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Dean A. Glawe
Department of Plant Pathology, Washington State University and College of Forest
Resources, University of Washington, Seattle 98195; email: [email protected]

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

The Annual Review of Phytopathology is online at climate change, Erysiphales, fungal taxonomy, life histories, pathogen
phyto.annualreviews.org
detection, phylogeny
This article’s doi:
10.1146/annurev.phyto.46.081407.104740 Abstract
Copyright  c 2008 by Annual Reviews. The past decade has seen fundamental changes in our understanding
All rights reserved
of powdery mildews (Erysiphales). Research on molecular phylogeny
0066-4286/08/0908/0027$20.00 demonstrated that Erysiphales are Leotiomycetes (inoperculate dis-
comycetes) 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 ma-
jor 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 re-
construct 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.

27
 INTRODUCTION mental morphology, cytology, and molecular
biology. Because they behave as obligate plant
Powdery mildews (Ascomycotina, Erysiphales)
pathogens, researchers have not had the advan-
are some of the world’s most frequently en-
tage of routinely cultivating these fungi on ar-
countered plant pathogenic fungi. They are of-
tificial media, although many powdery mildews
ten conspicuous owing to the profuse produc-
have been grown on detached leaves of their
tion of conidia that give them their common
hosts.
name (Figure 1). They infect leaves, stems,
Although one might expect there are few
Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org

flowers, and fruits of nearly 10,000 species

unanswered questions about such common,
of angiosperms (17). Among the economically
easy-to-recognize plant pathogens, this is not
important plants they infect are grapes, tree
the case. In fact, recent research has shown that
by Chiang Mai University on 12/07/10. For personal use only.

fruits, small grains, hops, and many ornamen-

powdery mildews are more diverse and their
tals. Immense expenditures are made annually
biology more complex than generally realized.
for fungicides and resistant varieties to control
Many commonly accepted beliefs about pow-
powdery mildews. Throughout the 250 years
dery mildews, such as that sexual states are
since Linnaeus first gave a scientific name to
necessary to determine species, and host and
a powdery mildew, they have figured promi-
geographical ranges are well understood, are
nently in the history of plant pathology. They
erroneous. This article provides an overview
have been used to study key aspects of plant
of the biology and systematics of powdery
disease etiology, epidemiology, and control.
mildews, focusing primarily on research of
Powdery mildews are also models for basic re-
the past decade relevant to plant pathologists.
search on host parasite interactions, develop-
Earlier work has been reviewed extensively (10,
15–17, 129, 152–154).
a b
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 distinctive
spore states, and they were among the first
fungi for which pleomorphism was described
c (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 be
lacking. Anamorphs are unknown in species of
Brasiliomyces, Typhulochaeta, and Parauncinula,
where all known reproduction involves chas-
mothecia (ascomata) (17, 132). Conversely, no
teleomorph has been found in the subgenus
Microidium of Oidium (140). In some species
Figure 1 teleomorphs are unknown in regions with mild
Representative symptoms and signs of powdery mildews. (a) Erysiphe alphitoides climates. For example, Erysiphe berberidis DC.
on Quercus garryana. (b) Podosphaera fuliginea on Kalanchoe blossfieldiana. produces chasmothecia in Europe (15) but they
(c) Erysiphe necator on Vitis vinifera. are unknown in western Washington (54). Life

28 Glawe
 cycle events in Erysiphales are synchronized
with host life cycles, and effective control strate-
a b c
gies depend on understanding how a given pow-
dery 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.
Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org

Infection
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Blumeria graminis (DC.) Speer has emerged e

d f
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 re-
search on Arabidopsis and the several powdery
mildews that infect it (144). The adoption of
additional 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 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 Figure 2
powdery mildews infect their hosts is based on Representative morphological features of Erysiphales. (a) Indistinct
this species. appressorium (Podosphaera epilobii ). (b) Lobed appressorium (Erysiphe knautiae).
(c) Nipple-shaped appressorium (Golovinomyces cynoglossi ).
An infection is initiated when an ascospore
(d ) Conidiophore with chain of conidia. (Podosphaera fusca). (e) Conidiophore
or conidium lands on a susceptible host, ger- forming a single conidium (Erysiphe knautiae). ( f ) Conidiophores forming
minates, and forms a germ tube that elon- single conidia, emerging from host stoma (Leveillula taurica).
gates to form a hypha with appressoria, penetra-
tion pegs, and haustoria. Appressoria are short, Spore germination and infection occurs
lateral hyphal outgrowths or swellings that rapidly. Within 60 seconds of a B. graminis
produce penetration pegs to infect host cells. conidium landing on a host, liquid extracellu-
Penetration pegs and haustoria, as well as the lar material with esterase and cutinase activity
physiological processes associated with them, has been observed fastening the spore to the
have been reviewed extensively (22, 67). Pen- host (25, 149). A similar process was observed
etration pegs are narrow protrusions produced in Erysiphe australiana (McAlpine) U. Braun &
from appressoria that penetrate the walls of host S. Takam. (108). Within 30–90 min, immuno-
cells by means of turgor pressure and enzymatic labeled antigen from conidia of B. graminis was
activity. The haustorium is an enlarged exten- detected within the plant cell wall and cyto-
sion of the penetration peg, formed within the plasm (156). The primary germ tube gener-
host cell. It is intimately involved in develop- ally is initiated in 30–60 min (93) and produces
ing and maintaining the parasitic relationship a minute “cuticular peg” (41) that penetrates
with the host, and causing the plant to shunt the plant cuticle but not the cell wall beneath
resources to the fungus (48). it. The cuticular peg and extracellular material

www.annualreviews.org • Powdery Mildews 29

 a b c
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d e f

g h i

Figure 3
Representative 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 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 host wall, the penetration peg extends into
the spore to the host (156). Upon sensing the the host cell, invaginating the cytoplasm, and
presence of the host, the primary germ tube enlarging to form the haustorium. The hausto-
induces production of the appressorial germ rium is surrounded by extrahaustorial matrix,
tube. The appressorium forms about 10 h after a noncytoplasmic, gel-like material that may
infection (156). In about two more hours the help protect the fungus from host responses
appressorium produces a penetration peg that (67). The haustorium, extrahaustorial matrix,
penetrates the cell wall and the dome-shaped and host cell are the sites of molecular signal-
deposit of host cell wall material (termed the ing events. Host responses and nutrient transfer
papilla) formed in response to the fungus (155, determine whether a successful parasitic rela-
156). If the fungus is successful in breaching tionship develops and is maintained (67, 156).

30 Glawe
 Fotopoulos et al. (48) noted that physiological of Martin & Gay (102) who described conidial
changes within the host extend beyond the in- development in Erysiphe pisi DC. Their pho-
fected cell to facilitate transfer of nutrients from tographs illustrated cytoplasmic continuity ex-
the plant to the fungus. Powdery mildews can tending through the complete series of cells
retard senescence of infected tissues, resulting from the haustoria to developing conidia, facili-
in the symptom known as “green islands” (27). tating transport of metabolites until the mature
conidium detached from the conidiophore.
Powdery mildew conidia are single cells
Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org

Asexual Reproduction (17). Except for one species with dematiaceous

After infection of the host, hyphae elongate and (dark-pigmented) conidia, they are colorless
branch repeatedly, forming circular colonies. (98). Conidia range in shape from nearly ovoid
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Young hyphae are transparent or whitish but to cylindrical or lanceolate (13, 15). In most
frequently turn grayish, reddish, or brownish species conidia are monomorphic. Dimorphic
during maturation (17). Hyphae of most pow- conidia are formed in species of Leveillula and
dery mildews grow superficially on their host Pleochaeta (15, 17) and Phyllactinia (97). Species
but species in the tribe Phyllactinieae can grow of Sawadaea form synanamorphs, with macro-
inside host tissue (17). Some species form differ- conidia and microconidia produced from coni-
entiated, secondary hyphae (17). Such hyphae diophores that also differ dramatically in size
are filiform to falcate in Cystotheca (17), forked (15, 58). Conidia are uninucleate and contain
in Queirozia (98), falcate in Blumeria (17), and vacuoles and large amounts of water, possi-
simple in Caespitotheca (137). Somatic (assim- bly contributing to their ability to germinate
ilative) hyphae eventually give rise to repro- in the absence of free water (126, 152, 154).
ductive structures (conidiophores and/or chas- Conidia in the tribe Cystotheceae (which in-
mothecia). cludes the genera Cystotheca, Podosphaera, and
Conidial production typically begins within Sawadaea) contain fibrosin bodies (17). These
several days of infecting the host. Repre- are refractive, variously shaped bodies that form
sentative anamorph features are shown in as rods, cones, tori, or curved or straight plates.
Figure 3. Conidiophores arise from vegetative Foex (46) believed they consisted of callose, and
hyphae and are oriented more or less perpen- Homma (80) reported fibrosin bodies to con-
dicularly to the surface of the host. The first tain B IV carbohydrate and nitrogen. Braun
complete cell of the conidiophore is termed et al. (17) noted that they still are poorly un-
the foot cell and it subtends one or more derstood.
additional cells, including the generative cell Powdery mildew conidia display various
involved in forming conidia. Conidial produc- kinds of surface ornamentation and a liquid
tion is basauxic—that is, conidia form succes- coating when viewed with scanning electron
sively with each new conidium forming at the microscopy (e.g., 39, 65, 73, 82, 108, 117). Some
base of the previous conidium (109, 111, 112). of the features also can be discerned using high
Species form conidia that mature singly (the magnifications with brightfield or differential
Pseudoidium group), or in a graduated series interference contrast microscopy (55, 60). The
(generally referred to as a chain of conidia) surface features are thought to be useful tax-
with the oldest conidium at the top (the Euoid- onomically (29). The appearance of conidial
ium group). Conidiophores generally are sim- surfaces varies according to whether they are
ple (unbranched), although branched ones are viewed while fresh and turgid or dry and col-
often illustrated for Leveillula taurica (Lév.) G. lapsed (17).
Arnaud (e.g., 13, 17). Proposed mechanisms for the release of
There is little published information on conidia from conidiophores include mechanical
the ultrastructure of conidiogenesis in powdery force (117), convection currents (49), wind (70,
mildews. A noteworthy exception is the study 75, 111, 130), electrostatic charges (1, 95), and

www.annualreviews.org • Powdery Mildews 31

 leaf shaking or fluttering (9). High relative hu- until after secession. Patterns of conidial germi-
midity appears negatively correlated with dis- nation are taxonomically useful (15, 17). Dis-
persal of conidia (70, 74, 130). Conidial pro- tinctions that have been noted include differ-
duction and release frequently follows a diurnal ences in location of germ tubes, time required
pattern, with most spores becoming airborne for germ tube production, and whether or not
in the period extending from mid-morning to appressoria form on germ tubes (15, 17).
early afternoon (24, 28, 70, 102, 113, 114, 125,
130, 151). Profusely sporulating colonies may
Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org

become covered with mats of clumped spores Sexual Reproduction

that are less prone to dissemination (75). The term chasmothecium was suggested by
Conidial dispersal appears to occur mostly Braun et al. (17) to distinguish powdery mildew
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over short distances. Peries (116) found that ascomata from those of other ascomycetes. Ear-
90% of conidia formed by Podosphaera macularis lier authors either termed them cleistothecia
(Wallr.) U. Braun & S. Takam. traveled less than because they lack ostioles (e.g., 3, 52, 147),
2 m from host plants. On the other hand, coni- or perithecia because multiascal species form a
dia of Golovinomyces cichoracearum (DC.) V.P. hymenium-like layer (7, 64). During ascospore
Heluta were reported to be dispersed 200 km discharge chasmothecia develop a more-or-less
in California (125), and airborne conidia of B. vertical or circumscissile split (or “chasm”) in
graminis traveled from the British Isles to in- the peridium. The rupture apparently results
fect plants in Denmark nearly 700 km away from increased turgor pressure that develops
(78). Examples of rapid dispersal over long dis- when free water is absorbed by chasmothecia
tances include Erysiphe betae (Vaňha) Weltzien (e.g., 51, 123, 124, 143). In Phyllactinia guttata
on beet crops in North America and Europe (Wallr.) Lév. the peridium splits equatorially to
(37); expansion of the range of Erysiphe neca- expose asci (123, 146), allowing the chasmoth-
tor Schwein. from the British Isles in 1845 to ecium to open in a clamshell-like fashion to
the rest of western and central Europe and expose asci for spore discharge.
the Mediterranean region by 1852 (148); and Chasmothecia are light-colored when first
expansion of P. macularis on hop from east- discernable, becoming yellowish or amber-
ern Washington, where it was first observed colored, and finally dark brown to black when
in 1996, to Idaho and Oregon by 1998 (100). mature (e.g., 59). They are not produced in
Effective dispersal over long distances may be stromata but can be closely associated with thick
favored by production of enormous numbers wefts of hyphae (e.g., 60). Chasmothecia (exclu-
of conidia when a high density of sporulat- sive of appendages) range from 50 μm to about
ing colonies occurs on a large host population. 400 μm; most ascomata are 100–200 μm in di-
Schnathorst (125) calculated that when lettuce ameter and the size range of individual species
plants supported 67 colonies per leaf, approxi- tends to be consistent (15). Work on B. grami-
mately 80 million conidia of G. cichoracearum nis indicated that while nutrients supplied by
were disseminated per hectare every 24 h. the host are critical in early stages of develop-
Hermansen et al. (78) reported that 5–10 h ment, sufficient reserves eventually are stored
of favorable conditions for B. graminis conidial within the mycelium that chasmothecial devel-
release in Britain produced spore showers re- opment proceeds without depending on a con-
sulting in 1–2 million infections per hectare in tinued supply of host metabolites (66). The ma-
Denmark. ture ascoma is self-contained and delimited by
Conidia are dispersed either singly or in the peridium, which consists of closely packed
short chains (125), germinate readily and, un- melanized cells (15, 17).
like those of other fungi, do not require free Major features of sexual reproduction were
water for germination (23, 67, 84, 126, 152). summarized by Braun et al. (17), with partic-
Conidia generally appear unable to germinate ular attention to work by Dörfelt et al. (36)

32 Glawe
 and Dörfelt & Ali (35), whose work helped tachment (84). In Phyllactinia two kinds of ap-
resolve longstanding questions and inconsis- pendages occur (17, 58). Acicular appendages
tencies. The following description is based are borne equatorially; penicillate cells, with
largely on Braun et al. (17). Species may be ho- deliquescing processes, are grouped together
mothallic or heterothallic. Sexual reproduction on the dorsal surface. In addition to dislodg-
in powdery mildews is initiated by production ing chasmothecia, acicular appendages act like
of gametangia (also termed gamocysts). Male vanes to orient the chasmothecium as it trav-
gametangia usually are termed antheridia or an- els through the air. The deliquescent processes
Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org

drogamocysts, and female gametangia termed of penicillate cells function like glue in at-
ascogonia or gynogamocysts (17). Following taching dispersed chasmothecia to new sub-
plasmogamy (establishment of a cytoplasmic strates (17, 123, 146). Erysiphe rosae (Golovin &
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connection between the two gametangial cells), Gamalizk.) U. Braun & S. Takam. also forms
a nucleus moves from the antheridium into the two kinds of appendages: equatorially arranged
ascogonium, a process referred to as dikary- dichotomously branched ones and subulate ap-
otization (because it results in a binucleate or pendages occurring dorsally (17). In Erysyphe
dikaryotic cell). In chasmothecia with a single flexuosa (Peck) U. Braun & S. Takam. and other
ascus the dikaryotic condition can persist for species formerly classified in Uncinuliella the
an extended period of time, whereas in polyas- equatorially arranged appendages are uncinate
cal species the nuclei tend to divide soon af- and subulate appendages are dorsal (59, 138).
ter dikaryotization. Following dikaryotization, Chasmothecial peridial structure varies
hyphae produced by monokaryotic cells com- across taxa (13, 15, 17). In most species peridia
prising the base of the ascogonium grow to consist of several layers of cells. Inner peridial
envelop it and form the developing peridium. cells are thin-walled and colorless whereas the
Antheridial cells also may contribute to the outer layer cells are thicker-walled, melanized,
peridium. The multinucleate ascogonium di- and closely packed to form a continuous outer
vides into a number of cells that are dikaryotic layer (17, 84). Appendages arise from the outer
or perhaps monokaryotic. Asci develop from cell layer. In Cystotheca peridia consist of two
dikaryotic cells. Karyogamy and meiosis occur layers that separate readily, whereas in Brasil-
early in ascus development. The number of as- iomyces the peridium is much reduced and nearly
cospores per ascus differs according to species, transparent. Surface topography and outlines of
ranging from two to eight (15). individual cells in peridia can vary according to
Mature chasmothecia are either persistent species. Persistent chasmothecia often are ap-
(remaining anchored to the substrate on which proximately sphaeroidal in shape whereas chas-
they were produced) or separable from the mothecia that detach from the mycelium are
parental mycelium (15, 17, 58, 84). Persistent often convex on the dorsal surface and flattened
chasmothecia are attached by mycelioid ap- or concave on the ventral surface (17, 50, 58,
pendages and hyphae. Chasmothecia that de- 59).
tach from mycelia bear appendages that may Asci generally are regarded as unituni-
be acicular (lance-shaped with a bulbous base), cate (e.g., 15) although some authors regard
uncinate (with a recurved or coiled apex), or them as bitunicate (17). Ascus walls vary from
dichotomously branched at the apex. In some thin to thick in different species, and dis-
taxa the same chasmothecium bears more than charge ascospores through the thin-walled apex
one kind of appendage. The appendages can (17). Shape varies from clavate to saccate or
assist in dislodging the chasmothecium from sphaeroidal (13, 15, 17). In multiascal species
the substrate, such as in species of Phyllactinia the asci are grouped together in a hymenium-
(146) and Erysiphe elevata (Burrill) U. Braun & like layer (17, 64). Paraphyses, as found in
S. Takam. (30). Uncinate and dichotomously pyrenomycetes and discomycetes, or pseudopa-
branched appendages can gelatinize to aid at- raphyses, as found in loculoascomycetes, are

www.annualreviews.org • Powdery Mildews 33

 lacking (7). Ascospores are single-celled, rang- stand phylogenetic relationships. The unbro-
ing in shape from globose to ovoid or rarely are ken history of powdery mildew taxonomy
curved. Most ascospores are colorless or sub- started with Linnaeus, who included a name
hyaline, but some are yellowish; they often con- for a powdery mildew (Mucor Erysiphe L.) in
tain vacuoles (17). Ascospores are discharged his Species Plantarum (99). Yarwood’s (154) re-
following rain events (69, 71, 72, 84), but also view of powdery mildew taxonomy included
have been observed to germinate within asci in a list of 74 genus names applied to powdery
chasmothecia (125, 143). mildews since the eighteenth century. Some of
Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org

those names, such as Aspergillus, Albugo, Scle-

rotium, Torula, and Thelebolus, represent early
Perennation notions that grouped powdery mildews with
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Perennation is the process of bridging a period other fungi. Other names, such as Kokkalera,
of restricted activity (overwintering or over- Salmonia, and Erysiphella, referred to powdery
summering) (15). Because powdery mildews are mildews in the modern sense but were based on
obligate parasites, they must be able to sur- taxonomic concepts that have not persisted.
vive during seasons when susceptible host tis- In 1851 Léveillé (96) published his system
sue is unavailable for infection. Knowledge of of powdery mildew genera based on chasmoth-
how perennation proceeds in a given powdery ecial appendages and ascus number. His ap-
mildew/host/environment system is useful in proach was adopted by many others, includ-
devising effective control strategies (84). ing T. J. Burrill, the first American authority on
There are three primary means of peren- Erysiphales (21, 42, 53), and later E. S. Salmon,
nation in powdery mildews. Chasmothecia are whose world monograph (123) employed a very
well-adapted to serve as resistant structures in broad species concept. The Léveillé genus con-
regions with cold winter temperatures and also cepts and Salmon species concepts dominated
provide a means of surviving hot, dry summers powdery mildew taxonomy throughout much
(84). Bud perennation occurs when the fungus of the twentieth century, particularly in North
overwinters within dormant buds and occurs on America. Perhaps the persistence of this ap-
diverse crop and landscape plants (84). Infected proach in North America can be traced to its
buds can contain hyphae with haustoria, conid- continued endorsement by leading educators
iophores, and conidia (120). After breaking dor- (e.g., 6, 7, 76, 85).
mancy, infected buds give rise to “flag shoots” Current taxonomic systems for powdery
that can be covered with profusely sporulating mildews use not only morphological informa-
mycelia, supplying the primary inoculum to ini- tion, but also host range data and inferred phy-
tiate the disease cycle (84). Several reports in- logenetic relationships based on molecular data.
dicate that the infected buds are less likely to Reports began appearing in the 1990s that used
survive low winter temperatures, resulting in ITS and 18S rDNA sequences to infer phyloge-
reduced powdery mildew populations during netic relationships of Erysiphales and other ma-
growing seasons that follow harsh winters (84). jor ascomycete groups (121, 122). Analyses of
The third kind of perennation involves mycelia 18S rDNA, ITS1–5.8S-ITS2, and 28S rDNA
that persist through unfavorable conditions, ei- sequences led Wang et al. (145) to suggest that
ther the winter on hosts with persistent leaves the order Erysiphales can be placed in class
(54, 84), or when high temperatures suppress Leotiomycetes along with the orders Cyttari-
growth and sporulation (26). ales, Helotiales, and Rhytismatales. It appears
therefore that the powdery mildews are part of
a lineage sharing an ancient, often parasitic as-
SYSTEMATICS sociation with angiosperms.
Biological systematics encompasses efforts to In recent work, molecular clock mod-
develop classification systems and to under- els are being used to address problems in

34 Glawe
 powdery mildew phylogeny and coevolution. as the tribes Erysipheae, Golovinomyceteae,
Using a molecular clock based on changes Cystotheceae, Phyllactinieae, and Blumerieae
in 18S rDNA, Takamatsu (131) estimated the (17). Recent research suggests that the phylo-
time of divergence of Erysiphales from Myx- genetic structure within the order may be more
otrichaceae at about 100 mya. Takamatsu & complex than initially realized. To-anun et al.
Matsuda (135) used molecular clock models (140) described a new subgenus of Oidium that,
based on changes in ITS and 28S rDNA while sharing affinities with Tribe Golovino-
sequences to estimate times of divergence myceteae, appeared distinct from any described
Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org

within the Erysiphales. Their analyses sug- tribe. Similarly, the recently described genera
gested that radiation of the major tribes of Parauncinula (132) and Caespitotheca (137), clus-
Erysiphales occurred rather rapidly near the tered near the base of the clade Erysiphales but
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Cretaceous/Tertiary boundary. Since that pa- were not assignable to any described tribe. Fur-
per molecular clock models have been used ther research on other gene sequences or on
to address a variety of evolutionary questions. additional taxa may clarify whether new tribes
Such reports have estimated times of diver- are warranted.
gence of cryptic species within a morpholog- Currently recognized genera (Table 1) are
ical species (90), among host-specific lineages consistent with phylogenetic relationships in-
within B. graminis (83), and possible coevolu- ferred on the basis of rDNA sequences (17, 18,
tion of clades within the genus Sawadaea and 132, 137). In many cases, anamorphic charac-
the host genus Acer (79). ters are of primary taxonomic importance in
recognizing genera, thereby simplifying deter-
mination when teleomorph features are un-
Tribes and Genera available (58). Names applied to anamorphic
Braun (15) summarized concepts regarding states, and taxonomically significant characters,
subfamilies, tribes, and genera based on mor- are summarized in Table 2.
phological features. He recognized the sub- Tribe Erysipheae includes clades repre-
families Erysiphoideae and Phyllactinioideae, sented by Brasiliomyces, Erysiphe, and Ty-
distinguished largely on the basis of whether phulochaeta (17). Brasiliomyces species lack
mycelia were external or internal to the host. anamorphs and produce chasmothecia with
Within the subfamily Erysiphoideae were the peridia consisting of a single layer of cells,
tribes Erysipheae, with multiascal ascocarps, unlike the more complex peridia of other
and Cystotheceae, with ascocarps each produc- Erysiphales (15, 17). Application of the genus
ing a single ascus. Tribe Erysipheae was further name Erysiphe differs from earlier concepts
subdivided into subtribes based on ascocarp ap- that emphasized teleomorph features to the ex-
pendages. clusion of characteristics of anamorphs (sum-
This morphology-based taxonomy has been marized in 15). Erysiphe now is applied to
extensively revised to incorporate results of species forming conidia singly (Pseudoidium
studies on rDNA sequences (17, 18). Molec- anamorphs) and with lobed appressoria, and
ular evidence suggests that in the Erysiphales includes not only many species traditionally
phylogenetic lineages are correlated with placed in Erysiphe but also those formerly clas-
anamorphic features such as conidial ontogeny sified in Microsphaera, Uncinula, and Uncin-
(production of conidia singly or in chains), ap- uliella (17). The genus Erysiphe sometimes is
pressorium morphology, and presence or ab- subdivided into sections Erysiphe, Microsphaera,
sence of distinct fibrosin bodies. The chasmoth- and Uncinula to designate artificial group-
ecial appendages that were traditionally used ings based on chasmothecial appendages (17).
to distinguish genera are now used to distin- Species forming conidia in chains (Euoidium
guish species, not genera (17, 18). The five anamorphs) were transferred either to Golovino-
major clades within the order are designated myces (species with nipple-shaped appressoria)

www.annualreviews.org • Powdery Mildews 35

 Table 1 Selected distinguishing features of genera applied to Erysiphales holomorphsa
Holomorph Specialized Fibrosin Chasmothecial Asci/
genus Mycelium hyphae Conidiogenesis body appendageb chasmothecium
Erysipheae
Brasiliomyces External Absent Unreported Unreported M Multiple
Erysiphe External Absent Single Absent M, U, D, S Multiple
Typhulochaeta External Absent Unreported Unreported C Multiple
Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org

Golovinomyceteae
Golovinomyces External Absent Catenate Absent M Multiple
Neoerysiphe External Absent Catenate Absent M Multiple
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Arthrocladiella External Absent Catenate Absent D Multiple

Cystotheceae
Cystotheca External Filiform to falcate Catenate Present M Single
Podosphaera External Absent Catenate Present M, D Single
Sawadaea External Absent Catenate Present D Single
Phyllactinieae
Leveillula Internal/external Absent Single Absent M Multiple
Phyllactinia Internal/external Absent Single Absent A and P Multiple
Pleochaeta Internal/external Absent Single Absent U Multiple
Queirozia Internal/external Forked Single Absent U Multiple
Blumerieae
Blumeria External Falcate Catenate Absent M Multiple
Unassigned to tribe
Oidium subg. External Absent Catenate Absent Unreported Unreported
Microidium
Parauncinula External Absent Unreported Unreported U Multiple
Caespitotheca External Simple Catenate Absent U Multiple

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

or Neoerysiphe (species with lobed appressoria) mougeotii (Lev.) Vassilkov with an anamorph re-
(17). The genus Typhulochaeta includes species sembling those of Golovinomyces but producing
producing chasmothecia with specialized, deli- chasmothecia with dichotomously branched
quescing appendage-like cells that can rupture appendages (15).
to eject mucilaginous material (15). Tribe Cystotheceae includes Erysiphales
Tribe Golovinomyceteae includes species of with Euoidium anamorphs, forming chains of
Golovinomyces, Neoerysiphe, and Arthrocladiella, conidia with fibrosin bodies (17). The three
all forming Euoidium anamorphs (forming coni- genera include Cystotheca, Podosphaera, and
dia in chains rather than singly) (17). Golovino- Sawadaea (17, 18). Cystotheca and Podosphaera
myces and Neoerysiphe include species formerly species form chasmothecia containing a sin-
referred to Erysiphe (e.g., 153). These two gen- gle ascus, whereas in Sawadaea chasmothecia
era are distinguished on the basis of appresso- contain multiple asci (17). Cystotheca is distin-
rial morphology, with species of Golovinomyces guished by peridia consisting of two separable
forming nipple-shaped appressoria and those wall layers, and by falcate aerial hyphae (15, 17).
Neoerysiphe forming lobed appressoria. Arthro- Podosphaera includes species formerly classified
cladiella includes only the single species A. in Sphaerotheca, and in contrast to Cystotheca the

36 Glawe
 Table 2 Selected distinguishing features of genera and subgenera applied to Erysiphales anamorphsa
Appressorium Foot Cell Conidiogenesis Conidia Teleomorph genus
Tribe Erysipheae
Oidium subg. Lobed Straight to Single Monomorphic Erysiphe
Pseudoidium bent
Tribe Golovinomyceteae
Oidium subg. Nipple-shaped Straight Catenate Monomorphic Golovinomyces
Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org

Reticuloidium
Oidium subg. Lobed Straight Catenate Monomorphic Neoerysiphe
Striatoidium
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Oidium subg. Nipple-shaped Straight Catenate Monomorphic Arthrocladiella

Graciloidium
Tribe Cystotheceae
Oidium subg. Setoidium Nipple-shaped Straight Catenate Monomorphic, Cystotheca
fibrosin bodies
Oidium subg. Fibroidium Nipple-shaped Straight Catenate Monomorphic Podosphaera
fibrosin bodies
Oidium subg. Nipple-shaped Straight Catenate Dimorphic fibrosin Sawadaea
Octagoidium bodies
Tribe Phyllactinieae
Oidiopsis Lobed to coralloid Straight Single Dimorphic Leveillula
Ovulariopsis Lobed Straight Single Dimorphic Phyllactinia
Streptopodium Reduced Twisted Single Dimorphic Pleochaeta
Streptopodium-like Reduced Straight Single Dimorphic, Queirozia
pigmented
Tribe Blumerieae
Oidium subgenus Oidium Lobed or reduced Base inflated Catenate Monomorphic Blumeria
Unassigned to tribes
Oidium subg. Microidium Lobed Twisted Catenate Monomorphic Unknown
Oidium Lobed to coralloid Straight Catenate Monomorphic Caespitotheca

a
Listed according to tribe (17, 98, 137, 140).

chasmothecia exhibit multilayered peridia (17, conidia and unusual chasmothecia with two
18). Sawadaea includes synanamorphic species kinds of appendages (15, 97). Acicular ap-
forming both microconidia and macroconidia pendages include bulb-shaped bases and lance-
(17, 58). shaped shafts. The appendages function both
Tribe Phyllactinieae includes species with in dislodging chasmothecia and in orienting
endophytic mycelia (17). Genera are based on them while airborne (123, 146). Penicillate cells
chasmothecial and anamorphic features (15, form on the dorsal surface of chasmothecia
17). Leveillula species produce ascomata with and gelatinize to form a sticky pad that at-
mycelioid appendages and form dimorphic taches conidia to new substrates following aerial
conidia; the first-formed conidium (the pri- dispersal (146). Pleochaeta species form chas-
mary conidium) on a conidiophore typically mothecia with dichotomously branched ap-
is lanceolate (with one pointed end) whereas pendages, and spirally twisted conidiophore
later ones (secondary conidia) lack a pointed foot cells (17, 90). Queirozia includes a single
end (15, 86, 87). Phyllactinia species form var- species. It forms both external and endophytic
iously shaped rhombiform and/or lanceolate hyphae, dichotomously branched aerial hyphae,

www.annualreviews.org • Powdery Mildews 37

 uncinate chasmothecial appendages, and a de- tury, species were distinguished using anatom-
matiaceous anamorph with singly formed coni- ical features including chasmothecial morphol-
dia that usually are lemon-shaped (98). ogy (size, shape, appendages, and peridial cells),
Tribe Blumerieae includes only the genus asci and ascospore morphology, mycelial char-
Blumeria. Occurring only on Poaceae, the sin- acteristics, and morphology of appressoria, foot
gle species B. graminis (DC.) Speer forms an cells, and conidia, and host range (e.g., 13, 17).
Euoidium anamorph with distinctively shaped About 650 species are recognized using this ap-
conidiophore foot cells, multilobed haustoria, proach (17).
Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org

and chasmothecia with mycelioid appendages The taxonomy of powdery mildew species
(15, 17, 128). is changing as new molecular data are obtained
Several species remain unassigned to tribes. and analyzed. This work has accelerated as im-
by Chiang Mai University on 12/07/10. For personal use only.

Oidium phyllanthi J. M. Yen appeared most proved techniques for extracting DNA and am-
closely related to tribe Golovinomyceteae based plifying sequences of interest have been devel-
on analyses of 28S and 18S sequence data, but oped (45, 83, 134). A wide variety of species and
was not regarded as a member of that tribe taxonomic problems have been addressed so far.
(140). Parauncinula was erected for two species Takamatsu et al. (133) analyzed ITS and 18S
with uncinate chasmothecial appendages and rDNA sequences and clarified the taxonomy
curved ascospores; anamorphs are unknown of several Quercus-infecting powdery mildews.
in this genus (132). It occupied a basal po- They showed that Erysiphe hypophylla (Nevod.)
sition within the Erysiphales but was not as- U. Braun & Cunningt. and E. alphitoides
signed to a tribe (132). Caespitotheca is an- (Griffon & Maubl.) U. Braun & S. Takam. can
other recently recognized genus, characterized be distinguished by conidial size and shape, and
by apically grouped uncinate chasmothecial that Erysiphe quercicola S. Takam. & U. Braun
appendages and an Euoidium anamorph with can be distinguished from E. alphitoides by the
coralloid appressoria (137). Phylogenetic anal- length of chasmothecial appendages. Analyses
yses of 28S, 5.8S, and 18S rDNA sequences in- of ITS sequences confirmed that differences
dicated that the genus occupies a basal position in conidial morphology are sufficient to dis-
within the Erysiphales clade (137). tinguish species of Leveillula (86, 87). Braun
et al. (19) showed that several species of Erysiphe
occurring on Carpinus are distinguishable on
Species the basis of chasmothecial appendage size and
Species concepts in biology remain varied and number, morphology of the coiled appendage
controversial (105) so it is not surprising that apices, and curvature of the conidiophore foot
differing species concepts have been applied cell. Golovinomyces cichoracearum in the broad
to powdery mildews. Early eighteenth- and sense was regarded as several similar species by
nineteenth-century researchers distinguished Braun (15) on the basis of host range and mor-
powdery mildew species largely on the ba- phological features. Analysis of sequence data is
sis of host (154). Salmon’s (123) influential resulting in further clarification of that species
monograph was distinguished by a broad, complex (104, 136). Phyllactinia guttata, an-
morphology-based species concept and it in- other widely distributed species reported from
cluded 49 species. He emphasized teleomorph many host families, appears also to be a species
features to the relative neglect of anamorph complex (15) but published studies on it us-
characteristics and host ranges. The twentieth ing molecular data are lacking. Liberato (97)
century saw an accumulation of information on recently showed that anamorphic features dis-
individual species, particularly by Asian and Eu- tinguished Phyllactinia chorisiae Viégas from
ropean authors (reviewed in 17) and it became P. guttata, with which it had been considered
clear that many of Salmon’s species were too conspecific. That report (97) reinforces the idea
broadly defined (15). By the late twentieth cen- that new taxonomic insights can be obtained

38 Glawe
 from observations on even commonly encoun- creasingly useful. It seems likely that the num-
tered powdery mildews. Kiss et al. (90) used ITS ber of recognized species will continue to grow.
and 28S rDNA sequences to distinguish two The powdery mildews of many parts of the
phylogenetic species of Pleochaeta that could not world have yet to be studied by taxonomists.
be separated morphologically. Areas identified by Braun et al. (17) that are
Taxonomic categories within species include in particular need of study include large parts
varieties, used when morphological differences of Africa, Asia, and North America. Surpris-
were insufficient to justify recognition of dis- ingly, information on North American species
Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org

tinct species (15), or formae speciales, applied to powdery mildews is both incomplete and based
reflect differences in host range within a mor- largely on obsolete taxonomic systems. A sig-
phological species (2, 83). An influential early nificant practical problem is that it can be diffi-
by Chiang Mai University on 12/07/10. For personal use only.

paper was that of Marchal (101), who reported cult, sometimes impossible, to determine which
specificity at the host genus level for strains species has been the subject of a given pub-
of Blumeria graminis, laying the foundation for lished report. The only compilation of fungi
the formae speciales still recognized within the in the United States (44) included about 70
species (83). Host range studies can be difficult species of Erysiphales, while research in the
to perform and interpret. Problems that com- Pacific Northwest of North America suggests
plicate such work are cross-contamination (123) that in that region alone there are 150 or more
and the possibility of enhanced host susceptibil- species (57). Reconnaissance of botanical gar-
ity in greenhouse environments (11, 15, 31, 33). dens, arboreta, or even weed-ridden fields regu-
Analysis of molecular data affords an alterna- larly yields new geographic or host records (38,
tive approach to assessing variation within sub- 56).
specific taxa and populations, and methodology
for such work is improving rapidly. Wyand &
Brown (150) examined relationships of some Determination of Species
formae speciales of B. graminis using β-tubulin The process of determining the species to
and ITS sequences and concluded that these which a powdery mildew can be referred is
sequences were not sufficiently variable for use sometimes called (incorrectly) identification.
in resolving relationships within that species. To identify something is to establish that it is
More recently, Inuma et al. (83) assessed re- identical with something else—a logical impos-
lationships among formae speciales of B. grami- sibility when dealing with organisms that are
nis using ITS and 28S rDNA, chitin synthase subject to genotypic and phenotypic variation.
gene and β-tubulin gene sequences and recog- In determining a species one works within the
nized nine distinct groups within the species. framework of a given taxonomic system to ap-
In a study of strains of Podosphaera tridactyla ply names to organisms in a manner consistent
(Wallr.) de Bary from Asia, Australia, and Eu- with that system. As biology has evolved, and as
rope, Cunnington et al. (32) suggested on the new information about powdery mildews has
basis of RFLP analysis of ITS sequences that become available, taxonomic systems for pow-
this taxon consist of three distinct clades. They dery mildews have changed considerably.
concluded that more research on strains from The taxonomic system described by Braun
additional geographical locations and hosts, and et al. (17) embodies the concepts used by most
perhaps using additional gene sequence data, is contemporary powdery mildew taxonomists.
needed to resolve fully the taxonomic implica- The species concept on which it is based in-
tions of their findings. corporates information on host, morphology of
In summary, the trend toward more nar- teleomorphs and anamorphs, and geographi-
rowly delimited species continues. Species are cal range. Useful teleomorph features include
based primarily on anamorph and teleomorph size and shape of chasmothecia; number, size,
morphology but molecular data are proving in- and morphology of chasmothecial appendages;

www.annualreviews.org • Powdery Mildews 39

 ascus number and shape; and ascospore size, Because powdery mildew conidia from many
shape, and number per ascus (17). Unfortu- species are similar in size and shape, using mor-
nately, information on anamorphs is lacking for phological features to determine the species
about 75% of powdery mildew species (17). represented in spore samples frequently has
Despite this limitation, anamorphic powdery been problematic (43). New techniques for ob-
mildews can be determined to species using taining gene sequence data from small num-
such features as host, presence or absence of bers of spores are promising to improve greatly
specialized hyphae, morphology of appresso- the accuracy of determining species from spore
Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org

ria, morphology and size of foot cells, coni- samples. Matsuda et al. (103) distinguished Oid-
dial size and shape, and presence or absence ium neolycopersici L. Kiss from Erysiphe trifolii
of fibrosin bodies (12, 17, 29). Useful compi- Grev. by removing single conidia from in-
by Chiang Mai University on 12/07/10. For personal use only.

lations with drawings or photographs of mor- fected tomato leaves and comparing the ITS
phological features can be seen in various re- sequences with archived sequence data. Falacy
cent works by Braun (15, 16), Braun et al. (17), et al. (43) developed primers specific to Erysiphe
Shin and La (127), Bolay (13), and Glawe (58). necator and used them to amplify DNA from
Braun’s (15) world monograph is the most re- conidia collected from air samples. They could
cent comprehensive work but many regional detect five or fewer conidia, and detected air-
taxonomic treatments have been published borne inoculum during periods of ascospore
since it appeared (13, 17). There is no North discharge. The approach appears to offer a cost-
American monograph of Erysiphales; conse- effective solution for growers needing near real-
quently, Braun’s (15) treatment remains the time information on inoculum availability to re-
most comprehensive source of taxonomic in- duce unnecessary fungicide treatments.
formation for this continent.
The combination of more complete mor-
phological descriptions and gene sequence data GEOGRAPHICAL
has increased the reliability of species deter- DISTRIBUTIONS
minations. ITS sequences were used to clarify Amano’s (8) compilation of host and geographi-
the taxonomy of Australian anamorphic pow- cal ranges of powdery mildews remains the most
dery mildews on Fabaceae (31) and Solanaceae comprehensive source of such information. It
(33). ITS sequences and morphological fea- appears that Erysiphales are most diverse in
tures were used to show that two species of temperate regions of the Northern Hemisphere
Erysiphe were associated with powdery mildew (8, 148). However, many regions of the world
outbreaks of soybean (Glycine max) in east Asia, remain unexplored for powdery mildews, in-
and that one of them is likely conspecific with cluding large parts of Africa, North and South
the species attacking soybean in the United America, and Asia (17).
States (139). Using ITS and 28S rDNA se- Assessing sequence data in combination with
quence data along with morphological informa- morphological, host, and paleontological in-
tion resolved long-standing difficulties in dis- formation is a powerful approach for study-
tinguishing several Erysiphe species occurring ing ancient origins and spread of powdery
on Quercus spp. (133). A combination of ap- mildews. Matsuda & Takamatsu (104) used
proaches involving light and scanning electron ITS and 28S rDNA sequence data to investi-
microscopy and analysis of ITS sequences dis- gate the ancient relationship between species of
tinguished two Oidium species attacking tomato Golovinomyces and hosts in the Asteraceae. They
(Lycopersicon esculentum) (89). Another study us- found evidence that host-parasite relationships
ing morphological and rDNA sequence data included both coevolution with asteraceous
distinguished several previously incompletely hosts and host-jumping to species in other
known species of Erysiphe occurring on Carpi- angiosperm families. Takamatsu et al. (136)
nus spp. (19). subsequently suggested that the Golovinomyces

40 Glawe
 clade arose in the Northern Hemisphere after was unnoticed on such a valuable crop, lead-
the Asteraceae invaded North American from ing one to conclude that it arrived in the region
South America. Furthermore, using a molecu- only shortly before its discovery.
lar clock model, Takamatsu & Matsuda (135) The years leading up to and including the
uncovered evidence that at least one clade of twenty-first century have seen numerous first
Golovinomyces species may have invaded South reports of powdery mildews from regions out-
America from North America following closure side their previously known distributions. Bolay
of the Isthmus of Panama (estimated at 3.1– et al. (14) suggested that recent climatic changes
Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org

2.8 mya). in Europe may favor spread of alien powdery

Geographical ranges of some species appear mildew species. Frequently, new records are
to be increasing. Kreisel & Scholler (92) re- published in succession by independently work-
by Chiang Mai University on 12/07/10. For personal use only.

viewed records of plant pathogenic fungi in- ing researchers. For example, Erysiphe flexuosa
troduced into Germany and nearby countries is thought native to Aesculus spp. in North
since 1750 and included 16 powdery mildew America (15). The fungus was found in Europe
species in the resulting list. Five species ap- in 2000 and soon its presence was documented
peared to have originated in North America, in Croatia, France, Germany, Poland, Slovakia,
five in Asia, one in another part of Europe, and Switzerland, the United Kingdom (157),
the others were of uncertain origin. Five species Hungary (5, 91), Slovenia (107), and Lithuania
were recorded for the first time in Germany (68). In North America, E. flexuosa first was
in the nineteenth century, five more between reported in the Pacific Northwest in 2006 and
1900 and 1950, and the other six species from probably is not native to the region because its
1956 to 1989. They believed the greatest pe- hosts were introduced (59). Erysiphe palczewskii
riod of introduction of powdery mildews into ( Jacz.) U. Braun & S. Takam. is another species
Germany began about 1900. There are several with rapidly expanding geographical distribu-
well-known examples of important pathogens tion. Occurring on Caragana species, it was first
of economic crops spreading to new regions described in 1927 from the Russian Far East
from the mid-nineteenth to the early twentieth (15). It was reported in Belarus in 1975, and
centuries. Erysiphe necator, originally described now is widespread in Europe (77). In Finland
from North America, was found in Europe in it seems to have displaced the native species
1845; by 1852 it occurred throughout Europe Erysiphe trifolii from this host (81). North
and the Mediterranean region (148). Given the American reports began in 2003 (110), and it
long history of viticulture, and great attention is now known to occur as far north as central
paid to wine grapes, it is extremely unlikely Alaska (62) and as far east as Minnesota (63).
that E. necator existed in Europe much ear- Erysiphe symphoricarpi (Howe) U. Braun &
lier than when it was reported there. Similarly, S. Takam., thought native to North America,
Podosphaera mors-uvae (Schwein.) U. Braun & first was reported in Europe in the 1980s but
S. Takam. was described in North America the teleomorph was unknown there until 2002
in 1834 and by the early twentieth century (88). Bolay et al. (14) noted that Erysiphe rus-
was widespread in western Europe and Japan sellii (Clinton) U. Braun & S. Takam. oc-
(148). A more recent example of an important curred in Europe since the nineteenth century
pathogen occurring in a new region is afforded but chasmothecia were reported for the first
by the hop powdery mildew fungus Podosphaera time in the late twentieth century. Powdery
humuli (Wallr.) U. Braun & S. Takam. It was un- mildews on Rhododendron species were observed
known in eastern Washington state, the major in Europe in the early 1980s but teleomorphs
North American production region of hops, un- were not reported until 2000 (82). There are
til the 1990s (142). It seems extremely unlikely many reports of newly recorded exotic species
that such a conspicuous, damaging pathogen for which teleomorphs have not yet been found.

www.annualreviews.org • Powdery Mildews 41

 An anamorphic fungus referable to Erysiphe et al. (81) reported that when Erysiphe pal-
deutziae (Bunkina) U. Braun & S. Takam. czewskii became established on Caragana ar-
is increasing its geographical distribution in borescens in Finland, the native Erysiphe trifolii
Europe, having previously occurred widely in soon could not be found on this host, apparently
the Russian Far East and Japan (14). Erysiphe having been displaced by the newly arrived
catalpae Simonyan and E. howeana U. Braun also species. Species endemic to a region also can
have been known in Europe for many years in coinfect hosts. For example, Phyllactinia gut-
only the anamorphic states (14). Such reports tata and Erysiphe penicillata (Wallr.) Link were
Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org

might involve heterothallic species where for a reported to coinfect leaves of Alnus species in
time only one mating type is present, or perhaps Ontario (115).
it takes time for new biotypes, well-adapted to Recent evidence suggests that air pollution
by Chiang Mai University on 12/07/10. For personal use only.

new environmental conditions, to emerge. At and climate change may be affecting the dis-
present a satisfactory explanation for this phe- tribution and activities of powdery mildews.
nomenon is not available. Dynowska (40) studied the occurrence of
Powdery mildew species can coinfect the Erysiphales in cities in northern Poland from
same host plant, increasing the likelihood that 1981 to 1991 and reported that although more
newly arrived species can be overlooked. Leveil- species were found in urban areas, severity of
lula taurica and Golovinomyces orontii (Castagne) diseases caused by them were higher in sub-
V.P. Heluta were found coinfecting leaves of urban areas. A likely cause was thought to be
potato in central Washington (61). The lat- the effects of air pollutants on powdery mildews
ter fungus, originally reported as Erysiphe ci- (40). Cook et al. (30) suggested that lengthen-
choracearum, occurred on potato in that state ing growing seasons in the United Kingdom
since the 1940s (106). Leveillula taurica occurred favored maturation of greater numbers of chas-
in the region since the 1980s or earlier (47) mothecia of Erysiphe elevata, contributing to its
and may have been overlooked on potato for increasing prevalence and ability to displace
years because its presence was masked by G. Neoerysiphe galeopsidis from coinfected leaves.
orontii (61). Cook et al. (30) reported that Neo- Such findings may offer the first indication that
erysiphe galeopsidis (DC.) U. Braun and Erysiphe extended growing seasons may produce signif-
elevata coinfected leaves of Catalpa species in icant changes in the life histories of powdery
England; N. galeopsidis appeared in June but mildews and epidemiology of the diseases they
was soon displaced by E. elevata. Huhtinen cause.

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 of
those occurring there. A similar situation exists in South America, Africa, and parts of
Asia.
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 powdery
mildew 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 to
be more closely correlated with features of anamorphs than teleomorphs. Genus concepts
also were modified to reflect the newly recognized phylogenic relationships.

42 Glawe
 4. Molecular data sets have proven useful in reassessing species and clarifying the taxonomic
significance of morphological and host data. Only a small percentage of the described
species have been reassessed using these approaches.
5. New PCR-based methods have been used to determine species on the basis of one or a
few spores. These approaches have the potential to facilitate the use of spore-trapping
Annu. Rev. Phytopathol. 2008.46:27-51. Downloaded from www.annualreviews.org

to assess inoculum levels for determining timing of fungicide applications.

6. Geographical distributions of some species appear to be expanding rapidly. Climate
change has been suggested as a possible explanation. Longer growing seasons also may
by Chiang Mai University on 12/07/10. For personal use only.

result in production of greater numbers of chasmothecia and higher powdery mildew

populations in succeeding growing seasons. In at least one case, an exotic species has
largely 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 taxonomic
systems. There is an urgent need for what is sometimes called alpha taxonomic work: the
collection, 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 will
be necessary to clarify species concepts and can provide information about disease cycles
that can be used to develop control strategies.
3. Very little information is available on the ultrastructure of conidiogenesis in powdery
mildews. 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 the
evolution of conidial states in the order.
4. PCR-based procedures for detecting powdery mildews have great potential to improve
capabilities in disease forecasting and management. Further work is needed to develop
them 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 growth
habit of many species, and the long history of records in some parts of the world, may
make powdery mildews unusually well-suited models for studying the effects of climate
change on plant diseases.

DISCLOSURE STATEMENT
The author is not aware of any biases that might be perceived as affecting the objectivity of this
review.

www.annualreviews.org • Powdery Mildews 43

 ACKNOWLEDGMENTS
PPNS No. 0474, Department of Plant Pathology, College of Agricultural, Human, and Natural
Resource Sciences, Agricultural Research Center, Project No. WNP00313, Washington State
University, 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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RELATED INTERNET RESOURCES

Index Fungorum: http://www.indexfungorum.org/Names/Names.asp
Online 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.asp
An 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 founded
several 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 plant
pathology.

www.annualreviews.org • Powdery Mildews 51

 AR351-FM ARI 23 June 2008 14:24

Annual Review of
Phytopathology

Contents Volume 46, 2008

The Phenotypic Expression of a Genotype: Bringing Muddy Boots

and Micropipettes Together
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Roger Hull p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
The Origin of Ceratocystis fagacearum, the Oak Wilt Fungus
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Jennifer Juzwik, Thomas C. Harrington, William L. MacDonald,

and David N. Appel p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p13
The Powdery Mildews: A Review of The World’s Most Familiar
(Yet Poorly Known) Plant Pathogens
Dean A. Glawe p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p27
Plants as a Habitat for Beneficial and/or Human Pathogenic Bacteria
Heather L. L. Tyler and Eric W. Triplett p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p53
The Origins of Plant Pathogens in Agro-Ecosystems
Eva H. Stukenbrock and Bruce A. McDonald p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p75
Role of Stomata in Plant Innate Immunity and Foliar Bacterial Diseases
Maeli Melotto, William Underwood, and Sheng-Yang He p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 101
Models of Fungicide Resistance Dynamics
Frank van den Bosch and Christopher A. Gilligan p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 123
Siderophores in Fungal Physiology and Virulence
Hubertus Haas, Martin Eisendle, and Gillian Turgeon p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 149
Breaking the Barriers: Microbial Effector Molecules Subvert
Plant Immunity
Vera Göhre and Silke Robatzek p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 189
Yeast as a Model Host to Explore Plant Virus-Host Interactions
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Living in Two Worlds: The Plant and Insect Lifestyles
of Xylella fastidiosa
Subhadeep Chatterjee, Rodrigo P.P. Almeida, and Steven Lindow p p p p p p p p p p p p p p p p p p p p p p p p 243

v
 AR351-FM ARI 23 June 2008 14:24

Identification and Rational Design of Novel Antimicrobial Peptides

for Plant Protection
Jose F. Marcos, Alberto Muñoz, Enrique Pérez-Payá, Santosh Misra,
and Belén López-García p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 273
Direct and Indirect Roles of Viral Suppressors of RNA Silencing
in Pathogenesis
Juan A. Díaz-Pendón and Shou-Wei Ding p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 303
Insect Vector Interactions with Persistently Transmitted Viruses
Saskia A. Hogenhout, El-Desouky Ammar, Anna E. Whitfield,
and Margaret G. Redinbaugh p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 327
Plant Viruses as Biotemplates for Materials and Their
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Use in Nanotechnology
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Epidemiological Models for Invasion and Persistence of Pathogens

Christopher A. Gilligan and Frank van den Bosch p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 385

Errata

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