Skip to main content
Log in

Genetic population structure of the ectomycorrhizal fungus Pisolithus microcarpus suggests high gene flow in south-eastern Australia

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Pisolithus are ectomycorrhizal fungi that associate with roots of numerous plant species in natural and plantation forests worldwide. Despite the fact that Pisolithus spp. are present in plantation forests in many countries, knowledge of the genetic population structure of Pisolithus spp. remains limited. In this study, we have tested the hypothesis that a propensity for long-distance spore dispersal in Pisolithus microcarpus, along with the widespread distribution of potential eucalypt and acacia plant hosts in south-eastern Australia facilitates gene flow that limits population differentiation. Five polymorphic simple sequence repeat markers were used to investigate the population structure of P. microcarpus. Isolates were grouped according to geographical origin and isolate genotypes were analysed among the geographical populations. Pairwise FST estimates indicated limited genetic differentiation among the geographical populations. Analysis of molecular variance revealed that most of the genetic variation present was within geographical populations, with only 1.3% of the genetic variation among P. microcarpus geographical populations. This was particularly pronounced for four geographical populations within a ca 7,000 km2 area New South Wales, which were each separated by <100 km and appeared to be genetically homogeneous. The lack of population structure is suggested to be due to a high degree of gene flow, via basidiospores, between the New South Wales geographical populations.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Anderson IC (1996) The molecular ecology of Pisolithus tinctorius around the greater Sydney region. Honours Thesis, University of Western Sydney

  • Anderson IC, Chambers SM, Cairney JWG (1998a) Molecular determination of genetic variation in Pisolithus isolates from a defined region in New South Wales, Australia. New Phytol 138:151–162

    Article  CAS  Google Scholar 

  • Anderson IC, Chambers SM, Cairney JWG (1998b) Use of molecular methods to estimate the size and distribution of mycelial individuals of the ectomycorrhizal basidiomycete Pisolithus tinctorius. Mycol Res 102:295–300

    Article  Google Scholar 

  • Anderson IC, Chambers SM, Cairney JWG (2001a) Distribution and persistence of Australian Pisolithus species genets at native sclerophyll forest field sites. Mycol Res 105:971–976

    Article  CAS  Google Scholar 

  • Anderson IC, Chambers SM, Cairney JWG (2001b) ITS-RFLP and ITS sequence diversity in Pisolithus from central and eastern Australian sclerophyll forests. Mycol Res 105:1304–1312

    Article  CAS  Google Scholar 

  • Bergemann SE, Miller SL (2002) Size, distribution, and persistence of genets in local populations of the late-stage ectomycorrhizal basidiomycete, Russula brevipes. New Phytol 156:313–320

    Article  CAS  Google Scholar 

  • Bergemann SE, Douhan GW, Garbelotto M, Miller SL (2006) No evidence of population structure across three isolated subpopulations of Russula brevipes in an oak/pine woodland. New Phytol 170:177–184

    Article  PubMed  Google Scholar 

  • Bougher NL, Syme K (1998) Fungi of Southeastern Australia. University of Western Australia Press, Nedlands

    Google Scholar 

  • Carriconde F, Gardes M, Jargeat P, Heilmann-Clausen J, Mouhamadou B, Gryta H (2008) Population evidence of cryptic species and geographical structure in the cosmopolitan ectomycorrhizal fungus, Tricholoma scalpturatum. Microbial Ecol 56:513–524

    Article  Google Scholar 

  • Chambers SM, Cairney JWG (1999) Pisolithus. In: Cairney JWG, Chambers SM (eds) Ectomycorrhizal fungi: key genera in profile. Springer-Verlag, Berlin, pp 1–31

    Google Scholar 

  • Dunham SM, O’Dell TE, Molina R (2006) Spatial analysis of within-population microsatellite variability reveals restricted gene flow in the Pacific golden chanterelle (Cantharellus formosus). Mycologia 98:250–259

    Article  CAS  PubMed  Google Scholar 

  • Fiore-Donno A-M, Martin F (2001) Populations of ectomycorrhizal Laccaria amethystina and Xerocomus spp. show contrasting colonization patterns in a mixed forest. New Phytol 152:533–542

    Article  CAS  Google Scholar 

  • Franzén I, Vasaitis R, Penttilä R, Stenlid J (2007) Population genetics of the wood-decay fungus Phlebia centrifuga P. Karst. in fragmented and continuous habitats. Mol Ecol 16:3326–3333

    Article  PubMed  Google Scholar 

  • Fuhrer B (1985) A field companion to Australian fungi. The Five Mile Press, Hawthorn

    Google Scholar 

  • Garbaye J, Delwaulle JC, Diagana D (1988) Growth response of Eucalyptus in the Congo to ectomycorrhizal inoculation. Forest Ecol Manag 24:151–157

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Grubisha LC, Bergemann SE, Bruns TD (2007) Host islands within the California Northern Channel Islands create fine-scale genetic structure in two sympatric species of the symbiotic ectomycorrhizal fungus Rhizopogon. Mol Ecol 16:1811–1822

    Article  PubMed  Google Scholar 

  • Hartl DL, Clark AG (1997) Principles of population genetics, 3rd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Hirst JM, Hurst GW (1967) Long-distance spore transport. In: Gregory PH, Monteith JL (eds) Airborne microbes. Cambridge University Press, Cambridge, pp 307–344

    Google Scholar 

  • Hitchcock CJ, Chambers SM, Anderson IC, Cairney JWG (2003) Development of markers for simple sequence repeat-rich regions that discriminate between Pisolithus albus and P. microcarpus. Mycol Res 107:699–706

    Article  CAS  PubMed  Google Scholar 

  • Hitchcock CJ, Chambers SM, Cairney JWG (2006) Development of polymorphic simple sequence repeat markers for Pisolithus microcarpus. Mol Ecol Notes 6:443–445

    Article  CAS  Google Scholar 

  • Högberg N, Stenlid J (1999) Population genetics of Fomitopsis rosea—a wood decay fungus of the old-growth European taiga. Mol Ecol 8:703–710

    Article  Google Scholar 

  • Högberg N, Holdenrieder O, Stenlid J (1999) Population structure of the wood decay fungus Fomitopsis pinicola. Heredity 83:354–360

    Article  PubMed  Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 65:65–70

    Google Scholar 

  • James TY, Vilgalys R (2001) Abundance and diversity of Schizophyllum commune spore clouds in the Caribbean detected by selective sampling. Mol Ecol 10:471–479

    Article  CAS  PubMed  Google Scholar 

  • James TY, Porter D, Hamrick JL, Vilgalys R (1999) Evidence for limited intercontinental gene flow in the cosmopolitan mushroom, Schizophyllum commune. Evolution 53:1665–1677

    Article  CAS  Google Scholar 

  • Kallio T (1970) Aerial distribution of the root-rot fungus Fomes annosus (Fr.) Cooke in Finland. Acta For Fenn 107:1–55

    Google Scholar 

  • Kauserud H, Schumacher T (2003) Genetic structure of Fennoscandian populations of the threatened wood-decay fungus Fomitopsis rosea (Basidiomycota). Mycol Res 107:155–163

    Article  CAS  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 

  • Kretzer AM, Dunham S, Molina R, Spatafora JW (2005) Patterns of vegetative growth and gene flow in Rhizopogon vinicolor and R. vesiculosis (Boletales, Basidiomycota). Mol Ecol 14:2259–2268

    Article  CAS  PubMed  Google Scholar 

  • Lian C, Narimatsu M, Nara K, Hogetsu T (2006) Tricholoma matsutake in a natural Pinus densiflora forest: correspondence between above- and below-ground genets, association with multiple host trees and alteration of existing ectomycorrhizal communities. New Phytol 171:825–836

    Article  PubMed  Google Scholar 

  • Martin F, Díez J, Dell B, Delaruelle C (2002) Phylogeography of the ectomycorrhizal Pisolithus species as inferred from nuclear ribosomal DNA ITS sequences. New Phytol 153:345–357

    Article  CAS  Google Scholar 

  • Marx DH, Bryan WC, Cordell CE (1977) Survival and growth of pine seedlings with Pisolithus ectomycorrhizae after two years on reforestations sites in North Carolina and Florida. Forest Sci 16:363–373

    Google Scholar 

  • Mitakakis TZ, Guest DI (2001) A fungal spore calendar for the atmosphere of Melbourne, Australia, for the year 1993. Aerobiologia 17:171–176

    Article  Google Scholar 

  • Moyersoen B, Beever RE, Martin F (2003) Genetic diversity of Pisolithus in New Zealand indicates multiple long-distance dispersal from Australia. New Phytol 160:569–579

    Article  Google Scholar 

  • Murat C, Díez J, Luis P, Delaruelle C, Dupré C, Chevalier G, Bonfante P, Martin F (2004) Polymorphism at the ribosomal DNA ITS and its relation to postglacial re-colonization routes of the Perigord truffle Tuber melanosporum. New Phytol 164:401–411

    Article  CAS  Google Scholar 

  • Parrent JL, Garbeletto M, Gilbert GS (2004) Population genetic structure of the polypore Datronia caperata in fragmented mangrove forests. Mycol Res 108:403–410

    Article  CAS  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:915–959

    Google Scholar 

  • Prospero S, Lung-Escarmant B, Dutech C (2008) Genetic structure of an expanding Armillaria root rot fungus (Armillaria ostoyae) population in a managed pine forest in southwestern France. Mol Ecol 17:3366–3378

    Article  CAS  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetic software for exact tests and ecumenicisms. J Hered 86:248–249

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Rishbeth J (1959) Dispersal of Fomes annosus Fr. and Peniophora gigantea (Fr.) Massee. T Brit Mycol Soc 42:243–260

    Article  Google Scholar 

  • Roy M, Dubois M-P, Proffit M et al (2008) Evidence from population genetics that the ectomycorrhizal basidiomycete Laccaria amethystina is an actual multihost symbiont. Mol Ecol 17:2825–2838

    Article  CAS  PubMed  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN (version 2.000): A software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic, London

    Google Scholar 

  • Stenlid J (1994) Regional differentiation in Heterobasidion annosum. In: Johansson M, Stenlid J (eds) Proceedings of the 8th IUFRO conference on root and butt rots. Swedish University of Agricultural Sciences, Uppsala, pp 243–248

  • Stenlid J, Gustafsson M (2001) Are rare wood decay fungi threatened by inability to spread? Ecol Bull 49:85–91

    Google Scholar 

  • Vainio EJ, Hantula J (2000) Genetic differentiation between European and North American populations of Phlebiopsis gigantea. Mycologia 92:436–446

    Article  CAS  Google Scholar 

  • van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Xu J, Sha T, Li Y-C, Zhao Z-W, Yang Z (2008) Recombination and genetic differentiation among natural populations of the ectomycorrhizal mushroom Tricholoma matsutake from southwestern China. Mol Ecol 17:1238–1247

    Article  PubMed  Google Scholar 

  • Zhou Z, Miwa M, Hogetsu T (2001) Polymorphism of simple sequence repeats reveals gene flow within and between ectomycorrhizal Suillus grevillei populations. New Phytol 149:339–348

    Article  CAS  Google Scholar 

Download references

Acknowledgements

CJH acknowledges receipt of an Australian Postgraduate Research Award and additional scholarship funding from UWS and the Centre for Plant and Food Science. This work was partially funded by a UWS Research Grant to JWGC. We thank Emilie Cameron for assistance with the statistical analyses, NSW National Parks and Wildlife Service for permission to collect P. microcarpus basidiomes, and the anonymous reviewers for their helpful comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John W. G. Cairney.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

Size and frequency of alleles for each P. microcarpus geographical population for the five polymorphic loci analysed. (DOC 106 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hitchcock, C.J., Chambers, S.M. & Cairney, J.W.G. Genetic population structure of the ectomycorrhizal fungus Pisolithus microcarpus suggests high gene flow in south-eastern Australia. Mycorrhiza 21, 131–137 (2011). https://doi.org/10.1007/s00572-010-0317-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-010-0317-3

Keywords

Navigation