Plant Ecology and Evolution 153(2): 229-245, doi: 10.5091/plecevo.2020.1667
New insights on Bjerkandera (Phanerochaetaceae, Polyporales) in the Neotropics with description of Bjerkandera albocinerea based on morphological and molecular evidence
expand article infoViviana Motato-Vásquez, Adriana M. Gugliotta, Mario Rajchenberg§, Myriam Catania|, Carlos Urcelay, Gerardo Robledo#¤
‡ Núcleo de Pesquisa em Micologia, Instituto de Botânica, Av. Miguel Stefano 3687, 04301-902, São Paulo, Brazil§ Centro de Investigación y Extensión Forestal Andino Patagónico, C.C. 14, 9200 Esquel, Chubut, Argentina| Laboratorio de Micología, Fundación M. Lillo, Miguel Lillo 251, T4000JFE San Miguel de Tucumán, Argentina¶ Instituto Multidisciplinario de Biología Vegetal-CONICET, Universidad Nacional de Córdoba, CC 495, CP 5000, Córdoba, Argentina# Universidad Nacional de Córdoba, Córdoba, Argentina¤ Fundación Fungicosmos, Córdoba, Argentina
Open Access
Abstract

Background and aimsBjerkandera is one of the few poroid genera in the Phanerochaetaceae family known to date. The genus has a worldwide distribution and is characterized by effused-reflexed, pileate basidiomata with a pale cream to smoky or mouse grey hymenophore that becomes darker when dried, and a monomitic hyphal structure with clamped generative hyphae. Morphological and phylogenetic studies have traditionally accepted only two species in the genus, B. adusta (generic type) and B. fumosa, both described from temperate Europe. Recently, three additional species, B. atroalba, B. centroamericana and B. mikrofumosa were described from the Neotropics. While studying polypores in the Yungas forests of northwest Argentina and the Atlantic Forest of southeast Brazil, several specimens of Bjerkandera were gathered. A comparative morphological study revealed that some of these specimens do not correspond to any of the known species in the genus. This study aimed to propose a broad species-level phylogenetic hypothesis for Bjerkandera in the Neotropics and worldwide and to discuss the taxonomic status and diversity of the species in this genus.

Methods – This study is based on a morphological examination of specimens collected between 2012 and 2017, and on a revision of original collections, including the type specimens. A total of eleven ITS and seven nLSU sequences were generated and phylogenetic analyses based on Bayesian Inference (BI) and Maximum Likelihood (ML) were performed.

Key results – An extensive documentation of the species diversity within Bjerkandera in the Neotropics is presented. Genetic data of B. mikrofumosa were obtained for the first time and its phylogenetic position was tested. Additionally, its geographic distribution was extended in the Neotropics to Argentina and Brazil. Finally, molecular and morphological evidence was used to propose a new species for the genus, Bjerkandera albocinerea sp. nov.

Conclusion – This study provides an update of the known diversity of the genus in the Neotropics and worldwide. In addition, our results indicate that the number of taxa in Bjerkandera has been underestimated by morphological evidence, and may actually be greater than traditionally accepted.

Keywords
cryptic species, Neotropical polypores, phylogeny, taxonomy

References

  • Arhipova N., Gaitnieks T., Donis J., Stenlid J., Vasaitis R. (2012) Heart-rot and associated fungi in Alnus glutinosa stands in Latvia. Scandinavian Journal of Forest Research 27(4): 327–336. https://doi.org/10.1080/02827581.2012.670727
  • Baltazar J.M., Gibertoni T.B. (2009) A checklist of the aphyllophoroid fungi (Basidiomycota) recorded from the Atlantic Rain Forest. Mycotaxon 109: 439–442. https://doi.org/10.5248/109.439
  • Baxter D.W. (1941) Some resupinate polypores from the region of the Great Lakes. XII. Papers of the Michigan Academy of Science, Arts and Letters 26: 107–121.
  • Bernicchia A. (2005) Polyporaceae s.l. Fungi Europaei. Vol 10. Italy, Candusso, Alassio.
  • Binder M., Juato A., Riley R., Salamov A., López-Giráldez F., Sjökvist E., Copeland A., Foster B., Sun H., Larsson E., Larsson K.H., Towsend J., Grigoriev I.V., Hibbett D.S. (2013) Phylogenetic and phylogenomic overview of the Polyporales. Mycologia 105: 1350–1373. https://doi.org/10.3852/13-003
  • Bondartseva M.A., Kotkova V.M., Zmitrovich I.V., Volobuev S.V. (2014) Aphyllophoroid and heterobasidioid fungi of the Peter the Great Botanical Garden of the Komarov Botanical Institute of RAS (St. Petesburg). In: Geltman D.V. (ed.) The Botany: history, theory, practice (to the 300-year anniversary of Komarov Botanical Institute of the Russian Academy of Sciences (St. Petersburg): 23–30. Saint Petersburg: SPbSETU (LETI).
  • Corner E.J.H. (1989) Ad Polyporaceas V. The genera Albatrellus, Boletopsis, Coriolopsis (dimitic), Cristelloporia, Diacanthodes, Elmerina, Fomitopsis (dimitic), Gloeoporus, Grifola, Hapalopilus, Heterobasidion, Hydnopolyporus, Ischnoderma, Loweporus, Parmastomyces, Perenniporia, Pyrofomes, Steccherinum, Trechispora, Truncospora and Tyromyces. Beihefte zur Nova Hedwigia 96: 1–218.
  • Darriba D., Taboada G.L., Doallo R., Posada D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9(8): 772–772. https://doi.org/10.1038/nmeth.2109
  • Doyle J.J. (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry bulletin 19: 11–15.
  • Ewing B., Green P. (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Research 8(3): 186–194. https://doi.org/10.1101/gr.8.3.186
  • Ewing B., Hillier L., Wendl M.C., Green P. (1998) Base-calling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Research 8(3): 175–185. https://doi.org/10.1101/gr.8.3.175
  • Floudas D., Hibbett D.S. (2015) Revisiting the taxonomy of Phanerochaete (Polyporales, Basidiomycota) using a four genes dataset and extensive ITS sampling. Fungal Biology 119(8): 679–719. https://doi.org/10.1016/j.funbio.2015.04.003
  • Gilbertson R.L., Ryvarden L. (1986) North American polypores. Vol. 1: Abortiporus – Lindtneria. Oslo, Fungiflora.
  • Hall T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.
  • Homolka L., Lisá L., Eichlerova I., Vala’s V., Baldrian P. (2010) Effect of long-term preservation of basidiomycetes on perlite in liquid nitrogen on their growth, morphological, enzymatic and genetic characteristics. Fungal Biology 114: 929–935. 10. https://doi.org/10.1016/j.funbio.2010.08.009
  • Hopple J.S., Vilgalys R. (1999) Phylogenetic relationships in the mushroom genus Coprinus and dark-spored allies based on sequence data from the nuclear gene coding for the large ribosomal subunit RNA: divergent domains, outgroups, and monophyly. Molecular Phylogenetics and Evolution 13(1): 1–19. https://doi.org/10.1006/mpev.1999.0634
  • Jang Y., Jang S., Lee J., Lee H., Lim Y.W., Kim C., Kim J.J. (2016) Diversity of wood-inhabiting polyporoid and corticioid fungi in Odaesan National Park, Korea. Mycobiology 44(4): 217–236. https://doi.org/10.5941/MYCO.2016.44.4.217
  • Jung P.E., Fong J.J., Park M.S., Oh S.Y., Kim C., Lim Y.W. (2014) Sequence validation for the identification of the white-rot fungi Bjerkandera in public sequence databases. Journal of Microbiology and Technology 24(10): 1313–1319. https://doi.org/10.4014/jmb.1404.04021
  • Justo A., Miettinen O., Floudas D., Ortiz-Santana B., Sjökvist E., Lindner D., Nakasone K., Niemelä T., Larsson K.H., Ryvarden L., Hibbett D.S. (2017) A revised family-level classification of the Polyporales (Basidiomycota). Fungal Biology 121(9): 798–824. https://doi.org/10.1016/j.funbio.2017.05.010
  • Karsten P.A. (1879) Rysslands, Finlands, och den Skandinaviska Halfons Hatsvamper. Meddelanden af Societatis pro Fauna et Flora Fennica 5: 1–571.
  • Katoh K., Standley D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Phylogenetics and Evolution 30(4): 772–780. https://doi.org/10.1093/molbev/mst010
  • Lygis V., Vasiliauskas R., Larsson K.H., Stenlid J. (2005) Wood-inhabiting fungi in stems of Fraxinus excelsior in declining ash stands of northern Lithuania, with particular reference to Armillaria cepistipes. Scandinavian Journal of Forest Research 20(4): 337–346. https://doi.org/10.1080/02827580510036238
  • Martin R., Gazis R., Skaltsas D., Chaverri P., Hibbett D. (2015) Unexpected diversity of basidiomycetous endophytes in sapwood and leaves of Hevea. Mycologia 107(2): 284–297. https://doi.org/10.3852/14-206
  • Miettinen O., Spirin V., Vlasák J., Rivoire B., Stenroos S., Hibbett D.S. (2016) Polypores and genus concepts in Phanerochaetaceae (Polyporales, Basidiomycota). Mycokeys 17: 1–46. https://doi.org/10.3897/mycokeys.17.10153
  • Miettinen O., Vlasák J., Rivoire B., Spirin V. (2018) Postia caesia complex (Polyporales, Basidiomycota) in temperate Northern Hemisphere. Fungal Systematics and Evolution 1(1): 101–129. https://doi.org/10.3114/fuse.2018.01.05
  • Miller M.A., Pfeiffer W., Schwartz T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: 2010 Gateway Computing Environments Workshop (GCE), New Orleans, LA, 2010: 1–8. https://doi.org/10.1109/GCE.2010.5676129
  • Moreno G., Blanco M.N., Checa J., Platas G., Peláez F. (2011) Taxonomic and phylogenetic revision of three rare irpicoid species within the Meruliaceae. Mycological Progress 10(4): 481–491. https://doi.org/10.1007/s11557-010-0717-y
  • Motato-Vásquez V., Pires R.M., Vitalli V.M., Gugliotta A.M. (2016) Cultural and ligninolytic activity studies of some polypores (Basidiomycota) from Brazilian Atlantic Forest, São Paulo State, Brazil. Hoehnea 43(2): 281–292. https://doi.org/10.1590/2236-8906-81/2015
  • Murrill W.A. (1907) (Agaricales) Polyporaceae. North American Flora vol. 9(1): 1–71.
  • Nobles M.K. (1965) Cultural characters as a guide to the taxonomy and phylogeny of the Polyporaceae. Canadian Journal of Botany 36(6): 883–926. https://doi.org/10.1139/b58-071
  • Núñez M., Ryvarden L. (2001) East Asian Polypores, vol 2. Oslo, Fungiflora.
  • Oghenekaro A.O., Miettinen O., Omorusi V.I., Evueh G.A., Farid M.A., Gazis R., Asiegbu F.O. (2014) Molecular phylogeny of Rigidoporus microporus isolates associated with white rot disease of rubber trees (Hevea brasiliensis). Fungal Biology 118(5): 495–506. https://doi.org/10.1016/j.funbio.2014.04.001
  • Persoon C.H. (1801) Synopsis methodica fungorum, Part 1. Göttingen, Dieterich.
  • Pilát A. (1937) 1. Polyporaceae. In: Kavina K., Pilát A. (eds) Atlas des Champignons de l’Europe. Tome III. Prague.
  • R Core Team (2013) R: a language and environment for statistical computing, version 3.2.2. Available at http://www.R-project.org [accessed 30 Mar. 2020].
  • Rajchenberg M. (2011) Nuclear behaviour of the mycelium and the phylogeny of Polyporales (Basidiomycota). Mycologia 103(4): 677–702. https://doi.org/10.3852/10-310
  • Rambaut A., Suchard M.A., Xie D., Drummond A.J. (2014) Tracer v.1.6. Available at http://beast.bio.ed. ac.uk/Tracer [accessed 10 Jan. 2018].
  • Rick J. (1935) Polysticti Riograndenses. Brotéria Série Trimestral: Ciências Naturais 4: 121–138.
  • Rick J. (1960) Basidiomycetes Eubasidii in Rio Grande do Sul, Brasília 4. Meruliaceae, Polyporaceae, Boletaceae. Iheringia, Série Botânica 7: 193–295.
  • Robledo G.L., Rajchenberg M. (2007) South American polypores: first annotated checklist from Argentinean Yungas. Mycotaxon 100: 5–9.
  • Robledo G.L., Urcelay M., Rajchenberg M., Dominguez L. (2003) Políporos (Aphyllophorales, Basidiomycota) parásitos y saprófitos de Alnus acuminate en el noroeste argentino. Boletín de la Sociedad Argentina de Botánica 38(3–4): 207–224.
  • Robledo G.L., Urcelay C., Domínguez L., Rajchenberg M. (2006) Taxonomy, ecology and biogeography of Polypores (Basidiomycetes) from Argentinian Polylepis woodlands. Canadian Journal of Botany 84(10): 1561–1572. https://doi.org/10.1139/b06-109
  • Robles C.A., Carmarán C.C., Lopez S.E. (2011) Screening of xylophagous fungi associated with Platanus acerifolia in urban landscapes: Biodiversity and potential biodeterioration. Landscape and urban planning 100(1–2): 129–135. https://doi.org/10.1016/j.landurbplan.2010.12.003
  • Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3): 539–542. https://doi.org/10.1093/sysbio/sys029
  • Ryvarden L. (2000) Studies in neotropical polypores 8. Poroid fungi from Jamaica – a preliminary check list. Mycotaxon 76: 349–360.
  • Ryvarden L. (2016) Studies in Neotropical polypores 43. Some new species from tropical America. Synopsis Fungorum 35: 43–52.
  • Ryvarden L., Gilbertson R.L. (1993) European polypores. Synopsis Fungorum 6, vol. 1. Oslo, Fungiflora.
  • Ryvarden L., Iturriaga T. (2001) Studies in Neotropical polypores 9. A critical checklist of poroid fungi from Venezuela. Mycotaxon 78: 393–405.
  • Ryvarden L., Melo I. (2017) Poroid fungi of Europe. Synopsis Fungorum 37. Oslo, Fungiflora.
  • Sjökvist E., Larsson E., Eberhardt U., Ryvarden L., Larsson K.H. (2012) Stipitate stereoid basidiocarps have evolved multiple times. Mycologia 104(5): 1046–1055. https://doi.org/10.3852/11-174
  • Spegazzini C. (1919) Los hongos de Tucumán. Primera Reunión Nacional de la Sociedad Argentina de Ciencias Naturales 1916: 254–274.
  • Thiers B. (continuously updated) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available at http://sweetgum.nybg.org/ih/ [accessed 1 Apr. 2019].
  • Tomšovský M., Ryvarden L. (2008) Gloeoporus dichrous var. niger comb. nov. Mycotaxon 105: 171–174.
  • Ţura S., Zmitrovich I.V., Wasser S.P., Spirin W.A., Nevo E. (2010) Biodiversity of Heterobasidiomycetes and non-gilled Hymenomycetes (former Aphyllophorales) of Israel. Ruggell, Gantner verlag K.-G.
  • Westphalen M.C., Tomšovský M., Kout J., Gugliotta A.M. (2015) Bjerkandera in the Neotropics: phylogenetic and morphological relations of Tyromyces atroalbus and description of a new species. Mycological Progress 14: 100. https://doi.org/10.1007/s11557-015-1124-1
  • Willdenow K.L. (1787) Florae Berolinensis prodromus: secundum systema Linneanum ab illustr. Viro eq. C.P. Thunbergio emendatum conscriptus. Berlin, Wilhelm Vieweg. https://doi.org/10.5962/bhl.title.6727
  • White T.J., Bruns T., Lee S.J.W.T., Taylor J.W. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M.A., Gelfand D.H., Sninsky J.J., White T.J. (eds) PCR protocols: A guide to methods and applications, 38: 315–322. Cambridge MA, Academic Press.
  • Yuan Z.L., Rao L.B. Chen Y.C. Zhang C.L. Wu Y.G. (2010) From pattern to process: species and functional diversity in fungal endophytes of Abies beshanzuensis. Fungal Biology 115(3): 197–213. https://doi.org/10.1016/j.funbio.2010.11.002
  • Zwickl D.J. (2006–2011) GARLI – Genetic Algorithm for Rapid Likelihood Inference. Available at https://code.google.com/archive/p/garli/ [accessed 30 Mar. 2020].