Skip to main content
Log in

Phylogeny and taxonomy of Golovinomyces orontii revisited

  • Original Article
  • Published:
Mycological Progress Aims and scope Submit manuscript

Abstract

Golovinomyces orontii is a common plurivorous powdery mildew species with wide host range and worldwide distribution, usually occurring as asexual morph. Ascomata (chasmothecia) are rarely formed on most hosts. Phylogenetic analyses based on rDNA ITS and 28S rDNA data of a wide range of powdery mildew collections of G. orontii s. lat. suggested a high degree of genetic heterogeneity of this species, which is undoubtedly not monophyletic. This study revealed that sequences retrieved from numerous collections referred to as G. orontii (s. lat.) split into three distinct main clusters, previously classified as groups 1 to 3. These groups have been genetically and morphologically analyzed, circumscribed, and named. One cluster (group 2), including a sequence retrieved from powdery mildew on the type host of Erysiphe orontii, Misopates orontium, constitutes G. orontii s. str. G. tabaci comb. nov. (≡ E. tabaci) is introduced for the second cluster in group 1 that is genetically and morphologically clearly distinct from G. orontii s. str. The third assemblage of sequences (group 3) comprises powdery mildews on hosts of the composite tribe Cichorieae, including Cichorium and Lactuca spp., and a wide range of hosts belonging to various other plant families for which the name G. bolayi sp. nov. is proposed. Euoidium longipes and Euoidium lycopersici, two additional powdery mildew species on solanaceous hosts, are briefly discussed and, based on previous phylogenetic analyses, reallocated to Golovinomyces. Oidium lactucae-debilis on Ixeris japonica in Asia is tentatively reduced to synonymy with G. sonchicola, i.e., it does not pertain to the G. orontii s. lat. complex. G. orontii s. lat. on Vinca spp. (Apocynaceae), mostly known as asexual morph, represents a separate species only distantly related to G. orontii s. str., which is described herein as Golovinomyces vincae sp. nov. Some re-examined collections on Vinca major from Germany misidentified as G. orontii turned out to belong to Ramularia vincae and represent first records of this species for Germany. Golovinomyces spadiceus is a further plurivorous Golovinomyces species discussed in this work, which, however, does not belong to the G. orontii complex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Adam L, Ellwood S, Wilson I, Saenz G, Xiao S, Oliver RP, Turner JG, Somerville S (1999) Comparison of Erysiphe cichoracearum and E. cruciferarum and a survey of 360 Arabidopsis thaliana accessions for resistance to these two powdery mildew pathogens. Mol Plant-Microbe Interact 12:1031–1043

    Article  PubMed  CAS  Google Scholar 

  • Almarza MD (2009) Determinacion de especies de los Generos Erysiphe y Alternaria que afectan el cultivo de achicoria (Cichorium intybus L. var. sativum Biskoff) en Chile. Dissertation, Universidad Austral de Chile

  • Amano (Hirata) K (1986) Host range and geographical distribution of the powdery mildew fungi. Japan Scientific Societies Press, Tokyo, 741 pp

    Google Scholar 

  • Bappammal M, Hosagoudar VB, Udaiyan K (1995) Powdery mildews of Tamil Nadu, India. New Botanist, Int Quart J Pl Sci Res 22:81–175

    Google Scholar 

  • Bensch K, Groenewald JZ, Dijksterhuis J, Starink-Willemse M, Andersen B, Summerell BA, Shin HD, Dugan FH, Schroers H-J, Braun U, Crous PW (2010) Species and ecological diversity within the Cladosporium cladosporioides complex (Davidiellaceae, Capnodiales). Stud Mycol 67:1–96

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bensch K, Braun U, Groenewald JZ, Crous PW (2012) The genus Cladosporium. Stud Mycol 72:1–401

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Blumer S (1933) Die Erysiphaceen Mitteleuropas unter besonderer Berücksichtigung der Schweiz. Beiträge zur Kryptogamenflora der Schweiz 7:1–483

    Google Scholar 

  • Blumer S (1952) Beiträge zur Spezialisierung der Erysiphaceen. Ber Schweiz Bot Ges 62:384–401

    Google Scholar 

  • Blumer S (1967) Echte Mehltaupilze (Erysiphaceae). G. Fischer, Jena, 436 pp

  • Bolay A (2005) Les Oïdiums de Suisse (Erysiphacées). Cryptog Helv 20:1–173

    Google Scholar 

  • Bradshaw M, Braun U, Götz M, Meeboon J, Takamatsu S (2017) Powdery mildew of Chrysanthemum × morifolium: phylogeny and taxonomy in the context of Golovinomyces species on Asteraceae hosts. Mycologia 109:508–519

    Article  PubMed  Google Scholar 

  • Braun U (1978) Beitrag zur Systematik und Nomenklatur der Erysiphales. Feddes Repert 88:655–665

    Article  Google Scholar 

  • Braun U (1980) Morphological studies in the genus Oidium. Flora 170:77–90

    Article  Google Scholar 

  • Braun U (1987) A monograph of the Erysiphales (powdery mildews). Nova Hedwigia Beih 89:1–700

    Google Scholar 

  • Braun U (1998) Neufunde Echter Mehltaupilze (Erysiphales) aus der BR Deutschland. Schlechtendalia 1:31–40

    Google Scholar 

  • Braun U (2012) The impact of the discontinuation of dual nomenclature of pleomoprhic fungi: the trivial facts, problems, and strategies. IMA Fungus 3:81–86

    Article  PubMed  PubMed Central  Google Scholar 

  • Braun U (2013) (2210-2232) Proposals to conserve the teleomorph-typified name Blumeria against the anamorph-typified name Oidium and twenty-two teleomorph-typified powdery mildew species names against competing anamorph-typified names (Ascomycota: Erysiphaceae). Taxon 62:1328–1331

    Article  Google Scholar 

  • Braun U, Cook RTA (2012) Taxonomic manual of the Erysiphales (powdery mildews). CBS Biodiversity Series 11:1–707

    Google Scholar 

  • Braun U, Nakashima C, Crous PW, Groenewald JZ, Moreno-Rico O, Rooney-Latham S, Blomquist CL, Haas J, Marmolejo J (2018) Phylogeny and taxonomy of the genus Tubakia s. lat. Fungal Syst Evol 1:41–99

    Article  Google Scholar 

  • Bresinski A (2016) Echte Mehltaupilze (Erysiphales) in Bayern – eine vorläufige Übersicht. Ber Bayer Bot Ges 86:163–212

    Google Scholar 

  • Cabral CS, Santos MDM, Borges RCF, Fonseca MEN, Reis A, Boiteux LS (2017) Lettuce powdery mildew caused by Golovinomyces orontii in Brazil. Anais do 50° Congresso Brasileiro de Fitopatologia: 0750

  • Castagne L (1851) Supplément au catalogue des plantes qui croissent naturellement aux environs de Marseille. Nicot et Pardignon, Aix, 125 pp

  • Cho SE, Choi YJ, Han KS, Park MJ, Shin HD (2016) First report of powdery mildew caused by Golovinomyces orontii on Lactuca sativa in Korea. Pl Dis 100:1015

    Article  Google Scholar 

  • Cho SE, Lee SH, Lee SK, Seo ST, Shin HD (2018) Erysiphe alphitoides causes powdery mildew on Eucalyptus gunnii. Forest Pathol 48:e12377

    Article  Google Scholar 

  • Cho SE, Park MJ, Park JH, Han KS, Shin HD (2012) First report of Golovinomyces cichoracearum associated with powdery mildew on Helianthus tuberosus in Korea. Australas Pl Dis Notes 7:35–37

    Article  Google Scholar 

  • Cho SE, Park JH, Park MJ, Shin HD (2011) First report of powdery mildew caused by Golovinomyces ambrosiae on Ambrosia trifida in Korea. Pl Dis 95:1480

    Article  CAS  Google Scholar 

  • Choi IY, Hong SH, Cho SE, Zhao TT, Shin HD (2018) First report of powdery mildew caused by Golovinomyces orontii on common poppy in Korea. Pl Dis 102:244

    Article  Google Scholar 

  • Choi JK, Kim BS, Hong SH, Cho SE, Shin HD (2014) First report of powdery mildew caused by Golovinomyces sonchicola on Ixeris chinensis in Korea. Pl Dis 98:999

    Article  CAS  Google Scholar 

  • Cook RTA, Braun U (2009) Conidial germination patterns in powdery mildews. Mycol Res 113:616–636

    Article  PubMed  CAS  Google Scholar 

  • Cunnington JH, Lawrie SC, Pascoe IG (2010) Genetic characterization of the Golovinomyces cichoracearum complex in Australia. Pl Pathol 59:158–164

    Article  Google Scholar 

  • Cunnington JH, Lawrie AC, Pascoe IG (2005) Molecular identification of Golovinomyces (Ascomycota: Erysiphales) anamorphs on Solanaceae in Australia. Australas Pl Pathol 34:51–55

    Article  CAS  Google Scholar 

  • Cunnington JH, Takamatsu S, Lawrie AC, Pascoe IG (2003) Molecular identification of anamorphic powdery mildew fungi. Australas Pl Pathol 32:421–428

    Article  CAS  Google Scholar 

  • Delhey R, Braun U, Kiehr M (2003) Some new records of powdery mildew fungi from Argentina (2). Schlechtendalia 10:79–90

    Google Scholar 

  • Deslandes JA (1954) Studies and observations on lettuce powdery mildew. Pl Dis Reporter 38:560–562

    Google Scholar 

  • Dowling M, Schnabel G, Williamsson M (2016) First report of powdery mildew caused by Golovinomyces orontii (Erysiphe orontii) on Vinca major in South Carolina. Pl Dis 100:218

    Article  Google Scholar 

  • Dugan FM (2013) Golovinomyces spadiceus causing powdery mildew on Coreopsis hybrid ‘Full Moon’ (Heliantheae, Asteraceae) in Washington State. N Amer Fungi 8:1–3

    Article  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenetics: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Garibaldi A, Bertetti D, Frati S, Gullino ML (2008) First report of powdery mildew caused by Golovinomyces cichoracearum on orange coneflower (Rudbeckia fulgida) in Italy. Pl Dis 92:975

    Article  CAS  Google Scholar 

  • Garibaldi A, Bertetti D, Poli A, Gullino ML (2012) Powdery mildew caused by Golovinomyces orontii on creeping bellflower (Campanula rapunculoides) in Italy. Pl Dis 96:291

    Article  CAS  Google Scholar 

  • Gevens AJ, Maia G, Jordan SA (2009) First report of powdery mildew caused by Golovinomyces cichoracearum on Crotalaria juncea (Tropic Sun Sunn hemp). Pl Dis 93:427

    Article  CAS  Google Scholar 

  • Glawe DA, Koike ST (2008) First report of powdery mildew of periwinkle caused by Golovinomyces orontii in North America. Pl Health Progr. https://doi.org/10.1094/PHP-2008-1212-03-BR

  • Gorter GJMA, Eicker A (1984) New South African records of Erysiphaceae from Transvaal. S Afr J Bot 50:38–42

    Article  Google Scholar 

  • Grigaliūnaitė B (1997) Lietuvos grybai, III, Milteniečiai 1 (Erysiphales). Mokslo ir Enciklopedijų Leidybos Institutas, Vilnius, 195 pp

  • Groenewald JZ, Nakashima C, Nishikawa J, Shin HD, Park JH, Jama AN, Groenewald M, Braun U, Crous PW (2013) Species concepts in Cercospora: spotting the weeds among the roses. Stud Mycol 75:115–170

    Article  PubMed  CAS  Google Scholar 

  • Hammarlund C (1945) Beiträge zur Revision einiger imperfekter Mehltau-Arten. Erysiphe polyphaga nov. sp. Bot Not 1945:101–108

  • Hammett KRW (1977) Taxonomy of the Erysiphaceae in New Zealand. New Zealand J Bot 15:687–711

    Article  Google Scholar 

  • Han KS, Zhao TT, Cho SE, Shin HD (2018) First report of powdery mildew caused by Golovinomyces ambrosiae on Brachyscome multifida in Korea. Pl Dis 102:1851

    Article  Google Scholar 

  • Heluta VP (1988a) Filogeneticheskie vzaimosvyazi mezhdu rodami erizifal’nykh gribov i nekotorye voprosy sistematika poryadka Erysiphales. Biol Zhurn Armenii 41:351–358

    Google Scholar 

  • Heluta VP (1988b) Novi taksonomichni kombinatsyyi v rodini Erysiphaceae. Ukrayins’k Bot Zhurn 45:62–63

    Google Scholar 

  • Heluta VP, Korytnyanska VG (2011) Golovinomyces greeneanus (U. Braun) Heluta (Erysiphales) – novij dla Ukraini vid boroshnistorosyanikh gribyv. Ukrayins’k Bot Zhurn 68:773–779

    Google Scholar 

  • Hosagoudar VB, Agarwal DK (2009) Powdery mildews of India—check list. Associated Publishing Company, New Delhi 106 pp

    Google Scholar 

  • Jaczewski AA (1927) Karmanny opredelitel’ gribov. Vyp. 2. Muchnisto-rosyanye griby. Mikologicheskaya Laboratoriya Imeni Professora A.A. Jaczewskogo, Gosudarstvennogo Instituta Opytnoy Agronomii, Leningrad, 626 pp

  • Jage H, Klenke F, Kummer V (2010) Neufunde und bemerkenswerte Bestätigungen von phytoparasitischen Kleinpilzen in Deutschland – Erysiphales (Echte Mehltaupilze). Schlechtendalia 21:1–140

    Google Scholar 

  • Khodoparast SA (2016) Molecular identification of some anamorphic powdery mildews (Erysiphales) in Guilan province, north of Iran. Mycol Iran 3:127–133

    Google Scholar 

  • Kiss L (1994) Erysiphe cichoracearum DC. on Begonia tuberhybrida in Hungary. Acta Phytopathol Entomol Hung 19:57–59

    Google Scholar 

  • Kiss L, Cook RTA, Saenz GS, Cunnington JH, Takamatsu S, Pascoe I, Bardin MB, Nicot PC, Sato Y, Rossman AY (2001) Identification of two powdery mildew fungi, Oidium neolycopersici sp. nov. and O. lycopersici, infecting tomato in different parts of the world. Mycol Res 105:684–697

    Article  Google Scholar 

  • Kiss L, Jankovics T, Kovacs GM, Daughtrey ML (2008) Oidium longipes, a new powdery mildew fungus on petunia in the USA: a potential threat to ornamental and vegetable solanaceous crops. Pl Dis 92:818–825

    Article  CAS  Google Scholar 

  • Kiss L, Stuart K, Grigg J, Calvert J, Dearnaley JDW (2018) First report of powdery mildew on goji berry (Lycium barbarum) caused by Arthrocladiella mougeotii in Queensland, Australia. Pl Dis 102:446

    Article  Google Scholar 

  • Koike ST, Saenz GS (1996) Occurrence of powdery mildew, caused by Erysiphe cichoracearum, on endive and radicchio in California. Pl Dis 80:1080

    Article  Google Scholar 

  • Kovács GM, Jankovics T, Kiss L (2011) Variation in the nrDNA ITS sequences of some powdery mildew species: do routine molecular identification procedures hide valuable information? Eur J Pl Pathol 131:135–141

    Article  Google Scholar 

  • Kumar S, Steche G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  PubMed  CAS  Google Scholar 

  • Lebeda A, Buczkowski J (1986) Occurrence of Erysiphe cichoracearum perithecia on wild Lactuca species. J Phytopathol 115:21–28

    Article  Google Scholar 

  • Lebeda A, Mieslerová B (2011) Taxonomy, distribution and biology of lettuce powdery mildew (Golovinomyces cichoracearum sensu stricto). Plant Pathol 60:400–415

    Article  Google Scholar 

  • Lebeda A, Doležalová I, Feráková V, Astley D (2004) Geographical distribution of wild Lactuca species (Asteraceae, Lactuceae). Bot Rev 70:328–356

    Article  Google Scholar 

  • Lebeda A, Doležalová I, Novotná A (2012a) Wild and weedy Lactuca species, their distribution, ecogeography and ecobiology in USA and Canada. Genet Resour Crop Evol 59:1805–1822

    Article  Google Scholar 

  • Lebeda A, Mieslerová B, Petrželová I, Korbelová P, Česneková E (2012b) Patterns of virulence variation in the interaction between Lactuca spp. and lettuce powdery mildew (Golovinomyces cichoracearum). Fungal Ecol 5:670–682

    Article  Google Scholar 

  • Lebeda A, Mieslerová B, Petrželová I, Korbelová P (2013) Host specificity and virulence variation in populations of lettuce powdery mildew pathogen (Golovinomyces cichoracearum s. str.) from prickly lettuce (Lactuca serriola). Mycol Progr 12:533–545

    Article  Google Scholar 

  • Matsuda S, Takamatsu S (2003) Evolution of host–parasite relationship of Golovinomyces (Ascomycota: Erysiphaceae) inferred from nuclear rDNA sequences. Mol Phylogenet Evol 27:314–327

    Article  PubMed  CAS  Google Scholar 

  • Meeboon J, Kokaew J, Takamatsu S (2018) Notes on powdery mildews (Erysiphales) from Thailand. V. Golovinomyces. Trop Pl Pathol 43:202–217

    Article  Google Scholar 

  • Mirhosseini H, Babaeizad V, Hashemi L, Basavand E (2015) Powdery mildew caused by Golovinomyces cichoracearum on Conyzanthus squamatus in Iran. J Pl Pathol 97:209

    Google Scholar 

  • Moparthi S, Bradshaw M, Frost K, Hamm PG, Buck JW (2018a) First report of powdery mildew caused by Golovinomyces spadiceus on okra in the United States. Pl Dis 102:1664

    Article  Google Scholar 

  • Moparthi S, Bradshaw M, Grove GG (2018b) First report of powdery mildew caused by Golovinomyces spadiceus on Helianthus annuus. Pl Dis 102:1176

    Article  Google Scholar 

  • Mori Y, Sato Y, Takamatsu S (2000) Evolutionary analysis of the powdery mildew fungi nucleotide sequences of the nuclear ribosomal DNA. Mycologia 92:74–93

    Article  CAS  Google Scholar 

  • Mork EK, Kristiansen K, Jorgensen HJL, Sundelin T (2011) First report of Golovinomyces cichoracearum as the causal agent of powdery mildew on Symphyotrichum novi-belgii (synonym Aster novi-belgii) in Denmark. Pl Dis 95:228

    Article  CAS  Google Scholar 

  • Nomura Y (1997) Taxonomical study of Erysiphaceae of Japan. Yokendo, Tokyo 281 pp

    Google Scholar 

  • Park MJ, Han KS, Hong SB, Shin HD (2010) Powdery mildew of Inula britannica var. chinensis in Korea. Pl Pathol J 26:99

    Article  Google Scholar 

  • Park MJ, Hong SH, Cho SE, Park JH, Shin HD (2015a) First report of powdery mildew caused by Golovinomyces orontii on invasive weed Lactuca serriola in Korea. Pl Dis 99:889

    Article  Google Scholar 

  • Park MJ, Kim BS, Choi IY, Cho SE, Shin HD (2015b) First report of powdery mildew caused by Golovinomyces ambrosiae on sunflower in Korea. Pl Dis 99:557

    Article  Google Scholar 

  • Pei DL, Zhu XQ, Xu YY, Li CW (2017a) First report of powdery mildew of strawberry (Fragaria ×ananassa) caused by Golovinomyces orontii in China. Pl Dis 101:506

    Article  Google Scholar 

  • Pei DL, Zhu XQ, Xu YY, Li CW (2017b) First report of powdery mildew caused by Golovinomyces orontii on Galium aparine in China. Pl Dis 101:251

    Article  Google Scholar 

  • Pintye A, Legler SE, Kiss L (2011) New records of microcyclic conidiogenesis in some powdery mildew fungi. Mycoscience 52:213–216

    Article  Google Scholar 

  • Pirondi A, Kitner M, Iotti M, Sedláková B, Lebeda A, Collina M (2016) Genetic structure and phylogeny of Italian and Czech populations of the cucurbit powdery mildew fungus Golovinomyces orontii inferred by Multilocus Sequence Typing. Pl Pathol 65:959–967

    Article  Google Scholar 

  • Plotnikova JM, Reuber TL, Ausubel FM, Pfister D (1998) Powdery mildew pathogenesis of Arabidopsis thaliana. Mycologia 90:1009–1016

    Article  Google Scholar 

  • Puttemans A (1911) Nouvelles maladies de plantes cultivées. Bull Soc Roy Bot Belgique 48:235–247

    Google Scholar 

  • Qiu PL, Nguyen V, Guan GX, Takamatsu S, Liu SY (2018) Occurrence of powdery mildew caused by Golovinomyces orontii on Lactuca sativa var. ramosa (lettuce) in China. Crop Protect 110:108–111

    Article  Google Scholar 

  • Radisek S, Jakse J, Zhao TT, Cho SE, Shin HD (2018) First report of powdery mildew of Capsella bursa-pastoris caused by Golovinomyces orontii in Slovenia. J Pl Pathol 100:359

    Article  Google Scholar 

  • Reed GM (1908a) Infection experiments with the mildew of cucurbits. Trans Wisconsin Acad Sci 15:527–547

    Google Scholar 

  • Reed GM (1908b) Infection experiments with Erysiphe cichoracearum. Bull Univ Wisconsin 3:327–416

    Google Scholar 

  • Rusanov VA, Bulgakov TS (2008) Powdery mildew of Rostov region. Mikol Fitopatol 42:314–322

    Google Scholar 

  • Saenz GS, Taylor JW (1999) Phylogeny of the Erysiphales (powdery mildews) inferred from internal transcribed spacer ribosomal DNA sequences. Canad J Bot 77:150–168

    Article  CAS  Google Scholar 

  • Salmon E (1900) A monograph of the Erysiphaceae. Mem Torrey Bot Club 9:1–292

    Google Scholar 

  • Sawada K (1927) Classification of the genus Erysiphe from Taiwan based on conidial stages. Bull Dept Agric Gov Res Inst Formosa 24:1–55

    Google Scholar 

  • Schmitt JA (1955) The host specialization of Erysiphe cichoracearum from Zinnia, Phlox and cucurbits. Mycologia 47:688–701

    Article  Google Scholar 

  • Schnathorst WC (1959) Heterothallism in the lettuce strain of Erysiphe cichoracearum. Mycologia 51:708–711

    Article  Google Scholar 

  • Schnathorst WC, Grocan RG, Bardin R (1958) Distribution, host range and origin of lettuce powdery mildew. Phytopathology 48:538–543

    Google Scholar 

  • Seijo TE, Czarnecki D, Deng Z, Peres NA (2006) First report of powdery mildew caused by Golovinomyces cichoracearum on Coreopsis leavenworthii. Pl Health Progr. https://doi.org/10.1094/PHP-2006-1214-01-BR

  • Shin HD (1988) Erysiphaceae of Korea. Thesis, Department of Agricultural Biology, Graduate School of Seoul National University, 305 pp

  • Shin HD (2000). Erysiphaceae of Korea [Plant pathogens of Korea 1]. National Institute of Agricultural Science and Technology, Suwon, 320 pp

  • Shin HD, Kim WB (1997) Fungal diseases of Capsella bursa-pastoris in Korea. Kor J Pl Resour 10:360–368

    Google Scholar 

  • Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337

    Article  Google Scholar 

  • Soylu S, Cho SE, Shin HD (2011) First report of powdery mildew caused by Golovinomyces cichoracearum on Zinnia elegans in Turkey. Pl Dis 95:1317

    Article  CAS  Google Scholar 

  • Stone OM (1962) Alternate hosts of cucumber powdery mildew. Ann Appl Biol 50:203–210

    Article  Google Scholar 

  • Swiderska U, Wolczanska A, Kozlowska M, Mułenko W, Mamczarz M (2005) Recent collections of powdery mildews (Erysiphales) in Poland. Acta Mycol 40:49–61

    Article  Google Scholar 

  • Swofford DL (2002) PAUP: phylogenetic analysis using parsimony (and other methods) 4.0b10. Sinauer, Sunderland

  • Takamatsu S, Heluta V, Havrylenko M, Divarangkoon R (2009) Four powdery mildew species with catenate conidia infect Galium: molecular and morphological evidence. Mycol Res 113:117–129

    Article  PubMed  Google Scholar 

  • Takamatsu S, Hirata T, Sato Y (1998) Phylogenetic analysis and predicted secondary structures of the rDNA internal transcribed spacers of the powdery mildew fungi (Erysiphaceae). Mycoscience 39:441–453

    Article  CAS  Google Scholar 

  • Takamatsu S, Matsuda S, Grigaliūnaitė B (2013) Comprehensive phylogenetic analysis of the genus Golovinomyces (Ascomycota: Erysiphales) reveals close evolutionary relationships with its host plants. Mycologia 105:1135–1152

    Article  PubMed  CAS  Google Scholar 

  • Takamatsu S, Matsuda S, Niinomi S, Havrylenko M (2006) Molecular phylogeny supports a Northern Hemisphere origin of Golovinomyces (Ascomycota: Erysiphales). Mycol Res 110:1093–1101

    Article  PubMed  CAS  Google Scholar 

  • Trigiano RN, Bernard EC, Hadziabdic D, Dattilo AJ, Wadl PA (2016) First report of powdery mildew on whorled sunflower (Helianthus verticillatus) caused by Golovinomyces ambrosiae. Pl Dis 100:1017

    Article  Google Scholar 

  • Trigiano RN, Bogges SL, Bernard EC (2018) First report of powdery mildew caused by Golovinomyces spadiceus on green and gold (Chrysopogon virginianum) in the United States. Pl Dis 102:252

    Google Scholar 

  • Troisi M, Bertetti D, Garibaldi A, Gullino ML (2010) First report of powdery mildew caused by Golovinomyces cichoracearum on gerbera (Gerbera jamesonii) in Italy. Pl Dis 94:130

    Article  CAS  Google Scholar 

  • Uchida K, Takamatsu S, Matsuda S, So K, Sato Y (2009) Morphological and molecular characterization of Oidium subgenus Reticuloidium (powdery mildew) newly occurred on cucumber in Japan. J Gen Pl Pathol 75:92–100

    Article  Google Scholar 

  • Utkhede RS, Koch CA, Menzies JG, Ehret DL (2001) Host range of a powdery mildew (Erysiphe orontii) on tomato. Can J Pl Sci 81:179–182

    Article  Google Scholar 

  • Vági P, Kovács GM, Kiss L (2007) Host range expansion in a powdery mildew fungus (Golovinomyces sp.) infecting Arabidopsis thaliana: Torenia fournieri as a new host. Eur J Pl Pathol 117:89–93

    Article  Google Scholar 

  • Videira SIR, Groenewald JZ, Braun U, Shin HD, Crous PW (2016) All that glitters is not Ramularia. Stud Mycol 83:49–163

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Woodward JE, Vandiver MR, Ong KL, McBride (2012) . First report of Vinca minor with Puccinia vincae and Golovinomyces orontii in Texas. Pl Health Progr, https://doi.org/101094/PHP-2012-0724-01-BR

  • Zhao TT, Cho SE, Kim JY, Lee HJ, Shin HD (2018) First report of powdery mildew caused by Golovinomyces ambrosiae on Helianthus salicifolius in Korea. Pl Dis 102:1453

    Article  Google Scholar 

Download references

Acknowledgements

This work was financially supported in part by a Grant-in-Aid for Scientific Research (Nos. 16K07613 and 16F16097) from the Japan Society for the Promotion of Science to Susumu Takamatsu and the JSPS postdoctoral fellowship to Jamjan Meeboon. This work was also supported by a grant (No. K1705841) from Korea University to H.D. Shin, grant MSM 6198959215 (Ministry of Education, Youth and Sports, Czech Republic), and the Internal Grant Agency of Palacký University (IGA 2018_001) to Aleš Lebeda and Miloslav Kitner. Sincere thanks are due to R.T.A. Cook (UK) for reading the text, critical comments, and corrections. M. Götz is much obliged to Elvira Dressler for her excellent technical support. The authors are grateful to Dr. Alexandra Pintye for her photographs of G. tabaci and to A/Prof. John W. D. Dearnaley for his collection of G. spadiceus infecting P. decipiens.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to U. Braun.

Additional information

Section Editor: Roland Kirschner

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Braun, U., Shin, H., Takamatsu, S. et al. Phylogeny and taxonomy of Golovinomyces orontii revisited. Mycol Progress 18, 335–357 (2019). https://doi.org/10.1007/s11557-018-1453-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11557-018-1453-y

Keywords

Navigation