The powdery mildews: a review of the world's most familiar (yet poorly known) plant pathogens.

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

[1]  Y. Homma ERYSIPHACEAE OF JAPAN , 1937 .

[2]  A. Jones,et al.  Analysis of factors affecting dispersal of Podosphaera leucotricha conidia. , 1979 .

[3]  D. Hibbett,et al.  Toward a phylogenetic classification of the leotiomycetes based on rDNA data. , 2006, Mycologia.

[4]  D. Walters,et al.  Polyamine metabolism in 'green-islands' on powdery mildew-infected barley leaves: possible interactions with senescence. , 1990, The New phytologist.

[5]  S. Takamatsu,et al.  Multilocus phylogenetic analyses within Blumeria graminis, a powdery mildew fungus of cereals. , 2007, Molecular phylogenetics and evolution.

[6]  J. Manners,et al.  Conidium liberation in Erysiphe graminis , 1971 .

[7]  S. Takamatsu,et al.  Phylogenetic structure of the genus Leveillula (Erysiphales: Erysiphaceae) inferred from the nucleotide sequences of the rDNA ITS region with special reference to the L. taurica species complex. , 2001 .

[8]  T. Nonomura,et al.  Formation of Conidial Pseudochains by Tomato Powdery Mildew Oidium neolycopersici. , 2006, Plant disease.

[9]  D. Glawe Synopsis of genera of Erysiphales (powdery mildew fungi) occurring in the Pacific Northwest , 2006 .

[10]  L. Prahm,et al.  Studies of Transport of Live Spores of Cereal Mildew and Rust Fungi across the North Sea , 1978 .

[11]  S. Takamatsu,et al.  Molecular and morphological characterization of Leveillula (Ascomycota: Erysiphales) on monocotyledonous plants. , 2007, Mycological research.

[12]  A. Rossman,et al.  Fungi on Plants and Plant Products in the United States , 1989 .

[13]  U. Braun,et al.  Phylogenetic relationships and generic affinity of Uncinula septata inferred from nuclear rDNA sequences , 2005 .

[14]  D. Roberts,et al.  Ultrastructure of the ungerminated conidium of Blumeria graminis f.sp. hordei , 1996 .

[15]  D. Spencer The Powdery mildews , 1979 .

[16]  Uwe Braun,et al.  The taxonomy of the powdery mildew fungi. , 2002 .

[17]  S. Takamatsu,et al.  Identification of two powdery mildew fungi, Oidium neolycopersici sp. nov. and O. lycopersici, infecting tomato in different parts of the world , 2001 .

[18]  C. C. Gordon A REINTERPRETATION OF THE ONTOGENY OF THE ASCOCARP OF SPECIES OF THE ERYSIPHACEAE , 1966 .

[19]  Joost A. Stalpers,et al.  Ainsworth and Bisby's dictionary of the fungi: 9th edition. , 1995 .

[20]  S. Takamatsu,et al.  Two Erysiphe species associated with recent outbreak of soybean powdery mildew: results of molecular phylogenetic analysis based on nuclear rDNA sequences , 2002 .

[21]  T. Gottwald,et al.  Environmental factors initiating liberation of conidia of powdery mildews , 1986 .

[22]  R. Barreto,et al.  Queirozia turbinata (Phyllactinieae, Erysiphaceae): a powdery mildew with a dematiaceous anamorph. , 2006, Mycological research.

[23]  G. Grove Meteorological Factors Affecting Airborne Conidia Concentrations and the Latent Period of Podosphaera clandestina on Sweet Cherry. , 1998, Plant disease.

[24]  S. Takamatsu,et al.  Evolution of host-parasite relationships of Golovinomyces (Ascomycete: Erysiphaceae) inferred from nuclear rDNA sequences. , 2003, Molecular phylogenetics and evolution.

[25]  Y. La,et al.  Morphology of edge lines of chained immature conidia on conidiophores in powdery mildew fungi and their taxonomic significance , 1993 .

[26]  S. Somerville,et al.  Powdery mildew of Arabidopsis: a model system for host-parasite interactions. , 2002 .

[27]  B. Henricot,et al.  Morphological and phylogenetic comparisons amongst powdery mildews on Catalpa in the UK. , 2006, Mycological research.

[28]  J. Rogers,et al.  First record and characterization of a powdery mildew on a member of the Juncaginaceae: Leveillula taurica on Triglochin maritima , 2005, Mycological progress.

[29]  R. Bélanger The Powdery Mildews: A Comprehensive Treatise , 2002 .

[30]  S. Takamatsu,et al.  Estimation of molecular clocks for ITS and 28S rDNA in Erysiphales , 2004 .

[31]  U. Braun,et al.  Phylogeny of Erysiphe, Microsphaera, Uncinula (Erysipheae) and Cystotheca, Podosphaera, Sphaerotheca (Cystotheceae) inferred from rDNA ITS sequences, some taxonomic consequences , 2000 .

[32]  Jennifer S. Falacy,et al.  Detection of Erysiphe necator in Air Samples Using the Polymerase Chain Reaction and Species-Specific Primers. , 2007, Phytopathology.

[33]  W. Bushnell,et al.  Epidemiology of powdery mildews in agricultural pathosystems. , 2002 .

[34]  James K. M. Brown,et al.  Genetic and forma specialis diversity in Blumeria graminis of cereals and its implications for host-pathogen co-evolution. , 2003, Molecular plant pathology.

[35]  G. Pelter,et al.  First Report of Powdery Mildew on Potato Caused by Leveillula taurica in North America , 2004 .

[36]  H. J. Boesewinkel The morphology of the imperfect states of powdery mildews (Erysiphaceae) , 1980, The Botanical Review.

[37]  H. Dörfelt,et al.  Studien zur Fruchtkörperentwicklung und Ultrastruktur von Sphaerotheca fusca (Ascomycetes/Erysiphales) , 1989 .

[38]  W. Bushnell,et al.  Localized induction of accessibility and inaccessibility by powdery mildew. , 2002 .

[39]  F. Dugan,et al.  First Report of Erysiphe (Uncinuliella) flexuosa in western North America , 2006 .

[40]  T. Nonomura,et al.  Consecutive monitoring for conidiogenesis by Oidium neolycopersici on tomato leaves with a high-fidelity digital microscope , 2004, Journal of General Plant Pathology.

[41]  A. Pérez-García,et al.  Multiple displacement amplification, a powerful tool for molecular genetic analysis of powdery mildew fungi , 2007, Current Genetics.

[42]  K. Amano Host Range and Geographical Distribution of the Powdery Mildew Fungi , 1990 .

[43]  D. Glawe First Report of Powdery Mildew of Platanus occidentalis caused by Microsphaera platani (Erysiphe platani) in Washington State , 2003 .

[44]  S. Takamatsu,et al.  Spread of the North American snowberry powdery mildew fungus, Erysiphe symphoricarpi (syn. Microsphaera symphoricarpi), to Europe , 2002 .

[45]  S. Takamatsu,et al.  PCR primers useful for nucleotide sequencing of rDNA of the powdery mildew fungi , 2001 .

[46]  W. Turechek,et al.  Development of Management Strategies for Hop Powdery Mildew in the Pacific Northwest , 2001 .

[47]  F. Dugan,et al.  Powdery Mildews on Weeds in the Pacific Northwest: A Miscellany of New Records , 2007 .

[48]  Phylogeny and taxonomy of powdery mildew fungi of Erysiphe sect. Uncinula on Carpinus species , 2006, Mycological Progress.

[49]  H H Edwards,et al.  Development of primary germ tubes by conidia of Blumeria graminis f.sp. hordei on leaf epidermal cells of Hordeum vulgare , 2002 .

[50]  A. J. Wright,et al.  Early adhesion of Blumeria graminis to plant and artificial surfaces demonstrated by centrifugation , 2002 .

[51]  Hitoshi Kunoh,et al.  Release and visualization of the extracellular matrix of conidia of Blumeria graminis , 1999 .

[52]  S. Takamatsu,et al.  A new subgenus, Microidium, of Oidium (Erysiphaceae) on Phyllanthus spp. , 2005 .

[53]  P. Beales,et al.  A Contribution to the Identity of Rhododendron Powdery Mildew in Europe , 2000 .

[54]  D. Gadoury,et al.  Initiation, development, dispersal, and survival of cleistothecia of Uncinula necator in New York vineyards. , 1988 .

[55]  B. Scholte,et al.  Dissemination of mildew spores in a glasshouse , 1983 .

[56]  B. Kendrick,et al.  The Fifth Kingdom , 1987 .

[57]  John W. Taylor,et al.  Phylogeny of the Erysiphales (powdery mildews) inferred from internal transcribed spacer ribosomal DNA sequences. , 1999 .

[58]  Canada.,et al.  The fungi of Ontario , 1960 .

[59]  B. Legg,et al.  Release of barley-mildew conidia from shaken leaves , 1976 .

[60]  C. Boyle,et al.  Haustorial Function During Development of Cleistothecia in Blumeria graminis f. sp. tritici. , 1998, Plant disease.

[61]  G. Celio,et al.  Conidial germination, infection structure formation, and early colony development of powdery mildew on poinsettia. , 1998, Phytopathology.

[62]  J. Webster Cleistocarps of Phyllactinia as shuttlecocks , 1979 .

[63]  D. Glawe Thomas j. Burrill, pioneer in plant pathology. , 1992, Annual review of phytopathology.

[64]  R. Stack,et al.  First report of powdery mildew on Caragana arborescens in Minnesota and North Dakota caused by Microsphaera (Erysiphe) palczewskii. , 2006 .

[65]  G. Durrieu,et al.  Spécificité parasitaire et systématique de quelques Leveillula (Erysiphaceae) , 1985 .

[66]  W. Turechek,et al.  Responding to an Introduced Pathogen: Podosphaera macularis (Hop Powdery Mildew) in the Pacific Northwest , 2003 .

[67]  M. Hausbeck,et al.  Factors Affecting Concentrations of Airborne Conidia of Oidium sp. Among Poinsettias in a Greenhouse. , 2000, Plant disease.

[68]  J. Manners,et al.  Conidium liberation in Erysiphe graminis: II. Conidial chain and pustule structure , 1973 .

[69]  U. Braun,et al.  Phylogeny and taxonomy of the oak powdery mildew Erysiphe alphitoides sensu lato. , 2007, Mycological research.

[70]  E. S. Salmon Notes on the Hop Mildew (Sphaerotheca humuli (DC.) Burr.) , 1907, The Journal of Agricultural Science.

[71]  T. Nonomura,et al.  Consecutive monitoring of lifelong production of conidia by individual conidiophores of Blumeria graminis f. sp. hordei on barley leaves by digital microscopic techniques with electrostatic micromanipulation. , 2006, Mycological research.

[72]  D. M. Turner Studies on cereal mildew in Britain , 1956 .

[73]  R. Heitefuss,et al.  Ultrastructural and Histochemical Studies on Mildew of Barley (Erysiphe graminis DC. F. sp. hordei Marchal).: I. The Cell Envelope of Conidia, Germ Tubes, and Appressoria , 1982 .

[74]  S. M. Pady Spore Release in Powdery Mildews , 1972 .

[75]  J. Parmelee The Fungi of Ontario. II. Erysiphaceae (mildews) , 1977 .

[76]  H. Dörfelt,et al.  Untersuchungen zur Sexualität und Fruchtkörperentwicklung der Echten Mehltaupilze (Erysiphales)*)*)Herrn Prof. Dr. habil. H. Kreisel (Greifswald) zum 65. Geburtstag gewidmet , 1996 .

[77]  U. Braun A monograph of the Erysiphales (powdery mildews) , 1987 .

[78]  J. Pittman,et al.  The Monosaccharide Transporter Gene, AtSTP4, and the Cell-Wall Invertase, Atβfruct1, Are Induced in Arabidopsis during Infection with the Fungal Biotroph Erysiphe cichoracearum1 , 2003, Plant Physiology.

[79]  A. Gargas,et al.  18S rRNA gene sequences and supraordinal classification of the Erysiphales , 1994 .

[80]  G. Grove Perennation of Uncinula necator in Vineyards of Eastern Washington. , 2004, Plant disease.

[81]  C. M. Leach,et al.  Leaf surface electrostatics: behavior of detached leaves of beans, maize, and other plants under natural conditions , 1984 .

[82]  R. Forster Powdery mildew of greenhouse cucumbers and tomatoes caused by Leveillula taurica in Idaho. , 1989 .

[83]  O. S. Peries Studies on strawberry mildew, caused by Sphaerotheca macularis (Wallr. ex Fries) Jaczewski* , 1962 .

[84]  S. Takamatsu,et al.  Molecular phylogeny and evolution of the maple powdery mildew (Sawadaea, Erysiphaceae) inferred from nuclear rDNA sequences. , 2005, Mycological research.

[85]  S. Takamatsu,et al.  Molecular phylogeny supports a Northern Hemisphere origin of Golovinomyces (Ascomycota: Erysiphales). , 2006, Mycological research.

[86]  D. Gadoury,et al.  Ascocarp dehiscence and ascospore discharge in Uncinula necator , 1990 .

[87]  R. Heitefuss,et al.  Ultrastructural and Histochemical Studies on Mildew of Barley (Erysiphe graminis DC. f. sp. hordei Marchal) , 1982 .

[88]  S. Blumer Echte Mehltaupilze (Erysiphaceae) : ein Bestimmungsbuch für die in Europa vorkommenden Arten , 1967 .

[89]  W. Schnathorst Environmental Relationships in the Powdery Mildews , 1965 .

[90]  Pari Skamnioti,et al.  Of genes and genomes, needles and haystacks: Blumeria graminis and functionality. , 2005, Molecular plant pathology.

[91]  S. Takamatsu,et al.  Identification of individual powdery mildew fungi infecting leaves and direct detection of gene expression by single conidium polymerase chain reaction. , 2005, Phytopathology.

[92]  J. Cunnington,et al.  Genetic variation within Podosphaera tridactyla reveals a paraphyletic species complex with biological specialization towards specific Prunus subgenera. , 2005, Mycological research.

[93]  M. Kohno,et al.  Are Primary Germ Tubes of Conidia Unique to Erysiphe graminis , 1979 .

[94]  H. Kreisel,et al.  Chronology of Phytoparasitic Fungi Introduced to Germany and Adjacent Countries , 1994 .

[95]  M. Lyngkjær,et al.  Epidermal cell papillae , 2002 .

[96]  G. Newcombe,et al.  First Report of Powdery Mildew (Microsphaera palczewskii) on Siberian Pea Tree (Caragana arborescens) in North America. , 2003, Plant disease.

[97]  James K. M. Brown,et al.  Comparative genetics of avirulence and fungicide resistance in the powdery mildew fungi. , 2002 .

[98]  J. B. Ellis,et al.  The North American Pyrenomycetes. , 1892 .

[99]  S. Takamatsu,et al.  Erysiphe wadae: a new species of Erysiphe sect. Uncinula on Japanese beech , 2003 .

[100]  W. Gubler,et al.  Susceptibility of grapevine buds to infection by powdery mildew Erysiphe necator , 2005 .

[101]  U. Braun,et al.  A morphologically ill-founded powdery mildew species, Pleochaeta indica, is recognized as a phylogenetic species based on the analysis of the nuclear ribosomal DNA sequences. , 2006, Mycological research.

[102]  E. Gäumann,et al.  Comparative morphology of Fungi , 1926 .

[103]  W. Bushnell,et al.  The formation and function of infection and feeding structures. , 2002 .

[104]  David L. Hawksworth,et al.  Ainsworth & Bisby's Dictionary of the Fungi , 1972 .

[105]  U. Braun,et al.  Caespitotheca gen. nov., an ancestral genus in the Erysiphales. , 2005, Mycological research.

[106]  K. Hammett Taxonomy of Erysiphaceae in New Zealand , 1977 .

[107]  S. Takamatsu Phylogeny and evolution of the powdery mildew fungi (Erysiphales, Ascomycota) inferred from nuclear ribosomal DNA sequences , 2004 .

[108]  R. Cook,et al.  Identification and classification of powdery mildew anamorphs using light and scanning electron microscopy and host range data , 1997 .

[109]  Y. Mäkinen,et al.  The invasion history of Microsphaera palczewskii (Erysiphales) in Finland , 2001 .

[110]  Introduction to Fungi , 1970 .