Advertisement

Fungal Diversity

, Volume 84, Issue 1, pp 43–74 | Cite as

A six-gene phylogenetic overview of Basidiomycota and allied phyla with estimated divergence times of higher taxa and a phyloproteomics perspective

  • Rui-Lin Zhao
  • Guo-Jie Li
  • Santiago Sánchez-Ramírez
  • Matt Stata
  • Zhu-Liang Yang
  • Gang Wu
  • Yu-Cheng Dai
  • Shuang-Hui He
  • Bao-Kai Cui
  • Jun-Liang Zhou
  • Fang Wu
  • Mao-Qiang He
  • Jean-Marc Moncalvo
  • Kevin D. Hyde
Article

Abstract

In this paper, we provide a phylogenetic overview of Basidiomycota and related phyla in relation to ten years of DNA based phylogenetic studies since the AFTOL publications in 2007. We selected 529 species to address phylogenetic relationships of higher-level taxa using a maximum-likelihood framework and sequence data from six genes traditionally used in fungal molecular systematics (nrLSU, nrSSU, 5.8S, tef1-α, rpb1 and rpb2). These species represent 18 classes, 62 orders, 183 families, and 392 genera from the phyla Basidiomycota (including the newly recognized subphylum Wallemiomycotina) and Entorrhizomycota, and 13 species representing 13 classes of Ascomycota as outgroup taxa. We also conducted a molecular dating analysis based on these six genes for 116 species representing 17 classes and 54 orders of Basidiomycota and Entorrhizomycota. Finally we performed a phyloproteomics analysis from 109 Basidiomycota species and 6 outgroup taxa using amino-acid sequences retrieved from 396 orthologous genes. Recognition of higher taxa follows the criteria in Zhao et al (Fungal Divers 78:239–292, 2016): (i) taxa must be monophyletic and statistically well-supported in molecular dating analyses, (ii) their respective stem ages should be roughly equivalent, and (iii) stem ages of higher taxa must be older than those of lower level taxa. The time-tree indicates that the mean of stem ages of Basidiomycota and Entorrhizomycota are ca. 530 Ma; subphyla of Basidiomycota are 406–490 Ma; most classes are 358–393 Ma for those of Agaricomycotina and 245–356 Ma for those of Pucciniomycotina and Ustilaginomycotina; most orders of those subphyla split 120–290 Ma. Monophyly of most higher-level taxa of Basidiomycota are generally supported, especially those taxa introduced in the recent ten years: phylum Entorrhizomycota, classes Malasseziomycetes, Moniliellomycetes, Spiculogloeomycetes, Tritirachiomycetes and orders Amylocorticiales, Golubeviales, Holtermanniales, Jaapiales, Lepidostromatales, Robbauerales, Stereopsidales and Trichosporonales. However, the younger divergence times of Leucosporidiales (Microbotryomycetes) indicate that its order status is not supported, thus we propose combining it under Microbotryales. On the other hand, the families Buckleyzymaceae and Sakaguchiaceae (Cystobasidiomycetes) are raised to Buckleyzymales and Sakaguchiales due to their older divergence times. Cystofilobasidiales (Tremellomycetes) has an older divergence time and should be amended to a higher rank. We however, do not introduce it as new class here for Cystofilobasidiales, as DNA sequences from these taxa are not from their respective types and thus await further studies. Divergence times for Exobasidiomycetes, Cantharellales, Gomphales and Hysterangiales were obtained based on limited species sequences in molecular dating study. More comprehensive phylogenetic studies on those four taxa are needed in the future because our ML analysis based on wider sampling, shows they are not monophyletic groups. In general, the six-gene phylogenies are in agreement with the phyloproteomics tree except for the placements of Wallemiomycotina, orders Amylocorticiales, Auriculariales, Cantharellales, Geastrales, Sebacinales and Trechisporales from Agaricomycetes. These conflicting placements in the six-gene phylogeny vs the phyloproteomics tree are discussed. This leads to future perspectives for assessing gene orthology and problems in deciphering taxon ranks using divergence times.

Keywords

Fungi Systematics Taxonomy Wallemiomycotina 

Notes

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China to R.-L. Zhao (Project IDs 31470152 and 31360014) and G.-J. Li (Project ID 31500013), the Innovative Group of Edible Mushrooms Industry of Beijing (Project ID: BAIC05-2017) and the Key Research and Development Program from Government of Guangxi Zhuang Autonomous Region (Project ID: 2016AB05317) to R.-L. Zhao, the Thailand Research Fund to K.D. Hyde (Grant BRG 5580009), and the Natural Sciences and Engineering Research Council of Canada and the ROM Governors to J.-M. Moncalvo.

Supplementary material

13225_2017_381_MOESM1_ESM.doc (715 kb)
Supplementary material 1 (DOC 715 kb)
13225_2017_381_MOESM2_ESM.docx (48 kb)
Supplementary material 2 (DOCX 48 kb)

References

  1. Aime MC, Matheny PB, Henk DA, Frieders EM et al (2006) An overview of the higher-level classification of Pucciniomycotina based on combined analyses of nuclear large and small subunit rDNA sequences. Mycologia 98:896–905PubMedCrossRefGoogle Scholar
  2. Aime MC, Toome M, McLaughlin D (2014) The Pucciniomycotina. In: McLaughlin D, Spatafora JW (eds) The mycota VII part A. Systematics and evolution, 2nd edn. Springer, Berlin, pp 271–294Google Scholar
  3. Avise JC, Johns GC (1999) Proposal for a standardized temporal scheme of biological classification for extant species. Proc Natl Acad Sci USA 96:7358–7363PubMedPubMedCentralCrossRefGoogle Scholar
  4. Bauer R, Begerow D, Nagler A, Oberwinkler F (2001) The Georgefischeriales: a phylogenetic hypothesis. Mycol Res 104:416–424CrossRefGoogle Scholar
  5. Bauer R, Begerow D, Sampaio JP, Weiß M, Oberwinkler F (2006) The simple-septate basidiomycetes: a synopsis. Mycol Prog 5:41–66CrossRefGoogle Scholar
  6. Bauer R, Garnica S, Oberwinkler F, Riess K et al (2015) Entorrhizomycota: A new fungal phylum reveals new perspectives on the evolution of fungi. PLoS ONE 10:e0128183PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bauer R, Oberwinkler F, Vánky K (1997) Ultrastructural markers and systematics in smut fungi and allied taxa. Can J Bot 75:1273–1314CrossRefGoogle Scholar
  8. Begerow D, Bauer R, Boekhout T (2000) Phylogenetic placements of ustilaginomycetous anamorphs as deduced from nuclear LSU rDNA sequences. Mycol Res 104:53–60CrossRefGoogle Scholar
  9. Begerow D, Bauer R, Oberwinkler F (1997) Phylogenetic studies on nuclear large subunit ribosomal DNA sequences of smut fungi and related taxa. Can J Bot 75:2045–2056CrossRefGoogle Scholar
  10. Begerow D, Stoll M, Bauer R (2006) A phylogenetic hypothesis of Ustilaginomycotina based on multiple gene analyses and morphological data. Mycologia 98:906–916PubMedCrossRefGoogle Scholar
  11. Beimforde C, Feldberg K, Nylinder S, Rikkinen J et al (2014) Estimating the Phanerozoic history of the Ascomycota lineages: combining fossil and molecular data. Mol Phylogenet Evol 78:386–398PubMedCrossRefGoogle Scholar
  12. Berbee ML, Taylor JW (2010) Dating the molecular clock in fungi—how close are we? Fungal Biol Rev 24:1–16CrossRefGoogle Scholar
  13. Binder M, Hibbett DS (2002) Higher-level phylogenetic relationships of homobasidiomycetes (mushroom-forming fungi) inferred from four rDNA regions. Mol Phylogenet Evol 22:76–90PubMedCrossRefGoogle Scholar
  14. Binder M, Hibbett DS, Larsson KH, Larsson E, Langer E (2005) The phylogenetic distribution of resupinate forms in the homobasidiomycetes. Syst Biodivers 3:113–157CrossRefGoogle Scholar
  15. Binder M, Larsson KH, Matheny PB, Hibbett DS (2010) Amylocorticiales ord. nov. and Jaapiales ord. nov.: early diverging clades of Agaricomycetidae dominated by corticioid forms. Mycologia 102:865–880PubMedCrossRefGoogle Scholar
  16. Blackwell M, Hibbett DS, Taylor JW, Spatafora JW (2006) Research coordination networks: a phylogeny for kingdom Fungi (Deep Hypha). Mycologia 98:829–837PubMedCrossRefGoogle Scholar
  17. Boekhout T, Fonseca A, Sampaio JP, Bandoni RJ et al (2011) Discussion of teleomorphic and anamorphic basidiomycetous yeasts. In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts: a taxonomic study. Elsevier, Amsterdam, pp 1356–1367Google Scholar
  18. Bonfante P, Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends Plant Sci 13:492–498PubMedCrossRefGoogle Scholar
  19. Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59–60PubMedCrossRefGoogle Scholar
  20. Budd GE (2001) Climbing life’s tree. Nature 412:487PubMedCrossRefGoogle Scholar
  21. Budd GE, Jensen S (2000) A critical reappraisal of the fossil record of the bilaterian phyla. Biol Rev 75:253–295PubMedCrossRefGoogle Scholar
  22. Bushley KE, Turgeon BG (2010) Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol Biol 10:26PubMedPubMedCentralCrossRefGoogle Scholar
  23. Capella-Gutiérrez S, Marcet-Houben M, Gabaldón T (2012) Phylogenomics supports microsporidia as the earliest diverging clade of sequenced fungi. BMC Biol 10:47PubMedPubMedCentralCrossRefGoogle Scholar
  24. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973PubMedPubMedCentralCrossRefGoogle Scholar
  25. Chapela IH, Rehner SA, Schultz TR, Mueller UG (1994) Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266:1691–1694PubMedCrossRefGoogle Scholar
  26. Chen ZH, Zhang P, Zhang ZG (2014) Investigation and analysis of 102 mushroom poisoning cases in Southern China from 1994 to 2012. Fungal Divers 64:123–131CrossRefGoogle Scholar
  27. Dai YC, Cui BK, Si J, He SH et al (2015) Dynamics of the worldwide number of fungi with emphasis on fungal diversity in China. Mycol Prog 14:62CrossRefGoogle Scholar
  28. Dai YC, Cui BK, Yuan HS, Li BD (2007) Pathogenic wood-decaying fungi in China. For Pathol 37:105–120CrossRefGoogle Scholar
  29. Dai YC, Yang ZL, Cui BK, Yu CJ, Zhou LW (2009) Species diversity and utilization of medicinal mushrooms and fungi in China (Review). Int J Med Mushrooms 11:287–302CrossRefGoogle Scholar
  30. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772PubMedPubMedCentralCrossRefGoogle Scholar
  31. De Silva DD, Rapior S, Fons F, Bahkali AH, Hyde KD (2012a) Medicinal mushrooms in supportive cancer therapies: an approach to anti-cancer effects and putative mechanisms of action. Fungal Divers 55:1–35CrossRefGoogle Scholar
  32. De Silva DD, Rapior S, Hyde KD, Bahkali AH (2012b) Medicinal mushrooms in prevention and control of diabetes mellitus. Fungal Divers 56:1–29CrossRefGoogle Scholar
  33. De Silva DD, Rapior S, Sudarman E, Stadler M et al (2013) Bioactive metabolites from macrofungi: ethnopharmacology, biological activities and chemistry. Fungal Divers 62:1–40CrossRefGoogle Scholar
  34. Delsuc F, Brinkmann H, Philippe H (2005) Phylogenomics and the reconstruction of the tree of life. Nat Rev Genet 6:361–375PubMedCrossRefGoogle Scholar
  35. Dentinger BT, Ammirati JF, Both EE, Desjardin DE et al (2010) Molecular phylogenetics of porcini mushrooms (Boletus section Boletus). Mol Phylogenet Evol 57:1276–1292PubMedCrossRefGoogle Scholar
  36. Drummond AJ, Ho SY, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88PubMedPubMedCentralCrossRefGoogle Scholar
  37. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Phylogenet Evol 29:1969–1973CrossRefGoogle Scholar
  38. Edgar RC (2004a) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedPubMedCentralCrossRefGoogle Scholar
  39. Edgar RC (2004b) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 5:113CrossRefGoogle Scholar
  40. Fell JW, Boekhout T, Fonseca A, Scorzetti G, Statzell-Tallman A (2000) Biodiversity and systematics of basidiomycetous yeasts as determined by large-subunit rDNA D1/D2 domain sequence analysis. Int J Syst Evol Microbiol 50:1351–1371PubMedCrossRefGoogle Scholar
  41. Floudas D, Binder M, Riley R, Barry K et al (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719PubMedCrossRefGoogle Scholar
  42. Garcia-Sandoval R, Wang Z, Binder M, Hibbett DS (2011) Molecular phylogenetics of the Gloeophyllales and relative ages of clades of Agaricomycotina producing a brown rot. Mycologia 103:510–524PubMedCrossRefGoogle Scholar
  43. Garnica S, Weiss M, Walther G, Oberwinkler F (2007) Reconstructing the evolution of agarics from nuclear gene sequences and basidiospore ultrastructure. Mycol Res 111:1019–1029PubMedCrossRefGoogle Scholar
  44. Gueidan C, Ruibal C, de Hoog GS, Schneider H (2011) Rock-inhabiting fungi originated during periods of dry climate in the late Devonian and middle Triassic. Fungal Biol 115:987–996PubMedCrossRefGoogle Scholar
  45. Hamamoto M, Nakase T (2000) Phylogenetic analysis of the ballistoconidium-forming yeast genus Sporobolomyces based on 18S rDNA sequences. Int J Syst Evol Microbiol 50:1373–1380PubMedCrossRefGoogle Scholar
  46. Hedges S, Marin J, Suleski M, Paymer M, Kumar S (2015) Tree of life reveals clock-like speciation and diversification. Mol Biol Evol. doi: 10.1093/molbev/msv037 PubMedPubMedCentralGoogle Scholar
  47. Hennig W (1966) Phylogenetic systematics. University of Illinois Press, UrbanaGoogle Scholar
  48. Hibbett DS (2001) Shiitake mushrooms and molecular clocks: historical biogeography of Lentinula. J Biogeogr 28:231–241CrossRefGoogle Scholar
  49. Hibbett DS (2006) A Phylogenetic overview of the Agaricomycotina. Mycologia 98:917–925PubMedCrossRefGoogle Scholar
  50. Hibbett DS (2014) Major events in the evolution of the Fungi. In: Losos J (ed) Princeton guide to evolution. Princeton University Press, Princeton, pp 152–158Google Scholar
  51. Hibbett DS, Bauer R, Binder M, Giachini AJ et al (2014) Agaricomycetes. In: McLaughlin DJ, Spatafora JW (eds) The mycota, vol. VII, part A. Systematics and evolution, 2nd edn. Springer, Berlin, pp 373–429Google Scholar
  52. Hibbett DS, Binder M, Bischoff JF, Blackwell M et al (2007) A higher- level phylogenetic classification of the Fungi. Mycol Res 111:509–547PubMedCrossRefGoogle Scholar
  53. Hibbett DS, Matheny PB (2009) Relative ages of ectomycorrhizal mushrooms and their plant hosts. BMC Biol 7:13PubMedPubMedCentralCrossRefGoogle Scholar
  54. Hibbett DS, Pine EM, Langer E, Langer G, Donoghue MJ (1997) Evolution of gilled mushrooms and puffballs inferred from ribosomal DNA sequences. Proc Natl Acad Sci USA 94:12002–12006PubMedPubMedCentralCrossRefGoogle Scholar
  55. Hibbett DS, Tsuneda A, Fukumasa-Nakai Y, Donoghue MJ (1995) Phylogenetic diversity in shiitake inferred from nuclear ribosomal DNA sequences. Mycologia 87:618–638CrossRefGoogle Scholar
  56. Hickerson MJ, Carstens BC, Cavender-Bares J (2010) Phylogeography’s past, present, and future: 10 years after Avise, 2000. Mol Phylogenet Evol 54:291–301PubMedCrossRefGoogle Scholar
  57. Hodkinson BP, Moncada B, Lücking R (2014) Lepidostromatales, a new order of lichenized fungi (Basidiomycota, Agaricomycetes), with two new genera, Ertzia and Sulzbacheromyces, and one new species, Lepidostroma winklerianum. Fungal Divers 64:165–179CrossRefGoogle Scholar
  58. Hongsanan S, Sánchez-Ramírez S, Crous PW, Ariyawansa HA et al (2016) The evolution of fungal epiphytes. Mycosphere 7:1690–1712Google Scholar
  59. Hosaka K, Bates ST, Beever RE, Castellano MA, Colgan W 3rd, Domínguez LS, Nouhra ER, Geml J, Giachini AJ, Kenney SR, Simpson NB, Spatafora JW, Trappe JM (2006) Molecular phylogenetics of the gomphoid-phalloid fungi with an establishment of the new subclass Phallomycetidae and two new orders. Mycologia 98:949–959PubMedCrossRefGoogle Scholar
  60. Hyde KD, Hongsanan S, Jeewon R, Bhat DJ et al (2016) Fungal Diversity Notes 367–490: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers. doi: 10.1007/s13225-016-0373-x Google Scholar
  61. Hyde KD, Jones EBG, Liu JK, Ariyawansa H et al (2013) Families of Dothideomycetes. Fungal Divers 63:1–313CrossRefGoogle Scholar
  62. Hyde KD, Nilsson RHSA, Ariyawansa HA et al (2014) One stop shop: backbones trees for important phytopathogenic genera: I. Fungal Divers 67:21–125CrossRefGoogle Scholar
  63. James TY, Kauff F, Schoch CL, Matheny PB et al (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 98:829–837Google Scholar
  64. Jančič S, Zalar P, Kocev D, Schroers H-J et al (2016) Halophily reloaded: new insights into the extremophilic life-style of Wallemia with the description of Wallemia hederae sp. nov. Fungal Divers 76:97–118CrossRefGoogle Scholar
  65. Jülich W (1981) Higher taxa of Basidiomycetes. Bibliogr Mycol 85:1–845Google Scholar
  66. Kemler M, Lutz M, Göker M, Oberwinkler F, Begerow D (2009) Hidden diversity in the non-caryophyllaceous plant-parasitic members of Microbotryum (Pucciniomycotina: Microbotryales). Syst Biodivers 7:297–306CrossRefGoogle Scholar
  67. Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Ainsworth & Bisby’s dictionary of the fungi, 10th edn. CABI, WallingfordGoogle Scholar
  68. Kottke I, Beiter A, Weiss M, Haug I et al (2003) Heterobasidiomycetes form symbiotic associations with hepatics: Jungermanniales have sebacinoid mycobionts while Aneura pinguis (Metzgeriales) is associated with a Tulasnella species. Mycol Res 107:957–968PubMedCrossRefGoogle Scholar
  69. Kozlov AM, Aberer AJ, Stamatakis A (2015) ExaML version 3: a tool for phylogenomic analyses on supercomputers. Bioinformatics 31:2577–2579PubMedPubMedCentralCrossRefGoogle Scholar
  70. Kuhnert E, Surup F, Sir EB, Lambert C, Hyde KD, Hladki AI, Romero AI, Stadler M (2015) Lenormandins A—G, new azaphilones from Hypoxylon lenormandii and Hypoxylon jaklitschii sp. nov., recognised by chemotaxonomic data. Fungal Divers 71:165–184CrossRefGoogle Scholar
  71. Largent DL (1986a) How to identify mushrooms to genus vol. 1. Macroscopic features. Mad River Press, EurekaGoogle Scholar
  72. Largent DL (1986b) How to identify mushrooms to genus vol. 3. Microscopic features. Mad River Press, EurekaGoogle Scholar
  73. Larsson KH, Larsson E, Kõljalg U (2004) High phylogenetic diversity among corticioid Homobasidiomycetes. Mycol Res 108:983–1002PubMedCrossRefGoogle Scholar
  74. Lawrey JD, Binder M, Diederich P, Molina MC et al (2007) Phylogenetic diversity of lichen-associated Homobasidiomycetes. Mol Phylogenet Evol 44:778–789PubMedCrossRefGoogle Scholar
  75. LePage BA, Currah RS, Stockey RA, Rothwell GW (1997) Fossil ectomycorrhizae from the Middle Eocene. Am J Bot 84:410–412PubMedCrossRefGoogle Scholar
  76. Lepage T, Bryant D, Philippe H, Lartillot N (2007) A general comparison of relaxed molecular clock models. Mol Biol Evol 24:2669–2680PubMedCrossRefGoogle Scholar
  77. Li GJ, Hyde KD, Zhao RL, Hongsanan S et al (2016) Fungal Diversity Notes 253–366: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers 78:1–237CrossRefGoogle Scholar
  78. Liu JK (2004) Mycochemistry of high fungi. China Sci and Tech Press, BeijingGoogle Scholar
  79. Liu NN, Ariyawansa HA, Hyde KD, Maharachchikumbura SSN et al (2016) Mycosphere essays X Perspectives into the value of genera, families and orders in fungal classification. Mycosphere 7:1649–1668Google Scholar
  80. Liu XZ, Wang QM, Göker M, Groenewald M et al (2015a) Towards an integrated phylogenetic classification of the Tremellomycetes. Stud Mycol 81:85–147PubMedCrossRefGoogle Scholar
  81. Liu XZ, Wang QM, Theelen B, Groenewald M et al (2015b) Phylogeny of tremellomycetous yeasts and related dimorphic and filamentous basidiomycetes reconstructed from multiple gene sequence analyses. Stud Mycol 81:1–26PubMedPubMedCentralCrossRefGoogle Scholar
  82. Lutzoni F, Kauff F, Cox CJ, McLaughlin D et al (2004) Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. Am J Bot 91:1146–1180CrossRefGoogle Scholar
  83. Maddison WP, Maddison DR (2016). Mesquite: a modular system for evolutionary analysis. Version 3.2. http://mesquiteproject.org/mesquite/mesquite.html
  84. Maharachchikumbura SSN, Hyde KD, Jones EBG, McKenzie EHC et al (2015) Towards a natural classification and backbone tree for Sodariomycetes. Fungal Divers 72:199–301CrossRefGoogle Scholar
  85. Maharachchikumbura SSN, Hyde KD, Jones EBG, McKenzie EHC et al (2016) Families of Sordariomycetes. Fungal Divers 79:1–317CrossRefGoogle Scholar
  86. Matheny PB, Aime MC, Bougher NL, Buyck B et al (2009) Out of the Palaeotropics? Historical biogeography and diversification of the cosmopolitan ectomycorrhizal mushroom family Inocybaceae. J Biogeogr 36:577–592CrossRefGoogle Scholar
  87. Matheny PB, Curtis JM, Hofstetter V, Aime MC et al (2006) Major clades of Agaricales: a multilocus phylogenetic overview. Mycologia 98:982–995PubMedCrossRefGoogle Scholar
  88. Matheny PB, Gossmann JA, Zalar P, Kumar TKA, Hibbett DS (2007a) Resolving the phylogenetic position of the Wallemiomycetes: an enigmatic major lineage of Basidiomycota. Can J Botany 84:1794–1805CrossRefGoogle Scholar
  89. Matheny PB, Liu YJ, Ammirati JF, Hall BD (2002) Using RPB1 sequences to improve phylogenetic inference among mushrooms (Inocybe, Agaricales). Am J Bot 89:688–698PubMedCrossRefGoogle Scholar
  90. Matheny PB, Wang Z, Binder M, Curtis JM et al (2007b) Contributions of rpb2 and tef1 to the phylogeny of mushrooms and allies (Basidiomycota, Fungi). Mol Phylogenet Evol 43:430–451PubMedCrossRefGoogle Scholar
  91. McPeek MA, Brown JM (2007) Clade age and not diversification rate explains species richness among animal taxa. Am Nat 169:E97–E106PubMedCrossRefGoogle Scholar
  92. Medina ME, Jones GW, Fitzpatrick DA (2011) Reconstructing the fungal tree of life using phylogenomics and a preliminary investigation of the distribution of yeast prion-like proteins in the fungal kingdom. J Mol Evol 73:116–133PubMedCrossRefGoogle Scholar
  93. Mikheyev AS, Mueller UG, Abbot P (2010) Comparative dating of attine ant and lepiotaceous cultivar phylogenies reveals coevolutionary synchrony and discord. Am Nat 175(6):E126–E133PubMedCrossRefGoogle Scholar
  94. Moncalvo J-M, Lutzoni FM, Rehner SA, Johnson J, Vilgalys R (2000) Phylogenetic relationships of agaric fungi based on nuclear large subunit ribosomal DNA sequences. Syst Biol 49:278–305PubMedCrossRefGoogle Scholar
  95. Moncalvo J-M, Nilsson RH, Koster B, Dunham SM et al (2006) The cantharelloid clade: dealing with incongruent gene trees and phylogenetic reconstruction methods. Mycologia 98:937–948PubMedCrossRefGoogle Scholar
  96. Moore RT (1980) Taxonomic proposals for the classification of marine yeasts and other yeast-like fungi including the smuts. Bot Mar 23:361–373Google Scholar
  97. Morehouse EA, James TY, Ganley ARD, Vilgalys R et al (2003) Multilocus sequence typing suggests the chytrid pathogen of amphibians is a recently emerged clone. Mol Ecol 12:395–403PubMedCrossRefGoogle Scholar
  98. Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR (2005) The evolution of agriculture in insects. Annu Rev Ecol Evol S 36:563–569CrossRefGoogle Scholar
  99. Nakase T (2000) Expanding world of ballistosporous yeasts: distribution in the phyllosphere, systematics and phylogeny. J Gen Appl Microbiol 46:189–216PubMedCrossRefGoogle Scholar
  100. Nobre T, Fernandes C, Boomsma JJ, Korb J, Aanen DK (2011) Farming termites determine the genetic population structure of Termitomyces fungal symbionts. Mol Ecol 20:2023–2033PubMedCrossRefGoogle Scholar
  101. Oberwinkler F (2012) Evolutionary trends in Basidiomycota. Stapfia 96:45–104Google Scholar
  102. Padamsee M, Kumar TK, Riley R, Binder M et al (2012) The genome of the xerotolerant mold Wallemia sebi reveals adaptations to osmotic stress and suggests cryptic sexual reproduction. Fungal Genet Biol 49:217–226PubMedCrossRefGoogle Scholar
  103. Peláez F, Martínez MJ, Martínez AT (1995) Screening of 68 species of Basidiomycetes for enzymes involved in lignin degradation. Mycol Res 99:37–42CrossRefGoogle Scholar
  104. Pointing S (2001) Feasibility of bioremediation by white-rot fungi. Appl Microbiol Biotechnol 57:20–33PubMedCrossRefGoogle Scholar
  105. Pointing SB, Pelling AL, Smith GJD, Hyde KD, Reddy CA (2005) Screening of basidiomycetes and xylariaceous fungi for lignin peroxidase and laccase gene-specific sequences. Mycol Res 109:115–124PubMedCrossRefGoogle Scholar
  106. Rambaut A, Suchard M, Drummond A (2013) Tracer. http://tree.bio.ed.ac.uk/software/tracer/. Accessed 15 Sept 2016
  107. Riess K, Bauer R, Kellner R, Kemler M et al (2015) Identification of a new order of root-colonising fungi in the Entorrhizomycota: Talbotiomycetales ord. nov. on eudicotyledons. IMA Fungus 6:129–133PubMedPubMedCentralCrossRefGoogle Scholar
  108. Rinaldi AC, Comandini O, Kuyper TW (2008) Ectomycorrhizal fungal diversity: Separating the wheat from the chaff. Fungal Divers 33:1–45Google Scholar
  109. Robinson NE, Robinson AB (2001) Molecular clocks. Proc Natl Acad Sci USA 98:944–949PubMedPubMedCentralCrossRefGoogle Scholar
  110. Rokas A, Chatzimanolis S (2010) From gene-scale to genome-scale phylogenetics: the data flood in, but the challenges remain. In: Murphy WJ (ed) Phylogenomics. Humana Press, TotowaGoogle Scholar
  111. Rokas A, Williams BL, King N, Carroll SB (2003) Genome-scale approachs to resolving incongruence in molecular phylogenies. Nature 425:798–804PubMedCrossRefGoogle Scholar
  112. Ruiz-Dueñas FJ, Martínez AT (2009) Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this. Microbiol Biotechnol 2:164–167CrossRefGoogle Scholar
  113. Ryberg M, Matheny PB (2012) Asynchronous origins of ectomycorrhizal clades of Agaricales). Proc R Soc B Biol Sci 279:2003–2011CrossRefGoogle Scholar
  114. Samarakoon MC, Hyde KD, Ariyawansa HA, Hongsanan S (2016) Mycosphere Essays X: divergence and ranking of taxa across the kingdoms Animalia, Fungi and Plantae. Mycosphere 7:1678–1689Google Scholar
  115. Sánchez-Ramírez S, Wilson AW, Ryberg M (2017) An overview of phylogenetic and historical approaches to mycorrhizal biogeography, diversity, and evolution. In: Tedersoo L (ed) Mycorrhizal biogeography, ecological studies 230. Springer, BerlinGoogle Scholar
  116. Sánchez-Ramírez S, Tulloss RE, Amalfi M, Moncalvo J-M (2015) Palaeotropical origins, boreotropical distribution and increased rates of diversification in a clade of edible ectomycorrhizal mushrooms (Amanita section Caesareae). J Biogeogr 42:351–363CrossRefGoogle Scholar
  117. Schell WA, Lee AG, Aime MC (2011) A new lineage in Pucciniomycotina: class Tritirachiomycetes, order Tritirachiales, family Tritirachiaceae. Mycologia 103:1331–1340PubMedCrossRefGoogle Scholar
  118. Scorzetti G, Fell JW, Fonseca A, Statzell-Tallman A (2002) Systematics of basidiomycetous yeasts: a comparison of large subunit D1/D2 and internal transcribed spacer rDNA regions. FEMS Yeast Res 2:495–517PubMedCrossRefGoogle Scholar
  119. Shelest E, Voigt K (2014) Genomics to study basal lineage fungal biology: phylogenomics suggests a common origin. Fungal genomics. In: Nowrousian M (ed) The mycota XIII, 2nd edn. Springer, BerlinGoogle Scholar
  120. Shirouzu T, Hirose D, Oberwinkler F, Shimomura N et al (2013) Combined molecular and morphological data for improving phylogenetic hypothesis in Dacrymycetes. Mycologia 105:1110–1125PubMedCrossRefGoogle Scholar
  121. Shirouzu T, Hirose D, Tokumasu S (2009) Taxonomic study of the Japanese Dacrymycetes. Persoonia 23:16–34PubMedPubMedCentralCrossRefGoogle Scholar
  122. Sinclair WA, Lyon HH, Johnson WT (1987) Diseases of trees and shrubs. Cornell University Press, Ithaca, p 574Google Scholar
  123. Sjökvist E, Pfeil BE, Larsson E, Larsson KH (2014) Stereopsidales—a new order of mushroom-forming fungi. PLoS ONE 9:e95227PubMedPubMedCentralCrossRefGoogle Scholar
  124. Skrede I, Engh IB, Binder M, Carlsen T et al (2011) Evolutionary history of Serpulaceae (Basidiomycota): molecular phylogeny, historical biogeography and evidence for a single transition of nutritional mode. BMC Evol Biol 11:230PubMedPubMedCentralCrossRefGoogle Scholar
  125. Slippers B, Coutinho TA, Wingfield BD, Wingfield MJ (2003) A review of the genus Amylostereum and its association with woodwasps. S Afr J Sci 99:70–74Google Scholar
  126. Smith SY, Currah RS, Stockey RA (2004) Cretaceous and Eocene poroid hymenophores from Vancouver Island, British Columbia. Mycologia 96:180–186PubMedCrossRefGoogle Scholar
  127. Stadler T, Rabosky DL, Ricklefs R, Bokma F (2014) On age and species richness of higher taxa. Am Nat 184:447–455PubMedCrossRefGoogle Scholar
  128. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690PubMedCrossRefGoogle Scholar
  129. Stefani FOP, Jones RH, May TW (2014) Concordance of seven gene genealogies compared to phenotypic data reveals multiple cryptic species in Australian dermocyboid Cortinarius (Agaricales). Mol Phylogenet Evol 71:249–260PubMedCrossRefGoogle Scholar
  130. Swann EC, Taylor JW (1993) Higher taxa of Basidiomycetes: an 18S rRNA gene perspective. Mycologia 85:923–936CrossRefGoogle Scholar
  131. Swann EC, Taylor JW (1995) Phylogenetic perspectives on basidiomycete systematics: evidence from the 18S rRNA gene. Can J Bot 73:S862–S868CrossRefGoogle Scholar
  132. Talavera G, Lukhtanov VA, Pierce NE, Vila R (2013) Establishing criteria for higher-level classification using molecular data: the systematics of Polyommatus blue butterflies (Lepidoptera, Lycaenidae). Cladistics 29:166–192CrossRefGoogle Scholar
  133. Tamura K, Battistuzzib FU, Billing-Rossb P, Murillob O et al (2012) Estimating divergence times in large molecular phylogenies. Proc Natl Acad Sci USA 109(47):19333–19338PubMedPubMedCentralCrossRefGoogle Scholar
  134. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729PubMedPubMedCentralCrossRefGoogle Scholar
  135. Taylor JW, Jacobson DJ, Kroken S, Kasuga T et al (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Gen Biol 31:21–32CrossRefGoogle Scholar
  136. van Dongen S (2000) Graph clustering by flow simulation. PhD thesis, University of Utrecht, NetherlandsGoogle Scholar
  137. Van Driel GA, Humbel BM, Verkleu AJ, Stalpers J et al (2009) Septal pore complex morphology on the Agaricomycotina (Basidiomycota) with emphasis on the Cantharellales and Hymenochaetales. Mycol Res 113:559–576PubMedCrossRefGoogle Scholar
  138. Veldrea V, Abarenkova K, Bahrama M, Martosc F et al (2013) Evolution of nutritional modes of Ceratobasidiaceae (Cantharellales, Basidiomycota) as revealed from publicly available ITS sequences. Fungal Ecol 6:256–268CrossRefGoogle Scholar
  139. Vilgalys R, Hopple JS, Hibbett DS (1994) Phylogenetic implications of generic concepts in fungi: the impact of molecular systematic studies. Mycol Helv 6:73–91Google Scholar
  140. Wang QM, Begerow D, Groenewald M, Liu XZ et al (2015a) Multigene phylogeny and taxonomic revision of yeasts and related fungi in the Ustilaginomycotina. Stud Mycol 81:55–83PubMedPubMedCentralCrossRefGoogle Scholar
  141. Wang QM, Groenewald M, Takashima M, Theelen B et al (2015b) Phylogeny of yeasts and related filamentous fungi within Pucciniomycotina determined from multigene sequence analyses. Stud Mycol 81:27–53PubMedPubMedCentralCrossRefGoogle Scholar
  142. Wang QM, Theelen B, Groenewald M, Bai FY, Boekhout T (2014) Moniliellomycetes and Malasseziomycetes, two new classes in Ustilaginomycotina. Persoonia 33:41–47PubMedPubMedCentralCrossRefGoogle Scholar
  143. Wang QM, Yurkov AM, Göker M, Lumbsch HT et al (2015c) Phylogenetic classification of yeasts and related taxa within Pucciniomycotina. Stud Mycol 81:146–189Google Scholar
  144. Wang YZ, Zhuang JY (1998) Flora fungorum sinicorum vol. 10 Pucciniales 1. Scinece Press, Beijing (in Chinese) Google Scholar
  145. Wannathes N, Desjardin DE, Hyde KD, Perry BA, Lumyong S (2009) A monograph of Marasmius (Basidiomycota) from Northern Thailand based on morphological and molecular (ITS sequences) data. Fungal Divers 37:209–306Google Scholar
  146. Weiß M, Bauer R, Begerow D (2004) Spotlights on heterobasidiomycetes. In: Agerer R, Blanz P, Piepen-bring M (eds) Frontiers in Basidiomycete mycology. Germany, IHW-Verlag, München, pp 7–48Google Scholar
  147. Weiss M, Bauer R, Sampaio JP, Oberwinkler F (2014) Tremellomycetes and related groups. In: McLaughlin DJ, Spatafora JW (eds) Systematics and evolution, the mycota VII part A. Springer, Berlin, pp 349–350Google Scholar
  148. 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 methods and applications. Academic Press, New York, pp 315–322Google Scholar
  149. Wilson AW, Binder M, Hibbett DS (2012) Diversity and evolution of ectomycorrhizal host associations in the Sclerodermatineae (Boletales, Basidiomycota). New Phytol 194:1079–1095PubMedCrossRefGoogle Scholar
  150. Wu G, Feng B, Xu J, Zhu XT et al (2014) Molecular phylogenetic analyses redefine seven major clades and reveal 22 new generic lineages in the fungal family Boletaceae. Fungal Divers 69:93–115CrossRefGoogle Scholar
  151. Wuczkowski M, Passoth V, Turchetti B, Andersson AC et al (2011) Description of Holtermanniella gen. nov., including Holtermanniella takashimae sp. nov. and four new combinations, and proposal of the order Holtermanniales to accommodate tremellomycetous yeasts of the Holtermannia clade. Int J Syst Evol Microbiol 61:680–689PubMedCrossRefGoogle Scholar
  152. Yang ZL (2011) Molecular techniques revolutionize knowledge of basidiomycete evolution. Fungal Divers 50:47–58CrossRefGoogle Scholar
  153. Zajc J, Liu Y, Dai W, Yang Z, Hu J, Gostinčar C, Gunde-Cimerman N (2013) Genome and transcriptome sequencing of the halophilic fungus Wallemia ichthyophaga: haloadaptations present and absent. BMC Genom 14:617CrossRefGoogle Scholar
  154. Zalar P, de Hoog GS, Schroers H-J, Frank JM, Gunde-Cimerman N (2005) Taxonomy and phylogeny of the xerophilic genus Wallemia (Wallemiomycetes and Wallemiales, cl. et ord. nov.). Antonie Van Leeuwenhoek J Microb 87:311–328CrossRefGoogle Scholar
  155. Zhang JX, Chen Q, Huang CY, Gao W, Qu JB (2015) History, current situation and trend of edible mushroom industry development. Mycosystema 34:524–540Google Scholar
  156. Zhao Q, Feng B, Yang ZL, Dai YC et al (2013) New species and distinctive geographical divergences of the genus Sparassis (Basidiomycota): evidence from morphological and molecular data. Mycol Prog 12:445–454CrossRefGoogle Scholar
  157. Zhao RL, Karunarathna SC, Raspé O, Parra LA et al (2011) Major clades in tropical Agaricus. Fungal Divers 51:279–296CrossRefGoogle Scholar
  158. Zhao RL, Zhou JL, Chen J, Margaritescu S et al (2016) Towards standardizing taxonomic ranks using divergence times—a case study for reconstruction of the Agaricus taxonomic system. Fungal Divers 78:239–292CrossRefGoogle Scholar
  159. Zhuang JY (2003) Flora Fungorum Sinicorum Vol. 19 Pucciniales 2. Scinece Press, Beijing, 324 pp (In Chinese)Google Scholar
  160. Zhuang JY (2005) Flora fungorum sinicorum vol. 25 Pucciniales 3. Scinece Press, Beijing (in Chinese) Google Scholar
  161. Zhuang JY (2012) Flora fungorum sinicorum vol. 41 Pucciniales 4. Scinece Press, Beijing (in Chinese) Google Scholar
  162. Zundel GL (1953) The Ustilaginales of the world, vol 176. Contributions from the Department of Botany Pennsylvania State College, pp. 1–410Google Scholar

Copyright information

© School of Science 2017

Authors and Affiliations

  • Rui-Lin Zhao
    • 1
    • 2
  • Guo-Jie Li
    • 1
  • Santiago Sánchez-Ramírez
    • 3
    • 4
  • Matt Stata
    • 3
    • 4
  • Zhu-Liang Yang
    • 5
  • Gang Wu
    • 5
  • Yu-Cheng Dai
    • 6
  • Shuang-Hui He
    • 6
  • Bao-Kai Cui
    • 6
  • Jun-Liang Zhou
    • 6
  • Fang Wu
    • 6
  • Mao-Qiang He
    • 1
  • Jean-Marc Moncalvo
    • 3
    • 4
  • Kevin D. Hyde
    • 7
    • 8
  1. 1.State Key Laboratory of Mycology, Institute of MicrobiologyChinese Academy of SciencesBeijingChina
  2. 2.College of Life SciencesUniversity of Chinese Academy of SciencesBeijingChina
  3. 3.Department of Ecology and Evolutionary BiologyUniversity of TorontoTorontoCanada
  4. 4.Department of Natural HistoryRoyal Ontario MuseumTorontoCanada
  5. 5.Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of BotanyChinese Academy of SciencesKunmingChina
  6. 6.Institute of Microbiology and Beijing Key Laboratory for Forest Pest ControlBeijing Forestry UniversityBeijingChina
  7. 7.Center of Excellence in Fungal ResearchMae Fah Luang UniversityChiang RaiThailand
  8. 8.Key Laboratory of Economic Plants and Biotechnology, Kunming Institute of BotanyChinese Academy of SciencesKunmingChina

Personalised recommendations