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The Activation of Phytophthora Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b

Plant pathogens secrete an arsenal of effector proteins to impair host immunity. Some effectors possess enzymatic activities that can modify their host targets. Previously, we demonstrated that a Phytophthora sojae RXLR effector Avr3b acts as a Nudix hydrolase when expressed in planta; and this enzy...

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Autores principales: Kong, Guanghui, Zhao, Yao, Jing, Maofeng, Huang, Jie, Yang, Jin, Xia, Yeqiang, Kong, Liang, Ye, Wenwu, Xiong, Qin, Qiao, Yongli, Dong, Suomeng, Ma, Wenbo, Wang, Yuanchao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4552650/
https://www.ncbi.nlm.nih.gov/pubmed/26317500
http://dx.doi.org/10.1371/journal.ppat.1005139
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author Kong, Guanghui
Zhao, Yao
Jing, Maofeng
Huang, Jie
Yang, Jin
Xia, Yeqiang
Kong, Liang
Ye, Wenwu
Xiong, Qin
Qiao, Yongli
Dong, Suomeng
Ma, Wenbo
Wang, Yuanchao
author_facet Kong, Guanghui
Zhao, Yao
Jing, Maofeng
Huang, Jie
Yang, Jin
Xia, Yeqiang
Kong, Liang
Ye, Wenwu
Xiong, Qin
Qiao, Yongli
Dong, Suomeng
Ma, Wenbo
Wang, Yuanchao
author_sort Kong, Guanghui
collection PubMed
description Plant pathogens secrete an arsenal of effector proteins to impair host immunity. Some effectors possess enzymatic activities that can modify their host targets. Previously, we demonstrated that a Phytophthora sojae RXLR effector Avr3b acts as a Nudix hydrolase when expressed in planta; and this enzymatic activity is required for full virulence of P. sojae strain P6497 in soybean (Glycine max). Interestingly, recombinant Avr3b produced by E. coli does not have the hydrolase activity unless it was incubated with plant protein extracts. Here, we report the activation of Avr3b by a prolyl-peptidyl isomerase (PPIase), cyclophilin, in plant cells. Avr3b directly interacts with soybean cyclophilin GmCYP1, which activates the hydrolase activity of Avr3b in a PPIase activity-dependent manner. Avr3b contains a putative Glycine-Proline (GP) motif; which is known to confer cyclophilin-binding in other protein substrates. Substitution of the Proline (P132) in the putative GP motif impaired the interaction of Avr3b with GmCYP1; as a result, the mutant Avr3b(P132A) can no longer be activated by GmCYP1, and is also unable to promote Phytophthora infection. Avr3b elicits hypersensitive response (HR) in soybean cultivars producing the resistance protein Rps3b, but Avr3b(P132A) lost its ability to trigger HR. Furthermore, silencing of GmCYP1 rendered reduced cell death triggered by Avr3b, suggesting that GmCYP1-mediated Avr3b maturation is also required for Rps3b recognition. Finally, cyclophilins of Nicotiana benthamiana can also interact with Avr3b and activate its enzymatic activity. Overall, our results demonstrate that cyclophilin is a “helper” that activates the enzymatic activity of Avr3b after it is delivered into plant cells; as such, cyclophilin is required for the avirulence and virulence functions of Avr3b.
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spelling pubmed-45526502015-09-10 The Activation of Phytophthora Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b Kong, Guanghui Zhao, Yao Jing, Maofeng Huang, Jie Yang, Jin Xia, Yeqiang Kong, Liang Ye, Wenwu Xiong, Qin Qiao, Yongli Dong, Suomeng Ma, Wenbo Wang, Yuanchao PLoS Pathog Research Article Plant pathogens secrete an arsenal of effector proteins to impair host immunity. Some effectors possess enzymatic activities that can modify their host targets. Previously, we demonstrated that a Phytophthora sojae RXLR effector Avr3b acts as a Nudix hydrolase when expressed in planta; and this enzymatic activity is required for full virulence of P. sojae strain P6497 in soybean (Glycine max). Interestingly, recombinant Avr3b produced by E. coli does not have the hydrolase activity unless it was incubated with plant protein extracts. Here, we report the activation of Avr3b by a prolyl-peptidyl isomerase (PPIase), cyclophilin, in plant cells. Avr3b directly interacts with soybean cyclophilin GmCYP1, which activates the hydrolase activity of Avr3b in a PPIase activity-dependent manner. Avr3b contains a putative Glycine-Proline (GP) motif; which is known to confer cyclophilin-binding in other protein substrates. Substitution of the Proline (P132) in the putative GP motif impaired the interaction of Avr3b with GmCYP1; as a result, the mutant Avr3b(P132A) can no longer be activated by GmCYP1, and is also unable to promote Phytophthora infection. Avr3b elicits hypersensitive response (HR) in soybean cultivars producing the resistance protein Rps3b, but Avr3b(P132A) lost its ability to trigger HR. Furthermore, silencing of GmCYP1 rendered reduced cell death triggered by Avr3b, suggesting that GmCYP1-mediated Avr3b maturation is also required for Rps3b recognition. Finally, cyclophilins of Nicotiana benthamiana can also interact with Avr3b and activate its enzymatic activity. Overall, our results demonstrate that cyclophilin is a “helper” that activates the enzymatic activity of Avr3b after it is delivered into plant cells; as such, cyclophilin is required for the avirulence and virulence functions of Avr3b. Public Library of Science 2015-08-28 /pmc/articles/PMC4552650/ /pubmed/26317500 http://dx.doi.org/10.1371/journal.ppat.1005139 Text en © 2015 Kong et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Kong, Guanghui
Zhao, Yao
Jing, Maofeng
Huang, Jie
Yang, Jin
Xia, Yeqiang
Kong, Liang
Ye, Wenwu
Xiong, Qin
Qiao, Yongli
Dong, Suomeng
Ma, Wenbo
Wang, Yuanchao
The Activation of Phytophthora Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b
title The Activation of Phytophthora Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b
title_full The Activation of Phytophthora Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b
title_fullStr The Activation of Phytophthora Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b
title_full_unstemmed The Activation of Phytophthora Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b
title_short The Activation of Phytophthora Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b
title_sort activation of phytophthora effector avr3b by plant cyclophilin is required for the nudix hydrolase activity of avr3b
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4552650/
https://www.ncbi.nlm.nih.gov/pubmed/26317500
http://dx.doi.org/10.1371/journal.ppat.1005139
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