Tomato MED25 regulates fruit ripening by interacting with EIN3-like transcription factors

• Published in: The Plant cell 2023-03, Vol.35 (3), p.1038-1057
• Main Authors: Deng, Lei, Yang, Tianxia, Li, Qian, Chang, Zeqian, Sun, Chuanlong, Jiang, Hongling, Meng, Xianwen, Huang, Tingting, Li, Chang-Bao, Zhong, Silin, Li, Chuanyou
• Format: Article
• Language: English
• Subjects: Ethylenes - metabolism; Fruit - metabolism; Gene Expression Regulation, Plant; Plant Proteins - genetics; Plant Proteins - metabolism; Solanum lycopersicum - genetics; Transcription Factors - genetics; Transcription Factors - metabolism
• ISSN: 1040-4651; 1532-298X
• DOI: 10.1093/plcell/koac349

Abstract Fruit ripening relies on the precise spatiotemporal control of RNA polymerase II (Pol II)-dependent gene transcription, and the evolutionarily conserved Mediator (MED) coactivator complex plays an essential role in this process. In tomato (Solanum lycopersicum), a model climacteric fruit, ripening is tightly coordinated by ethylene and several key transcription factors. However, the mechanism underlying the transmission of context-specific regulatory signals from these ripening-related transcription factors to the Pol II transcription machinery remains unknown. Here, we report the mechanistic function of MED25, a subunit of the plant Mediator transcriptional coactivator complex, in controlling the ethylene-mediated transcriptional program during fruit ripening. Multiple lines of evidence indicate that MED25 physically interacts with the master transcription factors of the ETHYLENE-INSENSITIVE 3 (EIN3)/EIN3-LIKE (EIL) family, thereby playing an essential role in pre-initiation complex formation during ethylene-induced gene transcription. We also show that MED25 forms a transcriptional module with EIL1 to regulate the expression of ripening-related regulatory as well as structural genes through promoter binding. Furthermore, the EIL1–MED25 module orchestrates both positive and negative feedback transcriptional circuits, along with its downstream regulators, to fine-tune ethylene homeostasis during fruit ripening. The tomato Mediator subunit MED25 physically interacts with EIN3-like transcription factors to orchestrate ethylene-mediated transcriptional reprogramming during fruit ripening.