A plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosis

Abstract

Morphogens provide positional information and their concentration is key to the organized development of multicellular organisms. Nitrogen-fixing root nodules are unique organs induced by Nod factor-producing bacteria. Localized production of Nod factors establishes a developmental field within the root where plant cells are reprogrammed to form infection threads and primordia. We found that regulation of Nod factor levels by Lotus japonicus is required for the formation of nitrogen-fixing organs, determining the fate of this induced developmental program. Our analysis of plant and bacterial mutants shows that a host chitinase modulates Nod factor levels possibly in a structure-dependent manner. In Lotus, this is required for maintaining Nod factor signalling in parallel with the elongation of infection threads within the nodule cortex, while root hair infection and primordia formation are not influenced. Our study shows that infected nodules require balanced levels of Nod factors for completing their transition to functional, nitrogen-fixing organs.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Anna Malolepszy

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    No competing interests declared.
  2. Simon Kelly

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    No competing interests declared.
  3. Kasper Kildegaard Sørensen

    Department of Chemistry, University of Copenhagen, Frederiksberg, Denmark
    Competing interests
    No competing interests declared.
  4. Euan Kevin James

    The James Hutton Institute, Dundee, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7969-6570
  5. Christina Kalisch

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    Christina Kalisch, affiliated with Novozymes. The author has no other competing interests to declare.
  6. Zoltan Bozsoki

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4267-9969
  7. Michael Panting

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    No competing interests declared.
  8. Stig U Andersen

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1096-1468
  9. Shusei Sato

    Kazusa DNA Research Institute, Kisarazu, Japan
    Competing interests
    No competing interests declared.
  10. Ke Tao

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    No competing interests declared.
  11. Dorthe Bødker Jensen

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    No competing interests declared.
  12. Maria Vinther

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    No competing interests declared.
  13. Noor de Jong

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    No competing interests declared.
  14. Lene Heegaard Madsen

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    No competing interests declared.
  15. Yosuke Umehara

    Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, Tsukuba, Japan
    Competing interests
    No competing interests declared.
  16. Kira Gysel

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    No competing interests declared.
  17. Mette U Berentsen

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    Mette U Berentsen, affiliated with Eurofins Steins Laboratorium A-S. The author has no other competing interests to declare.
  18. Michael Blaise

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    No competing interests declared.
  19. Knud Jørgen Jensen

    Department of Chemistry, University of Copenhagen, Frederiksberg, Denmark
    Competing interests
    No competing interests declared.
  20. Mikkel B Thygesen

    Department of Chemistry, University of Copenhagen, Frederiksberg, Denmark
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0158-2802
  21. Niels Sandal

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    No competing interests declared.
  22. Kasper Røjkjær Andersen

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4415-8067
  23. Simona Radutoiu

    Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark
    For correspondence
    radutoiu@mbg.au.dk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8841-1415

Funding

Danish Reasearch Foundation (DNRF79)

  • Anna Malolepszy
  • Simon Kelly
  • Kasper Kildegaard Sørensen
  • Christina Kalisch
  • Zoltan Bozsoki
  • Michael Panting
  • Stig U Andersen
  • Dorthe Bødker Jensen
  • Maria Vinther
  • Noor de Jong
  • Lene Heegaard Madsen
  • Kira Gysel
  • Mette U Berentsen
  • Michael Blaise
  • Knud Jørgen Jensen
  • Mikkel B Thygesen
  • Niels Sandal
  • Kasper Røjkjær Andersen
  • Simona Radutoiu

China Scholarship Council (201604910506)

  • Ke Tao

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: June 3, 2018
  2. Accepted: October 2, 2018
  3. Accepted Manuscript published: October 4, 2018 (version 1)
  4. Version of Record published: October 17, 2018 (version 2)

Copyright

© 2018, Malolepszy 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. Anna Malolepszy
  2. Simon Kelly
  3. Kasper Kildegaard Sørensen
  4. Euan Kevin James
  5. Christina Kalisch
  6. Zoltan Bozsoki
  7. Michael Panting
  8. Stig U Andersen
  9. Shusei Sato
  10. Ke Tao
  11. Dorthe Bødker Jensen
  12. Maria Vinther
  13. Noor de Jong
  14. Lene Heegaard Madsen
  15. Yosuke Umehara
  16. Kira Gysel
  17. Mette U Berentsen
  18. Michael Blaise
  19. Knud Jørgen Jensen
  20. Mikkel B Thygesen
  21. Niels Sandal
  22. Kasper Røjkjær Andersen
  23. Simona Radutoiu
(2018)
A plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosis
eLife 7:e38874.
https://doi.org/10.7554/eLife.38874

Share this article

https://doi.org/10.7554/eLife.38874

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