A plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosis
- Aarhus University, Denmark
- University of Copenhagen, Denmark
- The James Hutton Institute, United Kingdom
- Kazusa DNA Research Institute, Japan
- National Agriculture and Food Research Organization, Japan
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
Kasper Røjkjær Andersen
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
- Gary Stacey, University of Missouri, United States
Publication history
- Received: June 3, 2018
- Accepted: October 2, 2018
- Accepted Manuscript published: October 4, 2018 (version 1)
- 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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A plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosis
eLife 7:e38874.
https://doi.org/10.7554/eLife.38874
Further reading
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- Plant Biology
Plant genomes encode hundreds of secreted peptides; however, relatively few have been characterised. We report here an uncharacterised, stress-induced family of plant signalling peptides, which we call CTNIPs. Based on the role of the common co-receptor BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1) in CTNIP-induced responses, we identified in Arabidopsis thaliana the orphan receptor kinase HAESA-LIKE 3 (HSL3) as the CTNIP receptor via a proteomics approach. CTNIP-binding, ligand-triggered complex formation with BAK1, and induced downstream responses all involve HSL3. Notably, the HSL3-CTNIP signalling module is evolutionarily conserved amongst most extant angiosperms. The identification of this novel signalling module will further shed light on the diverse functions played by plant signalling peptides and will provide insights into receptor-ligand co-evolution.
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- Developmental Biology
- Plant Biology
Positional information is a central concept in developmental biology. In developing organs, positional information can be idealized as a local coordinate system that arises from morphogen gradients controlled by organizers at key locations. This offers a plausible mechanism for the integration of the molecular networks operating in individual cells into the spatially coordinated multicellular responses necessary for the organization of emergent forms. Understanding how positional cues guide morphogenesis requires the quantification of gene expression and growth dynamics in the context of their underlying coordinate systems. Here, we present recent advances in the MorphoGraphX software (Barbier de Reuille et al., 2015) that implement a generalized framework to annotate developing organs with local coordinate systems. These coordinate systems introduce an organ-centric spatial context to microscopy data, allowing gene expression and growth to be quantified and compared in the context of the positional information thought to control them.
