Abstract
Fabaceae, one of the largest flowering plant families, comprises several subfamilies and genera. Fabaceous plant species host a large number of powdery mildew species belonging to the genus Erysiphe. The affiliation of these species to Erysiphe is readily possible, but they represent a morphologically and taxonomically complicated complex of closely related, morphologically similar species with overlapping traits. Precise morphological examinations along with phylogenetic analyses, including type collections and other representative samples, are needed to solve the complexity of Erysiphe spp. on legumes. In this study, we sequenced a number of collections of powdery mildews on Pisum, Lathyrus, Vicia and Ononis spp., with a special focus on specimens from Iran, to clarify species delimitations within the Erysiphe pisi complex and other Erysiphe species complexes on legumes. Sequences retrieved from powdery mildew on Pisum and Ononis fall into separate, well supported clades. Hence, the original status of E. cruchetiana as a species of its own on Ononis spp. is reinstated instead of E. pisi var. cruchetiana. Ten species, viz., E. astragali, E. bremeri, E. caulicola, E. cruchetiana, E. iranica, E. medicaginis, E. pisi, E. rayssiae, E. sesbaniae and E. trifoliorum were confirmed for Iran, redescribed and illustrated on the basis of Iranian collections. Erysiphe astragali, E. bremeri, E. coluteae and E. crispula form a genetically little differentiated clade in ITS/LSU analyses, which is referred to as E. astragali clade (complex), comparable to the E. trifoliorum clade (complex). Based on our results, E. coluteae and E. crispula are reduced to synonymy with E. astragali and E. sophorae is considered a synonym of E. bremeri. Sequences of the North American E. intermedia on Lupinus species form a small clade nested within the big E. astragali clade. DNA of the holotype of E. sesbaniae was sequenced for the first time in this study. To use the sequences obtained from some new collections as reference sequences for phylogenetic-taxonomic purposes, we propose, for the interim, reference sequences for E. bremeri, E. caulicola, E. cruchetiana, E. pisi and E. viciae-unijugae.
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The datasets generated during the current study can be found in online repositories or available from the corresponding author on reasonable request. The names of the repository/repositories and accession numbers can be found in the article.
References
Azani N, Babineau M, Bailey CD et al (2017) A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon 66:44–77. https://doi.org/10.12705/661.3
Blumer S (1933) Die Erysiphaceen Mitteleuropas unter besonderer Berucksichtigung der Schweiz. Beitr Krypt-FI Schweiz 7:1–483
Bradshaw M, Braun U, Götz M, Jurick ΙΙW (2022) Phylogeny and taxonomy of powdery mildew caused by Erysiphe species on Lupinus hosts. Mycologia 114:76–88. https://doi.org/10.1080/00275514.2021.1973287
Bradshaw M, Tobin PC (2020) Sequencing herbarium specimens of a common detrimental plant disease (powdery mildews). Phytopathology 110:1248–1254. https://doi.org/10.1094/PHYTO-04-20-0139-PER
Braun U (1981) Taxonomic studies in the genus Erysiphe I. Generic delimitation and position in the system of the Erysiphaceae. Nova Hedwigia 34:679–719
Braun U, Cook R (2012) Taxonomic manual of the Erysiphales (powdery mildews). CBS-KNAW Fungal Biodiversity Series, Utrecht, The Netherlands
Crous PW, Wingfield MJ, Chooi Y-H et al (2020) Fungal Planet description sheets: 1042–1111. Persoonia 44:301–459. https://doi.org/10.3767/persoonia.2020.44.11
Cunnington J, Takamatsu S, Lawrie A, Pascoe I (2003) Molecular identification of anamorphic powdery mildews (Erysiphales). Australas Plant Pathol 32:421–428. https://doi.org/10.1071/AP03045
Darsaraei H, Pirnia M, Khodaparast SA, Behrooz SY (2022) Erysiphe iranica sp. nov. on Onobrychis caput-galli in Iran. Mycotaxon 137:271–282
Darsaraei H, Khodaparast SA, Mousanejad S, Sepahvand K, Asgari B, Sajedi S (2023) Taxonomic update with DNA barcoding and phylogenetic analysis of Erysiphe sect. Microsphaera (Erysiphaceae, Helotiales) in Iran. Mycol Iran 10(2):11–32
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.2307/2408678
Hirata T, Cunnington JH, Paksiri U et al (2000) Evolutionary analysis of subsection Magnicellulatae of Podosphaera section Sphaerotheca (Erysiphales) based on the rDNA internal transcribed spacer sequences with special reference to host plants. Can J Bot 78:1521–1530
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
Khodaparast SA, Darsaraei H, Abbasi M (2021) The genus Arthrocladiella: a new report of powdery mildew fungi from Iran. Mycol Iran 8(2):135–140. https://doi.org/10.22043/MI.2022.359598.1227
Khodaparast SA, Takamatsu S, Hedjaroude G-A (2001) 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. Mycol Res 105:909–918
Khodaparast SA, Hedjaroude GA, Takamatsu S (2003) Phylogenetic relationships between Iranian isolates of Microsphaera and Erysiphe s. lat. based on rDNA internal transcribed spacers sequences. Rostaniha 4(2):93–104
Kirschner R, Lotz H, Piepenbring M (2020) A new species of the elm powdery mildew species complex (Erysiphaceae) on Chinese elm (Ulmus parvifolia) in East Asia segregated from Erysiphe ulmi. Phytotaxa 447:276–282. https://doi.org/10.11646/phytotaxa.447.4.5
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Matsuda S, Takamatsu S (2003) Evolution of host–parasite relationships of Golovinomyces (Ascomycete: Erysiphaceae) inferred from nuclear rDNA sequences. Mol Phylogenet Evol 27:314–327
Moghaddam M, Kazempour Osaloo S, Hosseiny H, Azimi F (2017) Phylogeny and divergence times of the Coluteoid clade with special reference to Colutea (Fabaceae) inferred from nrDNA ITS and two cpDNAs, mat K and rpl 32-trn L (UAG) sequences data. Plant Biosyst Int J Deal Asp Plant Biol 151:1082–1093
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
Qiu P-L, Braun U, Li Y, Liu S (2019) Erysiphe deutziicola sp. nov. (Erysiphaceae, Ascomycota), a powdery mildew species found on Deutzia parviflora (Hydrangeaceae) with unusual appendages. MycoKeys 51:97–106. https://doi.org/10.3897/mycokeys.51.34956
Schmidt A, Braun U (2020) Asexual morphs of powdery mildew species (Erysiphaceae)–new and supplementary morphological descriptions and illustrations. Schlechtendalia 37:30–79
Silvestro D, Michalak I (2010) raxmlGUI: a graphical front-end for RaxML. Org Divers Evol 12:1–3. https://doi.org/10.1007/s13127-011-0056-0
Takamatsu S, Kano Y (2001) PCR primers useful for nucleotide sequencing of rDNA of the powdery mildew fungi. Mycoscience 42:135–139
Takamatsu S, Ito H, Shiroya Y, Kiss L, Heluta V (2015) First comprehensive phylogenetic analysis of the genus Erysiphe (Erysiphales, Erysiphaceae) II: the Uncinula lineage. Mycologia 107:903914
Walsh PS, Metzger DA, Higuchi R (2013) Chelex 100 as a medium for simple extraction of dna for pcr-based typing from forensic material. BioTechniques 54:134–139. https://doi.org/10.2144/000114018
Zhang Y-J, Zhang S, Liu X et al (2010) A simple method of genomic DNA extraction suitable for analysis of bulk fungal strains. Lett Appl Microbiol 51:114–118. https://doi.org/10.1111/j.1472-765X.2010.02867.x
Acknowledgments
The authors are grateful to Dr. M.R. Asef, curator of the Fungus Reference Collection of “IRAN” Herbarium for providing the specimens. This study was supported by a research grant from the Iran National Science Foundation (INSF), No. 96007836 to S.A. Khodaparast.
Funding
This work was supported by a grant from the Iran National Science Foundation (No. 96007836) to S. A. Khodaparast.
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Hamideh Darsaraei, Seyed Akbar Khodaparast, Uwe Braun, Susumu Takamatsu, and Monika Götz. The first draft of the manuscript was written by Hamideh Darsaraei, Seyed Akbar Khodaparast, and Uwe Braun, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Darsaraei, H., Khodaparast, S.A., Asgari, B. et al. Erysiphe spp. on Fabaceae from Iran: A new insights into some complex species. Mycol Progress 23, 10 (2024). https://doi.org/10.1007/s11557-024-01945-5
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DOI: https://doi.org/10.1007/s11557-024-01945-5