Cited by 52Plant Pathogens and Fungal DiseasesPlant Disease Resistance and GeneticsPlant-Microbe Interactions and Immunity

The Venturia inaequalis effector repertoire is dominated by expanded families with predicted structural similarity, but unrelated sequence, to avirulence proteins from other plant-pathogenic fungi

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Rocafort, Mercedes, Bowen, Joanna K., Hassing, Berit, Cox, Murray P., McGreal, Brogan, de la Rosa, Silvia, Plummer, Kim M., Bradshaw, Rosie E. +1 more·2022·BMC Biology

Published version of a preprint

Abstract

Background: Scab, caused by the biotrophic fungus Venturia inaequalis , is the most economically important disease of apples worldwide. During infection, V. inaequalis occupies the subcuticular environment, where it secretes virulence factors, termed effectors, to promote host colonization. Consistent with other plant-pathogenic fungi, many of these effectors are expected to be non-enzymatic proteins, some of which can be recognized by corresponding host resistance proteins to activate plant defences, thus acting as avirulence determinants. To develop durable control strategies against scab, a better understanding of the roles that these effector proteins play in promoting subcuticular growth by V. inaequalis , as well as in activating, suppressing, or circumventing resistance protein-mediated defences in apple, is required. Results: We generated the first comprehensive RNA-seq transcriptome of V. inaequalis during colonization of apple. Analysis of this transcriptome revealed five temporal waves of gene expression that peaked during early, mid, or mid-late infection. While the number of genes encoding secreted, non-enzymatic proteinaceous effector candidates (ECs) varied in each wave, most belonged to waves that peaked in expression during mid-late infection. Spectral clustering based on sequence similarity determined that the majority of ECs belonged to expanded protein families. To gain insights into function, the tertiary structures of ECs were predicted using AlphaFold2. Strikingly, despite an absence of sequence similarity, many ECs were predicted to have structural similarity to avirulence proteins from other plant-pathogenic fungi, including members of the MAX, LARS, ToxA and FOLD effector families. In addition, several other ECs, including an EC family with sequence similarity to the AvrLm6 avirulence effector from Leptosphaeria maculans , were predicted to adopt a KP6-like fold. Thus, proteins with a KP6-like fold represent another structural family of effectors shared among plant-pathogenic fungi. Conclusions: Our study reveals the transcriptomic profile underpinning subcuticular growth by V. inaequalis and provides an enriched list of ECs that can be investigated for roles in virulence and avirulence. Furthermore, our study supports the idea that numerous sequence-unrelated effectors across plant-pathogenic fungi share common structural folds. In doing so, our study gives weight to the hypothesis that many fungal effectors evolved from ancestral genes through duplication, followed by sequence diversification, to produce sequence-unrelated but structurally similar proteins.

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Authors
Rocafort, M., Bowen, J. K., Hassing, B., Cox, M. P., McGreal, B., de la Rosa, S., Plummer, K. M., Bradshaw, R. E., & Mesarich, C. H.
Affiliations
  • Massey University (NZ)
  • Plant & Food Research (NZ)
  • La Trobe University (AU)
Corresponding author
Mesarich, Carl H.
Venue
BMC Biology
Published
2022-11-03
Volume
20
Issue
1
Pages
246-246
ISSN
1741-7007 (ISSN-L)
OpenAlex
W4308496352
Cited by
52
References
180
Citations by year
2026: 7 · 2025: 15 · 2024: 13 · 2023: 12 · 2022: 5
FWCI
6.15
Type
journal article
Language
en
Open access
Locations
  • BMC Biology (publishedVersion, 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)
  • Figshare (submittedVersion, cc-by)
  • La Trobe University (cc-by)
Funders
Joint Genome Institute
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Plant Pathogens and Fungal Diseases
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Disease Resistance and Genetics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
Keywords
Venturia inaequalis, apple scab, effector repertoire, avirulence proteins, protein structural similarity, Leptosphaeria maculans, gene duplication
MeSH terms
Fungal Genus Venturia, Ascomycota, Plant Diseases, Malus

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