Unique findings of Phoma-like fungi associated with soybean

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Ascochyta leaf blight of soybean is a widespread disease caused by several closely related Phoma-like species, this disease often leads to significant crop losses. Among Phoma-like species from Didymellaceae family, the most frequently associated with symptomatic soybean tissues are species of the genera Boeremia and Didymella. Currently reliable species identification in Didymellaceae relies on polyphasic approach based on consolidated species concept and combined molecular phylogenetic, micromorphological and cultural features. At least three loci are commonly used for reconstruction of the molecular phylogeny of Didymellaceae: internal transcribed spacer (ITS) of the ribosomal DNA, partial RNA-polymerase II gene (rpb2), and β-tubulin (tub2). As a result of long-term phytosanitary monitoring of soybean crops, soybean leaves with symptoms of Ascochyta blight were collected from major soybean producing areas of Russia. From surface sterilized plant tissues more than 100 isolates of Phoma-like fungi were obtained and stored in the collection of pure cultures of the Laboratory of Mycology and Phytopathology (MF, All-Russian Institute of Plant Protection). Most of them, as a result of multilocus phylogenetic analysis, were identified as Boeremia and Didymella species. Eight isolates were identified as species of other genera, suspected to be rare findings. The aim of this study was to identify these eight isolates based on multilocus phylogenetic analysis, as well micromorphological, cultural, and pathogenicity data. Multilocus phylogenetic analysis has resulted in identification of all eight isolates to species level. Single isolate from the Ryazan region was Neoascochyta graminicola. Three other from three different districts of the Amur region were Remotididymella capsici. Two isolates from the Primorskiy territory and Amur region were Stagonosporopsis heliopsidis. Another two from two districts of the Amur region were S. stuijvenbergii. Pathogenicity tests have resulted in conclusion, that all studied isolates were not pathogenic for soybean leaves. Probably, these Phoma-like species are associate with soybean as saprophytes or endophytes. For all these Phoma-like species Glycine max was detected as substrate for the first time. Neoascochyta graminicola is widespread in Europe in association with Poaceae plants. There are only two findings of Remotididymella capsici in the world, both from leaves of Capsicum annuum. First finding was made in the former USSR in 1977 and was identified based on only morphological features. Second findings was collected in the Fiji and verified with multilocus phylogenetic analysis. Stagonosporopsis heliopsidis isolates were revealed in the USA, Canada, Netherlands and Russia and this fungus was believed to be specific for Asteraceae plants. Isolates of Stagonosporopsis stuijvenbergii are known only from soil in the Netherlands. Thus, such species as Neoascochyta graminicola and Stagonosporopsis stuijvenbergii were revealed in the Russia for the first time. Studied Remotididymella capsici isolates were first confirmed findings of this fungus in Russia. Additionally to detailed phylogenetic data, the manuscript is supplement with a detailed description of the cultural and micromorphological features of all species.

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М. Gomzhina

All-Russian Institute of Plant Protection

编辑信件的主要联系方式.
Email: gomzhina91@mail.ru
俄罗斯联邦, St. Petersburg

E. Gasich

All-Russian Institute of Plant Protection

Email: elena_gasich@mail.ru
俄罗斯联邦, St. Petersburg

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2. Fig. 1. Soybean leaves with symptoms of ascochyta blight, from which the studied isolates were isolated: A - Ryazan region, isolated Neoascochyta graminicola MF 1.42, 2020 (LEP 123703); B — Amur region, isolated Remotididymella capsici MF 1.28, 2019 (LEP 123702); B - Amur region, isolated Stagonosporopsis stuijvenbergii MF 1.30, 2019 (LEP 123704).

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3. Fig. 2. Combined phylogenetic tree of the species Neoascochyta, Remotididymella, Stagonosporopsis, constructed by the ML method, based on the nucleotide sequences of ITS, rpb2 and tub2. Numerical values of bootstrap support obtained by the ML (≥ 70), MP ≥ 70) and Bayesian statistics (≥ 0.7) methods are given at the nodes of the dendrogram branches, respectively. Numbers of type or representative strains are indicated by the letters T or R. Numbers of tested isolates are indicated in blue.

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4. Fig. 3. Morphological features of Neoascochyta graminicola MF 1.42: A–E - cultures (A - on KSA, 7 days; B - on OA, 7 days; C - on MEA, 7 days; D - on KSA, 14 days; E - on OA, 14 days; E - on MEA, 14 days); F, Z - pycnidia; I - the inner wall of the pycnida, lined with conidiogenic cells; K - conidia. The left half is the top of the colony, the right half is the reverse of the colony. Scale: F - 500 µm; W - 100 µm; I and K - 20 µm.

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5. Fig. 4. Morphological features of Remotididymella capsici MF 1.28: A–E - cultures (A - on KSA, 7 days; B - on OA, 7 days; C - on MEA, 7 days; D - on KSA, 14 days; E - OA , 14 days; E - MEA, 14 days); F, H - fruiting bodies; And - immature bag; K - ascospores; L - bag. The left half is the top of the colony, the right half is the reverse of the colony. Scale: F - 1 mm; W - 100 µm; I and K - 20 µm.

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6. Fig. 5. Morphological features of Stagonosporopsis heliopsidis MF 1.25: A–E — cultures (A — on KSA, 7 days; B — on OA, 7 days; C — on MEA, 7 days; D — on KSA, 14 days; E — OA , 14 days; E - MEA, 14 days); F–I—pycnidia; K - conidiogenic cell; L - conidia. The left half is the top of the colony, the right half is the reverse of the colony. Scale: F - 2 mm; H, I - 50 µm; K, L - 20, microns.

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7. Fig. 6. Morphological features of Stagonosporopsis stuijvenbergii MF 6.1: A–E - cultures (A - on KSA, 7 days; B - on OA, 7 days; C - on MEA, 7 days; D - on KSA, 14 days; E - OA , 14 days; E - MEA, 14 days); F, Z - pycnidia; And - conidia. The left half is the top of the colony, the right half is the reverse of the colony. Scale: F - 5 mm; W - 100 µm; I - 20, microns.

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8. Fig. 7. Results of the pathogenicity test, pieces of soybean leaves, Selecta 201 variety, 14 days after inoculation. Inoculation options: A - negative control, sterile water; B — mycelial suspension of isolate MF 6.1 Stagonosporopsis stuijvenbergii; B — positive control, mycelial suspension of Cercospora cf. sigesbeckiae MF 3.13. The first row in each Petri dish is the inoculum applied to the upper side of the intact segment. Second row - inoculum is applied to the upper side of the segment with preliminary wounding. Third row - inoculum is applied to the underside of the intact segment. Fourth row - inoculum is applied to the underside of the segment with preliminary wounding.

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