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Plunging hands into the mushroom jar: a phylogenetic framework for Lyophyllaceae (Agaricales, Basidiomycota)

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Abstract

During the last two decades, the unprecedented development of molecular phylogenetic tools has propelled an opportunity to revisit the fungal kingdom under an evolutionary perspective. Mycology has been profoundly changed but a sustained effort to elucidate large sections of the astonishing fungal diversity is still needed. Here we fill this gap in the case of Lyophyllaceae, a species-rich and ecologically diversified family of mushrooms. Assembly and genealogical concordance multigene phylogenetic analysis of a large dataset that includes original, vouchered material from expert field mycologists reveal the phylogenetic topology of the family, from higher (generic) to lower (species) levels. A comparative analysis of the most widely used phylogenetic markers in Fungi indicates that the nuc rDNA region encompassing the internal transcribed spacers 1 and 2, along with the 5.8S rDNA (ITS) and portions of the genes for RNA polymerase II second largest subunit (RPB2) is the most performing combination to resolve the broadest range of taxa within Lyophyllaceae. Eleven distinct evolutionary lineages are identified, that display partial overlap with traditional genera as well as with the phylogenetic framework previously proposed for the family. Eighty phylogenetic species are delineated, which shed light on a large number of morphological concepts, including rare and poorly documented ones. Probing these novel phylogenetic species to the barcoding method of species limit delineation, indicates that the latter method fully resolves Lyophyllaceae species, except in one clade. This case study provides the first comprehensive phylogenetic overview of Lyophyllaceae, a necessary step towards a taxonomical, ecological and nomenclatural revision of this family of mushrooms. It also proposes a set of methodological guidelines that may be of relevance for future taxonomic works in other groups of Fungi.

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References

  • Abarenkov K, Henrik Nilsson R, Larsson KH, Alexander IJ, Eberhardt U, Erland S et al (2010) The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol 186(2):281–285

    Article  PubMed  Google Scholar 

  • Alvarado P, Moreno G, Vizzini A, Consiglio G, Manjón JL, Setti L (2014) Atractosporocybe, Leucocybe and Rhizocybe: three new clitocyboid genera in the Tricholomatoid clade (Agaricales) with notes on Clitocybe and Lepista. Mycologia 106(5):13–369

    Google Scholar 

  • Anisimova M, Gil M, Dufayard J-F, Dessimoz C, Gascuel O (2011) Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Syst Biol 60(5):685–699

    Article  PubMed Central  PubMed  Google Scholar 

  • Baroni TJ, Franco-Molano AE, Lodge J, Linder DL, Horak E, Hofstetter V (2007) Arthromyces and Blastosporella, two new genera of conidia-producing lyophylloid agarics (Agaricales, Basidiomycota) from the neotropics. Mycol Res 111:572–580

    Article  PubMed  Google Scholar 

  • Bon, M. (1992) Clé monographique des espèces galéro-naucorioïdes. Association d’écologie et de mycologie

  • Bon M (1994) Deux Lyophylloideae intéressantes et le genre Gerhardtia st. et nom. nov. Doc Mycol 24(93):65–68

    Google Scholar 

  • Bon M (1999). Flore mycologique d’Europe 5. Collybio-marasmioïdes et ressemblants. Documents Mycologiques, Mémoire hors série n°5. Lille

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17(4):540–552

    Article  CAS  PubMed  Google Scholar 

  • Chevenet F, Brun C, Bañuls A-L, Jacq B, Christen R (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinform 7:439

    Article  Google Scholar 

  • Consiglio G, Contu M (2002) Il genere Lyophyllum P. Karst. emend. Kühner, in Italia. Rivista di Micologia 45:99–181

    Google Scholar 

  • Contu M, Consiglio G (2005) “2004” Il genere Gerhardtia (Lyophyllaceae) in Europa, con osservazioni sulle rimanenti specie conosciute. Micologia e Vegetazione Mediterranea 19(2): 151–162

  • Cooper JA (2014) New species and combinations of some New Zealand agarics belonging to Clitopilus, Lyophyllum, Gerhardtia, Clitocybe, Hydnangium, Mycena, Rhodocollybia and Gerronema. Mycosphere 5(2):263–288

    Article  Google Scholar 

  • Courtecuisse R, Duhem B (2012) Champignons de France et d’Europe. 2e édition. Delachaux & Niestlé, Lausanne

  • Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F et al (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36(2):465–469

    Article  Google Scholar 

  • Donk MA (1962) The generic names proposed for Agaricaceae. Beihefte zur Nova Hedwigia 5:320

    Google Scholar 

  • Du X-H, Zhao Q, Yang ZL, Hansen K, Taşkın H, Büyükalaca S et al (2012) How well do ITS rDNA sequences differentiate species of true morels (Morchella)? Mycologia 104:1351–1368

    Article  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Frøslev TG, Jeppesen TS, Laessøe T, Kjøller R (2007) Molecular phylogenetics and delimitation of species in Cortinarius section Calochroi (Basidiomycota, Agaricales) in Europe. Mol Phylogenet Evol 44(1):217–227

    Article  PubMed  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  CAS  PubMed  Google Scholar 

  • Giraud T, Refrégier G, Le Gac M, de Vienne DM, Hood ME (2008) Fungal Genet Biol 45(6):791–802

    Article  CAS  PubMed  Google Scholar 

  • Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W et al (2010) New algorithms and methods to estimate maximum likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59(3):307–321

    Article  CAS  PubMed  Google Scholar 

  • Harder CB, Laessøe T, Frøslev TG, Ekelund F, Rosendhal S, Kjøller R (2013) A three-gene phylogeny of the Mycena pura complex reveals 11 phylogenetic species and shows ITS to be unreliable for species identification. Fungal Biol 117:764–775

    Article  CAS  PubMed  Google Scholar 

  • Hibbett DS (2007) After the gold rush, or before the flood? Evolutionary morphology of mushroom-forming fungi (Agaricomycetes) in the early 21st century. Mycol Res 111:1001–1018

    Article  PubMed  Google Scholar 

  • Hofstetter V, Clémençon H, Vilgalys R, Moncalvo JM (2002) Phylogenetic analyses of the Lyophylleae (Agaricales, Basidiomycota) based on nuclear and mitochondrial rDNA sequences. Mycol Res 106(9):1043–1059

    Article  CAS  Google Scholar 

  • Hofstetter V, Redhead SA, Kauff F, Moncalvo J-M, Matheny PB, Vilgalys R (2014) Taxonomic revision and examination of ecological transitions of the Lyophyllaceae (Basidiomycota, Agaricales) based on a multigene phylogeny. Cryptogam Mycol 35(4):399–425

    Article  Google Scholar 

  • Holec J, Kolařík M (2013) Ossicaulis lachnopus (Agaricales, Lyophyllaceae), a species similar to O. lignatilis, is verified by morphological and molecular methods. Mycol Prog 12(3):589–597

    Article  Google Scholar 

  • James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ et al (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818–822

    Article  CAS  PubMed  Google Scholar 

  • Jargeat P, Martos F, Carriconde F, Gryta H, Moreau P-A, Gardes M (2010) Phylogenetic species delimitation in ectomycorrhizal fungi and implications for barcoding: the case of the Tricholoma scalpturatum complex (Basidiomycota). Mol Ecol 19:5216–5230

    Article  CAS  PubMed  Google Scholar 

  • Jülich W (1982) Lyophyllaceae. Bibl Mycol 85:378

    Google Scholar 

  • Karsten PA (1881) Hymenomycetes Fennici. Acta Societatis pro Fauna et Flora Fennica 2(1):40

    Google Scholar 

  • Kiss L (2012) Limits of nuclear ribosomal DNA internal transcribed spacer (ITS) sequences as species barcodes for Fungi. Proc Natl Acad Sci USA 109(27):E1811

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Knudsen H, Vesterholt J, (eds) (2012) Funga Nordica. Nordsvamp, Copenhagen

  • Kühner R (1938) Utilisation du carmin acétique dans la classification des Agarics leucosporés. Bulletin Mensuel de la Société Linnéenne de Lyon 7:204–211

    Google Scholar 

  • Kühner R (1980) Les Hyménomycètes agaricoides. Bulletin Mensuel de la Société Linnéenne de Lyon 49:1–1027

    Google Scholar 

  • Kühner R, Romagnesi H (1953) Flore analytique des champignons supérieurs (agarics, bolets, chanterelles). Masson & Cie, Paris

    Google Scholar 

  • Larsson E, Sundberg H (2011) Lyophyllum shimeji, a species associated with lichen pine forest in northern Fennoscandia. Mycoscience 52(5):289–295

    Article  Google Scholar 

  • Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799–1808

    Article  CAS  PubMed  Google Scholar 

  • Matheny PB (2005) Improving phylogenetic inference of mushrooms with RPB1 and RPB2 nucleotide sequences (Inocybe, Agaricales). Mol Phylogenet Evol 35:1–20

    Article  CAS  PubMed  Google Scholar 

  • Matheny PB, Curtis JM, Hofstetter V, Aime MC, Moncalvo JM, Ge ZW (2006) Major clades of Agaricales: a multilocus phylogenetic overview. Mycologia 98(6):982–995

    Article  PubMed  Google Scholar 

  • Moreau P-A, Vila J, Aime MC, Antonin V, Horak E, Pérez-Butron JL, Richard F, Urban A, Welti S, Vizzini A (2015) Cibaomyces and Cyptotrama, two new genera for Europe, and an emendation of Rhizomarasmius (Basidiomycota, Physalacriaceae). Mycol Prog (in press)

  • Neville P, Poumarat S (1997) Premiere récolte française de Tephrocybe gibberosa et sa position par rapport aux Tephrocybe carbonicoles. Bollettino del Gruppo Micologico Bresadola 40:347–366

    Google Scholar 

  • Norvell LL (2010) Report of the nomenclature committee for fungi: 15. Taxon 59(1):291–293

    Google Scholar 

  • O’Donnell K, Rooney AP, Mills GL, Kuo M, Weber NS, Rehner SA (2011) Phylogeny and historical biogeography of true morels (Morchella) reveals an early Cretaceous origin and high continental endemism and provincialism in the Holarctic. Fungal Genet Biol 48:252–265

    Article  PubMed  Google Scholar 

  • Osmundson TW, Robert VA, Schoch CL, Baker LJ, Smith A, Robich G et al (2013) Filling gaps in biodiversity knowledge for macrofungi: contributions and assessment of an herbarium collection DNA barcode sequencing project. PLoS One 8(4):e62419

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. http://www.R-project.org/

  • Redhead SA (1981) Parasitism of bryophytes by agarics. Can J Bot 59:63–67

    Article  Google Scholar 

  • Redhead SA (2014) Nomenclatural novelties. Index Fungorum 202:1

    Google Scholar 

  • Redhead SA, Hofstetter V, Clémençon H, Moncalvo J-M (2006) 1742) Proposal to conserve the name Lyophyllum with a conserved type (Basidiomycota. Taxon 55(4):1034–1036

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci USA 109(16):6241–6246

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Seifert KA (2009) Progress towards DNA barcoding of fungi. Mol Ecol Res 9:83–89

    Article  CAS  Google Scholar 

  • Singer R (1986) The agaricales in modern taxonomy. Koeltz Scientific Books, Koenigstein, p 981p

    Google Scholar 

  • Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56(4):564–577

    Article  CAS  PubMed  Google Scholar 

  • Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 31(1):21–32

    Article  CAS  PubMed  Google Scholar 

  • Vesterholt J, Ludwig E (2012) Lyophyllum. In: Knudsen H, Vesterholt J, (eds): 583

  • Wang X-Q, Zhou D-Q, Zhao Y-C, Zhang X-L, Li L, Li S-H (2013) Lyophyllum rhombisporum sp. nov. from China. Mycotaxon 123(5):473–477

    Article  Google Scholar 

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Acknowledgments

This work is dedicated to the memory of the French mycologist Marcel Bon, who contributed major advances in our current knowledge of the biodiversity of Lyophyllaceae, and recently passed away. This project was supported by the grant “Diversité des champignons mycorhiziens des plantes” (DivMyc, to M.-A. Selosse) from the network Bibliothèque Du Vivant (BDV) funded by the CNRS, the Museum National d’Histoire Naturelle, the INRA and the CEA (Centre National de Séquençage). DNA extracts were generated at the Service of Genetic Markers of UMR-CEFE 5175. We are grateful to M.-P. Dubois, F. Kjellberg and J.-Y Rasplus for their support from the sequencing programs. We thank C. Hannoire, R. Courtecuisse and Y. Deneyer for providing precious material to the present study. J.-M. B. is personally grateful to A. Taudière for his introduction to the R software.

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Authors and Affiliations

  1. UMR 5175 CEFE - INSERM - Campus CNRS, 1919 Route de Mende, 34293, Montpellier, France

    J. -M. Bellanger

  2. EA 4483, Faculté des sciences pharmaceutiques et biologiques, Université de Lille, BP 83, 59006, Cedex Lille, France

    P. -A. Moreau

  3. Conservatoire botanique national des Pyrénées et de Midi-Pyrénées, Vallon de Salut, BP 70315, 65203, Bagnères de Bigorre Cedex, France

    G. Corriol

  4. 2436, route de Brailles, 38510, Vézeronce-Curtin, France

    A. Bidaud

  5. 45, rue du docteur Calmette, 91170, Viry-Chatillon, France

    R. Chalange

  6. Department of Botany, Charles University, Prague, Czech Republic

    Z. Dudova

  7. UMR 5175 CEFE - Université de Montpellier – Campus CNRS, 1919 Route de Mende, 34293, Montpellier, France

    F. Richard

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  1. J. -M. Bellanger
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Correspondence to J. -M. Bellanger.

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Bellanger, J.M., Moreau, P.A., Corriol, G. et al. Plunging hands into the mushroom jar: a phylogenetic framework for Lyophyllaceae (Agaricales, Basidiomycota). Genetica 143, 169–194 (2015). https://doi.org/10.1007/s10709-015-9823-8

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  • DOI: https://doi.org/10.1007/s10709-015-9823-8

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