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Organization of genetic variation in individuals of arbuscular mycorrhizal fungi


Arbuscular mycorrhizal (AM) fungi (Glomeromycota) are thought to be the oldest group of asexual multicellular organisms. They colonize the roots of most land plants, where they facilitate mineral uptake from the soil in exchange for plant-assimilated carbon1. Cells of AM fungi contain hundreds of nuclei. Unusual polymorphism of ribosomal DNA observed in individual spores of AM fungi inspired a hypothesis that heterokaryosis—that is, the coexistence of many dissimilar nuclei in cells—occurs throughout the AM fungal life history2,3. Here we report a genetic approach to test the hypothesis of heterokaryosis in AM fungi. Our study of the transmission of polymorphic genetic markers in natural isolates of Glomus etunicatum, coupled with direct amplification of rDNA from microdissected nuclei by polymerase chain reaction, supports the alternative hypothesis of homokaryosis, in which nuclei populating AM fungal individuals are genetically uniform. Intrasporal rDNA polymorphism contained in each nucleus signals a relaxation of concerted evolution4, a recombination-driven process that is responsible for homogenizing rDNA repeats5. Polyploid organization of glomeromycotan genomes could accommodate intranuclear rDNA polymorphism and buffer these apparently asexual organisms against the effects of accumulating mutations.

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Figure 1: Sorting of variants of a polymorphic marker in single-spore cultures of Glomus.
Figure 2: PLS1 variation in G. etunicatum field isolates.
Figure 3: rDNA variation in G. etunicatum field isolates.
Figure 4: Distribution of rDNA variation among individual nuclei in two Glomus species.


  1. Smith, S. E. & Read, D. J. Mycorrhizal Symbiosis (Academic, San Diego, 1997)

    Google Scholar 

  2. Kuhn, G., Hijri, M. & Sanders, I. R. Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414, 745–748 (2001)

    Article  ADS  CAS  Google Scholar 

  3. Bever, J. D. & Morton, J. Heritable variation and mechanisms of inheritance of spore shape within a population of Scutellospora pellucida, an arbuscular mycorrhizal fungus. Am. J. Bot. 86, 1209–1216 (1999)

    Article  CAS  Google Scholar 

  4. Arnheim, N. et al. Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes. Proc. Natl Acad. Sci. USA 77, 7323–7327 (1980)

    Article  ADS  CAS  Google Scholar 

  5. Dover, G. Molecular drive: a cohesive mode of species evolution. Nature 299, 111–117 (1982)

    Article  ADS  CAS  Google Scholar 

  6. Simon, L., Bousquet, J., Lévesque, R. C. & Lalonde, M. Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363, 67–69 (1993)

    Article  ADS  Google Scholar 

  7. Redecker, D., Kodner, R. & Graham, L. E. Glomalean fungi from the Ordovician. Science 289, 1920–1921 (2000)

    Article  ADS  CAS  Google Scholar 

  8. Remy, W., Taylor, T. N., Hass, H. & Kerp, H. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl Acad. Sci. USA 91, 11841–11843 (1994)

    Article  ADS  CAS  Google Scholar 

  9. Welch, D. M. & Meselson, M. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288, 1211–1215 (2000)

    Article  ADS  CAS  Google Scholar 

  10. Redecker, D., Hijri, M., Dulieu, H. & Sanders, I. R. Phylogenetic analysis of a dataset of fungal 5.8S rDNA sequences shows that highly divergent copies of internal transcribed spacers reported from Scutellospora castanea are of ascomycete origin. Fungal Genet. Biol. 28, 238–244 (1999)

    Article  CAS  Google Scholar 

  11. Schüßler, A. Glomales SSU rRNA gene diversity. New Phytol. 144, 205–207 (1999)

    Article  Google Scholar 

  12. Zhang, J. Z., Kumar, S. & Nei, M. Small-sample tests of episodic adaptive evolution—a case study of primate lysozymes. Mol. Biol. Evol. 14, 1335–1338 (1997)

    Article  CAS  Google Scholar 

  13. Bécard, G. & Pfeffer, P. E. Status of nuclear division in arbuscular mycorrhizal fungi during in vitro development. Protoplasma 174, 62–68 (1993)

    Article  Google Scholar 

  14. Giovannetti, M. et al. Genetic diversity of isolates of Glomus mosseae from different geographic areas detected by vegetative compatibility testing and biochemical and molecular analysis. Appl. Environ. Microbiol. 69, 616–624 (2003)

    Article  CAS  Google Scholar 

  15. Klironomos, J. N. & Moutoglis, P. Colonization of nonmycorrhizal plants by mycorrhizal neighbours as influenced by the collembolan, Folsomia candida. Biol. Fertil. Soils 29, 277–281 (1999)

    Article  Google Scholar 

  16. Kasuga, T., White, T. J. & Taylor, J. Estimation of nucleotide substitution rates in eurotiomycete fungi. Mol. Biol. Evol. 19, 2318–2324 (2002)

    Article  CAS  Google Scholar 

  17. Wendel, J. F., Schnabel, A. & Seelanan, T. Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc. Natl Acad. Sci. USA 92, 280–284 (1995)

    Article  ADS  CAS  Google Scholar 

  18. Schlötterer, C. & Tautz, D. Chromosomal homogeneity of Drosophila ribosomal DNA arrays suggests intrachromosomal exchanges drive concerted evolution. Curr. Biol. 4, 777–783 (1994)

    Article  Google Scholar 

  19. Arnheim, N., Treco, D., Taylor, B. & Eicher, E. M. Distribution of ribosomal gene length variants among mouse chromosomes. Proc. Natl Acad. Sci. USA 79, 4677–4680 (1982)

    Article  ADS  CAS  Google Scholar 

  20. Birky, C. W. Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics 144, 427–437 (1996)

    PubMed  Google Scholar 

  21. Hosny, M., Gianinazzi-Pearson, V. & Dulieu, H. Nuclear DNA content of 11 fungal species in Glomales. Genome 41, 422–428 (1998)

    Article  CAS  Google Scholar 

  22. Otto, S. P. & Whitton, J. Polyploid incidence and evolution. Annu. Rev. Genet. 34, 401–437 (2000)

    Article  CAS  Google Scholar 

  23. Mogie, M. & Ford, H. Sexual and asexual Taraxacum species. Biol. J. Linn. Soc. 35, 155–168 (1988)

    Article  Google Scholar 

  24. Kondrashov, A. S. The asexual ploidy cycle and the origin of sex. Nature 370, 213–216 (1994)

    Article  ADS  CAS  Google Scholar 

  25. Swofford, D. L. PAUP: phylogenetic analysis using parsimony (and other methods). Ver. 4 (Sinauer, Sunderland, MA, 1998).

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We thank W. Pawlowski for help with the spore nuclei count; P. Bethke for advice on nuclei microdissection; D. Baker, T. Galagher, B. King, T. Lee and T. Szaro for technical assistance; J. A. Fortin for G. intraradices; D. Douds for the DC1 isolate of Ri T-DNA-transformed carrot roots developed by G. Bécard; and D. J. Read, T. Bruns, A. Burt and the members of the Taylor laboratory for comments on the manuscript. This work was supported by the Torrey Mesa Research Institute-Syngenta Biotechnology and the National Research Initiative Competitive Grants Program (NRICGP) of the US Department of Agriculture.

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Correspondence to Teresa E. Pawlowska.

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Pawlowska, T., Taylor, J. Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 427, 733–737 (2004).

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