Host-induced bacterial cell wall decomposition mediates pattern-triggered immunity in Arabidopsis

Abstract

Peptidoglycans (PGN) are immunogenic bacterial surface patterns that trigger immune activation in metazoans and plants. It is generally unknown, how complex bacterial structures, such as PGN, are perceived by plant pattern recognition receptors (PRR) and whether host hydrolytic activities facilitate decomposition of bacterial matrices and generation of soluble PRR ligands. Here, we show that Arabidopsis thaliana upon bacterial infection or exposure to microbial patterns produces a metazoan lysozyme-like hydrolase (lysozyme 1, LYS1). LYS1 activity releases soluble PGN fragments from insoluble bacterial cell walls and cleavage products are able to trigger responses typically associated with plant immunity. Importantly, LYS1 mutant genotypes exhibit super-susceptibility to bacterial infections similar to that observed on PGN receptor mutants. We propose that plants employ hydrolytic activities for the decomposition of complex bacterial structures, and that soluble pattern generation might aid PRR-mediated immune activation in cell layers adjacent to infection sites.

Article and author information

Author details

  1. Xiaokun Liu

    University of Tübingen, Tübingen, Germany
    Competing interests
    No competing interests declared.
  2. Heini M Grabherr

    University of Tübingen, Tübingen, Germany
    Competing interests
    No competing interests declared.
  3. Roland Willmann

    University of Tübingen, Tübingen, Germany
    Competing interests
    No competing interests declared.
  4. Dagmar Kolb

    University of Tübingen, Tübingen, Germany
    Competing interests
    No competing interests declared.
  5. Frédéric Brunner

    University of Tübingen, Tübingen, Germany
    Competing interests
    No competing interests declared.
  6. Ute Bertsche

    University of Tübingen, Tübingen, Germany
    Competing interests
    No competing interests declared.
  7. Daniel Kühner

    University of Tübingen, Tübingen, Germany
    Competing interests
    No competing interests declared.
  8. Mirita Franz-Wachtel

    University of Tübingen, Tübingen, Germany
    Competing interests
    No competing interests declared.
  9. Bushra Amin

    University of Tübingen, Tübingen, Germany
    Competing interests
    No competing interests declared.
  10. Georg Felix

    University of Tübingen, Tübingen, Germany
    Competing interests
    No competing interests declared.
  11. Marc Ongena

    University of Liege-Gembloux Agro-Bio Tech, Gembloux, Belgium
    Competing interests
    No competing interests declared.
  12. Thorsten Nürnberger

    University of Tübingen, Tübingen, Germany
    Competing interests
    Thorsten Nürnberger, Reviewing editor, eLife.
  13. Andrea A Gust

    University of Tübingen, Tübingen, Germany
    For correspondence
    andrea.gust@zmbp.uni-tuebingen.de
    Competing interests
    No competing interests declared.

Copyright

© 2014, Liu 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

  • 3,994
    views

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. Xiaokun Liu
  2. Heini M Grabherr
  3. Roland Willmann
  4. Dagmar Kolb
  5. Frédéric Brunner
  6. Ute Bertsche
  7. Daniel Kühner
  8. Mirita Franz-Wachtel
  9. Bushra Amin
  10. Georg Felix
  11. Marc Ongena
  12. Thorsten Nürnberger
  13. Andrea A Gust
(2014)
Host-induced bacterial cell wall decomposition mediates pattern-triggered immunity in Arabidopsis
eLife 3:e01990.
https://doi.org/10.7554/eLife.01990

Share this article

https://doi.org/10.7554/eLife.01990

Further reading

    1. Cell Biology
    2. Plant Biology
    Baihong Zhang, Shuqin Huang ... Wenli Chen
    Research Article

    Autophagy-related gene 6 (ATG6) plays a crucial role in plant immunity. Nonexpressor of pathogenesis-related genes 1 (NPR1) acts as a signaling hub of plant immunity. However, the relationship between ATG6 and NPR1 is unclear. Here, we find that ATG6 directly interacts with NPR1. ATG6 overexpression significantly increased nuclear accumulation of NPR1. Furthermore, we demonstrate that ATG6 increases NPR1 protein levels and improves its stability. Interestingly, ATG6 promotes the formation of SINCs (SA-induced NPR1 condensates)-like condensates. Additionally, ATG6 and NPR1 synergistically promote the expression of pathogenesis-related genes. Further results showed that silencing ATG6 in NPR1-GFP exacerbates Pst DC3000/avrRps4 infection, while double overexpression of ATG6 and NPR1 synergistically inhibits Pst DC3000/avrRps4 infection. In summary, our findings unveil an interplay of NPR1 with ATG6 and elucidate important molecular mechanisms for enhancing plant immunity.

    1. Plant Biology
    Sonal Gupta, Simon Niels Groen ... Michael D Purugganan
    Research Article

    Populations can adapt to stressful environments through changes in gene expression. However, the fitness effect of gene expression in mediating stress response and adaptation remains largely unexplored. Here, we use an integrative field dataset obtained from 780 plants of Oryza sativa ssp. indica (rice) grown in a field experiment under normal or moderate salt stress conditions to examine selection and evolution of gene expression variation under salinity stress conditions. We find that salinity stress induces increased selective pressure on gene expression. Further, we show that trans-eQTLs rather than cis-eQTLs are primarily associated with rice’s gene expression under salinity stress, potentially via a few master-regulators. Importantly, and contrary to the expectations, we find that cis-trans reinforcement is more common than cis-trans compensation which may be reflective of rice diversification subsequent to domestication. We further identify genetic fixation as the likely mechanism underlying this compensation/reinforcement. Additionally, we show that cis- and trans-eQTLs are under balancing and purifying selection, respectively, giving us insights into the evolutionary dynamics of gene expression variation. By examining genomic, transcriptomic, and phenotypic variation across a rice population, we gain insights into the molecular and genetic landscape underlying adaptive salinity stress responses, which is relevant for other crops and other stresses.