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Schroeteria decaisneana, S. poeltii, and Ciboria ploettneriana (Sclerotiniaceae, Helotiales, Ascomycota), three parasites on Veronica seeds: first report of teleomorphs in Schroeteria

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Abstract

Ciboria ploettneriana, Schroeteria decaisneana, and S. poeltii produce morphologically very similar apothecia emerging from fallen stromatized seeds of Veronica spp., the former two on V. hederifolia agg. in temperate central Europe and S. poeltii on V. cymbalaria in mediterranean southern Europe. They are described and illustrated in detail based on fresh collections or moist chamber cultures of infected seeds. A key is provided to differentiate the three species from their teleomorphs. For the first time, connections between two teleomorphs and two Schroeteria anamorphs are reported. Members of the anamorph-typified genus Schroeteria are known as host-specific plant parasites that infect seeds of different Veronica spp. In earlier times, they were classified in the Ustilaginales (Basidiomycota), but since more than 30 years, they are referred to as false smut fungi producing smut-like chlamydospores, based on light microscopic and ultrastructural studies which referred them to the Sclerotiniaceae (Helotiales). During the present study, rDNA sequences were obtained for the first time from chlamydospores of Schroeteria bornmuelleri (on V. rubrifolia), S. decaisneana (on V. hederifolia), S. delastrina (generic type, on V. arvensis), and S. poeltii (on V. cymbalaria) and from apothecia of C. ploettneriana, S. decaisneana, and S. poeltii. As a result, the anamorph-teleomorph connection could be established for S. decaisneana and S. poeltii by a 100% ITS similarity, whereas C. ploettneriana could not be connected to a smut-like anamorph. Ciboria ploettneriana in the here-redefined sense clustered in our combined phylogenetic analyses of ITS and LSU in relationship of Sclerotinia s.l., Botrytis, and Myriosclerotinia rather than Ciboria, but its placement was not supported. Its affiliation in Ciboria was retained until a better solution is found. Also Schroeteria poeltii clustered unresolved in this relationship but with a much higher molecular distance. The remaining three Schroeteria spp. formed a strongly supported monophyletic group, here referred to as “Schroeteria core clade”, which clustered with medium to high support as a sister clade of Monilinia jezoensis, a member of the Monilinia alpina group of section Disjunctoriae. We observed ITS distances of 5–6.3% among members of the Schroeteria core clade, but 13.8–14.7% between this clade and S. poeltii, which appears to be correlated with the deviating chlamydospore morphology of S. poeltii. Despite its apparent paraphyly, Schroeteria is accepted here in a wide sense as a genus distinct from Monilinia, particularly because of its very special anamorphs. A comparable heterogeneity in rDNA analyses was observed in Monilinia and other genera of Sclerotiniaceae. Such apparent heterogeneity should be met with skepticism, however, because the inclusion of protein-coding genes in phylogenetic analyses resulted in a monophyletic genus Monilinia. More sclerotiniaceous taxa should be analysed for protein-coding genes in the future, including Schroeteria. Four syntype specimens of Ciboria ploettneriana in B were reexamined in the present study, revealing a mixture of the two species growing on V. hederifolia agg. Based on its larger ascospores in comparison with S. decaisneana, a lectotype is proposed for C. ploettneriana.

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Data availability

The sequences generated in this study are available in the NCBI GenBank (https://www.ncbi.nlm.nih.gov/genbank/) under the accession numbers given in Table 1.

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Acknowledgements

We want to thank Gunnar Hensel (Merseburg), Lothar Krieglsteiner (Schwäbisch Gmünd-Bettringen), Matthias Reul (Marktredwitz), and Torsten Richter (Rehna) for collecting apothecia and/or sending us their documentations, and Manfred Huth (Freyburg/U.) for culturing infected seeds. Konstanze Bensch (München) and Uwe Braun (Halle) is thanked for supplying a photo of Schröter’s herbarium label of Geminella delastrina and François Valade (Saint-Michel-sur-Orge) for a calibrated copy of Boudier’s illustration of G. delastrina and G. decaisneana. We thank Robert Lücking for sending Kirschstein’s specimens from B, and Jason Grant (Neuchâtel) for Terrier’s specimen from NEU. Thomas Laessøe (Kopenhagen) is thanked for supplying the paper of Buchwald. We are grateful to the members of the Mandragora de Ronda naturalist group for their help in collecting and obtaining data for the Schroeteria poeltii teleomorph and for identification of the associated plants and geology. Finally, Sebastian Ploch (Frankfurt/M.) is thanked for generating the sequences and D. Haelewaters (Cambridge/USA) for calculating a ML analysis with IQ-tree for comparison.

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H.O. Baral made the main morphological evaluation and worked on the taxonomical conclusions, wrote text and tables, arranged most of the plates, and made the molecular analyses and illustration. P. Rönsch and U. Richter wrote a German draft about their observations on the teleomorph of Ciboria ploettneriana and Schroeteria decaisneana. H.O. Baral, P. Rönsch, and G. Hensel documented some of these collections by drawings and/or photographs. W. Huth studied and identified cultured apothecia and supplied data about the ecology of the two species. A. Urban obtained sequences from the teleomorphs of these species and some other Sclerotiniaceae, and J. Kruse from four different anamorphs of Schroeteria spp. and the teleomorph of S. poeltii. F.J. Valencia documented the teleomorph of S. poeltii and arranged the plate. Martin Bemmann contributed variously regarding literature reports and particularly with his hypothesis of an anamorph-teleomorph connection in Schroeteria decaisneana. V. Kummer reexamined and documented original material of Kirschstein’s collections in B and Terrier’s specimen on Veronica campylopoda in NEU.

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Correspondence to Hans-Otto Baral.

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Baral, HO., Rönsch, P., Richter, U. et al. Schroeteria decaisneana, S. poeltii, and Ciboria ploettneriana (Sclerotiniaceae, Helotiales, Ascomycota), three parasites on Veronica seeds: first report of teleomorphs in Schroeteria. Mycol Progress 21, 359–407 (2022). https://doi.org/10.1007/s11557-021-01742-4

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