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Abstract

Throughout their life span, plants keep the ability to generate new tissues and organs. This remarkable developmental property relies on the continuous activity of pluripotent stem cells localized in meristems, which generate cell progenies acquiring specific cellular identities. Thus, the regulatory processes controlling the progression of stem cell lineages and their final differentiation are essential to establish the whole body plan and to ultimately define plant reproductive success. The integration of phytohormonal signals like auxin or cytokinin with key transcriptional regulators is central for balancing stem cell activity and differentiation (reviewed in Gaillochet and Lohmann, 2015), however our current understanding of the regulatory interactions mediating this molecular communication remains elusive. In this study, we used an integrated approach–including live-cell imaging, computational modeling, genome-wide profiling and genetic functional characterization–to investigate the function of the bHLH transcription factors HECATE (HEC) in controlling stem cell homeostasis and organ patterning. We found that HEC regulatory function is highly versatile and tightly interacts with cytokinin and auxin signalling pathways under multiple developmental contexts. We show in the shoot apical meristem that HEC function regulates the timing of stem cell differentiation by locally promoting cytokinin at the centre of the meristem and repressing auxin signals at the periphery. In contrast, we found that HEC genes pattern style differentiation at the gynoecium by regulating auxin flow and by buffering cytokinin responses. Using a gene network reconstruction approach, we started to unravel the regulatory interactions mediating HEC functional versatility and identified NGATHA transcription factors as relevant direct targets controlling shoot meristem activity. Together, our findings refine the molecular and developmental framework for shoot meristem activity and gynoecium differentiation.