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
