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
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. C...
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| Format: | Article |
| Language: | English |
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BMC
2022-11-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-022-01442-9 |
| _version_ | 1828094971700314112 |
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| author | Mercedes Rocafort Joanna K. Bowen Berit Hassing Murray P. Cox Brogan McGreal Silvia de la Rosa Kim M. Plummer Rosie E. Bradshaw Carl H. Mesarich |
| author_facet | Mercedes Rocafort Joanna K. Bowen Berit Hassing Murray P. Cox Brogan McGreal Silvia de la Rosa Kim M. Plummer Rosie E. Bradshaw Carl H. Mesarich |
| author_sort | Mercedes Rocafort |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-11T07:06:34Z |
| format | Article |
| id | doaj.art-2660844a6e2941cbaf57f65a35c37829 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-11T07:06:34Z |
| publishDate | 2022-11-01 |
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| series | BMC Biology |
| spelling | doaj.art-2660844a6e2941cbaf57f65a35c378292022-12-22T04:38:23ZengBMCBMC Biology1741-70072022-11-0120112410.1186/s12915-022-01442-9The Venturia inaequalis effector repertoire is dominated by expanded families with predicted structural similarity, but unrelated sequence, to avirulence proteins from other plant-pathogenic fungiMercedes Rocafort0Joanna K. Bowen1Berit Hassing2Murray P. Cox3Brogan McGreal4Silvia de la Rosa5Kim M. Plummer6Rosie E. Bradshaw7Carl H. Mesarich8Laboratory of Molecular Plant Pathology/Bioprotection Aotearoa, School of Agriculture and Environment, Massey UniversityThe New Zealand Institute for Plant and Food Research Limited, Mount Albert Research CentreLaboratory of Molecular Plant Pathology/Bioprotection Aotearoa, School of Agriculture and Environment, Massey UniversityBioprotection Aotearoa, School of Natural Sciences, Massey UniversityThe New Zealand Institute for Plant and Food Research Limited, Mount Albert Research CentreLaboratory of Molecular Plant Pathology/Bioprotection Aotearoa, School of Agriculture and Environment, Massey UniversityDepartment of Animal, Plant and Soil Sciences, La Trobe University, AgriBio, Centre for AgriBiosciences, La Trobe UniversityBioprotection Aotearoa, School of Natural Sciences, Massey UniversityLaboratory of Molecular Plant Pathology/Bioprotection Aotearoa, School of Agriculture and Environment, Massey UniversityAbstract 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.https://doi.org/10.1186/s12915-022-01442-9Venturia inaequalisApple scab fungusBiotrophic subcuticular pathogenEffectors and effector familiesVirulence and avirulenceRNA-seq transcriptome |
| spellingShingle | Mercedes Rocafort Joanna K. Bowen Berit Hassing Murray P. Cox Brogan McGreal Silvia de la Rosa Kim M. Plummer Rosie E. Bradshaw Carl H. Mesarich 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 BMC Biology Venturia inaequalis Apple scab fungus Biotrophic subcuticular pathogen Effectors and effector families Virulence and avirulence RNA-seq transcriptome |
| title | 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 |
| title_full | 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 |
| title_fullStr | 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 |
| title_full_unstemmed | 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 |
| title_short | 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 |
| title_sort | venturia inaequalis effector repertoire is dominated by expanded families with predicted structural similarity but unrelated sequence to avirulence proteins from other plant pathogenic fungi |
| topic | Venturia inaequalis Apple scab fungus Biotrophic subcuticular pathogen Effectors and effector families Virulence and avirulence RNA-seq transcriptome |
| url | https://doi.org/10.1186/s12915-022-01442-9 |
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