A taxonomic revision of Erysiphe sect. Uncinula (Erysiphaceae, Helotiales) in Iran

Document Type : Original Article

Authors

1 Department of Plant Protection, Faculty of Agricultural Sciences, University of Guilan, Rasht, Iran

2 Department of Botany, Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran

Abstract

 
Since the publication of the latest monograph of powdery mildews by Braun and Cook in 2012, no comprehensive revision has been done to check the accuracy of the hitherto recorded species of the genus Erysiphe in Iran. In this study, we present a taxonomic revision of Erysiphe sect. Uncinula in Iran using morphological traits of voucher specimens and ITS-LSU rDNA sequence analysis. Thirty-eight voucher specimens were obtained from the University of Guilan Mycological herbarium (fungarium, GUM) and the Fungus Reference Collection of Herbarium Ministerii Iranici Agriculturae (IRAN), as well as newly collected specimens during 2019–2021, were examined morphologically. The ITS sequences were generated for 26 selected specimens, and the LSU sequences were generated for 16 specimens. Two ITS sequences of E. paradoxa (OM574846 and OM574845), as well as ITS and LSU sequences of E. celtidis (OM574855 and OM574834, respectively), were sequenced for the first time in this study. Precise morphological observations and molecular analyses of Iranian specimens changed the number of accepted species of Erysiphe sect. Uncinula from six taxa in 2009 to 10 taxa in 2021. All species identified from Iran are here described and illustrated. A key to species of Erysiphe sect. Uncinula in Iran is also provided.

Keywords


Abbasi M, Boujari J, Donyadost–Chalan M. 2013. Notes on the powdery mildews (Erysiphaceae) in Iran. Iranian Journal of Plant Pathology, 49(3): 345–349.
Arzanlou M, Torbati M. 2016. Powdery mildew on Ulmus carpinifolia in Tabriz, East Azerbaijan, Iran. Plant Pathology and Quarantine, 6(2): 133–135.
Assadi M. 2019. Flora of Iran. Journal of Iran Nature, 4(2): 29–41.
Bradshaw M, Tobin P. 2020. Sequencing herbarium specimens of a common detrimental plant disease (powdery mildew). Phytopathology, 110(7): 1248–1254.
Braun U, Takamatsu S. 2000. Phylogeny of Erysiphe, Microsphaera, Uncinula (Erysipheae) and Cystotheca, Podosphaera, Sphaerotheca (Cystotheceae) inferred from rDNA ITS sequences—some taxonomic consequences. Schlechtendalia, 4:1–33.
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. Mycological Progress, 5(3): 139–53.
Braun U, Cook R. 2012. Taxonomic manual of the Erysiphales. Utrecht: CBS–KNAW Fungal Biodiversity Centre.
Cunnington JH, Takamatsu S, Lawrie AC, Pascoe IG. 2003. Molecular identification of anamorphic powdery mildews (Erysiphales). Australasian Plant Pathology, 32(3): 421–428.
Darsaraei H, Khodaparast SA, Takamatsu S, Abbasi M, Asgari B, Sajedi S, Gotz M, Liu Sh, Feng J, Bradshaw M, Bulgakov T, Braun U. 2021. Phylogeny and taxonomy of the Erysiphe adunca complex (Erysiphaceae, Helotiales) on poplars and willows. Mycological Progress, 20: 517–537.
Ellingham O, David J, Culham A. 2019. Enhancing identification accuracy for powdery mildews using previously underexploited DNA loci. Mycologia, 111: 798–812.
Fonseca WL, Cardoso JE, Ootani MA, Brasil SO, Assunção FS, Lima CS, Viana FM, Muniz CR, Andrade IL, Martins MV. 2019. Morphological, molecular phylogenetic and pathogenic analyses of Erysiphe spp. causing powdery mildew on cashew plants in Brazil. Plant Pathology, 68(6): 1157–64.
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(3): 283–288.
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 Research, 30: 3059–3066.
Khodaparast S. 2016. Molecular identification of some anamorphic powdery mildews (Erysiphales) in Guilan province, north of Iran. Mycologia Iranica, 3(2): 127–133.
Khodaparast S, Abbasi M. 2009. Species, host range, and geographical distribution of powdery mildew fungi in Iran. Mycotaxon, 108 (1): 213–216.
Khodaparast S, Hedjaroude GA, Ershad D, Zad J, Termeh F. 2000. A study on identification of Erysiphaceae in Gilan province, Iran (I). Rostaniha, 1(1/4): 53–63.
Khodaparast SA, Pourmoghaddam MJ, Amirmijani A, Byrami F. 2020. Phylogenetic structure of the Iranian capnodiaceous sooty mould fungi inferred from the sequences of rDNA regions and TEF1-a. Mycological Progress, 19(2): 155–69.
Khodaparast S, Takamatsu S, Hejaroud GA. 2005. Phylogenetic analysis of Iranian powdery mildew fungi using nucleotide sequences of 28S ribosomal DNA. Journal of Agricultural Science and Technology (JAST), 7(1): 49–58.
Kirschner R, Lotz–winter H, Piepenbring M. 2020. A new species of the elm poedery mildew species complex (Erysiphaceae) on Chinese elm (Ulmus parvifolia) in East Asia segregated from Erysiphe ulmi. Phytotaxa, 447(4): 276–282.
Kumar S, Stecher G, Tamura K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology Evolution, 33(7): 1870–1874.
Makhdoum M.F. 1990. National Parks as reservoirs of genetic resources. Mohit-e-Zist, 3–(2): 63–75.
Matsuda S, Takamatsu S. 2003. Evolution of host–parasite relationships of Golovinomyces (Ascomycete: Erysiphaceae) inferred from nuclear rDNA sequences. Molecular Phylogenetics and Evolution, 27(2): 314–327.
Meeboon J, Divarangkoon R, Takamatsu S. 2013. Two new species of Erysiphe sect. Uncinula (Erysiphales): Erysiphe fernandoae and E. michikoae. Mycoscience, 54(1): 2–7.
Meeboon J, Takamatsu S. 2013a. Erysiphe havrylenkoana and E. prunastri var. japonica: a new species and a new variety of Erysiphe sect. Uncinula (Erysiphaceae, Ascomycota). Mycological progress, 12(2): 277–282.
Meeboon J, Takamatsu S. 2013b. Erysiphe paracarpinicola: a new species of Erysiphe sect. Uncinula on Carpinus cordata (Betulaceae). Mycoscience, 54(3): 210–216.
Meeboon J, Takamatsu S. 2017. New records of Erysiphe sect. Uncinula spp. (Erysiphales) from Thailand and E. liquidambaris var. acalycinae var. nov. Mycoscience, 58(4): 236–241.
Mori Y, Sato Y, Takamatsu S. 2000a. Evolutionary analysis of the powdery mildew fungi using nucleotide sequences of the nuclear ribosomal DNA. Mycologia, 92(1): 74–93.
Mori Y, Sato Y. Takamatsu S. 2000b. Molecular phylogeny and radiation time of Erysiphales inferred from the nuclear ribosomal DNA sequences. Mycoscience, 41(5): 437–447.
Niinomi S, Takamatsu S, Havrylenko M. 2008. Molecular data do not support a southern hemisphere base of Nothofagus powdery mildews. Mycologia, 100(5): 716–726.
Qiu P–L, Braun U, Li Y, Liu S–Y. 2019. Erysiphe deutziicola sp. nov. (Erysiphaceae, Ascomycota), a powdery mildew species found on Deutzia parviflora (Hydrangeaceae) with unusual appendages. MycoKeys, 51:97–106.
Sharifi K, Khodaparast S, Mousanejad S. 2013. A contribution to the knowledge of taxonomy and identification of anamorphic genus Oidium in Guilan province, Iran. Iranian Journal of Plant Protection Science, 44(1): 1–13.
Siahaan SA, Sakamoto H, Shinoda T, Takamatsu S. 2018. Geographic and temporal distributions of four genotypes found in Erysiphe gracilis var. gracilis, a powdery mildew of evergreen oaks (Erysiphales). Mycoscience, 59(2): 110–118.
Silvestro D, Michalak I. 2012. raxmlGUI: a graphical front–end for RAxML. Organisms Diversity Evolution, 12(4): 335–337.
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(4): 441–453.
Takamatsu S. 2004. Phylogeny and evolution of the powdery mildew fungi (Erysiphales, Ascomycota) inferred from nuclear ribosomal DNA sequences. Mycoscience, 45(2): 147–157.
Takamatsu S. 2013a. Origin and evolution of the powdery mildews (Ascomycota, Erysiphales). Mycoscience, 54(1): 75–86.
Takamatsu S. 2013b. Molecular phylogeny reveals phenotypic evolution of powdery mildews (Erysiphales, Ascomycota). Journal of General Plant Pathology, 79(4): 218–226.
Takamatsu S, Ito H, Shiroya Y, Kiss L, Heluta V. 2015a. First comprehensive phylogenetic analysis of the genus Erysiphe (Erysiphales, Erysiphaceae) I. The Microsphaera lineage. Mycologia, 107(3): 475–489.
Takamatsu S, Ito H, Shiroya Y, Kiss L, Heluta V. 2015b. First comprehensive phylogenetic analysis of the genus Erysiphe (Erysiphales, Erysiphaceae) II: The Uncinula lineage. Mycologia, 107(5): 903–914.
Takamatsu S, Kano Y. 2001. PCR primers useful for nucleotide sequencing of rDNA of the powdery mildew fungi. Mycoscience, 42(1): 135–139.
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(4): 506–513.
Yamaguchi Y, Meeboon J, Heluta VP, Liu SY, Feng J, Takamatsu S. 2021. Phylogeny and taxonomy of Erysiphe species (powdery mildew: Erysiphaceae) occurring on the ash trees (Fraxinus spp.). Mycoscience, 62(2): 115–123.