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Erysiphe kenjiana (Erysiphales), a new invasive fungus in Europe

Abstract

An Asian powdery mildew fungus Erysiphe (Uncinula) kenjiana (Erysiphales, Ascomycota) has been found in Ukraine. This is the first record of this fungus in Europe. In 2007, E. kenjiana was collected on four Ulmus species in Kiev. All locations adjoined railways or an airport. Development of E. kenjiana was epiphytotic. This species was not found on elms surveyed at towns situated north-east, east or south of Kiev. The fungus may have been brought directly to Ukraine by rail or air transport. In 2008, the fungus was also collected in Chernihiv situated north-east of Kiev. It is likely that E. kenjiana will spread over all Ukraine and into countries of central and western Europe in 2009 or later. Molecular phylogenetic analyses using D1/D2 domains of the 28S rDNA and ITS sequences revealed that the Ulmaceae-Cannabaceae-parasitic powdery mildews, including E. kenjiana, form a clade with strong supports, suggesting that these species diverged from a single ancestor and expanded their host ranges within the Ulmaceae and allied Cannabaceae. This hypothesis is supported by these species sharing the unique morphology of enlarged apices on their chasmothecial appendages. These fungi formed part of a larger grouping with species on Fagaceae, Nothofagaceae, Rosaceae, and Sapindaceae with strong statistical supports. These results suggest that Uncinula-like powdery mildew fungi on these plant families exhibit close evolutionary relationships with their hosts.

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References

  • Ale-Agha N, Braun U, Feige B, Jage H (2000) A new powdery mildew disease on Aesculus spp. introduced in Europe. Cryptogam Mycol 21:89–92

    Article  Google Scholar 

  • Ale-Agha N, Bolay A, Braun U, Feige B, Jage H, Kummer V, Lebeda A, Piatek M, Shin HD, Zimmermannová-Pastirčáková K (2004) Erysiphe catalpae and Erysiphe elevata in Europe. Mycol Prog 3:291–296

    Article  Google Scholar 

  • APG II (Angiosperm Phylogeny Group) (2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants. Bot J Linn Soc 141:399–436

    Article  Google Scholar 

  • Bolay A (2000) L'oїdium des marroniers envahit la Suisse. Rev Suisse Vitic Arboric Hortic 32:311–313

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Braun U (2002) Erysiphe miurae and E. syringae-japonicae - new records from Russia. Mikol Fitopatol 36(2):15–16

    Google Scholar 

  • Braun U, Takamatsu S, Heluta V, Limkaisang S, Divarangkoon R, Cook R, Boyle H (2006) Phylogeny and taxonomy of powdery mildew fungi of Erysiphe sect. Uncinula on Carpinus species. Mycol Prog 5:139–153

    Article  Google Scholar 

  • Bunkina IA (1978) Muchnisto-rosyanye griby (sem. Erysiphaceae) Dal’nego Vostoka. Dal’nevostochnyi universitet, Vladivostok

  • Bunkina IA (1991) Poryadok erysiphales Gwinne-Vaughan. In: Azbukina ZM (ed) Nizshie rasteniya, griby i mokhoobrasnye sovetskogo Dal’nego Vostoka. Griby, vol. 2. Askomitsety. Erizifalnye, klavicipitalnye, gelotsialnye. Nauka, Leningrad, pp 11–142

    Google Scholar 

  • Chen G, Han S, Lai Y, Yu Y, Zheng R, Zhao Z (1987) Flora fungorum sinicorum, vol. 1. Erysiphales (in Chinese). Science Press, Beijing

    Google Scholar 

  • Cook RTA, Henricot B, Kiss L (2004) First record of Erysiphe elevata on Catalpa bignonioides in the UK. Plant Pathol 53:807

    Article  Google Scholar 

  • Cook RTA, Henricot B, Henrici A, Beales P (2006) Morphological and phylogenetic comparisons amongst powdery mildews on Catalpa in the UK. Mycol Res 110:672–685

    Article  CAS  PubMed  Google Scholar 

  • Fakirova VI (1993) Distribution of Microsphaera vanbruntiana Ger. var. sambuci-racemosae U. Braun and Erysiphe magnicellulata U. Braun (Fam. Erysiphaceae) in Bulgaria. Fitol 44:32–34

    Google Scholar 

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

    Article  Google Scholar 

  • Gaponenko NI, Akhmedova FG, Ramazanova SS, Sagdullaeva MSh, Kirgizbaeva KhM (1983) Fungus flora of Uzbekistan, vol. 1. Powdery mildew fungi (in Russian). FAN, Tashkent

    Google Scholar 

  • Heluta VP, Gorlenko MV (1981) Sistematika i rasprostraneniye Microsphaera van-bruntiana Ger. v evropeiskoi chasti SSSR. Bull Mosk Obŝ Ispyt Prir. Otd Biol 86:117–124

    Google Scholar 

  • Heluta VP, Gorlenko MV (1984) Microsphaera palczewskii Jacz. v SSSR. Mikol Fitopatol 18(3):177–182

    Google Scholar 

  • Heluta VP [Geluta WP] (1989) Flora gribov Ukrainy. Muchnistorosyanye griby. Naukova dumka, Kiev

  • Heluta VP, Minter DW (1998) Microsphaera palczewskii. IMI Descr Fungi Bact 138(1375):1–3

    Google Scholar 

  • Hirata T, Takamatsu S (1996) Nucleotide sequence diversity of rDNA internal transcribed spacers extracted from conidia and cleistothecia of several powdery mildew fungi. Mycoscience 37:283–288

    Article  Google Scholar 

  • Homma Y (1930) Notes on the Erysiphaceae of Manchuria. Trans Sapporo Nat Hist Soc 11:169–174

    Google Scholar 

  • Ing B (2000) Microsphaera azaleae, the perfect state of the Rhododendron mildew in England. Mycologist 14:165

    Article  Google Scholar 

  • Inman AJ, Cook RTA, Beales PA (2000) A contribution to the identity of rhododendron powdery mildew in Europe. J Phytopathol 148:17–27

    Google Scholar 

  • Kiss L (2005) Powdery mildew as invasive plant pathogens: new epidemics caused by two North American species in Europe. Mycol Res 109:259–260

    Article  PubMed  Google Scholar 

  • Kravtsev BI (1950) Gribnye bolezni topolei v Kazakhstane. Izv AN KazSSR Ser Biol 98:106–127

    Google Scholar 

  • Kreisel H, Scholler M (1994) Chronology of Phytoparasitic Fungi Introduced to Germany and Adjacent Countries. Bot Acta 107:369–472

    Google Scholar 

  • Kusaba M, Tsuge T (1995) Phylogeny of Alternaria fungi known to produce hostspecifictoxins on the basis of variation in internal transcribed spacers of ribosomal DNA.Curr Genet 28:491–498

    Google Scholar 

  • Millevoj L (2004) The occurence of some pests and diseases on horse chestnut, plane tree and Indian bean tree in urban areas of Slovenia. Acta Agric Slov 83:297–300

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mułenko W (1989) Mikroskopowe grzyby fitopatogeniczne Pojezierza Łęczyńsko-Włodawskiego. II. Acta Mycol 24:125–171

    Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. Evolutionary Biology Centre, Uppsala University: Program distributed by the author

  • Piątek M (2002) Erysiphe flexuosa, a new for Poland powdery mildew causing disease of Aesculus hippocastanum. Phytopatol Pol 24:67–71

    Google Scholar 

  • Romaszewska-Sałata J, Sałata B, Mułenko W (1986) O interesuacych przewstawicielach Peronosporales i Erysiphales, zebranych ostatnio w Polsce. Folia Soc Lublinensis Biol 28:11–18

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Scholler M (1994) Morphologische und chorologische Untersuchungen an Microsphaera palczewskii (Erysiphales). Feddes Repert 105:377–382

    Google Scholar 

  • Seko Y, Bolay A, Kiss L, Heluta V, Grigaliunaite B, Takamatsu S (2008) Molecular evidence in support of recent migration of a powdery mildew fungus on Syringa spp. into Europe from East Asia. Plant Pathol 57:243–250

    Article  CAS  Google Scholar 

  • Shin HD (2000) Erysiphaceae of Korea. National Institute of Agricultural Science and Technology, Suwon

    Google Scholar 

  • Stevens PF (2008) Angiosperm Phylogeny Website. Version 9. http://www.mobot.org/mobot/research/apweb/

  • Swofford DL (2001) PAUP: Phylogenetic analysis using parsimony (and other methods) 4.0b8. Sinauer, Sunderland, MA

    Google Scholar 

  • Takamatsu S, Kano Y (2001) PCR primers useful for nucleotide sequencing of rDNA ofthe powdery mildew fungi. Mycoscience 42:135–139

    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  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Vajna L (2006) Powdery mildew caused by Erysiphe carpinicola on Carpinus betulus in Hungary: first European report. New Dis Rep 12, Aug. 2005 – Jan. 2006. http://www.bspp.org.uk/ndr/jan2006/2006-08.asp

  • Vajna L, Fischl G, Kiss L (2004) Erysiphe elevata (syn. Microsphaera elevata), a new North American powdery mildew fungus in Europe infecting Catalpa bignonioides trees. Plant Pathol 53:244

    Article  Google Scholar 

  • Vasyagina MP, Kuznetsova NM, Pisareva NF, Shwartsman SR (1961) Flora sporovykh rastenii Kazakhstana, vol 3. Muchnisto-rosyanye griby, AN KazSSR, Alma-Ata

    Google Scholar 

  • Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10:506–513

    CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, San Diego, pp 315–322

  • Zimmermannová-Pastirčáková K, Adamska I, Blaszkowski J, Bolay A, Braun U (2000) Epidemic spread of Erysiphe flexuosa (North American powdery mildew of horse-chestnut) in Europe. Schlechtendalia 8:39–45

    Google Scholar 

  • Zimmermannová-Pastirčáková K, Pastirčák M (2002) Erysiphe flexuosa - a new species of powdery mildew for Slovakia. Biol Bratislava 57:437–440

    Google Scholar 

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Acknowledgments

Authors are grateful to Dr. O. Lukash (Chernihiv), Dr. Yu. Golubtsova (Sumy), Dr. I. Besedina (Poltava), Ms. I. Bondarenko-Borysova (Donetsk), and Ms. O. Dzyunenko (Simpheropol) for examination of elms. We thank Dr. Roger Cook for help with the English and valuable comments on the manuscript. We also gratefully acknowledge the late Mr. D. Diomenko, for his help with scanning electron microscopy.

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Correspondence to Vasyl Heluta.

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Heluta, V., Takamatsu, S., Voytyuk, S. et al. Erysiphe kenjiana (Erysiphales), a new invasive fungus in Europe. Mycol Progress 8, 367 (2009). https://doi.org/10.1007/s11557-009-0610-8

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  • DOI: https://doi.org/10.1007/s11557-009-0610-8

Keywords

  • Invasion
  • Molecular phylogeny
  • Powdery mildew fungi
  • Ukraine
  • Ulmus