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.

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.

Metrics

  • 2,931
    views
  • 609
    downloads
  • 38
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Microbiology and Infectious Disease
    2. Plant Biology
    Nyasha Charura, Ernesto Llamas ... Alga Zuccaro
    Research Article

    Programmed cell death occurring during plant development (dPCD) is a fundamental process integral for plant growth and reproduction. Here, we investigate the connection between developmentally controlled PCD and fungal accommodation in Arabidopsis thaliana roots, focusing on the root cap-specific transcription factor ANAC033/SOMBRERO (SMB) and the senescence-associated nuclease BFN1. Mutations of both dPCD regulators increase colonization by the beneficial fungus Serendipita indica, primarily in the differentiation zone. smb-3 mutants additionally exhibit hypercolonization around the meristematic zone and a delay of S. indica-induced root-growth promotion. This demonstrates that root cap dPCD and rapid post-mortem clearance of cellular corpses represent a physical defense mechanism restricting microbial invasion of the root. Additionally, reporter lines and transcriptional analysis revealed that BFN1 expression is downregulated during S. indica colonization in mature root epidermal cells, suggesting a transcriptional control mechanism that facilitates the accommodation of beneficial microbes in the roots.

    1. Cell Biology
    2. Plant Biology
    Masanori Izumi, Sakuya Nakamura ... Shinya Hagihara
    Research Article

    Plants distribute many nutrients to chloroplasts during leaf development and maturation. When leaves senesce or experience sugar starvation, the autophagy machinery degrades chloroplast proteins to facilitate efficient nutrient reuse. Here, we report on the intracellular dynamics of an autophagy pathway responsible for piecemeal degradation of chloroplast components. Through live-cell monitoring of chloroplast morphology, we observed the formation of chloroplast budding structures in sugar-starved leaves. These buds were then released and incorporated into the vacuolar lumen as an autophagic cargo termed a Rubisco-containing body. The budding structures did not accumulate in mutants of core autophagy machinery, suggesting that autophagosome creation is required for forming chloroplast buds. Simultaneous tracking of chloroplast morphology and autophagosome development revealed that the isolation membranes of autophagosomes interact closely with part of the chloroplast surface before forming chloroplast buds. Chloroplasts then protrude at the site associated with the isolation membranes, which divide synchronously with autophagosome maturation. This autophagy-related division does not require DYNAMIN-RELATED PROTEIN 5B, which constitutes the division ring for chloroplast proliferation in growing leaves. An unidentified division machinery may thus fragment chloroplasts for degradation in coordination with the development of the chloroplast-associated isolation membrane.