PreprintCited by 64Plant-Microbe Interactions and ImmunityPlant Pathogens and Fungal DiseasesPlant Disease Resistance and Genetics

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The structural repertoire of Fusarium oxysporum f. sp. lycopersici effectors revealed by experimental and computational studies

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Preprint — published as 10.7554/elife.89280.3

Abstract

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 d ual-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 the development of novel control and engineering strategies to combat plant pathogens.

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Metadata

Authors
Yu, D. S., Outram, M. A., Smith, A., McCombe, C. L., Khambalkar, P. B., Rima, S. A., Sun, X., Ma, L., Ericsson, D. J., Jones, D. A., & Williams, S. J.
Affiliations
  • Australian National University (AU)
  • Hebei Agricultural University (CN)
Corresponding author
  • Outram, Megan A.
  • Williams, Simon J.
Venue
eLife
Publisher
openRxiv
Published
2021-12-15
Volume
12
ISSN
2050-084X (ISSN-L)
OpenAlex
W4384693301
Cited by
64
References
1
Citations by year
2026: 13 · 2025: 27 · 2024: 11 · 2023: 8 · 2022: 5
FWCI
9.30
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • eLife (publishedVersion, cc-by)
  • eLife (acceptedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Australian Nuclear Science and Technology Organisation
  • ICAR - National Agricultural Science Fund
  • Australian Cancer Research Foundation
  • Australian Academy of Science
  • Australian National University
  • Australian Institute of Nuclear Science and Engineering
  • Australian Synchrotron
  • Indian Council of Agricultural Research
  • Australian Research Council (DE170101165, DP200100388, FT200100135)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Pathogens and Fungal Diseases
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Disease Resistance and Genetics
Keywords
Fusarium oxysporum f. sp. lycopersici, fungal effectors, disease resistance, tomato, plant-fungal interactions
MeSH terms
Biological Transport, Cell Membrane, Fusarium, Crystallography, X-Ray, Solanum lycopersicum, Disease Resistance

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