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Fontanet-Manzaneque JB, Laibach N, Herrero-García I, Coleto-Alcudia V, Blasco-Escámez D, Zhang C, Orduña L, Alseekh S, Miller S, Bjarnholt N, Fernie AR, Matus JT, Caño-Delgado AI
Drought is a critical issue in modern agriculture; therefore, there is a need to create crops with drought resilience. The complexity of plant responses to abiotic stresses, particularly in the field of brassinosteroid (BR) signalling, has been the subject of extensive research. In this study, we unveil compelling insights indicating that the BRASSINOSTEROID-INSENSITIVE 1 (BRI1) receptor in Arabidopsis and Sorghum plays a critical role as a negative regulator of drought responses. Introducing untargeted mutation in the sorghum BRI1 receptor (SbBRI1) effectively enhances the plant's ability to withstand osmotic and drought stress. Through DNA Affinity Purification sequencing (DAP-seq), we show that the sorghum BRI1-EMS-SUPPRESSOR 1 (SbBES1) transcription factor, a downstream player of the BR signalling, binds to a conserved G-box binding motif, and it is responsible for regulating BR homeostasis, as its Arabidopsis ortholog AtBES1. We further characterized the drought tolerance of sorghum bri1 mutants and decipher SbBES1-mediated regulation of phenylpropanoid pathway. Our findings suggest that SbBRI1 signalling serves a dual purpose: under normal conditions, it regulates lignin biosynthesis by SbBES1, but during drought conditions, BES1 becomes less active, allowing the activation of the flavonoid pathway. This adaptive shift improves the photosynthetic rate and photoprotection, reinforcing crop adaptation to drought.