Comparative genomics reveals the in planta-secreted Verticillium dahliae Av2 effector protein recognized in tomato plants that carry the V2 resistance locus

Edgar A Chavarro-Carrero; Jasper P Vermeulen; David E Torres; Toshiyuki Usami; Henk J Schouten; Yuling Bai; Michael F Seidl; Bart P H J Thomma

doi:10.1111/1462-2920.15288

Comparative genomics reveals the in planta-secreted Verticillium dahliae Av2 effector protein recognized in tomato plants that carry the V2 resistance locus

Edgar A Chavarro-Carrero, Jasper P Vermeulen, David E Torres, Toshiyuki Usami, Henk J Schouten, Yuling Bai, Michael F Seidl, Bart P H J Thomma

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Plant pathogens secrete effector molecules during host invasion to promote colonization. However, some of these effectors become recognized by host receptors to mount a defence response and establish immunity. Recently, a novel resistance was identified in wild tomato, mediated by the single dominant V2 locus, to control strains of the soil-borne vascular wilt fungus Verticillium dahliae that belong to race 2. With comparative genomics of race 2 strains and resistance-breaking race 3 strains, we identified the avirulence effector that activates V2 resistance, termed Av2. We identified 277 kb of race 2-specific sequence comprising only two genes encoding predicted secreted proteins that are expressed during tomato colonization. Subsequent functional analysis based on genetic complementation into race 3 isolates and targeted deletion from the race 1 isolate JR2 and race 2 isolate TO22 confirmed that one of the two candidates encodes the avirulence effector Av2 that is recognized in V2 tomato plants. Two Av2 allelic variants were identified that encode Av2 variants that differ by a single acid. Thus far, a role in virulence could not be demonstrated for either of the two variants.

Original language	English
Pages (from-to)	1941-1958
Number of pages	18
Journal	Environmental Microbiology
Volume	23
Issue number	4
Early online date	2020
DOIs	https://doi.org/10.1111/1462-2920.15288
Publication status	Published - Apr 2021

Bibliographical note

Funding Information:
E.A.C.C. and D.T. acknowledge receipt of PhD fellowships from CONACyT. Work in the laboratories of B.P.H.J.T. and M.F.S. is supported by the Research Council for Earth and Life Science (ALW) of the Netherlands Organization for Scientific Research (NWO). B.P.H.J.T. acknowledges support by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany's Excellence Strategy – EXC 2048/1 – Project ID: 390686111. Part of the work was funded by Foundation Topconsortium voor Kennis en Innovatie (TKI) Starting Materials, project number 1409‐026.

Funding Information:
E.A.C.C. and D.T. acknowledge receipt of PhD fellowships from CONACyT. Work in the laboratories of B.P.H.J.T. and M.F.S. is supported by the Research Council for Earth and Life Science (ALW) of the Netherlands Organization for Scientific Research (NWO). B.P.H.J.T. acknowledges support by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany's Excellence Strategy ? EXC 2048/1 ? Project ID: 390686111. Part of the work was funded by Foundation Topconsortium voor Kennis en Innovatie (TKI) Starting Materials, project number 1409-026.

Publisher Copyright:
© 2020 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.

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1462-2920.15288Final published version, 4.99 MBLicence: CC BY

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Chavarro-Carrero, E. A., Vermeulen, J. P., E Torres, D., Usami, T., Schouten, H. J., Bai, Y., Seidl, M. F., & Thomma, B. P. H. J. (2021). Comparative genomics reveals the in planta-secreted Verticillium dahliae Av2 effector protein recognized in tomato plants that carry the V2 resistance locus. Environmental Microbiology, 23(4), 1941-1958. https://doi.org/10.1111/1462-2920.15288

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title = "Comparative genomics reveals the in planta-secreted Verticillium dahliae Av2 effector protein recognized in tomato plants that carry the V2 resistance locus",

abstract = "Plant pathogens secrete effector molecules during host invasion to promote colonization. However, some of these effectors become recognized by host receptors to mount a defence response and establish immunity. Recently, a novel resistance was identified in wild tomato, mediated by the single dominant V2 locus, to control strains of the soil-borne vascular wilt fungus Verticillium dahliae that belong to race 2. With comparative genomics of race 2 strains and resistance-breaking race 3 strains, we identified the avirulence effector that activates V2 resistance, termed Av2. We identified 277 kb of race 2-specific sequence comprising only two genes encoding predicted secreted proteins that are expressed during tomato colonization. Subsequent functional analysis based on genetic complementation into race 3 isolates and targeted deletion from the race 1 isolate JR2 and race 2 isolate TO22 confirmed that one of the two candidates encodes the avirulence effector Av2 that is recognized in V2 tomato plants. Two Av2 allelic variants were identified that encode Av2 variants that differ by a single acid. Thus far, a role in virulence could not be demonstrated for either of the two variants.",

author = "Chavarro-Carrero, {Edgar A} and Vermeulen, {Jasper P} and {E Torres}, David and Toshiyuki Usami and Schouten, {Henk J} and Yuling Bai and Seidl, {Michael F} and Thomma, {Bart P H J}",

note = "Funding Information: E.A.C.C. and D.T. acknowledge receipt of PhD fellowships from CONACyT. Work in the laboratories of B.P.H.J.T. and M.F.S. is supported by the Research Council for Earth and Life Science (ALW) of the Netherlands Organization for Scientific Research (NWO). B.P.H.J.T. acknowledges support by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany's Excellence Strategy – EXC 2048/1 – Project ID: 390686111. Part of the work was funded by Foundation Topconsortium voor Kennis en Innovatie (TKI) Starting Materials, project number 1409‐026. Funding Information: E.A.C.C. and D.T. acknowledge receipt of PhD fellowships from CONACyT. Work in the laboratories of B.P.H.J.T. and M.F.S. is supported by the Research Council for Earth and Life Science (ALW) of the Netherlands Organization for Scientific Research (NWO). B.P.H.J.T. acknowledges support by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany's Excellence Strategy ? EXC 2048/1 ? Project ID: 390686111. Part of the work was funded by Foundation Topconsortium voor Kennis en Innovatie (TKI) Starting Materials, project number 1409-026. Publisher Copyright: {\textcopyright} 2020 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.",

year = "2021",

month = apr,

doi = "10.1111/1462-2920.15288",

language = "English",

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Chavarro-Carrero, EA, Vermeulen, JP, E Torres, D, Usami, T, Schouten, HJ, Bai, Y, Seidl, MF & Thomma, BPHJ 2021, 'Comparative genomics reveals the in planta-secreted Verticillium dahliae Av2 effector protein recognized in tomato plants that carry the V2 resistance locus', Environmental Microbiology, vol. 23, no. 4, pp. 1941-1958. https://doi.org/10.1111/1462-2920.15288

Comparative genomics reveals the in planta-secreted Verticillium dahliae Av2 effector protein recognized in tomato plants that carry the V2 resistance locus. / Chavarro-Carrero, Edgar A; Vermeulen, Jasper P; E Torres, David et al.
In: Environmental Microbiology, Vol. 23, No. 4, 04.2021, p. 1941-1958.

Research output: Contribution to journal › Article › Academic › peer-review

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N2 - Plant pathogens secrete effector molecules during host invasion to promote colonization. However, some of these effectors become recognized by host receptors to mount a defence response and establish immunity. Recently, a novel resistance was identified in wild tomato, mediated by the single dominant V2 locus, to control strains of the soil-borne vascular wilt fungus Verticillium dahliae that belong to race 2. With comparative genomics of race 2 strains and resistance-breaking race 3 strains, we identified the avirulence effector that activates V2 resistance, termed Av2. We identified 277 kb of race 2-specific sequence comprising only two genes encoding predicted secreted proteins that are expressed during tomato colonization. Subsequent functional analysis based on genetic complementation into race 3 isolates and targeted deletion from the race 1 isolate JR2 and race 2 isolate TO22 confirmed that one of the two candidates encodes the avirulence effector Av2 that is recognized in V2 tomato plants. Two Av2 allelic variants were identified that encode Av2 variants that differ by a single acid. Thus far, a role in virulence could not be demonstrated for either of the two variants.

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Comparative genomics reveals the in planta-secreted Verticillium dahliae Av2 effector protein recognized in tomato plants that carry the V2 resistance locus

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