Coordination of meristem and boundary functions by transcription factors in the SHOOT MERISTEMLESS regulatory network

The Arabidopsis homeodomain transcription factor SHOOT MERISTEMLESS (STM) is critical for shoot apical meristem (SAM) function, yet the components and structure of the STM gene regulatory network (GRN) are largely unknown. Here we show that transcriptional regulators are overrepresented amongst STM-regulated genes, and using these as GRN components in Bayesian network analysis we infer STM GRN associations and reveal regulatory relationships between STM and factors involved in multiple aspects of SAM function, including hormone regulation, TCP-mediated control of cell differentiation, AIL/PLT-mediated regulation of pluripotency and phyllotaxis, and specification of meristem-organ boundary zones via CUC1. We demonstrate a direct positive transcriptional feedback loop between STM and CUC1, despite their distinct expression patterns in the meristem and organ boundary respectively. Our further finding that STM activates expression of the CUC1-targeting microRNA miR164c combined with mathematical modelling provides a potential solution for this apparent contradiction, demonstrating that these proposed regulatory interactions coupled with STM mobility could be sufficient to provide a mechanism for CUC1 localisation at the meristem-organ boundary. Our findings highlight the central role of the STM GRN in coordinating SAM functions.