Skip to main content
SpringerLink
Log in

Phylogenetic relationships and taxonomy of Grifola (Polyporales)

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

Abstract

Grifola is a genus of poroid wood–rotting fungi that produces compound, multipileate basidiomes that are edible. We analyzed the phylogenetic and taxonomic diversity of Grifola on the basis of phylogenetic analysis of internal transcripter space (ITS) and β–tubulin (TUBB) DNA sequences, comparison of morphological features and host relationships. Results revealed a Northern Hemisphere (NH) and a Southern Hemisphere (SH) group of species. The NH clade is represented by G. frondosa (growing on Fagaceae and Betulaceae). The SH clade is represented by 4 taxa: G. gargal (growing on Lophozonia alpina and L. obliqua, Nothofagacea, in southern South America) is sister to a new taxon G. odorata (New Zealand, growing on Fuscospora spp., Nothofagaceae, and Metrosideros, Myrtaceae), and both are characterized by a strong almond smell, while G. sordulenta (southern south America, growing on Nothofagus dombeyi, Nothofagaceae), is sister to G. colensoi (New Zealand and Australia, growing on Fuscospora spp., Nothofagaceae and Eucalyptus spp., Myrtaceae). Results showed a complex evolutionary history of species evolving from Gondwanan ancestors and, in southern South America, Nothofagaceae was selected as principal host.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

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 Automat Contr 19:716–723

    Article  Google Scholar 

  • Baeza RVM (1930) Los nombres vulgares de las plantas silvestres de Chile y su concordancia con los nombres científicos. Imprenta El Globo, Santiago, Chile

    Google Scholar 

  • Barroetaveña C, Toledo CV (2020) Diversity and ecology of edible mushrooms from Patagonia native forests, Argentina. In: Perez Moreno J, Guerin Laguette A, Flores Arzú R (eds) Mushrooms, humans and nature in a changing world. Springer, The Netherlands, pp 297–320. https://doi.org/10.1007/978-3-030-37378-8_11

  • Bernicchia A, Gorjón SP (2020) Polypores of the Mediterranean region. Romar, Milano, Italy, p 904

  • Bradford JC (1998) A cladistic analysis of species groups in Weinmannia (Cunoniaceae) based on morphology and inflorescence architecture. Ann Missouri Bot Gard 85(4):565–593

    Article  Google Scholar 

  • Brujin J, Loyola C, Aqueveque P, Cañumir J, Cortéz M, France A (2009) Antioxidant properties of extracts obtained from Grifola gargal mushrooms. Micol Aplicada Int 21:11–18

    Google Scholar 

  • Buchanan PK, Ryvarden L (2000) An annotated checklist of polypore and polypore-like fungi recorded from New Zealand. New Zealand J Bot 38(2):265–323

    Article  Google Scholar 

  • Carpenter RJ, Buchanan AM (1993) Oligocene leaves, fruits and flowers of the Cunoniaceae from Cethana, Tasmania. Austral Syst Bot 6:91–109

    Article  Google Scholar 

  • Corner EJH (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, Stecchericium, Trechispora, Truncospora and Tyromyces. Beih Nova Hedwigia 96:1–218

    Google Scholar 

  • Cunningham GH (1948) New Zealand Polyporaceae. 3. The genus Polyporus. New Zealand Department of Scientific and Industrial Research, Plant Diseases Division. Bulletin. 74

  • Cunningham GH (1965) Polyporaceae of New Zealand. New Zealand Depart Sci Indust Rese Bull 164:1–304

    Google Scholar 

  • Dai YC (2012) Polypore diversity in China with an annotated checklist of Chinese polypores. Mycoscience 53:49–80

    Article  Google Scholar 

  • Espinosa M (1934) Hongos Chilenos. Rev Chil Hist Nat 38:94–103

    Google Scholar 

  • Floudas D (2021) Evolution of lignin decomposition systems in fungi. In: Morel-Rouhier M, Sormani R (eds.) Wood Degradation and Ligninolytic Fungi. Adv Botan Res, Academic Press 99:37–76. https://doi.org/10.1016/bs.abr.2021.05.003

    Article  CAS  Google Scholar 

  • Gargano ML, Zervakis GI, Isikhuemen OS, Venturella G, Calvo R, Giammanco A, Fasciana T, Ferraro V (2020) Ecology, phylogeny, and potential nutritional and medicinal value of a rare white “Maitake” collected in a Mediterranean forest. Diversity 12:230. https://doi.org/10.3390/d12060230

    Article  Google Scholar 

  • Gilbertson RL, Ryvarden L (1986) North American Polypores vol. I. Fungiflora, Oslo

    Google Scholar 

  • Gómez-Montoya N, Rajchenberg M, Robledo GL (2018) Aegis boa (Polyporales, Basidiomycota) a new neotropical genus and species based on morphological data and phylogenetic evidences. Mycosphere 8(6):1261–1269. https://doi.org/10.5943/mycosphere/8/6/11

    Article  Google Scholar 

  • González G, Barroetaveña C, Visnovsky S, Rajchenberg M, Pildain B (2021) A new species, phylogeny, and a worldwide key of the edible wood decay Fistulina (Agaricales). Mycol Prog 20(5):733–746. https://doi.org/10.1007/s11557-021-01696-7

    Article  Google Scholar 

  • Gray SF (1821) A natural arrangement of British plants according to their relations to each other as pointed out by Jussieu, De Candolle, Brown, &c. Printed for Baldwin, Cradock and Joy, London, p 824

  • Guevara T (1908) Psicolojia del pueblo araucano. Imprenta Cervantes, Santiago de Chile, Chile, p 412

  • Gusinde M (1917) Medicina e higiene entre los antiguos Araucanos. Publicaciones del Museo de Etnología y Antropología de Chile 1:177–294

    Google Scholar 

  • Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harada E, Kawade M, Matsuda Y, Meguro S (2010) Morphological and molecular characterization of Grifola gargal, an edible mushroom from Chile. Nippon Kingakukai Kaiho 51:71–76

    Google Scholar 

  • Harada E, D'Alessandro-Gabazza CN, Toda M, Morizono T, Chelakkot-Govindalayathil AL, Roeen Z, Urawa M, Yasuma T, Yano Y, Sumiya T, Gabazza EC (2015) Amelioration of atherosclerosis by the new medicinal mushroom Grifola gargal Singer. J Med Food 18(8):872–881. https://doi.org/10.1089/jmf.2014.3315

    Article  Google Scholar 

  • Hattori T (2003) Type studies of the polypores described by E.J.H. Corner from Asia and West Pacific Areas. V. Species described in Tyromyces (2), Mycoscience 44 (4):265–276. https://doi.org/10.1007/s10267-003-0114-3.

  • Haumman L (1947) La vegetación de la Argentina. Geografía de la República Argentina (ed. by Sociedad Argentina de Estudios Geográficos GAEA), pp. 5–346. Casa Coni, Buenos Aires.

  • Hibbett DS, Donoghue MJ (2001) Analysis of character correlations among wood decay mechanisms, mating systems and substrate ranges in Homobasidiomycetes. Syst Biol 50:215–242

    Article  CAS  Google Scholar 

  • Hood I (1992) An illustrated guide to Fungi on wood in New Zealand. Auckland University Press, New Zealand

    Google Scholar 

  • Imtiaj A, Lee TS, Ohga S (2011) Sequence variation of Pleurotus species collected from Eastern Asia. Micol Aplicada Int 23:1–10

    Google Scholar 

  • Jansen GM, Schalkwijk J (1979) A survey of the mycoflora and its relation to the phanerogamic flora in the South-Chilean laurel forest. Rijksherbarium Leiden, Department of Botany, Division of Geobotany Nijmegen, The Netherlands, p 267

  • Justo A, Hibbett DS (2011) Phylogenetic classification of Trametes (Basidiomycota, Polyporales) based on a five-marker dataset. Taxon 60:1567–1583. https://doi.org/10.1002/tax.606003

    Article  Google Scholar 

  • Justo A, Miettinen O, Floudas D, Ortiz-Santana B, Sjökvist E, Lindner D, Nakasone K, Niemelä T, Larsson KH, Ryvarden L, Hibbett DS (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

    Article  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  Google Scholar 

  • Krah FS, Bässler C, Heibl C, Soghigian J, Schaefer H, Hibbett DS (2018) Evolutionary dynamics of host specialization in wood-decay fungi. BMC Evol Biol 18(1). https://doi.org/10.1186/s12862-018-1229-7

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  Google Scholar 

  • Ladiges PY (1997) Phylogenetic history and classification of eucalypts. In: Williams JE, Woinarski JCZ (eds) Eucalypt ecology: individuals to ecosystems. Cambridge University Press, Cambridge, pp 16–29

    Google Scholar 

  • Loizides M, Bellanger JM, Clowez P, Richard F, Moreau PA (2016) Combined phylogenetic and morphological studies of true morels (Pezizales, Ascomycota) in Cyprus reveal significant diversity, including Morchella arbutiphila and M. disparilis spp. nov. Mycol Prog 15(4):39. https://doi.org/10.1007/s11557-016-1180-1.

  • Manos PS, Steele KP (1997) Phylogenetic analyses of “Higher” Hamamelididae based on plastid sequence data. Am J Bot 84(10):1407–1419

    Article  CAS  Google Scholar 

  • McKenzie HC, Buchanan PK, Johnston PR (2000) Checklist of fungi on Nothofagus species in New Zealand. New Zealand J Bot 38:4,635–4,720. https://doi.org/10.1080/0028825X.2000.9512711

    Article  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 112:9–23. https://doi.org/10.1080/00275514.2019.1680219

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  Google Scholar 

  • Nobles MK (1965) Identification of cultures of wood-inhabiting Hymenomycetes. Can J Bot 43:1097–1139. https://doi.org/10.1139/b65-126

    Article  Google Scholar 

  • Peterson KR, Pfister DH (2010) Phylogeny of Cyttaria inferred from nuclear and mitochondrial sequence and morphological data. Mycologia 102(6):1398–1416. https://doi.org/10.3852/10-046

    Article  Google Scholar 

  • Pilát A (1936) Polyporaceae. In: Kavina C, Pilát A (Eds.) Atlas de Champignons d’Europe vol. III. Chez Les éditeurs, Prague, Czech Republic

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

    Article  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  Google Scholar 

  • Postemsky P, Curvetto N (2014) Enhancement of wheat grain antioxidant activity by solid state fermentation with Grifola spp. J Med Food 17:543–549. https://doi.org/10.1089/jmf.2013.0108

    Article  CAS  Google Scholar 

  • Postemsky P (2015) Grifola gargal and G. sordulenta, two wild edible mushrooms with perspectives as biotech products. Omics International, Fermentol Techno 4(2):1–2. https://doi.org/10.4172/2167-7972.1000124

  • Pozzi C, Lorenzo L, Rajchenberg M (2009) Un hospedaje exótico del hongo comestible Grifola gargal (Basidiomycota, Fungi). Bol Soc Argent Bot 44(1–2):9–10

    Google Scholar 

  • Rajchenberg M (2002) The genus Grifola (Aphyllophorales, Basidiomycota) in Argentina revisited. Bol Soc Argent Bot 37(1–2):19–27

    Google Scholar 

  • Rajchenberg M (2006) Los Políporos (Basidiomycetes) de los Bosques Andino Patagónicos de Argentina. Polypores (Basidiomycetes) from the Patagonian Andes Forests of Argentina. Bibliotheca Mycologica, Band 201, J. Cramer, Stuttgart, p 300

  • Rajchenberg M, Pildain MB, Madriaga DC, de Errasti A, Riquelme C, Becerra J (2019) New Poroid Hymenochaetaceae (Basidiomycota, Hymenochaetales) from Chile. Mycol Prog 18:865–877. https://doi.org/10.1007/s11557-019-01495-1

    Article  Google Scholar 

  • Raven PH, Axelrod DI (1972) Plate tectonics and Australasian paleobiogeography: the complex biogeographic relations of the region reflect its geologic history. Science 176(4042):1379–1386. https://doi.org/10.1126/science.176.4042.1379

    Article  CAS  Google Scholar 

  • Riquelme C, Rajchenberg M (2021) Aphyllophoroid fungi (Basidiomycota) of Chile: an annotated checklist. Mycotaxon 136:3. https://doi.org/10.5248/136.691

    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  Google Scholar 

  • Rugolo M, Spréa RM, Dias MI, Pires TCSP, Añibarro-Ortega M, Barroetaveña C, Caleja C, Barros L (2022) Nutritional composition and bioactive properties of wild edible mushrooms from native Nothofagus Patagonian forests. Foods 11:3516. https://doi.org/10.3390/foods11213516

    Article  CAS  Google Scholar 

  • Ryvarden L (2004) Studies in neotropical polypores 20. Some new polypores from the Amazonas region. Synopsis Fungorum 18:62–67

    Google Scholar 

  • Ryvarden L, Melo I (2014) Poroid fungi of Europe. Synopsis Fungorum 31:1–455

    Google Scholar 

  • Sanmartin I, Ronquist F (2004) Southern Hemisphere biogeography inferred by event-based models: Plant versus animal patterns. Syst Biol 53(2):216–243. https://doi.org/10.1080/10635150490423430

    Article  Google Scholar 

  • Schemeda-Hirschmann G, Razmilic I, Gutierrez MI, Loyola JI (1999) Proximate composition and biological activity of food plants gathered by Chilean Amerindians. Econ Bot 53:177–187

    Article  Google Scholar 

  • Shen Q, Geiser DM, Royse DJ (2002) Molecular phylogenetic analysis of Grifola frondosa (maitake) reveals a species partition separating eastern North American and Asian isolates. Mycologia 94(3):472–482. https://doi.org/10.1080/15572536.2003.11833

    Article  CAS  Google Scholar 

  • Singer R (1969) Mycoflora Australis. Beih Nova Hedwigia 29:1–405

    Google Scholar 

  • Smith AG, Briden JC (1977) Palaeocontinental maps for the Mesozoic and Cenozoic 63. Cambridge University Press, Cambridge

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tacón Clavaín A, Palma Martínez J, Fernández U, Ortega F (2006) El mercado de los PFNM y la conservación de los bosques del sur de Chile y Argentina. WWF, Red de Productos Forestales No Madereros de Chile, Valdivia, Chile, p 98

  • The Global Fungal Red List Initiative (2019) [cited 2022]. Available from: http://iucn.ekoo.se/iucn/species_view/331520/

  • Thiers B (2016) [cited 2022 Aug] Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available from: http://sweetgum.nybg.org/science/ih/

  • Toledo CV, Barroetaveña C, Fernandes A, Barros L, Ferreira ICFR (2016a) Chemical and antioxidant properties of wild edible mushrooms from native Nothofagus spp. forest, Argentina. Molecules 21(9):1201. https://doi.org/10.3390/molecules21091201

  • Toledo CV, Barroetaveña C, Rajchenberg M (2016b) Hongos comestibles silvestres de la región Andino Patagónica de la Argentina. Centro Forestal CIEFAP, Esquel, Argentina, pp 1–71

    Google Scholar 

  • Toledo CV, Barroetaveña C (2017) Crecimiento miceliar de especies silvestres de hongos comestibles de los bosques andino-patagónicos: primeros pasos para su domesticación. Bol Soc Argent Bot 52(3):435–446

    Article  Google Scholar 

  • Troung C, Sanchez-Ramirez S, Kuhar F, Kaplan Z, Smith ME (2017) The Gondwanan connection – Southern temperate Amanita lineages and the description of the first sequestrate species from the Americas. Fungal Biol 121(8). https://doi.org/10.1016/j.funbio.2017.04.006

  • Vento B, Agraín FA (2018) Phylogenetic relationships and time-calibration of the South American fossil and extant species of southern beeches (Nothofagus). Acta Palaeontol Pol 63:815–825. https://doi.org/10.4202/app.00493.2018

    Article  Google Scholar 

  • White TJ, Bruns TD, Lee SB, Taylor JW (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, pp 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1

  • Wright SD, Liddell LG, Lacap-Bugler DC, Gillman LN (2021) Metrosideros (Myrtaceae) in Oceania: origin, evolution and dispersal. Austral Ecol. https://doi.org/10.1111/aec.13053

  • Wu F, Zhou LW, Yang ZL, Bau T, Li TH, Dai YC (2019) Resource diversity of Chinese macrofungi: edible, medicinal and poisonous species. Fungal Divers 98:1–76

    Article  CAS  Google Scholar 

  • Wu JY, Siu KC, Geng P (2021) Bioactive ingredients and medicinal values of Grifola frondosa (Maitake). Foods 10(1). https://doi.org/10.3390/foods10010095

  • Zhao JD, Zhang X (1992) The polypores of China. Bibliotheca Mycologica, Band 145, J. Cramer, Stuttgart, p 524

Download references

Acknowledgements

Authors thank Dr Peter Buchanan (Landcare Research, Auckland, New Zealand) and Dr Genevieve Gates (Tasmanian Institute of Agriculture, Hobart, Australia) for their valuable feedback and assistance; Dr. Ian Dickie (University of Canterbury, New Zealand); Viviana Salazar Vidal, Matthias Theiss and Michael Pilkington kindly permitted to use their photographs. We express our gratitude to A. de Errasti, G. González and P. Masera for technical and field help. Staff of the Australian Tropical Herbarium and the National Herbarium of Victoria are thanked for their assistance with specimen loans. The funding assistance by the National Research Council of Argentina (CONICET; PIP 11220200101167CO01) and Ministry of Science, Technology and Productive Innovation (PICT 2018-3234) is acknowledged; the National Parks Administration (APN, Argentina) provided authorization for collecting specimens (project No. 1630). The Ministry of Foreign Affairs of Mexico supported this study through the Program for Research Stays.

Funding

The research is supported by the CONICET; PIP 11220200101167CO01 and MINCyT, PICT 2018-3234.

Author information

Authors and Affiliations

  1. Centro de Investigación y Extensión Forestal Andino Patagónico (CIEFAP), Fitopatología y Microbiología Aplicada, Argentina and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Ruta 259 km 16.5, 9200, Esquel, Chubut, Argentina

    Maximiliano Rugolo, Carolina Barroetaveña, Mario Rajchenberg & María B. Pildain

  2. Universidad Nacional de la Patagonia S.J. Bosco, Sarmiento 849, 9200, Esquel, Chubut, Argentina

    Carolina Barroetaveña, Mario Rajchenberg & María B. Pildain

  3. Australian Tropical Herbarium, James Cook University, Sir Robert Norman Building, PO Box 6811, Cairns, Australia

    Matt D. Barrett

  4. Instituto de Ecología, A.C., Carretera Antigua a Coatepec 351, El Haya CP 91073, Xalapa, Veracruz, México

    Gerardo Mata

  5. SCION New Zealand, Forest Protection, Tītokorangi Drive, Rotorua, New Zealand

    Ian A. Hood

Authors
  1. Maximiliano Rugolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carolina Barroetaveña
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matt D. Barrett
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gerardo Mata
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ian A. Hood
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mario Rajchenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. María B. Pildain
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: Maximiliano Rugolo, Carolina Barroetaveña, Maria Belén Pildain; Methodology: Maximiliano Rugolo, Carolina Barroetaveña, Matt Barrett, Ian Hood, Maria Belén Pildain; formal analysis and investigation: Maximiliano Rugolo, Matt Barrett, Ian Hood, Mario Rajchenberg; writing — original draft preparation: Maximiliano Rugolo; writing — review and editing: Carolina Barroetaveña, Matt Barrett, Gerardo Mata, Mario Rajchenberg, Maria Belén Pildain; funding acquisition: Carolina Barroetaveña, Gerardo Mata, Maria Belén Pildain; resources: Carolina Barroetaveña, Matt Barrett, Gerardo Mata, Maria Belén Pildain; supervision: Carolina Barroetaveña, Mario Rajchenberg, Maria Belén Pildain.

Corresponding author

Correspondence to María B. Pildain.

Ethics declarations

Ethics approval

Not applicable

Consent to participate

Not applicable

Consent for publication

Not applicable

Competing interests

The authors declare no competing interests.

Additional information

Section Editor: Yu-Cheng Dai

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

Rugolo, M., Barroetaveña, C., Barrett, M.D. et al. Phylogenetic relationships and taxonomy of Grifola (Polyporales). Mycol Progress 22, 7 (2023). https://doi.org/10.1007/s11557-022-01857-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11557-022-01857-2

Keywords

Search

Navigation