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

The 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 of WUS and CLV3. Here, we show that four ligands of ERfs redundantly inhibit CLV3 and WUS expression. Transcriptome analysis confirmed that WUS and CLV3 are the main targets of ERf signaling and uncovered several new ones. Analysis of promoter reporters indicated that in the vegetative meristem, the WUS expression domain mostly overlapped with the CLV3 domain and did not shift along the apical-basal axis in clv3. A 3D mathematical model reproduced the experimentally observed CLV3 and WUS expression patterns with fewer assumptions than earlier models. Based on these findings, we propose that CLV3 regulates cellular levels of WUS expression through autocrine signaling, while ERfs regulate WUS spatial expression, preventing its encroachment into the peripheral zone. One Sentence SummaryThrough autocrine signaling, CLV3 regulates the level of WUS expression in the vegetative SAM but not its location, while ERfs regulate the WUS spatial pattern, preventing its expansion into the peripheral zone.