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.

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

  • 2,612
    views
  • 402
    downloads
  • 36
    citations

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

Download links

Share this article

https://doi.org/10.7554/eLife.65306

Further reading

    1. Plant Biology
    Maryam Rahmati Ishka, Hayley Sussman ... Magdalena M Julkowska
    Research Article

    Soil salinity is one of the major threats to agricultural productivity worldwide. Salt stress exposure alters root and shoots growth rates, thereby affecting overall plant performance. While past studies have extensively documented the effect of salt stress on root elongation and shoot development separately, here we take an innovative approach by examining the coordination of root and shoot growth under salt stress conditions. Utilizing a newly developed tool for quantifying the root:shoot ratio in agar-grown Arabidopsis seedlings, we found that salt stress results in a loss of coordination between root and shoot growth rates. We identify a specific gene cluster encoding domain-of-unknown-function 247 (DUF247), and characterize one of these genes as Salt Root:shoot Ratio Regulator Gene (SR3G). Further analysis elucidates the role of SR3G as a negative regulator of salt stress tolerance, revealing its function in regulating shoot growth, root suberization, and sodium accumulation. We further characterize that SR3G expression is modulated by WRKY75 transcription factor, known as a positive regulator of salt stress tolerance. Finally, we show that the salt stress sensitivity of wrky75 mutant is completely diminished when it is combined with sr3g mutation. Together, our results demonstrate that utilizing root:shoot ratio as an architectural feature leads to the discovery of a new stress resilience gene. The study’s innovative approach and findings not only contribute to our understanding of plant stress tolerance mechanisms but also open new avenues for genetic and agronomic strategies to enhance crop environmental resilience.

    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.