Powdery Mildews

Abstract

Powdery mildews are an important group of parasitic fungi causing disease in over 7600 species of host plants. They are obligate biotrophic parasites, obtaining their nutrients from the host through intracellular feeding structures known as haustoria. Many species of powdery mildews have a high degree of host specialization, infecting only one or a few closely related host genera. Some powdery mildews have well‐documented gene‐for‐gene (GFG) resistance interactions with their host plant, revealing information about the nature of host specificity. This article focuses on the interactions between powdery mildews and the host plant. Events in the establishment of haustoria and biotrophy are reviewed and their influence of infection on host metabolism described. GFG, durable mlo and nonhost‐resistance mechanisms are also described.

Key Concepts

  • Importance of powdery mildews: Powdery mildews are extremely successful fungal parasites. Over 700 species have been described infecting over 7600 species of host plants, many of which are important crops species. Chemicals (fungicides) and resistance genes are used against them, but powdery mildews have the ability to rapidly adapt and defeat these control measures.

  • Obligate biotrophy: All powdery mildews are obligate biotrophs, requiring a living host to grow and reproduce.

  • Haustoria: The feeding structures produced by powdery mildews to obtain nutrients from epidermal cells of the host plants.

  • Host specificity: Many powdery mildews have a high degree of host specialization, and can only grow on one or a few closely related plant genera. Infection can even be restricted to single genotypes of a specific host, as typified by gene‐for‐gene (GFG) resistance.

  • GFG resistance: GFG resistance has been extensively investigated in the interaction between barley powdery mildew (Blumeria graminis f. sp. hordei) and the host plant, barley. In GFG resistance, an avirulence (avr) gene in the parasite matches a resistance (R) gene in the host causing a recognition event that triggers defence responses and prevents infection by the parasite. If either the avr gene or the R gene is lacking, the parasite is not recognized and can become established as a parasite. In barley, over 85 powdery mildew R genes have been described, and over 25 avr gene loci have been mapped in Bgh.

  • mlo resistance: A loss‐of‐function mutation in the barley MLO protein results in failure of Bgh to establish a successful infection.mlo resistance has been widely used in barley breeding, and has so far proved to be durable.

  • Nonhost resistance: Plants are resistant to most invading pathogens, a feature described as nonhost resistance (NHR). Only those adapted microbes that are able to overcome this NHR are able to infect and become pathogens. The extreme specificity of some powdery mildew/host interactions has enabled investigation into the basis of NHR. A series of penArabidopsis mutants with enhanced penetration by nonadapted Bgh have been defined. Genes coding for pen1‐pen3 have been identified, enabling key proteins required for NHR to be identified.

Keywords: powdery mildew; haustoria; gene‐for‐gene resistance; mlo resistance; nonhost resistance

Figure 1.

(a) Lifecycle of powdery mildews. Infection of host plants during the growing season is from wind‐dispersed asexual conidiospores produced abundantly on leaves and other aerial parts of plants. Many powdery mildews have a sexual phase resulting in the formation of ascospores within a cleistothecium, a closed spherical ascocarp. Many powdery mildews, including Erysiphe cichoracearum, do not have a sexual stage. (b) Cleistothecium from Podosphaeria fusca on the surface of courgette (zucchini) plant (left) and squashed to reveal an ascus and eight ascospores contained inside (right). Photographs reproduced by permission of Alejandro Pérez, University of Malaga.

Figure 2.

Host and nonhost interactions with Blumeria graminis f. sp. hordei: (a)–(b) Nonhost interactions. (a) Germination of Bgh spore on Arabidopsis 72 h after inoculation showing appressorium (Ap), cell wall apposition (CWA) and associated vesicles (V) stained brown with 3,3‐diaminobenzidine for hydrogen peroxide. Contact points beneath the primary germ tube (PGT) and an Appressorial lobe (Apl) also stain for hydrogen peroxide. (b) Accumulation of PEN2‐GFP‐TM (green) at the attempted penetration point of Bgh approximately 14 hpi on the Arabidopsis leaf surface. The fungus is stained with the organic dye FM 4‐64 form (red). (c) Successful infection of Bgh on barley showing the formation of haustoria in epidermal cells. Photographs are reproduced by permission of (a) Ralph Hückelhoven, Technical University of Munich and (b) Rene Fuchs, The Sainsbury Laboratory and (c) Pietro Spanu, Imperial College London.

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Further Reading

Bélanger RR, Bushnell WR, Dik AJ and Carver TLW (eds) (2002) The Powdery Mildews: A Comprehensive Treatise. St. Paul, MN. This detailed book provides a thorough review of all aspects of powdery mildew biology, epidemiology and control. American Phytopathological Society.

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Cherewick WJ (1944) Studies on the biology of Erysiphe graminis DC. Canadian Journal of Research 22: 52–86. Interesting historic paper that is as valid today as it was when first published.

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O'Connell RJ and Panstruga R (2006) Tete a tete inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytologist 171(4): 699–718.

Shirasu K and Schulze‐Lefert P (2000) Regulators of cell death in disease resistance. Plant Molecular Biology 44: 371–385 This review provide an overview of the functioning of molecular chaperones in resistance protein function.

Thordal‐Christensen H, Zhang ZG, Wei YD and Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley–powdery mildew interaction. Plant Journal 11: 1187–1194.

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Web Links

Blumeria graminis sequencing project website. http://www.blugen.org/. For access to the genome sequence and stage‐specific cDNA sequence libraries.

Home Grown Cereals Authority, UK. www.hgca.com. Provides current information about the control of powdery mildew, and a link to the encyclopedia of Cereal Diseases.

Plant Disease Control: Oregon State University. http://plant‐disease.ippc.orst.edu/index.cfm. This searchable website provides detail on the symptoms and control of powdery mildews in North America.

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Ridout, Christopher James(Sep 2009) Powdery Mildews. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021263]