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BIODIVERSITY REFERENCE
 


PROFILE:

Order: ERYSIPHALES   (Powdery Mildews)

kingdom: Fungi,  phylum: Ascomycota


 

Powdery Mildews (Erysiphales) are obligate parasites of flowering plants (Magnoliophytina). Over 850 species are currently recognised (Braun & Cook, 2012).

Most are relatively benign parasites, forming localised colonies on leaf surfaces without noticably affecting the vigour of their hosts, though some have much greater impact, particularly some Podosphaera species. P. mors-uvae is the American Gooseberry Mildew, an introduced and damaging parasite on gooseberries and currants in Britain, causing extensive leaf and shoot deformations. Blumeria graminis (= Erysiphe graminis) is the sometimes troublesome Corn Mildew of cereals and is the only powdery mildew on grasses. Erysiphe platani, another introduction, is beginning to appear on planted trees of London Plane (Platanus x hispanica) along city streets, coating and distortorting the leaves of new shoots and branch tips.

Erysiphe aquilegiae
Erysiphe aquilegiae, anamorph with abundant conidia, on leaf of Meadow Buttercup (Ranunculus acris)

Powdery mildews can be unsightly even when causing no significant damage. Thus they can still cause serious economic losses in horticulture and ruin garden displays, where aesthetic appeal is vital. Particularly in warm, dry periods in late summer, they can appear extensively on garden plants and the impression is one of epidemic spread. However, since most are highly host-specific, the true situation is that a number of different species are similtaneously being favoured by the weather. They perhaps are more sulphur tolerant than some other competing fungi on leaf surfaces, and so benefit in urban areas.

Probable Euoideum longipes
Golovinomyces sp. (probably the host-specific Euoideum longipes anamorph
but unconfirmed), causing heavy infection of Petunia in a public floral display

Infection is typically superficial, the mycelium being predominantly on the leaf (or stem) surfaces, attached to those surfaces by appressoria, and with individual hyphae penetrating the epidermal cells to form intracellular haustoria (hyphal branches adapted for food absorption from within the host). Entry into the cells is both by mechanical penetration and by enzymatic degradation of the cuticle and cell wall. The haustorium is normally a simple, swollen hyphal tip, but in Blumeria graminis it is branched into finger-like processes.

Not all powdery mildews remain superficial. In the genera Leveillula, Phyllactinia and Pleochaeta, the hyphae enter more deeply into the leaf tissues, often via the stomata.

A very good general account of the Erysiphales was included in Webster (1980), though the taxonomy is now out of date, and the description of Erysiphe is based around the atypical Blumeria graminis (as Erysiphe graminis). More recently, a splendid overview of the group, with scanning electron micrographs as well as numerous, detailed line drawings of micromorphological features, has been provided by Braun, et al., (2002).

Note that the "downy mildews" (Peronosporales, Oomycota) and "dark mildews" (Meliolales, Ascomycota) are quite different groups of fungal plant-pathogens.


Reproduction and spread
Asexual state (anamorph)
Powdery mildews appear initially in their anamorphic state, forming usually conspicuous, white, powdery patches on leaf surfaces. The 'powder' is a result of copious production of conidia (asexual spores, produced by mitosis). The conidia are usually produced in short chains from erect conidiophores on the leaf surface, though produced singly from conidiophores in some genera.

The conidia are thin walled, colourless and evidently not for long-term survival, but they are readily blown from one plant to another. Spread through a host colony can be efficient and rapid. Conidia germinate rapidly, within 10 hours in most cases, to produce a germ-tube with an appressorium. Conidial surfaces may be smooth or with walls minutely wrinkled, striate or 'rough-cast'.

Golovinomyces sonchicola: conidiophores and conidium
 

In the genera Podosphaera and Sawadaea, and the mainly Asian Cystotheca, the conidia contain long, narrow, refractive particles termed "fibrosin bodies". These are valuable in generic identification but may require fresh conidia and a correctly set microscope.

Conidia with fibrosin bodies (arrowed):
a) Podosphaera xanthii, on Pot Marigold (Calendula officinalis)); b) Podosphaera plantaginis, on Ribwort Plantain, (Plantago lanceolata).


Sexual state (teleomorph)
The teleomorph may occur with the anamorph, or later, or not be seen at all. The fruit-body (ascoma or ascocarp) is a cleistothecium, based on the definition of a cleistothecium as a fruit-body entirely enclosing the asci, there being no pore (ostiole) through which spore release takes place. The wall of the cleistothecium has to break open before the spores can be liberated. However, the organised internal arrangement of asci is more like that seen in perithecia (which are, however, defined by the presence of an ostiole). Braun et al. (2002) introduced the the term 'chasmothecium' for powdery mildew ascomata and this term is also used in Braun & Cook (2012). In that it is well accepted that different fruit-body types have evolved several times in the Ascomycota and so have different internal structures, the simpler morphological classification is used here (for now).

Cleistothecia are produced most usually towards the end of the season, as sparse or aggregated, brown, then black, minute dots amongst the superficial mycelium, or where the mycelium has been.

Erysiphe trifoliorum on Lathyrus pratensis
Erysiphe trifoliorum with numerous, dot-like cleistothecia,
on late-season leaves of Meadow Pea (Lathyrus pratensis)
 
Erysiphe polygoni: cleistothecia on Knotgrass (Polgonum aviculare agg., probably P. agrestinum).
 

Depending on genus and species, the cleistothecia are sparsely to densely covered by various types of appendages: usually thick-walled, often pigmented, irregular hyphae. Other types of appenadage include uniform, stiff, radiating, hooked hyphae in, e.g., Sawadaea and Erysiphe sect. Uncinula, and hyphae with multiply branched tips in Erysiphe sect. Microsphaera. Some are illustrated below.

Podosphaera erigerontis-canadensis on Autumnal Hawkbit (Scorzoneroides autumnalis): cleistothecia with short, simple appendages.
Podosphaera epilobii on Great Hairy Willowherb (Epilobium hirsutum): cleistothecia with very long, brown appendages.
[Note also the single ascus, characteristic of the genus Podosphaera.]
Erysiphe capreae on Goat Sallow (Salix caprea): cleistothecial appendages dense, curved to coiled (circinate) at the tips.
Phyllactinia betulae on White Iberian Birch (Betula celtiberica): cleistothecial surface with dense, brush-like (penicillate) cells and spine-like appendages with bulbous bases.
Erysiphe penicillata (formerly Microsphaera penicillata) on Alder (Alnus glutinosa): cleistothecial appendages rigid, apices multiply dichotomously branched.
 

Each cleistothecium contains one or more asci, containing between 2 and 8 ascospores.

Golovinomyces sonchicola: multiple asci from broken cleistothecium,
in this species mostly 2 ascospores per ascus

Being thick-walled, cleistothecia can be regarded as resting stages, and they certainly have greater survival potential than conidia. In some species, ascospore development only takes place after over-wintering. However, in many cases, their longevity is limited and over-wintering may be primarily by mycelial survival on the host plant.


Host specificity
Powdery mildews are usually highly host-specific, being restricted to single or closely related hosts, or to a particular plant family. Furthermore, when a powdery mildew infects closely related species, it may possess races with physiological specialisation to single hosts, without cross infection being possible. When recognisable, such a strain may be distinguished as a "forma specialis" (plural: formae speciales) and given its own name.
     Example:
     Podosphaera pannosa f.sp. rosae has been used as a name for a physiological race (or races?) that only attacks roses, even though the species as a whole also attacks peaches and other Prunus species.

This informal naming system, not covered by the International Code of Nomenclature for Algae, Fungi and Plants (ICN), is not used to the same extent as it has been for rust fungi and it may well give a false impression of fixed intraspecific variants. On the other hand, given the excessive 'splitting' resulting from certain molecular work on plant-pathogenic fungi, it is not unlikely that some of these will be declared 'cryptic species' in the future, and named accordingly. Braun & Cook do indeed now recognise a number of new, host-specific species, e.g. in the Golovinomyces cichoracearum complex, but here the species are also supported on micro-morphological grounds and appear well founded.

Golovinomyces orontii is a widespread and frequent generalist species, confirmed on many species and often confused with specialist species on the same host (see below). This unfortunately means that many, many records of powdery mildews named only on the host, without microscopic confirmation, are of little or no value and should be discounted.


Principal British genera
The Erysiphales contain one family, the Erysiphaceae. Kirk et al. (2008) recognised 19 genera; Braun & Cook (2012, pg. 39) reduce these to 16, plus 9 additional form-genera to accomodate those species known only from asexual (anamorphic) states and not (yet) formally given names in the primary taxonomy of the family. Powdery mildews occur throughout the world.

In the UK, the principal genera are:

  • Erysiphe - many species. Cleistothecia with several asci; cleistothecial appendages often irregular, thick-walled hyphae. Includes the majority of species formerly placed in Uncinula (species with cleistothecial appendages stiff, radiating, with hooked tips) and in Microsphaera (species with cleistothecial appendages stiff, radiating, with multiply branched tips). Anamorphic states with, as yet, no formal name in Erysiphe are placed in the form-genus Pseudoidium.
  • Golovinomyces - a number of species recently separated from Erysiphe, often forming dense growths on leaf surfaces, includes the common, sometimes troublesome, non-host-specific G. orontii, and also G. cichoracearum, on many species of composites (Asteraceae). Anamorphic states with no formal name in Golovinomyces are placed in the form-genus Euoidium.
  • Neoërysiphe - a small genus, comprising species formerly included in Erysiphe but separated on clear molecular evidence and features of micro-morphology and conidial maturation. The asci do not mature before overwintering. A common species in the UK is N. galeopsidis, occuring especially on the plant family Lamiaceae (labiates).
  • Phyllactinia - a large genus but with very few British species, mostly on trees and shrubs, perhaps most notably P. fraxini on Ash (Fraxinus) and related genera. Cleistothecia with several asci; cleistothecial appendages stiff, radiating, with bulbous bases; cleistothecial apices with penicellate cells terminating in numerous filaments. Many records have been made under the name "P. guttata", regarding this as a plurivorous species on a wide range of hosts, but it is now known to be restricted to Hazel (Corylus) and other records need re-evaluation.
  • Sawadaea - a small genus, almost confined to maples (Acer) and mostly in Asia. However, S. bicornis is very common on Sycamore (Acer pseudoplatanus) here. Cleistothecia with several asci; cleistothecial appendages stiff, radiating, with dichotomously or trichotomously branched, curved tips; conidia with fibrosin bodies.
  • Podosphaera - numerous species (many formerly placed in the separate genus, Sphaerotheca), some causing considerable growth distortions and foliar damage. Cleistothecia with a single ascus; cleistothecial appendages irregular, thick-walled hyphae, sometimes stiff, radiating, with multiply branched tips; conidia with fibrosin bodies. Anamorphic states with no formal name in Podosphaera are placed in the form-genus Fibroidium.
  • Blumeria - only a single species in the genus, B. graminis, common on grasses. Differs from Erysiphe in its digitate haustoria and in details of the conidial wall.

Elsewhere in the world, Leveillula is a significant genus in warmer and drier regions, predominently Asia and mediterranean Europe. L. taurica is a wide ranging, non-host-limited species that has occurred as an introduction on garden plants in Britain.


Identification
The authoritative world monographs on the Erysiphales have been those of Braun (1987) and Braun & Cook (2012). The treatment in the latter is followed here. Ing (1990-91) provided useful summaries and keys to the British species.

Ellis & Ellis (1997) give valuable inclusion of the Erysiphales along with other microfungi, ordered by host, but the bulk of the book was first published in 1985 and uses now outdated nomenclature, and, seriously, leads to over-confident and often erroneous identifications based simply on host species without microscopic checking and confirmation.
     [Examples: the book gives only Erysiphe urticae on Urtica (stinging nettles), but of Wicken Fen (Cambridgeshire) finds that have been checked by me, only one has been E. urticae, the rest being the generalist, Golovinomyces orontii. The text also implies that the only powdery mildew on Plantago lanceolata (Ribwort Plantain) in Britain is Podosphaera plantaginis (as Sphaerotheca plantaginis), and the only species on Plantago major (Great Plantain) is Golovinomyces sordidus (as Erysiphe sordida). In fact both species occur frequently on either host and there is evidence of much misidentification.]

A very substantial and excellent on-line gallery of powdery mildew photographs, including photomicrographs, is available at Obligat Phytoparasitische Kleinpilze: Echte Mehltaupilze.


Hyperparasite
The hyphae of powdery mildews are frequently themselves parasitised by another fungus, Ampelomyces quisqualis, which has golden-brown pycnidia that look under the microscope like net shopping-bags. This net-like, surface ornamentation could lead these pycnidia to be confused with the cleistothecia of the host, but they are variably ovoid and produce large numbers of small, smooth, bean-shaped conidia.

Pycnidia of Ampelomyces quisqualis, parasitic on mycelium of powdery mildews:
a) on Neoërysiphe galeopsidis / Bear's-breech (Acanthus mollis));  b) on Podosphaera erigerontis-canadensis / Bilbao Fleabane (Conyza floribunda).


References
•   Braun, U. (1987). A monograph of the Erysiphales (powdery mildews). Beihefte zur Nova Hedwigia 89, J.Cramer, Berlin.
•   Braun, U., & Cook, R.T.A., (2012). Taxonomic manual of the Erysiphales (Powdery Mildews), CBS-GNAW Fungal Biodiversity Centre, Utrecht.
•   Braun, U., Cook, R.T.A., Inman, A.J., & Shin, H.-D. (2002). The taxonomy of the powdery mildew fungi, in Bélanger, R.R., Bushnell, W.R., Dik, A.J., & Carver, L.L.W., The powdery mildews. A comprehensive treatise. American Phytopathological Society, St. Paul, Minnesota, chapter 2, pp. 13–55
•   Ellis, M.B., & Ellis, J.P., (1997). Microfungi on land plants, an identification handbook (2nd ed.), Richmond Publishing Co., Slough.
•   Ing, B. (1990-91). articles in The Mycologist, 4 & 5.
•   Kirk, P.M., Cannon, P.F., Minter, D.W., & Stalpers, J.A., (eds.) (2008). Ainsworth & Bisby's Dictionary of the Fungi (10th ed.), CAB International, Wallingford.
•   Webster, J. (1980). Introduction to fungi (2nd ed.), Cambridge University Press, Cambridge.



© A.J. Silverside
Page first hosted at www-biol.paisley.ac.uk/bioref/, April 2001; revised and transferred to lastdragon.org, October 2010, substantially updated April 2015
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