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Mycological Progress

, Volume 17, Issue 9, pp 989–998 | Cite as

Tying up loose threads: revised taxonomy and phylogeny of an avian-dispersed Neotropical rhizomorph-forming fungus

  • Rachel A. Koch
  • D. Jean Lodge
  • Susanne Sourell
  • Karen Nakasone
  • Austin G. McCoy
  • M. Catherine Aime
Original Article

Abstract

Rhizomorpha corynecarpos Kunze was originally described from wet forests in Suriname. This unusual fungus forms white, sterile rhizomorphs bearing abundant club-shaped branches. Its evolutionary origins are unknown because reproductive structures have never been found. Recent collections and observations of R. corynecarpos were made from Belize, Brazil, Ecuador, Guyana, and Peru. Phylogenetic analyses of three nuclear rDNA regions (internal transcribed spacer, large ribosomal subunit, and small ribosomal subunit) were conducted to resolve the phylogenetic relationship of R. corynecarpos. Results show that this fungus is sister to Brunneocorticium bisporum—a widely distributed, tropical crust fungus. These two taxa along with Neocampanella blastanos form a clade within the primarily mushroom-forming Marasmiaceae. Based on phylogenetic evidence and micromorphological similarities, we propose the new combination, Brunneocorticium corynecarpon, to accommodate this species. Brunneocorticium corynecarpon is a pathogen, infecting the crowns of trees and shrubs in the Neotropics; the long, dangling rhizomorphs with lateral prongs probably colonize neighboring trees. Longer-distance dispersal can be accomplished by birds as it is used as construction material in nests of various avian species.

Keywords

Agaricales Fungal systematics Marasmiineae Marasmius Phytopathogenic fungi Tetrapyrgos New taxon 

Notes

Acknowledgements

The authors wish to thank David Hibbett, Tim Baroni, and one anonymous reviewer for their helpful comments on this manuscript; Chris Andrew, Francino Edmund, Justin Edmund, Peter Joseph, and Ramkin Joseph for the assistance in the field; NSF DDIG (DEB-1501782), NSF DEB-1556412, NSF DEB-0103621, the Mycological Society of America Undergraduate Research Award, and USDA Hatch #1010662 for the financial resources; Richard C. Hoyer/Birdernaturalist and Joseph M. Wunderle, Jr. who graciously provided photographs; and Amy Rossman, Drew Minnis, Shannon Dominick, and Melanie Schori for assistance in resolving the nomenclature issues related to R. corynecarpos.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Aime MC, Phillips-Mora W (2005) The causal agents of witches’ broom and frosty pod rot of cacao (chocolate, Theobroma cacao) form a new lineage of Marasmiaceae. Mycologia 97:1012–1022PubMedGoogle Scholar
  2. Antonín V (2007) Fungus Flora of tropical Africa, Volume 1: Monograph of Marasmius, Gloiocephala, Palaeocephala and Setulipes in Tropical Africa. National Botanic Garden, BelgiumGoogle Scholar
  3. Aubrecht G, Huber W, Weissenhofer A (2013) Coincidence or benefit? The use of Marasmius (horse-hair fungus) filaments in bird nests. Avian Biol Res 6:26–30CrossRefGoogle Scholar
  4. Berkeley MJ (1856) Decades of fungi. Decades LXI–LXII. Rio Negro fungi. Hooker’s J Bot Kew Gard Misc 8:272–280Google Scholar
  5. Berlese AN (1892) Rapporti tra Dematophora e Rosellinia. Riv Patol Veg 1:5–17Google Scholar
  6. Boddy L (1993) Saprotrophic cord-forming fungi: warfare strategies and other ecological aspects. Mycol Res 97:641–655CrossRefGoogle Scholar
  7. Boidin J, Lanquetin P, Duhem B (1996) Contribution à la connaissance du genre Dendrothele (Basidiomycotina, Aphyllophorales). Bull Trimest Soc Mycol Fr 112:87–126Google Scholar
  8. Bonito G, May TW (2014) Barcoding of Australian fungi. NCBI GenBank. https://www.ncbi.nlm.nih.gov/genbank/. Accessed 4 June 2018
  9. Burdsall HH Jr, Nakasone KK (1983) Species of effused Aphyllophorales (Basidiomycotina) from the southeastern United States. Mycotaxon 17:253–268Google Scholar
  10. Burt EA (1918) Corticiums causing Pellicularia disease of the coffee plant, hypochnose of pomaceous fruits, and Rhizoctonia disease. Ann Mo Bot Gard 5:119–132CrossRefGoogle Scholar
  11. Cairney JWG (1991a) Rhizomorphs: organs of exploration or exploitation? Mycologist 5:5–10CrossRefGoogle Scholar
  12. Cairney JWG (1991b) Rhizomorph structure and development in Marasmius crinisequi. Mycol Res 95:1429–1432CrossRefGoogle Scholar
  13. Ceresini PC, Costa-Souza E, Zala M, Furtado EL, Souza NL (2012) Evidence that the Ceratobasidium-like white-thread blight and black rot fungal pathogens from persimmon and tea crops in the Brazilian Atlantic Forest agroecosystem are two distinct phylospecies. Genet Mol Biol 35:480–497CrossRefPubMedPubMedCentralGoogle Scholar
  14. Dentinger BTM, Gaya E, O’Brien H, Suz LM, Lachlan R, Díaz-Valderrama JR, Koch RA, Aime MC (2016) Tales from the crypt: genome mining from fungarium specimens improves resolution of the mushroom tree of life. Biol J Linnean Soc 117:11–32CrossRefGoogle Scholar
  15. Donk MA (1962) The generic names proposed for Agaricaceae. Beih Nova Hedwigia 5:1–320Google Scholar
  16. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefPubMedPubMedCentralGoogle Scholar
  17. Freymann BP (2008) Physical properties of fungal rhizomorphs of marasmioid basidiomycetes used as nesting material by birds. Ibis 150:395–399CrossRefGoogle Scholar
  18. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118CrossRefPubMedGoogle Scholar
  19. Golley FB (1983) Decomposition. In: Golley FB (ed) Tropical Rain Forest Ecosystems. Structure and Function. Elsevier Scientific Publishing Company, Amsterdam, pp 157–166Google Scholar
  20. Gónzalez D, Rodriguez-Carres M, Boekhout T, Stalpers J, Kuramae EE, Nakatani AK, Vilgalys R, Cubeta MA (2016) Phylogenetic relationships of Rhizoctonia fungi within the Cantharellales. Fungal Biol 120:603–619CrossRefPubMedPubMedCentralGoogle Scholar
  21. Granlund HI, Jennings DH, Thompson W (1985) Translocation of solutes along rhizomorphs of Armillaria mellea. Trans Br Mycol Soc 84:111–119CrossRefGoogle Scholar
  22. Hedger J (1990) Fungi in the tropical forest canopy. Mycologist 4:200–202CrossRefGoogle Scholar
  23. Hedger J, Lewis P, Gitay H (1993) Litter-trapping by fungi in moist tropical forest. In: Isaac S, Frankland JC, Watling R, AJS W (eds) Aspects of Tropical Mycology. Cambridge University Press, Cambridge, pp 15–36Google Scholar
  24. Henkel TW (2003) Monodominance in the ectomycorrhizal Dicymbe corymbosa (Caesalpiniaceae) from Guyana. J Trop Ecol 19:417–437CrossRefGoogle Scholar
  25. Henkel TW, Aime MC, Chin MML, Miller SL, Vilgalys R, Smith ME (2012) Ectomycorrhizal fungal sporocarp diversity and discovery of new taxa in Dicymbe monodominant forests of the Guiana shield. Biodivers Conserv 21:2195–2220CrossRefGoogle Scholar
  26. Hennings P (1904) Fungi Amazonici a cl. Ernesto Ule collecti III Hedwigia 43:351–400Google Scholar
  27. Hu CC (1984) Horse-hair blight, new disease of tea bush caused by Marasmius equicrinis Mull in Taiwan. Taiwan Tea Res Bull 3:1–4Google Scholar
  28. Isaacs R, Gillman MP, Johnston M, Marsh F, Wood BC (1996) Size structure of a dominant Neotropical forest tree species, Dicymbe altsonii, in Guyana and some factors reducing seedling leaf area. J Trop Ecol 12:599–606CrossRefGoogle Scholar
  29. Koch RA, Wilson AW, Séné O, Henkel TW, Aime MC (2017) Resolved phylogeny and biogeography of the root pathogen Armillaria and its gasteroid relative, Guyanagaster. BMC Evol Biol 17:33CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lanfear R, Calcott B, Ho SY, Guindon S (2012) Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701CrossRefPubMedGoogle Scholar
  31. Matheny PB, Hibbett DS (2005) Assembling the fungal tree of life. NCBI GenBank. https://www.ncbi.nlm.nih.gov/genbank/. Accessed 4 June 2018
  32. Matheny PB, Bougher NL, Hibbett DS (2004) Assembling the fungal tree of life. NCBI GenBank. https://www.ncbi.nlm.nih.gov/genbank/. Accessed 4 June 2018
  33. Matheny PB, Curtis JM, Hibbett DS (2006a) Assembling the fungal tree of life. NCBI GenBank. https://www.ncbi.nlm.nih.gov/genbank/. Accessed 4 June 2018
  34. Matheny PB, Curtis JM, Hofstetter V, Aime MC, Moncalvo JM, Ge ZW, Slot JC, Ammirati JF, Baroni TJ, Bougher NL, Hughes KW, Lodge DJ, Kerrigan RW, Seidl MT, Aanen DK, DeNitis M, Daniele GM, Desjardin DE, Kropp BR, Norvell LL, Parker A, Vellinga EC, Vilgalys R, Hibbett DS (2006b) Major clades of Agaricales: a multilocus phylogenetic overview. Mycologia 98:982–995CrossRefPubMedGoogle Scholar
  35. Moncalvo JM, Lutzoni FM, Rehner SA, Johnson J, Vilgalys R (2000) Phylogenetic relationships of agaric fungi based on nuclear large subunit ribosomal DNA sequences. Syst Biol 49:278–305CrossRefPubMedGoogle Scholar
  36. Moncalvo JM, Vilgalys R, Redhead SA, Johnson JE, James TY, Aime MC, Hofstetter V, Verduin SJ, Larsson E, Baroni TJ, Thorn RG, Jacobsson S, Clémençon H, Miller OK Jr (2002) One hundred and seventeen clades of euagarics. Mol Phylogenet Evol 23:357–400CrossRefPubMedGoogle Scholar
  37. Nakasone KK, Hibbett DS, Goranova G (2009) Neocampanella, a new corticioid fungal genus, and a note on Dendrothele bispora. Botany 87:875–882CrossRefGoogle Scholar
  38. Pegler DN (1983) Agaric flora of the lesser Antilles. Kew Bull Add Ser 9:1–668Google Scholar
  39. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefPubMedPubMedCentralGoogle Scholar
  40. Roth AG (1791) Vegetabilia cryptogamica minus hucusque cognita. Ann Bot Usteri 1:5–12Google Scholar
  41. Sick H (1957) Roßhaarpilze als Nestbau-Material brasilianischer Vögel. J Ornithol 98:421–431CrossRefGoogle Scholar
  42. Singleton DR, Harper RG (1998) Bacteria in old house wren nests. J Field Ornithol 69:71–74Google Scholar
  43. Stalpers J, Redhead S, Rossman A, Cubeta M, Kirschner R, Lange G, Larsson K-H, Norvell L, Oberwinkler F, Rajchenberg M, Roberts P, Thorn RG, et al (in press) Recommendations of fungal genera competing for use: Agaricomycotina (Basidiomycota). IMA FungusGoogle Scholar
  44. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690CrossRefPubMedPubMedCentralGoogle Scholar
  45. Su HJ, Thseng FM, Chen JS, Ko W-H (2011) Production of volatile substances by rhizomorphs of Marasmius crinisequi and its significance in nature. Fungal Divers 49:199–202CrossRefGoogle Scholar
  46. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  47. Thompson W (1984) Distribution, development and functioning of mycelial cord systems of decomposer basidiomycetes of the deciduous woodland floor. In: Jennings DH, ADM R (eds) The Ecology and Physiology of the Fungal Mycelium. Cambridge University Press, Cambridge, pp 185–214Google Scholar
  48. Thompson W, Rayner ADM (1983) Extent, development and function of mycelial cord systems in soil. Trans Br Mycol Soc 81:333–345CrossRefGoogle Scholar
  49. Vinnere O, Fatehi J, Sivasithamparam K, Gerhardson B (2005) A new plant pathogenic sterile white basidiomycete from Australia. Eur J Plant Pathol 112:63–77CrossRefGoogle Scholar
  50. Wakefield EM (1934) Contributions to the flora of tropical America: XXI. Fungi collected in British Guiana, chiefly by the Oxford university expedition, 1929. Bull Misc Inform Kew 1934:238–258Google Scholar
  51. White TJ, Bruns T, Lee S, Taylor TW (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, London, pp 315–322Google Scholar
  52. Wood TM, Gallo F, Donahue PK (1992) Observations at a paradise tanager nest. Wilson Bull 104:360–362Google Scholar
  53. Wu SH, Wang DM, Tschen E (2007) Brunneocorticium pyriforme, a new corticioid fungal genus and species belonging to the euagarics clade. Mycologia 99:302–309CrossRefPubMedGoogle Scholar

Copyright information

© This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2018

Authors and Affiliations

  • Rachel A. Koch
    • 1
  • D. Jean Lodge
    • 2
    • 3
  • Susanne Sourell
    • 4
  • Karen Nakasone
    • 5
  • Austin G. McCoy
    • 1
    • 6
  • M. Catherine Aime
    • 1
  1. 1.Department of Botany and Plant PathologyPurdue UniversityWest LafayetteUSA
  2. 2.Center for Forest Mycology Research, USDA-Forest ServiceNorthern Research StationLuquilloUSA
  3. 3.Department of Plant Pathology and Odum School of EcologyUniversity of GeorgiaAthensUSA
  4. 4.The Cristalino Fungi ProjectFundação Ecológica CristalinoAlta FlorestaBrazil
  5. 5.Center for Forest Mycology Research, Northern Research StationUSDA-Forest ServiceMadisonUSA
  6. 6.Department of Plant, Soil and Microbial SciencesMichigan State UniversityEast LansingUSA

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