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

Version 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

  • 2,348
    views
  • 366
    downloads
  • 29
    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. 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

Share this article

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

Further reading

    1. Plant Biology
    Ivan Kulich, Julia Schmid ... Jiří Friml
    Research Article

    Root gravitropic bending represents a fundamental aspect of terrestrial plant physiology. Gravity is perceived by sedimentation of starch-rich plastids (statoliths) to the bottom of the central root cap cells. Following gravity perception, intercellular auxin transport is redirected downwards leading to an asymmetric auxin accumulation at the lower root side causing inhibition of cell expansion, ultimately resulting in downwards bending. How gravity-induced statoliths repositioning is translated into asymmetric auxin distribution remains unclear despite PIN auxin efflux carriers and the Negative Gravitropic Response of roots (NGR) proteins polarize along statolith sedimentation, thus providing a plausible mechanism for auxin flow redirection. In this study, using a functional NGR1-GFP construct, we visualized the NGR1 localization on the statolith surface and plasma membrane (PM) domains in close proximity to the statoliths, correlating with their movements. We determined that NGR1 binding to these PM domains is indispensable for NGR1 functionality and relies on cysteine acylation and adjacent polybasic regions as well as on lipid and sterol PM composition. Detailed timing of the early events following graviperception suggested that both NGR1 repolarization and initial auxin asymmetry precede the visible PIN3 polarization. This discrepancy motivated us to unveil a rapid, NGR-dependent translocation of PIN-activating AGCVIII kinase D6PK towards lower PMs of gravity-perceiving cells, thus providing an attractive model for rapid redirection of auxin fluxes following gravistimulation.

    1. Plant Biology
    Daniel S Yu, Megan A Outram ... Simon J Williams
    Research Article

    Plant pathogens secrete proteins, known as effectors, that function in the apoplast or inside plant cells to promote virulence. Effector recognition by cell-surface or cytosolic receptors results in the activation of defence pathways and plant immunity. Despite their importance, our general understanding of fungal effector function and recognition by immunity receptors remains poor. One complication often associated with effectors is their high sequence diversity and lack of identifiable sequence motifs precluding prediction of structure or function. In recent years, several studies have demonstrated that fungal effectors can be grouped into structural classes, despite significant sequence variation and existence across taxonomic groups. Using protein X-ray crystallography, we identify a new structural class of effectors hidden within the secreted in xylem (SIX) effectors from Fusarium oxysporum f. sp. lycopersici (Fol). The recognised effectors Avr1 (SIX4) and Avr3 (SIX1) represent the founding members of the Fol dual-domain (FOLD) effector class, with members containing two distinct domains. Using AlphaFold2, we predicted the full SIX effector repertoire of Fol and show that SIX6 and SIX13 are also FOLD effectors, which we validated experimentally for SIX6. Based on structural prediction and comparisons, we show that FOLD effectors are present within three divisions of fungi and are expanded in pathogens and symbionts. Further structural comparisons demonstrate that Fol secretes effectors that adopt a limited number of structural folds during infection of tomato. This analysis also revealed a structural relationship between transcriptionally co-regulated effector pairs. We make use of the Avr1 structure to understand its recognition by the I receptor, which leads to disease resistance in tomato. This study represents an important advance in our understanding of Fol-tomato, and by extension plant–fungal interactions, which will assist in the development of novel control and engineering strategies to combat plant pathogens.