The FvABF3-FvALKBH10B-FvSEP3 cascade regulates fruit ripening in strawberry

Fruit ripening is a highly-orchestrated process that requires the fine-tuning and precise control of gene expression, which is mainly governed by phytohormones, epigenetic modifiers, and transcription factors. How these intrinsic regulators coordinately modulate the ripening remains elusive. Here we report the identification and characterization of FvALKBH10B as an N6-methyladenosine (m6A) RNA demethylase necessary for the normal ripening of strawberry (Fragaria vesca) fruit. FvALKBH10B is induced by phytohormone abscisic acid (ABA), and ABA-Responsive Element Binding Factor 3 (FvABF3), a master regulator in ABA signaling, is responsible for this activation. FvALKBH10B mutation leads to a delay in fruit ripening and causes global m6A hypermethylation of 1859 genes. Further analyses show that FvALKBH10B positively modulates the mRNA stability of SEPALLATA3 (FvSEP3) encoding a transcription factor via m6A demethylation. In turn, FvSEP3 targets numerous ripening-related genes including those associated with biosynthesis of ABA and anthocyanin and regulates their expression. Our findings uncover an FvABF3-FvALKBH10B-FvSEP3 cascade in controlling fruit ripening in strawberry and provide insights into the complex regulatory networks involved in this process.