trap crops, or green manures.
Exclusion. Plant-­parasitic nematodes have become estab- The length of rotation necessary for good nematode manage-
lished in vineyards throughout the world because they were ment depends upon the survival capabilities of the target spe-
introduced with rooted planting material. Where nursery cies, with a shorter time period for the citrus nematode (1 year)
certification programs are available, only certified nematode-­ and longer for dagger nematodes (≥4 years). If a fallow period is
free stock should be planted. There is a high risk of introduc- implemented, good weed management must be achieved since
ing nematodes in rooted cuttings that have been propagated many weeds are hosts to nematodes. The selection of a rotation

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or cover crop should be made with knowledge of the host range However, at least one rootstock, O39-­16, which is resistant to
of the target plant-­parasitic nematode. Options may be limited X. index, also confers tolerance to the virus and vines remain
for root knot nematodes, which have a very broad host range, productive for long periods even though they are infected.
and more abundant for the citrus nematode, which has only a
few known hosts. Ring nematode also has a wide host range, Postplant Management
including grasses and, particularly, legumes. Nemabase, a data- Vine health. The decline in vigor of vines damaged by nema-
base on the Nemaplex website (http://plpnemweb.ucdavis.edu/ todes can be slowed or offset in part by providing more frequent
Nemaplex) maintained by University of California, Davis has irrigation, improving soil water-­holding capacity, avoiding over
over 47,000 records on the nematode host status of plants, a cropping, applying fertilizer levels to support a limited root
valuable resource when selecting rotation and cover crops for system, and controlling other diseases and pests that stress the
vineyard renovation. vines. Drip irrigation systems allow frequent irrigation and fer-
Virus vector considerations. For nematodes that are vectors tilizer application to alleviate nematode stress on vines.
of plant viruses, such as dagger nematodes, very low numbers of Postplant nematicides. As with soil fumigants, the avail-
viruliferous individuals can cause serious damage by transmit- ability of registered postplant nematicides varies among grape-­
ting virus particles to new vines. Xiphinema index and the X. producing regions and countries. Postplant nematicides that
americanum species complex are two taxa that are particularly have proven effective in vineyards are drip-­applied sodium
important in this regard, and it is important to attempt elimina- tetrathiocarbonate or 1,3-­ dichloropropene and foliar-­ applied
tion of these species prior to establishing a new vineyard. In the systemic spirotetramat. The advantage of a systemic material
past, this has been attempted through the use of high rates of is that relatively small applied quantities can move to the plant-­
soil fumigants. Where such practices are no longer available, nematode interaction zone at the root surface, avoiding treat-
a long nonhost crop rotation may be necessary. X. america- ment of the entire soil volume potentially occupied by the root
num, vector of Tomato ringspot virus (ToRSV) and Tobacco system. Because of the complex carbon dynamics in perennial
ringspot virus, has a wide host range. However, Brassica and plants such as grapevines, repeated applications of nematicides
grass cover crops, although supporting nematode feeding, are over time may be necessary to realize yield benefits. Once a
not hosts of the grapevine Nepoviruses, and new generations of previously-­damaged plant is protected from nematode damage,
the nematode are virus-­free after a 2-­year rotation with them. some time is required to rebuild its root system to the point that
Management of broadleaf weeds is an important component of productive vine growth is supported.
this strategy because many are hosts for ToRSV. X. index, vec-
tor of Grapevine fanleaf virus, has a narrow host range con- Selected References
sisting primarily of woody perennial plants. Some rootstocks Ferris, H. 2010. Contribution of nematodes to the structure and func-
are available with resistance to X. index, although this does not tion of the soil food web. J. Nematol. 42:63-­67.
necessarily confer resistance to the virus because the nema- Ferris, H., Zheng, L., and Walker, M.  A. 2012. Resistance of grape
tode may transmit particles during exploratory stylet thrusts. rootstocks to plant-­parasitic nematodes. J. Nematol. 44:377-­386.

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Ferris, H., Zheng, L., and Walker, M. A. 2013. Soil temperature effects Pinkerton, J.  N., and Martin, R.  R. 2008. Management of tomato
on the interaction of grape rootstocks and plant-­parasitic nema- ringspot virus in red raspberry with crop rotation. Int. J. Fruit Sci.
todes. J. Nematol. 45:49-­57. 5:55-­67.
Halbrendt, J. M., and LaMondia, J. A. 2004. Crop rotation and other Reisch, B. I., Owens, C. L., and Cousins, P. S. 2012. Grape. Pages
cultural practices. Pages 909-­930 in: Nematology, Advances and 225-­262 in: Fruit Breeding (Handbook of Plant Breeding). M. L.
Perspectives, Vol. 2: Nematode Management and Utilization. Z. X. Badenes and D.  H. Byrne, eds. Springer, Rueil-­ Malmaison,
Chen, S.  Y. Chen, D.  W. Dickson, eds. CAB International, Wall- France.
ingford, UK. Zasada, I.  A., Halbrendt, J.  M., Kokalis-­Burelle, N., LaMondia, J.,
McKenry, M.  V. 1999. The Replant Problem and Its Management. McKenry, M.  V., and Noling, J.  W. 2010. Managing nematodes
Catalina Publishing, Fresno, CA. without methyl bromide. Annu. Rev. Phytopathol. 48:311-­328.
Nicol, J. M., Stirling, G. R., Rose, B. J., May, P., and Van Heeswijck, R.
1999. Impact of nematodes on grapevine growth and productivity: (Prepared by I. A. Zasada and H. Ferris)
Current knowledge and future directions, with special reference to
Australia. Aust. J. Grape Wine Res. 5:109-­127.

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