The brassinosteroid signaling component SlBZR1 promotes tomato fruit ripening and carotenoid accumulation

The plant hormone ethylene is essential for climacteric fruit ripening, although it is unclear how other phytohormones and their interactions with ethylene might affect fruit ripening. Here, we explored how brassinosteroids(BRs) regulate fruit ripening in tomato(Solanum lycopersicum) and how they interact with ethylene. Exogenous BR treatment and increased endogenous BR contents in tomato plants overexpressing the BR biosynthetic gene SlCYP90B3promoted ethylene production and fruit ripening.Genetic analysis indicated that the BR signaling regulators Brassinazole-resistant1(SlBZR1) and BRI1-EMS-suppressor1(SlBES1) act redundantly in fruit softening. Knocking out Sl BZR1 inhibited ripening through transcriptome reprogramming at the onset of ripening. Combined transcriptome deep sequencing and chromatin immunoprecipitation followed by sequencing identified 73 Sl BZR1-repressed targets and 203 Sl BZR1-induced targets involving major ripening-related genes, suggesting that Sl BZR1 positively regulates tomato fruit ripening.Sl BZR1 directly targeted several ethylene and carotenoid biosynthetic genes to contribute to the ethylene burst and carotenoid accumulation to ensure normal ripening and quality formation. Furthermore,knock-out of Brassinosteroid-insensitive2(Sl BIN2),a negative regulator of BR signaling upstream of Sl BZR1, promoted fruit ripening and carotenoid accumulation. Taken together, our results highlight the role of Sl BZR1 as a master regulator of tomato fruit ripening with potential for tomato quality improvement and carotenoid biofortification.