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Stepwise artificial evolution of an Sw‐5b immune receptor extends its resistance spectrum against resistance‐breaking isolates of Tomato spotted wilt virus

Plants use intracellular nucleotide‐binding leucine‐rich repeat immune receptors (NLRs) to recognize pathogen‐encoded effectors and initiate immune responses. Tomato spotted wilt virus (TSWV), which has been found to infect >1000 plant species, is among the most destructive plant viruses worldwid...

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Autores principales: Huang, Haining, Huang, Shen, Li, Jia, Wang, Huiyuan, Zhao, Yaqian, Feng, Mingfeng, Dai, Jing, Wang, Tongkai, Zhu, Min, Tao, Xiaorong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8541788/
https://www.ncbi.nlm.nih.gov/pubmed/34036713
http://dx.doi.org/10.1111/pbi.13641
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author Huang, Haining
Huang, Shen
Li, Jia
Wang, Huiyuan
Zhao, Yaqian
Feng, Mingfeng
Dai, Jing
Wang, Tongkai
Zhu, Min
Tao, Xiaorong
author_facet Huang, Haining
Huang, Shen
Li, Jia
Wang, Huiyuan
Zhao, Yaqian
Feng, Mingfeng
Dai, Jing
Wang, Tongkai
Zhu, Min
Tao, Xiaorong
author_sort Huang, Haining
collection PubMed
description Plants use intracellular nucleotide‐binding leucine‐rich repeat immune receptors (NLRs) to recognize pathogen‐encoded effectors and initiate immune responses. Tomato spotted wilt virus (TSWV), which has been found to infect >1000 plant species, is among the most destructive plant viruses worldwide. The Sw‐5b is the most effective and widely used resistance gene in tomato breeding to control TSWV. However, broad application of tomato cultivars carrying Sw‐5b has resulted in an emergence of resistance‐breaking (RB) TSWV. Therefore, new effective genes are urgently needed to prevent further RB TSWV outbreaks. In this study, we conducted artificial evolution to select Sw‐5b mutants that could extend the resistance spectrum against TSWV RB isolates. Unlike regular NLRs, Sw‐5b detects viral elicitor NSm using both the N‐terminal Solanaceae‐specific domain (SD) and the C‐terminal LRR domain in a two‐step recognition process. Our attempts to select gain‐of‐function mutants by random mutagenesis involving either the SD or the LRR of Sw‐5b failed; therefore, we adopted a stepwise strategy, first introducing a NSm(RB)‐responsive mutation at the R927 residue in the LRR, followed by random mutagenesis involving the Sw‐5b SD domain. Using this strategy, we obtained Sw‐5b(L33P/K319E/R927A) and Sw‐5b(L33P/K319E/R927Q) mutants, which are effective against TSWV RB carrying the NSm(C118Y) or NSm(T120N) mutation, and against other American‐type tospoviruses. Thus, we were able to extend the resistance spectrum of Sw‐5b; the selected Sw‐5b mutants will provide new gene resources to control RB TSWV.
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spelling pubmed-85417882021-10-29 Stepwise artificial evolution of an Sw‐5b immune receptor extends its resistance spectrum against resistance‐breaking isolates of Tomato spotted wilt virus Huang, Haining Huang, Shen Li, Jia Wang, Huiyuan Zhao, Yaqian Feng, Mingfeng Dai, Jing Wang, Tongkai Zhu, Min Tao, Xiaorong Plant Biotechnol J Research Articles Plants use intracellular nucleotide‐binding leucine‐rich repeat immune receptors (NLRs) to recognize pathogen‐encoded effectors and initiate immune responses. Tomato spotted wilt virus (TSWV), which has been found to infect >1000 plant species, is among the most destructive plant viruses worldwide. The Sw‐5b is the most effective and widely used resistance gene in tomato breeding to control TSWV. However, broad application of tomato cultivars carrying Sw‐5b has resulted in an emergence of resistance‐breaking (RB) TSWV. Therefore, new effective genes are urgently needed to prevent further RB TSWV outbreaks. In this study, we conducted artificial evolution to select Sw‐5b mutants that could extend the resistance spectrum against TSWV RB isolates. Unlike regular NLRs, Sw‐5b detects viral elicitor NSm using both the N‐terminal Solanaceae‐specific domain (SD) and the C‐terminal LRR domain in a two‐step recognition process. Our attempts to select gain‐of‐function mutants by random mutagenesis involving either the SD or the LRR of Sw‐5b failed; therefore, we adopted a stepwise strategy, first introducing a NSm(RB)‐responsive mutation at the R927 residue in the LRR, followed by random mutagenesis involving the Sw‐5b SD domain. Using this strategy, we obtained Sw‐5b(L33P/K319E/R927A) and Sw‐5b(L33P/K319E/R927Q) mutants, which are effective against TSWV RB carrying the NSm(C118Y) or NSm(T120N) mutation, and against other American‐type tospoviruses. Thus, we were able to extend the resistance spectrum of Sw‐5b; the selected Sw‐5b mutants will provide new gene resources to control RB TSWV. John Wiley and Sons Inc. 2021-06-07 2021-11 /pmc/articles/PMC8541788/ /pubmed/34036713 http://dx.doi.org/10.1111/pbi.13641 Text en © 2021 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Research Articles
Huang, Haining
Huang, Shen
Li, Jia
Wang, Huiyuan
Zhao, Yaqian
Feng, Mingfeng
Dai, Jing
Wang, Tongkai
Zhu, Min
Tao, Xiaorong
Stepwise artificial evolution of an Sw‐5b immune receptor extends its resistance spectrum against resistance‐breaking isolates of Tomato spotted wilt virus
title Stepwise artificial evolution of an Sw‐5b immune receptor extends its resistance spectrum against resistance‐breaking isolates of Tomato spotted wilt virus
title_full Stepwise artificial evolution of an Sw‐5b immune receptor extends its resistance spectrum against resistance‐breaking isolates of Tomato spotted wilt virus
title_fullStr Stepwise artificial evolution of an Sw‐5b immune receptor extends its resistance spectrum against resistance‐breaking isolates of Tomato spotted wilt virus
title_full_unstemmed Stepwise artificial evolution of an Sw‐5b immune receptor extends its resistance spectrum against resistance‐breaking isolates of Tomato spotted wilt virus
title_short Stepwise artificial evolution of an Sw‐5b immune receptor extends its resistance spectrum against resistance‐breaking isolates of Tomato spotted wilt virus
title_sort stepwise artificial evolution of an sw‐5b immune receptor extends its resistance spectrum against resistance‐breaking isolates of tomato spotted wilt virus
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8541788/
https://www.ncbi.nlm.nih.gov/pubmed/34036713
http://dx.doi.org/10.1111/pbi.13641
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