Letter

Evidence for the sexual origin of heterokaryosis in arbuscular mycorrhizal fungi

  • Nature Microbiology 1, Article number: 16033 (2016)
  • doi:10.1038/nmicrobiol.2016.33
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Abstract

Sexual reproduction is ubiquitous among eukaryotes, and fully asexual lineages are extremely rare. Prominent among ancient asexual lineages are the arbuscular mycorrhizal fungi (AMF), a group of plant symbionts with a multinucleate cytoplasm. Genomic divergence among co-existing nuclei was proposed to drive the evolutionary success of AMF in the absence of sex1, but this hypothesis has been contradicted by recent genome analyses that failed to find significant genetic diversity within an AMF isolate2,3. Here, we set out to resolve issues surrounding the genome organization and sexual potential of AMF by exploring the genomes of five isolates of Rhizophagus irregularis, a model AMF. We find that genetic diversity in this species varies among isolates and is structured in a homo-dikaryon-like manner usually linked with the existence of a sexual life cycle. We also identify a putative AMF mating-type locus, containing two genes with structural and evolutionary similarities with the mating-type locus of some Dikarya. Our analyses suggest that this locus may be multi-allelic and that AMF could be heterothallic and bipolar. These findings reconcile opposing views on the genome organization of these ubiquitous plant symbionts and open avenues for strain improvement and environmental application of these organisms.

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Acknowledgements

The authors thank J.W. Taylor, T. James, D. Beaudet, T. Giraud, M. Lόpez-Villavicencio and I. de la Providencia, for constructive comments and suggestions on previous versions of this manuscript. The authors also thank I. Sanders (University of Lausanne) and Y. Dalpé (Agriculture Canada, Ottawa) for providing the in vitro isolates of Rhizophagus irregularis used in this study, M. Griesmann (Faculty of Biology, LMU Munich) for help with the BUSCO analyses and S. Dreissig (IPK, Gatersleben) for help with WGA work. N.C. is a fellow of the Canadian Institute for Advanced Research. N.C.'s work is supported by the Discovery programme from the Natural Sciences and Engineering Research Council of Canada (NSERC-Discovery), an Early Researcher Award from the Ontario Ministry of Research and Innovation (ER13-09-190) and the ZygoLife project funded by the National Science Foundation (DEB 1441677). M.K. was financed by the European Social Fund (ESF) and the state budget of Czech Republic through the Operational Programme Education for Competitiveness (OPEC) under project number CZ.1.07/2.3.00/30.0048.

Author information

Author notes

    • Jeanne Ropars
    •  & Kinga Sędzielewska Toro

    These authors contributed equally to this work.

Affiliations

  1. Canadian Institute for Advanced Research, Department of Biology, University of Ottawa, Ottawa, Ontario, Canada

    • Jeanne Ropars
    • , Jessica Noel
    • , Adrian Pelin
    • , Philippe Charron
    • , Timea Marton
    • , Manuela Krüger
    •  & Nicolas Corradi
  2. LMU Munich, Faculty of Biology, Genetics, D-82152 Planegg-Martinsried, Germany

    • Kinga Sędzielewska Toro
    •  & Andreas Brachmann
  3. FASTERIS S.A., Ch. du Pont-du-Centenaire 109, PO Box 28, CH-1228 Plan-les-Ouates, Switzerland

    • Laurent Farinelli
  4. Institute of Botany, Academy of Sciences of the Czech Republic, Zámek 1, Průhonice, CZ-25243, Czech Republic

    • Manuela Krüger
  5. Leibniz Institute of Plant Genetics and Crop Plant Research, D-06466 Gatersleben, Germany

    • Jörg Fuchs

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Contributions

J.R., K.S.T., A.B. and N.C. planned the experiments. J.R., K.S.T., J.N., P.C., L.F., T.M., M.K. and J.F. performed experiments. J.R., A.P., A.B. and N.C. performed bioinformatic analyses. J.R. and N.C. drafted the manuscript with contributions from K.S.T. and A.B.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Nicolas Corradi.

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