ANRV351-PY46-03 ARI 22 June 2008 11:1

The Powdery Mildews:A Review of the World’s MostFamiliar (Yet Poorly Known)Plant PathogensDean A. GlaweDepartment of Plant Pathology, Washington State University and College of ForestResources, University of Washington, Seattle 98195; email: glawe@wsu.edu

Annu. Rev. Phytopathol. 2008. 46:27–51

The Annual Review of Phytopathology is online atphyto.annualreviews.org

This article’s 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 Words

climate change, Erysiphales, fungal taxonomy, life histories, pathogendetection, phylogeny

AbstractThe past decade has seen fundamental changes in our understandingof powdery mildews (Erysiphales). Research on molecular phylogenydemonstrated that Erysiphales are Leotiomycetes (inoperculate dis-comycetes) rather than Pyrenomycetes or Plectomycetes. Life cyclesare surprisingly variable, including both sexual and asexual states, oronly sexual states, or only asexual states. At least one species producesdematiaceous conidia. Analyses of rDNA sequences indicate that ma-jor lineages are more closely correlated with anamorphic features suchas conidial ontogeny and morphology than with teleomorph features.Development of molecular clock models is enabling researchers to re-construct patterns of coevolution and host-jumping, as well as ancientmigration patterns. Geographic distributions of some species appear tobe increasing rapidly but little is known about species diversity in manylarge areas, including North America. Powdery mildews may alreadybe responding to climate change, suggesting they may be useful modelsfor studying effects of climate change on plant diseases.

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INTRODUCTION

Powdery mildews (Ascomycotina, Erysiphales)are some of the world’s most frequently en-countered plant pathogenic fungi. They are of-ten conspicuous owing to the profuse produc-tion of conidia that give them their commonname (Figure 1). They infect leaves, stems,flowers, and fruits of nearly 10,000 speciesof angiosperms (17). Among the economicallyimportant plants they infect are grapes, treefruits, small grains, hops, and many ornamen-tals. Immense expenditures are made annuallyfor fungicides and resistant varieties to controlpowdery mildews. Throughout the 250 yearssince Linnaeus first gave a scientific name toa powdery mildew, they have figured promi-nently in the history of plant pathology. Theyhave been used to study key aspects of plantdisease etiology, epidemiology, and control.Powdery mildews are also models for basic re-search on host parasite interactions, develop-

a b

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

mental morphology, cytology, and molecularbiology. Because they behave as obligate plantpathogens, researchers have not had the advan-tage of routinely cultivating these fungi on ar-tificial media, although many powdery mildewshave been grown on detached leaves of theirhosts.

Although one might expect there are fewunanswered questions about such common,easy-to-recognize plant pathogens, this is notthe case. In fact, recent research has shown thatpowdery mildews are more diverse and theirbiology more complex than generally realized.Many commonly accepted beliefs about pow-dery mildews, such as that sexual states arenecessary to determine species, and host andgeographical ranges are well understood, areerroneous. This article provides an overviewof the biology and systematics of powderymildews, focusing primarily on research ofthe past decade relevant to plant pathologists.Earlier work has been reviewed extensively (10,15–17, 129, 152–154).

LIFE CYCLES

Powdery mildew cells and spores are simi-lar to those of other filamentous ascomycetes.They form cell walls and contain nuclei, vac-uoles, Woronin bodies, and other organelles(4, 102, 108, 118, 119). They are pleomorphic,forming multiple morphologically distinctivespore states, and they were among the firstfungi for which pleomorphism was described(34, 141). Representative morphological fea-tures are shown in Figures 2 and 3. Life cy-cles can involve both a sexual state (teleomorph)and asexual state (anamorph), or either can belacking. Anamorphs are unknown in species ofBrasiliomyces, Typhulochaeta, and Parauncinula,where all known reproduction involves chas-mothecia (ascomata) (17, 132). Conversely, noteleomorph has been found in the subgenusMicroidium of Oidium (140). In some speciesteleomorphs are unknown in regions with mildclimates. For example, Erysiphe berberidis DC.produces chasmothecia in Europe (15) but theyare unknown in western Washington (54). Life

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cycle events in Erysiphales are synchronizedwith host life cycles, and effective control strate-gies depend on understanding how a given pow-dery mildew and host combination operatesin a given environment (84). The followingoutline of powdery mildew life cycles focuseson three aspects: infection, reproduction, andperennation.

Infection

Blumeria graminis (DC.) Speer has emergedas the most common subject of research oncellular- and molecular-level interactions ofpowdery mildews and their hosts (20, 156).Such work increasingly is complemented by re-search on Arabidopsis and the several powderymildews that infect it (144). The adoption ofadditional powdery mildew species as investiga-tive tools is fortunate because B. graminis dif-fers significantly from other powdery mildews.It is phylogenetically distinct, occupying a dis-tinct clade within the Erysiphales, occurs onlyon Poaceae, and is unique in forming conidiathat produce a primary germ tube and digitateappressoria (17, 83, 94). Despite these potentiallimitations, much of what we know about howpowdery mildews infect their hosts is based onthis species.

An infection is initiated when an ascosporeor conidium lands on a susceptible host, ger-minates, and forms a germ tube that elon-gates to form a hypha with appressoria, penetra-tion pegs, and haustoria. Appressoria are short,lateral hyphal outgrowths or swellings thatproduce penetration pegs to infect host cells.Penetration pegs and haustoria, as well as thephysiological processes associated with them,have been reviewed extensively (22, 67). Pen-etration pegs are narrow protrusions producedfrom appressoria that penetrate the walls of hostcells by means of turgor pressure and enzymaticactivity. The haustorium is an enlarged exten-sion of the penetration peg, formed within thehost cell. It is intimately involved in develop-ing and maintaining the parasitic relationshipwith the host, and causing the plant to shuntresources to the fungus (48).

a b c

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

Spore germination and infection occursrapidly. Within 60 seconds of a B. graminisconidium landing on a host, liquid extracellu-lar material with esterase and cutinase activityhas been observed fastening the spore to thehost (25, 149). A similar process was observedin Erysiphe australiana (McAlpine) U. Braun &S. Takam. (108). Within 30–90 min, immuno-labeled antigen from conidia of B. graminis wasdetected within the plant cell wall and cyto-plasm (156). The primary germ tube gener-ally is initiated in 30–60 min (93) and producesa minute “cuticular peg” (41) that penetratesthe plant cuticle but not the cell wall beneathit. The cuticular peg and extracellular material

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a b c

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

from the conidium appear involved in attachingthe spore to the host (156). Upon sensing thepresence of the host, the primary germ tubeinduces production of the appressorial germtube. The appressorium forms about 10 h afterinfection (156). In about two more hours theappressorium produces a penetration peg thatpenetrates the cell wall and the dome-shapeddeposit of host cell wall material (termed thepapilla) formed in response to the fungus (155,156). If the fungus is successful in breaching

the host wall, the penetration peg extends intothe host cell, invaginating the cytoplasm, andenlarging to form the haustorium. The hausto-rium is surrounded by extrahaustorial matrix,a noncytoplasmic, gel-like material that mayhelp protect the fungus from host responses(67). The haustorium, extrahaustorial matrix,and host cell are the sites of molecular signal-ing events. Host responses and nutrient transferdetermine whether a successful parasitic rela-tionship develops and is maintained (67, 156).

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Fotopoulos et al. (48) noted that physiologicalchanges within the host extend beyond the in-fected cell to facilitate transfer of nutrients fromthe plant to the fungus. Powdery mildews canretard senescence of infected tissues, resultingin the symptom known as “green islands” (27).

Asexual Reproduction

After infection of the host, hyphae elongate andbranch repeatedly, forming circular colonies.Young hyphae are transparent or whitish butfrequently turn grayish, reddish, or brownishduring maturation (17). Hyphae of most pow-dery mildews grow superficially on their hostbut species in the tribe Phyllactinieae can growinside host tissue (17). Some species form differ-entiated, secondary hyphae (17). Such hyphaeare filiform to falcate in Cystotheca (17), forkedin Queirozia (98), falcate in Blumeria (17), andsimple in Caespitotheca (137). Somatic (assim-ilative) hyphae eventually give rise to repro-ductive structures (conidiophores and/or chas-mothecia).

Conidial production typically begins withinseveral days of infecting the host. Repre-sentative anamorph features are shown inFigure 3. Conidiophores arise from vegetativehyphae and are oriented more or less perpen-dicularly to the surface of the host. The firstcomplete cell of the conidiophore is termedthe foot cell and it subtends one or moreadditional cells, including the generative cellinvolved in forming conidia. Conidial produc-tion is basauxic—that is, conidia form succes-sively with each new conidium forming at thebase of the previous conidium (109, 111, 112).Species form conidia that mature singly (thePseudoidium group), or in a graduated series(generally referred to as a chain of conidia)with the oldest conidium at the top (the Euoid-ium group). Conidiophores generally are sim-ple (unbranched), although branched ones areoften illustrated for Leveillula taurica (Lev.) G.Arnaud (e.g., 13, 17).

There is little published information onthe ultrastructure of conidiogenesis in powderymildews. A noteworthy exception is the study

of Martin & Gay (102) who described conidialdevelopment in Erysiphe pisi DC. Their pho-tographs illustrated cytoplasmic continuity ex-tending through the complete series of cellsfrom the haustoria to developing conidia, facili-tating transport of metabolites until the matureconidium detached from the conidiophore.

Powdery mildew conidia are single cells(17). Except for one species with dematiaceous(dark-pigmented) conidia, they are colorless(98). Conidia range in shape from nearly ovoidto cylindrical or lanceolate (13, 15). In mostspecies conidia are monomorphic. Dimorphicconidia are formed in species of Leveillula andPleochaeta (15, 17) and Phyllactinia (97). Speciesof Sawadaea form synanamorphs, with macro-conidia and microconidia produced from coni-diophores that also differ dramatically in size(15, 58). Conidia are uninucleate and containvacuoles and large amounts of water, possi-bly contributing to their ability to germinatein the absence of free water (126, 152, 154).Conidia in the tribe Cystotheceae (which in-cludes the genera Cystotheca, Podosphaera, andSawadaea) contain fibrosin bodies (17). Theseare refractive, variously shaped bodies that formas rods, cones, tori, or curved or straight plates.Foex (46) believed they consisted of callose, andHomma (80) reported fibrosin bodies to con-tain B IV carbohydrate and nitrogen. Braunet al. (17) noted that they still are poorly un-derstood.

Powdery mildew conidia display variouskinds of surface ornamentation and a liquidcoating when viewed with scanning electronmicroscopy (e.g., 39, 65, 73, 82, 108, 117). Someof the features also can be discerned using highmagnifications with brightfield or differentialinterference contrast microscopy (55, 60). Thesurface features are thought to be useful tax-onomically (29). The appearance of conidialsurfaces varies according to whether they areviewed while fresh and turgid or dry and col-lapsed (17).

Proposed mechanisms for the release ofconidia from conidiophores include mechanicalforce (117), convection currents (49), wind (70,75, 111, 130), electrostatic charges (1, 95), and

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leaf shaking or fluttering (9). High relative hu-midity appears negatively correlated with dis-persal of conidia (70, 74, 130). Conidial pro-duction and release frequently follows a diurnalpattern, with most spores becoming airbornein the period extending from mid-morning toearly afternoon (24, 28, 70, 102, 113, 114, 125,130, 151). Profusely sporulating colonies maybecome covered with mats of clumped sporesthat are less prone to dissemination (75).

Conidial dispersal appears to occur mostlyover short distances. Peries (116) found that90% of conidia formed by Podosphaera macularis(Wallr.) U. Braun & S. Takam. traveled less than2 m from host plants. On the other hand, coni-dia of Golovinomyces cichoracearum (DC.) V.P.Heluta were reported to be dispersed 200 kmin California (125), and airborne conidia of B.graminis traveled from the British Isles to in-fect plants in Denmark nearly 700 km away(78). Examples of rapid dispersal over long dis-tances include Erysiphe betae (Vanha) Weltzienon beet crops in North America and Europe(37); expansion of the range of Erysiphe neca-tor Schwein. from the British Isles in 1845 tothe rest of western and central Europe andthe Mediterranean region by 1852 (148); andexpansion of P. macularis on hop from east-ern Washington, where it was first observedin 1996, to Idaho and Oregon by 1998 (100).Effective dispersal over long distances may befavored by production of enormous numbersof conidia when a high density of sporulat-ing colonies occurs on a large host population.Schnathorst (125) calculated that when lettuceplants supported 67 colonies per leaf, approxi-mately 80 million conidia of G. cichoracearumwere disseminated per hectare every 24 h.Hermansen et al. (78) reported that 5–10 hof favorable conditions for B. graminis conidialrelease in Britain produced spore showers re-sulting in 1–2 million infections per hectare inDenmark.

Conidia are dispersed either singly or inshort chains (125), germinate readily and, un-like those of other fungi, do not require freewater for germination (23, 67, 84, 126, 152).Conidia generally appear unable to germinate

until after secession. Patterns of conidial germi-nation are taxonomically useful (15, 17). Dis-tinctions that have been noted include differ-ences in location of germ tubes, time requiredfor germ tube production, and whether or notappressoria form on germ tubes (15, 17).

Sexual Reproduction

The term chasmothecium was suggested byBraun et al. (17) to distinguish powdery mildewascomata from those of other ascomycetes. Ear-lier authors either termed them cleistotheciabecause they lack ostioles (e.g., 3, 52, 147),or perithecia because multiascal species form ahymenium-like layer (7, 64). During ascosporedischarge chasmothecia develop a more-or-lessvertical or circumscissile split (or “chasm”) inthe peridium. The rupture apparently resultsfrom increased turgor pressure that developswhen free water is absorbed by chasmothecia(e.g., 51, 123, 124, 143). In Phyllactinia guttata(Wallr.) Lev. the peridium splits equatorially toexpose asci (123, 146), allowing the chasmoth-ecium to open in a clamshell-like fashion toexpose asci for spore discharge.

Chasmothecia are light-colored when firstdiscernable, becoming yellowish or amber-colored, and finally dark brown to black whenmature (e.g., 59). They are not produced instromata but can be closely associated with thickwefts of hyphae (e.g., 60). Chasmothecia (exclu-sive of appendages) range from 50 μm to about400 μm; most ascomata are 100–200 μm in di-ameter and the size range of individual speciestends to be consistent (15). Work on B. grami-nis indicated that while nutrients supplied bythe host are critical in early stages of develop-ment, sufficient reserves eventually are storedwithin the mycelium that chasmothecial devel-opment proceeds without depending on a con-tinued supply of host metabolites (66). The ma-ture ascoma is self-contained and delimited bythe peridium, which consists of closely packedmelanized cells (15, 17).

Major features of sexual reproduction weresummarized by Braun et al. (17), with partic-ular attention to work by Dorfelt et al. (36)

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and Dorfelt & Ali (35), whose work helpedresolve longstanding questions and inconsis-tencies. The following description is basedlargely on Braun et al. (17). Species may be ho-mothallic or heterothallic. Sexual reproductionin powdery mildews is initiated by productionof gametangia (also termed gamocysts). Malegametangia usually are termed antheridia or an-drogamocysts, and female gametangia termedascogonia or gynogamocysts (17). Followingplasmogamy (establishment of a cytoplasmicconnection between the two gametangial cells),a nucleus moves from the antheridium into theascogonium, a process referred to as dikary-otization (because it results in a binucleate ordikaryotic cell). In chasmothecia with a singleascus the dikaryotic condition can persist foran extended period of time, whereas in polyas-cal species the nuclei tend to divide soon af-ter dikaryotization. Following dikaryotization,hyphae produced by monokaryotic cells com-prising the base of the ascogonium grow toenvelop it and form the developing peridium.Antheridial cells also may contribute to theperidium. The multinucleate ascogonium di-vides into a number of cells that are dikaryoticor perhaps monokaryotic. Asci develop fromdikaryotic cells. Karyogamy and meiosis occurearly in ascus development. The number of as-cospores per ascus differs according to species,ranging from two to eight (15).

Mature chasmothecia are either persistent(remaining anchored to the substrate on whichthey were produced) or separable from theparental mycelium (15, 17, 58, 84). Persistentchasmothecia are attached by mycelioid ap-pendages and hyphae. Chasmothecia that de-tach from mycelia bear appendages that maybe acicular (lance-shaped with a bulbous base),uncinate (with a recurved or coiled apex), ordichotomously branched at the apex. In sometaxa the same chasmothecium bears more thanone kind of appendage. The appendages canassist in dislodging the chasmothecium fromthe substrate, such as in species of Phyllactinia(146) and Erysiphe elevata (Burrill) U. Braun &S. Takam. (30). Uncinate and dichotomouslybranched appendages can gelatinize to aid at-

tachment (84). In Phyllactinia two kinds of ap-pendages occur (17, 58). Acicular appendagesare borne equatorially; penicillate cells, withdeliquescing processes, are grouped togetheron the dorsal surface. In addition to dislodg-ing chasmothecia, acicular appendages act likevanes to orient the chasmothecium as it trav-els through the air. The deliquescent processesof penicillate cells function like glue in at-taching dispersed chasmothecia to new sub-strates (17, 123, 146). Erysiphe rosae (Golovin &Gamalizk.) U. Braun & S. Takam. also formstwo kinds of appendages: equatorially arrangeddichotomously branched ones and subulate ap-pendages occurring dorsally (17). In Erysypheflexuosa (Peck) U. Braun & S. Takam. and otherspecies formerly classified in Uncinuliella theequatorially arranged appendages are uncinateand subulate appendages are dorsal (59, 138).

Chasmothecial peridial structure variesacross taxa (13, 15, 17). In most species peridiaconsist of several layers of cells. Inner peridialcells are thin-walled and colorless whereas theouter layer cells are thicker-walled, melanized,and closely packed to form a continuous outerlayer (17, 84). Appendages arise from the outercell layer. In Cystotheca peridia consist of twolayers that separate readily, whereas in Brasil-iomyces the peridium is much reduced and nearlytransparent. Surface topography and outlines ofindividual cells in peridia can vary according tospecies. Persistent chasmothecia often are ap-proximately sphaeroidal in shape whereas chas-mothecia that detach from the mycelium areoften convex on the dorsal surface and flattenedor concave on the ventral surface (17, 50, 58,59).

Asci generally are regarded as unituni-cate (e.g., 15) although some authors regardthem as bitunicate (17). Ascus walls vary fromthin to thick in different species, and dis-charge ascospores through the thin-walled apex(17). Shape varies from clavate to saccate orsphaeroidal (13, 15, 17). In multiascal speciesthe asci are grouped together in a hymenium-like layer (17, 64). Paraphyses, as found inpyrenomycetes and discomycetes, or pseudopa-raphyses, as found in loculoascomycetes, are

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lacking (7). Ascospores are single-celled, rang-ing in shape from globose to ovoid or rarely arecurved. Most ascospores are colorless or sub-hyaline, but some are yellowish; they often con-tain vacuoles (17). Ascospores are dischargedfollowing rain events (69, 71, 72, 84), but alsohave been observed to germinate within asci inchasmothecia (125, 143).

Perennation

Perennation is the process of bridging a periodof restricted activity (overwintering or over-summering) (15). Because powdery mildews areobligate parasites, they must be able to sur-vive during seasons when susceptible host tis-sue is unavailable for infection. Knowledge ofhow perennation proceeds in a given powderymildew/host/environment system is useful indevising effective control strategies (84).

There are three primary means of peren-nation in powdery mildews. Chasmothecia arewell-adapted to serve as resistant structures inregions with cold winter temperatures and alsoprovide a means of surviving hot, dry summers(84). Bud perennation occurs when the fungusoverwinters within dormant buds and occurs ondiverse crop and landscape plants (84). Infectedbuds can contain hyphae with haustoria, conid-iophores, and conidia (120). After breaking dor-mancy, infected buds give rise to “flag shoots”that can be covered with profusely sporulatingmycelia, supplying the primary inoculum to ini-tiate the disease cycle (84). Several reports in-dicate that the infected buds are less likely tosurvive low winter temperatures, resulting inreduced powdery mildew populations duringgrowing seasons that follow harsh winters (84).The third kind of perennation involves myceliathat persist through unfavorable conditions, ei-ther the winter on hosts with persistent leaves(54, 84), or when high temperatures suppressgrowth and sporulation (26).

SYSTEMATICS

Biological systematics encompasses efforts todevelop classification systems and to under-

stand phylogenetic relationships. The unbro-ken history of powdery mildew taxonomystarted with Linnaeus, who included a namefor a powdery mildew (Mucor Erysiphe L.) inhis Species Plantarum (99). Yarwood’s (154) re-view of powdery mildew taxonomy includeda list of 74 genus names applied to powderymildews since the eighteenth century. Some ofthose names, such as Aspergillus, Albugo, Scle-rotium, Torula, and Thelebolus, represent earlynotions that grouped powdery mildews withother fungi. Other names, such as Kokkalera,Salmonia, and Erysiphella, referred to powderymildews in the modern sense but were based ontaxonomic concepts that have not persisted.

In 1851 Leveille (96) published his systemof powdery mildew genera based on chasmoth-ecial appendages and ascus number. His ap-proach was adopted by many others, includ-ing T. J. Burrill, the first American authority onErysiphales (21, 42, 53), and later E. S. Salmon,whose world monograph (123) employed a verybroad species concept. The Leveille genus con-cepts and Salmon species concepts dominatedpowdery mildew taxonomy throughout muchof the twentieth century, particularly in NorthAmerica. Perhaps the persistence of this ap-proach in North America can be traced to itscontinued endorsement by leading educators(e.g., 6, 7, 76, 85).

Current taxonomic systems for powderymildews use not only morphological informa-tion, but also host range data and inferred phy-logenetic relationships based on molecular data.Reports began appearing in the 1990s that usedITS and 18S rDNA sequences to infer phyloge-netic relationships of Erysiphales and other ma-jor ascomycete groups (121, 122). Analyses of18S rDNA, ITS1–5.8S-ITS2, and 28S rDNAsequences led Wang et al. (145) to suggest thatthe order Erysiphales can be placed in classLeotiomycetes along with the orders Cyttari-ales, Helotiales, and Rhytismatales. It appearstherefore that the powdery mildews are part ofa lineage sharing an ancient, often parasitic as-sociation with angiosperms.

In recent work, molecular clock mod-els are being used to address problems in

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powdery mildew phylogeny and coevolution.Using a molecular clock based on changesin 18S rDNA, Takamatsu (131) estimated thetime of divergence of Erysiphales from Myx-otrichaceae at about 100 mya. Takamatsu &Matsuda (135) used molecular clock modelsbased on changes in ITS and 28S rDNAsequences to estimate times of divergencewithin the Erysiphales. Their analyses sug-gested that radiation of the major tribes ofErysiphales occurred rather rapidly near theCretaceous/Tertiary boundary. Since that pa-per molecular clock models have been usedto address a variety of evolutionary questions.Such reports have estimated times of diver-gence of cryptic species within a morpholog-ical species (90), among host-specific lineageswithin B. graminis (83), and possible coevolu-tion of clades within the genus Sawadaea andthe host genus Acer (79).

Tribes and Genera

Braun (15) summarized concepts regardingsubfamilies, tribes, and genera based on mor-phological features. He recognized the sub-families Erysiphoideae and Phyllactinioideae,distinguished largely on the basis of whethermycelia were external or internal to the host.Within the subfamily Erysiphoideae were thetribes Erysipheae, with multiascal ascocarps,and Cystotheceae, with ascocarps each produc-ing a single ascus. Tribe Erysipheae was furthersubdivided into subtribes based on ascocarp ap-pendages.

This morphology-based taxonomy has beenextensively revised to incorporate results ofstudies on rDNA sequences (17, 18). Molec-ular evidence suggests that in the Erysiphalesphylogenetic lineages are correlated withanamorphic features such as conidial ontogeny(production of conidia singly or in chains), ap-pressorium morphology, and presence or ab-sence of distinct fibrosin bodies. The chasmoth-ecial appendages that were traditionally usedto distinguish genera are now used to distin-guish species, not genera (17, 18). The fivemajor clades within the order are designated

as the tribes Erysipheae, Golovinomyceteae,Cystotheceae, Phyllactinieae, and Blumerieae(17). Recent research suggests that the phylo-genetic structure within the order may be morecomplex than initially realized. To-anun et al.(140) described a new subgenus of Oidium that,while sharing affinities with Tribe Golovino-myceteae, appeared distinct from any describedtribe. Similarly, the recently described generaParauncinula (132) and Caespitotheca (137), clus-tered near the base of the clade Erysiphales butwere not assignable to any described tribe. Fur-ther research on other gene sequences or onadditional taxa may clarify whether new tribesare warranted.

Currently recognized genera (Table 1) areconsistent with phylogenetic relationships in-ferred on the basis of rDNA sequences (17, 18,132, 137). In many cases, anamorphic charac-ters are of primary taxonomic importance inrecognizing genera, thereby simplifying deter-mination when teleomorph features are un-available (58). Names applied to anamorphicstates, and taxonomically significant characters,are summarized in Table 2.

Tribe Erysipheae includes clades repre-sented by Brasiliomyces, Erysiphe, and Ty-phulochaeta (17). Brasiliomyces species lackanamorphs and produce chasmothecia withperidia consisting of a single layer of cells,unlike the more complex peridia of otherErysiphales (15, 17). Application of the genusname Erysiphe differs from earlier conceptsthat emphasized teleomorph features to the ex-clusion of characteristics of anamorphs (sum-marized in 15). Erysiphe now is applied tospecies forming conidia singly (Pseudoidiumanamorphs) and with lobed appressoria, andincludes not only many species traditionallyplaced in Erysiphe but also those formerly clas-sified in Microsphaera, Uncinula, and Uncin-uliella (17). The genus Erysiphe sometimes issubdivided into sections Erysiphe, Microsphaera,and Uncinula to designate artificial group-ings based on chasmothecial appendages (17).Species forming conidia in chains (Euoidiumanamorphs) were transferred either to Golovino-myces (species with nipple-shaped appressoria)

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Table 1 Selected distinguishing features of genera applied to Erysiphales holomorphsa

Holomorphgenus Mycelium

Specializedhyphae Conidiogenesis

Fibrosinbody

Chasmothecialappendageb

Asci/chasmothecium

ErysipheaeBrasiliomyces External Absent Unreported Unreported M MultipleErysiphe External Absent Single Absent M, U, D, S MultipleTyphulochaeta External Absent Unreported Unreported C MultipleGolovinomyceteaeGolovinomyces External Absent Catenate Absent M MultipleNeoerysiphe External Absent Catenate Absent M MultipleArthrocladiella External Absent Catenate Absent D MultipleCystotheceaeCystotheca External Filiform to falcate Catenate Present M SinglePodosphaera External Absent Catenate Present M, D SingleSawadaea External Absent Catenate Present D SinglePhyllactinieaeLeveillula Internal/external Absent Single Absent M MultiplePhyllactinia Internal/external Absent Single Absent A and P MultiplePleochaeta Internal/external Absent Single Absent U MultipleQueirozia Internal/external Forked Single Absent U MultipleBlumerieaeBlumeria External Falcate Catenate Absent M MultipleUnassigned to tribeOidium subg.Microidium

External Absent Catenate Absent Unreported Unreported

Parauncinula External Absent Unreported Unreported U MultipleCaespitotheca External Simple Catenate Absent U Multiple

aListed according to tribe (17, 98, 137, 140).bAbbreviations: M, myceliod; U, uncinate; D, dichotomously branched; S, subulate; C, clavate; A, acicular; P, penicillate.

or Neoerysiphe (species with lobed appressoria)(17). The genus Typhulochaeta includes speciesproducing chasmothecia with specialized, deli-quescing appendage-like cells that can ruptureto eject mucilaginous material (15).

Tribe Golovinomyceteae includes species ofGolovinomyces, Neoerysiphe, and Arthrocladiella,all forming Euoidium anamorphs (forming coni-dia in chains rather than singly) (17). Golovino-myces and Neoerysiphe include species formerlyreferred to Erysiphe (e.g., 153). These two gen-era are distinguished on the basis of appresso-rial morphology, with species of Golovinomycesforming nipple-shaped appressoria and thoseNeoerysiphe forming lobed appressoria. Arthro-cladiella includes only the single species A.

mougeotii (Lev.) Vassilkov with an anamorph re-sembling those of Golovinomyces but producingchasmothecia with dichotomously branchedappendages (15).

Tribe Cystotheceae includes Erysiphaleswith Euoidium anamorphs, forming chains ofconidia with fibrosin bodies (17). The threegenera include Cystotheca, Podosphaera, andSawadaea (17, 18). Cystotheca and Podosphaeraspecies form chasmothecia containing a sin-gle ascus, whereas in Sawadaea chasmotheciacontain multiple asci (17). Cystotheca is distin-guished by peridia consisting of two separablewall layers, and by falcate aerial hyphae (15, 17).Podosphaera includes species formerly classifiedin Sphaerotheca, and in contrast to Cystotheca the

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Table 2 Selected distinguishing features of genera and subgenera applied to Erysiphales anamorphsa

Appressorium Foot Cell Conidiogenesis Conidia Teleomorph genusTribe ErysipheaeOidium subg.Pseudoidium

Lobed Straight tobent

Single Monomorphic Erysiphe

Tribe GolovinomyceteaeOidium subg.Reticuloidium

Nipple-shaped Straight Catenate Monomorphic Golovinomyces

Oidium subg.Striatoidium

Lobed Straight Catenate Monomorphic Neoerysiphe

Oidium subg.Graciloidium

Nipple-shaped Straight Catenate Monomorphic Arthrocladiella

Tribe CystotheceaeOidium subg. Setoidium Nipple-shaped Straight Catenate Monomorphic,

fibrosin bodiesCystotheca

Oidium subg. Fibroidium Nipple-shaped Straight Catenate Monomorphicfibrosin bodies

Podosphaera

Oidium subg.Octagoidium

Nipple-shaped Straight Catenate Dimorphic fibrosinbodies

Sawadaea

Tribe PhyllactinieaeOidiopsis Lobed to coralloid Straight Single Dimorphic LeveillulaOvulariopsis Lobed Straight Single Dimorphic PhyllactiniaStreptopodium Reduced Twisted Single Dimorphic PleochaetaStreptopodium-like Reduced Straight Single Dimorphic,

pigmentedQueirozia

Tribe BlumerieaeOidium subgenus Oidium Lobed or reduced Base inflated Catenate Monomorphic BlumeriaUnassigned to tribesOidium subg. Microidium Lobed Twisted Catenate Monomorphic UnknownOidium Lobed to coralloid Straight Catenate Monomorphic Caespitotheca

aListed according to tribe (17, 98, 137, 140).

chasmothecia exhibit multilayered peridia (17,18). Sawadaea includes synanamorphic speciesforming both microconidia and macroconidia(17, 58).

Tribe Phyllactinieae includes species withendophytic mycelia (17). Genera are based onchasmothecial and anamorphic features (15,17). Leveillula species produce ascomata withmycelioid appendages and form dimorphicconidia; the first-formed conidium (the pri-mary conidium) on a conidiophore typicallyis lanceolate (with one pointed end) whereaslater ones (secondary conidia) lack a pointedend (15, 86, 87). Phyllactinia species form var-iously shaped rhombiform and/or lanceolate

conidia and unusual chasmothecia with twokinds of appendages (15, 97). Acicular ap-pendages include bulb-shaped bases and lance-shaped shafts. The appendages function bothin dislodging chasmothecia and in orientingthem while airborne (123, 146). Penicillate cellsform on the dorsal surface of chasmotheciaand gelatinize to form a sticky pad that at-taches conidia to new substrates following aerialdispersal (146). Pleochaeta species form chas-mothecia with dichotomously branched ap-pendages, and spirally twisted conidiophorefoot cells (17, 90). Queirozia includes a singlespecies. It forms both external and endophytichyphae, dichotomously branched aerial hyphae,

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uncinate chasmothecial appendages, and a de-matiaceous anamorph with singly formed coni-dia that usually are lemon-shaped (98).

Tribe Blumerieae includes only the genusBlumeria. Occurring only on Poaceae, the sin-gle species B. graminis (DC.) Speer forms anEuoidium anamorph with distinctively shapedconidiophore foot cells, multilobed haustoria,and chasmothecia with mycelioid appendages(15, 17, 128).

Several species remain unassigned to tribes.Oidium phyllanthi J. M. Yen appeared mostclosely related to tribe Golovinomyceteae basedon analyses of 28S and 18S sequence data, butwas not regarded as a member of that tribe(140). Parauncinula was erected for two specieswith uncinate chasmothecial appendages andcurved ascospores; anamorphs are unknownin this genus (132). It occupied a basal po-sition within the Erysiphales but was not as-signed to a tribe (132). Caespitotheca is an-other recently recognized genus, characterizedby apically grouped uncinate chasmothecialappendages and an Euoidium anamorph withcoralloid appressoria (137). Phylogenetic anal-yses of 28S, 5.8S, and 18S rDNA sequences in-dicated that the genus occupies a basal positionwithin the Erysiphales clade (137).

Species

Species concepts in biology remain varied andcontroversial (105) so it is not surprising thatdiffering species concepts have been appliedto powdery mildews. Early eighteenth- andnineteenth-century researchers distinguishedpowdery mildew species largely on the ba-sis of host (154). Salmon’s (123) influentialmonograph was distinguished by a broad,morphology-based species concept and it in-cluded 49 species. He emphasized teleomorphfeatures to the relative neglect of anamorphcharacteristics and host ranges. The twentiethcentury saw an accumulation of information onindividual species, particularly by Asian and Eu-ropean authors (reviewed in 17) and it becameclear that many of Salmon’s species were toobroadly defined (15). By the late twentieth cen-

tury, species were distinguished using anatom-ical features including chasmothecial morphol-ogy (size, shape, appendages, and peridial cells),asci and ascospore morphology, mycelial char-acteristics, and morphology of appressoria, footcells, and conidia, and host range (e.g., 13, 17).About 650 species are recognized using this ap-proach (17).

The taxonomy of powdery mildew speciesis changing as new molecular data are obtainedand analyzed. This work has accelerated as im-proved techniques for extracting DNA and am-plifying sequences of interest have been devel-oped (45, 83, 134). A wide variety of species andtaxonomic problems have been addressed so far.Takamatsu et al. (133) analyzed ITS and 18SrDNA sequences and clarified the taxonomyof several Quercus-infecting powdery mildews.They showed that Erysiphe hypophylla (Nevod.)U. Braun & Cunningt. and E. alphitoides(Griffon & Maubl.) U. Braun & S. Takam. canbe distinguished by conidial size and shape, andthat Erysiphe quercicola S. Takam. & U. Brauncan be distinguished from E. alphitoides by thelength of chasmothecial appendages. Analysesof ITS sequences confirmed that differencesin conidial morphology are sufficient to dis-tinguish species of Leveillula (86, 87). Braunet al. (19) showed that several species of Erysipheoccurring on Carpinus are distinguishable onthe basis of chasmothecial appendage size andnumber, morphology of the coiled appendageapices, and curvature of the conidiophore footcell. Golovinomyces cichoracearum in the broadsense was regarded as several similar species byBraun (15) on the basis of host range and mor-phological features. Analysis of sequence data isresulting in further clarification of that speciescomplex (104, 136). Phyllactinia guttata, an-other widely distributed species reported frommany host families, appears also to be a speciescomplex (15) but published studies on it us-ing molecular data are lacking. Liberato (97)recently showed that anamorphic features dis-tinguished Phyllactinia chorisiae Viegas fromP. guttata, with which it had been consideredconspecific. That report (97) reinforces the ideathat new taxonomic insights can be obtained

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from observations on even commonly encoun-tered powdery mildews. Kiss et al. (90) used ITSand 28S rDNA sequences to distinguish twophylogenetic species of Pleochaeta that could notbe separated morphologically.

Taxonomic categories within species includevarieties, used when morphological differenceswere insufficient to justify recognition of dis-tinct species (15), or formae speciales, applied toreflect differences in host range within a mor-phological species (2, 83). An influential earlypaper was that of Marchal (101), who reportedspecificity at the host genus level for strainsof Blumeria graminis, laying the foundation forthe formae speciales still recognized within thespecies (83). Host range studies can be difficultto perform and interpret. Problems that com-plicate such work are cross-contamination (123)and the possibility of enhanced host susceptibil-ity in greenhouse environments (11, 15, 31, 33).Analysis of molecular data affords an alterna-tive approach to assessing variation within sub-specific taxa and populations, and methodologyfor such work is improving rapidly. Wyand &Brown (150) examined relationships of someformae speciales of B. graminis using β-tubulinand ITS sequences and concluded that thesesequences were not sufficiently variable for usein resolving relationships within that species.More recently, Inuma et al. (83) assessed re-lationships among formae speciales of B. grami-nis using ITS and 28S rDNA, chitin synthasegene and β-tubulin gene sequences and recog-nized nine distinct groups within the species.In a study of strains of Podosphaera tridactyla(Wallr.) de Bary from Asia, Australia, and Eu-rope, Cunnington et al. (32) suggested on thebasis of RFLP analysis of ITS sequences thatthis taxon consist of three distinct clades. Theyconcluded that more research on strains fromadditional geographical locations and hosts, andperhaps using additional gene sequence data, isneeded to resolve fully the taxonomic implica-tions of their findings.

In summary, the trend toward more nar-rowly delimited species continues. Species arebased primarily on anamorph and teleomorphmorphology but molecular data are proving in-

creasingly useful. It seems likely that the num-ber of recognized species will continue to grow.The powdery mildews of many parts of theworld have yet to be studied by taxonomists.Areas identified by Braun et al. (17) that arein particular need of study include large partsof Africa, Asia, and North America. Surpris-ingly, information on North American speciespowdery mildews is both incomplete and basedlargely on obsolete taxonomic systems. A sig-nificant practical problem is that it can be diffi-cult, sometimes impossible, to determine whichspecies has been the subject of a given pub-lished report. The only compilation of fungiin the United States (44) included about 70species of Erysiphales, while research in thePacific Northwest of North America suggeststhat in that region alone there are 150 or morespecies (57). Reconnaissance of botanical gar-dens, arboreta, or even weed-ridden fields regu-larly yields new geographic or host records (38,56).

Determination of Species

The process of determining the species towhich a powdery mildew can be referred issometimes called (incorrectly) identification.To identify something is to establish that it isidentical with something else—a logical impos-sibility when dealing with organisms that aresubject to genotypic and phenotypic variation.In determining a species one works within theframework of a given taxonomic system to ap-ply names to organisms in a manner consistentwith that system. As biology has evolved, and asnew information about powdery mildews hasbecome available, taxonomic systems for pow-dery mildews have changed considerably.

The taxonomic system described by Braunet al. (17) embodies the concepts used by mostcontemporary powdery mildew taxonomists.The species concept on which it is based in-corporates information on host, morphology ofteleomorphs and anamorphs, and geographi-cal range. Useful teleomorph features includesize and shape of chasmothecia; number, size,and morphology of chasmothecial appendages;

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ascus number and shape; and ascospore size,shape, and number per ascus (17). Unfortu-nately, information on anamorphs is lacking forabout 75% of powdery mildew species (17).Despite this limitation, anamorphic powderymildews can be determined to species usingsuch features as host, presence or absence ofspecialized hyphae, morphology of appresso-ria, morphology and size of foot cells, coni-dial size and shape, and presence or absenceof fibrosin bodies (12, 17, 29). Useful compi-lations with drawings or photographs of mor-phological features can be seen in various re-cent works by Braun (15, 16), Braun et al. (17),Shin and La (127), Bolay (13), and Glawe (58).Braun’s (15) world monograph is the most re-cent comprehensive work but many regionaltaxonomic treatments have been publishedsince it appeared (13, 17). There is no NorthAmerican monograph of Erysiphales; conse-quently, Braun’s (15) treatment remains themost comprehensive source of taxonomic in-formation for this continent.

The combination of more complete mor-phological descriptions and gene sequence datahas increased the reliability of species deter-minations. ITS sequences were used to clarifythe taxonomy of Australian anamorphic pow-dery mildews on Fabaceae (31) and Solanaceae(33). ITS sequences and morphological fea-tures were used to show that two species ofErysiphe were associated with powdery mildewoutbreaks of soybean (Glycine max) in east Asia,and that one of them is likely conspecific withthe species attacking soybean in the UnitedStates (139). Using ITS and 28S rDNA se-quence data along with morphological informa-tion resolved long-standing difficulties in dis-tinguishing several Erysiphe species occurringon Quercus spp. (133). A combination of ap-proaches involving light and scanning electronmicroscopy and analysis of ITS sequences dis-tinguished two Oidium species attacking tomato(Lycopersicon esculentum) (89). Another study us-ing morphological and rDNA sequence datadistinguished several previously incompletelyknown species of Erysiphe occurring on Carpi-nus spp. (19).

Because powdery mildew conidia from manyspecies are similar in size and shape, using mor-phological features to determine the speciesrepresented in spore samples frequently hasbeen problematic (43). New techniques for ob-taining gene sequence data from small num-bers of spores are promising to improve greatlythe accuracy of determining species from sporesamples. Matsuda et al. (103) distinguished Oid-ium neolycopersici L. Kiss from Erysiphe trifoliiGrev. by removing single conidia from in-fected tomato leaves and comparing the ITSsequences with archived sequence data. Falacyet al. (43) developed primers specific to Erysiphenecator and used them to amplify DNA fromconidia collected from air samples. They coulddetect five or fewer conidia, and detected air-borne inoculum during periods of ascosporedischarge. The approach appears to offer a cost-effective solution for growers needing near real-time information on inoculum availability to re-duce unnecessary fungicide treatments.

GEOGRAPHICALDISTRIBUTIONS

Amano’s (8) compilation of host and geographi-cal ranges of powdery mildews remains the mostcomprehensive source of such information. Itappears that Erysiphales are most diverse intemperate regions of the Northern Hemisphere(8, 148). However, many regions of the worldremain unexplored for powdery mildews, in-cluding large parts of Africa, North and SouthAmerica, and Asia (17).

Assessing sequence data in combination withmorphological, host, and paleontological in-formation is a powerful approach for study-ing ancient origins and spread of powderymildews. Matsuda & Takamatsu (104) usedITS and 28S rDNA sequence data to investi-gate the ancient relationship between species ofGolovinomyces and hosts in the Asteraceae. Theyfound evidence that host-parasite relationshipsincluded both coevolution with asteraceoushosts and host-jumping to species in otherangiosperm families. Takamatsu et al. (136)subsequently suggested that the Golovinomyces

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clade arose in the Northern Hemisphere afterthe Asteraceae invaded North American fromSouth America. Furthermore, using a molecu-lar clock model, Takamatsu & Matsuda (135)uncovered evidence that at least one clade ofGolovinomyces species may have invaded SouthAmerica from North America following closureof the Isthmus of Panama (estimated at 3.1–2.8 mya).

Geographical ranges of some species appearto be increasing. Kreisel & Scholler (92) re-viewed records of plant pathogenic fungi in-troduced into Germany and nearby countriessince 1750 and included 16 powdery mildewspecies in the resulting list. Five species ap-peared to have originated in North America,five in Asia, one in another part of Europe, andthe others were of uncertain origin. Five specieswere recorded for the first time in Germanyin the nineteenth century, five more between1900 and 1950, and the other six species from1956 to 1989. They believed the greatest pe-riod of introduction of powdery mildews intoGermany began about 1900. There are severalwell-known examples of important pathogensof economic crops spreading to new regionsfrom the mid-nineteenth to the early twentiethcenturies. Erysiphe necator, originally describedfrom North America, was found in Europe in1845; by 1852 it occurred throughout Europeand the Mediterranean region (148). Given thelong history of viticulture, and great attentionpaid to wine grapes, it is extremely unlikelythat E. necator existed in Europe much ear-lier than when it was reported there. Similarly,Podosphaera mors-uvae (Schwein.) U. Braun &S. Takam. was described in North Americain 1834 and by the early twentieth centurywas widespread in western Europe and Japan(148). A more recent example of an importantpathogen occurring in a new region is affordedby the hop powdery mildew fungus Podosphaerahumuli (Wallr.) U. Braun & S. Takam. It was un-known in eastern Washington state, the majorNorth American production region of hops, un-til the 1990s (142). It seems extremely unlikelythat such a conspicuous, damaging pathogen

was unnoticed on such a valuable crop, lead-ing one to conclude that it arrived in the regiononly shortly before its discovery.

The years leading up to and including thetwenty-first century have seen numerous firstreports of powdery mildews from regions out-side their previously known distributions. Bolayet al. (14) suggested that recent climatic changesin Europe may favor spread of alien powderymildew species. Frequently, new records arepublished in succession by independently work-ing researchers. For example, Erysiphe flexuosais thought native to Aesculus spp. in NorthAmerica (15). The fungus was found in Europein 2000 and soon its presence was documentedin Croatia, France, Germany, Poland, Slovakia,Switzerland, the United Kingdom (157),Hungary (5, 91), Slovenia (107), and Lithuania(68). In North America, E. flexuosa first wasreported in the Pacific Northwest in 2006 andprobably is not native to the region because itshosts were introduced (59). Erysiphe palczewskii( Jacz.) U. Braun & S. Takam. is another specieswith rapidly expanding geographical distribu-tion. Occurring on Caragana species, it was firstdescribed in 1927 from the Russian Far East(15). It was reported in Belarus in 1975, andnow is widespread in Europe (77). In Finlandit seems to have displaced the native speciesErysiphe trifolii from this host (81). NorthAmerican reports began in 2003 (110), and itis now known to occur as far north as centralAlaska (62) and as far east as Minnesota (63).

Erysiphe symphoricarpi (Howe) U. Braun &S. Takam., thought native to North America,first was reported in Europe in the 1980s butthe teleomorph was unknown there until 2002(88). Bolay et al. (14) noted that Erysiphe rus-sellii (Clinton) U. Braun & S. Takam. oc-curred in Europe since the nineteenth centurybut chasmothecia were reported for the firsttime in the late twentieth century. Powderymildews on Rhododendron species were observedin Europe in the early 1980s but teleomorphswere not reported until 2000 (82). There aremany reports of newly recorded exotic speciesfor which teleomorphs have not yet been found.

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An anamorphic fungus referable to Erysiphedeutziae (Bunkina) U. Braun & S. Takam.is increasing its geographical distribution inEurope, having previously occurred widely inthe Russian Far East and Japan (14). Erysiphecatalpae Simonyan and E. howeana U. Braun alsohave been known in Europe for many years inonly the anamorphic states (14). Such reportsmight involve heterothallic species where for atime only one mating type is present, or perhapsit takes time for new biotypes, well-adapted tonew environmental conditions, to emerge. Atpresent a satisfactory explanation for this phe-nomenon is not available.

Powdery mildew species can coinfect thesame host plant, increasing the likelihood thatnewly arrived species can be overlooked. Leveil-lula taurica and Golovinomyces orontii (Castagne)V.P. Heluta were found coinfecting leaves ofpotato in central Washington (61). The lat-ter fungus, originally reported as Erysiphe ci-choracearum, occurred on potato in that statesince the 1940s (106). Leveillula taurica occurredin the region since the 1980s or earlier (47)and may have been overlooked on potato foryears because its presence was masked by G.orontii (61). Cook et al. (30) reported that Neo-erysiphe galeopsidis (DC.) U. Braun and Erysipheelevata coinfected leaves of Catalpa species inEngland; N. galeopsidis appeared in June butwas soon displaced by E. elevata. Huhtinen

et al. (81) reported that when Erysiphe pal-czewskii became established on Caragana ar-borescens in Finland, the native Erysiphe trifoliisoon could not be found on this host, apparentlyhaving been displaced by the newly arrivedspecies. Species endemic to a region also cancoinfect hosts. For example, Phyllactinia gut-tata and Erysiphe penicillata (Wallr.) Link werereported to coinfect leaves of Alnus species inOntario (115).

Recent evidence suggests that air pollutionand climate change may be affecting the dis-tribution and activities of powdery mildews.Dynowska (40) studied the occurrence ofErysiphales in cities in northern Poland from1981 to 1991 and reported that although morespecies were found in urban areas, severity ofdiseases caused by them were higher in sub-urban areas. A likely cause was thought to bethe effects of air pollutants on powdery mildews(40). Cook et al. (30) suggested that lengthen-ing growing seasons in the United Kingdomfavored maturation of greater numbers of chas-mothecia of Erysiphe elevata, contributing to itsincreasing prevalence and ability to displaceNeoerysiphe galeopsidis from coinfected leaves.Such findings may offer the first indication thatextended growing seasons may produce signif-icant changes in the life histories of powderymildews and epidemiology of the diseases theycause.

SUMMARY POINTS

1. The diversity of powdery mildews in many parts of the world is significantly underes-timated. The number of species reported for North America is likely only a fraction ofthose occurring there. A similar situation exists in South America, Africa, and parts ofAsia.

2. Although the anamorphs of most powdery mildew species have yet to be character-ized, anamorphic features and host information can be used to determine most powderymildew species.

3. Research on molecular phylogeny is revolutionizing powdery mildew systematics.Erysiphales are now regarded as Leotiomycetes rather than Pyrenomycetes or Plec-tomycetes. Tribes within the order designate the major clades of Erysiphales, shown tobe more closely correlated with features of anamorphs than teleomorphs. Genus conceptsalso were modified to reflect the newly recognized phylogenic relationships.

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4. Molecular data sets have proven useful in reassessing species and clarifying the taxonomicsignificance of morphological and host data. Only a small percentage of the describedspecies have been reassessed using these approaches.

5. New PCR-based methods have been used to determine species on the basis of one or afew spores. These approaches have the potential to facilitate the use of spore-trappingto assess inoculum levels for determining timing of fungicide applications.

6. Geographical distributions of some species appear to be expanding rapidly. Climatechange has been suggested as a possible explanation. Longer growing seasons also mayresult in production of greater numbers of chasmothecia and higher powdery mildewpopulations in succeeding growing seasons. In at least one case, an exotic species haslargely displaced an endemic one.

FUTURE ISSUES

1. Communication about powdery mildews in many regions, especially North America,is hampered by incomplete descriptions of species and reliance on obsolete taxonomicsystems. There is an urgent need for what is sometimes called alpha taxonomic work: thecollection, characterization, and description of taxa. The combined use of morphological,molecular, and host data will greatly increase the impact of such work.

2. The complete life cycles of most species are unknown. Obtaining such information willbe necessary to clarify species concepts and can provide information about disease cyclesthat can be used to develop control strategies.

3. Very little information is available on the ultrastructure of conidiogenesis in powderymildews. This is in contrast to the situation for most groups of fungi where such infor-mation is available and considered basic to classification systems. Characterizing coni-diogenesis at the ultrastructural level is expected to yield important insights into theevolution of conidial states in the order.

4. PCR-based procedures for detecting powdery mildews have great potential to improvecapabilities in disease forecasting and management. Further work is needed to developthem into practical, cost-effective systems to support management decisions.

5. It appears that longer growing seasons may result in significant changes in the distribu-tions of powdery mildews and in their effects on host species. The superficial growthhabit of many species, and the long history of records in some parts of the world, maymake powdery mildews unusually well-suited models for studying the effects of climatechange on plant diseases.

DISCLOSURE STATEMENT

The author is not aware of any biases that might be perceived as affecting the objectivity of thisreview.

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ACKNOWLEDGMENTS

PPNS No. 0474, Department of Plant Pathology, College of Agricultural, Human, and NaturalResource Sciences, Agricultural Research Center, Project No. WNP00313, Washington StateUniversity, Pullman, WA 99164-6430. The author thanks Drs. Joe Ammirati, Frank Dugan,Ginger Harstad Glawe, Gary Grove, and Jack Rogers for reviewing the manuscript.

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108. Mims CW, Liljebjelke KA, Richardson EA. 1995. Surface morphology, wall structure, andinitial adhesion of conidia of the powdery mildew Uncinuliella australiana. Phytopathology85:352–58

109. Moriura N, Matsuda Y, Oichi W, Nakashima S, Hirai T, et al. 2006. Consecutive monitoringof lifelong production of conidia by individual conidiophores of Blumeria graminis f. sp. hordeion barley leaves by digital microscopic techniques with electrostatic micromanipulation.Mycol. Res. 110:18–27

110. Nischwitz C, Newcombe G. 2003. First report of powdery mildew (Microsphaera palczewskii )on Siberian pea tree (Caragana arborescens) in North America. Plant Dis. 87:451

111. Oichi W, Matsuda Y, Sameshima T, Nonomura T, Kakutani K, et al. 2004. Consecutivemonitoring for conidiogenesis by Oidium neolycopersici on tomato leaves with a high-fidelitydigital microscope. J. Gen. Plant Pathol. 70:318–21

112. Oichi W, Matsuda Y, Nonomura T, Toyoda H, Xu L, et al. 2006. Formation of conidialpseudochains by tomato powdery mildew Oidium neolycopersici. Plant Dis. 90:915–19

113. Pady SM. 1972. Spore release in powdery mildews. Phytopathology 62:1099–100114. Pady SM, Kramer CL, Clary R. 1969. Sporulation in some species of Erysiphe. Phytopathology

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128. Speer EO. 1973. Untersuchungen zur Morphologie und Systematik der Erysiphaceen I. DieGattung Blumeria Golovin und ihre Typusart Erysiphe graminis DC. Sydowia Ann. Mycol. Ser.2, 27:1–6

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129. Spencer DM, ed. 1978. The Powdery Mildews. London: Academic. 565 pp.130. Sutton BB, Jones AL. 1979. Analysis of factors affecting dispersal of Podosphaera leucotricha

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153. Yarwood CE. 1973. Pyrenomycetes: Erysiphales. In The Fungi. An Advanced Treatise. VolumeIVA. A Taxonomic Review WITH Keys: Ascomycetes and Fungi Imperfecti, ed. GC Ainsworth,FK Sparrow, AS Sussman, pp. 71–86. New York: Academic

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RELATED INTERNET RESOURCES

Index Fungorum: http://www.indexfungorum.org/Names/Names.aspOnline database that includes names and synonyms for all fungi, including powdery mildews.LIAS—A Global Information System for Lichenized and Non-Lichenized Ascomycetes: http://

www.lias.net/An online database with information on a wide range of fungi, it is an excellent source of infor-

mation on powdery mildews with extensive descriptions of taxa.New Disease Reports: http://www.bspp.org.uk/ndr/An online publication that specializes in rapid publication of new plant diseases. Published by the

British Society for Plant Pathology, it includes color photographs.Pacific Northwest Fungi: http://pnwfungi.org/The venue for publications on powdery mildews resulting from a sustained effort to catalog the

fungi of the Pacific Northwest region of North America.Plant Health Progress: http://www.plantmanagementnetwork.org/php/default.aspAn online publication of the American Phytopathological Society, this journal has published dozens

of new disease reports and articles, illustrated with color photographs, since it was foundedseveral years ago.

US National Fungus Collection Databases: http://nt.ars-grin.gov/fungaldatabases/fungushost/fungushost.cfm

Excellent collection of databases on fungi, their host associations, and the literature of plantpathology.

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Annual Review ofPhytopathology

Volume 46, 2008Contents

The Phenotypic Expression of a Genotype: Bringing Muddy Bootsand Micropipettes TogetherRoger Hull � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

The Origin of Ceratocystis fagacearum, the Oak Wilt FungusJennifer Juzwik, Thomas C. Harrington, William L. MacDonald,

and David N. Appel � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �13

The Powdery Mildews: A Review of The World’s Most Familiar(Yet Poorly Known) Plant PathogensDean A. Glawe � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �27

Plants as a Habitat for Beneficial and/or Human Pathogenic BacteriaHeather L. L. Tyler and Eric W. Triplett � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �53

The Origins of Plant Pathogens in Agro-EcosystemsEva H. Stukenbrock and Bruce A. McDonald � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �75

Role of Stomata in Plant Innate Immunity and Foliar Bacterial DiseasesMaeli Melotto, William Underwood, and Sheng-Yang He � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 101

Models of Fungicide Resistance DynamicsFrank van den Bosch and Christopher A. Gilligan � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 123

Siderophores in Fungal Physiology and VirulenceHubertus Haas, Martin Eisendle, and Gillian Turgeon � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 149

Breaking the Barriers: Microbial Effector Molecules SubvertPlant ImmunityVera Gohre and Silke Robatzek � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 189

Yeast as a Model Host to Explore Plant Virus-Host InteractionsPeter D. Nagy � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 217

Living in Two Worlds: The Plant and Insect Lifestylesof Xylella fastidiosaSubhadeep Chatterjee, Rodrigo P.P. Almeida, and Steven Lindow � � � � � � � � � � � � � � � � � � � � � � � � 243

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AR351-FM ARI 23 June 2008 14:24

Identification and Rational Design of Novel Antimicrobial Peptidesfor Plant ProtectionJose F. Marcos, Alberto Muñoz, Enrique Pérez-Payá, Santosh Misra,

and Belén López-García � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 273

Direct and Indirect Roles of Viral Suppressors of RNA Silencingin PathogenesisJuan A. Díaz-Pendón and Shou-Wei Ding � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 303

Insect Vector Interactions with Persistently Transmitted VirusesSaskia A. Hogenhout, El-Desouky Ammar, Anna E. Whitfield,

and Margaret G. Redinbaugh � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 327

Plant Viruses as Biotemplates for Materials and TheirUse in NanotechnologyMark Young, Debbie Willits, Masaki Uchida, and Trevor Douglas � � � � � � � � � � � � � � � � � � � � � � 361

Epidemiological Models for Invasion and Persistence of PathogensChristopher A. Gilligan and Frank van den Bosch � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 385

Errata

An online log of corrections to Annual Review of Phytopathology articles may be found athttp://phyto.annualreviews.org/

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