Abstract
Matsutake fungi include a complex of edible mushrooms highly prized worldwide, particularly in Japan where they are considered one of the most luxurious ingredients. These species establish ectomycorrhizal symbioses with angiosperms and gymnosperms in the Northern Hemisphere and in North America only three species are currently known. In the present contribution a fourth species of this geographical area is described, Tricholoma colposii sp. nov. is described from Veracruz state, in eastern Mexico based on morphological and molecular (nrITS) data. This species is characterized by middle size basidiomata, with orange brown to brown pileus and stipe, squamose when young and with appressed scales in maturity, cylindric, fibrillous to scaly stipe, with globose to ellipsoid (4.5–)5–6 (–7) × (3–) 4–5 (–6) μm smooth spores, sporomes with sweet fruit odor and raw green bean flavour. The species grows associated with Pinus teocote forests. The macro- and micromorphological characters in conjunction with the nrITS-based phylogenetic analysis using Maximum Likelihood method and Bayesian inference support the proposal of this new species of Mexican matsutake. Detailed descriptions, photographs and comparisons with phenetic and phylogenetic related species are presented.
References
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Binder, M., Hibbett, D.S., Wang, Z. & Farnham, W. (2006) Evolutionary relationships of Mycaureola dilseae (Agaricales), a basidiomycete pathogen of a subtidal rhodophyte. American Journal of Botany 93: 547–556. https://dx.doi.org/10.3732/ajb.93.4.547
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Christensen, M. & Heilmann-Clausen, J. (2013) The genus Tricholoma. In: Fungi of Northern Europe, vol. 4. Svampetryk, Denmark.
Doðan, H.H. & Akata, I. (2011) Ecological features of Tricholoma anatolicum in Turkey. African Journal of Biotechnology 10: 12626?12638. https://dx.doi.org/10.5897/AJB11.1001
Frandsen, P.B., Calcott, B., Mayer, C. & Lanfear, R. (2015) Automatic selection of partitioning schemes for phylogenetic analyses using iterative k-means clustering of site rates. BMC Evolutionary Biology 15: 1?17. https://doi.org/10.1186/s12862-015-0283-7
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Garnica, S., Weiss, M., Walther, G. & Oberwinkler, F. (2007) Reconstructing the evolution of agarics from nuclear gene sequences and basidiospore ultrastructure. Mycological Research 111: 1019–1029. https://dx.doi.org/10.1016/j.mycres.2007.03.019
Gernandt, D.S. & Pérez-de la Rosa, J.A. (2014) Biodiversidad de Pinophyta (coníferas) en México. Revista Mexicana de Biodiversidad 85: 126?133. https://doi.org/10.7550/rmb.32195
Heilmann-Clausen, J., Christensen, M., Froslev, T.G. & Kjoller, R. (2017) Taxonomy of Tricholoma in northern Europe based on ITS sequence data and morphological characters. Persoonia 38: 38–57. https://dx.doi.org/10.3767/003158517X693174
Hofstetter, V., Clémençon, H., Vilgalys, R. & Moncalvo, J. (2002) Phylogenetic analyses of the Lyophylleae (Agaricales, Basidiomycota) based on nuclear and mitochondrial rDNA. Mycological Research 106: 1043–1059. https://dx.doi.org/10.1017/S095375620200641X
Intini, M., Dogan, H.H. & Riva, A. (2003) Tricholoma anatolicum spec. nov.: un nuovo membro del gruppo matsutake. Micologia e Vegetazione Mediterranea 18: 135–142.
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Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772?780. https://doi.org/10.1093/molbev/mst010
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Kikuchi, K., Matsushita, N., Guerin-Laguette, A., Ohta, A. & Suzuki, K. (2000) Detection of Tricholoma matsutake by specific ITS primers. Mycological Research 104: 1427–1430.
Kytövuori, I. (1989) The Tricholoma caligatum group in Europe and North Africa. Karstenia 28: 65–77. https://doi.org/10.29203/ka.1988.266
Lanfear, R., Calcott, B., Kainer, D., Mayer, C. & Stamatakis, A. (2014) Selecting optimal partitioning schemes for phylogenomic datasets. BMC Evolutionary Biology 14: 1?14. https://doi.org/10.1186/1471-2148-14-82
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2017) Partition Finder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34: 772?773. https://doi.org/10.1093/molbev/msw260
Lodge, D.J., Ammirati, J.F., Dell, T.O. & Mueller, G.M. (2004) Terrestrial and Lignicolous Macrofungi: Colecting and describing macrofungi. In: Mueller, G., Bills, G.F. & Foster, M.S. (Eds.) Biodiversity of Fungi. Inventary and Monitoring Methods. Elsevier Academic Press pp. 128–158.
Lodge, D.J., Padamsee, M., Matheny, P.B., Aime, M.C., Cantrell, S.A., Boertmann, D., Kovalenko, A., Vizzini, A., Dentinger, B.T.M., Kirk, P.M., Ainsworth, A.M., Moncalvo, J.-M., Vilgalys, R., Larsson, E., Lücking, R., Griffith, G.W., Smith, M.E., Norvell, L.L., Desjardin, D.E., Redhead, S.A., Ovrebo, C.L., Lickey, E.B., Ercole, E., Hughes, K.W., Courtecuisse, R., Young, A., Binder, M., Minnis, A.M., Lindner, D.L., Ortiz-Santana, B., Haight, J., Læssøe, T., Baroni, T.J., Geml, J. & Hattori, T. (2014) Molecular phylogeny, morphology, pigment chemistry and ecology in Hygrophoraceae (Agaricales). Fungal Diversity 64: 1–99. https://dx.doi.org/10.1007/s13225-013-12559-0
Martínez-González, C.R., Ramírez-Mendoza, R., Jiménez-Ramírez, J., Gallegos-Vázquez, C. & Luna-Vega, I. (2017) Improved method for genomic DNA extraction for Opuntia Mill. (Cactaceae). Plant Methods 13: 1?10. https://doi.org/10.1186/s13007-017-0234-y
Matheny, P.B., Curtis, J.M., Hofstetter, V., Aime, M.C., Moncalvo, J.-M., Ge, Z.-W., Slot, J.C., Ammirati, J.F., Baroni, T.J., Bougher, N.L., Hughes, K.W., Lodge, D.J., Kerrigan, R.W., Seidl, M.T., Aanen, D.K., DeNitis, M., Daniele, G.M., Desjardin, D.E., Kropp, B.R., Norvell, L.L., Parker, A., Vellinga, E.C., Vilgalys, R. & Hibbett, D.S. (2006) Major clades of Agaricales: A multilocus phylogenetic overview. Mycologia 98: 982–995. https://dx.doi.org/10.3852/mycologia.98.6.982
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Moncalvo, J.-M., Vilgalys, R., Redhead, S.A, Johnson, J.E., James, T.Y., Catherine Aime, M., Hofstetter, V., Verduin, S.J.W., Larsson, E., Baroni, T.J., Greg Thorn, R., Jacobsson, S., Clémençon, H. & Miller, O.K. (2002) One hundred and seventeen clades of euagarics. Molecular Phylogenetics and Evolution 23: 357–400. https://dx.doi.org/10.1016/S1055-7903(02)00027-1
Müller, K., Quandt, D., Müller, J. & Neinhuis, C. (2005) PhyDE®-Phylogenetic data editor. Program distributed by the authors, versión 10.0. Available from: https://www.phyde.de (accessed 16 February 2022).
Murata, H., Ota, Y., Yamaguchi, M., Yamada, A., Katahata, S., Otsuka, Y., Babasaki, K. & Neda, H. (2013) Mobile DNA distributions refine the phylogeny of “matsutake” mushrooms, Tricholoma sect. Caligata. Mycorrhiza 23: 447–461. https://doi.org/10.1007/s00572-013-0487-x
Pérez-Moreno, J., Guerin-Laguette, A., Rinaldi, A.C., Yu, F., Verbeken, A., Hernández-Santiago, F. & Martínez-Reyes, M. (2021b) Edible mycorrhizal fungi of the world: What is their role in forest sustainability, food security, biocultural conservation and climate change? Plants People Planet. 3: 471?490. https://doi.org/10.1002/ppp3.10199
Pérez-Moreno, J., Martínez-Reyes, M., Yescas-Pérez, A., Delgado-Alvarado, A. & Xoconostle-Cázares, B. (2008) Wild mushroom markets in Central Mexico and a case study at Ozumba. Economic Botany 62: 425–436. https://doi.org/10.1007/s12231-008-9043-6
Pérez-Moreno, J., Mortimer, P.E., Xu, J., Karunarathna, S.C. & Li, H. (2021a) Global perspectives on the ecological, cultural, and socioeconomic relevance of wild edible fungi. Studies in Fungi 6: 408–424. https://doi.org/10.5943/sif/6/1/31
Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. (2014) Tracer v1.6. Available from: http://beast.bio.ed.ac.uk/Tracer (accessed 16 February 2022).
Ryberg, M. & Matheny, P.B. (2011) Asynchronous origins of ectomycorrhizal clades of Agaricales. Proceedings of the Royal Society B 279: 2013–2011. https://doi.org/10.1098/rspb.2011.2428
Sánchez-García, M., Matheny, P.B., Palfner, G. & Lodge, D.J. (2014) Deconstructing the Tricholomataceae (Agaricales) and introduction of the new genera Albomagister, Corneriella, Pogonoloma and Pseudotricholoma. Taxon 63: 993?1007. https://doi.org/10.12705/635.635.3
Sandor, S.R., Wang, H., Vaario, L., Trudell, S.A. & Xu, J. (2020) Mitochondrial multilocus DNA sequence analyses reveal limited genetic variability within and consistent differences between species of the global matsutake species complex. Acta Edulis Fungi 27: 1–19.
Sanmee R, Dell B, Lumyong P & Lumyong S (2007) First record of Tricholoma fulvocastaneum from Thailand. Mycoscience 48: 131–133. https://doi.org/10.1007/s10267-006-0341-5
Singer, R. (1986) The Agaricales in modern taxonomy. Königstein: Koeltz Scientific Books, 981 pp.
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312?1313. https://doi.org/10.1093/bioinformatics/btu033
Staude, F. (1857) Die Schwämme Mitteldeutschlands, in besondere des Herzogthums. Coburg, Germany, 150 pp.
Tedersoo, L., May, T.W. & Smith, M.E. (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20: 217–263.
Trudell, S.A., Xu, J., Saar, I., Justo, A. & Cifuentes, J. (2017) North American matsutake: names clarified and a new species described. Mycologia 109: 379?390. https://doi.org/10.1080/00275514.2017.1326780
Valencia, A.S. (2004) Diversidad del género Quercus (Fagaceae) en México. Boletín de la Sociedad Botánica de México 75: 33?53. https://dx.doi.org/10.17129/botsci.1692
Villarreal, L. & Pérez-Moreno, J. (1989) Aprovechamiento y conservación del matsutake americano (Tricholoma magnivelare) en los bosques de México. Micología Neotropical Aplicada 2: 131?144.
Wang, Y., Yu FQ., Zhang, CX & Li SH. (2017) Tricholoma matsutake: an edible mycorrhizal mushroom of high socioeconomic relevance in China. Scientia Fungorum 46: 55?61
White, T.J., Bruns, T.D., Lee, S.B. & Taylor, J.W. (1990) Amplification and direct sequencing of fungal ribosomal RNA Genes for phylogenetics. In: Protocols and Applications - A Laboratory Manual. Publisher: Academic Press. pp. 315?322.
Zhang, S., Bai, X., Ren LY., Sun HH., Tang HT., Vaario LM., Xu, J. & Zhang YJ. (2021) Dynamic evolution of eukaryotic mitochondrial and nuclear genomes: a case study in the gourmet pine mushroom Tricholoma matsutake. Environmental Microbiology 23: 7214–7230.
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Bergius, N. & Danell, E. (2000) The Swedish matsutake (Tricholoma nauseosum syn. T. matsutake): Distribution, Abundance and Ecology. Scandinavian Journal of Forest Research 15: 318?325. https://dx.doi.org/10.1080/028275800447940
Binder, M., Hibbett, D.S., Wang, Z. & Farnham, W. (2006) Evolutionary relationships of Mycaureola dilseae (Agaricales), a basidiomycete pathogen of a subtidal rhodophyte. American Journal of Botany 93: 547–556. https://dx.doi.org/10.3732/ajb.93.4.547
Bon, M. (1991) Flore mycologique d’Europe. 2. Les tricholomes et ressemblants. Tricholomataceae (Fayod) Heim (1ère partie). Doc Mycol, Mémoire hors série no 2. Edité par l’association d’écologie et mycologie, Lille.
Christensen, M. & Heilmann-Clausen, J. (2012) Tricholoma (Fr.) P. Kumm. In: Vesterholt, J. & Knudsen, H. (Eds.) Funga Nordica. 2nd edn. Nordsvamp, Copenhagen, Denmark. pp. 494–510.
Christensen, M. & Heilmann-Clausen, J. (2013) The genus Tricholoma. In: Fungi of Northern Europe, vol. 4. Svampetryk, Denmark.
Doðan, H.H. & Akata, I. (2011) Ecological features of Tricholoma anatolicum in Turkey. African Journal of Biotechnology 10: 12626?12638. https://dx.doi.org/10.5897/AJB11.1001
Frandsen, P.B., Calcott, B., Mayer, C. & Lanfear, R. (2015) Automatic selection of partitioning schemes for phylogenetic analyses using iterative k-means clustering of site rates. BMC Evolutionary Biology 15: 1?17. https://doi.org/10.1186/s12862-015-0283-7
Fries, E. (1821) Systema Mycologicum. Lundoe, Sweden. 520 pp.
Garnica, S., Weiss, M., Walther, G. & Oberwinkler, F. (2007) Reconstructing the evolution of agarics from nuclear gene sequences and basidiospore ultrastructure. Mycological Research 111: 1019–1029. https://dx.doi.org/10.1016/j.mycres.2007.03.019
Gernandt, D.S. & Pérez-de la Rosa, J.A. (2014) Biodiversidad de Pinophyta (coníferas) en México. Revista Mexicana de Biodiversidad 85: 126?133. https://doi.org/10.7550/rmb.32195
Heilmann-Clausen, J., Christensen, M., Froslev, T.G. & Kjoller, R. (2017) Taxonomy of Tricholoma in northern Europe based on ITS sequence data and morphological characters. Persoonia 38: 38–57. https://dx.doi.org/10.3767/003158517X693174
Hofstetter, V., Clémençon, H., Vilgalys, R. & Moncalvo, J. (2002) Phylogenetic analyses of the Lyophylleae (Agaricales, Basidiomycota) based on nuclear and mitochondrial rDNA. Mycological Research 106: 1043–1059. https://dx.doi.org/10.1017/S095375620200641X
Intini, M., Dogan, H.H. & Riva, A. (2003) Tricholoma anatolicum spec. nov.: un nuovo membro del gruppo matsutake. Micologia e Vegetazione Mediterranea 18: 135–142.
Huelsenbeck, J.P. & Ronquist, F. (2001) MrBayes: Bayesian inference of phylogeny. Bioinformatics 17: 754?755. https://doi.org/10.1093/bioinformatics/17.8.754
Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772?780. https://doi.org/10.1093/molbev/mst010
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
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
Kikuchi, K., Matsushita, N., Guerin-Laguette, A., Ohta, A. & Suzuki, K. (2000) Detection of Tricholoma matsutake by specific ITS primers. Mycological Research 104: 1427–1430.
Kytövuori, I. (1989) The Tricholoma caligatum group in Europe and North Africa. Karstenia 28: 65–77. https://doi.org/10.29203/ka.1988.266
Lanfear, R., Calcott, B., Kainer, D., Mayer, C. & Stamatakis, A. (2014) Selecting optimal partitioning schemes for phylogenomic datasets. BMC Evolutionary Biology 14: 1?14. https://doi.org/10.1186/1471-2148-14-82
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2017) Partition Finder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34: 772?773. https://doi.org/10.1093/molbev/msw260
Lodge, D.J., Ammirati, J.F., Dell, T.O. & Mueller, G.M. (2004) Terrestrial and Lignicolous Macrofungi: Colecting and describing macrofungi. In: Mueller, G., Bills, G.F. & Foster, M.S. (Eds.) Biodiversity of Fungi. Inventary and Monitoring Methods. Elsevier Academic Press pp. 128–158.
Lodge, D.J., Padamsee, M., Matheny, P.B., Aime, M.C., Cantrell, S.A., Boertmann, D., Kovalenko, A., Vizzini, A., Dentinger, B.T.M., Kirk, P.M., Ainsworth, A.M., Moncalvo, J.-M., Vilgalys, R., Larsson, E., Lücking, R., Griffith, G.W., Smith, M.E., Norvell, L.L., Desjardin, D.E., Redhead, S.A., Ovrebo, C.L., Lickey, E.B., Ercole, E., Hughes, K.W., Courtecuisse, R., Young, A., Binder, M., Minnis, A.M., Lindner, D.L., Ortiz-Santana, B., Haight, J., Læssøe, T., Baroni, T.J., Geml, J. & Hattori, T. (2014) Molecular phylogeny, morphology, pigment chemistry and ecology in Hygrophoraceae (Agaricales). Fungal Diversity 64: 1–99. https://dx.doi.org/10.1007/s13225-013-12559-0
Martínez-González, C.R., Ramírez-Mendoza, R., Jiménez-Ramírez, J., Gallegos-Vázquez, C. & Luna-Vega, I. (2017) Improved method for genomic DNA extraction for Opuntia Mill. (Cactaceae). Plant Methods 13: 1?10. https://doi.org/10.1186/s13007-017-0234-y
Matheny, P.B., Curtis, J.M., Hofstetter, V., Aime, M.C., Moncalvo, J.-M., Ge, Z.-W., Slot, J.C., Ammirati, J.F., Baroni, T.J., Bougher, N.L., Hughes, K.W., Lodge, D.J., Kerrigan, R.W., Seidl, M.T., Aanen, D.K., DeNitis, M., Daniele, G.M., Desjardin, D.E., Kropp, B.R., Norvell, L.L., Parker, A., Vellinga, E.C., Vilgalys, R. & Hibbett, D.S. (2006) Major clades of Agaricales: A multilocus phylogenetic overview. Mycologia 98: 982–995. https://dx.doi.org/10.3852/mycologia.98.6.982
Moncalvo, J.M., Lutzoni, F.M., Rehner, S.A., Johnson, J. & Vilgalys, R. (2000) Phylogenetic relationships of agaric fungi based on nuclear large subunit ribosomal DNA sequences. Systematic Biology 49: 278–305. https://dx.doi.org/10.1093/sysbio/49.2.278
Moncalvo, J.-M., Vilgalys, R., Redhead, S.A, Johnson, J.E., James, T.Y., Catherine Aime, M., Hofstetter, V., Verduin, S.J.W., Larsson, E., Baroni, T.J., Greg Thorn, R., Jacobsson, S., Clémençon, H. & Miller, O.K. (2002) One hundred and seventeen clades of euagarics. Molecular Phylogenetics and Evolution 23: 357–400. https://dx.doi.org/10.1016/S1055-7903(02)00027-1
Müller, K., Quandt, D., Müller, J. & Neinhuis, C. (2005) PhyDE®-Phylogenetic data editor. Program distributed by the authors, versión 10.0. Available from: https://www.phyde.de (accessed 16 February 2022).
Murata, H., Ota, Y., Yamaguchi, M., Yamada, A., Katahata, S., Otsuka, Y., Babasaki, K. & Neda, H. (2013) Mobile DNA distributions refine the phylogeny of “matsutake” mushrooms, Tricholoma sect. Caligata. Mycorrhiza 23: 447–461. https://doi.org/10.1007/s00572-013-0487-x
Pérez-Moreno, J., Guerin-Laguette, A., Rinaldi, A.C., Yu, F., Verbeken, A., Hernández-Santiago, F. & Martínez-Reyes, M. (2021b) Edible mycorrhizal fungi of the world: What is their role in forest sustainability, food security, biocultural conservation and climate change? Plants People Planet. 3: 471?490. https://doi.org/10.1002/ppp3.10199
Pérez-Moreno, J., Martínez-Reyes, M., Yescas-Pérez, A., Delgado-Alvarado, A. & Xoconostle-Cázares, B. (2008) Wild mushroom markets in Central Mexico and a case study at Ozumba. Economic Botany 62: 425–436. https://doi.org/10.1007/s12231-008-9043-6
Pérez-Moreno, J., Mortimer, P.E., Xu, J., Karunarathna, S.C. & Li, H. (2021a) Global perspectives on the ecological, cultural, and socioeconomic relevance of wild edible fungi. Studies in Fungi 6: 408–424. https://doi.org/10.5943/sif/6/1/31
Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. (2014) Tracer v1.6. Available from: http://beast.bio.ed.ac.uk/Tracer (accessed 16 February 2022).
Ryberg, M. & Matheny, P.B. (2011) Asynchronous origins of ectomycorrhizal clades of Agaricales. Proceedings of the Royal Society B 279: 2013–2011. https://doi.org/10.1098/rspb.2011.2428
Sánchez-García, M., Matheny, P.B., Palfner, G. & Lodge, D.J. (2014) Deconstructing the Tricholomataceae (Agaricales) and introduction of the new genera Albomagister, Corneriella, Pogonoloma and Pseudotricholoma. Taxon 63: 993?1007. https://doi.org/10.12705/635.635.3
Sandor, S.R., Wang, H., Vaario, L., Trudell, S.A. & Xu, J. (2020) Mitochondrial multilocus DNA sequence analyses reveal limited genetic variability within and consistent differences between species of the global matsutake species complex. Acta Edulis Fungi 27: 1–19.
Sanmee R, Dell B, Lumyong P & Lumyong S (2007) First record of Tricholoma fulvocastaneum from Thailand. Mycoscience 48: 131–133. https://doi.org/10.1007/s10267-006-0341-5
Singer, R. (1986) The Agaricales in modern taxonomy. Königstein: Koeltz Scientific Books, 981 pp.
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312?1313. https://doi.org/10.1093/bioinformatics/btu033
Staude, F. (1857) Die Schwämme Mitteldeutschlands, in besondere des Herzogthums. Coburg, Germany, 150 pp.
Tedersoo, L., May, T.W. & Smith, M.E. (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20: 217–263.
Trudell, S.A., Xu, J., Saar, I., Justo, A. & Cifuentes, J. (2017) North American matsutake: names clarified and a new species described. Mycologia 109: 379?390. https://doi.org/10.1080/00275514.2017.1326780
Valencia, A.S. (2004) Diversidad del género Quercus (Fagaceae) en México. Boletín de la Sociedad Botánica de México 75: 33?53. https://dx.doi.org/10.17129/botsci.1692
Villarreal, L. & Pérez-Moreno, J. (1989) Aprovechamiento y conservación del matsutake americano (Tricholoma magnivelare) en los bosques de México. Micología Neotropical Aplicada 2: 131?144.
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