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Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi

Nature volume 414, pages 745–748 (2001)Cite this article

Abstract

Ancient asexuals directly contradict the evolutionary theories that explain why organisms should evolve a sexual life history1,2. The mutualistic, arbuscular mycorrhizal fungi are thought to have been asexual for approximately 400 million years3,4. In the absence of sex, highly divergent descendants of formerly allelic nucleotide sequences are thought to evolve in a genome2. In mycorrhizal fungi, where individual offspring receive hundreds of nuclei from the parent, it has been hypothesized that a population of genetically different nuclei should evolve within one individual5,6. Here we use DNA–DNA fluorescent in situ hybridization to show that genetically different nuclei co-exist in individual arbuscular mycorrhizal fungi. We also show that the population genetics techniques4 used in other organisms are unsuitable for detecting recombination because the assumptions and underlying processes do not fit the fungal genomic structure shown here. Instead we used a phylogenetic approach to show that the within-individual genetic variation that occurs in arbuscular mycorrhizal fungi probably evolved through accumulation of mutations in an essentially clonal genome, with some infrequent recombination events. We conclude that mycorrhizal fungi have evolved to be multi-genomic.

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Figure 1: Nuclei of Scutellospora castanea taken with scanning laser confocal microscopy after single-target and double-target DNA–DNA FISH.
Figure 2: Within- and among-spore polymorphism.
Figure 3: Frequency distributions for the index of association for a population of 30 hypothetical spores of an arbuscular mycorrhizal fungus.

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Acknowledgements

We thank T. Boller and A. Wiemken for allowing part of this work to be conducted in the Botanical Institute Basle, T. Mes and M. Wilkinson for advice on the analysis, A. Rodriguez and J. P. Clapp for providing 28S sequences, E. Stöckli and H. Reichert for use of the confocal microscope, P. Heslop-Harrison for advice on in situ controls and J. P. Clapp, M. G. A. van der Heijden, L. Keller, A. M. Koch and F. Mery for critically reading the manuscript. We thank the Swiss National Science Foundation for supporting this work with a standard research grant and a fellowship awarded to I.R.S. under the professorial fellowship programme.

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  1. Gerrit Kuhn and Mohamed Hijri: These authors contributed equally to this work

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  1. Institute of Ecology, University of Lausanne, Biology Building, Lausanne, 1015, Switzerland

    Gerrit Kuhn, Mohamed Hijri & Ian R. Sanders

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  1. Gerrit Kuhn
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  3. Ian R. Sanders
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Correspondence to Ian R. Sanders.

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Kuhn, G., Hijri, M. & Sanders, I. Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414, 745–748 (2001). https://doi.org/10.1038/414745a

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