The tRNA thiolation-mediated translational control is essential for plant immunity

Plants have evolved sophisticated mechanisms to regulate gene expression to activate immune responses against pathogen infections. However, how the translation system contributes to plant immunity is largely unknown. The evolutionarily conserved thiolation modification of transfer RNA (tRNA) ensures...

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Main Authors: Xueao Zheng, Hanchen Chen, Zhiping Deng, Yujing Wu, Linlin Zhong, Chong Wu, Xiaodan Yu, Qiansi Chen, Shunping Yan
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/93517
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author Xueao Zheng
Hanchen Chen
Zhiping Deng
Yujing Wu
Linlin Zhong
Chong Wu
Xiaodan Yu
Qiansi Chen
Shunping Yan
author_facet Xueao Zheng
Hanchen Chen
Zhiping Deng
Yujing Wu
Linlin Zhong
Chong Wu
Xiaodan Yu
Qiansi Chen
Shunping Yan
author_sort Xueao Zheng
collection DOAJ
description Plants have evolved sophisticated mechanisms to regulate gene expression to activate immune responses against pathogen infections. However, how the translation system contributes to plant immunity is largely unknown. The evolutionarily conserved thiolation modification of transfer RNA (tRNA) ensures efficient decoding during translation. Here, we show that tRNA thiolation is required for plant immunity in Arabidopsis. We identify a cgb mutant that is hyper-susceptible to the pathogen Pseudomonas syringae. CGB encodes ROL5, a homolog of yeast NCS6 required for tRNA thiolation. ROL5 physically interacts with CTU2, a homolog of yeast NCS2. Mutations in either ROL5 or CTU2 result in loss of tRNA thiolation. Further analyses reveal that both transcriptome and proteome reprogramming during immune responses are compromised in cgb. Notably, the translation of salicylic acid receptor NPR1 is reduced in cgb, resulting in compromised salicylic acid signaling. Our study not only reveals a regulatory mechanism for plant immunity but also uncovers an additional biological function of tRNA thiolation.
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spelling doaj.art-7b86e34db196453dacb6ac993a188fa82024-02-13T15:30:41ZengeLife Sciences Publications LtdeLife2050-084X2024-01-011310.7554/eLife.93517The tRNA thiolation-mediated translational control is essential for plant immunityXueao Zheng0https://orcid.org/0000-0001-6204-7611Hanchen Chen1https://orcid.org/0009-0004-5323-6989Zhiping Deng2https://orcid.org/0000-0001-9663-3088Yujing Wu3Linlin Zhong4https://orcid.org/0000-0003-1908-1413Chong Wu5Xiaodan Yu6Qiansi Chen7https://orcid.org/0000-0003-2800-5703Shunping Yan8https://orcid.org/0000-0002-3665-1310Hubei Hongshan Laboratory, Wuhan, China; Zhengzhou Tobacco Research Institute of CNTC, Zhengzhou, China; College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China; Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Shenzhen, China; Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China; Shenzhen Institute of Nutrition and Health, Huazhong Agricultural University, Shenzhen, ChinaHubei Hongshan Laboratory, Wuhan, China; College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China; Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Shenzhen, China; Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China; Shenzhen Institute of Nutrition and Health, Huazhong Agricultural University, Shenzhen, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaHubei Hongshan Laboratory, Wuhan, China; College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China; Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Shenzhen, China; Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China; Shenzhen Institute of Nutrition and Health, Huazhong Agricultural University, Shenzhen, ChinaKey Laboratory of Horticultural Plant Biology, Ministry of Education, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, ChinaHubei Hongshan Laboratory, Wuhan, China; College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China; Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Shenzhen, China; Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China; Shenzhen Institute of Nutrition and Health, Huazhong Agricultural University, Shenzhen, ChinaHubei Hongshan Laboratory, Wuhan, China; College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China; Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Shenzhen, China; Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China; Shenzhen Institute of Nutrition and Health, Huazhong Agricultural University, Shenzhen, ChinaZhengzhou Tobacco Research Institute of CNTC, Zhengzhou, ChinaHubei Hongshan Laboratory, Wuhan, China; College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China; Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Shenzhen, China; Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China; Shenzhen Institute of Nutrition and Health, Huazhong Agricultural University, Shenzhen, ChinaPlants have evolved sophisticated mechanisms to regulate gene expression to activate immune responses against pathogen infections. However, how the translation system contributes to plant immunity is largely unknown. The evolutionarily conserved thiolation modification of transfer RNA (tRNA) ensures efficient decoding during translation. Here, we show that tRNA thiolation is required for plant immunity in Arabidopsis. We identify a cgb mutant that is hyper-susceptible to the pathogen Pseudomonas syringae. CGB encodes ROL5, a homolog of yeast NCS6 required for tRNA thiolation. ROL5 physically interacts with CTU2, a homolog of yeast NCS2. Mutations in either ROL5 or CTU2 result in loss of tRNA thiolation. Further analyses reveal that both transcriptome and proteome reprogramming during immune responses are compromised in cgb. Notably, the translation of salicylic acid receptor NPR1 is reduced in cgb, resulting in compromised salicylic acid signaling. Our study not only reveals a regulatory mechanism for plant immunity but also uncovers an additional biological function of tRNA thiolation.https://elifesciences.org/articles/93517plant immunitytranslationtRNA thiolationNPR1Arabidopsis
spellingShingle Xueao Zheng
Hanchen Chen
Zhiping Deng
Yujing Wu
Linlin Zhong
Chong Wu
Xiaodan Yu
Qiansi Chen
Shunping Yan
The tRNA thiolation-mediated translational control is essential for plant immunity
eLife
plant immunity
translation
tRNA thiolation
NPR1
Arabidopsis
title The tRNA thiolation-mediated translational control is essential for plant immunity
title_full The tRNA thiolation-mediated translational control is essential for plant immunity
title_fullStr The tRNA thiolation-mediated translational control is essential for plant immunity
title_full_unstemmed The tRNA thiolation-mediated translational control is essential for plant immunity
title_short The tRNA thiolation-mediated translational control is essential for plant immunity
title_sort trna thiolation mediated translational control is essential for plant immunity
topic plant immunity
translation
tRNA thiolation
NPR1
Arabidopsis
url https://elifesciences.org/articles/93517
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