Lipid transfer from plants to arbuscular mycorrhiza fungi

  1. Andreas Keymer
  2. Priya Pimprikar
  3. Vera Wewer
  4. Claudia Huber
  5. Mathias Brands
  6. Simone L Bucerius
  7. Pierre-Marc Delaux
  8. Verena Klingl
  9. Edda von Röpenack-Lahaye
  10. Trevor L Wang
  11. Wolfgang Eisenreich
  12. Peter Dörmann
  13. Martin Parniske
  14. Caroline Gutjahr  Is a corresponding author
  1. LMU Munich, Biocenter Martinsried, Germany
  2. University of Cologne Biocenter, Germany
  3. Technical University Munich, Germany
  4. University of Bonn, Germany
  5. Unité Mixte de Recherche 5546, France
  6. University of Tübingen, Germany
  7. Norwich Research Park, United Kingdom

Abstract

Arbuscular mycorrhiza (AM) symbioses contribute to global carbon cycles as plant hosts divert up to 20% of photosynthate to the obligate biotrophic fungi. Previous studies suggested carbohydrates as the only form of carbon transferred to the fungi. However, de novo fatty acid (FA) synthesis has not been observed in AM fungi in absence of the plant. In a forward genetic approach, we identified two Lotus japonicus mutants defective in AM-specific paralogs of lipid biosynthesis genes (KASI and GPAT6). These mutants perturb fungal development and accumulation of emblematic fungal 16:1ω5 FAs. Using isotopolog profiling we demonstrate that 13C patterns of fungal FAs recapitulate those of wild-type hosts, indicating cross-kingdom lipid transfer from plants to fungi. This transfer of labelled FAs was not observed for the AM-specific lipid biosynthesis mutants. Thus, growth and development of beneficial AM fungi is not only fueled by sugars but depends on lipid transfer from plant hosts.

Article and author information

Author details

  1. Andreas Keymer

    Faculty of Biology, Genetics, LMU Munich, Biocenter Martinsried, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Priya Pimprikar

    Faculty of Biology, Genetics, LMU Munich, Biocenter Martinsried, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Vera Wewer

    Mass Spectrometry Metabolomics Facility, Cluster of Excellence on Plant Sciences, University of Cologne Biocenter, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Claudia Huber

    Biochemistry, Technical University Munich, Garching, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Mathias Brands

    Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6548-1448
  6. Simone L Bucerius

    Faculty of Biology, Genetics, LMU Munich, Biocenter Martinsried, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Pierre-Marc Delaux

    Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5546, Castanet Tolosan, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6211-157X
  8. Verena Klingl

    Faculty of Biology, Genetics, LMU Munich, Biocenter Martinsried, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Edda von Röpenack-Lahaye

    Analytics Facility, Center for Plant Molecular Biology, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Trevor L Wang

    John Innes Centre, Norwich Research Park, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  11. Wolfgang Eisenreich

    Biochemistry, Technical University Munich, Garching, Germany
    Competing interests
    The authors declare that no competing interests exist.
  12. Peter Dörmann

    Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5845-9370
  13. Martin Parniske

    Faculty of Biology, Genetics, LMU Munich, Biocenter Martinsried, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8561-747X
  14. Caroline Gutjahr

    Faculty of Biology, Genetics, LMU Munich, Biocenter Martinsried, Martinsried, Germany
    For correspondence
    caroline.gutjahr@lmu.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6163-745X

Funding

Deutsche Forschungsgemeinschaft (SFB924 B03 Function of the GRAS protein RAM1 in arbuscule development)

  • Caroline Gutjahr

Deutsche Forschungsgemeinschaft (Emmy Noether program GU1423/1-1)

  • Caroline Gutjahr

Deutsche Forschungsgemeinschaft (PA493/7-1 Plant genes required for arbuscular mycorrhiza symbiosis)

  • Martin Parniske

Deutsche Forschungsgemeinschaft (SFB924 B03 Genetic dissection of arbuscular mycorrhiza development)

  • Martin Parniske

Deutsche Forschungsgemeinschaft (SPP1212)

  • Peter Dörmann

Deutsche Forschungsgemeinschaft (Research Training Group GRK 2064 Do520/15-1)

  • Peter Dörmann

Hans Fischer Gesellschaft e. V.

  • Wolfgang Eisenreich

Biotechnology and Biological Sciences Research Council

  • Trevor L Wang

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Gary Stacey, University of Missouri, United States

Version history

  1. Received: May 31, 2017
  2. Accepted: July 13, 2017
  3. Accepted Manuscript published: July 20, 2017 (version 1)
  4. Version of Record published: August 16, 2017 (version 2)
  5. Version of Record updated: April 12, 2018 (version 3)

Copyright

© 2017, Keymer et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Andreas Keymer
  2. Priya Pimprikar
  3. Vera Wewer
  4. Claudia Huber
  5. Mathias Brands
  6. Simone L Bucerius
  7. Pierre-Marc Delaux
  8. Verena Klingl
  9. Edda von Röpenack-Lahaye
  10. Trevor L Wang
  11. Wolfgang Eisenreich
  12. Peter Dörmann
  13. Martin Parniske
  14. Caroline Gutjahr
(2017)
Lipid transfer from plants to arbuscular mycorrhiza fungi
eLife 6:e29107.
https://doi.org/10.7554/eLife.29107

Share this article

https://doi.org/10.7554/eLife.29107

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