Heat-inducible SlWRKY3 confers thermotolerance by activating the SlGRXS1 gene cluster in tomato

High temperature stress is one of the major environmental factors that affect the growth and development of plants. Although WRKY transcription factors play a critical role in stress responses, there are few studies on the regulation of heat stress by WRKY transcription factors, especially in tomato...

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Main Authors: Ying Wang, Wenxian Gai, Liangdan Yuan, Lele Shang, Fangman Li, Zhao Gong, Pingfei Ge, Yaru Wang, Jinbao Tao, Xingyu Zhang, Haiqiang Dong, Yuyang Zhang
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2024-03-01
Series:Horticultural Plant Journal
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2468014122001443
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author Ying Wang
Wenxian Gai
Liangdan Yuan
Lele Shang
Fangman Li
Zhao Gong
Pingfei Ge
Yaru Wang
Jinbao Tao
Xingyu Zhang
Haiqiang Dong
Yuyang Zhang
author_facet Ying Wang
Wenxian Gai
Liangdan Yuan
Lele Shang
Fangman Li
Zhao Gong
Pingfei Ge
Yaru Wang
Jinbao Tao
Xingyu Zhang
Haiqiang Dong
Yuyang Zhang
author_sort Ying Wang
collection DOAJ
description High temperature stress is one of the major environmental factors that affect the growth and development of plants. Although WRKY transcription factors play a critical role in stress responses, there are few studies on the regulation of heat stress by WRKY transcription factors, especially in tomato. Here, we identified a group I WRKY transcription factor, SlWRKY3, involved in thermotolerance in tomato. First, SlWRKY3 was induced and upregulated under heat stress. Accordingly, overexpression of SlWRKY3 led to an increase, whereas knock-out of SlWRKY3 resulted in decreased tolerance to heat stress. Overexpression of SlWRKY3 accumulated less reactive oxygen species (ROS), whereas knock-out of SlWRKY3 accumulated more ROS under heat stress. This indicated that SlWRKY3 positively regulates heat stress in tomato. In addition, SlWRKY3 activated the expression of a range of abiotic stress-responsive genes involved in ROS scavenging, such as a SlGRXS1 gene cluster. Further analysis showed that SlWRKY3 can bind to the promoters of the SlGRXS1 gene cluster and activate their expression. Collectively, these results imply that SlWRKY3 is a positive regulator of thermotolerance through direct binding to the promoters of the SlGRXS1 gene cluster and activating their expression and ROS scavenging.
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spelling doaj.art-0d47009e7d2740ae94ee5485d02bfd2d2024-03-07T05:28:44ZengKeAi Communications Co., Ltd.Horticultural Plant Journal2468-01412024-03-01102515531Heat-inducible SlWRKY3 confers thermotolerance by activating the SlGRXS1 gene cluster in tomatoYing Wang0Wenxian Gai1Liangdan Yuan2Lele Shang3Fangman Li4Zhao Gong5Pingfei Ge6Yaru Wang7Jinbao Tao8Xingyu Zhang9Haiqiang Dong10Yuyang Zhang11National Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, Huazhong Agricultural University, Wuhan, Hubei 430070, ChinaNational Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, Huazhong Agricultural University, Wuhan, Hubei 430070, ChinaNational Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, Huazhong Agricultural University, Wuhan, Hubei 430070, ChinaNational Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, Huazhong Agricultural University, Wuhan, Hubei 430070, ChinaNational Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, Huazhong Agricultural University, Wuhan, Hubei 430070, ChinaNational Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, Huazhong Agricultural University, Wuhan, Hubei 430070, ChinaNational Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, Huazhong Agricultural University, Wuhan, Hubei 430070, ChinaNational Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, Huazhong Agricultural University, Wuhan, Hubei 430070, ChinaNational Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, Huazhong Agricultural University, Wuhan, Hubei 430070, ChinaNational Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, Huazhong Agricultural University, Wuhan, Hubei 430070, ChinaNational Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, Huazhong Agricultural University, Wuhan, Hubei 430070, ChinaNational Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Hubei Hongshan Laboratory, Wuhan, Hubei 430070, China; Corresponding author. Tel.: +86 27 87282010.High temperature stress is one of the major environmental factors that affect the growth and development of plants. Although WRKY transcription factors play a critical role in stress responses, there are few studies on the regulation of heat stress by WRKY transcription factors, especially in tomato. Here, we identified a group I WRKY transcription factor, SlWRKY3, involved in thermotolerance in tomato. First, SlWRKY3 was induced and upregulated under heat stress. Accordingly, overexpression of SlWRKY3 led to an increase, whereas knock-out of SlWRKY3 resulted in decreased tolerance to heat stress. Overexpression of SlWRKY3 accumulated less reactive oxygen species (ROS), whereas knock-out of SlWRKY3 accumulated more ROS under heat stress. This indicated that SlWRKY3 positively regulates heat stress in tomato. In addition, SlWRKY3 activated the expression of a range of abiotic stress-responsive genes involved in ROS scavenging, such as a SlGRXS1 gene cluster. Further analysis showed that SlWRKY3 can bind to the promoters of the SlGRXS1 gene cluster and activate their expression. Collectively, these results imply that SlWRKY3 is a positive regulator of thermotolerance through direct binding to the promoters of the SlGRXS1 gene cluster and activating their expression and ROS scavenging.http://www.sciencedirect.com/science/article/pii/S2468014122001443TomatoWRKY transcription factorSlWRKY3ThermotoleranceSlGRXS1Gene cluster
spellingShingle Ying Wang
Wenxian Gai
Liangdan Yuan
Lele Shang
Fangman Li
Zhao Gong
Pingfei Ge
Yaru Wang
Jinbao Tao
Xingyu Zhang
Haiqiang Dong
Yuyang Zhang
Heat-inducible SlWRKY3 confers thermotolerance by activating the SlGRXS1 gene cluster in tomato
Horticultural Plant Journal
Tomato
WRKY transcription factor
SlWRKY3
Thermotolerance
SlGRXS1
Gene cluster
title Heat-inducible SlWRKY3 confers thermotolerance by activating the SlGRXS1 gene cluster in tomato
title_full Heat-inducible SlWRKY3 confers thermotolerance by activating the SlGRXS1 gene cluster in tomato
title_fullStr Heat-inducible SlWRKY3 confers thermotolerance by activating the SlGRXS1 gene cluster in tomato
title_full_unstemmed Heat-inducible SlWRKY3 confers thermotolerance by activating the SlGRXS1 gene cluster in tomato
title_short Heat-inducible SlWRKY3 confers thermotolerance by activating the SlGRXS1 gene cluster in tomato
title_sort heat inducible slwrky3 confers thermotolerance by activating the slgrxs1 gene cluster in tomato
topic Tomato
WRKY transcription factor
SlWRKY3
Thermotolerance
SlGRXS1
Gene cluster
url http://www.sciencedirect.com/science/article/pii/S2468014122001443
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