Abstract
The sequestrate genus Melanogaster is rich in mainland China. A total of ten taxa are supported by molecular evidence in this study, including five known species, four new species, and one putatively new species (supported by an ITS sequence from ectomycorrhizal root tip). Based on our morphological reexamination of the type or authentic specimens, four species recorded in China, including M. natsii, M. obovatisporus, M. ovoidisporus, and M. ovoidisporus var. angustatisporus, are treated as questionable species. Consequently, four new species, M. minobovatus, M. panzhihuaensis, M. quercicola, and M. tomentellus, are described and illustrated; M. fusisporus var. obovatus is recombined as M. obovatus; both M. spinisporus and M. subglobisporus are epitypified and re-described. A key for Chinese Melanogaster species is provided.
Similar content being viewed by others
Data availability
The DNA sequences generated during the current study are available in NCBI Genbank. The alignment used for the phylogenetic analyses has been submitted as Supplementary material.
References
Alfaro ME, Zoller S, Lutzoni F (2003) Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Mol Biol Evol 20:255–266. https://doi.org/10.1093/molbev/msg028
Alvarado P, Cabero J, Moreno-Mateos D, Vizzini A, Alonso J, Lebeuf R, Siquier JL, Vidal JM (2021) Phylogenetic relationships among false truffle genera of Paxillaceae—Alpova, Melanogaster, Neoalpova, and Paralpova, gen. nov. Mycologia 113(4):828–841. https://doi.org/10.1080/00275514.2021.1911552
Bergemann SE, Garbelotto M (2006) High diversity of fungi recovered from the roots of mature tanoak (Lithocarpus densiflorus) in northern California. Can J Bot 84(9):1380–1394. https://doi.org/10.1139/b06-097
Berkeley MJ (1844) XLII – notices of British fungi. Ann Mag Nat Hist 13:340–360. https://doi.org/10.1080/03745484409442617
Binder M, Hibbett DS (2006) Molecular systematics and biological diversification of Boletales. Mycologia 98(6):971–981. https://doi.org/10.1080/15572536.2006.11832626
Brock PM, Döring H, Bidartondo MI (2009) How to know unknown fungi: the role of a herbarium. New Phytol 181(3):719–724. https://doi.org/10.1111/j.1469-8137.2008.02703.x
Castellano MA, Trappe JM, Maser Z, Maser S (1986) Key to spores of the genera of hypogeous fungi of North America, with reference to animal mycophagy. Mad River Press, Eureka, USA, 185 pp
Castresana J (2000) Selection of conserved blocks from multiple alignments and their use in phylogenetic analysis. Mol Biol Evol 17(4):540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
Cázares E, Guevara G, García J, Trappe JM (2008) Melanogaster minisporus sp. nov., a new sequestrate member of the Boletales from Mexico. Rev Mex Mic 28:67–69
Corda ACJ (1831) Deutschlands Flora, Abtheilung III. Die Pilze Deutschlands 3(11):1–32
de la Fuente JI, Martínez-González CR, Oros-Ortega I, Guevara G, Bandala VM, Córdova-Lara I, Vela-Hernández RY, López CY, García Jiménez J (2021) Melanogaster coccolobae sp. nov. (Paxillaceae, Boletales), a tropical hypogeous fungus from the urban areas of Quintana Roo, Mexico. Acta bot Mex 128:e1896. https://doi.org/10.21829/abm128.2021.1896
Dring DM (1971) Techniques for microscopic preparation. In: booth C (ed) methods in microbiology, Vol. 4. Academic Press, New York, 95–111 pp. https://doi.org/10.1016/S0580-9517(09)70008-X
Frank JL, Barry S, Southworth D (2006) Mammal mycophagy and dispersal of mycorrhizal inoculum in Oregon white oak woodlands. Northwest Sci 80(4):264–273
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes–application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Grubisha LC, Trappe JM, Molina R, Spatafora JW (2002) Biology of the ectomycorrhizal genus Rhizopogon. VI Re-examination of infrageneric relationships inferred from phylogenetic analyses of ITS sequences. Mycologia 94(4):607–619. https://doi.org/10.1080/15572536.2003.11833189
Halász K (2008) Különböző stressztűrőképességű nagygombanemzetségek Kárpát-medencei leletanyagának molekuláris azonosítása és rendszerezése. PhD dissertation. Eötvös Loránd University, Budapest, Hungaria. Available on the web: http: //teo.elte.hu/minosites/ertekezes2009/halasz_k.pdf, accessed 30 sept 2008.
He MQ, Zhao RL, Hyde KD, Begerow D, Kemler M, Yurkov A, McKenzie EHC, Raspé O, Kakishima M, Sánchez-Ramírez S, Vellinga EC, Halling R, Papp V, Zmitrovich IV, Buyck B, Ertz D, Wijayawardene NN, Cui BK, Schoutteten N et al (2019) Notes, outline and divergence times of Basidiomycota. Fungal Divers 99:105–367. https://doi.org/10.1007/s13225-019-00435-4
Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42(2):182–192. https://doi.org/10.1093/sysbio/42.2.182
Izzo AD, Meyer M, Trappe JM, North M, Bruns TD (2005) Hypogeous ectomycorrhizal fungal species on roots and in small mammal diet in a mixed-conifer forest. For Sci 51:243–254
Jargeat P, Chaumeton JP, Navaud O, Vizzini A, Gryta H (2014) The Paxillus involutus (Boletales, Paxillaceae) complex in Europe: genetic diversity and morphological description of the new species Paxillus cuprinus, typification of P. involutus s.s., and synthesis of species boundaries. Fungal Biol 118(1):12–31. https://doi.org/10.1016/j.funbio.2013.10.008
Jargeat P, Moreau PA, Gryta H, Chaumeton JP, Gardes M (2016) Paxillus rubicundulus (Boletales, Paxillaceae) and two new alder-specific ectomycorrhizal species, Paxillus olivellus and Paxillus adelphus, from Europe and North Africa. Fungal Biol 120(5):711–728. https://doi.org/10.1016/j.funbio.2016.02.008
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Keissler K, Lohwag H (1937) Fungi, in Handel-Mazzeti. Symb Sin 2:1–83
Lacheva M (2015) New records of Melanogaster species (Fungi, Boletales) in Bulgaria. J Bio Env Sci 6(1):492–498
Lange M (1956) Danish hypogeous macromycetes. Dansk Botanisk Arkiv 16:1–84
Liu B, Tao K, Cang MC (1989) Two new species of Melanogaster from China. Acta Mycol Sin 8(3):210–213
Liu B (1998) Flora Fungorum Sinicorum vol. 7—Hymenogastrales Melanogastrales et Gautieriales. Science Press, Beijing, China:87 pp
Massee G (1889) A monograph of British Gastromycetes. Ann Bot 4:1–103
Montecchi A, Lazzari G (1993) Atlante fotografico di funghi ipogei. Associazione Micologica Bresadola, Centro Studi Micologici - Vicenza. Pp. 180–181.
Moreau PA, Rochet J, Richard F, Chassagne F, Manzi S, Gardes M (2011) Taxonomy of Alnus-associated hypogeous species of Alpova and Melanogaster (Basidiomycota, Paxillaceae) in Europe. Cryptogamie Mycol 32(1):33–62. https://doi.org/10.7872/crym.v32.iss1.2012.033
Nylander JAA (2004) Mr Modeltest 2.2. Computer software distributed by the University of Uppsala. Uppsala, Sweden: evolutionary biology Centre, University of Uppsala.
Page RD (2001) TreeView. Glasgow University, Glasgow
Pegler DN, Spooner BM, Young TWK (1993) British truffles: a revision of British hypogeous fungi. Royal Botanical Gardens, Kew. London, UK:216 pp
Rambaut A (2000) Estimating the rate of molecular evolution: incorporating non-contemporaneous sequences into maximum likelihood phylogenies. Bioinformatics 16:395–399. https://doi.org/10.1093/bioinformatics/16.4.395
Rinaldi AC, Comandini O, Kuyper TW (2008) Ectomycorrhizal fungal diversity: separating the wheat from the chaff. Fungal Divers 33:1–45
Ronquist F, Huelsenbeck JP (2003) MrBayes3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Séne S, Avril R, Chaintreuil C, Geoffroy A, Ndiaye C, Diédhiou AG, Sadio O, Courtecuisse R, Sylla SN, Selosse MA, Bâ A (2015) Ectomycorrhizal fungal communities of Coccoloba uvifera (L.) L. mature trees and seedlings in the neotropical coastal forests of Guadeloupe (Lesser Antilles). Mycorrhiza 25(7):547–559
Stamatakis A (2014) RAxMLversion 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263. https://doi.org/10.1007/s00572-009-0274-x
Teng SC (1963) Fungi of China. Science Press, Beijing, China, 660 pp
Trappe JM, Molina R, Luoma DL, Cázares E, Pilz D, Smith JE, Castellano MA, Miller SL, Trappe MJ (2009) Diversity, ecology, and conservation of truffle fungi in forests of the Pacific northwest. USDA general technical report, Forest Service, Pacific northwest Research Station. Portland, Oregon:196 pp
Truong C, Mujic AB, Healy R, Kuhar F, Furci G, Torres D, Niskanen T, Sandoval-Leiva PA, Fernandez N, Escobar JM, Moretto A, Palfner G, Pfister D, Nouhra E, Swenie R, Sanchez-Garcıa M, Matheny PB, Smith ME (2017) How to know the fungi: combining field inventories and DNA-barcoding to document fungal diversity. New Phytol 214(3):913–919
Türkoğlu A, Castellano MA (2013) New records of truffle fungi (Basidiomycetes) from Turkey. Turk J Bot 37:970–976. https://doi.org/10.3906/bot-1212-54
Wang Q, He XH, Guo LD (2012) Ectomycorrhizal fungus communities of Quercus liaotungensis Koidz of different ages in a northern China temperate forest. Mycorrhiza 22(6):461–470. https://doi.org/10.1007/s00572-011-0423-x
Wang Y, Castellano MA, Trappe JM (2005) Melanogaster utriculatus sp. nov. from Japan. Mycotaxon 93(1):315–317
Wang Y, Chang MC, Tao K, Liu B (1995) New species and new varieties in the genus Melanogaster from China. J Shanxi Univ (Nat. Sci. Ed.) 18(4):449–453
White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (Eds.) PCR protocols: a guide to the methods and applications. Academic press, New York, 315–322 pp. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Zeller SM, Dodge CW (1936) Melanogaster. Ann Mo Bot Gard 23(1):639–655
Zeller SM (1949) Keys to the orders, families, and genera of the Gasteromycetes. Mycologia 41:36–58
Zhang J, Taniguchi T, Xu M, Du S, Liu GB, Yamanaka N (2014) Ectomycorrhizal fungal communities of Quercus liaotungensis along different successional stands on the Loess Plateau, China. J For Res 19(4):395–403. https://doi.org/10.1007/s10310-013-0433-y
Acknowledgements
The authors thank the curators of the herbaria of HMAS for providing specimens and permission of the DNA extraction from them. The authors are grateful to Dr. Jing-zhong Cao and Mr. Jin-song Xu for collecting specimens and providing valuable suggestions. The authors also appreciate the two anonymous reviewers and editors for their suggestions and corrections to improve this paper.
Funding
This study was supported by the National Natural Science Foundation of China (No. 31750001) and the Beijing Natural Science Foundation (No. 5172003).
Author information
Authors and Affiliations
Contributions
All authors contributed to the conception and design of the study. Yu-yan Xu, Xiang-yuan Yan, Ting Li, Tao-yu Zhao, Jing-chong Lv, and Li Fan prepared material. Ting Li, Tao-yu Zhao, and Jing-chong Lv isolated DNA and prepared samples for sequencing. Yu-yan Xu and Xiang-yuan Yan conducted phylogenetic analyses and morphological observations. Yu-yan Xu and Xiang-yuan Yan wrote the first draft of the manuscript, and Yu-yan Xu and Li Fan revised the manuscript. All authors contributed to previous drafts of the manuscript and read and approved the final draft of the manuscript.
Corresponding author
Ethics declarations
Consent for publication
Not applicable
Consent to participate
Not applicable
Conflict of interest
The authors declare no competing interests.
Additional information
Section Editor: Zhu-Liang Yang
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
The alignment of Melanogaster used for the phylogenetic analyses. (FAS 41 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Xu, Yy., Yan, Xy., Li, T. et al. The taxonomic revision of Melanogaster (Paxillaceae, Boletales) in China based on molecular and morphological evidence. Mycol Progress 21, 98 (2022). https://doi.org/10.1007/s11557-022-01842-9
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11557-022-01842-9