Powdery mildews are probably the most common, conspicuous, wide
spread, and easily recognizable plant diseases. They affect all kinds of plants: cereals and grasses, vegetables, ornamentals, weeds, shrubs, fruit trees, and broad-leaved shade and forest trees.
Powdery mildews are characterized by the appearance of spots or patches of a white to grayish, powdery, mildewy growth on young plant tissues, or of entire leaves and other organs being completely covered by the white powdery mildew. Tiny, pinhead-sized, spherical fruiting bodies, at first white, later yellow-brown, and finally black cleistothecia may be present singly or in groups on the white to grayish mildew in the older areas of infection. Powdery mildew is most commonly observed on the upper side of the leaves but it also affects the under side of leaves, young shoots and stems, buds, flowers, and young fruit.
The fungi causing powdery mildews are obligate parasites—they can
not be cultured on artificial nutrient media. They produce mycelium that grows only on the surface of plant tissues, never invading the tissues themselves. They obtain nutrients from the plant by sending haustoria, i.e., feeding organs, into the epidermal cells of the plant organs. The mycelium produces short conidiophores on the plant surface. Each con
idiophore produces chains of rectangular, ovoid, or round conidia that are carried by air currents. When environmental conditions or nutrition become unfavorable, the fungus may produce one or a few asci inside a closed ascocarp, the cleistothecium. The powdery mildew fungi, al
though they are common and cause serious diseases in cool or warm, humid areas, are even more common and severe in warm, dry climates.
This happens because their spores can be released, germinate, and cause infection even when only the relative humidity in the air is fairly high without need for the presence of a film of water on the plant surface. Also
because, once infection has begun, the mycelium continues to spread on the plant surface regardless of the moisture conditions in the atmosphere.
The powdery mildew diseases of the various crop or other plants are caused by many species of fungi of the family Erysiphaceae grouped into six main genera. These genera are distinguished from each other by the number (one versus several) of asci per cleistothecium and by the mor-phology of hyphal appendages growing out of the wall of the cleis-tothecium. The main genera are illustrated in Fig. 63, and the most important diseases they cause are listed below.
Erysiphe dehoracearum, causes powdery mildew of begonia, chrysanthemum, cosmos, cucurbits, dahlia, flax, lettuce, phlox, zinnia.
E. graminis, causes powdery mildew of cereals and grasses (Fig. 72G).
E. polygoni, causes powdery mildew of beans, soybeans, clovers and other legumes, beets, cabbage and other crucifers, cucumber and cantaloupe, delphinium, hydrangea.
Microsphaera aini, causes powdery mildew of blueberries, catalpa, elm, lilac, linden, oak, rhododendron, and sweet pea.
Phyllactinia sp., causes powdery mildew of catalpa, elm, maple, oak.
Podosphaera leucotricha, causes powdery mildew of apple (Fig. 72F), pear and quince.
P. oxyacanthae, causes powdery mildew of apricot, cherry, peach and plum.
Sphaerotheca macularis, causes powdery mildew of strawberry.
5. mors-uvae, causes powdery mildew of gooseberry and current.
5. pannosa, causes powdery mildew of peach and rose (Fig. 72, A - C ) . Uncinula necator, causes powdery mildew of grape, horsechestnut, linden (Fig.
72, D, E).
• Powdery Mildew of Rose and Peach
Powdery mildew of roses occurs everywhere in the world where roses are grown. The disease is less common on peaches although it has been found to affect peaches in the U.S., Europe, and Africa.
Powdery mildew is one of the most important diseases of roses, both in the garden and in the greenhouse. The disease appears on roses year after year and causes reduced flower production and weakening of the plants by attacking the buds, young leaves, and growing tips of the plants.
Powdery mildew is usually less severe 'on peach, but when weather conditions are favorable for infection, peach seedlings are stunted, fruit production is reduced, and the quality of infected fruit is very poor.
Symptoms. On the young leaves the disease appears at first as slightly raised blisterlike areas that soon become covered with a grayish white, powdery fungus growth, and as the leaves expand they become curled and distorted (Fig. 72). On the older leaves, large white patches of fungus growth appear, but there is usually little distortion. Lesions on leaves may appear more or less discolored and may eventually become necrotic.
White patches of fungus growth, similar to those on the leaves, usually appear on young, green shoots, and they may coalesce and cover the entire terminal portions of the growing shoots, which may become
FIGURE 72.
Powdery mildew on rose leaves (A) and petals (B), and on peach fruit (C) caused by Sphaerotheca pannosa. (D, E) Mycelium, conidia and dark cleistothecia on grape leaves (D) and fruit cluster (E) caused by the powdery mildew fungus Uncinula necator. (F) Powdery mildew on apple twigs caused by Podosphaera leucotricha.
(G) Powdery mildew on wheat leaves caused by Erysiphe graminis. The dark dots are cleistothecia. (Photos D, Ε courtesy Shade Tree Lab, Univ. of Mass. Photo G courtesy U.S.D.A.)
arched or curved at their tip. Sometimes buds may be attacked and become covered with white mildew before they open, and they either fail to open or open improperly, the infection spreading to the flower parts, which become discolored, dwarfed, and eventually dried.
When peach fruit becomes infected, white circular spots appear which may spread over a large portion or the whole surface of the fruit. The fruit color becomes pinkish at first and later turns to a dark brown, while the fruit surface becomes leathery and hard and sometimes it appears swollen or cracked.
The pathogen: Sphaerotheca pannosa. The pathogen that causes powdery mildew on roses seems to be a distinct variety of S. pannosa, since it has been shown in some cases that the fungus from roses does not attack peaches, and vice versa. The life history and the behavior of the fungus, however, are the same in both cases, and therefore they will be described as one.
The mycelium is white and grows on the surface of the plant tissues, sending globose haustoria into the epidermal cells of the plant (Fig. 73).
FIGURE 73.
Disease cycle of powdery mildew of roses and peach caused by Sphaerotheca pannosa.
The mycelium forms a weft of hyphae on the surface, some of which develop into short, erect, conidiophores. At the tip of each conidiophore egg-shaped conidia are produced which cling together in chains.
With the coming of cool weather late in the season, conidia production ceases and cleistothecia may be formed. The young cleistothecia are globose and at first white, then brown, and finally black when mature.
The mature cleistothecia also have several mycelioid appendages, which are flaccid, indefinite hyphae arising from cells of the cleistothecium.
The cleistothecia are more or less buried in the mycelial wefts on the plant tissues. The ascospores continue to develop during the fall, and in the spring they are mature and ready for dissemination. In the spring the cleistothecia absorb water and crack open. The single ascus in each cleistothecium protrudes its tip, bursts open and discharges its 8 mature ascospores, which the wind carries away. The ascospores are about the size of conidia and behave exactly like conidia with respect to germina-tion, infecgermina-tion, and formation of subsequent structures.
Development of disease. On peaches and outdoor roses the fungus apparently overwinters mostly as mycelium in the buds, although on outdoor roses cleistothecia form occasionally on leaves, petals, and stems, especially around the thorns, toward the end of the season. Cleis-tothecia are much more rare on peach. On greenhouse roses the pathogen overwinters almost exclusively as mycelium and conidia.
When the fungus overwinters as mycelium in dormant buds, shoots arising from such buds become infected and provide inoculum for sub-sequent secondary mycelial or spore infection and disease development on foliage and fruit. When the fungus overwinters as cleistothecia the discharged mature ascospores also serve as primary inoculum (Fig. 73).
Ascospores or conidia are carried by wind to young green tissues, and if temperature and relative humidity are sufficiently high the spores germi-nate by putting out a germ tube. The germ tube quickly produces a short, fine hypha growing directly through the cuticle and the epidermal cell wall into the epidermal cells. The penetrating hypha enlarges im-mediately upon entrance into the cell lumen and forms a globose haus-torium by which the fungus obtains its nutrients. The germ, tube con-tinues to grow and branch on the surface of the plant tissue producing a network of superficial mycelium. As the mycelium spreads on the plant, it continues to send haustoria into the epidermal cells. The absorption of nutrients from the cells depletes their food supply, weakens them, and may sometimes lead to their death. Photosynthesis in the affected areas is greatly reduced and the other functions of the cells are also impaired.
Infection of young leaves also causes irritation and uneven growth of the affected and the surrounding cells resulting in slight raised areas on the leaf and distortion of the leaf. The aerial mycelium produces short, erect conidiophores each bearing a chain of 5 to 10 conidia. The conidia are disseminated by air currents and cause new infections on the expanding leaves, shoots, and on peach, on the fruit. Greenhouse roses are suscepti-ble throughout the year. In the field, however, expanding tissues seem to be the most susceptible ones and only under very favorable humidity and
temperature do fully developed tissues become infected. Growth of se-verely infected shoots is inhibited. Infected buds often do not open. If they do open, the flowers become infected and do not develop. Peach fruits are susceptible from the time of their formation until they are approximately 2.5 to 3.0 cm in diameter, beyond which they become resistant to powdery mildew. Once fruit infections are established, how-ever, the lesions continue to enlarge for several weeks after the fruit becomes resistant to new infections. Infected fruits are smaller and un-sightly and must be sold at a much lower price.
Control. Powdery mildew can be controlled by application of sulfur, dinocap, benomyl, or certain other fungicides. Sulfur may be used as a spray, as a dust and, in the greenhouse, as a vapor also. Dinocap, benomyl, and cycloheximide are used as sprays. Under most conditions weekly applications give adequate protection, but during rapid development of new growth, temperature fluctuations and frequent rains, more frequent applications may be necessary.
SELECTED REFERENCES
Cherewick, W. J. 1944. Studies on the biology of Erysiphe graminis. Can. f. Res.
2 2 : 5 2 - 8 6 .
Hills, F. J., et al. 1975. Effect of powdery mildew on sugarbeet production. Plant Disease Reptr. 5 9 : 5 1 3 - 5 1 5 .
Keil, H. L., and R. A. Wilson. 1961. Powdery mildew of peach. Plant Disease Reptr. 4 5 : 1 0 - 1 1 .
Longree, Karla. 1939. The effect of temperature and relative humidity on the powdery mildew of roses. Cornell Univ. Agr. Expt. Sta. Mem. 223:43 p.
Massey, L. M. 1948. Understanding powdery mildew. Am. Rose Ann. 3 3 : 1 3 6 -145.
Moseman, J. G. 1966. Genetics of powdery mildews. Ann. Rev. Phytopathol.
4 : 2 6 9 - 2 9 0 .
Salmon, E. S. 1900. A monograph of the Erysiphaceae. Mem. Torrey Bot. Club Vol.
9: 292 p.
Schnathorst, W. C. 1965. Environmental relationships in the powdery mildews.
Ann. Rev. Phytopathol. 3 : 3 4 3 - 3 6 6 .
Weinhold, A. R. 1961. Temperature and moisture requirements for germination of conidia of Sphaerotheca pannosa from peach. Phytopathology 5 1 : 6 9 9 - 7 0 3 . Yarwood, C. E. 1957. Powdery mildews. Bot. Rev. 2 3 : 2 3 5 - 3 0 0 .
FOLIAR DISEASES
CAUSED BY ASCOMYCETES AND IMPERFECT FUNGI
Many species of Ascomycetes and of Imperfect Fungi cause primarily foliage diseases but some may also affect blossoms, young stems, and
fruit and even roots.
Most of the foliar Ascomycetes reproduce by means of conidia formed on free hyphae or in pycnidia but a few produce conidia in sporodochia, or in acervuli. In many the conidia overwinter; others reproduce by means
of conidia during the growing season and by their perfect ascigerous stage at the end of the season and over winter; some produce their ascocarps and ascospores, along with conidia, throughout the growing season. The primary inoculum of these fungi, therefore, may be either ascospores or conidia and usually originates from infected fallen or hanging leaves of the previous year.
Some of the most common Ascomycetes causing primarily foliar dis-eases are the following:
Coccomyces sp., causing leaf spot or shot-hole of cherries and plums.
Dothidella ulei, causing South American leaf blight of rubber.
Elytroderma deformans, causing a leaf spot and witches'-broom of pines.
Lophodermium pinastri, causing needle blight of pines.
Guignardia, causing leaf spot and black rot of grape, G. bidwellii, leaf blotch of horsechestnut (G. aesculi), and leaf spots on Boston ivy and Virginia creeper.
Mycosphaerella, causing the extremely destructive Sigatoka disease of banana [M. musicola), leaf spots of strawberry (M. fragariae), of pear (M. sentina), leaf spot and black rot of cucurbits (M. melonis), citrus greasy spot [M. citri), and other diseases.
Pseudopeziza, causing the common leaf spot of alfalfa (Fig. 74 A) and clovers and the yellow leaf blotch of alfalfa.
Rhabdocline pseudotsugae, causing needle cast of Douglas fir.
Rhytisma, causing tar spot of maple and willow.
Scirrhia, causing brown spot needle blight of pine [S. acicola, the conidial stage of which is Lecanosticta or Septoria), and Dothistroma needle blight of pine [S. pini, the conidial stage of which is Dothistroma pini).
Some of the most common Imperfect Fungi causing primarily foliar, but also other, symptoms on a large variety of host plants are: Ascochyta, Cercospora (Fig. 74B), Cladosporium (Fig. 74C), Helminthosporium, Phyl-losticta, Pyricularia (Fig. 75), and Septoria. Many other fungi, e.g., Alter-naria and Botrytis, could be listed here, but they so frequently affect other plant parts that they are discussed elsewhere.
The foliar spots and blights caused by Imperfect Fungi affect numer-ous hosts and appear in many variations. However, the disease cycles and controls of these diseases are quite similar, although considerable vari-ability may exist between diseases caused by specific fungi on different hosts, especially when the diseases develop under different environmen-tal conditions. Thus, these fungi attack primarily the foliage of annual and/or perennial plants by means of conidia produced on free, single or grouped hyphae [Cercospora, Cladosporium, Helminthosporium, and Pyricularia) or in pycnidia [Ascochyta, Phyllosticta, and Septoria). On the infected areas numerous conidia are produced which spread by wind, water, insects, etc. to other plants and cause more infections. In most cases these fungi overwinter primarily as conidia or mycelium in fallen leaves or other plant debris. Some, however, can overwinter as conidia in or on seed of infected plants, or in the soil. When perennial plants are infected, they may overwinter as mycelium in infected tissues of the plant.
When these fungi are carried with the seed of annual plants, damping off of seedlings may develop. Control of such diseases is accomplished by using resistant varieties and fungicidal sprays, but disease-free seed and/or
re-FIGURE 74.
(A) Alfalfa leaf spot caused by Pseudopeziza medicaginis. (B) Sugar beet leaf spot caused by Cercospora beticola. (C) Tomato leaf mold caused by Cladosporium fulvum. (Photo C courtesy of U.S.D.A.).
moval and destruction of contaminated debris may be most important in some diseases.
• Coccomyces Leaf Spot or Shot-hole of Cherries and Plums
Widespread and serious throughout the world, especially in areas with humid climate, it is most severe on sour cherries and less so on sweet
FIGURE 75.
Foliar symptoms on rice leaves caused by the rice blast fungus Pyricularia oryzae. (Photo courtesy U.S.D.A.)
cherries and plums. In cherries, the symptoms appear as numerous mi-nute, red to purplish-black spots on the upper sides of leaves and, in severe infections, on the petioles, fruit and pedicels (Fig. 76A). On the under sides of the spots on the leaves, slightly raised, waxy pustules appear that after heavy dews or rains produce a white, mildewlike growth. Infected leaves usually turn yellow and fall, or the spots may drop out and the leaves have a shot-hole appearance. The shot-hole effect is even more common and more pronounced on plum and prune leaves which may appear completely skeletonized. Severe leaf drop and shot-holing early in the season are common and weaken the trees which may die back during the same or in subsequent years. The disease is especially common and serious in nursery plantings.
The fungus, Coccomyces sp. (or Higginsia sp.), produces ascospores in apothecia formed in fallen infected leaves and Cylindrosporium-type conidia formed in acervuli on the under side of infected leaves. The conidia are colorless, threadlike, straight or curved and consisting of one or several cells. The ascospores are produced in the spring over a period of 6 to 7 weeks and are forcibly ejected when the leaves are thoroughly soaked. The ascospores are then carried by air currents and cause the primary infections on the leaves which then produce large numbers of conidia that are spread by rain from leaf to leaf and cause all the sub-sequent infections.
Control of the disease is achieved by 4 to 5 sprays starting at petal-fall, and one postharvest spray with benomyl, captan, or certain other fun-gicides such as dodine, sulfur, or ferbam.
• Guignardia Leaf Spot and Black Rot of Grape
It is present in Europe and in the U.S. and Canada east of the Rocky Mountains. It is probably the most serious disease of grapes where it commonly occurs, particularly in warm, humid regions. In the absence of control measures and in favorable weather, the crop it usually destroyed completely either through direct rotting of the berries or through blasting of the blossom clusters.
The disease causes numerous scattered, circular, red necrotic spots on leaves in late spring (Fig. 76, C-G). The spots form usually between the veins and are most apparent on the upper side of the leaves. Later, when the spots are about 2 to 6 mm or more in diameter, the main area of the spots appears brown to grayish-tan while their margins appear as a black line. Black dotlike, Phyllosticta-type pycnidia are formed on the upper
side of the spots in a ring near the outer edge of the brown area of the spot.
On the shoots, tendrils, the leaf and flower stalks, and on leaf veins, the spots are purple to black, somewhat depressed and elongated, and bear scattered pycnidia. Spots begin to appear on berries when the latter are about half grown. These spots are at first whitish but are soon surrounded by a rapidly widening brown ring with a black margin. The central area of the spot remains flat or becomes depressed and dark pycnidia appear near the center. The whole berry soon becomes rotten and shrinks, and be-comes coal black as the surface bebe-comes studded with numerous black pycnidia.
The fungus, Guignardia bidwellii, in addition to conidia-bearing pyc-nidia, also produces ascospores in globose perithecia forming in rotten, mummied fruit. The perithecia supposedly develop from transformed pycnidia. The fungus overwinters mostly as ascospores in perithecia, but conidia can also survive the winter in most locations where grapes grow, so both ascospores and conidia can cause primary infections in the spring (Fig. 77). The release of ascospores and conidia takes place only when the
The fungus, Guignardia bidwellii, in addition to conidia-bearing pyc-nidia, also produces ascospores in globose perithecia forming in rotten, mummied fruit. The perithecia supposedly develop from transformed pycnidia. The fungus overwinters mostly as ascospores in perithecia, but conidia can also survive the winter in most locations where grapes grow, so both ascospores and conidia can cause primary infections in the spring (Fig. 77). The release of ascospores and conidia takes place only when the