Overexpression of AtBES1D in tomato enhances BR response and accelerates fruit ripening

Brassinosteroids (BRs) are essential plant hormones that regulate growth and development, with BRI1-EMS SUPPRESSOR 1 (BES1) and BRASSINAZOLE-RESISTANT 1 (BZR1) serving as central transcription factors in BR signaling. However, the role of BES1 in regulating tomato fruit ripening remains poorly understood. Here, we generated three independent transgenic tomato lines overexpressing Arabidopsis thaliana BES1D (AtBES1D). Overexpression of AtBES1D enhanced BR responses, as demonstrated by enhanced responsiveness to BRs and reduced sensitivity to the BR biosynthesis inhibitor brassinazole (BRZ). AtBES1D-transgenic tomato plants exhibited pleiotropic phenotypic alterations, including stunted growth, curled leaves, suppressed root elongation, delayed flowering, accelerated fruit ripening, and diminished fruit size, weight, and seed number. In addition, AtBES1D transgenic fruits exhibited upregulated expression of ethylene-related genes (ACS4, NR, ERF1, ERF4, E4, and E8) and ripening regulators (RIN, TAGL1, FUL1, FUL2, and PG). Chromatin immunoprecipitation sequencing (ChIP-seq) identified 1757 AtBES1D target genes, predominantly enriched in plant hormone signaling, transcriptional regulation, and metabolic pathways. Collectively, these findings establish AtBES1D as a multifunctional regulator modulating vegetative development, reproductive transition, and fruit ripening in tomato. AtBES1D likely promotes fruit ripening and improves fruit quality by modulating BR signaling, ethylene pathways, transcription factors, and metabolic processes.