Enhanced brassinosteroid signaling intensity via SlBRI1 overexpression negatively regulates drought resistance in a manner opposite of that via exogenous BR application in tomato

Brassinosteroids (BRs) regulate plant growth and stress responses. BRASSINOSTEROID-INSENSITIVE 1 (BRI1) is a BR receptor that perceives BRs and subsequently activates BR signaling. However, how BR contents and BRII expression levels affect the drought resistance of tomato requires further investigation. Here, we exogenously applied 24-epibrassinolide (EBR) and brassinazole (Brz) to tomato plants and generated different transgenic tomato SlBRII overexpression lines to study the drought stress response. Our results showed that EBR application 3 days before drought stress increased the contents of BRs and decreased abscisic acid (ABA) and reactive oxygen species (ROS), after which stomatal aperture and drought resistance eventually increased. Brz application reduced the drought resistance. Astonishingly, overexpression of 35S:SlBRI1, which increased BR signaling intensity, led to slightly improved contents of ABA and ROS and ultimately reduced both stomatal aperture and drought resistance. Moreover, plants expressing SlBRII driven by a stress-inducible promoter (Atrd29A) also exhibited reduced plant drought resistance. In all cases, enhancing the BR signaling intensity reduced antioxidant enzyme activity and reduced the expression of drought stress-related genes, ultimately compromising the drought resistance. Additionally, SlBRII mutants with altered brassinolide sensitivity (abs), which was weak BR signaling, exhibited significantly increased drought resistance. Therefore, our results reveal that BR contents positively regulated tomato drought resistance and that BR signaling intensity via BRI1 was negatively related to the drought resistance. These imply that the increased drought resistance in response to BRs is a newly discovered BR signaling branch that is located downstream of BRs and that differs from that of BRI1.