SlERF.F12 modulates the transition to ripening in tomato fruit by recruiting the corepressor topless and histone deacetylases to repress key ripening genes

Authors: DENG, HENG - Sichuan University; CHEN, YAO - Sichuan University; LIU, ZIYU - Sichuan University; LIU, ZHAIQIAO - Sichuan University; PENG, SHU - Sichuan University; WANG, ROUCHEN - Sichuan University; HAO, YANWEI - South China Agricultural Univerisity; SU, DAN - Sichuan University; PIRELLO, JULIEN - University Of Toulouse; Giovannoni, James; LIU, YONGSHENG - Sichuan University; GRIERSON, DONALD - University Of Nottingham; BOUZAYEN, MONDHER - University Of Toulouse; LIU, MICHUNG - Sichuan University

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/22/2021
Publication Date: N/A
Citation: N/A
DOI: https://doi.org/10.1093/plcell/koac025

Interpretive Summary: The ripening of fleshy fruits is a complex, genetically programmed process. Tomato has been widely used as a model system for studying fleshy fruit ripening. Although ripening is complex, the plant hormone ethylene has long been accepted as the main trigger of ripening in many fruits, and its downstream transcriptional regulators ethylene response factors (ERFs) are responsible for the ethylene signal. We identified a ERF gene named SlERF.F12, which encodes a protein whose expression levels dramatically decrease at the transition to ripening, therefore being an ideal candidate to play an important role in controlling this process. Functional studies allowed us to test the importance of this gene in ripening control and indeed indicate it works through repression of other genes necessary for ripening to proceed.

Technical Abstract: Ethylene response factors (ERFs) are downstream components of ethylene-signaling pathways known to play critical roles in ethylene-controlled 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.