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

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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.

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References

  • 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 97:1012–1022

    PubMed  CAS  Google Scholar 

  • Antonín V (2007) Fungus Flora of tropical Africa, Volume 1: Monograph of Marasmius, Gloiocephala, Palaeocephala and Setulipes in Tropical Africa. National Botanic Garden, Belgium

    Google Scholar 

  • Aubrecht G, Huber W, Weissenhofer A (2013) Coincidence or benefit? The use of Marasmius (horse-hair fungus) filaments in bird nests. Avian Biol Res 6:26–30

    Article  Google Scholar 

  • Berkeley MJ (1856) Decades of fungi. Decades LXI–LXII. Rio Negro fungi. Hooker’s J Bot Kew Gard Misc 8:272–280

    Google Scholar 

  • Berlese AN (1892) Rapporti tra Dematophora e Rosellinia. Riv Patol Veg 1:5–17

    Google Scholar 

  • Boddy L (1993) Saprotrophic cord-forming fungi: warfare strategies and other ecological aspects. Mycol Res 97:641–655

    Article  Google Scholar 

  • Boidin J, Lanquetin P, Duhem B (1996) Contribution à la connaissance du genre Dendrothele (Basidiomycotina, Aphyllophorales). Bull Trimest Soc Mycol Fr 112:87–126

    Google Scholar 

  • Bonito G, May TW (2014) Barcoding of Australian fungi. NCBI GenBank. https://www.ncbi.nlm.nih.gov/genbank/. Accessed 4 June 2018

  • Burdsall HH Jr, Nakasone KK (1983) Species of effused Aphyllophorales (Basidiomycotina) from the southeastern United States. Mycotaxon 17:253–268

    Google Scholar 

  • Burt EA (1918) Corticiums causing Pellicularia disease of the coffee plant, hypochnose of pomaceous fruits, and Rhizoctonia disease. Ann Mo Bot Gard 5:119–132

    Article  Google Scholar 

  • Cairney JWG (1991a) Rhizomorphs: organs of exploration or exploitation? Mycologist 5:5–10

    Article  Google Scholar 

  • Cairney JWG (1991b) Rhizomorph structure and development in Marasmius crinisequi. Mycol Res 95:1429–1432

    Article  Google Scholar 

  • 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 35:480–497

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 117:11–32

    Article  Google Scholar 

  • Donk MA (1962) The generic names proposed for Agaricaceae. Beih Nova Hedwigia 5:1–320

    Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Freymann BP (2008) Physical properties of fungal rhizomorphs of marasmioid basidiomycetes used as nesting material by birds. Ibis 150:395–399

    Article  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  PubMed  CAS  Google Scholar 

  • Golley FB (1983) Decomposition. In: Golley FB (ed) Tropical Rain Forest Ecosystems. Structure and Function. Elsevier Scientific Publishing Company, Amsterdam, pp 157–166

    Google Scholar 

  • 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 120:603–619

    Article  PubMed  PubMed Central  Google Scholar 

  • Granlund HI, Jennings DH, Thompson W (1985) Translocation of solutes along rhizomorphs of Armillaria mellea. Trans Br Mycol Soc 84:111–119

    Article  Google Scholar 

  • Hedger J (1990) Fungi in the tropical forest canopy. Mycologist 4:200–202

    Article  Google Scholar 

  • 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 15–36

    Google Scholar 

  • Henkel TW (2003) Monodominance in the ectomycorrhizal Dicymbe corymbosa (Caesalpiniaceae) from Guyana. J Trop Ecol 19:417–437

    Article  Google Scholar 

  • 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 21:2195–2220

    Article  Google Scholar 

  • Hennings P (1904) Fungi Amazonici a cl. Ernesto Ule collecti III Hedwigia 43:351–400

    Google Scholar 

  • Hu CC (1984) Horse-hair blight, new disease of tea bush caused by Marasmius equicrinis Mull in Taiwan. Taiwan Tea Res Bull 3:1–4

    CAS  Google Scholar 

  • 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 12:599–606

    Article  Google Scholar 

  • 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 17:33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lanfear R, Calcott B, Ho SY, Guindon S (2012) Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701

    Article  PubMed  CAS  Google Scholar 

  • Matheny PB, Hibbett DS (2005) Assembling the fungal tree of life. NCBI GenBank. https://www.ncbi.nlm.nih.gov/genbank/. Accessed 4 June 2018

  • 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

  • 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

  • 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 98:982–995

    Article  PubMed  Google Scholar 

  • 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 49:278–305

    Article  PubMed  CAS  Google Scholar 

  • 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 23:357–400

    Article  PubMed  CAS  Google Scholar 

  • Nakasone KK, Hibbett DS, Goranova G (2009) Neocampanella, a new corticioid fungal genus, and a note on Dendrothele bispora. Botany 87:875–882

    Article  Google Scholar 

  • Pegler DN (1983) Agaric flora of the lesser Antilles. Kew Bull Add Ser 9:1–668

    Google Scholar 

  • 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 61:539–542

    Article  PubMed  PubMed Central  Google Scholar 

  • Roth AG (1791) Vegetabilia cryptogamica minus hucusque cognita. Ann Bot Usteri 1:5–12

    Google Scholar 

  • Sick H (1957) Roßhaarpilze als Nestbau-Material brasilianischer Vögel. J Ornithol 98:421–431

    Article  Google Scholar 

  • Singleton DR, Harper RG (1998) Bacteria in old house wren nests. J Field Ornithol 69:71–74

    Google Scholar 

  • 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 Fungus

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  PubMed  CAS  Google Scholar 

  • 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 49:199–202

    Article  Google Scholar 

  • 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 28:2731–2739

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 185–214

    Google Scholar 

  • Thompson W, Rayner ADM (1983) Extent, development and function of mycelial cord systems in soil. Trans Br Mycol Soc 81:333–345

    Article  Google Scholar 

  • Vinnere O, Fatehi J, Sivasithamparam K, Gerhardson B (2005) A new plant pathogenic sterile white basidiomycete from Australia. Eur J Plant Pathol 112:63–77

    Article  Google Scholar 

  • 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 1934:238–258

    Google Scholar 

  • 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 315–322

    Google Scholar 

  • Wood TM, Gallo F, Donahue PK (1992) Observations at a paradise tanager nest. Wilson Bull 104:360–362

    Google Scholar 

  • Wu SH, Wang DM, Tschen E (2007) Brunneocorticium pyriforme, a new corticioid fungal genus and species belonging to the euagarics clade. Mycologia 99:302–309

    Article  PubMed  Google Scholar 

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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.

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  1. Austin G. McCoy

    Present address: Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI, USA

Authors and Affiliations

  1. Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, USA

    Rachel A. Koch, Austin G. McCoy & M. Catherine Aime

  2. Center for Forest Mycology Research, USDA-Forest Service, Northern Research Station, Luquillo, PR, USA

    D. Jean Lodge

  3. Department of Plant Pathology and Odum School of Ecology, University of Georgia, Athens, GA, USA

    D. Jean Lodge

  4. The Cristalino Fungi Project, Fundação Ecológica Cristalino, Alta Floresta, MT, Brazil

    Susanne Sourell

  5. Center for Forest Mycology Research, Northern Research Station, USDA-Forest Service, Madison, WI, USA

    Karen Nakasone

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  1. Rachel A. Koch
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Correspondence to M. Catherine Aime.

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Koch, R.A., Jean Lodge, D., Sourell, S. et al. Tying up loose threads: revised taxonomy and phylogeny of an avian-dispersed Neotropical rhizomorph-forming fungus. Mycol Progress 17, 989–998 (2018). https://doi.org/10.1007/s11557-018-1411-8

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