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9 October 2023

Podosphaera leucotricha (powdery mildew of apple)

Identity

Preferred Scientific Name
Podosphaera leucotricha (Ellis & Everh.) E.S. Salmon
Preferred Common Name
powdery mildew of apple
Other Scientific Names
Oidium farinosum Cooke
Oidium mespili Cooke
Sphaerotheca leucotricha Ellis & Everh.
Sphaerotheca mali Burrill
International Common Names
English
powdery mildew
Spanish
cenicilla polvorienta del manzano
mal blanco del manzano
oidio del manzano
French
blanc du cognassier
blanc du poirier
blanc du pommier
oidium du cognassier
oidium du poirier
oidium du pommier
Local Common Names
Germany
Mehltau: Apfel
EPPO code
PODOLE (Podosphaera leucotricha)

Pictures

Symptoms on apple leaves
Podosphaera leucotricha
Symptoms on apple leaves
Magnus Gammelgaard. www.plant-diseases.com
Comparison of P. leucotricha-infected and healthy vegetal and flower buds.
Symptoms
Comparison of P. leucotricha-infected and healthy vegetal and flower buds.
P. Creemers
Primary powdery mildew infections, baleen structure.
Symptoms
Primary powdery mildew infections, baleen structure.
P. Creemers
Secondary powdery mildew symptom, underside of leaf.
Symptoms
Secondary powdery mildew symptom, underside of leaf.
P. Creemers
Secondary powdery mildew symptom, upperside of leaf, chlorotic spot.
Symptoms
Secondary powdery mildew symptom, upperside of leaf, chlorotic spot.
P. Creemers
Podosphaera leucotricha symptoms on apple variety 'Golden Delicious' leaves.
Symptoms
Podosphaera leucotricha symptoms on apple variety 'Golden Delicious' leaves.
Thorsten Kraska, University of Bonn, Germany
Podosphaera leucotricha symptoms on apple variety 'Goldparmäne' leaves.
Symptoms
Podosphaera leucotricha symptoms on apple variety 'Goldparmäne' leaves.
Thorsten Kraska, University of Bonn, Germany
Podosphaera leucotricha symptoms on apple variety 'Goldparmäne' leaves.
Symptoms
Podosphaera leucotricha symptoms on apple variety 'Goldparmäne' leaves.
Thorsten Kraska, University of Bonn, Germany
Secondary powdery mildew symptoms on apple fruit (Jonagold), skin russet in network pattern.
Symptoms
Secondary powdery mildew symptoms on apple fruit (Jonagold), skin russet in network pattern.
P. Creemers
Secondary powdery mildew symptoms on apple fruit (Golden Delicious), skin russet in network pattern.
Symptoms
Secondary powdery mildew symptoms on apple fruit (Golden Delicious), skin russet in network pattern.
P. Creemers
Secondary powdery mildew symptoms on apple fruit (Jonagold), skin russet spots.
Symptoms
Secondary powdery mildew symptoms on apple fruit (Jonagold), skin russet spots.
P. Creemers
Secondary powdery mildew symptoms on pear fruit (Doyenne du Comice), skin russet and mycelium.
Symptoms
Secondary powdery mildew symptoms on pear fruit (Doyenne du Comice), skin russet and mycelium.
©P. Creemers

Distribution

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Host Plants and Other Plants Affected

HostHost statusReferences
Cydonia oblonga (quince)Main 
Malus (ornamental species apple)Main 
Malus domestica (apple)Main
Abkhoo (2015)
Malus orientalisOther 
Mespilus germanica (medlar)Other 
Photinia fraseriOther
Garibaldi et al. (2005)
Liu et al. (2023)
Photinia serratifoliaOther
Liang et al. (2012)
Prunus (stone fruit)Other 
Prunus africana (red stinkwood)Other
Mwanza et al. (2001)
Prunus domestica (plum)Other 
Pyrus (pears)Main 
Pyrus calleryana (bradford pear)Other
Vajna and Kiss (2008)
Minnis et al. (2010)
Pyrus communis (European pear)Main 
Spiraea bumaldaOther 

Symptoms

Powdery mildew attacks leaves, blossoms, fruits, buds, shoots and twigs. Primary mildew occurs in spring on flower trusses and shoots, emerging from infected flowers or vegetative buds. These organs are completely covered with a floury layer of fungal mycelium and conidia. The phenological development of infected flower buds is retarded. They are significantly reduced in size, flower stalks are stunted, and petals are fleshy, distorted and likely to be greenish-white. Diseased blossoms fail to set fruit.Shoots emerging from infected buds remain short. The leaves are narrower than normal and folded longitudinally in the form of a gutter. During the season the basal leaves wilt, becoming stiff and brittle. These primary infections on leaves and shoots often turn brown, and the leaves abscise by mid-summer. Only a brush of very small leaves may remain at the apex. Several shoots may emerge from one infected terminal bud, giving raise to a baleen structure.Secondary infections appear on leaves as small grey to white felt-like patches of fungal mycelium and spores, frequently on the underside, most commonly near the midrib. This often results in leaf curling and crinkling. The lesions appear on the upper surface as chlorotic spots. Leaf symptoms either remain localized or may develop further. The leaves on the top of the shoots roll upwards and rise up. The mycelium grows along the midrib to the petiole and the shoot, and from there to the terminal bud. Infected terminals may be silvery-grey, misshapen and more susceptible to winter frost.Infection of the fruit is most common on severely infected trees; affected fruits become russeted. On apples the surface is covered with a network pattern of fine lines. On pear, white mycelium remains visible on the fruits for a few weeks, then sloughs off giving rise to a russeted area, which expands as the fruit enlarges (Hickey and Yoder, 1997).

List of Symptoms/Signs

Symptom or signLife stagesSign or diagnosis
Plants/Fruit/abnormal patterns  
Plants/Fruit/reduced size  
Plants/Inflorescence/discoloration (non-graminaceous plants)  
Plants/Inflorescence/dwarfing; stunting  
Plants/Inflorescence/twisting and distortion  
Plants/Leaves/abnormal colours  
Plants/Leaves/abnormal leaf fall  
Plants/Leaves/fungal growth  
Plants/Leaves/leaves rolled or folded  
Plants/Leaves/wilting  
Plants/Stems/discoloration  
Plants/Stems/stunting or rosetting  

Prevention and Control

Introduction

The management of powdery mildew on apple and pear is based on the importance of primary inoculum, cultivar susceptibility, weather conditions, other diseases and the anti-resistance strategy for the available fungicides. Mildew control is very important on young trees. In nurseries, it may provoke severe stunting of the vegetative terminal growth.

Varietal Susceptibility

Although commercial apple varieties differ in the degree of susceptibility to powdery mildew, they will all become infected if large amounts of inoculum are present or if weather conditions are favourable for the spread of the disease (Aldwinckle, 1974). Highly susceptible varieties include: Jonathan, Idared, Baldwin, Cortland, Rome Beauty, Monroe, Gravenstein Holly, Stayman Winesap, Granny Smith, Paulared, Prime Gold, Britemac and Ginger Gold. Moderate susceptibility is observed on: Jonagold, Golden delicious, Cox's Orange Pippin, Gold Rush, McIntosh, Mutsu and Summerred. The newer varieties like Braeburn, Fuji and Gala are classified either as very susceptible (Grove, 1999) or tolerant (Hickey et al., 1997).Only a few apple cultivars with Vf resistance to scab (Venturia inaequalis) also carry resistance towards powdery mildew (Goerre et al., 1999). The identification of the first molecular markers for mildew resistance (Pl1 from Malus robusta and Pl2 from Malus zumi) offered breeders the opportunity to select seedlings that carry more than one resistance gene. Ariwa is an example of a resistant apple cultivar that carries both Vf and Pl1 genes. However, physiological races have been isolated from scab and powdery mildew that are able to overcome these resistance genes. Other breeding strategies are, therefore, needed in order to develop more durable resistance for cultures with rotations of generally more than 15 years. Pear cultivars are less susceptible to powdery mildew. The economic damage concerns skin russeting of the fruits (Spotts, 1984). It may be necessary to spray cultivars like Doyenne du Comice, d'Anjou and Louise Bonne. Pear orchards situated more than 200 m from an infested apple orchard must not be treated against powdery mildew because overwintering inoculum is not observed on pears.

Sanitation

Pruning infected shoots in winter and again in the following spring removes visible primary infections on emerging buds and improves the efficacy of chemical control of secondary infections later in the season. Although this practice is labour intensive and may interfere with crop production and training the tree structure, it is necessary as part of a durable control strategy.

Chemical Control

The number of fungicides available for use against powdery mildew is limited. The sterol demethylation inhibitors (DMIs) form the largest group and can be divided into fungicides with specific activity against powdery mildew, such as triadimefon and triadimenol, and those that are also effective against scab. DMIs with a distinct scab activity, such as difenoconazol, are weaker against powdery mildew, and DMIs with a distinct powdery mildew activity, such as penconazol, are weaker against scab. Different researchers have shown a shift in susceptibility of the scab fungus to DMIs. There are also indications that there has been a loss in efficacy against powdery mildew in some regions. It is important to prevent this loss in efficacy spreading by using a good anti-resistance programme for the spray schedule (Breniaux, 1996; Creemers, 1997). A limited number of treatments per season is possible with DMIs. The timing of applications is an important factor in anti-resistance management. Early treatments before blossoming sterilize primary infections emerging from the infected buds and reduce the number of applications possible later in the season when climatological conditions are more favourable to secondary mildew infections. The importance of protecting the terminal buds from secondary infections must be emphasized when controlling the pathogen, because this is the source of new infection the following year. The critical period is during rapid leaf development, from flowering till a few weeks after petal fall (Roosje, 1961; Butt, 1972; Soenen and Verheyden, 1978). Condensing the post-blossom spray programme into early summer may be more effective than dispersing spray applications throughout a long season. Interruptions to the spraying programme during this period were not rectified by later applications. Fungicide treatments during the post-bloom period controlled the infection in terminal buds by retarding the progress of the secondary mildew epidemic, thereby reducing the amount of inoculum available later in the season. The spray programme must be continued until the end of leaf growth, especially in cultivars such as Jonagold, which has strong vigour late in the season. Some of the newer apple varieties such as Braeburn, Fuji and Gala are extremely susceptible to powdery mildew and may require several treatments for effective control (Grove, 1999). Growth regulators can shorten the growth period and, indirectly, the length of the infection period of powdery mildew. In discussions about the future use and registration of growth regulators and, more particularly, their use in integrated pest management, this side effect must be stressed with regard to the pomological value. A single treatment to stop shoot growth can compensate for several applications at the end of the season and can reduce the levels of residues of products applied shortly before harvest.Other fungicides registered for powdery mildew control are sulphur, bupirimate, nitrothal-isopropyl, dinocap, pyrazophos and benzimidazoles. The use of some of these compounds is restricted because of side effects on predatory mites, plant tolerance or phytotoxicity (burning symptoms at high temperatures). Others remain under discussion because of toxicological reasons. Although benzimidazoles are registered for powdery mildew control, they are not recommended for use against the disease. Benzimidazoles are standard products for the control of storage-rot fungi, and more widespread use may increase the development of tolerant strains within the fungal storage-rot spectrum.A new group of fungicides, which offers possibilities in powdery mildew control, is the strobilurines or methoxyacrylates, which are highly effective against scab. Representatives of this new class are kresoxim-methyl and trifloxystrobin. These compounds inhibit mitochondrial respiration and strongly inhibit spore germination, germ tube elongation and appressorium formation. Deposits of strobilurines provide a protective reservoir on the plant surface. The molecule has high affinity for the waxy layers ensuring high retention against wash-off by rainfall and it can be redistributed over small distances to untreated plant parts by superficial vapour movement. Small amounts of chemical penetrate the cuticle and provide protectant activity and also some curative and eradicant activity against pathogens located close to the plant surface. They especially prevent the formation of conidiophores and conidia.The detection of resistant strains of powdery mildew on wheat in nothern Germany in 1998 and 1999, and to some extent in other western countries, has stressed the importance of the introduction of anti-resistance strategies. The FRAC-STAR (Fungicide Resistance Action Committee-Strobilurin Type Action and Resistance) working group recommends a maximum of three chemical treatments per pome fruit crop, the preventative use of fungicides, and adherence to recommended rates.Reduced water volumes in spray solution is the most viable solution to controlling diseases such as apple scab. Most growers apply a fungicide with combined efficacy on apple scab and powdery mildew or a mixture. For control of powdery mildew, the water quantity needed to cover the susceptible tissues to prevent powdery mildew infection influences the efficacy of the compound. Unlike scab, powdery mildew infects leaves during periods of relatively hot and humid weather, when the trees are growing rapidly and without rain to redistribution the fungicide. Temperature, relative humidity and leaf coverage are important factors influencing penetration (Schmitz and Noga, 1996; Mantinger et al., 1993).The eradication of primary infections with compounds which kill the mycelium in the buds was not successful in practice because of the risk of killing healthy buds (Hislop et al., 1978).Disease assessment and forecasting systems should be highly effective in the optimal timing of sprays. PodemTM, developed in East Malling, UK, is one such model, which simulates epidemics of secondary mildew on vegetative shoots at daily intervals (Xu, 1999). This forecast infection model is incorporated in a commercial PC-based software package called AdemTM (Apple Diseases, East Malling, UK) which also contains models for apple scab, Nectria fruit rot and canker, and fireblight on apple and pear (Berrie, 1997).

Impact

Economic losses from powdery mildew vary with climatic conditions, cultivar susceptibility and cultural practices in orchards and nurseries. Leaf attack reduces the photosynthetic area and leads to smaller fruit and consequent loss in yield. Yoder and Hickey (1983) harvested 26 kg fruit/tree from untreated plots and 95 kg/tree from plots where mildew was controlled. Infected trees have an increased water requirement (Müller, 1957). Heavily mildewed trees are weakened and are more susceptible to other pests and winter injury (Ellis, 1994). The most critical loss in commercial value is through skin russeting of the fruits. Powdery mildew can be particularly severe in nurseries. Good control at this stage is needed to prevent control failures later in the commercial orchard.

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Published online: 9 October 2023

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English

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