SCFSlRAE1 regulates tomato resistance to Botrytis cinerea by modulating SlWRKY1 stability

doi:10.1111/jipb.13930

• Research Article •

SCF^SlRAE1 regulates tomato resistance to Botrytis cinerea by modulating SlWRKY1 stability

Xuewei Wang^1,2†, Ming Gao^1†, Hongxin Li¹, Congyang Jia¹, Yiran Wang¹, Xianting Lei¹, Peng Yang³, Na Zhang^1,2* and Yang‐Dong Guo^1,2*

1. College of Horticulture, China Agricultural University, Beijing 100193, China
2. Sanya Institute of China Agricultural University, Sanya 572000, China
3. Nanchong Academy of Agricultural Sciences, Nanchong 637000, China

^†The ﬁrst two authors contributed equally to this work.
^*Correspondences: Na Zhang (zhangna_cau@163.com); Yang‐Dong Guo (yaguo@cau.edu.cn, Dr. Zhang is fully responsible for the distribution of all materials associated with this article)

Received:2025-02-10 Accepted:2025-04-13 Online:2025-05-16
Supported by:
This work was supported by the National Natural Science Foundation of China (32172599), the Beijing Rural Revitalization Agricultural Science and Technology Project (NY2401080000), and the Beijing Agriculture Innovation Consortium (BAIC01‐2025)

Abstract

Abstract: Ubiquitination, a critical post-translational modification, plays a pivotal role in fine tuning the immune responses of plants. The tomato (Solanum lycopersicum) suffers significant yield and quality losses caused by the devastating pathogen Botrytis cinerea. We have discovered the role of SlRAE1, a gene encoding an E3 ubiquitin ligase, as a pivotal negative regulator of resistance to B. cinerea. SlRAE1 interacts with SlSKP1, a component of the SKP1–Cullin1–F-box (SCF) complex, to modulate the protein stability of the transcription factor SlWRKY1 through the 26S proteasome pathway. SlWRKY1 targets and inhibits the transcription of SlJAZ7, a suppressor of jasmonic acid (JA) signaling, thereby activating the JA-induced defense system and affecting tomato susceptibility to B. cinerea. The resistance enhancement observed with knock-out SlRAE1 was reduced when SlWRKY1 was also knocked out, highlighting SlWRKY1's role in SlRAE1's regulation of tomato defense against B. cinerea. Our findings elucidate the defense mechanism in tomato and suggest that targeting SlRAE1, by modulating SlWRKY1 stability, could help to develop resistant tomato varieties. These insights have broader implications for using gene-editing technologies to enhance crop defense against fungi.

Key words: B. cinerea, E3 ubiquitin ligase, JA signaling, SCF complex, tomato, WRKY

Xuewei Wang, Ming Gao, Hongxin Li, Congyang Jia, Yiran Wang, Xianting Lei, Peng Yang, Na Zhang, Yang‐Dong Guo. SCF^SlRAE1 regulates tomato resistance to Botrytis cinerea by modulating SlWRKY1 stability[J]. J Integr Plant Biol., DOI: 10.1111/jipb.13930.

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[3]	Lu Yang, Siyu Fang, Lei Liu, Lirong Zhao, Wanqin Chen, Xia Li, Zhiyu Xu, Shidie Chen, Houping Wang, Diqiu Yu. WRKY transcription factors: Hubs for regulating plant growth and stress responses [J]. J Integr Plant Biol., 2025, 67(3): 488-509.
[4]	Minmin Du, Chuanlong Sun, Lei Deng, Ming Zhou, Junming Li, Yongchen Du, Zhibiao Ye, Sanwen Huang, Tianlai Li, Jingquan Yu, Chang-Bao Li, Chuanyou Li. Molecular breeding of tomato: Advances and challenges [J]. J Integr Plant Biol., 2025, 67(3): 669-721.
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SCF^SlRAE1 regulates tomato resistance to Botrytis cinerea by modulating SlWRKY1 stability

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