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The heat shock transcription factor SlHSFA3 enhances heat tolerance in tomato by directly modulating both APX activity and SlAPX1 expression

Chunrui Chen1, Licheng Xiao1, Yaling Wang2, Rong Huang1, Sunan Gao1, Wenran Su1, Jiajun Ran1, Lei Song1Taotao Wang1, Jie Ye1, Yongen Lu1, Zhibiao Ye1, Jinhua Li 2#, Junhong Zhang1# 

1 National Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops, Huazhong Agricultural University, Wuhan 430070, China

2 Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River (Ministry of Education), Southwest University; College of Horticulture and Landscape Architecture, Southwest University, No.2 Tiansheng Road, Beibei, Chongqing 400715, China

 

 Highlights 

l The heat shock transcription factor SlHSFA3 positively regulates heat tolerance in tomato.

l SlHSFA3 interacts with SlAPX1 and specifically binds to the SlAPX1 promoter region.

l The SlHSFA3-SlAPX1 regulatory module improves heat tolerance in tomato by coordinately enhancing ROS-scavenging capacity via both enzymatic and transcriptional regulation.

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摘要  

全球气候变暖与极端高温事件对作物生长、发育及经济产量产生显著影响。植物通常通过调控热激转录因子(HSFs)和抗氧化酶系统来增强耐热性,从而减轻高温胁迫的损害。然而,HSFs介导番茄耐热性的具体调控机制仍有待阐明。本研究揭示了热诱导转录因子SlHSFA3在番茄耐热性中的关键作用,发现敲除SlHSFA3后使番茄植株对热胁迫更敏感,而超量表达SlHSFA3可以提升抗坏血酸过氧化物酶(APX)活性并促进活性氧(ROS)清除,从而增强植株耐热性。同样地,过表达SlAPX1可通过减少ROS积累提高番茄耐热性,而其敲除则会增加热胁迫的敏感性。此外,SlHSFA3与SlAPX1相互作用能进一步增强APX酶活性。分子实验分析表明,SlHSFA3可直接结合SlAPX1启动子区域并上调其表达。本研究解析了SlHSFA3-SlAPX1调控通路在番茄耐热性中的分子机制,为开发耐高温作物的基因工程或育种策略提供了理论依据。



Abstract  

Global climate warming and extreme high-temperature events significantly impact crop growth, development, and economic productivity. Plants typically enhance heat tolerance by regulating heat shock transcription factors (HSFs) and antioxidant enzymes to reduce the detrimental impacts of heat stress. However, the precise regulatory mechanisms by which HSFs confer heat tolerance in tomato remain to be elucidated. In this study, we investigated the role of the heat-induced transcription factor SlHSFA3 in tomato heat tolerance. We demonstrated that knockout of SlHSFA3 increases tomato plants' sensitivity to heat stress, while enhanced expression of SlHSFA3 improves heat tolerance by promoting reactive oxygen species (ROS) scavenging through increased ascorbate peroxidase (APX) activity. Similarly, overexpression of SlAPX1 enhances heat tolerance in tomato by reducing ROS accumulation, whereas its knockout increases heat stress sensitivity. Furthermore, SlHSFA3 interacts with SlAPX1 to further augment APX activity. Molecular analysis revealed that SlHSFA3 directly upregulates the expression of SlAPX1 by binding to its promoter region. In summary, our findings elucidate the molecular mechanism of the SlHSFA3-SlAPX1 regulatory pathway in tomato heat tolerance, providing a theoretical foundation for developing advanced biotechnological and breeding strategies to improve crop adaptation under elevated temperature conditions.

Keywords:  SlHSFA3       heat tolerance       SlAPX1       ROS       tomato  
Online: 31 December 2025  
Fund: 

This work was supported by National Key Research and Development Program of China (No. 2022YFF1003001), Special Key Project of Technological Innovation and Application Development of Chongqing (No. CSTB2023TIAD-KPX0026) and the Earmarked fund for China Agriculture Research System (CARS-23-A13).

About author:  Chunrui Chen, E-mail: chenchunrui@webmail.hzau.edu.cn; #Correspondence, Jinhua Li, E-mail: ljh502@swu.edu.cn; Junhong Zhang, E-mail: zhangjunhng@mail.hzau.edu.cn

Cite this article: 

Chunrui Chen, Licheng Xiao, Yaling Wang, Rong Huang, Sunan Gao, Wenran Su, Jiajun Ran, Lei Song, Taotao Wang, Jie Ye, Yongen Lu, Zhibiao Ye, Jinhua Li, Junhong Zhang. 2025. The heat shock transcription factor SlHSFA3 enhances heat tolerance in tomato by directly modulating both APX activity and SlAPX1 expression. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.12.071

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