A fungal member of the Arabidopsis thaliana phyllosphere antagonizes Albugo laibachii via a GH25 lysozyme

  1. Katharina Eitzen
  2. Priyamedha Sengupta
  3. Samuel Kroll
  4. Eric Kemen  Is a corresponding author
  5. Gunther Doehlemann  Is a corresponding author
  1. University of Cologne, Germany
  2. Max Planck Institute for Plant Breeding Research, Germany
  3. University of Tübingen, Germany

Abstract

Plants are not only challenged by pathogenic organisms, but also colonized by commensal microbes. The network of interactions these microbes establish with their host and amongst each other is suggested to contribute to the immune responses of plants against pathogens. In wild Arabidopsis thaliana populations, the oomycete pathogen Albugo laibachii plays an influential role in structuring the leaf phyllosphere. We show that the epiphytic yeast Moesziomyces bullatus ex Albugo on Arabidopsis, a close relative of pathogenic smut fungi, is an antagonistic member of the A. thaliana phyllosphere, which reduces infection of A. thaliana by A. laibachii. Combination of transcriptomics, reverse genetics and protein characterization identified a GH25 hydrolase with lysozyme activity as a major effector of this microbial antagonism. Our findings broaden the understanding of microbial interactions within the phyllosphere, provide insights into the evolution of epiphytic basidiomycete yeasts and pave the way for novel biocontrol strategies.

Data availability

Genome information and RNA sequencing have been submitted to NCBI Genbank and are available under the following links: https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE148670

Article and author information

Author details

  1. Katharina Eitzen

    Institute for Plant Sciences and Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Priyamedha Sengupta

    Institute for Plant Sciences and Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Samuel Kroll

    AG Kemen, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Eric Kemen

    Center for Plant Molecular Biology, University of Tübingen, Tübingen, Germany
    For correspondence
    eric.kemen@uni-tuebingen.de
    Competing interests
    The authors declare that no competing interests exist.
  5. Gunther Doehlemann

    Institute for Plant Sciences and Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, Cologne, Germany
    For correspondence
    g.doehlemann@uni-koeln.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7353-8456

Funding

Deutsche Forschungsgemeinschaft (SPP 2125 DECRyPT)

  • Katharina Eitzen
  • Priyamedha Sengupta

Deutsche Forschungsgemeinschaft (EXC-2048/1,Project ID 390686111)

  • Katharina Eitzen

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

Reviewing Editor

  1. Caroline Gutjahr, Technical University of Munich, Germany

Publication history

  1. Received: November 30, 2020
  2. Accepted: January 10, 2021
  3. Accepted Manuscript published: January 11, 2021 (version 1)
  4. Version of Record published: February 8, 2021 (version 2)

Copyright

© 2021, Eitzen 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

  • 1,715
    Page views
  • 296
    Downloads
  • 5
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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. Katharina Eitzen
  2. Priyamedha Sengupta
  3. Samuel Kroll
  4. Eric Kemen
  5. Gunther Doehlemann
(2021)
A fungal member of the Arabidopsis thaliana phyllosphere antagonizes Albugo laibachii via a GH25 lysozyme
eLife 10:e65306.
https://doi.org/10.7554/eLife.65306

Further reading

    1. Plant Biology
    Jack Rhodes et al.
    Short Report Updated

    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.

    1. Developmental Biology
    2. Plant Biology
    Sören Strauss et al.
    Tools and Resources Updated

    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.