Deletion of TaBSK3-2B attenuates BR signaling to regulate the Rht4 semi-dwarf phenotype and drought tolerance in wheat.

The application of Green Revolution alleles Rht-B1b and Rht-D1b in wheat semi-dwarf breeding has remarkably improved lodging resistance and increased global wheat production. However, these gibberellin (GA)-insensitive genes require higher water and fertilizer inputs and impair seedling emergence and early vigor, prompting the search for alternative GA-sensitive dwarfing genes to breed environmentally friendly wheat varieties for sustainable wheat production. Here, we reported the map-based cloning of Rht4 and functional characterization of its potential causal gene TaBSK3-2B, which encodes a plasma membrane-localized serine/threonine-protein kinase involved in the brassinosteroid (BR) signaling pathway. Loss function of TaBSK3-2B attenuated BR responses and inhibited stem elongation by reducing cell expansion, which was accompanied by decreased levels of the bioactive gibberellins GA1 and GA4. Under controlled conditions, TaBSK3-2B positively regulates wheat drought tolerance by integrating transcriptional level changes of key drought-related genes and physiological adjustments under water deficit. Furthermore, we identified a natural haplotype TaBSK3-2BH2 which was associated with reduced plant height and improved yield-related traits, with the potential to mitigate the yield penalty associated with the original Rht4 allele, a major limitation on its application in wheat breeding. The frequency of TaBSK3-2BH2 is dramatically higher in cultivars compared to landraces, indicating a strong artificial selection of TaBSK3-2BH2 during semi-dwarf wheat breeding. Our study not only provides new insights into the synergistic improvement of plant height and grain yield by fine-tuning BR signaling but also offers potential genetic resources for breeding drought-adapted semi-dwarf wheat varieties.