The AP2/ERF Transcription Factor TINY Modulates Brassinosteroid-Regulated Plant Growth and Drought Responses in Arabidopsis

AP2/ERF family transcription factors have well-documented functions in stress responses, but their roles in brassinosteroid (BR)-regulated growth and stress responses have not been established. Here we show that the Arabidopsis thaliana stress-inducible AP2/ERF transcription factor TINY inhibits BR-regulated growth while promoting drought responses. TINY overexpressing plants have stunted growth, increased sensitivity to BR biosynthesis inhibitors and compromised BR-responsive gene expression. By contrast, tiny tiny2 tiny3 triple mutants have increased BR-regulated growth and BR-responsive gene expression. TINY positively regulates drought responses by activating drought-responsive genes and promoting abscisic acid-mediated stomatal closure. Global gene expression studies revealed that TINY and BRs have opposite effects on plant growth and stress response genes. TINY interacts with and antagonizes BRASSINOSTERIOID INSENSITIVE1-EMS SUPRESSOR 1 (BES1) in the regulation of these genes. The Glycogen synthase kinase 3-like protein kinase BR-INSENSITIVE2 (BIN2), a negative regulator in the BR pathway, phosphorylates and stabilizes TINY, providing a mechanism for BR-mediated down-regulation of TINY to prevent activation of stress responses under optimal growth conditions. Taken together, our results demonstrate that BR signaling negatively regulates TINY through BIN2 phosphorylation and TINY positively regulates drought responses, as well as inhibiting BR-mediated growth through TINY-BES1 antagonistic interactions. Our results thus provide insight into the coordination of BR-regulated growth and drought responses.