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Genetic diversity of ectomycorrhizal Basidiomycetes from African and Indian tropical rain forests

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Abstract

Ectomycorrhizal (ECM) fungi have a worldwide distribution. However, the ecology of tropical ECM fungi is poorly documented, limiting our understanding of the symbiotic associations between tropical plants and fungi. ECM Basidiomycete diversity was investigated for the first time in two tropical rain forests in Africa (Western Upper Guinea) and in Asia (Western Ghats, India), using a fragment of the mitochondrial large subunit rRNA gene to type 140 sporocarps and 54 ectomycorrhizas. To evaluate taxonomic diversity, phylogenetic analyses were performed, and 40 sequences included from identified European specimens were used as taxonomic benchmarks. Five clades were recovered corresponding to six taxonomic groups: boletoids, sclerodermatoids, russuloids, thelephoroids, and a clade grouping the Amanitaceae and Tricholomataceae families. Our results revealed that the Russulaceae species display a great diversity with several putative new species, especially in Guinea. Other taxonomic issues at family/section levels are also briefly discussed. This study provides preliminary insights into taxonomic diversity, ECM status, and biogeographic patterns of ECM fungi in tropical two rain forest ecosystems, which appear to be as diverse as in temperate and boreal forests.

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References

  • Alexander IJ, Högberg P (1986) Ectomycorrhizas of tropical angiospermous trees. New Phytol 102:541–549

    Article  Google Scholar 

  • Baura G, Szaro TM, Bruns TD (1992) Gastrosuillus laricinus is a recent derivative of Suillus grevilleii: molecular evidence. Mycologia 84:592–597

    Article  CAS  Google Scholar 

  • Berbee ML, Taylor JW (1993) Dating the evolutionary radiations of the true fungi. Can J Bot 71:1114–1127

    Article  Google Scholar 

  • Berbee ML, Taylor JW (2001) Fungal molecular evolution: gene trees and geologic time. In: McLaughlin DJ, McLaughlin RG, Lemke PA (eds) The Mycota VII. Part B. Systematics and evolution. Springer, Berlin, pp 229–245

    Chapter  Google Scholar 

  • Binder M, Hibbett DS (2002) Higher-level phylogenetic relationships of Homobasidiomycetes (Mushroom-forming fungi) inferred from four rDNA regions. Mol Phylogenet Evol 22:76–90

    Article  CAS  PubMed  Google Scholar 

  • Bruns TD, Szaro TM (1992) Rate and mode differences between nuclear and mitochondrial small-subunit rRNA genes in mushrooms. Mol Biol Evol 9:836–855

    Google Scholar 

  • Bruns TD, Szaro TM, Gardes M et al (1998) A sequence database for the identification of ectomycorrhizal Basidiomycetes by phylogenetic analysis. Mol Ecol 7:257–272

    Article  CAS  Google Scholar 

  • Bull JJ, Huelsenbeck PP, Cunningham CW, Swofford DL, Waddell PJ (1993) Partitioning and combining data in phylogenetic analysis. Syst Biol 42:384–397

    Article  Google Scholar 

  • Buyck B (1994a) Russula I (Russulaceae). Flore Illus Champignons Afr Cent 15:335–408

    Google Scholar 

  • Buyck B (1994b) Russula II (Russulaceae). Flore Illus Champignons Afr Cent 16:411–542

    Google Scholar 

  • Buyck B (1997) Russula III (Russulaceae). Flore Illus Champignons Afr Cent 17:545–597

    Google Scholar 

  • Buyck B, Thoen D, Walting R (1996) Ectomycorrhizal fungi of the Guinea–Congo Region. Proc R Soc Edinb Sect B 104:313–333

    Google Scholar 

  • Dahlberg A, Jonsson L, Nylund JE (1997) Species diversity and distribution of biomass above and belowground among ectomycorrhizal fungi in an old-growth Norway spruce forest in south Sweden. Can J Bot 75:1323–1335

    Article  Google Scholar 

  • Debaud JC, Marmeisse R, Gay G (1999) Intraspecific genetic variation and populations of ecomycorrhizal fungi. In: Varma AK, Hock B (eds) Mycorrhiza: structure, molecular biology and function. Springer, Berlin, pp 75–110

    Chapter  Google Scholar 

  • den Bakker HC, Zuccarello GC, Kuyper TH W, Noordeloos ME (2004) Evolution and host specificity in the ectomycorrhizal genus Leccinum. New Phytol 163:201–215

    Article  Google Scholar 

  • Doyle JJ (1992) Gene trees and species trees: molecular systematics as one-character taxonomy. Syst Bot 17:144–163

    Article  Google Scholar 

  • Eberhardt U (2002) Molecular analyses of the agaricoid Russulaceae: correspondence with mycorrhizal and sporocarp features in the genus Russula. Mycol Prog 1(2):201–224

    Article  Google Scholar 

  • Eberhardt U, Verbeken A (2004) Sequestrate Lactarius species from tropical Africa: L. angiocarpus sp. nov. and L. dolichocaulis comb. nov. Mycol Res 108:1042–1052

    Article  PubMed  Google Scholar 

  • Egger KN (1995) Molecular analysis of ectomycorrhizal fungal communities. Can J Bot 73:S1415–S1422

    Article  CAS  Google Scholar 

  • Erland S, Jonsson T, Mahmood S, Finlay RD (1999) Below-ground ectomycorrhizal community structure in two Picea abies forests in southern Sweden. Scand J For Res 14:209–217

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gardes M, Bruns TD (1996) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: above and below-ground views. Can J Bot 74:1572–1583

    Article  Google Scholar 

  • Gardes M, White TJ, Fortin J, Bruns TD, Taylor JW (1991) Identification of indigenous and introduced symbiotic fungi in ectomycorrhizas by amplification of nuclear and mitochondrial ribosomal DNA. Can J Bot 69:180–190

    Article  CAS  Google Scholar 

  • Grogan P, Baar J, Bruns TD (2000) Below-ground ectomycorrhizal community structure in a recently burned bishop pine forest. J Ecol 88:1051–1062

    Article  Google Scholar 

  • Hibbett DS, Gilbert LB, Donoghue MJ (2000) Evolutionary instability of ectomycorrhizal symbioses in Basidiomycetes. Nature 407:506–508

    Article  CAS  PubMed  Google Scholar 

  • Horton TR, Bruns TD (2001) The molecular revolution in ectomycorrhizal ecology: peeking into the black-box. Mol Ecol 10:1855–1871

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck JO, Rannala B (1997) Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science 276:227–232

    Article  CAS  PubMed  Google Scholar 

  • Jonsson L, Dahlberg A, Nilsson M-C, Kårén O, Zackrisson O (1999) Continuity of ectomycorrhizal fungi in self-regenerating boreal Pinus sylvestris forests studied in comparing mycobiont diversity on seedlings and mature trees. New Phytol 142:151–162

    Article  Google Scholar 

  • Jonsson L, Dahlberg A, Brandrud T-E (2000) Spatiotemporal distribution of an ectomycorrhizal community in an oligotrophic Swedish Picea abies forest subjected to experimental nitrogen addition: above and below-ground views. For Ecol Manag 132:143–156

    Article  Google Scholar 

  • Kõljalg U, Dahlberg A, Taylor AFS et al (2000) Diversity and abundance of resupinate thelephoroid fungi as ectomycorrhizal symbionts in Swedish boreal forests. Mol Ecol 9:1985–1996

    Article  PubMed  Google Scholar 

  • Kõljalg U, Larsson KH, Abarenkov K et al (2005) UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol 166:1063–1068

    Article  PubMed  Google Scholar 

  • Kretzer AM, Dunham S, Molina R, Spatafora JW (2003) Microsatellite markers reveal the below ground distribution of genets in two species of Rhizopogon forming tuberculate ectomycorrhizas on Douglas fir. New Phytol 161:313–320

    Article  Google Scholar 

  • Lee SS, Alexander IJ, Watling R (1997) Ectomycorrhizas and putative ectomycorrhizal fungi of Shorea leprosula Miq. (Dipterocarpaceae). Mycorrhiza 7:63–81

    Article  Google Scholar 

  • Marx DH (1969) The influence of ectotrophic mycorrhizal fungi on the resistance of pine roots to pathogenic infections. I. Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59:153–163

    Google Scholar 

  • Maury-Lechon G, Curtet L (1998) Biogeography and evolutionary systematics of Dipterocarpaceae. In: Appanah S, TurnbullU MJ (eds) A review of dipterocarps taxonomy, ecology and silviculture. CIFOR, Jakarta, pp 5–44

    Google Scholar 

  • Miller SL, Buyck B (2002) Molecular phylogeny of the genus Russula in Europe with a comparison of modern infrageneric classifications. Mycol Res 106:259–276

    Article  CAS  Google Scholar 

  • Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena in mycorrhizal symbiosis: community—ecological consequences and practical implications. In: Allen MF (ed) Mycorrhizal functioning. Chapman & Hall, London, UK, pp 357–423

    Google Scholar 

  • Moncalvo JM, Drehmel D, Vilgalys R (2000) Variation in modes and rates of evolution in nuclear and mitochondrial ribosomal DNA in the mushroom genus Amanita (Agaricales, Basidiomycota): phylogenetic implications. Mol Phylogenet Evol 16:48–63

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Natarajan K, Senthilarasu G, Kumaresan V, Rivière T (2005) Diversity in ectomycorrhizal fungi of a dipterocarp forest in Western Ghats. Curr Sci 88(12):1893–1895

    Google Scholar 

  • Newbery DM, Alexander IJ, Rother LA (1997) Phosphorus dynamics in lowland African rain forest: the influence of ectomycorrhizal trees. Ecol Monogr 67:367–409

    Google Scholar 

  • Nicholas KB, Nicholas HB, Deerfield DW II (1997) GeneDoc: analysis and visualization of genetic variation. Embnet News 4:1–4

    Google Scholar 

  • Onguene NA, Kuyper TW (2001) Mycorrhizal associations in the rain forest of South Cameroon. For Ecol Manag 140:277–287

    Article  Google Scholar 

  • Pascal JP, Pélissier R (1996) Structure and floristic composition of a tropical evergreen forest in south-west India. J Trop Ecol 12:191–211

    Article  Google Scholar 

  • Pélissier R, Pascal JP, Houllier F, Laborde H (1998) Impact of selective logging on the dynamics of a low elevation dense moist evergreen forest in the Western Ghats (South India). For Ecol Manag 105:107–119

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Redhead JF (1980) Mycorrhiza in natural tropical forests. In: Mikola P (ed) Tropical mycorrhiza research. Clarendon, Oxford, pp 127–142

    Google Scholar 

  • Rivière T (2004) Biodiversity, molecular ecology and phylogeography of tropical ectomycorrhizal symbiosis. Ph.D. thesis, Université de Montpellier II, France

  • Rivière T, Natarajan K, Dreyfus B (2005) Spatial distribution of ectomycorrhizal Basidiomycete Russula subsect. Foetentinae populations in a primary dipterocarp rainforest. Mycorrhiza 16:143–148

    Article  PubMed  Google Scholar 

  • Romagnesi H (1985) Les Russules d’Europe et d’Afrique du Nord. J. Cramer, Lehre (reprint with supplement)

  • Sanon KB, Bâ AM, Dexheimer J (1997) Mycorrhizal status of some fungi fruiting beneath indigenous trees in Burkina Faso. For Ecol Manag 98:61–69

    Article  Google Scholar 

  • Shimono Y, Kato M, Takamatsu S (2004) Molecular phylogeny of Russulaceae (Basidiomycetes; Russulales) from the nucleotide sequences of nuclear large subunit rDNA. Mycoscience 45:303–316

    Article  CAS  Google Scholar 

  • Singer R (1986) The Agaricales in modern taxonomy, 4th edn. Koeltz Scientific, Koeningstein

    Google Scholar 

  • Singer R, Araujo IJS (1979) Litter decomposition and ectomycorrhiza in Amazonian forests: 1. A comparison of litter decomposition and ectomycorrhizal Basidiomycetes in latosol–terra firme rain forest and white podzol Campinarana. Acta Amazon 9:25–41

    Article  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San Diego, CA

    Google Scholar 

  • Smits WTM (1992) Mycorrhizal studies in dipterocarp forests in Indonesia. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystems. Cambridge, pp 283–292

  • Swofford DL (2001) PAUP‡: phylogenetic analysis using parsimony (‡and other methods), ver. 4. Sinauer, Sunderland, MA

  • Thoen D, Bâ AM (1989) Ectomycorrhizas and putative ectomycorrhizal fungi of Afzelia africana Sm. and Uapaca guineensis Müll. Arg. in southern Senegal. New Phytol 113:549–559

    Article  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wall JD (2003) Estimating ancestral population sizes and divergence times. Genetics 163:395–404

    CAS  PubMed  PubMed Central  Google Scholar 

  • Watling R, Lee SS (1995) Ectomycorrhizal fungi associated with members of the Dipterocarpaceae in Peninsular Malaysia. J Trop For Sci 7:657–669

    Google Scholar 

  • White TJ, Bruns TD, Lee SS, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelf DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and application. Academic, San Diego, pp 315–322

    Google Scholar 

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Acknowledgements

We thank P. Deschères, G. Ifono (Eaux et Forêts, Guinée), A. Fontana (IRD, Guinée) for their help in identifying several tree species. We thank Dr. V. Kumaresan (CASB, India) for fruitful collaboration. The authors are grateful to Dr. D. McKey (CNRS, France) and Dr. O. Dangles (IRD, France) for useful comments, discussion, and support. This work was supported by a doctoral grant from the French Institute of Pondicherry to Taiana Rivière.

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Authors and Affiliations

  1. UMR 113, Symbioses Tropicales et Méditerranéennes (LSTM), 34998, Montferrier-sur-Lez, France

    Taiana Riviere, Abdallah G. Diedhiou, Bernard Dreyfus, Gilles Bena & Amadou M. Ba

  2. Institut Français de Pondichéry, 11 St Louis Street, Pondicherry, India

    Taiana Riviere

  3. Institut de Recherche Agronomique de Guinée, Conakry, Guinea

    Moussa Diabate

  4. Centre of Advanced Study in Botany (CASB), University of Madras, Chennai, India

    G. Senthilarasu & K. Natarajan

  5. Department of Biology, Ghent University, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium

    Annemieke Verbeken

  6. Muséum National d’Histoire Naturelle (MNHN), Cryptogamie, 12 rue Buffon, 75005, Paris, France

    Bart Buyck

  7. Laboratoire de Biologie et Physiologie Végétales, Université Antilles–Guyane, BP. 592, 97159, Pointe-à-Pitre, Guadeloupe, France

    Amadou M. Ba

  8. Centre de Biologie pour la Gestion des Populations, Campus International de Baillarguet, CS 30016, 34988, Montferrier-sur-Lez cedex, France

    Taiana Riviere

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  1. Taiana Riviere
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  2. Abdallah G. Diedhiou
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  3. Moussa Diabate
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Correspondence to Taiana Riviere.

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Riviere, T., Diedhiou, A.G., Diabate, M. et al. Genetic diversity of ectomycorrhizal Basidiomycetes from African and Indian tropical rain forests. Mycorrhiza 17, 415–428 (2007). https://doi.org/10.1007/s00572-007-0117-6

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