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Cell death triggering and effector recognition by Sw‐5 SD‐CNL proteins from resistant and susceptible tomato isolines to Tomato spotted wilt virus

Only a limited number of dominant resistance genes acting against plant viruses have been cloned, and further functional studies of these have been almost entirely limited to the resistance genes Rx against Potato virus X (PVX) and N against Tobacco mosaic virus (TMV). Recently, the cell‐to‐cell mov...

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Autores principales: De Oliveira, Athos Silva, Koolhaas, Ivo, Boiteux, Leonardo Silva, Caldararu, Octav F., Petrescu, Andrei‐Jose, Oliveira Resende, Renato, Kormelink, Richard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6638320/
https://www.ncbi.nlm.nih.gov/pubmed/27271212
http://dx.doi.org/10.1111/mpp.12439
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author De Oliveira, Athos Silva
Koolhaas, Ivo
Boiteux, Leonardo Silva
Caldararu, Octav F.
Petrescu, Andrei‐Jose
Oliveira Resende, Renato
Kormelink, Richard
author_facet De Oliveira, Athos Silva
Koolhaas, Ivo
Boiteux, Leonardo Silva
Caldararu, Octav F.
Petrescu, Andrei‐Jose
Oliveira Resende, Renato
Kormelink, Richard
author_sort De Oliveira, Athos Silva
collection PubMed
description Only a limited number of dominant resistance genes acting against plant viruses have been cloned, and further functional studies of these have been almost entirely limited to the resistance genes Rx against Potato virus X (PVX) and N against Tobacco mosaic virus (TMV). Recently, the cell‐to‐cell movement protein (NS(M)) of Tomato spotted wilt virus (TSWV) has been identified as the avirulence determinant (Avr) of Sw‐5b‐mediated resistance, a dominant resistance gene which belongs to the class of SD‐CC‐NB‐LRR (Solanaceae domain‐coiled coil‐nucleotide‐binding‐leucine‐rich repeat, SD‐CNL) resistance genes. On transient expression of the NS(M) protein in tomato and transgenic Nicotiana benthamiana harbouring the Sw‐5b gene, a hypersensitive cell death response (HR) is triggered. Here, it is shown that high accumulation of the Sw‐5b protein in N. benthamiana leaves, achieved by co‐expression of the Sw‐5b protein with RNA silencing suppressors (RSSs), leads to auto‐activity in the absence of NS(M). In a similar approach, Sw‐5a, the highest conserved paralogue of Sw‐5b from Solanum peruvianum, also triggered HR by auto‐activation, whereas the highest conserved orthologue from susceptible S. lycopersicum, named Sw‐5a(S), did not. However, neither of the last two homologues was able to trigger an NS(M)‐dependent HR. Truncated and mutated versions of these Sw‐5 proteins revealed that the NB‐ARC [nucleotide‐binding adaptor shared by Apaf‐1 (from humans), R proteins and CED‐4 (from nematodes)] domain is sufficient for the triggering of HR and seems to be suppressed by the SD‐CC domain. Furthermore, a single mutation was sufficient to restore auto‐activity within the NB‐ARC domain of Sw‐5a(S). When the latter domain was fused to the Sw‐5b LRR domain, NS(M)‐dependent HR triggering was regained, but not in the presence of its own Sw‐5a(S) LRR domain. Expression analysis in planta revealed a nucleocytoplasmic localization pattern of Sw‐5b, in which the SD‐CC domain seems to be required for nuclear translocation. Although the Sw‐5 N‐terminal CC domain, in contrast with Rx, contains an additional SD, most findings from this study support a conserved role of domains within NB‐LRR (NLR) proteins against plant viruses.
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spelling pubmed-66383202019-09-16 Cell death triggering and effector recognition by Sw‐5 SD‐CNL proteins from resistant and susceptible tomato isolines to Tomato spotted wilt virus De Oliveira, Athos Silva Koolhaas, Ivo Boiteux, Leonardo Silva Caldararu, Octav F. Petrescu, Andrei‐Jose Oliveira Resende, Renato Kormelink, Richard Mol Plant Pathol Original Articles Only a limited number of dominant resistance genes acting against plant viruses have been cloned, and further functional studies of these have been almost entirely limited to the resistance genes Rx against Potato virus X (PVX) and N against Tobacco mosaic virus (TMV). Recently, the cell‐to‐cell movement protein (NS(M)) of Tomato spotted wilt virus (TSWV) has been identified as the avirulence determinant (Avr) of Sw‐5b‐mediated resistance, a dominant resistance gene which belongs to the class of SD‐CC‐NB‐LRR (Solanaceae domain‐coiled coil‐nucleotide‐binding‐leucine‐rich repeat, SD‐CNL) resistance genes. On transient expression of the NS(M) protein in tomato and transgenic Nicotiana benthamiana harbouring the Sw‐5b gene, a hypersensitive cell death response (HR) is triggered. Here, it is shown that high accumulation of the Sw‐5b protein in N. benthamiana leaves, achieved by co‐expression of the Sw‐5b protein with RNA silencing suppressors (RSSs), leads to auto‐activity in the absence of NS(M). In a similar approach, Sw‐5a, the highest conserved paralogue of Sw‐5b from Solanum peruvianum, also triggered HR by auto‐activation, whereas the highest conserved orthologue from susceptible S. lycopersicum, named Sw‐5a(S), did not. However, neither of the last two homologues was able to trigger an NS(M)‐dependent HR. Truncated and mutated versions of these Sw‐5 proteins revealed that the NB‐ARC [nucleotide‐binding adaptor shared by Apaf‐1 (from humans), R proteins and CED‐4 (from nematodes)] domain is sufficient for the triggering of HR and seems to be suppressed by the SD‐CC domain. Furthermore, a single mutation was sufficient to restore auto‐activity within the NB‐ARC domain of Sw‐5a(S). When the latter domain was fused to the Sw‐5b LRR domain, NS(M)‐dependent HR triggering was regained, but not in the presence of its own Sw‐5a(S) LRR domain. Expression analysis in planta revealed a nucleocytoplasmic localization pattern of Sw‐5b, in which the SD‐CC domain seems to be required for nuclear translocation. Although the Sw‐5 N‐terminal CC domain, in contrast with Rx, contains an additional SD, most findings from this study support a conserved role of domains within NB‐LRR (NLR) proteins against plant viruses. John Wiley and Sons Inc. 2016-08-14 /pmc/articles/PMC6638320/ /pubmed/27271212 http://dx.doi.org/10.1111/mpp.12439 Text en © 2016 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
De Oliveira, Athos Silva
Koolhaas, Ivo
Boiteux, Leonardo Silva
Caldararu, Octav F.
Petrescu, Andrei‐Jose
Oliveira Resende, Renato
Kormelink, Richard
Cell death triggering and effector recognition by Sw‐5 SD‐CNL proteins from resistant and susceptible tomato isolines to Tomato spotted wilt virus
title Cell death triggering and effector recognition by Sw‐5 SD‐CNL proteins from resistant and susceptible tomato isolines to Tomato spotted wilt virus
title_full Cell death triggering and effector recognition by Sw‐5 SD‐CNL proteins from resistant and susceptible tomato isolines to Tomato spotted wilt virus
title_fullStr Cell death triggering and effector recognition by Sw‐5 SD‐CNL proteins from resistant and susceptible tomato isolines to Tomato spotted wilt virus
title_full_unstemmed Cell death triggering and effector recognition by Sw‐5 SD‐CNL proteins from resistant and susceptible tomato isolines to Tomato spotted wilt virus
title_short Cell death triggering and effector recognition by Sw‐5 SD‐CNL proteins from resistant and susceptible tomato isolines to Tomato spotted wilt virus
title_sort cell death triggering and effector recognition by sw‐5 sd‐cnl proteins from resistant and susceptible tomato isolines to tomato spotted wilt virus
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6638320/
https://www.ncbi.nlm.nih.gov/pubmed/27271212
http://dx.doi.org/10.1111/mpp.12439
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