Brassinosteroid signaling regulates shoot apical meristem homeostasis via orchestrating cytokinin and WUSCHEL activity.

Abstract

In flowering plants, the shoot apical meristem (SAM) is maintained through cross-talk between the stem cell identity gene <i>WUSCHEL</i> (<i>WUS</i>) and several phytohormone-signaling pathways. However, whether the well-known sterol phytohormone brassinosteroid (BR) signaling directly regulates SAM activity remains mysterious. Here, we showed that BR signaling maintains SAM homeostasis through both enhancing <i>WUS</i> expression and modulating WUS activity in organizing center. Plants with compromised BR signaling exhibited reduced SAM size, prematurely terminated SAM, and decreased total flower numbers. BRs synergize with cytokinin (CK) to activate <i>WUS</i> expression via a protein complex formed by the BR transcription factor brassinazole-resistant 1 (BZR1) and the CK-responsive factor <i>Arabidopsis</i> response regulator 1 (ARR1). In addition, BR promotes nuclear accumulation of BZR1-WUS protein complex, which binds E-box (CANNTG) motifs genome-wide and represses type A <i>ARRs</i> and <i>FRUITFUL</i>, thereby sustaining CK output and delaying SAM arrest. This BZR1-WUS module under BR signaling is conserved in tomatoes, revealing a general regulatory mechanism of SAM maintenance by BR signaling.