Skip to main content
Log in

Ramaria species in Nothofagus forests of Patagonia, with the description of two new species

  • Original Article
  • Published:
Mycological Progress Aims and scope Submit manuscript

Abstract

Within the wide diversity of fungal species of the Patagonian Andes forests, species of Ramaria sensu lato are some of the most attractive, due to their coral-like, medium size, and colorful basidiomata. The genus was recognized as paraphyletic and is currently divided into four subgenera: Ramaria, Laeticolora, Lentoramaria, and Echinoramaria. In Patagonia (Argentina and Chile), 18 species of Ramaria have been reported associated with Nothofagaceae; however, their diversity and phylogenetic relationships are largely unknown. This study presents a detailed account of Ramaria in Patagonia, based on an integrative analysis of phylogenetic, macro-, and micro-morphological features. Internal transcribed spacer (ITS) and nuclear 28S rDNA (LSU) genes were analyzed to identify specimens from Argentina and to examine their phylogenetic relationships with other Ramaria species. The phylogenetic analyses revealed six Ramaria species in Argentinian Patagonia: R. patagonica, R. botrytis, R. inedulis, R. paraconcolor, and two new phylogenetic groups that are proposed as new species: R. flavinedulis and R. dendrophora. Ramaria flavinedulis produces brightly colored yellow or yellow-orange basidiomata with a fused, twisted compound stipe, simple-septate basidia, and ellipsoid to cylindrical basidiospores. Ramaria dendrophora exhibits pale yellow to pale pink basidiomata and ornamented basidiospores with conspicuous and irregular warts. This study increased our knowledge of the phylogenetic diversity and taxonomy in Ramaria from the Patagonian Andes Forests compared with those found elsewhere.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article.

References

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19(6):716–723

    Article  Google Scholar 

  • Balasundaram SV, Engh IB, Skrede I, Kauserud H (2015) How many DNA markers are needed to reveal cryptic fungal species? Fungal Biol 119(10):940–945

    Article  CAS  PubMed  Google Scholar 

  • Barroetaveña C, & Toledo C V (2020) Diversity and ecology of edible mushrooms from Patagonia native forests, Argentina. Mushrooms, humans and nature in a changing world: Perspectives from ecological, agricultural and social sciences, pp 297–318

  • Barroetaveña C, Salomón MES, Bassani V (2019) Rescuing the ectomycorrhizal biodiversity associated with South American Nothofagaceae forest, from the 19th century naturalists up to molecular biogeography. J for Res 92(5):500–511. https://doi.org/10.1093/forestry/cpz047

    Article  Google Scholar 

  • Carlsen T, Engh IB, Decock C, Rajchenberg M, Kauserud H (2011) Multiple cryptic species with divergent substrate affinities in the Serpula himantioides species complex. Fungal Biol 115(1):54–61

    Article  CAS  PubMed  Google Scholar 

  • Coker WC (1923) The Clavarias of the United States and Canada. University North Carolina Press, Chapel Hill, N. C.

    Google Scholar 

  • Corner EJH (1950) A monograph of Clavaria and allied genera. Annals of Botany Memoirs. Oxford University Press, London

    Google Scholar 

  • Corner EJH (1957) Some Clavarias from Argentina. Darwiniana 11:193–206

    Google Scholar 

  • Corner EJH (1970) Supplement to “A Monograph of Clavaria and allied Genera”. Beih Nova Hedwing 33:1–299

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das K, Hembrom ME, Arun KD, Arvind P, Soumitra P, Acharya K (2016) Ramaria subalpina (Gomphaceae): a new edible fungus from India. Phytotaxa 246(2):137–144

    Article  Google Scholar 

  • Deschamps JR (2002) Hongos silvestres comestibles del Mercosur con valor gastronómico. Documentos de trabajo, Universidad de Belgrano. Retrieved April 26, 2023, from http://repositorio.ub.edu.ar/handle/123456789/433

  • Donoso Zegers C (2006) Las especies arbóreas de los bosques templados de Chile y Argentina: Autoecología. Marisa Cuneo ediciones

  • Doty MS (1944) Clavaria, the species known from Oregon and the Pacific Northwest. Oregon State College, Corvallis, p 91

    Google Scholar 

  • Doyle J (1991) DNA protocols for plants. In: Hewitt GM, Johnston AWB, Young JPW (eds) Molecular Techniques in Taxonomy. Nato ASI Series (Series H: Cell Biology), Berlin, vol 57. Springer, Heildelberg, pp 283–293

    Chapter  Google Scholar 

  • Dunk CW, Lebel T, Keane PJ (2012) Characterisation of ectomycorrhizal formation by the exotic fungus Amanita muscaria with Nothofagus cunninghamii in Victoria. Australia Mycorrhiza 22(2):135–147

    Article  PubMed  Google Scholar 

  • Dutta AK, Wilson AW, Antonín V, Acharya K (2015) Taxonomic and phylogenetic study on gymnopoid fungi from Eastern India. I. Mycol Prog 14(10):1–18

    Article  Google Scholar 

  • Exeter RL, Norvell L, & Cazares E (2006) Ramaria of the Pacific Northwestern United States. U. S Department of the Interior, Bureau of Land Management. https://agris.fao.org/agris-search/search.do?recordID=GB2021457125

  • Furci George-Nascimento GM (2007) Fungi Austral: Guía de campo de los hongos más vistosos de Chile. CORMA

  • 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  CAS  PubMed  Google Scholar 

  • Giachini AJ, Hosaka K, Nouhra E, Spatafora J, Trappe JM (2010) Phylogenetic relationships of the Gomphales based on nuc- 25S-rDNA, mit-12S-rDNA, and mit-atp6-DNA combined sequences. Fungal Biol 114:224–234. https://doi.org/10.1016/j.funbio.2010.01.00

    Article  CAS  PubMed  Google Scholar 

  • Giachini AJ (2004) Systematics of the Gomphales: the genus Gomphus Pers. sensu lato. PhD Dissertation, Oregon State University. file:///C:/Users/cbarroetavena/Downloads/Giachini_Admir_J_2004.pdf

  • Giles PV, Salgado Salomón ME, & Barroetaveña C (2021) ¿Está Amanita muscaria invadiendo los bosques de Nothofagus dombeyi en Patagonia, Argentina? XXXVIII Jornadas Argentina de Botánica.https://botanicaargentina.org.ar/wp-content/uploads/2021/07/Resu%CC%81menes-aceptados-para-publicar.pdf

  • Gomez JVL (2015) Caracterización de hongos comestibles del género Ramaria, asociados a bosques siempreverdes en el predio Llancahue, Región de Los Ríos. Degree Thesis, Universidad Austral de Chile. http://cybertesis.uach.cl/tesis/uach/2015/fifl435c/doc/fifl435c.pdf

  • González GC, Barroetaveña C, Visnovsky SB, Rajchenberg M, Pildain MB (2021) A new species, phylogeny, and a worldwide key of the edible wood decay Fistulina (Agaricales). Mycol Prog 20(5):733–746

    Article  Google Scholar 

  • Hanif M, Khalid AN, Exeter RL (2019) Ramaria flavescentoides sp. nov. with clamped basidia from Pakistan. Mycotaxon 134(2):399–406

    Article  Google Scholar 

  • Hosaka K, Bates ST, Beever RE, Castellano MA, Colgan III W, Dominguez LS, ..., Trappe JM (2006) Molecular phylogenetics of the gomphoid-phalloid fungi with an establishment of the new subclass Phallomycetidae and two new orders. Mycologia 98(6):949–959

  • Humpert AJ, Muench EL, Giachini AJ, Castellano MA, Spatafora JW (2001) Molecular phylogenetics of Ramaria and related genera: evidence from nuclear large subunit and mitochondrial small subunit rDNA sequences. Mycologia 93:465–477. https://doi.org/10.2307/3761733

    Article  CAS  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knudson AG (2012) The genus Ramaria in Minnesota. Msc Thesis, University of Minnesota. https://conservancy.umn.edu/bitstream/handle/11299/122161/Knudson_Alicia_February2012.pdf;jsessionid=E8F8F8C4A049862EE070EED63D2601FF?sequence=1

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lazo W (2001) Hongos de Chile. Atlas Micológico. Universidad de Chile, Facultad de Ciencias

  • Marr CD, Stuntz DE (1973) Ramaria of Western Washingtin. Bibliotheca Mycologica 38:1–232

    Google Scholar 

  • Martin MP, Daniels PP, Erickson D, Spouge JL (2020) Figures of merit and statistics for detecting faulty species identification with DNA barcodes: a case study in Ramaria and related fungal genera. PLoS ONE 15(8):e0237507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Molares S, Toledo CV, Stecher G, Barroetaveña C (2020) Traditional mycological knowledge and processes of change in Mapuche communities from Patagonia, Argentina: a study on wild edible fungi in Nothofagaceae forests. Mycologia 112(1):9–23

    Article  PubMed  Google Scholar 

  • Nouhra ER, Horton TR, Cazares E, Castellano M (2005) Morphological and molecular characterization of selected Ramaria mycorrhizae. Mycorrhiza 15(1):55–59

    Article  CAS  PubMed  Google Scholar 

  • Petersen RH (1988) Contribution toward a monograph of Ramaria VII. New Taxa and Miscellany. Mycologia 80(2):223–234

    Article  Google Scholar 

  • Petersen RH, Hughes K, Justice J (2014) Two new species of Ramaria from Arkansas. MycoKeys 8:17–29

    Article  Google Scholar 

  • Petersen RH (1981) Ramaria Subgenus Echinoramaria. Bibliotheca Mycologica 79:1–261

    Google Scholar 

  • Peterson KR, Pfister DH (2010) Phylogeny of Cyttaria inferred from nuclear and mitochondrial sequence and morphological data. Mycologia 102(6):1398–1416

    Article  PubMed  Google Scholar 

  • Pildain MB, Rajchenberg M (2013) The phylogenetic position of Postia sl (Polyporales, Basidiomycota) from Patagonia. Argentina Mycologia 105(2):357–367

    Article  CAS  PubMed  Google Scholar 

  • Pildain MB, Coetzee MPA, Rajchenberg M, Petersen RH, Wingfield MJ, Wingfield BD (2009) Molecular phylogeny of Armillaria from the Patagonian Andes. Mycol Prog 8(3):181–194

    Article  Google Scholar 

  • Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, 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 

  • Rugolo M, Barroetaveña C, Barrett MD, Mata G, Hood IA, Rajchenberg M, Pildain MB (2023) Phylogenetic relationships and taxonomy of Grifola (Polyporales). Mycol Prog 22(1):7. https://doi.org/10.1007/s11557-022-01857-2

    Article  Google Scholar 

  • Rugolo M, Mascoloti Spréa R, Dias MI, Pires TC, Añibarro-Ortega M, Barroetaveña C, ... Barros L (2022) Nutritional composition and bioactive properties of wild edible mushrooms from native Nothofagus Patagonian forests. Foods 11(21) 3516. 10.3390/foods11213516

  • Scattolin L, Di Marino E, Bodensteiner P, Agerer R (2008) Sistotrema is a genus with ectomycorrhizal species confirmation of what sequence studies already suggested. Mycol Prog 7(3):169–176

    Article  Google Scholar 

  • Singer R (1969) Mycoflora autralis. Beihefte Nova Hedwigia 29. Cramer, Lehre, Germany

  • Spegazzini CL (1887) Fungi Patagonici. Boletín De La Academia Nacional De Ciencias En Córdoba 11:5–64

    Google Scholar 

  • Spegazzini CL (1921) Mycetes chilenses. Boletín De La Academia Nacional De Ciencias En Córdoba 25:1–124

    Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steenkamp ET, Wingfield BD, Desjardins AE, Marasas WF, Wingfield MJ (2002) Cryptic speciation in Fusarium subglutinans. Mycologia 94(6):1032–1043

    Article  CAS  PubMed  Google Scholar 

  • Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijesundera R, ... Abarenkov K (2014) Global diversity and geography of soil fungi. Science, 346 1256688. https://doi.org/10.1126/science.1256688

  • Tedersoo L, Smith ME (2013) Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biol Rev 27(3–4):83–99

    Article  Google Scholar 

  • Toledo CV, Barroetaveña C, Rajchenberg M (2014) Fenología y variables ambientales asociadas a la fructificación de hongos silvestres comestibles de los bosques andino-patagónicos en Argentina. Revista Mexicana De Biodiversidad 85(4):1093–1103

    Article  Google Scholar 

  • Toledo CV, Barroetaveña C, Fernandes Â, Barros L, Ferreira IC (2016) Chemical and antioxidant properties of wild edible mushrooms from native Nothofagus spp. forest, Argentina. Molecules 21(9):1201

    Article  PubMed  PubMed Central  Google Scholar 

  • Trappe JM (1962) Fungus associates of ectotrophic mycorrhizae. Bot Rev 28(4):538–606

    Article  Google Scholar 

  • Valenzuela E (2003) Hongos comestibles silvestres colectados en la X región de Chile. Boletín Micológico 18. https://doi.org/10.22370/bolmicol.2003.18.0.374

  • Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Authors thank Dr. Kerry Everett from The New Zealand Institute for Plant and Food Research Limited for her valuable feedback on the manuscript. We express our gratitude to BAFC and LPS herbaria and their curators for the loan of specimens. Field assistance to the first author rendered by Maximiliano Rugolo and Masera Pablo is duly acknowledged. This study is part of the Patagonia Fungi trails and tastes project.

Funding

The research is supported by the COFECyT, P-BIO R 2016 (to BC and MBP), PICT 2018–3234 (to MBP), and PIP 11220200101167CO01 (to MBP).

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: Gabriela González, Carolina Barroetaveña, and Maria Belén Pildain; methodology: Gabriela González, Carolina Barroetaveña, and Maria Belén Pildain; formal analysis and investigation: Gabriela González; writing—original draft preparation: Gabriela González; writing—review and editing: Carolina Barroetaveña, Mario Rajchenberg, and Maria Belén Pildain; funding acquisition: Carolina Barroetaveña and Maria Belén Pildain; resources: Carolina Barroetaveña, Sandra B. Visnovsky, and Maria Belén Pildain; supervision: Carolina Barroetaveña, Mario Rajchenberg, and Maria Belén Pildain.

Corresponding author

Correspondence to Carolina Barroetaveña.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Section Editor: Zhu-Liang Yang

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

González, G.C., Barroetaveña, C., Visnovsky, S.B. et al. Ramaria species in Nothofagus forests of Patagonia, with the description of two new species. Mycol Progress 22, 60 (2023). https://doi.org/10.1007/s11557-023-01905-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11557-023-01905-5

Keywords

Navigation