18 Diseases of Passion Fruit PDF

Tropical Fruit - Chap 18 7/5/03 1:08 PM Page 413
18 Diseases of Passion Fruit
Barry Manicom1, Carlos Ruggiero2, Randy C. Ploetz3 and

Antonio de Goes2
1Institute of Tropical and Subtropical Crops, Nelspruit, Republic of South Africa;
2UNESP, Campus Jaboticabal, Jaboticabal, Brazil; 3University of Florida, Tropical
Research and Education Center, Homestead, Florida, USA
Introduction all but three of these are native to the New

World. Fifty or 60 species in the genus pro-
Passion flowers were valued ornamentals in duce edible fruit, but relatively few of these
Europe as early as 1610, and created a sensa- are palatable, and fewer still are significant as
tion when the first specimens arrived from fruit crops (Martin and Nakasone, 1970).
the New World (Killip, 1938). Jacomo Bosio, Three major factors determine the useful-
a monk in Rome, saw in the flower structure ness of a species of Passiflora in a given area:
symbols of the passion of Christ and called it (i) adaptation to temperature and elevation;
‘Flos passionis’. From this association came (ii) self-incompatibility; and (iii) reaction to
the plant’s common and scientific names. important diseases (Purseglove, 1968).
The leaves of some species are used as a Several species that produce desirable fruit
substitute for tea, and the leaves and roots of do so only at high elevations that have cool
others have medicinal properties. However, night temperatures, whereas other species
fruit are the most significant economic prod- that do well in the humid lowland environ-
uct of members of the Passifloraceae. The aro- ments of the tropics do not tolerate the for-
matic pulp that surrounds the seed of several mer conditions. Self-incompatible types
species is used in sherbets, jams and jellies. must be cross-pollinated, either by hand or
The juice is a natural concentrate and will by insects (usually bees), in order for fruit to
impart its distinctive flavour to beverage and set. This can be a serious constraint in com-
dessert items even when highly diluted (Chan, mercial production. Diseases can seriously
1980). Purees and punches, in which its juice is reduce the productivity of all of the species
added to those of orange, banana, papaya and that are important commercially. Due to their
guava, are popular tropical drinks. impact, most plantations around the world
are productive for 5 or less years (Rínderman
and Cruz, 1997).
Origins, Taxonomy and Traits
The Passifloraceae contains ⬃500 species and The Important Species

12 genera (Purseglove, 1968). They are peren-
nial herbaceous and woody plants that usually P. edulis is the most common and important
have a vine-like growth habit. The most impor- species. It originated in southern Brazil, but
tant genus, Passiflora, contains ⬃400 species; was widely distributed in the tropics and
© CAB International 2003. Diseases of Tropical Fruit Crops (ed. R.C. Ploetz) 413
414 B. Manicom et al.
subtropics during the 19th century. Two become a naturalized, aggressive weed on
forms, the purple, edulis, and yellow, flavi- Hawaii, Kauai and Maui. Biological control
carpa, are recognized. Although the purple programmes in the islands recently have
form has superior flavour, it can be grown employed the Septoria blotch pathogen
commercially only in the subtropics or at (Trujillo et al., 1994; Norman and Trujillo,
high elevations in the tropics (up to 2000 m). 1995). Another disease, brown spot, limits
The yellow form does better in hot, lowland commercial production of the species.
environments, produces more and larger P. foetida, the stinking passion flower, is
fruit (5–7 versus 4–5 cm in diameter), and from the West Indies and South America,
tolerates Phytophthora blight, nematodes and produces an edible, but rarely used fruit.
and brown spot (Winks et al., 1988). It also It has been introduced to many tropical
has resistance to Fusarium wilt, and is used countries where it has become a naturalized
as a rootstock for f. edulis in affected areas weed. It has been grown as a cover crop in
(Cox and Kiely, 1961). Malaysia and East Africa, and has been used
Hybrids between f. edulis and f. flavicarpa to control erosion.
have been developed in Australia, Hawaii,
Israel, South Africa and the USA (Florida),
and are commercially important in the low- Production and Importance
land environments that are inhospitable to f.
edulis (Knight, 1980; Winks et al., 1988). They Worldwide production figures for passion
are usually high yielding, and tolerate nema- fruit are not available. However, statistics
todes, Fusarium wilt and woodiness. These from different producing regions clearly indi-
hybrids must be propagated clonally since cate that it is an important crop. Abeysinghe
seedling progeny segregate. For this reason, (1973) listed 26 areas in which passion fruit
rooted cuttings are used, but they also per- was produced commercially, and Winks et al.
petuate diseases such as Haematonectria (1988) estimated that 80–90% of all produc-
canker and some that are caused by viruses. tion occurred in Australia, Brazil, Fiji,
P. quadrangularis, the giant granadilla, is a Hawaii, Kenya, Papua New Guinea, South
native of tropical South America. It was first Africa, Sri Lanka, Taiwan and Venezuela.
cultivated in the 18th century, and is now Latin America is the most important produc-
widely distributed (Purseglove, 1968). It is ing region, and Brazil, Colombia, Ecuador
adapted to hot, humid environments, and and Peru supply the world export market for
does not do well at the elevations that are juice. Given the crop’s popularity and wide-
required by P. edulis f. edulis. In addition to spread cultivation, worldwide production
the common beverage and dessert uses for its probably approaches 1 Mt per annum.
pulp and juice, the green fruit are boiled and The area under production fluctuates dra-
used as a vegetable, and the fleshy, tuberous matically. The crop has a short cycle (fruit are
root is used as a substitute for yams. produced 6–9 months after planting and full
P. ligularis, the sweet granadilla, is distrib- production is reached after 18 months), but the
uted from central Mexico to Venezuela, economic life of a plantation is only 3–5 years.
south-central Peru and western Bolivia, and Because growers can rapidly enter or leave the
is generally not utilized outside this region market in response to market conditions, the
(Martin and Nakasone, 1970). It does poorly area under production is price sensitive.
at low elevations and can be grown as high
as 3000 m. It has become naturalized at high
elevations in Hawaii. PASSION FRUIT DISEASES THAT ARE
P. mollissima, the curuba, tacso, tacsonia or CAUSED BY BACTERIA
banana passion fruit, originated in the Andes
and is adapted to high elevations (2000–3000 Bacteria cause diverse symptoms on passion
m) and cool temperatures. Known as banana fruit. Agrobacterium tumefaciens causes
poka in the Hawaiian Islands, where it was tumours; Erwinia carotovora ssp. carotovora
introduced as an ornamental in 1921, it has causes a soft rot; Ralstonia solanacearum causes
Diseases of Passion Fruit 415
a vascular wilt; and Pseudomonas syringae pv. (Fig. 18.1). They are translucent, dark green,
syringae, P. syringae pv. passiflorae and P. viridi- anasarcous, encircled by a chlorotic halo, and
flava cause leaf spots (Bradbury, 1986). have an oily aspect. As the disease pro-
Premature plant death, a disease whose aeti- gresses, it may cause defoliation. Leaf infec-
ology is still uncertain, has been associated tions may become systemic and affect
with a bacterium (Malavolta, 1998). branches, which suffer progressive drying
and develop longitudinal grooves and dark-
ened vascular bundles (Fig. 18.2). Necrotic,
Bacterial spot circular or irregular lesions are formed on
fruit. These are dark or brownish green and
The most important bacterial disease is bac- oily with well-defined edges. They form a
terial spot. Bacterial spot has been recorded hard crust that may cover several originally
in Australia and Colombia, and is especially separate lesions. These spots penetrate to the
important in Brazil (Malavolta, 1998). It is pulp, making the fruit unmarketable. The
the most important bacterial disease of pas- disease may also occur on petals and flowers
sion fruit due to the high susceptibility of of P. alata (J. Rodrigues Neto, Campinas,
economically important cultivars, the high 1999, personal communication).
level of damage the disease causes and the
difficulty with which it is controlled.
Causal agent
Xanthomonas campestris pv. passiflorae is rod
Symptoms
shaped, 0.50 ⫻ 1.50 ␮m, Gram-negative, aero-
Small, well defined, generally circular spots bic and has a polar flagellum (Bradbury, 1986).
that reach 1 cm in diameter under favourable In culture, there is a strain of the pathogen that
conditions are the most common symptoms produces yellow pigments that are typical of
on leaves. They may occur on any part of the xanthomonads and another that is colourless.
leaf, but are most common along the edges Its optimum temperature for growth is 27°C.
Fig. 18.1. Bacterial spot lesions, caused by Xanthomonas campestris pv. passiflorae, on the underside of a
passion fruit leaf (photo: V.A. Malavolta).
Fig. 18.2. Symptoms of systemic infection of a passion fruit leaf, caused by Xanthomonas campestris pv.
passiflorae (photo: V.A. Malavolta).
Biochemical, serological and pathogenic vari- gloeosporioides in leaves and fruit and Fusarium
ability is recognized in the taxon, and different sp. in stems and roots. These interactions
strategies are required to manage disease remain little studied.
caused by different strains. This behaviour has
important practical significance when genetic
Management
resistance to this disease is sought.
Seeds and seedlings should be from healthy
plants and, if possible, should be obtained
Epidemiology
from disease-free areas. Alternatively, seeds
P. alata, P. amethystina, P. serrato-digitata and P. should be treated at 50°C for 15–30 min
edulis ff. edulis and flavicarpa are affected (Dias, 1990). Other complementary measures
(L.O.S. Beriam, Campinas, 1999, personal that should be adopted include: planting in
communication). areas that have not had the disease for the
Penetration by X. campestris pv. passiflorae preceding 2 years; use of wind breaks; avoid-
occurs most frequently via stomata and ing work on plants when they are wet; disin-
hydrathodes. Injury probably also con- festing pruning tools and hands; and using
tributes to the infection process. Infection is fertilizers judiciously, especially with respect
favoured by high relative humidity, a water to nitrogen.
film on the leaf surface and frequent rainfall. Chemical control is based on the use of
Local dissemination of the pathogen is mixtures of cupric and carbamate fungi-
enhanced by wind-blown rain and irrigation, cides, or products that contain streptomycin
and by workers handling wet plants, or oxytetracycline. These measures have
whereas long-distance dispersal occurs on shown variable effectiveness that may be
seedlings and, according to Dias (1990), due to crop management, the quality and
externally and internally on seeds. Insect dis- frequency of applications, the level of infec-
semination has not been demonstrated. tion and susceptibility of the host plant, and
The bacterium survives better in waste virulence of the pathogen. Currently avail-
from contaminated crops than it does in conta- able products rarely afford satisfactory con-
minated seeds. Often, X. campestris pv. passiflo- trol of systemic infections under favourable
rae occurs simultaneously with Colletotrichum environmental conditions.
Genetic resistance would be a most effec- leaf die, resulting, eventually, in abscission.
tive and desirable alternative for the control of Dark brown spots, 4–6 mm in diameter, are
bacterial spot. Thus, much effort has been produced on the branches and tendrils,
channelled towards the search for resistant eventually turning into cankers. Severe
materials that possess good agronomic and lesions can cause the death of shoots and a
commercial characteristics (Malavolta, 1998). partial blighting of the plant (Fig. 18.3).
Among the species that have shown resistance Affected flowers abort, and immature
are P. caerulea, P. cincinata, P. foetida, P. gilberti, P. fruit abscise. Lesions on fruit initially are
mollissima and two non-identified species, superficial and light brown, and later
Introduction I 48669 (‘curuba de la Sierra de become sunken and greyish to dark brown
Santa Marta’) and ‘maracujá-de-cobra’. (Plate 106). They may be larger than 1 cm in
diameter and may reach interior portions of
the fruit. As fruit mature, the spots enlarge
PASSION FRUIT DISEASES THAT ARE and become oily or light tan. The fruit skin
CAUSED BY FUNGI AND FUNGUS-LIKE becomes papery and acervuli are formed on
ORGANISMS lesions here and on leaves. Under high
humidity, masses of red and orange spores
Aboveground Diseases form in acervuli.
Dieback, characterized by reduced elonga-
The most important fungal diseases of the tion of shoots, shortened internodes and an
aerial portions of the plant are anthracnose eventual wilting and death of these structures,
and brown spot. They affect leaves and cause has been described in several countries.
pre- and postharvest fruit spoilage in most However, these symptoms are associated nor-
producing countries. Several other diseases mally with other causes such as water stress,
vary in importance in different countries. nutritional problems or a poor root system.
These include Diplodia rot, Phomopsis rot, Although C. gloeosporioides was isolated con-
stem-end rot and soft rot. Less important sistently from plants with dieback in
postharvest diseases are Fusarium rot, Suriname, these symptoms were associated
Penicillium rot and Septoria rot.
Anthracnose and fruit canker
Anthracnose and fruit canker probably occur

wherever this crop is grown in humid envi-
ronments (Cedeño et al., 1993; Lutchmeah,
1993; de Goes, 1998; Wolcan and Larran,
2000). P. alata, P. edulis and P. quadrangularis
may suffer extensive defoliation, and affected
fruit command a lower market price and
have greatly reduced postharvest shelf lives.
SYMPTOMS All aerial organs of the plant

are attacked (Persley, 1993; de Goes, 1998).
Spots, initially 2–3 mm in diameter and oily
in appearance, are produced on the leaf.
They become dark brown, round or irregu-
larly shaped and ⬎1 cm in diameter. The
centres of spots become brittle and may
break apart. Under high temperature and
humidity, lesions also develop on petioles. Fig. 18.3. Death of the terminal of a passion fruit
As foliar lesions coalesce, large areas of the vine caused by anthracnose (photo: R.C. Ploetz).
with root disease caused by Fusarium solani Fruit should not be harvested during wet
(Power and Verhoff, 1984). In Brazil, dieback conditions, unduly exposed to the sun, or
symptoms normally are associated with fac- kept for long in the absence of refrigeration.
tors that cause plant stress, which may include In areas where there is no history of bacter-
a simultaneous infection by other pathogens, ial spot, pruning to eliminate affected areas
particularly the bacterial spot agent, X. and improve ventilation and light condi-
campestris pv. passiflorae (de Goes, 1998). tions helps control the disease. Pruning
should be done when plants are dry, and
CAUSAL AGENT C. gloeosporioides is described should be followed with applications of a
in Chapter 1. Its teleomorph, Glomerella cingu- protective fungicide. Applications of mixed
lata, has not been observed on passion fruit in formulations of protective and curative
nature, but isolates from P. edulis have pro- fungicides are needed during disease con-
duced it in culture (Wolcan and Larran, 2000). ducive conditions.
Unlike strains of C. gloeosporioides from other
hosts, there does not appear to be physiologi-
cal specialization among those recovered Brown spot
from passion fruit (Dodd et al., 1992).
Brown spot has been recorded in Australia,
EPIDEMIOLOGY Conidia are produced in Canada, Indonesia, Kenya, Mauritius, New
lesions and dead and senescent tissues of the Zealand, New Guinea, South Africa,
plant (Dodd et al., 1992). Within vines and Tanzania, the USA and Zambia (Reid, 1938;
plantings, the pathogen is spread mainly by Holliday, 1980; Lutchmeah, 1993; Persley,
rain or irrigation water, whereas long-dis- 1993; de Goes, 1998). P. quadrangularis, P.
tance dissemination relies on infected seeds, edulis f. edulis and P. edulis f. flavicarpa are
seedlings and cuttings. High temperature and susceptible, and the incidence on the latter
humidity, reduced ventilation and light, and taxon in areas of high rainfall can be as high
host injury encourage disease development. as 98%.
Maximum germination of conidia occurred
between 30 and 33°C in the dark, and was SYMPTOMS The two most common brown
accelerated between 22 and 25°C in the pres- spot agents produce distinct symptoms.
ence of light (Francisco Neto et al., 1994). Alternaria passiflorae causes reddish brown
Host injury increases infection, but is not spots on leaves, ⬃5 mm in diameter (Plate
an obligate requirement. Quiescent infec- 107) (Holliday, 1980; de Goes, 1998). They
tions occur on immature fruit of P. alata and enlarge and become zonate under high
P. edulis f. flavicarpa, whereby infections stop humidity. Conidia and conidiophores of the
development after appressorium formation causal fungus are found in the centre of the
(Jeffries et al., 1990). The mechanisms that lesion. Since a single lesion can cause abscis-
regulate the dormancy of appressoria are sion, much of the plant may defoliate. Small,
not known. dark, elongated lesions form on branches
next to the insertion point of the leaf petioles,
MANAGEMENT Interspecific hybrids between and drying and death of branches may occur
P. mollissima and P. tripartita, and P. mixta and during conducive conditions. Slightly circu-
P. cumbalensis have exhibited stable resis- lar spots develop on fruit. They are reddish
tance. Studies are needed on the agronomic brown, exceed 1 cm in diameter, form on
characteristics of their fruit before they could fruit at an advanced stage of development,
be used in production (Sanudo-Sotelo and and damage the fruit’s commercial value
Zunga-Ravelo, 1991). (Plate 108).
Control involves the use of pathogen-free In contrast, A. alternata causes smaller
seeds or seedlings, adequate spacing, plant- spots, 1–5 mm in diameter, with chlorotic
ing in areas that are free of strong or con- haloes on leaves (Plate 109) (K.G. Pegg, per-
stant winds (wind breaks are helpful), and sonal communication). The stem lesions it
avoiding injury to the plant and its fruit. causes rarely kill vines. Spots on fruit have
dark green, greasy margins (Plate 110). A. ␮m wide at the widest point, have 5–12
alternata is more virulent on hybrids on transverse and a few longitudinal or oblique
which it induces rapid defoliation (K.G. septa, and are constricted at septa.
Pegg, personal communication). Conidiophores are produced singly or in
groups, usually simple, straight or flexuous,
CAUSAL AGENTS Nine species of Alternaria pale to mid brown, smooth, with several
have been described as pathogens of passion conidial scars, and up to 120 ␮m long and
fruit. After A. passiflorae and A. alternata 6–10 ␮m wide.
(Holliday, 1980; de Goes, 1998), the less com- A. macrospora produces solitary or some-
mon species are A. macrospora (Ram et al., times chains of two conidia that are mid to
1977); A. aliena, A. aragakii, A. hawaiiensis, A. mid-dark reddish brown, straight or curved,
tenuissima and A. tropica (Simmons, 1993); usually minutely verrucose, and obclavate or
and A. guangxiensis and A. bannaensis (Chen with the body of the conidium ellipsoidal
and Zhang, 1977). A. tomato has also been tapering abruptly to a very narrow simple
associated with the disease. beak which is usually the same length or
A. alternata is described in Chapter 1. A. twice as long as the body (Fig. 18.5) (Ellis,
passiflorae produces solitary conidia on its 1971). They are 90–180 (134) ␮m long and
host, but chains of up to five in culture (Ellis, 15–22 (17.7) ␮m wide at the widest point,
1971). They are pale to mid brown, smooth have 4–9 transverse and several longitudinal
or occasionally minutely verrucose, straight or oblique septa, and are slightly constricted
to slightly curved, and obclavate or with the at septa. Conidiophores are produced singly
body of the conidium ellipsoidal tapering to or in groups, simple, straight or flexuous,
the simple or branched beak which is usually pale to mid brown, smooth, with one to sev-
the same length or longer than the body (Fig. eral conidial scars, and up to 80 ␮m long and
18.4). They are 100–250 ␮m long and 14–29 4–9 ␮m wide.
Fig. 18.4. Conidia and a conidiophore of Alternaria passiflorae (from Ellis, 1971).
Fig. 18.5. Conidia and conidiophores of Alternaria macrospora (from Ellis, 1971).
A. tenuissima produces solitary or short MANAGEMENT Thinning vines to increase

chains of conidia that are pale to mid-clear ventilation and penetration by fungicides
golden brown, straight or curved, sometimes can reduce disease pressure (de Goes, 1998).
minutely verrucose, and obclavate or with The most efficient fungicides include the car-
the body of the conidium ellipsoidal tapering bamates, iprodione and copper compounds.
gradually to the beak which is up to half the Mancozeb should be applied every 2 weeks
length of the conidium (Fig. 18.6) (Ellis, 1971). during the period most favourable for dis-
They are 22–95 (54) ␮m long and 8–19 (13.8) ease development, and over greater intervals
␮m wide at the widest point, have 4–7 trans- when conditions are less favourable. In
verse and several longitudinal or oblique Australia, good control has been obtained
septa, and are slightly or not constricted at with dicarboximide fungicides, although
septa. Conidiophores are produced singly or they become ineffective as resistance to them
in groups, simple or branched, straight or develops. Hybrids between P. edulis f. edulis
flexuous, pale or mid pale brown, smooth, and f. flavicarpa have been selected in
with one to several conidial scars, and up to Australia, most of which are resistant to A.
115 ␮m long and 4–6 ␮m wide. passiflorae but susceptible to A. alternata (K.
Pegg, personal communication).
EPIDEMIOLOGY The conidia are dispersed
by wind, irrigation water and rain, and,
occasionally, by infected seedlings. Little is Scab (Cladosporium rot)
known about the pre- and post-infection
events in the host and physiological special- Scab, which is also known as Cladosporium
ization in the pathogen. rot, has been reported in Australia and Brazil
Fig. 18.6. Conidia and conidiophores of Alternaria tenuissima (from Ellis, 1971).
(Persley, 1993; de Goes, 1998). When scab is reduce the number of flower buds.
severe, especially on branches, it can delay Circular spots, up to 5 mm in diameter,
flowering and production, as well as reduce are produced on fruit. They are translucent,
the commercial quality of fruit. Passion fruit and are later covered with a brown, rough
of the Amazon, P. nitida and P. edulis f. flavi- tissue that rises several millimetres above the
carpa are susceptible. fruit surface (Pio-Ribeiro and Mariano, 1997).
Several lesions may form on the same fruit,
SYMPTOMS Symptoms develop on young causing it to be deformed and stunted. The
leaves, branches, tendrils, flower buds and fungus does not directly affect the internal
fruit (Fig. 18.7, Plate 111) (Persley, 1993; de parts of the fruit. On fruit of P. nitida, dark
Goes, 1998). Small spots, 3–5 mm in diame- brown lesions are restricted to the skin. In
ter, form on leaves. They are light brown, large numbers, they coalesce and seriously
translucent, round and become necrotic. affect the fruit’s growth.
Lesions can perforate leaves or, when they
occur on veins, cause them to be deformed; CAUSAL AGENTS Cladosporium oxysporum is
they often cause abscission. Small brown responsible in Australia, and C. cladospori-
spots form on branches and tendrils, and oides and C. herbarum in Brazil (Persley, 1993;
become elongated and sunken in the form of Barreto et al., 1996). C. cladosporioides and C.
a canker. As scar tissue forms, branches herbarum are described in Chapter 6. C. oxys-
become weakened and break in the wind. porum produces macronematous, straight or
Lesions on flower buds are 5 mm in slightly flexuous conidiophores that are
length, brown and contain greenish grey nodulose, pale or mid pale brown, smooth,
powdery signs. High numbers of lesions on and up to 500 ␮m long and 3–5 ␮m wide,
flower buds or on peduncles can greatly with terminal and intercalary swellings 6–8
Fig. 18.8. Conidia and conidiophores of

Cladosporium oxysporum (from Ellis, 1971).
Australia, scab is a winter disease (K.G.

Pegg, personal communication). Elsewhere,
a complex of scab symptoms develops under
mild conditions on leaves, branches, tendrils,
flower buds and fruit, whereas hot condi-
tions result in more frequent development
on the external parts of the floral organs,
especially the bracts and the buds.
Dissemination occurs through infected
seedlings, and by wind and sprinkler
water. Although conidia are found fre-
quently on seeds, there is no evidence for
seed dissemination.
Fig. 18.7. Scab symptoms on a passion fruit (A)
leaf, (B) flower and (C) stem (photos: A. de Goes). MANAGEMENT The measures that are rec-
ommended for anthracnose are also effective
␮m in diameter (Fig. 18.8) (Ellis, 1971). against scab. Regular fungicide applications
Conidia are cylindrical and rounded at the are needed when disease-conducive condi-
ends, ellipsoidal, limoniform or subspheri- tions prevail, especially during periods of
cal, subhyaline or pale olivaceous brown, intense growth and flowering.
smooth, 5–30 ⫻ 3–6 ␮m, and arise simply or
in branched chains from terminal swellings,
which later become intercalary. Septoria blotch (spot)
EPIDEMIOLOGY The optimum temperature Septoria blotch, which is also known as

for the agents varies: C. oxysporum, Septoria spot, has been recorded in
19.5–24°C; C. cladosporioides, 20–28°C; and C. Australia, Florida, Central and South
herbarum, 28–30°C (Domsch et al., 1980; K.G. America, India, Oceania, Mauritius and
Pegg, personal communication). In South Africa (Inch, 1978; Holliday, 1980;
Lutchmeah, 1993; Alfieri et al., 1994). It They may erupt and become ostiolate. The
occurs on P. edulis f. flavicarpa, P. quadrangu- short conidiophores bear at their extremities
laris, and weed species such as P. mollissima conidia that are 2 ⫻ 23 ␮m, one- to four-
(Trujillo et al., 1994; Norman and Trujillo, celled, and filiform at either end or slightly
1995). The disease damages both seedlings obtuse and round. The conidia are released
and adult plants, but is less severe and in hyaline cirri and are agglutinated by a
prevalent than anthracnose. mucilaginous substance. The presence of
pycnidia on the lesion surface is an impor-
SYMPTOMS Symptoms are most common tant identifying characteristic for the disease.
on leaves, and occur less commonly on fruit
and branches (Holliday, 1980). Leaf lesions EPIDEMIOLOGY Conidia contained in cirri
are necrotic, light brown, 2–8 mm in diame- are moved by water and insects. The fungus
ter, slightly rounded, and normally accompa- survives in infected tissues, and mucilage in
nied by a yellow halo (Plate 112). Pycnidia of the cirrus is thought to aid survival.
the pathogen occur in the centre of lesions. A Prolonged rains and mild temperatures
single lesion per leaf is sufficient to cause favour disease development.
abscission, and even leaves without visible
symptoms may fall prematurely. Under dis- MANAGEMENT The use of carbamate and
ease-conducive conditions, leaves of all ages benzimidazole fungicides, with measures to
may fall, resulting in drying of the branches control anthracnose and brown spot, are
and, at times, plant death. effective against Septoria blotch. To reduce
According to Inch (1978), infection of fruit the buildup of resistance in the latter fungi-
may occur at any stage of development. cides, they should be mixed or alternated
Lesions are light brown with dark green bor- with those with different modes of action
ders (Plate 113). Lesions may coalesce and (Peterson, 1977).
cover extensive areas of a fruit, affecting its
development or maturation.
Postharvest Diseases
CAUSAL AGENTS Three different species
have been reported, although the literature Postharvest diseases often result from
is confused on their identity. Septoria fructi- infections of immature or maturing fruit in
gena has been reported in Kenya, South the field. Latent infection of fruit is
Carolina and perhaps other locations increased by prolonged exposure to rain
(Nattrass, 1939; Farr et al., 1989) but, based and high humidity.
on its description is apparently a species of Typically, producers harvest fruit only
Phomopsis (M. Priest, personal communica- after they have abscised. This is done at vari-
tion). S. passiflorae has been described for able intervals, depending mainly on the
isolates from diseased passion fruit in quantity produced.
South Africa. Shortly after it was described Some of the most frequent postharvest dis-
Louw (1941) reported a new species in eases are anthracnose, Fusarium patch (caused
South Africa but, because he was not aware by Fusarium pallidoroseum), Phomopsis rot and
of the earlier report, also used the epithet S. stem-end rot (Phomopsis tersa; Fig. 18.10).
passiflorae. In 1980, Punithalingam reported Occurring less frequently are Diplodia rot
that these fungi were distinct, and renamed (Diplodia theobromae), Fusarium dry rot (F. pro-
Louw’s species S. passifloricola. Although S. liferatum), Penicillium rot (Penicillium expan-
passifloricola appears to be more widely sum), Pestalotiopsis brown spot (Pestalotiopsis
spread than S. passiflorae, unfortunately it is sp.) and soft rot (Rhizopus stolonifer). The most
called S. passiflorae in much of the recent lit- common pathogens on P. alata are C. gloeospori-
erature. oides, Sclerotium rolfsii, D. theobromae,
S. passifloricola produces dark, spherical Gliocladium roseum, Alternari passiflorae and R.
and subepidermic pycnidia that are 50–160 stolonifer. D. theobromae causes a black rot of
␮m in diameter (Fig. 18.9) (Holliday, 1980). the skin and the pulp. G. roseum and R.
Fig. 18.9. (A) Pycnidium and (B) conidia of Septoria passifloricola (from CMI description no. 670).
Fig. 18.10. (A) Vertical section of stromatic conidiomata and (B) conidiophores, conidiogenous cells and
conidia of Phomopsis tersa (from CMI description no. 1169).
stolonifer initiate infection via the peduncular Control of this complex of diseases
region, whereas S. rolfsii may initiate it on any involves adequate care of plants and sup-
part of the fruit. A. passiflorae causes spots and pression of disease-predisposing factors.
rotting (Anselmo and Junqueira, 1997). Careful harvest, transport and storage are
Simultaneous infections by other pathogens indispensable measures to improve the
often occur. longevity of the fruit. Good anthracnose con-
trol has been obtained by treating fruit at that are water soaked on the interior of the
47.5°C for 5–10 min, or at 54°C for 1–5 min flower bud, especially on the sepals and
(Jesus et al., 1994). petals (Fig. 18. 11). Later, spots occur over the
entire flower bud, and dark grey mycelia
and sporangia develop. The flower bud
becomes putrid and abscises easily. Control
Miscellaneous Aboveground Diseases
has been difficult under conditions that
favour for the disease. To date, only tebu-
Vine dieback differs from that which results
conazole has been effective.
from the interaction between F. solani and C.
gloeosporioides (Power and Verhoeff, 1984), in
that symptoms are not restricted to sprouts Soilborne Diseases
and it does not cause plant death. According
to Cedeño et al. (1995), it is caused by D. theo- Fusarium wilt
bromae. The fungus causes lesions on the
internodes of main branches and where Fusarium wilt was once a major disease of P.
leaves and secondary branches emerge, later edulis f. edulis in Queensland and New South
invading the internal tissues and inducing Wales, Australia. This vascular wilt was first
dieback. The disease is associated with struc- reported by McKnight (1951), and was one of
tural damage caused by the mite, Tetranychus the most important constraints to production
urticae, and with water stress. in Australia prior to the use of resistant root-
A flower rot caused by R. stolonifer stocks. The disease may also be present in
resulted in losses of up to 63% of the flowers Brazil (Carvalho-Dias et al., 1998) and South
of P. alata in Brazil (de Goes, 1998). More Africa (Grech and Rijkenberg, 1991), but the
recently, a similar disease on flowers of P. incomplete nature of these reports makes it
edulis f. flavicarpa has been associated with a unclear whether Haematonectria canker or
non-identified species of Rhizopus. Flower rot Fusarium wilt was reported. Although a
occurs mainly in the summer, during periods clear distinction between Haematonectria
of prolonged rain. Little is known about its canker and Fusarium wilt is made in this
geographic distribution, incidence, impact chapter, this is not the case in other publica-
and control. Symptoms include dark spots tions (e.g. Cole et al., 1992).
Fig. 18.11. Rot of passion fruit flower caused by Rhizopus stolonifer. Note the black sporangia of the
pathogen covering the flower’s base (photo: A. de Goes).
SYMPTOMS The first external symptoms of as rootstocks. Their results agreed with
Fusarium wilt are a pale colour of new those of Groszmann and Purss (1958) in
growth which proceeds to a wilt of one or Queensland who indicated that P. edulis f.
more shoots as soon as 24–48 h after symp- flavicarpa was generally tolerant of the dis-
toms first appear (Holliday, 1980). ease. Groszmann and Purss (1958) identi-
Eventually, affected plants die. Symptom fied a superior wilt-resistant selection of P.
development may be unilateral or encom- edulis f. flavicarpa that had the added attrib-
pass the entire plant. Fruit shrivel and utes of resistance to nematodes and
remain attached to the vine if they are imma- Phytophthora blight; it was still a standard
ture. Unlike the somewhat localized vascular in commercial production 30 years later
browning that occurs in plants affected by (Winks et al., 1988).
Haematonectria canker, internal symptoms More recently, interform and interspe-
of Fusarium wilt may extend to 2 m above cific hybrids have been evaluated for
the soil line. Fusarium wilt resistance and other traits
(Winks et al., 1988). A third generation cross
CAUSAL AGENT Fusarium oxysporum f. sp. between P. edulis and P. incarnata, 3–19/F3,
passiflorae causes Fusarium wilt of passion grew to a graftable size more quickly and
fruit. The species is described in Chapter 1. was more vigorous than P. edulis f.
Purss (1954) determined that F. oxysporum flavicarpa. However, it was intermediate in
f. sp. passiflorae was a distinct forma speciales its susceptibility between P. edulis f. flavi-
after showing that it was pathogenic on P. carpa and P. edulis f. edulis and was not rec-
edulis f. edulis but not on other Fusarium wilt ommended for release to the industry. It
suscepts (i.e. tomato, watermelon and pea). was hoped that useful hybrids would be
Gardner (1989) demonstrated that P. foetida, produced in crosses with new accessions of
P. ligularis and P. mollissima were also suscep- P. incarnata and P. caerulea.
tible, but that P. edulis f. flavicarpa, P. suberosa
and 24 miscellaneous monocots and dicots
were resistant. Haematonectria canker, sudden wilt, collar
P. edulis is in the subgenus Granadilla,
rot, crown canker, base rot
series Incarnatae. Since the susceptible species
were not closely related (foetida is in subgenus
Haematonectria canker has been identified
Dysomia, mollissima in the subgenus Tacsonia,
in Australia, Florida (USA), Suriname,
and ligularis in the subgenus Granadilla, series
Taiwan, Uganda, Venezuela and Zimbabwe
Tiliaefoliae), Gardner (1989) speculated that the
(Emchembe and Mukiibi, 1976; Power and
host range of F. oxysporum f. sp. passiflorae
Verhoeff, 1984; Lin and Chang, 1985;
probably included more species of Passiflora
Cedeño et al., 1990; Ploetz, 1991; Cole et al.,
than were identified in his work.
1992; K.G. Pegg, personal communication).
MANAGEMENT Considerable effort was Based on symptoms and the fungi that have
made in Australia to identify or breed resis- been recovered from affected plants, it may
tant rootstocks during the 1950s and 1960s. also occur in New Zealand, Réunion, Samoa
Due to the widespread and damaging nature and South Africa (Simmonds, 1938; Young,
of Fusarium wilt, resistant rootstocks are now 1970; Gerlach, 1983; Terblanche et al., 1986;
viewed as essential for the production of pas- Aubert, 1987).
sion fruit in Australia (Winks et al.., 1988). Several different names are used to
In New South Wales, Cox and Kiely describe this serious disease including,
(1961) determined that P. edulis f. flavicarpa, unfortunately, Fusarium wilt (Cole et al.,
P. coerulea (sic = caerulea), P. incarnata and P. 1992). Haematonectria canker and Fusarium
herbertiana were highly resistant. However, wilt produce many of the same symptoms on
since P. herbertiana had a slender stem and P. passion fruit, and are both caused by species
caerulea and P. incarnata had a suckering of Fusarium. Thus, it is not surprising that
growth habit, they were deemed unsuitable these diseases are frequently confused.
SYMPTOMS The first aboveground symptom is decay also occurs, and in some locations this
a dramatic decrease in the rate of shoot elon- is the only symptom reported from beneath
gation, beginning within 3 months of planting the canopy (Power and Verhoeff, 1984). In
(Power and Verhoeff, 1984). In Suriname, it Australia, root damage is associated with
was reported that affected terminals may wilt swelling of the stem at the soil line and
and/or die back, or may continue sporadic adventitious root formation (Fig. 18.13) (K.G.
growth during subsequent rainy seasons. In Pegg, personal communication).
most cases, however, a sudden and terminal A reddish brown to brown discoloration of
collapse of vines is most common (Emchembe the host vascular system occurs in association
and Mukiibi, 1976). Terminal wilting of vines with cankers and root decay, but usually does
begins to occur shortly after they are trellised not progress more than 0.5 m from the
(Cole et al., 1992) or after they begin to set affected area. Emchembe and Mukiibi (1976)
fruit (Ploetz, 1991). All leaves in an affected examined affected tissues microscopically,
vine lose turgor and become chlorotic, but are and reported that the pathogen invaded and
usually not shed. Fruit on bearing vines also colonized the cortical and xylem parenchyma.
remain attached and become shrivelled after
vine death. Within 3–5 years, all vines in an CAUSAL AGENTS Haematonectria canker is
affected planting die. caused by homothallic strains of
Wilting and dieback of the canopy result Haematonectria haematococca (anamorph:
from the damage which the disease causes to Fusarium solani). The fungus usually produces
stems and roots, and the corresponding crimson coloured perithecia, singly or in
reduction of the host’s capacity to extract groups, on the surface of cankers and affected
and conduct water (Fig. 18.12) (Cole et al., roots. They are ⬃200 ␮m in diameter, and
1992). Cankers that develop at the root collar produce unitunicate asci, 80 ␮m long, in
or at physically wounded locations along the which eight bicellular ascospores, 14 ␮m long,
stem ultimately can girdle the entire stem are produced (Fig. 18.14) (Hanlin, 1990).
(Plate 114) (Ploetz, 1991). Considerable root Colonies of the pathogen grow 7.5 mm in
Fig. 18.12. (A) Stem canker and (B) root necrosis of passion fruit cuttings caused by artificial inoculation
with Haematonectria haematococca (photos: R.C. Ploetz and A.W. Cooke, respectively).
diameter day⫺1 on oatmeal agar, with abun-

dant aerial mycelium and, eventually, numer-
ous sporodochia; they are cream, aqua or
blue, but never orange (Domsch et al., 1980;
Nelson et al., 1983). The anamorph produces
micro- and macroconidia on branched and
non-branched monophialides. Microconidia
are sparse to abundant, usually one-celled,
oval to kidney shaped, and have thicker cell
walls than those that are produced by F. oxys-
porum. Macroconidia are abundant, cylindri-
cal, thick-walled and stout, with rounded,
foot-shaped or notched basal and blunt or
rounded apical cells. Chlamydospores are
often abundant and form singly or in pairs.
Both ascospores and conidia of the fungus are
pathogenic (Emchembe and Mukiibi, 1976).
Other species of Fusarium and their respec-
tive teleomorphs may cause crown canker
and sudden wilt of passion fruit. Young (as
reported by Emchembe and Mukiibi (1976))
‘…observed a crown rot of passion fruit after
invasion by F. sambucinum…’. Sale (1987) indi-
cated that F. redolens, F. avenaceum, Gibberella
baccata (anamorph: F. lateritium) and G. saubi-
Fig. 18.13. Swelling of a passion fruit stem at the
netii (anamorph: F. graminearum) were also
soil line caused by Haematonectria
‘known to be involved’ in New Zealand. It is
haematococca. This symptom is common in
not clear whether Koch’s postulates were
Australia (photo: A.W. Cooke).
completed with these fungi.
Fig. 18.14. (A) Asci and ascospores of Haematonectria haematococca, and (B) microconidia and
conidiophores and (C) macroconidia and conidiophores of its anamorph, Fusarium solani (from CMI
description no. 29).
EPIDEMIOLOGY Artificial inoculation studies presented. The same authors reported that
indicate that H. haematococca is not a particu- three taxa, P. edulis f. flavicarpa, P. maliformis and
larly aggressive pathogen on passion fruit, P. ex Queensland (‘Queensland Purple’) were
and that wounding has a profound effect on significantly more resistant than the suscepti-
disease development. Several authors have ble P. edulis f. edulis. Resistance has also been
shown that the onset of symptoms is hastened, reported among selections of P. edulis f. flavi-
and the incidence and severity of the disease is carpa in Taiwan. During 1981–1982, an 800 ha
increased, if vines are wounded mechanically plantation was established using the selections
prior to inoculation (Emchembe and Mukiibi, as rootstocks (Lin and Chang, 1985).
1976; Lin and Chang, 1985; Ploetz, 1991; Cole
et al., 1992). Emchembe and Mukiibi (1976)
increased the percentage of affected plants by Phytophthora root and crown rot
100% by simply hoeing in between rows, a
practice that presumably injured roots, thereby This destructive disease, which is also called
providing entry points for the pathogen. Ants Phytophthora blight, has been reported from
of the genera Solenopsis and Cromatogaster Australia, India, Sarawak, South Africa,
may play a role in disease development in Taiwan and Venezuela (Simmonds, 1959b;
Venezuela (Cedeño et al., 1990), and the dis- Van den Boom and Huller, 1970; Turner,
ease is known to interact with Phytophthora 1974; Hseih, 1979; Erwin and Ribiero, 1996;
blight, particularly where P. edulis is grown Gonzalez et al., 1999). Due to the wide distri-
(Lin and Chang, 1985; Cole et al., 1992). bution and host range of the causal agent
Ploetz (1991) demonstrated that the (Erwin and Ribiero, 1996), the disease may
pathogen colonizes the host vascular system occur in other countries.
in advance of visible external or internal
symptoms, and that the pathogen could be
Symptoms
recovered from asymptomatic plants in a
commercial nursery. Thus, the pathogen The pathogen causes diverse symptoms on
could be moved in ‘healthy’ nursery stock or P. edulis. Affected plants first exhibit yellow
by cuttings from asymptomatic plants. or scorched leaves throughout the canopy
Cuticle thickness or composition on the host (Plate 115). Vine apices die and are black.
may be important, since the disease can be Subsequently, necrosis of leaf veins, wilt-
reproduced in the absence of wounding ing, and defoliation occur (Fig. 18.15). In its
when the cuticle is removed from stems with terminal phases, branches die back and
acetone prior to inoculation (R.C. Ploetz, extensive bark and cortical decay develop
unpublished). at the root collar, which thickens to three to
Resistance to Haematonectria canker five times its normal diameter. Grey green,
increases as plants age. Emchembe and
water-soaked lesions develop on immature
Mukiibi (1976) reported that 76–100% of the
fruit, which then usually abscise (Plate
10-week-old plants that were root-dip or
116).
wound inoculated wilted, whereas only
28–48% of 12-month-old plants inoculated in
the same manner succumbed. Causal agent
Phytophthora nicotianae causes the above
MANAGEMENT When cuttings are used to
propagate the crop, it is imperative that symptoms on P. edulis (Erwin and Ribiero,
pathogen-free stock be used. No effective 1996). It is described in Chapter 1.
chemical measure has been described.
Ssekeyewa et al. (1999) reported that biweekly Epidemiology
drenches of copper oxychloride reduced the
numbers of plants that developed collar rot in P. nicotianae is a ‘watermould’ that requires
a small experiment in Uganda, but the experi- moist conditions to complete many phases of
ment was not repeated and no statistical evi- its life cycle. The general epidemiology of the
dence for the significance of this treatment was diseases its causes are discussed in Chapter 1.
Management incognita and M. javanica, are important.

They can cause economic losses of fruit and
New plantings should be made in freely
reduce the life of a plantation.
drained soil, preferably on a site with
R. reniformis is widely distributed and has
enough slope to encourage runoff of rainfall
a host range of 140 species, including P.
and irrigation. In South Africa, P. edulis f.
edulis. In Fiji, the nematode was reported to
flavicarpa is used as a rootstock for the sus-
cause foliar chlorosis and was found in 84%
ceptible P. edulis f. edulis, and bud unions of
of the areas that were surveyed (Kirby, 1978).
at least 0.6 m above the soil line are recom-
In Brunei, the nematode was reported to pre-
mended to discourage disease development
dispose P. edulis f. flavicarpa to root rot
on the scion due to soil splash (Brodrick et
caused by Phytophthora spp. (Perregrine and
al., 1976). Although P. edulis f. flavicarpa is
Yunton, 1980).
resistant to root and crown rot in Australia
Nematodes are disseminated in infested
(K.G. Pegg, personal communication), this
soil, water and equipment, as well as
taxon is reported to be susceptible in
infected plant materials. They are best con-
Venezuela (Gonzalez et al., 1999). Fungicides
trolled with strict exclusion and sanitation
decrease the spread of the disease, and
measures. In general, the registrations of var-
canopies should be thinned when they are
ious nematicides are being lost rapidly due
used to ensure good penetration.
to their high toxicity and adverse environ-
mental impacts.
PASSION FRUIT DISEASES THAT ARE
CAUSED BY NEMATODES PASSION FRUIT DISEASES THAT ARE
CAUSED BY VIRUSES
Nematodes are important pathogens in
many different growing regions (dos Santos, Passiflora spp. are affected by viruses in several
1998). The reniform nematode, Rotylenchus different families. Although many of the dis-
reniformis, and at least three species of root- eases they cause are localized or are laboratory
knot nematode, Meloidogyne arenaria, M. curiosities, others impact production over
Fig. 18.15. Large-scale damage in a passion fruit planting caused by Phytophthora nicotianae. Note the dry,
necrotic foliage in the foreground and the numerous skips throughout the planting (photo: A.W. Cooke).
large areas. Undoubtedly, a key reason for the potyviruses, in particular, Passionfruit woodi-
importance of these pathogens is the extent to ness virus (PWV). The latter agents now
which this crop is propagated vegetatively. appear to play more important roles in the
Worldwide, the most important virus- development of this disease than CMV.
induced disease of passion fruit is woodiness Since the diseases that are caused by the dif-
and other similar diseases, all of which are ferent viruses are so intertwined, historically
caused by potyviruses. Although vines are and in practice, they will be dealt with
rarely killed, production is severely affected together below.
and the crop can become unprofitable in its
first year.
Symptoms
Symptoms are not very useful to identify
viruses that affect Passiflora spp. since many The pericarp is malformed, thickened and
are caused by more than one virus and hardened with a much reduced pulp cavity
mixed infections are common. Furthermore, and fewer seeds. Orange brown gum pockets
detailed symptom descriptions are often are common in the rind (Plate 117). The
lacking in the literature. Commercially avail- lumpiness and distortion can be detected at
able enzyme-linked immunosorbent assay an early stage, but may be confused with
(ELISA) kits enable the identification of fruit fly stings. In a given vineyard, an out-
viruses in the Potyvirus genus. break of woody fruit can be preceded or fol-
Whilst it is somehow comforting to know lowed by normal-appearing fruit that may
the exact virus that affects a crop, there is be smaller or have slightly thickened peri-
usually little that can be done to rectify a sit- carps. Ring spots, 3–8 mm in diameter, may
uation once symptoms appear. For these dis- occur on woody fruit, and can fuse to pro-
eases, prevention is the preferred means of duce irregular blotching. Fruit may also be
control. This and other control measures are finely stippled.
discussed at the end of this section. Due to Temperature influences the development
its importance, extensive coverage of the of fruit and leaf symptoms. Symptoms are
woodiness disease is given below, whereas more common on fruit that set during
brief overviews of other, less important autumn and winter and ripen from late win-
virus-induced diseases follow. ter to early summer, and on leaves are less
pronounced in summer.
Leaf mosaic, mottle and ringspot symp-
Woodiness toms are often associated with fruit woodi-
ness. Mosaic symptoms appear as dark
Woodiness was first described in southern green, raised blisters on a centimetre scale on
Australia, where it was first recognized in a yellow–green background (Fig. 18.16).
the 1890s and seriously affected production Leaves are hardened and frequently dis-
by 1930 (Magee, 1948). The disease has also torted and puckered by the differential
been reported in Brazil, Nigeria, South Africa growth rates of the infected tissue. Where
and Taiwan and, based on symptoms alone, young terminal growth is affected, leaves
was also diagnosed in Hawaii, India, Italy, have translucent yellow–white membranous
Japan, Kenya, Malaysia and the Philippines. areas where cells have collapsed to cause
The term ‘woodiness’ describes the clas- major distortions or missing lobes. Vein
sical symptom of this disease, the distortion, clearing may occur. Growth is slowed,
hardening and thickening of the fruit peri- internodes shorten and the terminals have a
carp. As work was conducted on this prob- bunchy appearance. Mottle appears as
lem, it became clear that several different numerous, small, yellow spots or flecks on
causal agents were responsible for this and young, mature leaves. These can be up to 3
other symptoms that were associated with mm in diameter, round and bright yellow, or
the disease. Although Magee (1948) ascribed the small spots can coalesce into yellow
the disease to Cucumber mosaic virus (CMV), patches. The mottle may disappear as the
subsequent reports indicted different leaf ages. Ringspots on leaves are rare.
Fig. 18.16. (A) Dark green, raised blisters and (B) vein clearing, and small, yellow flecks caused by passion
fruit woodiness (photos: A.W. Cooke and E.W. Kitajima, respectively).
Several authors indicated that dual infec- protein. The particles with RNA3 also con-
tions resulted in increased symptom severity, tain a subgenomic coat protein messenger,
even leading to vine dieback (Taylor and RNA4. The presence of all three particles is
Kimble, 1964; Pares et al., 1985; Kitajima et al., required for infection. The particles are ⬃30
1986; Brand, 1992). Teakle et al. (1963) reported nm in diameter, icosahedrally symmetric
that CMV caused leaf mottling, distortion and and consist of 180 capsid units.
stunted growth, whereas Kitajima et al. (1986) In Queensland, McKnight (1953) was
observed only local lesions on yellow passion unable to associate CMV with woodiness
fruit and no fruit woodiness with the same symptoms. Taylor and Kimble (1964) later
virus. Taylor and Kimble (1964) wrote that demonstrated that two viruses were associ-
CMV caused vein clearing and epinasty of the ated with woodiness, CMV and a long flexu-
terminal leaves of small seedlings of P. edulis ous virus, PWV. They suggested that the
which disappeared as plants matured, that major cause of woodiness in Victoria and
PWV caused a systemic mosaic which per- New South Wales was CMV, but in
sisted, and that dual infection led to tip necro- Queensland was PWV.
sis, leaf fall and severe stunting and yellowing. PWV is a member of the genus Potyvirus,
family Potyviridae, the largest plant virus fam-
ily. Virions are flexuous rods, 680–900 ⫻ 11–15
Causal agents
nm, that contain single-stranded, positive-
Magee (1948) first reported that CMV caused sense RNA of ⬃9–10 kb, encapsidated with
woodiness in Australia. CMV is the type ⬃2000 helically arranged coat protein units.
species of the genus Cucumovirus, family The genome and protein products of the
Bromoviridae. It has a single-stranded, posi- potyviruses have been characterized exten-
tive-sense RNA genome consisting of three sively (Dougherty and Carrington, 1988).
unique RNAs, 1, 2 and 3, each of which is They induce cytoplasmic ‘pinwheel’ inclu-
encapsidated separately in the same capsid sions in infected cells that are diagnostic for
these viruses. Their morphology is indepen- In Brazil, CMV is regarded as a minor

dent of the host and has been used to divide pathogen, causing yellow rings or spots on
the Potyviridae into subgroups. Classical leaves, but no systemic mosaic or fruit woodi-
serology does not assess the relatedness of ness (Kitajima et al., 1986). However, severe
different potyviruses reliably, but antibodies damage is observed in co-infections with
that are specific for the N-terminus of the PWV. By itself, PWV causes severe losses. It
coat protein and monoclonal antibodies can appears to be restricted to northwestern pro-
be used for this purpose. Potyvirus taxon- duction areas of the country and is related,
omy currently is investigated with RNA and serologically, to other potyviruses. Symptoms
deduced amino acid sequences. in Brazil are identical to those in Australia,
Mild, severe and tip blight strains of but sequence comparisons between isolates
PWV exist. They are serologically insepara- from both countries have not been conducted.
ble and their coat protein sequences are at Woodiness was also reported from
least 96% homologous. However, these Nigeria (Martini, 1962). Although typical leaf
strains are only 85% homologous with a mottling and distortions were described, fruit
strain from a hybrid between P. edulis f. flavi- woodiness was not mentioned. CMV was not
carpa and P. edulis f. edulis (Shukla et al., observed, and Passion fruit mosaic virus was
1988; Gough and Shukla, 1992). the name proposed for the causal agent. The
It is possible that early workers who virus was not characterized sufficiently, and
described CMV in passion fruit were, in fact, is now considered a synonym of PWV.
dealing with mixed infections. The only time In Taiwan, woodiness is also a serious
CMV has been confirmed in passion fruit by disease. The disease is widespread on P.
itself was by Teakle et al. (1963) in California; edulis f. flavicarpa, reducing yields from 35 t
with electron microscopy, they observed ha⫺1 to 5 t ha⫺1 (C.A. Chang, 1992, personal
CMV virions in P. caerulea and P. alata- communication). PWV often occurs in con-
caerulea. Magee (1948) did not have the facili- junction with Passion fruit mottle virus
ties needed to detect dual infections, and (Chang, 1992).
Taylor and Kimble (1964) did not test their In summary, the classic woodiness symp-
CMV isolates for the presence of flexuous toms on fruit are caused by a number of dif-
virus particles. ferent potyviruses. The available evidence
In South Africa, Brand (1992) occasionally suggests that CMV is not a prime cause of the
found Tobacco necrosis virus (TNV; now split disease, but that co-infection with potyviruses
into two viruses Tobacco necrosis virus A and is common and enhances the damage they
Tobacco necrosis virus D) and always found cause on passion fruit. It is also possible that
CMV in association with a potyvirus in other viruses (see below) cause woodiness
woodiness-affected plants. In contrast, Da under cool conditions. Leaf mosaic and mottle
Graça (1976) found only a potyvirus in seem to be consistent characteristics of
affected plants. It was isolated from P. edulis potyvirus infection. Work is warranted to
in Mpumalanga Province and had a modal determine the relationships between
length of 650 nm, whereas the virus charac- potyviruses from different countries and the
terized by Brand (1992) was isolated from P. Australian PWV type strain of this pathogen.
caerulea in Kwa-Zulu Natal and had a modal
length of 670 nm. The coat protein region of
Epidemiology
the latter was sequenced, and found to be
distinct from PWV in Australia. It was Members of the genus Potyvirus are vectored
termed PWV-SA but, based on sequence by aphids, and are also transmitted mechani-
data, has since been identified as a strain of cally and by grafting (Nattrass, 1944). PWV
Cowpea aphid-borne mosaic virus (CABMV) reportedly is not seedborne (Chang, 1992).
and renamed CABMV-SAP (McKern et al., CMV is transmitted by aphids in a non-
1994). Recently, Gerhard Pietersen serologi- persistent fashion. It can also be transmit-
cally identified PWV in South Africa (J.E. ted mechanically, and seed transmission is
Thomas, personal communication). common.
OTHER POTYVIRUSES laris in Colombia. Symptoms included mosaic,

chlorosis and epinasty that was followed by
Passionfruit ringspot virus hardening of the leaves, defoliation and, ulti-
mately, plant death. Prominent ringspots were
De Wijs (1974) described a disease of P. edulis present on fruit, and on P. edulis mild mottle
f. flavicarpa in the Ivory Coast. The most symptoms and red coloration of the leaves in
common symptoms were yellow spots and an oak-leaf pattern were also observed.
mottling on otherwise normal leaves, and Viruses isolated from P. edulis and P. ligu-
ringspots on younger leaves, especially laris were transmitted mechanically, by the
where they were shaded. A few plants had aphids A. gossipii and, less efficiently,
severe mosaic and malformation on some of Toxoptera citricida, but not by seed. Based on
the leaves, and severely affected plants were host range, symptomatology and serology,
stunted and bore few fruit. Woodiness was
the isolates were similar to SMV. Further
not seen, but fruit were small and shrivelled
confirmation of the isolates as SMV was
before ripening. Young, developing leaves
based on their 98% homology with the
showed yellow veins and epinasty after inoc-
ulation, followed by mottling. amino acid sequence of the coat protein and
The cause was identified as a potyvirus, dot-blot DNA complementation hybridiza-
Passionfruit ringspot virus (PRV), which was tion with the 3⬘ terminus of the coat protein-
serologically related, but not identical, to coding region of a strain of SMV.
PWV. It could be transmitted non-persis-
tently by the aphids Aphis gossypii and A. spi-
raecola, but not by seed. De Wijs (1975) later Passionfruit Sri Lankan mottle virus
demonstrated that an indigenous member of
the Passifloraceae, Adenia lobata, was a native Dassanayake and Hicks (1992) described a
source of the virus. In the wild, infected A. potyvirus that affected P. edulis f. flavicarpa in
lobata often was symptomless. Infection of Sri Lanka. Symptoms began as vein yellow-
cultivated plants depended on aphid incur- ing and mild crinkling of new leaves, devel-
sions from these sources. oping later into numerous yellow spots and
a yellow–green mottle and mosaic. Fruit
Passionfruit mottle virus were shrunken and showed slightly
depressed green spots on ripe fruit. The
Chang (1992) described passionfruit mottle in virus caused flower break symptoms on arti-
Taiwan. Symptoms included mottling of ficially infected P. mollisima.
leaves and the skin of the fruit, but not wood- The virus was non-persistently aphid (M.
iness. On the basis of particle morphology, persicae, A. gossypii, A. craccivora and A
serology, production of cytoplasmic inclu-
spiroecola), graft and mechanically transmis-
sions, aphid transmissibility (Myzus persicae
sible, and possessed the characteristic mor-
Sulzer), and host range studies, the virus was
phology of potyviruses. The virus produced
classified as a potyvirus, Passionfruit mottle
virus (PaMV). It had a different host range typical pinwheel inclusions in plants. It was
and caused different symptoms than PWV, serologically related to, but distinct from,
and was serologically related to PWV, Bean PRV, PWV and Potato virus Y, and reacted
common mosaic virus (BCMV), Blackeye cowpea only weakly with WMV2 and BCMV.
mosaic virus (synonym: BCMV), Watermelon
mosaic virus 2 (WMV2) and Soybean mosaic
virus (SMV). In Taiwan, PaMV was as widely Incompletely described potyviruses
spread as PWV and often occurred in mixed
infections with this virus. Chang et al. (1996) reported another potyvirus
in Taiwan, provisionally designated
Soybean mosaic virus Passionfruit crinkle potyvirus. It produced crin-
kle symptoms on leaves but did not affect
Benscher et al. (1996) described a severe dis- fruit. Serologically, it was indistinguishable
ease of P. edulis, P. ligularis and P. quadrangu- from a virus recorded by Escudero et al. (1988)
from Puerto Rico that was later named Puerto and mechanical means, but not through seed
Rican passionfruit virus (PRPV). PRPV or by insects.
appeared to occupy a taxonomic position
between PWV and WMV2, and may be a
strain of BCMV-US1 (Benscher et al., 1993).
Rhabdoviruses
Based on coat protein sequences, another
potyvirus from the Dominican Republic The plant-associated rhabdoviruses are
appeared to be closely related to CABMV, divided into two genera, Cytorhabdovirus and
whereas a strain from Thailand was distinct Nucleorhabdovirus, but those that affect pas-
from these and the SMV strains from sion fruit have not been assigned. The viri-
Colombia (Benscher et al., 1993, 1996). ons have a characteristic envelope, are
Finally, Bean yellow mosaic virus has been 100–430 ⫻ 30–130 nm, and contain single-
recorded on P. caerulea with CMV (Pleše and stranded RNA. Transmission is by aphids
Wrisher, 1984). and Cicadellidae in a persistent manner, and
the virus is transmitted to progeny of the
vectors. These viruses can be transmitted by
Carlavirus grafting but do not pass through seed. Only
some members of these genera can be trans-
Passionfruit latent virus mitted mechanically.
Passionfruit latent virus (PLV) is a carlavirus.

Virions are filamentous, flexuous rods, Passion fruit vein-clearing rhabdovirus
600–700 ⫻ 12–13 nm, and contain single-
stranded RNA. They are transmitted by A widespread disease in Brazil was first
aphids in a non-persistent manner, by graft- described by Batista and co-workers in 1981
ing and by mechanical inoculation, but not on P. edulis f. flavicarpa (Kitajima et al., 1986).
by contact between plants. They occasionally Affected plants exhibited shortened inter-
are transmitted by seed and rarely by pollen. nodes, small crinkled leaves and vein clear-
PLV appears to be a problem primarily on ing. Branches lignified and fruit on heavily
vegetatively propagated ornamental infected plants was, similar to woodiness,
Passiflora spp. It was first identified in malformed with reduced pulp and a hard
glasshouse plants of P. caerulea and P. suberosa pericarp. Production was severely affected
in Germany (Brandes and Wetter, 1963), and but plants did not die. The disease was trans-
caused concern in The Netherlands in the late mitted by grafting, but not seed. Spread in
1970s where P. caerulea was an important the field appeared to involve a vector, but
ornamental (Hakkart and Versluys, 1981). tests excluded certain aphids and mites as
PLV was found later in Florida in the orna- candidates. A rhabdovirus was observed by
mental species Passiflora ⫻ Incense (St Hill et electron microscopy mostly in the vascular
al., 1992), and was common in European col- parenchyma.
lections of ornamental Passiflora spp. (Hicks Pares et al. (1983) recorded a rhabdovirus
et al., 1996). The virus has also been found in in a mixed infection with PWV in P. edulis in
imported ornamental Passiflora spp. in South garden plants in New South Wales, Australia,
Africa. but not in commercial fields. It was not possi-
Pares et al. (1997) reported that PLV was ble to separate the viruses for further study,
found widely in Australia in cultivated P. and it is not known whether this virus, provi-
edulis that had been graft propagated. sionally termed Passion fruit nucleorhabdovirus,
Seedlings only rarely were infected. P. edulis is related to the Brazilian rhabdovirus.
f. flavicarpa was also infected, but only where
it was grown in association with infected P.
edulis. Green spot
PLV causes an inconspicuous systemic
foliar mosaic. In cooler weather, older leaves Kitajima et al. (1997) reported a severe dis-
are mottled. PLV is transmitted by grafting ease in São Paulo state, Brazil, that killed
P. edulis. It caused necrotic lesions on stems, but could not be related serologically to
green spots on fruit and leaf senescence. other isometric viruses and is as yet unclassi-
Death occurred when stems were girdled by fied. It was readily transmitted mechanically
confluent lesions. The disease was associated by grafting and experimentally by the beetle
with heavy infestations of the mite, D. speciosa in a non-persistent manner. Its
Brevipalpus phoenicis, which could transmit host range appeared to be limited to the
the disease. Electron microscopy revealed Passifloraceae.
typical bacilliform rhabdovirus particles.
Citrus tristeza virus

Other Viruses
Passiflora is the only genus outside the
Passionfruit yellow mosaic virus
Rutaceae that is affected by Citrus tristeza
virus (CTV). Müller et al. (1974), following up
Passion fruit yellow mosaic was first recorded
a report by Dr A. Osores, managed to infect
from the state of Rio de Janeiro in Brazil
P. gracilis with CTV by aphid transmission.
(Kitajima et al., 1986). Symptoms started with
This was repeated, with difficulty, by
vein clearing that became a brilliant yellow,
Roistacher and Bar-Joseph (1987) with P.
net-like pattern. Chlorosis extended to the
caerulea, who were then able to transmit CTV
interveinal areas to form patches and, in
by grafting to other species.
severe cases, only the main veins retained a
Symptoms in P. gracilis were severe stunt-
green border. There was some crinkling of the
ing, interveinal yellowing followed by total
leaves. Fruit was unaffected and, although
chlorosis and death. Faint vein clearing was
plants were unthrifty, overall effects on yield
only seen on very young leaves. P. caerulea
could not be determined since a limited num-
was severely stunted, with small leaves, but
ber of plants were affected.
death did not ensue. Other species, notably
The cause was shown to be a tymovirus,
P. edulis, were not affected. Another clos-
Passionfruit yellow mosaic virus. It is isometric,
terovirus has been found in a complex of
28 nm in diameter, and was transmitted
viruses affecting P. edulis in Colombia (Varón
experimentally by the beetle Diabrotica spe-
de Agudelo et al., 1992).
ciosa in a non-persistent manner. It was also
easily transmitted mechanically and by graft-
ing, but did not pass through seed. The host
range is limited to the genus Passiflora Miscellaneous Viruses
(Crestani et al., 1986). A tymovirus forming
part of a complex has also been recorded Tomato ringspot virus has been recorded from
from Colombia (Varón de Agudelo et al., P. edulis f. flavicarpa in Peru (Koenig and
1992). Fribourg, 1986) in association with a virus
for which the name Maracuja mosaic virus
(MrMV) was later proposed (Fribourg et al.,
Purple granadilla mosaic virus 1987). MrMV is a tobamovirus that causes
systemic mosaic, is transmitted mechanically,
Purple granadilla mosaic currently is limited but is only distantly related to other
to a small area in the state of São Paulo in tobamoviruses. A serologically related strain
Brazil where it was discovered during the of MrMV has also been found in P. incarnata
course of a survey in the early 1980s in Florida (St Hill et al., 1992).
(Kitajima et al., 1986). Symptoms are a mild Jatropha mosaic virus, a geminivirus, was
mosaic, yellowing of major veins, woodiness transmitted by the whitefly Bemesia argen-
of fruits and reduced yield. Symptoms are tifolii (formerly the ‘B’ biotype of B. tabaci) to
more severe during cooler months. An iso- cultivated P. edulis in Puerto Rico (Brown
metric virus, 30 nm in diameter, was found and Bird, 1995).
Management have been launched without great success.

Passiflora spp. are not favoured by aphids
P. edulis is self-pollinated and genetically when other hosts are available. Thus, signifi-
fairly homogeneous. Since potyviruses are cant infestations of the vectors of the major
rarely transmitted through seed, seed selec- virus pathogens are not common. Visiting
tion from good producers can eliminate alates, however, are capable of initiating
these pathogens as factors in the production these diseases in the field. Field control of
of this crop. Unfortunately, seed transmis- aphids is rarely justified economically.
sion of CMV can be as high as 50%. Thus, Where practised, pruning operations can
rigorous selection in the nursery is needed to transmit these viruses. Sterilization of prun-
eliminate this virus. Symptoms can be ing implements can be easily applied and is
evanescent, which further complicates mat- effective. Suitable sterilants or inhibitors of
ters. transmission are sodium hypochlorite
P. edulis f. flavicarpa is generally self- (which aggressively rusts tools), formalde-
incompatible. Since seed progeny of this hyde, skim milk and soap. Tools should be
form segregate, it is desirable to propagate dipped in these products as often as possi-
superior selections used for production clon- ble.
ally, a practice that increases the risk of prop- Roguing of infected plants is best applied
agating and spreading viruses. The use of where a limited percentage of plants are
clonal rootstocks incurs the same risks. A affected. The same applies when a plantation
case in point is the use of P. caerulea as a root- becomes uneconomic and needs to be
stock for P. edulis in South Africa in the destroyed before re-establishment. Elimina-
1970s. Although it was tolerant of Fusarium tion of weeds in and around the plantation
wilt, the clonally propagated stocks were will assist in reducing alternative hosts of the
latently infected with PWV and CMV. The viruses. In the special cases of green spot and
spread and use of grafted plants across the jatropha mosaic, directed control of the
country brought the industry to its knees. insect vectors is indicated.
In Australia, a certification scheme using
mild strain cross-protection was used for the
control of woodiness (Simmonds, 1959a). Acknowledgements
Good producing clones that contain mild
strains of PWV are used as budwood The authors thank Ken Pegg and John
sources. P. edulis f. flavicarpa and P. edulis f. Thomas for useful editorial comments on
flavicarpa ⫻ P. edulis f. edulis hybrids are also this chapter, and Cornelia Büchen-Osmond
more resistant than P. edulis. Various small for current information on virus taxonomy
breeding programmes for virus tolerance and nomenclature.
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Tropical Fruit - Chap 18 7/5/03 1:08 PM Page 413

18 Diseases of Passion Fruit

Barry Manicom1, Carlos Ruggiero2, Randy C. Ploetz3 and

Introduction all but three of these are native to the New

The Passiﬂoraceae contains ⬃500 species and The Important Species

414 B. Manicom et al.

Diseases of Passion Fruit 415

416 B. Manicom et al.

Diseases of Passion Fruit 417

Anthracnose and fruit canker

Anthracnose and fruit canker probably occur

SYMPTOMS All aerial organs of the plant

418 B. Manicom et al.

Diseases of Passion Fruit 419

420 B. Manicom et al.

A. tenuissima produces solitary or short MANAGEMENT Thinning vines to increase

Diseases of Passion Fruit 421

422 B. Manicom et al.

Fig. 18.8. Conidia and conidiophores of

Australia, scab is a winter disease (K.G.

EPIDEMIOLOGY The optimum temperature Septoria blotch, which is also known as

Diseases of Passion Fruit 423

424 B. Manicom et al.

Diseases of Passion Fruit 425

426 B. Manicom et al.

Diseases of Passion Fruit 427

428 B. Manicom et al.

diameter day⫺1 on oatmeal agar, with abun-

Diseases of Passion Fruit 429

430 B. Manicom et al.

Management incognita and M. javanica, are important.

Diseases of Passion Fruit 431

432 B. Manicom et al.

Diseases of Passion Fruit 433

these viruses. Their morphology is indepen- In Brazil, CMV is regarded as a minor

434 B. Manicom et al.

OTHER POTYVIRUSES laris in Colombia. Symptoms included mosaic,

Diseases of Passion Fruit 435

Passionfruit latent virus (PLV) is a carlavirus.

436 B. Manicom et al.

Citrus tristeza virus

Diseases of Passion Fruit 437

Management have been launched without great success.

438 B. Manicom et al.

Diseases of Passion Fruit 439

440 B. Manicom et al.

Diseases of Passion Fruit 441

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