SlERF-RD1 acts as a developmental coordinator integrating plant canopy architecture and the ethylene-mediated ripening cascade in tomato

Abstract Key message SlERF-RD1 acts as a molecular brake, resulting in a decoupled ripening phenotype with delayed softening, while simultaneously optimizing plant architecture and flowering time, suggesting its potential for improving tomato shelf-life and productivity. Abstract Fruit ripening in tomato ( Solanum lycopersicum ) is a complex developmental process coordinated by a hierarchical network of transcription factors and the phytohormone ethylene. In this study, we identified and characterized SlERF-RD1 ( Solyc02g077790 ), a member of the AP2/ERF superfamily, as a strategic negative regulator of ripening and a coordinator of plant architecture. Transcriptomic meta-analysis revealed that SlERF-RD1 is highly sensitive to ethylene and displays spatiotemporal enrichment in locular tissues, suggesting an early role in the ripening cascade. Stable overexpression of SlERF-RD1 in tomato resulted in a significantly delayed onset of ripening, characterized by a 40–47% reduction in climacteric ethylene production and altered, tissue-specific carotenoid accumulation. Molecular analysis showed that these phenotypes are driven by the transcriptional down-regulation of the master regulator SlRIN and the rate-limiting carotenoid gene SlPSY1 . Notably, SlERF - RD1 -OE fruits maintained superior firmness during late ripening stages, which was correlated with the significant suppression of the cell wall-modifying genes SlPG2A and SlEXP1 . Furthermore, we identified Solyc01g108880 as a novel co-expressed target that is up-regulated explicitly at the red-ripe stage, suggesting a late-stage cell wall reinforcement mechanism. Beyond fruit attributes, SlERF-RD1 overexpression reconfigured plant architecture into a more compact canopy and accelerated the floral transition by up-regulating SlSFT . Our findings demonstrate that SlERF-RD1 promotes an asynchronous, firm-ripe fruit phenotype, while supporting optimized vegetative growth. This study highlights SlERF - RD1 as a high-potential target for genetic strategies aimed at enhancing both crop architecture and post-harvest shelf-life.