An updated model of shoot apical meristem regulation by ERECTA family and CLAVATA3 signaling pathways

Abstract

ABSTRACTThe shoot apical meristem (SAM) gives rise to above-ground organs. The size of the SAM is relatively constant due to the balance of stem cell replenishment versus cell recruitment into developing organs. In angiosperms, the transcription factor WUSCHEL (WUS) promotes stem cell identity in the central zone of the SAM. WUS forms a negative feedback loop with a signaling pathway activated by CLAVATA3 (CLV3). In the periphery of the SAM, the ERECTA family (ERf) receptors promote cell differentiation and constrain the expression ofWUSandCLV3. Here, we show that four ligands of ERfs redundantly inhibitCLV3andWUSexpression. Transcriptome analysis confirmed thatWUSandCLV3are the main targets of ERf signaling and uncovered several new ones. Analysis of promoter reporters indicated that in the vegetative meristem, theWUSexpression domain mostly overlapped with theCLV3domain and did not shift along the apical-basal axis inclv3. A 3D mathematical model reproduced the experimentally observedCLV3andWUSexpression patterns with fewer assumptions than earlier models. Based on these findings, we propose that CLV3 regulates cellular levels ofWUSexpression through autocrine signaling, while ERfs regulateWUSspatial expression, preventing its encroachment into the peripheral zone.One Sentence SummaryThrough autocrine signaling, CLV3 regulates the level ofWUSexpression in the vegetative SAM but not its location, while ERfs regulate theWUSspatial pattern, preventing its expansion into the peripheral zone.