SlERF.F12 modulates the transition to ripening in tomato fruit by recruiting the co-repressor TOPLESS and histone deacetylases to repress key ripening genes.

Heng Deng, Yao Chen, Ziyu Liu, Zhaoqiao Liu, Peng Shu, Ruochen Wang, Yanwei Hao, Dan Su, Julien Pirrello, Yongsheng Liu, Zhengguo Li, Don Grierson, James J Giovannoni, Mondher Bouzayen, Mingchun Liu

The Plant cell 2022 Mar 29

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Ethylene response factors (ERFs) are downstream components of ethylene-signaling pathways known to play critical roles in ethylene-controlled climacteric fruit ripening, yet little is known about the molecular mechanism underlying their mode of action. Here, we demonstrate that SlERF.F12, a member of the ERF.F subfamily containing Ethylene-responsive element-binding factor-associated Amphiphilic Repression (EAR) motifs, negatively regulates the onset of tomato (Solanum lycopersicum) fruit ripening by recruiting the co-repressor TOPLESS 2 (TPL2) and the histone deacetylases (HDAs) HDA1/HDA3 to repress the transcription of ripening-related genes. The SlERF.F12-mediated transcriptional repression of key ripening-related genes 1-AMINO-CYCLOPROPANE-1-CARBOXYLATE SYNTHASE 2 (ACS2), ACS4, POLYGALACTURONASE 2a, and PECTATE LYASE is dependent on the presence of its C-terminal EAR motif. We show that SlERF.F12 interacts with the co-repressor TPL2 via the C-terminal EAR motif and recruits HDAs SlHDA1 and SlHDA3 to form a tripartite complex in vivo that actively represses transcription of ripening genes by decreasing the level of the permissive histone acetylation marks H3K9Ac and H3K27Ac at their promoter regions. These findings provide new insights into the ripening regulatory network and uncover a direct link between repressor ERFs and histone modifiers in modulating the transition to ripening of climacteric fruit. © American Society of Plant Biologists 2022. All rights reserved. For permissions, please email: journals.permissions@oup.com.

Citation

Heng Deng, Yao Chen, Ziyu Liu, Zhaoqiao Liu, Peng Shu, Ruochen Wang, Yanwei Hao, Dan Su, Julien Pirrello, Yongsheng Liu, Zhengguo Li, Don Grierson, James J Giovannoni, Mondher Bouzayen, Mingchun Liu. SlERF.F12 modulates the transition to ripening in tomato fruit by recruiting the co-repressor TOPLESS and histone deacetylases to repress key ripening genes. The Plant cell. 2022 Mar 29;34(4):1250-1272