Updated data on the diversity and distribution of lycoperdon s. L. In russia, with the description of a new species, lycoperdon bulakhiae

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

The study of collection materials from LE, YSU, MAG, and YuR, using a combination of morphological and molecular genetic methods, led to the recording of Lycoperdon subumbrinum as a new species for Russia from the territory of Yugra and the Magadan region, confirmed the records of L. rupicola and L. marginatum, and refined the geographic distribution of several other species. A new species, L. bulakhiae, was discovered and described. It is widespread across Asian Russia and morphologically and genetically close to L. caudatum but differs in having thin, short exoperidial spines and more elongated spores. An examination of the original label of the L. yasudae specimen stored in VLA, which was previously listed for Russia, revealed that it actually originates from South Korea. It was excluded from the species list. The phylogenetic and taxonomic positions of the noteworthy species L. estonicum, L. cf. gulmargense and L. aff. molle were discussed. Since the taxonomy of Lycoperdaceae remains unstable, Apioperdon, Bovistella, Morganella, Vascellum, Utraria and newly described at the end of 2024 genera are treated as part of Lycoperdon s. l., and its species list in Russia contains at least 36 species.

Full Text

Restricted Access

About the authors

E. A. Zvyagina

Moscow State University; Yugra State University

Author for correspondence.
Email: mycena@yandex.ru
Russian Federation, Moscow; Khanty-Mansiysk

Yu. A. Rebriev

Southern Scientific Centre of Russian Academy of Sciences

Email: rebriev@yandex.ru
Russian Federation, Rostov-on-Don

References

  1. Ahmad S. Gasteromycetes from the Western Himalayas II. J. Indian Bot. Soc. 1942. V. 21. P. 283–293.
  2. Alfredo D.S. Revisão do Gênero Lycoperdon Pers. (Lycoperdaceae, Agaricales) Mediante Análises Morfológicas e Moleculares. Tese (Doutorado em Sistemática e Evolução). Centro de Biociências, Universidade Federal do Rio Grande do Norte, Natal, 2017.
  3. Bates S.T., Roberson R.W., Desjardin D.E. Arizona gasteroid fungi I: Lycoperdaceae (Agaricales, Basidiomycota). Fungal Diversity. 2009. V. 37. P. 153–207.
  4. Benson D.A., Cavanaugh M., Clark K., et al. GenBank. Nucleic Acids Res. 2013 V. 41. (Database issue). P. D36–D42. https://doi: 10.1093/nar/gks1195
  5. Bisht D., Sharma J., Kreisel H. et al. A new species and a new record of Lycoperdaceae from India. Mycotaxon. 2006. V. 95. P. 91–96.
  6. Clements T.A. Lycoperdon excipuliforme voucher MO502016 internal transcribed spacer 1, partial sequence; 5.8S ribosomal RNA gene and internal transcribed spacer 2, complete sequence; and large subunit ribosomal RNA gene, partial sequence. NCBI. 2023. https://www.ncbi.nlm.nih.gov/nuccore/OR203571. Accessed 11.11.2024.
  7. Demoulin V. Le genre Lycoperdon en Europe et en Amérique du Nord. Étude Taxonomique et Phytogéographique. Dr. Sci. Thesis. Université de Liège, 1971.
  8. Demoulin V. Especes nouvelles ou meconnues du genre Lycoperdon (Gasteromycetes). Lejeunia. 1972. V. 62. P. 1–30.
  9. Dirks A., Russell S. DNA barcoding of macrofungi from the 2018 Smith Foray: New fungal records for Wisconsin and the United States of America. The Great Lakes Botanist. 2020. V. 59. P. 191–201.
  10. Dirks A.C. Lycoperdon perlatum voucher MICH:340466 small subunit ribosomal RNA gene, partial sequence; internal transcribed spacer 1, 5.8S ribosomal RNA gene, and internal transcribed spacer 2, complete sequence; and large subunit ribosomal RNA gene, partial sequence. Alden Dirks Personal Collection. NCBI. 2022. https://www.ncbi.nlm.nih.gov/nuccore/MT913627 Accessed 11.11.2024.
  11. Gardes M., Bruns T.D. ITS primers with enhanced specificity for basidiomycetes application to the identification of mycorrhizae and rusts. Mol. Ecol. 1993. V. 2. P. 132–118. 10.1111/j.1365-294x.1993.tb00005.x' target='_blank'>https://doi: 10.1111/j.1365-294x.1993.tb00005.x
  12. GBIF Occurrence Download. 2025. https://doi.org/10.15468/dl.q8gx8f. Accessed 11.11.2024
  13. Hofstetter V., Buyck B., Eyssartier G. et al. The unbearable lightness of sequenced-based identification. Fungal Diversity. 2019. V. 96. P. 243–284. https://doi.org/10.1007/s13225-019-00428-3
  14. Hyde K.D., Noorabadi M.T., Thiyagaraja V. et al. The 2024 Outline of Fungi and fungus-like taxa. Mycosphere. 2024. V. 15 (1). P. 5146–6239. https://doi.org/10.5943/mycosphere/15/1/25
  15. Jeppson M., Larsson E., Martin M.P. Lycoperdon rupicola and L. subumbrinum: two new puffballs from Europe. Mycol. Prog. 2012. V. 11. P. 887–897.
  16. Kalyaanamoorthy S., Minh B., Wong T. et al. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods. 2017. V. 14. P. 587–589. https://doi.org/10.1038/nmeth.4285
  17. Kasuya T., Kawahara E., Toga N. et al. The genus Lycoperdon (Basidiomycota, Agaricales) in the alpine zone of Mt. Hakusan, central Japan. Ann. Rep. Hakusan Nat. Conserv. Ctr. 2016. V. 42. P. 23–31.
  18. Kasuya T., Nakajima Y., Kawahara E. et al. Bryoperdon acuminatum (Lycoperdaceae), a new record for Japan. Japanese J. Mycology. 2023. V. 64 (1). P. 15–21. https://doi.org/10.18962/jjom.jjom.R4-9
  19. Katoh K., Rozewicki J., Yamada K.D. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics. 2019. V. 20. P. 1160–1166. https://doi.org/10.1093/bib/bbx108
  20. Kim C.S., Jo J.W., Kwag Y.-N. et al. Two new Lycoperdon species collected from Korea: L. albiperidium and L. subperlatum spp. nov. Phytotaxa. 2016. V. 260 (2). P. 101–115. http://dx.doi.org/10.11646/phytotaxa.260.2.1
  21. Kimura M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Molec. Evol. 1980. V. 16. P. 111–120.
  22. Kirk P.M., Cannon P.F., Minter D.W. et al. Ainsworth and Bisby’s Dictionary of the Fungi. 10th Edition. CABI-Wallingford, 2008.
  23. Kotkova V.M., Chernyadyeva I.V., Davydov E.A. et al. Novyye nakhodki vodorosley, gribov, lishaynikov i mokhoobraznykh. 11. Novosti sistematiki nizshikh rasteniy. 2023. V. 57 (1). P. 155–204. (In Russ.) https://doi.org/10.31111/nsnr/2023.57.1.155
  24. Krakhmalnyi M., Isikhuemhen O.S., Jeppson M. et al. Species Diversity of Lycoperdaceae (Agaricales) in Israel, with some insights into the phylogenetic structure of the family. J. Fungi. 2023. V. 9 (10). P. 1038. https://doi.org/10.3390/jof9101038
  25. Kreisel H.L. Gasteromyzeten aus Nepal. Khumbu Himal. 1969. V. 6. P. 25–36.
  26. Landry J., Berube J. Lycoperdon caudatum voucher ANT254-QFB28773 small subunit ribosomal RNA gene, partial sequence; internal transcribed spacer 1, 5.8S ribosomal RNA gene, and internal transcribed spacer 2, complete sequence; and large subunit ribosomal RNA gene, partial sequence. NCBI. 2020. URL: https://www.ncbi.nlm.nih.gov/nuccore/MN992462. Accessed 11.11.2024.
  27. Larsson E., Jeppson M. Phylogenetic relationships among species and genera of Lycoperdaceae based on ITS and LSU sequence data from north European taxa. Mycol. Res. 2008. V. 112. P. 4–22.
  28. Li J.X., Cao B., Phurbu D. et al. The revision of the taxonomic system of Lycoperdaceae. Mycosphere. 2024. V. 15 (1). P. 4919–5016. https://doi.org/10.5943/mycosphere/15/1/22
  29. Lloyd C.G. Mycological Writings. 1906. V. 2 (Letter 23). P. 282.
  30. Omeonu F.C., Jonathan S.G., Azuh V.O. Lycoperdon rimulatum isolate FFUI_-1 small subunit ribosomal RNA gene, partial sequence; internal transcribed spacer 1, 5.8S ribosomal RNA gene, and internal transcribed spacer 2, complete sequence; and large subunit ribosomal RNA gene, partial sequence. Anti ulcer and blood busting activities of selected higher fungi. NCBI. 2019. URL: https://www.ncbi.nlm.nih.gov/nuccore/MN596942. Accessed 11.11.2024.
  31. Rebriev Yu.A. Gasteromycetes of the genus Calvatia in Russia. Mikologiya i fitopatologiya. 2013. V. 47 (4). P. 231–239. (In Russ.)
  32. Rebriev Y.A., Gorbunova I.A. The gasteromycetes on the south of the Western and Average Siberia. Siberian Botanical Bulletin: an electronic journal. 2007. V. 2 (1). P. 51–60. (In Russ.)
  33. Rebriev Yu.A. Gasteromycetes of the genus Lycoperdon in Russia. Mycologia i fitopathologia. 2016. V. 50 (5). P. 302– 312. (In Russ.)
  34. Rebriev Yu., Zai-Wei G., Voronina E. et al. An annotated key to the Bovista (Lycoperdaceae, Basidiomycota) species in Russia. Phytotaxa. 2020. V. 464. P. 1–28. https://doi.org/10.11646/phytotaxa.464.1.1
  35. Rebriev Yu.A., Bulakh E.M. Morganella sosinii sp. nov. from the Russian Far East. Mikologiya i fitopatologiya. 2015. V. 49 (5). P. 293–296.
  36. Rebriev Yu.A., Bulakh E.M., Gorbunova I.A. et al. Rare species of gasteromycetes in asian part of Russia. Mikologiya i fitopatologiya. 2018. V. 52 (5). P. 349–355. (In Russ.) https://doi.org/10.1134/S0026364818050069
  37. Rivas-Ferreiro M. Lycoperdon rupicola voucher MRF402 small subunit ribosomal RNA gene, partial sequence; internal transcribed spacer 1, 5.8S ribosomal RNA gene, and internal transcribed spacer 2, complete sequence; and large subunit ribosomal RNA gene, partial sequence. A little surprise: Lycoperdon rupicola cited for the first time in Galicia (NW Iberian Peninsula). NCBI. 2023. URL: https://www.ncbi.nlm.nih.gov/nuccore/OR518420. Accessed 11.11.2024.
  38. Ronquist F., Teslenko M., van der Mark P. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biol. 2012. V. 61. P. 539–542. https://doi.org/10.1093/sysbio/sys029
  39. Sharma B.M. A new species of Lycoperdon from India. Mycol. Res. 1991. V. 95. P. 1144–1145.
  40. Shi L. Lycoperdon molle isolate HBAU15544 internal transcribed spacer 1, partial sequence; 5.8S ribosomal RNA gene and internal transcribed spacer 2, complete sequence; a nd large subunit ribosomal RNA gene, partial sequence. NCBI. 2021. URL: https://www.ncbi.nlm.nih.gov/nuccore/MZ145083. Accessed 11.11.2024.
  41. Tamura K., Stecher G., Kumar S. MEGA 11: Molecular Evolutionary Genetics Analysis Version 11. Molec. Biol. Evol. 2021. V. 38 (7). P. 3022–3027. https://doi.org/10.1093/molbev/msab120
  42. Thind K.S., Thind I.P.S. The Gasteromycetes of the Himalayas – VII. Indian Phytopath. 1987. V. 40 (4). P. 451–458.
  43. Trifinopoulos J., Nguyen L.T., von Haeseler A. et al. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucl. Acids Res. 2016. V. 44 (W1). P. W232–W235. https://doi: 10.1093/nar/gkw256
  44. Vlasenko V.A. Lycoperdon molle voucher NSK 1017218 small subunit ribosomal RNA gene, partial sequence; internal transcribed spacer 1, 5.8S ribosomal RNA gene, and internal transcribed spacer 2, complete sequence; and large subunit ribosomal RNA gene, partial sequence. NCBI. 2022a. URL: https://www.ncbi.nlm.nih.gov/nuccore/OP725695. Accessed 11.11.2024.
  45. Vlasenko V.A. Lycoperdon perlatum voucher NSK 1017224 small subunit ribosomal RNA gene, partial sequence; internal transcribed spacer 1, 5.8S ribosomal RNA gene, and internal transcribed spacer 2, complete sequence; and large subunit ribosomal RNA gene, partial sequence. NCBI. 2022b. URL: https://www.ncbi.nlm.nih.gov/nuccore/OP725697. Accessed 11.11.2024.
  46. White T.J., Bruns T., Lee S. et al. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: a Guide to Methods and Applications. N.Y., Acad. Press, 1990. P. 315–322.
  47. Yasuda A. Miscellaneous notes on Fungi 127. Botanical Magazine. 1922. V. 36. P. 177–178.
  48. Ребриев Ю.А., Булах Е.М., Горбунова И.А. и др. (Rebriev et al.) Редкие виды гастеромицетов из Азиатской части России // Микология и фитопатология. 2018. Т. 52. № 5. С. 349–355.
  49. Ребриев Ю.А. (Rebriev) Гастеромицеты рода Lycoperdon в России // Микология и фитопатология. 2016. Т. 50. № 5. С. 302–312.
  50. Ребриев Ю.А. (Rebriev) Гастеромицеты рода Сalvatia в России // Микология и фитопатология. 2013. Т. 47. № 4. С. 231–239.
  51. Ребриев Ю.А., Горбунова И.А. (Rebriev, Gorbunova) Гастеромицеты юга Западной и Средней Сибири // Сибирский ботанический вестник: электронный журнал. 2007. Т. 2. Вып. 1. С. 51–60.

Supplementary files

Supplementary Files
Action
1. JATS XML
2. Fig. 1. Lycoperdon s. l. Bayesian ITS rDNA phylogenetic tree. Posterior probability/bootstrap support are above the branches. For the collapsed clades, see Fig. 2.

Download (379KB)
3. Fig. 2. Lycoperdon s. l. Bayesian ITS rDNA phylogenetic tree. Posterior probability/bootstrap support are above the branches. For the collapsed clade, see Fig.1. The type specimens are pointed with asterisk. The novel species is in grey box.

Download (310KB)
4. Fig. 3. Basidiomata in situ, herbarium specimens and spores on SEM of the L. bulakhiae: a, d – YSU-F-08614 (holotype); b, c – YSU-F-1304) in left and L. caudatum (е – YSU-F-8724, f, g, h – YuR3479) in right. Scale bars a, b, e, f – 1 cm; c, g – 1 mm; d, h – 5 μm.

Download (843KB)
5. Fig. 4. Basidiomata in situ of Lycoperdon aff. molle YSU-EZ-1041 (a), L. subumbrinum YSU-F-08077 (b) and dried specimens L. estonicum LE305418 (c), L. yasudae VLA-M-21509 (d). Scale bars – 1 cm.

Download (294KB)
6. Fig. 5. Spores of Lycoperdon aff. molle YSU-EZ-1041 (a), L. subumbrinum YSU-F-08077 (b), L. estonicum holotype TAAM071974 (c), and L. yasudae VLA-M-21509 (d) under SEM. Scale bar – 5 μm.

Download (173KB)

Copyright (c) 2025 Russian Academy of Sciences