First records of the powdery mildews Erysiphe platani and E. alphitoides on Ailanthus altissima reveal host jumps independent of host phylogeny
Tóm tắt
The tree-of-heaven Ailanthus altissima (family Simaroubaceae, order Sapindales) is one of the most invasive neophytes in Europe. The tree originated in China and became invasive worldwide in areas with Mediterranean to temperate climates. As known from other invasive plants, only a few pathogens have been reported from A. altissima in Europe, and, to date, powdery mildews on it have been unknown in the European region. Recently, two powdery mildews were found on A. altissima during a survey of neomycetes on non-native plants in Switzerland. Because they did not fit with any of the species known to occur on Simaroubaceae in Asia, they were identified by DNA barcoding using sequences of the ITS region of the n-rDNA, revealing them to be the powdery mildews of plane and oak trees, Erysiphe platani and E. alphitoides. This is the first record of E. platani on a host outside the genus Platanus and its family Platanaceae, as well as its order Proteales. In contrast, E. alphitoides has been reported to occur on several host families and orders. Host jumps over great phylogenetic distances—such as across plant families and orders—appear to be quite common in biogeographically novel associations between Erysiphales species and plants. The consequences of such host jumps for identity and taxonomic placement of species are discussed here. It is further questioned whether both pathogens are usable as biological control agents against the tree-of-heaven.
Tài liệu tham khảo
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Antonovics J, Boots M, Ebert D, Koskella B, Poss M, Sadd BM (2013) The origin of specificity by means of natural selection: evolved and nonhost resistance in host-pathogen interactions. Evolution 67:1–9
Beenken L, Senn-Irlet B (2016) Neomyceten in der Schweiz, Stand des Wissens und Abschätzung des Schadpotentials der mit Pflanzen assoziierten gebietsfremden Pilze. WSL Berichte 50. www.wsl.ch/publikationen/pdf/15783.pdf
Beenken L, Zoller S, Berndt R (2012) Rust fungi on Annonaceae II: the genus Dasyspora Berk. & M.A. Curtis. Mycologia 104:659–681
Bereczky Z, Pintye A, Csontos P, Braun U, Kiss L (2015) Does the parasite follow its host? Occurrence of morphologically barely distinguishable powdery mildew anamorphs on Oenothera spp. in different parts of the world. Mycoscience 56:267–272. doi:10.1016/j.myc.2014.08.001
Bolay A (2005) Les Oidiums de Suisse (Erysiphacées). Cryptogam Helv 20:1–174
Braun U, Cook RTA (2012) Taxonomic manual of the Erysiphales (powdery mildews), CBS Biodiversity Ser 11. CBS, Utrecht
Braun U, Shi A, Mmbaga M, Takamatsu S, Divarangkoon R, Chen P (2007) Erysiphe abbreviata on cherry bark oak - morphology, phylogeny and taxonomy. Mycologia 99:655–663
Bufford JL, Hulme PE, Sikes BA, Cooper JA, Johnston PR, Duncan RP (2016) Taxonomic similarity, more than contact opportunity, explains novel plant–pathogen associations between native and alien taxa. New Phytol 212:657–667. doi:10.1111/nph.14077
Cheon W, Lee SG, Jeon YH (2014) First report of powdery mildew caused by Erysiphe alphitoides on Japanese snailseed (Cocculus trilobus) in Korea. Plant Dis 98:685. doi:10.1094/PDIS-01-13-0031-PDN
Cook RTA, Denton JO, Denton G (2015) Pathology of oak – wisteria powdery mildew. Fungal Biol 119:657–671
Cook RTA, Henricot B, Kiss L (2004) First record of Erysiphe elevata on Catalpa bignonioides in the UK. Plant Pathol 53:807
Cunnington JH, Lawrie AC, Pascoe IG (2010) Genetic characterization of the Golovinomyces cichoracearum complex in Australia. Plant Pathol 59:158–164. doi:10.1111/j.1365-3059.2009.02175.x
Cunnington JH, Takamatsu S, Lawrie AC, Pascoe IG (2003) Molecular identification of anamorphic powdery mildew (Erysiphales). Australas Plant Pathol 32:421–428
Denton GJ, Denton JO, Cook RTA (2013) First report of powdery mildew on Sorbaria. New Dis Rep 28:15. doi:10.5197/j.2044-0588.2013.028.015
Denton GJ, Denton JO, Cook RTA (2016) First record of Erysiphe alphitoides on Wisteria brachybotrys and W. frutescens, and first record of its chasmothecia on Wisteria. New Dis Rep 33:5. doi:10.5197/j.2044-0588.2016.033.005
Ding J, Wu Y, Hao Z, Weidong F, Reardon R, Liu M (2006) Assessing potential biological control of the invasive plant, tree-of-heaven, Ailanthus altissima. Biocontrol Sci Technol 16:547–566
Farr DF, Rossman AY (2016) Fungal Databases, Systematic Mycology and Microbiology Laboratory, ARS, USDA. http://nt.ars-grin.gov/fungaldatabases/. Accessed 18 Aug 2016
Gadgil PD (2005) Fungi on trees and shrubs in New Zealand. Fungi of New Zealand Volume 4. Fungal Diversity, Hong Kong
Gardes MT, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes, application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118
Gilbert GS, Magarey R, Suiter K, Webb CO (2012) Evolutionary tools for phytosanitary risk analysis: phylogenetic signal as a predictor of host range of plant pests and pathogens. Evol Appl 5:869–878. doi:10.1111/j.1752-4571.2012.00265.x
Gilbert GS, Webb CO (2007) Phylogenetic signal in plant pathogen-host range. Proc Natl Acad Sci U S A 104:4979–4983
Gill US, Lee S, Mysore KS (2015) Host versus nonhost resistance: distinct wars with similar arsenals. Phytopathology 105:580–587
Gurtner D, Conedera M, Rigling A, Wunder J (2015) Der Götterbaum dringt in die Wälder nördlich der Alpen vor. Wald Holz 7:22–24
Hajek AE (2004) Natural Enemies - An introduction to biological control. Cambridge University Press, Cambridge. doi:10.5197/j.2044-0588.2016.033.005
Henricot B, Cook RTA (2008) New report of a powdery mildew on Wisteria in the UK. Plant Pathol 57:374. doi:10.1111/j.1365-3059.2007.01671.x
Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, Rupp R (2007) Dendroscope - An interactive viewer for large phylogenetic trees. BMC Bioinformatics 8:460
Kasson MT, O’Neal ES, Davis DD (2015) Expanded host range testing for Verticillium nonalfalfae: potential biocontrol agent against the invasive Ailanthus altissima. Plant Dis 99:823–835
Kasson MT, Short DPG, O’Neal ES, Subbarao KV, Davis DD (2014) Comparative pathogenicity, biocontrol efficacy, and multilocus sequence typing of Verticillium nonalfalfae from the invasive Ailanthus altissima and other hosts. Phytopathology 104:282–292
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066
Kirschner R (2010) First record of Erysiphe magnifica on lotus, a host outside the Magnoliales. Mycol Prog 9:417–424
Kirschner R (2011) Observations on Erysiphe platani in Germany. Plant Pathol Quar 1:115–119
Kirschner R (2015) First record of the sexual stage of the powdery mildew Erysiphe pseudolonicerae in Taiwan. Fungal Sci 30:61–66
Kirschner R, Liu WA (2014) Two new hosts of anamorphic Erysiphe quercicola: Cinnamomum camphora and Murraya paniculata. Mycoscience 55:190–195. doi:10.1016/j.myc.2013.08.004
Klenke F, Scholler M (2015) Pflanzenparasitische Kleinpilze. Springer, Berlin
Knüsel S, Conedera M, Rigling A, Fonti P, Wunder J (2015) A tree-ring perspective on the invasion of Ailanthus altissima in protection forests. For Ecol Manag 354:334–343
Kowarik I, Säumel I (2007) Biological flora of Central Europe: Ailanthus altissima (Mill.) Swingle. Perspect Plant Ecol Evol Syst 8:207–237
Kreisel H, Scholler M (1994) Chronology of Phytoparasitic Fungi Introduced to Germany and Adjacent Countries. Bot Acta 107:387–392
La YJ, Cho S, Shin HD (2013) First report of powdery mildew of Platanus occidentalis caused by Erysiphe platani in Korea. Plant Dis 97:843
Lee HB, Kim CJ, Mun HY, Lee KH (2011) First report of Erysiphe quercicola causing powdery mildew on ubame oak in Korea. Plant Dis 95:77
Lee HB, Lee HW, Mun HY (2013) First report of powdery mildew caused by Erysiphe platani on sycamore (Platanus occidentalis) in South Korea. Plant Dis 97:841
Li CW, Zhang Y, Liu Y, Kang M, Ma XM, Fu LL (2011) First report of powdery mildew caused by Erysiphe euonymi-japonici on Euonymus japonicus in central China. Plant Dis 95:611
Ligoxigakis EK, Markakis EA, Papaioannou IA, Typas MA (2015) First report of powdery mildew of Platanus acerifolia and P. occidentalis caused by Erysiphe platani in Greece. Plant Dis 99:286
Limkaisang S, Cunnington JH, Liew KW, Salleh B, Sato Y, Divarangkoon R, Fangfuk W, To-anun C, Takamatsu S (2006) Molecular phylogenetic analyses reveal a close relationship between powdery mildew fungi on some tropical trees and Erysiphe alphitoides, an oak powdery mildew. Mycoscience 47:327–335. doi:10.1007/S10267-006-0311-Y
Limkaisang S, Kom-un S, Furtado EL, Liew KW, Salleh B, Sato Y, Takamatsu S (2005) Molecular phylogenetic and morphological analyses of Oidium heveae, a powdery mildew of rubber tree. Mycoscience 46:220–226. doi:10.1007/S10267-005-0238-8
Lipka U, Fuchs R, Kuhns C, Petutschnig E, Lipka V (2010) Live and let die – Arabidopsis nonhost resistance to powdery mildews. Eur J Cell Biol 89:194–199
Maschek O, Halmschlager E (2016) First report of Verticillium wilt on Ailanthus altissima in Europe caused by Verticillium nonalfalfae. Plant Dis 100:529
Mayor E (1908) Contribution à l’étude des érysiphées de la Suisse. Bull Soc Neuchâtel Sci Nat 35:43–61
Meeboon J, Takamatsu S (2015) Notes on powdery mildews (Erysiphales) in Japan: II. Erysiphe sect. Microsphaera. Mycoscience 56:230–236
Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–27
Mougou A, Dutech C, Desprez-Loustau ML (2008) New insights into the identity and origin of the causal agent of oak powdery mildew in Europe. For Path 38:275–287
Pastirčáková K, Pastirčák M, Adamčiková K, Bouznad Z, Kedad A, El Guilli M, Diminić D, Diminić M (2014) Global distribution of Erysiphe platani: new records, teleomorph formation and re-examination of herbarium collections. Cryptog Mycol 35:163–176
Saenz GS, Taylor JW (1999) Phylogeny of the Erysiphales (powdery mildews) inferred from internal transcribed spacer ribosomal DNA sequences. Can J Bot 77:150–168
Schaffner U, Escher R (2012) Grundlagen für die Umsetzung des Zulassungsverfahrens von gebietsfremden Organismen für die klassische biologische Bekämpfung von Schadorganismen in der Schweiz, Schlussbericht. CABI Delémont
Schoch CL, Seifert KA, Huhndorf S, Spouge RV, Levesque CA, Chen W, Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci U S A 109:6241–6246. doi:10.1073/pnas.1117018109
Scholler M, Hemm V, Lutz M (2012) Erysiphe platani: monitoring of an epidemic spread in Germany and molecular characterization based on rDNA sequence data. Andrias 19:263–272
Seko Y, Heluta V, Grigaliunaite B, Takamatsu S (2011) Morphological and molecular characterization of two ITS groups of Erysiphe (Erysiphales) occurring on Syringa and Ligustrum (Oleaceae). Mycoscience 52:174–182
Senn-Irlet BJ, Gross A, Blaser S (2016) SwissFungi: National data- and information center for the fungi of Switzerland (datebase). Version 2. Birmensdorf, Swiss Federal Institute WSL. http://www.swissfungi.ch. Accessed 12 Dec 2016.
Shiroya Y, Nakashima C, Takamatsu S (2008) Erysiphe monascogera sp. nov, an unusual powdery mildew fungus found on fruits of Styrax japonica. Mycoscience 49:199–206
Siahaan SAS, Takamatsu S (2016) Erysiphe aucubae sp. nov, a new powdery mildew species on Aucuba japonica from Japan. Mycoscience 57:251–254
Siegrist M, Holdenrieder O (2016) Die Verticillium-Welke – eine Option zur Bekämpfung des Götterbaumes in der Schweiz? Schweiz Z Forstwes 167:249–257
Sprenger C (1916) Die Freude an der Natur. Mitt Dtsch Dendrol Ges 25:113–118
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690
Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57:758–71
Takamatsu S, Bolay A, Limkaisang S, Kom-un S, To-anun C (2006) Identity of a powdery mildew fungus occurring on Paeonia and its relationship with Erysiphe hypophylla on oak. Mycoscience 47:367–373
Takamatsu S, Braun U, Limkaisang S, Kom-Un S, Sato Y, Cunnington JH (2007) Phylogeny and taxonomy of the oak powdery mildew Erysiphe alphitoides sensu lato. Mycol Res 111:809–826
Takamatsu S, Hirata T, Sato Y, Nomura Y, Sato Y (1999) Phylogenetic relationships of Microsphaera and Erysiphe section Erysiphe (powdery mildews) inferred from the rDNA ITS sequences. Mycoscience 40:259–268
Takamatsu S, Inagaki M, Niinomi S, Khodaparast SA, Shin HD, Grigaliunaite B, Havrylenko M (2008) Comprehensive molecular phylogenetic analysis and evolution of the genus Phyllactinia (Ascomycota: Erysiphales) and its allied genera. Mycol Res 112:299–315
Takamatsu S, Ito H, Shiroya Y, Kiss L, Heluta V (2015) First comprehensive phylogenetic analysis of the genus Erysiphe (Erysiphales, Erysiphaceae) I. The Microsphaera Lineage Mycologia 107:475–489
Takamatsu S, Matsuda S, Grigaliunaite B (2013) Comprehensive phylogenetic analysis of the genus Golovinomyces (Ascomycota: Erysiphales) reveals close evolutionary relationships with its host plants. Mycologia 105:1135–1152. doi:10.3852/13-046
Tanner RA, Pollard K, Varia S, Evans HC, Ellison CA (2015) First release of a fungal classical biocontrol agent against an invasive alien weed in Europe: biology of the rust, Puccinia komarovii var. glanduliferae. Plant Pathol 64:1130–1139
Van Kleunen M, Fischer M (2009) Release from foliar and floral fungal pathogen species does not explain the geographic spread of naturalized North American plants in Europe. J Ecol 97:385–392
Watanabe K, Sato Y (2009) First report of powdery mildew of Madagascar periwinkle caused by Eryisphe sp. in Japan. Plant Pathol 58:95
Weber E (2013) Invasive Pflanzen der Schweiz. Haupt, Bern
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