Powdery Mildew Review

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Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org by Chiang Mai University on 12/07/10. For personal use only.

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The Powdery Mildews: A Review of the Worlds Most Familiar (Yet Poorly Known) Plant PathogensDean A. GlaweDepartment of Plant Pathology, Washington State University and College of Forest Resources, University of Washington, Seattle 98195; email: glawe@wsu.edu

Annu. Rev. Phytopathol. 2008. 46:2751 The Annual Review of Phytopathology is online at phyto.annualreviews.org This articles doi: 10.1146/annurev.phyto.46.081407.104740 Copyright c 2008 by Annual Reviews. All rights reserved 0066-4286/08/0908/0027$20.00

Key Wordsclimate change, Erysiphales, fungal taxonomy, life histories, pathogen detection, phylogeny

AbstractThe past decade has seen fundamental changes in our understanding of powdery mildews (Erysiphales). Research on molecular phylogeny demonstrated that Erysiphales are Leotiomycetes (inoperculate discomycetes) rather than Pyrenomycetes or Plectomycetes. Life cycles are surprisingly variable, including both sexual and asexual states, or only sexual states, or only asexual states. At least one species produces dematiaceous conidia. Analyses of rDNA sequences indicate that major lineages are more closely correlated with anamorphic features such as conidial ontogeny and morphology than with teleomorph features. Development of molecular clock models is enabling researchers to reconstruct patterns of coevolution and host-jumping, as well as ancient migration patterns. Geographic distributions of some species appear to be increasing rapidly but little is known about species diversity in many large areas, including North America. Powdery mildews may already be responding to climate change, suggesting they may be useful models for studying effects of climate change on plant diseases.

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INTRODUCTIONPowdery mildews (Ascomycotina, Erysiphales) are some of the worlds most frequently encountered plant pathogenic fungi. They are often conspicuous owing to the profuse production of conidia that give them their common name (Figure 1). They infect leaves, stems, owers, and fruits of nearly 10,000 species of angiosperms (17). Among the economically important plants they infect are grapes, tree fruits, small grains, hops, and many ornamentals. Immense expenditures are made annually for fungicides and resistant varieties to control powdery mildews. Throughout the 250 years since Linnaeus rst gave a scientic name to a powdery mildew, they have gured prominently in the history of plant pathology. They have been used to study key aspects of plant disease etiology, epidemiology, and control. Powdery mildews are also models for basic research on host parasite interactions, develop-

Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org by Chiang Mai University on 12/07/10. For personal use only.

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mental morphology, cytology, and molecular biology. Because they behave as obligate plant pathogens, researchers have not had the advantage of routinely cultivating these fungi on articial media, although many powdery mildews have been grown on detached leaves of their hosts. Although one might expect there are few unanswered questions about such common, easy-to-recognize plant pathogens, this is not the case. In fact, recent research has shown that powdery mildews are more diverse and their biology more complex than generally realized. Many commonly accepted beliefs about powdery mildews, such as that sexual states are necessary to determine species, and host and geographical ranges are well understood, are erroneous. This article provides an overview of the biology and systematics of powdery mildews, focusing primarily on research of the past decade relevant to plant pathologists. Earlier work has been reviewed extensively (10, 1517, 129, 152154).

bLIFE CYCLESPowdery mildew cells and spores are similar to those of other lamentous ascomycetes. They form cell walls and contain nuclei, vacuoles, Woronin bodies, and other organelles (4, 102, 108, 118, 119). They are pleomorphic, forming multiple morphologically distinctive spore states, and they were among the rst fungi for which pleomorphism was described (34, 141). Representative morphological features are shown in Figures 2 and 3. Life cycles can involve both a sexual state (teleomorph) and asexual state (anamorph), or either can be lacking. Anamorphs are unknown in species of Brasiliomyces, Typhulochaeta, and Parauncinula, where all known reproduction involves chasmothecia (ascomata) (17, 132). Conversely, no teleomorph has been found in the subgenus Microidium of Oidium (140). In some species teleomorphs are unknown in regions with mild climates. For example, Erysiphe berberidis DC. produces chasmothecia in Europe (15) but they are unknown in western Washington (54). Life

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Figure 1 Representative symptoms and signs of powdery mildews. (a) Erysiphe alphitoides on Quercus garryana. (b) Podosphaera fuliginea on Kalanchoe blosseldiana. (c) Erysiphe necator on Vitis vinifera.28 Glawe

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cycle events in Erysiphales are synchronized with host life cycles, and effective control strategies depend on understanding how a given powdery mildew and host combination operates in a given environment (84). The following outline of powdery mildew life cycles focuses on three aspects: infection, reproduction, and perennation.

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InfectionBlumeria graminis (DC.) Speer has emerged as the most common subject of research on cellular- and molecular-level interactions of powdery mildews and their hosts (20, 156). Such work increasingly is complemented by research on Arabidopsis and the several powdery mildews that infect it (144). The adoption of additional powdery mildew species as investigative tools is fortunate because B. graminis differs signicantly from other powdery mildews. It is phylogenetically distinct, occupying a distinct clade within the Erysiphales, occurs only on Poaceae, and is unique in forming conidia that produce a primary germ tube and digitate appressoria (17, 83, 94). Despite these potential limitations, much of what we know about how powdery mildews infect their hosts is based on this species. An infection is initiated when an ascospore or conidium lands on a susceptible host, germinates, and forms a germ tube that elongates to form a hypha with appressoria, penetration pegs, and haustoria. Appressoria are short, lateral hyphal outgrowths or swellings that produce penetration pegs to infect host cells. Penetration pegs and haustoria, as well as the physiological processes associated with them, have been reviewed extensively (22, 67). Penetration pegs are narrow protrusions produced from appressoria that penetrate the walls of host cells by means of turgor pressure and enzymatic activity. The haustorium is an enlarged extension of the penetration peg, formed within the host cell. It is intimately involved in developing and maintaining the parasitic relationship with the host, and causing the plant to shunt resources to the fungus (48).

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Figure 2 Representative morphological features of Erysiphales. (a) Indistinct appressorium (Podosphaera epilobii ). (b) Lobed appressorium (Erysiphe knautiae). (c) Nipple-shaped appressorium (Golovinomyces cynoglossi ). (d ) Conidiophore with chain of conidia. (Podosphaera fusca). (e) Conidiophore forming a single conidium (Erysiphe knautiae). ( f ) Conidiophores forming single conidia, emerging from host stoma (Leveillula taurica).

Spore germination and infection occurs rapidly. Within 60 seconds of a B. graminis conidium landing on a host, liquid extracellular material with esterase and cutinase activity has been observed fastening the spore to the host (25, 149). A similar process was observed in Erysiphe australiana (McAlpine) U. Braun & S. Takam. (108). Within 3090 min, immunolabeled antigen from conidia of B. graminis was detected within the plant cell wall and cytoplasm (156). The primary germ tube generally is initiated in 3060 min (93) and produces a minute cuticular peg (41) that penetrates the plant cuticle but not the cell wall beneath it. The cuticular peg and extracellular materialwww.annualreviews.org Powdery Mildews 29

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Figure 3 Representative morphological features of Erysiphales. (a) Highly vacuolate conidia of Erysiphe berberidis. (b) Conidia of Podosphaera fusca, arrows designate brosin bodies. (c) Dimorphic conidia of Leveillula taurica. (d ) Chasmothecia of Golovinomyces cichoracearum with mycelioid appendages. (e) Chasmothecia of Erysiphe azaleae with dichotomously branched appendages. ( f ) Chasmothecium of Phyllactinia guttata with acicular appendages and dorsal gelatinous pad. ( g) Uncinate appendages of Erysiphe adunca. (h) Dichotomously branched appendages of Erysiphe azaleae. (i ) Ascus of Leveillula taurica, containing two ascospores.

from the conidium appear involved in attaching the spore to the host (156). Upon sensing the presence of the host, the primary germ tube induces production of the appressorial germ tube. The appressorium forms about 10 h after infection (156). In about two more hours the appressorium produces a penetration peg that penetrates the cell wall a