Ethylene response factor ERF.D7 activates auxin response factor 2 paralogs to regulate tomato fruit ripening

Despite the obligatory role of ethylene in climacteric fruit ripening and the identification of 77 ethylene response factors (ERFs) in the tomato (Solanum lycopersicum) genome, the role of few ERFs has been validated in the ripening process. Here, using a comprehensive morpho-physiological, molecular, and biochemical approach, we demonstrate the regulatory role of ERF D7 (SlERF.D7) in tomato fruit ripening. SlERF.D7 expression positively responded to exogenous ethylene and auxin treatments, most likely in a ripening inhibitor-independent manner. SlERF.D7 overexpression (OE) promoted ripening, and its silencing had the opposite effect. Alterations in its expression modulated ethylene production, pigment accumulation, and fruit firmness. Consistently, genes involved in ethylene biosynthesis and signaling, lycopene biosynthesis, and cell wall loosening were upregulated in the OE lines and downregulated in RNAi lines. These transgenic lines also accumulated altered levels of indole-3-acetic acid at late-breaker stages. A positive association between auxin response factor 2 (ARF2) paralog's transcripts and SlERF.D7 mRNA levels and that SlARF2A and SlARF2B are direct targets of SlERF.D7 underpinned the perturbed auxin-ethylene crosstalk for the altered ripening program observed in the transgenic fruits. Overall, this study uncovers that SlERF.D7 positively regulates SlARF2A/B abundance to amalgamate auxin and ethylene signaling pathways for controlling tomato fruit ripening.