Advertisement

Mycorrhiza

, Volume 17, Issue 5, pp 415–428 | Cite as

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

  • Taiana RiviereEmail author
  • Abdallah G. Diedhiou
  • Moussa Diabate
  • G. Senthilarasu
  • K. Natarajan
  • Annemieke Verbeken
  • Bart Buyck
  • Bernard Dreyfus
  • Gilles Bena
  • Amadou M. Ba
Original Paper

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.

Keywords

Ectomycorrhizal Basidiomycetes Tropical rain forests Mitochondrial LrRNA gene 

Notes

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.

References

  1. Alexander IJ, Högberg P (1986) Ectomycorrhizas of tropical angiospermous trees. New Phytol 102:541–549CrossRefGoogle Scholar
  2. Baura G, Szaro TM, Bruns TD (1992) Gastrosuillus laricinus is a recent derivative of Suillus grevilleii: molecular evidence. Mycologia 84:592–597CrossRefGoogle Scholar
  3. Berbee ML, Taylor JW (1993) Dating the evolutionary radiations of the true fungi. Can J Bot 71:1114–1127CrossRefGoogle Scholar
  4. 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 229–245CrossRefGoogle Scholar
  5. Binder M, Hibbett DS (2002) Higher-level phylogenetic relationships of Homobasidiomycetes (Mushroom-forming fungi) inferred from four rDNA regions. Mol Phylogenet Evol 22:76–90CrossRefPubMedGoogle Scholar
  6. Bruns TD, Szaro TM (1992) Rate and mode differences between nuclear and mitochondrial small-subunit rRNA genes in mushrooms. Mol Biol Evol 9:836–855Google Scholar
  7. Bruns TD, Szaro TM, Gardes M et al (1998) A sequence database for the identification of ectomycorrhizal Basidiomycetes by phylogenetic analysis. Mol Ecol 7:257–272CrossRefGoogle Scholar
  8. Bull JJ, Huelsenbeck PP, Cunningham CW, Swofford DL, Waddell PJ (1993) Partitioning and combining data in phylogenetic analysis. Syst Biol 42:384–397CrossRefGoogle Scholar
  9. Buyck B (1994a) Russula I (Russulaceae). Flore Illus Champignons Afr Cent 15:335–408Google Scholar
  10. Buyck B (1994b) Russula II (Russulaceae). Flore Illus Champignons Afr Cent 16:411–542Google Scholar
  11. Buyck B (1997) Russula III (Russulaceae). Flore Illus Champignons Afr Cent 17:545–597Google Scholar
  12. Buyck B, Thoen D, Walting R (1996) Ectomycorrhizal fungi of the Guinea–Congo Region. Proc R Soc Edinb Sect B 104:313–333Google Scholar
  13. 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 75:1323–1335CrossRefGoogle Scholar
  14. 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 75–110CrossRefGoogle Scholar
  15. den Bakker HC, Zuccarello GC, Kuyper TH W, Noordeloos ME (2004) Evolution and host specificity in the ectomycorrhizal genus Leccinum. New Phytol 163:201–215CrossRefGoogle Scholar
  16. Doyle JJ (1992) Gene trees and species trees: molecular systematics as one-character taxonomy. Syst Bot 17:144–163CrossRefGoogle Scholar
  17. Eberhardt U (2002) Molecular analyses of the agaricoid Russulaceae: correspondence with mycorrhizal and sporocarp features in the genus Russula. Mycol Prog 1(2):201–224CrossRefGoogle Scholar
  18. Eberhardt U, Verbeken A (2004) Sequestrate Lactarius species from tropical Africa: L. angiocarpus sp. nov. and L. dolichocaulis comb. nov. Mycol Res 108:1042–1052CrossRefPubMedGoogle Scholar
  19. Egger KN (1995) Molecular analysis of ectomycorrhizal fungal communities. Can J Bot 73:S1415–S1422CrossRefGoogle Scholar
  20. 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 14:209–217CrossRefGoogle Scholar
  21. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefPubMedGoogle Scholar
  22. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for Basidiomycetes—application for the identification of mycorrhizas and rusts. Mol Ecol 2:113–118CrossRefPubMedGoogle Scholar
  23. Gardes M, Bruns TD (1996) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: above and below-ground views. Can J Bot 74:1572–1583CrossRefGoogle Scholar
  24. 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 69:180–190CrossRefGoogle Scholar
  25. Grogan P, Baar J, Bruns TD (2000) Below-ground ectomycorrhizal community structure in a recently burned bishop pine forest. J Ecol 88:1051–1062CrossRefGoogle Scholar
  26. Hibbett DS, Gilbert LB, Donoghue MJ (2000) Evolutionary instability of ectomycorrhizal symbioses in Basidiomycetes. Nature 407:506–508CrossRefPubMedGoogle Scholar
  27. Horton TR, Bruns TD (2001) The molecular revolution in ectomycorrhizal ecology: peeking into the black-box. Mol Ecol 10:1855–1871CrossRefPubMedGoogle Scholar
  28. Huelsenbeck JO, Rannala B (1997) Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science 276:227–232CrossRefPubMedGoogle Scholar
  29. 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 142:151–162CrossRefGoogle Scholar
  30. 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 132:143–156CrossRefGoogle Scholar
  31. 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 9:1985–1996CrossRefPubMedGoogle Scholar
  32. 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 166:1063–1068CrossRefPubMedGoogle Scholar
  33. 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 161:313–320CrossRefGoogle Scholar
  34. Lee SS, Alexander IJ, Watling R (1997) Ectomycorrhizas and putative ectomycorrhizal fungi of Shorea leprosula Miq. (Dipterocarpaceae). Mycorrhiza 7:63–81CrossRefGoogle Scholar
  35. 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 59:153–163Google Scholar
  36. 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 5–44Google Scholar
  37. Miller SL, Buyck B (2002) Molecular phylogeny of the genus Russula in Europe with a comparison of modern infrageneric classifications. Mycol Res 106:259–276CrossRefGoogle Scholar
  38. 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 357–423Google Scholar
  39. 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 16:48–63CrossRefPubMedGoogle Scholar
  40. Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858CrossRefPubMedGoogle Scholar
  41. Natarajan K, Senthilarasu G, Kumaresan V, Rivière T (2005) Diversity in ectomycorrhizal fungi of a dipterocarp forest in Western Ghats. Curr Sci 88(12):1893–1895Google Scholar
  42. Newbery DM, Alexander IJ, Rother LA (1997) Phosphorus dynamics in lowland African rain forest: the influence of ectomycorrhizal trees. Ecol Monogr 67:367–409Google Scholar
  43. Nicholas KB, Nicholas HB, Deerfield DW II (1997) GeneDoc: analysis and visualization of genetic variation. Embnet News 4:1–4Google Scholar
  44. Onguene NA, Kuyper TW (2001) Mycorrhizal associations in the rain forest of South Cameroon. For Ecol Manag 140:277–287CrossRefGoogle Scholar
  45. Pascal JP, Pélissier R (1996) Structure and floristic composition of a tropical evergreen forest in south-west India. J Trop Ecol 12:191–211CrossRefGoogle Scholar
  46. 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 105:107–119CrossRefGoogle Scholar
  47. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  48. Redhead JF (1980) Mycorrhiza in natural tropical forests. In: Mikola P (ed) Tropical mycorrhiza research. Clarendon, Oxford, pp 127–142Google Scholar
  49. Rivière T (2004) Biodiversity, molecular ecology and phylogeography of tropical ectomycorrhizal symbiosis. Ph.D. thesis, Université de Montpellier II, FranceGoogle Scholar
  50. Rivière T, Natarajan K, Dreyfus B (2005) Spatial distribution of ectomycorrhizal Basidiomycete Russula subsect. Foetentinae populations in a primary dipterocarp rainforest. Mycorrhiza 16:143–148CrossRefPubMedGoogle Scholar
  51. Romagnesi H (1985) Les Russules d’Europe et d’Afrique du Nord. J. Cramer, Lehre (reprint with supplement)Google Scholar
  52. Sanon KB, Bâ AM, Dexheimer J (1997) Mycorrhizal status of some fungi fruiting beneath indigenous trees in Burkina Faso. For Ecol Manag 98:61–69CrossRefGoogle Scholar
  53. Shimono Y, Kato M, Takamatsu S (2004) Molecular phylogeny of Russulaceae (Basidiomycetes; Russulales) from the nucleotide sequences of nuclear large subunit rDNA. Mycoscience 45:303–316CrossRefGoogle Scholar
  54. Singer R (1986) The Agaricales in modern taxonomy, 4th edn. Koeltz Scientific, KoeningsteinGoogle Scholar
  55. 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 9:25–41CrossRefGoogle Scholar
  56. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San Diego, CAGoogle Scholar
  57. 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 283–292Google Scholar
  58. Swofford DL (2001) PAUP‡: phylogenetic analysis using parsimony (‡and other methods), ver. 4. Sinauer, Sunderland, MAGoogle Scholar
  59. Thoen D, Bâ AM (1989) Ectomycorrhizas and putative ectomycorrhizal fungi of Afzelia africana Sm. and Uapaca guineensis Müll. Arg. in southern Senegal. New Phytol 113:549–559CrossRefGoogle Scholar
  60. 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 22:4673–4680CrossRefPubMedPubMedCentralGoogle Scholar
  61. Wall JD (2003) Estimating ancestral population sizes and divergence times. Genetics 163:395–404PubMedPubMedCentralGoogle Scholar
  62. Watling R, Lee SS (1995) Ectomycorrhizal fungi associated with members of the Dipterocarpaceae in Peninsular Malaysia. J Trop For Sci 7:657–669Google Scholar
  63. 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 315–322Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Taiana Riviere
    • 1
    • 2
    • 8
    Email author
  • Abdallah G. Diedhiou
    • 1
  • Moussa Diabate
    • 3
  • G. Senthilarasu
    • 4
  • K. Natarajan
    • 4
  • Annemieke Verbeken
    • 5
  • Bart Buyck
    • 6
  • Bernard Dreyfus
    • 1
  • Gilles Bena
    • 1
  • Amadou M. Ba
    • 1
    • 7
  1. 1.UMR 113Symbioses Tropicales et Méditerranéennes (LSTM)Montferrier-sur-LezFrance
  2. 2.Institut Français de PondichéryPondicherryIndia
  3. 3.Institut de Recherche Agronomique de GuinéeConakryGuinea
  4. 4.Centre of Advanced Study in Botany (CASB)University of MadrasChennaiIndia
  5. 5.Department of BiologyGhent UniversityGhentBelgium
  6. 6.Muséum National d’Histoire Naturelle (MNHN)ParisFrance
  7. 7.Laboratoire de Biologie et Physiologie VégétalesUniversité Antilles–GuyanePointe-à-PitreFrance
  8. 8.Centre de Biologie pour la Gestion des PopulationsCampus International de BaillarguetMontferrier-sur-Lez cedexFrance

Personalised recommendations