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Mycological Progress

, Volume 15, Issue 9, pp 939–946 | Cite as

Phylogenetic evidence places the coralloid jelly fungus Tremellodendropsis tuberosa (Tremellodendropsidales) among early diverging Agaricomycetes

  • Mary L. BerbeeEmail author
  • Eunice Y. Y. Wong
  • Clement K. M. Tsui
Original Article

Abstract

We explored the phylogenetic relationships of Tremellodendropsis tuberosa from western North America. The species has tough, coralloid fruiting bodies that emerge from a basal tuber, as well as unusual, partially septate basidia, large elliptical spores, and regular clamp connections. It has been classified variously in Auriculariales, Tremellales, and in its own order, Tremellodendropsidiales. To evaluate support for these alternatives, we extracted DNA from four specimens and sequenced ∼5000 bp from the ribosomal large subunit, small subunit and internal transcribed spacer region from each. We aligned sequences from T. tuberosa with sequences from GenBank that represented 31 Basidiomycota orders and then analyzed the individual and concatenated sequence regions using Bayesian and maximum likelihood approaches. Analyses agreed that T. tuberosa is an early diverging member of Agaricomycetes, but did not provide unequivocal support for its sister group relationships within the class. From the concatenated alignment, after removal of poorly aligned sites using Gblocks, T. tuberosa appeared as the sister group to a clade encompassing four orders, three of them from Phallomycetidae. This relationship had a Bayesian posterior probability of 1.0 and appeared, although without bootstrap support, in maximum likelihood trees. Tree topology tests ruled out placing T. tuberosa within the Auriculariales. We accept that T. tuberosa should be placed in its own order, the Tremellodendropsidales, and not in Auriculariales or Tremellales. As a taxon that diverged early from other Basidiomycota clades, T. tuberosa should be included in further studies of phylogeny and character evolution in Agaricomycetes.

Keywords

Agaricomycetes Basidiomycota Basidium morphology Evolution Fungal phylogeny LSU SSU 

Notes

Acknowledgments

We thank O. and A. Ceska, D. Bojantchev, and L. Le Renard for specimens. Jaclyn M. Dee provided mentorship for students involved in sequencing. This research was supported by a National Science and Engineering Research Council of Canada Discovery Grant RGPIN-2016-03746 to M. Berbee

Supplementary material

11557_2016_1220_MOESM1_ESM.pdf (335 kb)
ESM 1 (PDF 335 kb)

References

  1. Allen TR, Millar T, Berch SM, Berbee ML (2003) Culturing and direct DNA extraction find different fungi from the same ericoid mycorrhizal roots. New Phytol 160:255–272. doi: 10.1046/j.1469-8137.2003.00885.x CrossRefGoogle Scholar
  2. Bunyard BA, Nicholson MS, Royse DJ (1994) A systematic assessment of Morchella using RFLP analysis of the 28s ribosomal-RNA gene. Mycologia 86:762–772. doi: 10.2307/3760589 CrossRefGoogle Scholar
  3. Corner EJH (1950) A Monograph of Clavaria and Allied Genera. Oxford University Press, LondonGoogle Scholar
  4. Corner EJH (1953) Addenda Clavariacea. III. Ann Bot 17:347–368Google Scholar
  5. Corner EJH (1966) Clavarioid complex of Aphelaria and Tremellodendropsis. Br Mycol Soc Trans 49:205–211CrossRefGoogle Scholar
  6. Corner EJH (1970) Supplement to a monograph of Clavaria and allied genera. Beih Nova Hedwigia 33:1–299Google Scholar
  7. Crawford DA (1954) Studies on New Zealand Clavariaceae. Trans R Soc N Z 82:617–631Google Scholar
  8. Greville RK (1825) Scottish cryptogamic flora, vol III. MacLachlan & Stewart, EdinburghGoogle Scholar
  9. Hosaka K, Bates ST, Beever RE, Castellano MA, Colgan W, Dominguez LS, Nouhra ER et al (2006) Molecular phylogenetics of the gomphoid-phalloid fungi with an establishment of the new subclass Phallomycetidae and two new orders. Mycologia 98:949–959CrossRefPubMedGoogle Scholar
  10. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. doi: 10.1093/bioinformatics/17.8.754 CrossRefPubMedGoogle Scholar
  11. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G et al (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818–822. doi: 10.1038/nature05110 CrossRefPubMedGoogle Scholar
  12. Jülich W (1981) Higher Taxa of Basidiomycetes. Bibliotheca Mycologica vol 85. J. Cramer, Vaduz, LiechtensteinGoogle Scholar
  13. Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701. doi: 10.1093/molbev/mss020 CrossRefPubMedGoogle Scholar
  14. Liu XZ, Wang QM, Goker M, Groenewald M, Kachalkin AV, Lumbsch HT, Millanes AM et al (2015) Towards an integrated phylogenetic classification of the Tremellomycetes. Stud Mycol 85–147 doi: 10.1016/j.simyco.2015.12.001
  15. Lowy B (1968) Taxonomic problems in the Heterobasidiomycetes. Taxon 17:118–127. doi: 10.2307/1216500 CrossRefGoogle Scholar
  16. Maddison WP, Maddison DR (2015) Mesquite: a modular system for evolutionary analysis ver. 3.04. http://mesquiteproject.org
  17. Millanes AM, Diederich P, Ekman S, Wedin M (2011) Phylogeny and character evolution in the jelly fungi (Tremellomycetes, Basidiomycota, Fungi). Mol Phylogenet Evol 61:12–28. doi: 10.1016/j.ympev.2011.05.014 CrossRefPubMedGoogle Scholar
  18. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA. pp 1–8. doi: 10.1109/GCE.2010.5676131
  19. Nguyen HDT, Nickerson NL, Seifert KA (2013) Basidioascus and Geminibasidium: a new lineage of heat-resistant and xerotolerant basidiomycetes. Mycologia 105:1231–1250. doi: 10.3852/12-351 CrossRefPubMedGoogle Scholar
  20. Nomura N, Ogura-Tsujita Y, Gale SW, Maeda A, Umata H, Hosaka K, Yukawa T (2013) The rare terrestrial orchid Nervilia nipponica consistently associates with a single group of novel mycobionts. J Plant Res 126:613–623. doi: 10.1007/s10265-013-0552-8 CrossRefPubMedGoogle Scholar
  21. Oberwinkler F, Lowy B (1981) Studies in Heterobasidiomycetes.10. Syzygospora alba, a mycoparasitic heterobasidiomycete. Mycologia 73:1108–1115. doi: 10.2307/3759680 CrossRefGoogle Scholar
  22. Oberwinkler F, Riess K, Bauer R, Selosse M-A, Weiss M, Garnica S, Zuccaro A (2013) Enigmatic Sebacinales. Mycol Prog 12:1–27. doi: 10.1007/s11557-012-0880-4 CrossRefGoogle Scholar
  23. Oberwinkler F, Riess K, Bauer R, Garnica S (2014) Morphology and molecules: the Sebacinales, a case study. Mycol Prog 13:445–470. doi: 10.1007/s11557-014-0983-1 CrossRefGoogle Scholar
  24. Olive LS (1957) Two new genera of the Ceratobasidiaceae and their phylogenetic significance. Am J Bot 44:429–435. doi: 10.2307/2438513 CrossRefGoogle Scholar
  25. Patouillard N (1900) Essai taxonomique sur les familles et les genres des Hyménomycètes. Dissertation, Université de ParisGoogle Scholar
  26. Petersen RH (1985) Type studies in the clavarioid fungi. 9. Miscellaneous taxa, with a section on Tremellodendropsis. Persoonia 12:401–413Google Scholar
  27. Petersen RH (1987) Notes on clavarioid fungi. XXI New Zealand taxa of Tremellodendropsis. Mycotaxon 29:45–65Google Scholar
  28. Rogers DP (1934) The basidium. Univ Iowa Stud Nat Hist 16:160–182Google Scholar
  29. Rogers DP (1971) Patterns of evolution to the Homobasidiomycetes. In: Petersen RH (ed) Evolution in the higher basidiomycetes. University of Tennessee Press, Knoxville USA, pp 241–257Google Scholar
  30. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B et al (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi: 10.1093/sysbio/sys029 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Shimodaira H, Hasegawa M (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17:1246–1247. doi: 10.1093/bioinformatics/17.12.1246 CrossRefPubMedGoogle Scholar
  32. Shirouzu T, Hirose D, Oberwinkler F, Shimomura N, Maekawa N, Tokumasu S (2013) Combined molecular and morphological data for improving phylogenetic hypothesis in Dacrymycetes. Mycologia 105:1110–1125. doi: 10.3852/12-147 CrossRefPubMedGoogle Scholar
  33. Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337. doi: 10.1007/s13127-011-0056-0 CrossRefGoogle Scholar
  34. Sjökvist E, Pfeil BE, Larsson E, Larsson KH (2014) Stereopsidales - A new order of mushroom-forming fungi. Plos One 9 doi: 10.1371/journal.pone.0095227
  35. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. doi: 10.1093/bioinformatics/btu033 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577. doi: 10.1080/10635150701472164 CrossRefPubMedGoogle Scholar
  37. Těšitelová T, Kotilínek M, Jersáková J, Joly FX, Košnar J, Tatarenko I, Selosse MA (2015) Two widespread green Neottia species (Orchidaceae) show mycorrhizal preference for Sebacinales in various habitats and ontogenetic stages. Mol Ecol 24:1122–1134. doi: 10.1111/mec.13088 CrossRefPubMedGoogle Scholar
  38. Van Driel KGA, Humbel BM, Verkleij AJ, Stalpers J, Muller WH, Boekhout T (2009) Septal pore complex morphology in the Agaricomycotina (Basidiomycota) with emphasis on the Cantharellales and Hymenochaetales. Mycol Res 113:559–576. doi: 10.1016/j.mycres.2008.12.007 CrossRefPubMedGoogle Scholar
  39. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246PubMedPubMedCentralGoogle Scholar
  40. Vizzini A (2014) Tremellodendropsidales Vizzini, Ord. nov. Index Fungorum 152Google Scholar
  41. Warcup JH (1988) Mycorrhizal associations of isolates of Sebacina vermifera. New Phytol 110:227–231. doi: 10.1111/j.1469-8137.1988.tb00256.x CrossRefGoogle Scholar
  42. Weiss M, Oberwinkler F (2001) Phylogenetic relationships in Auriculariales and related groups - hypotheses derived from nuclear ribosomal DNA sequences. Mycol Res 105:403–415. doi: 10.1017/s095375620100363x CrossRefGoogle Scholar
  43. Weiss M, Sykorova Z, Garnica S, Riess K, Martos F, Krause C, Oberwinkler F et al. (2011) Sebacinales everywhere: Previously overlooked ubiquitous fungal endophytes. PloS One 6 doi: 10.1371/journal.pone.0016793
  44. Wells K (1994) Jelly fungi, then and now. Mycologia 86:18–48. doi: 10.2307/3760717 CrossRefGoogle Scholar
  45. Wells K, Oberwinkler F (1982) Tremelloscypha gelatinosa, a species of a new family Sebacinaceae. Mycologia 74:325–331CrossRefGoogle Scholar
  46. White TJ, Bruns T, Lee S, Taylor J (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, San Diego, California, pp 315–322Google Scholar
  47. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214CrossRefPubMedGoogle Scholar

Copyright information

© German Mycological Society and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Mary L. Berbee
    • 1
    Email author
  • Eunice Y. Y. Wong
    • 1
  • Clement K. M. Tsui
    • 1
    • 2
  1. 1.Department of BotanyUniversity of British ColumbiaVancouverCanada
  2. 2.Department of Pathology and Laboratory Medicine, Faculty of MedicineThe University of British ColumbiaVancouverCanada

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