RNAi-Based Gene Silencing of RXLR Effectors Protects Plants Against the Oomycete Pathogen Phytophthora capsici

Phytophthora capsici is a broad–host range oomycete pathogen that can cause severe phytophthora blight disease of pepper and hundreds of other plant species worldwide. Natural resistance against P. capsici is inadequate, and it is very difficult to control by most of existing chemical fungicides. Th...

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Main Authors: Wei Cheng, Menglan Lin, Moli Chu, Guixiang Xiang, Jianwen Guo, Yan Jiang, Deyi Guan, Shuilin He
Format: Article
Language:English
Published: The American Phytopathological Society 2022-06-01
Series:Molecular Plant-Microbe Interactions
Subjects:
Online Access:https://apsjournals.apsnet.org/doi/10.1094/MPMI-12-21-0295-R
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author Wei Cheng
Menglan Lin
Moli Chu
Guixiang Xiang
Jianwen Guo
Yan Jiang
Deyi Guan
Shuilin He
author_facet Wei Cheng
Menglan Lin
Moli Chu
Guixiang Xiang
Jianwen Guo
Yan Jiang
Deyi Guan
Shuilin He
author_sort Wei Cheng
collection DOAJ
description Phytophthora capsici is a broad–host range oomycete pathogen that can cause severe phytophthora blight disease of pepper and hundreds of other plant species worldwide. Natural resistance against P. capsici is inadequate, and it is very difficult to control by most of existing chemical fungicides. Therefore, it is urgent to develop alternative strategies to control this pathogen. Recently, host-induced or spray-induced gene silencing of essential or virulent pathogen genes provided an effective strategy for disease controls. Here, we demonstrate that P. capsici can effectively take up small interfering RNAs (siRNAs) from the environment. According to RNA-seq and quantitative reverse transcription PCR analysis, we identified four P. capsici RXLR effector genes that are significantly up-regulated during the infection stage. Transient overexpression and promote-infection assays indicated that RXLR1 and RXLR4 could promote pathogen infection. Using a virus-induced gene silencing system in pepper plants, we found that in planta–expressing RNA interference (RNAi) constructs that target RXLR1 or RXLR4 could significantly reduce pathogen infection, while co-interfering RXLR1 and RXLR4 could confer a more enhanced resistance to P. capsici. We also found that exogenously applying siRNAs that target RXLR1 or RXLR4 could restrict growth of P. capsici on the pepper and Nicotiana benthamiana leaves; when targeting RXLR1 and RXLR4 simultaneously, the control effect was more remarkable. These data suggested that RNAi-based gene silencing of RXLR effectors has great potential for application in crop improvement against P. capsici and also provides an important basis for the development of RNA-based antioomycete agents.[Graphic: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
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spelling doaj.art-26c2e1f780ef4dbd83837944897330c12022-12-22T00:37:34ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062022-06-0135644044910.1094/MPMI-12-21-0295-RRNAi-Based Gene Silencing of RXLR Effectors Protects Plants Against the Oomycete Pathogen Phytophthora capsiciWei Cheng0Menglan Lin1Moli Chu2Guixiang Xiang3Jianwen Guo4Yan Jiang5Deyi Guan6Shuilin He7Anhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources/College of Life Sciences, Anhui Normal University, Wuhu, Anhui 241000, ChinaNational Education Minister Key Laboratory of Plant Genetic Improvement and Comprehensive Utilization/College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou, Fujian 350002, ChinaAnhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources/College of Life Sciences, Anhui Normal University, Wuhu, Anhui 241000, ChinaNational Education Minister Key Laboratory of Plant Genetic Improvement and Comprehensive Utilization/College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou, Fujian 350002, ChinaNational Education Minister Key Laboratory of Plant Genetic Improvement and Comprehensive Utilization/College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou, Fujian 350002, ChinaNational Education Minister Key Laboratory of Plant Genetic Improvement and Comprehensive Utilization/College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou, Fujian 350002, ChinaNational Education Minister Key Laboratory of Plant Genetic Improvement and Comprehensive Utilization/College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou, Fujian 350002, ChinaNational Education Minister Key Laboratory of Plant Genetic Improvement and Comprehensive Utilization/College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou, Fujian 350002, ChinaPhytophthora capsici is a broad–host range oomycete pathogen that can cause severe phytophthora blight disease of pepper and hundreds of other plant species worldwide. Natural resistance against P. capsici is inadequate, and it is very difficult to control by most of existing chemical fungicides. Therefore, it is urgent to develop alternative strategies to control this pathogen. Recently, host-induced or spray-induced gene silencing of essential or virulent pathogen genes provided an effective strategy for disease controls. Here, we demonstrate that P. capsici can effectively take up small interfering RNAs (siRNAs) from the environment. According to RNA-seq and quantitative reverse transcription PCR analysis, we identified four P. capsici RXLR effector genes that are significantly up-regulated during the infection stage. Transient overexpression and promote-infection assays indicated that RXLR1 and RXLR4 could promote pathogen infection. Using a virus-induced gene silencing system in pepper plants, we found that in planta–expressing RNA interference (RNAi) constructs that target RXLR1 or RXLR4 could significantly reduce pathogen infection, while co-interfering RXLR1 and RXLR4 could confer a more enhanced resistance to P. capsici. We also found that exogenously applying siRNAs that target RXLR1 or RXLR4 could restrict growth of P. capsici on the pepper and Nicotiana benthamiana leaves; when targeting RXLR1 and RXLR4 simultaneously, the control effect was more remarkable. These data suggested that RNAi-based gene silencing of RXLR effectors has great potential for application in crop improvement against P. capsici and also provides an important basis for the development of RNA-based antioomycete agents.[Graphic: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/MPMI-12-21-0295-RCapsicum annuumeffectorgene silencingNicotiana benthamianaPhytophthoraRNAi
spellingShingle Wei Cheng
Menglan Lin
Moli Chu
Guixiang Xiang
Jianwen Guo
Yan Jiang
Deyi Guan
Shuilin He
RNAi-Based Gene Silencing of RXLR Effectors Protects Plants Against the Oomycete Pathogen Phytophthora capsici
Molecular Plant-Microbe Interactions
Capsicum annuum
effector
gene silencing
Nicotiana benthamiana
Phytophthora
RNAi
title RNAi-Based Gene Silencing of RXLR Effectors Protects Plants Against the Oomycete Pathogen Phytophthora capsici
title_full RNAi-Based Gene Silencing of RXLR Effectors Protects Plants Against the Oomycete Pathogen Phytophthora capsici
title_fullStr RNAi-Based Gene Silencing of RXLR Effectors Protects Plants Against the Oomycete Pathogen Phytophthora capsici
title_full_unstemmed RNAi-Based Gene Silencing of RXLR Effectors Protects Plants Against the Oomycete Pathogen Phytophthora capsici
title_short RNAi-Based Gene Silencing of RXLR Effectors Protects Plants Against the Oomycete Pathogen Phytophthora capsici
title_sort rnai based gene silencing of rxlr effectors protects plants against the oomycete pathogen phytophthora capsici
topic Capsicum annuum
effector
gene silencing
Nicotiana benthamiana
Phytophthora
RNAi
url https://apsjournals.apsnet.org/doi/10.1094/MPMI-12-21-0295-R
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