SlARF11–SlGATA5 stimulates tomato leaf angle by feedback regulation with brassinosteroid signaling

Auxin response factor (ARF) and brassinosteroid (BR) play significant roles in plant growth and development, such as determining leaf angle. However, the relationship between ARFs and BR signaling in regulating tomato leaf angle remains unclear. Here, we report that auxin-responsive factor 11 (SlARF11) positively regulates tomato leaf angle and exhibits hypersensitivity to BR. SlARF11 is a non-canonical ARF that is highly expressed at the adaxial side of petiole bases. SlARF11 interacts with and acts upstream of SlGATA5, a GATA transcription factor that negatively regulates BR signaling by directly binding to the promoter of its downstream gene BRASINOSTEROID-INSENSITIVE 2 (SlBIN2.1), thereby inhibiting its expression in tomato. SlARF11-mediated regulation of leaf angle involves cell elongation at the petiole base, and lignin deposition, significantly facilitating the expression of U-type cyclin (SlCYCU2;1) and phenylalanine ammonia-lyase 4 (SlPAL4) mediated by SlGATA5. In addition, SlBIN2.1 is located upstream of SlARF11 and phosphorylates SlARF11, thereby enhancing the interaction between SlARF11 and SlGATA5. Some BRASSINOSTERIOD INSENSITIVE1-EMS-SUPPRESSOR 1 (SlBES1), located downstream of SlBIN2.1, could inhibit the expression of SlARF11. Briefly, these findings validate the SlARF11-mediated signaling pathway as linking auxin response factors to the traditional BR signaling pathway, ensuring effective crosstalk between tomato leaf angle and BR signaling.