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Type: Article
Published: 2024-06-18
Page range: 101-114
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Tulostoma subreticulatum (Agaricomycetes, Agaricales): a new species of stalked puffball from Mexico

Laboratorio de Micología, Instituto de Biología, Universidad Nacional Autónoma de México
Universidad Juárez Autónoma de Tabasco
Basidiomycota Gasteromycetes Tulostomataceae Fungi of Tabasco Fungi of Mexico Fungi

Abstract

Tulostoma subreticulatum is a new species to science. This species is characterized by its small to medium-size basidiomes, tubular stoma, verrucose exoperidium with flat and angulose verrucae up to 0.8 mm, reddish-brown endoperidium, and subreticulated 3.8–5 μm basidiospores. This new species was collected in the tropical forest of Tabasco, Mexico. Description of the specimens, macroscopic images of the basidiomes, light microscopy, and scanning electron micrographs are provided. DNA extraction was carried out following a CTAB protocol. GeneBank and newly generated ITS, LSU, and Tef1α sequences were used in Maximum Likelihood and Bayesian Inference analyses. Phylogenetically, T. subreticulatum is related to T. deltaconcavum and forms a sister group from Clade 11 of the monophyletic genus Tulostoma. Comparisons with related sequenced and non-sequenced species are discussed. With this species, a total of 51 species of Tulostoma are known in Mexico.

References

  1. Berkeley, M.J. (1842) Enumeration of fungi, collected by H. Cuming, Esq. F.L.S. in the Philippine Islands. Hooker’s London Journal of Botany 1: 142–157.
  2. Bresadola, J. (1904) Sul valore diagnostico del capillizio nel genere “Tylostoma” Pers. Annales Mycologici 2 (5): 412–438
  3. Cabral, T.S., Barbosa da Silva, B.D., Vargas-Isla, R., Souza de Oliveira, J.J., da Silva Ferreira, J.A., Castro, L., Martin, M.P. & Ishikawa, N.K. (2023) Diversity of Neotropical stalked-puffball: Two new species of Tulostoma with reticulated spores. Plos one 18 (12): e0294672. https://doi.org/10.1371/journal.pone.0294672
  4. Calonge, F.D. & Carranza, J. (2003) Tulostoma matae sp. nov. (Gasteromycetes) found in Costa Rica. Boletín de la Sociedad Micológica de Madrid 27: 37–42.
  5. Castillo-Acosta, O. (1995) Los recursos maderables del estado de Tabasco. Informe técnico, Consejo Nacional de Ciencia y Tecnología. Convenio PC22089. Villahermosa, México. 220 pp.
  6. Castillo, A.O. & Zavala, C.J. (1996) Fisiografía, recursos vegetales y alternativas de manejo en el Parque Estatal Agua Blanca, Tabasco. Universidad y Ciencia 12: 63–70.
  7. Doyle, J.J. & Doyle, J.L. (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11–15.
  8. Dourado-Barbosa, K., Oliveira, R.D.L., Lima, A.D.A.D., Baseia, I.G. & Cruz, R.H.S.F.D. (2023) Tulostoma irregulireticulatum (Agaricaceae, Basidiomycota): a new species from Cerrado Biome of northeastern Brazil. New Zealand Journal of Botany 1–8. https://doi.org/10.1080/0028825X.2023.2198721
  9. Esqueda, M., Moreno, G., Perez-Silva, E., Sanchez, A. & Altes, A. (2004) The genus Tulostoma in Sonora, Mexico. Mycotaxon 90: 409–422.
  10. Fan, L. & Lui, B. (2005) Two new species of Tulostoma from China. Mycosystema 24: 159–161.
  11. Finy, P., Jeppson, M., Knapp, D.G., Papp, V., Albert, L., Ölvedi, I., Bóka, K., Varga, D., Kovács, G.M. & Dima, B. (2023) Exploring diversity within the genus Tulostoma (Basidiomycota, Agaricales) in the Pannonian sandy steppe: four fascinating novel species from Hungary. MycoKeys 100: 153–170. https://doi.org/10.3897/mycokeys.100.112458
  12. Gardes, M. & Bruns, T.D. (1993) ITS primers with enhanced specificity for Basidiomycetes-Application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
  13. Guzmán, G., Montoya, L. & Bandala, V. (1992) Adiciones al conocimiento del género Tulostoma (Basidiomycotina, Gasteromycetes) en México y descripción de una nueva especie. Boletín Sociedad Argentina de Botánica 28: 113–121.
  14. Hennings, P. (1989) Fungi americani-borialis. Hedwigia 37: 274.
  15. Hennings, P. (1901) Fungi Indiae orientalis II. Cl. W. Gollan a. 1900 collecti. Hedwigia 40: 337.
  16. Hernández-Caffot, M.L., Domínguez, L.S., Hosaka, K. & Crespo, E.M. (2011) Tulostoma domingueziae sp. nov. from Polylepis australis woodlands in Cordoba Mountains, central Argentina. Mycologia 103: 1047–1054. https://doi.org/10.3852/10-266
  17. Hernández-Navarro, E., Gutiérrez, A., Ramírez-Prado, J.H., Sánchez-Teyer, F. & Esqueda, M. (2018) Tulostoma rufescens sp. nov. from Sonora, Mexico. Mycotaxon 133: 459–471. https://doi.org/10.5248/133.459
  18. Hernández-Navarro, E. (2023) Primer registro de Tulostoma exasperatum (Agaricaceae, Agaricales) en México. Acta Botanica Mexicana 130: e2171. https://doi.org/10.21829/abm130.2023.2171
  19. Hussain, S., Yousaf, N., Afshan, N.U.S., Niazi, A.R., Ahmad, H. & Khalid, A.N. (2016) Tulostoma ahmadii sp. nov. and T. squamosum from Pakistan. Turkish Journal of Botany 40: 218–225. https://doi.org/10.3906/bot-1501-9
  20. INEGI (1986) Síntesis Cartográfica, Nomenclátor y Anexo Cartográficos del Estado de Tabasco.
  21. INEGI (1994) Cuaderno Estadístico Municipal: Macuspana, Tabasco.
  22. INEGI (2003) Carta Geográfica Estatal Instituto Nacional de Estadística Geografía e Informática. Secretaria de Comunicaciones, Asentamientos y obras públicas de Tabasco, México.
  23. Jeppson, M., Altés, A., Moreno, G., Nilsson, R.H., Loarce, Y., de Bustos, A. & Larsson, E. (2017) Unexpected high species diversity among European stalked puffballs–a contribution to the phylogeny and taxonomy of the genus Tulostoma (Agaricales). MycoKeys 21: 33–88. https://doi.org/10.3897/mycokeys.21.12176
  24. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 14: 587–589. https://doi.org/10.1038/nmeth.4285
  25. Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30 (4): 772–780. https://doi.org/10.1093/molbev/mst010
  26. 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. https://doi.org/10.1093/nar/gkf436
  27. Katoh, K., Rozewicki, J. & Yamada, K.D. (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20: 1160–1166. https://doi.org/10.1093/bib/bbx108
  28. Kornerup, A. & Wanscher, J.H. (1978) Methuen Handbook of Colour. Eyre Methuen. London, UK. 252 pp.
  29. Larsson, E. & Jeppson, M. (2008) Phylogenetic relationships among species and genera of Lycoperdaceae based on ITS and LSU sequence data from north European taxa. Mycological Research 112 (1): 4–22. https://doi.org/10.1016/j.mycres.2007.10.018
  30. Leica Mycrosistems (2023) Leica Aplication Suite v. 4.3.0. Wetzlar, Alemania. Available from: https://www.leica-microsystems.com/es/productos/software-de-microscopia/p/leica-application-suite/downloads/ (accessed 17 June 2024)
  31. Li, F. & Bo, L. (2005) Two new species of Tulostoma from China. Mycosystema 24 (2): 159–161.
  32. Lima, A., Melanda, G., Marinho, P., Martín, M.P. & Baseia, I. (2023) Two new species of Tulostoma (Agaricales, Basidiomycota) from the Neotropics. Turkish Journal of Botany 47 (5): 399c407. https://doi.org/10.55730/1300-008X.2777
  33. Lloyd, G.C. (1906) The Tylostomeae. Mycological Writings 7: 25 1–28.
  34. Long, W.H. (1944) Studies in the Gasteromycetes X. Seven new species of Tylostoma. Mycologia 36: 318–339.
  35. Long, W.H. (1946) Studies in the Gasteromycetes XII: Five new species of Tylostoma with membranous exoperidia. Mycologia 38: 77–90.
  36. Long, W.H. (1947) Studies in the Gasteromycetes. XVII. Two interesting species from Argentina. Lloydia 11: 57–59.
  37. Long, W.H. & Ahmad, S. (1947) The genus Tylostoma in India. Farlowia 3: 225–267.
  38. Maddison, W.P. & Maddison, D.R. (2023) Mesquite: a modular system for evolutionary analysis. Version 3.81. Available from: http://www.mesquiteproject.org (accessed 17 June 2024)
  39. Miranda, F. & Hernández, X. (1963) Los tipos de vegetación de México y su clasificación. Boletín de la Sociedad Botánica de México 28: 29–179. https://doi.org/10.17129/botsci.1084
  40. Montagne, J.P.F.C. (1837) Centurie de plantes exotiques nouvelles. Annales des Sciences Naturelles Botanique 8: 345–370
  41. Moreno, G., Altes, A. & Wright, J.E. (1992a) Tulostoma pseudopulchellum sp. nov. (Tulostomatales, Gasteromycetes) and allied species. Mycotaxon 43: 479–486.
  42. Moreno, G., Altés, A. & Wright, J.E. (1992b) Tulostoma squamosum, T. verrucosum and T. mussooriense are the same species. Mycotaxon 43: 61–68.
  43. Niazi, A.R., Ghafoor, A., Afshan, N.U.S. & Moreno, G. (2022) Tulostoma loonbanglaense: A new species from Azad Jammu and Kashmir using light and scanning electron microscopy and DNA barcoding technique. Microscopy Research and Technique 85: 3720–3725. https://doi.org/10.1002/jemt.24240
  44. Paloi, S., Suwannarach, N., Kumla, J., Phonrob, W., Karunarathna, S.C. & Lumyong, S. (2023) An update on species Diversity, Distribution and Sequence Data of Tulostoma in Asia with the Addition of Tulostoma exasperatum, A New Record for Thailand. Chiang Mai Journal of Science 50: 1–14. https://doi.org/10.12982/CMJS.2023.018
  45. Persoon, C.H. (1794) Dispositio methodica fungorum. Neues Magazin für die Botanik 1: 81–128.
  46. Persoon, D.C. (1801) Synopsis Methodica Fungorum. Gotinga, 708 pp.
  47. Rehner, S.A. & Buckley, E. (2005) A Beauviera phylogeny inferred from nuclear ITS and Tef1–α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97: 84–98.
  48. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029
  49. Saccardo, PA. (1889) Notes mycologiques. Bulletin de la Société Mycologique de France 5 (2): 115–123.
  50. SEDESPA (2000) Áreas Naturales de Tabasco. 15 pp
  51. Schoch, C.L., Seifert, K.A., Huhndorf, S., Robert, V., Spouge, J.L., Levesque, C.A., Chen, W., Fungal Barcoding Consortium, Bolchacova, E., Voigt, K., Crous, P.W., Miller, A.N., Wingfield, M.J., Aime, M.C., An, K., Bai, F.Y., Barreto, R.W., Begerow, D., Bergeron, M.J., Blackwell, M., Boekhout, T., Bogale, M., Boonyuen, N., Burgaz, A.R., Buyck, B., Cai, L., Cai, Q., Cardinali, G., Chaverri, P., Coppins, B.J., Crespo, A., Cubas, P., Cummings, C., Damm, U., de Beer, Z.W., de Hoog, G.S., Del-Prado, R., Dentinger, B., Diéguez-Uribeondo, J., Divakar, P.K., Douglas, B., Dueñas, M., Duong, T.A., Eberhardt, U., Edwards, J.E., Elshahed, M.S., Fliegerova, K., Furtado, M., García, M.A., Ge, Z.W., Griffith, G.W., Griffiths, K., Groenewald, J.Z., Groenewald, M., Grube, M., Gryzenhout, M., Guo, L.D., Hagen, F., Hambleton, S., Hamelin, R.C., Hansen, K., Harrold, P., Heller, G., Herrera, C., Hirayama, K., Hirooka, Y., Ho, H.M., Hoffmann, K., Hofstetter, V., Högnabba, F., Hollingsworth, P.M., Hong, S.B., Hosaka, K., Houbraken, J., Hughes, K., Huhtinen, S., Hyde, K.D., James, T., Johnson, E.M., Johnson, J.E., Johnston, P.R., Jones, E.B.G., Kelly, L.J., Kirk, P.M., Knapp, D.G., Kõljalg, U., Kovács, G.M., Kurtzman, C.P., Landvik, S., Leavitt, S.D., Liggenstoffer, A.S., Liimatainen, K., Lombard, L., Luangsa-ard, J.J., Lumbsch, H.T., Maganti, H., Maharachchikumbura, S.S.N., Martin, M.P., May, T.W., McTaggart, A.R., Methven, A.S., Meyer, W., Moncalvo, J.M., Mongkolsamrit, S., Nagy, L.G., Nilsson, R.H., Niskanen, T., Nyilasi, I., Okada, G., Okane, I., Olariaga, I., Otte, J., Papp, T., Park, D., Petkovits, T., Pino-Bodas, R., Quaedvlieg, W., Raja, H.A., Redecker, D., Rintoul, T.L., Ruibal, C., Sarmiento-Ramírez, J.M., Schmitt, I., Schüßler, A., Shearer, C., Sotome, K., Stefani, F.O.P., Stenroos, S., Stielow, B., Stockinger, H., Suetrong, S., Suh, S.O., Sung, G.H., Suzuki, M., Tanaka, K., Tedersoo, L., Telleria, M.T., Tretter, E., Untereiner, W.A., Urbina, H., Vágvölgyi, C., Vialle, A., Vu, T.D., Walther, G., Wang, Q.M., Wang, Y., Weir, B.S., Weiß, M., White, M.M., Xu, J., Yahr, R., Yang, Z.L., Yurkov, A., Zamora, J.C., Zhang, N., Zhuang, W.Y. & Schindel, D. (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences 109: 6241–6246. https://doi.org/10.1073/pnas.1117018109
  52. Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.
  53. Trifinopoulos, J., Nguyen, L.T., von Haeseler, A. & Minh, B.Q. (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44: W232–W235. https://doi.org/10.1093/nar/gkw256
  54. Vlasenko, V.A. & Vlasenko, A.V. (2023) A new species of Tulostoma genus from Siberia. Phytotaxa 600: 25–34. https://doi.org/10.11646/phytotaxa.600.1.4
  55. White, V.S. (1901) The Tylostomataceae of North America. Bulletin of the Torrey Botanical Club 28 (8): 421–444.
  56. Wright, J.E. (1987) The genus Tulostoma (Gasteromycetes): a world monograph. Stuttgart: J Cramer. Berlin, Germany. 338 pp.
  57. Zarco-Espinosa, V.M., Valdez-Hernández, J.I., Ángeles-Pérez, G. & Castillo-Acosta, O. (2010) Estructura y diversidad de la vegetación arbórea del Parque Estatal Agua Blanca, Macuspana, Tabasco. Universidad y Ciencia 26: 1–17.