Control of plant stem cell function by conserved interacting transcriptional regulators
Plant stem cells in the shoot apical meristem (SAM) and root apical meristem are necessary for postembryonic development of aboveground tissues and roots, respectively, while secondary vascular stem cells sustain vascular development. WUSCHEL (WUS), a homeodomain transcription factor expressed in the rib meristem of the Arabidopsis SAM, is a key regulatory factor controlling SAM stem cell populations, and is thought to establish the shoot stem cell niche through a feedback circuit involving the CLAVATA3 (CLV3) peptide signalling pathway. WUSCHEL-RELATED HOMEOBOX 5 (WOX5), which is specifically expressed in the root quiescent centre, defines quiescent centre identity and functions interchangeably with WUS in the control of shoot and root stem cell niches. WOX4, expressed in Arabidopsis procambial cells, defines the vascular stem cell niche. WUS/WOX family proteins are evolutionarily and functionally conserved throughout the plant kingdom and emerge as key actors in the specification and maintenance of stem cells within all meristems. However, the nature of the genetic regime in stem cell niches that centre on WOX gene function has been elusive, and molecular links underlying conserved WUS/WOX function in stem cell niches remain unknown. Here we demonstrate that the Arabidopsis HAIRY MERISTEM (HAM) family of transcription regulators act as conserved interacting cofactors with WUS/WOX proteins. HAM and WUS share common targets in vivo and their physical interaction is important in driving downstream transcriptional programs and in promoting shoot stem cell proliferation. Differences in the overlapping expression patterns of WOX and HAM family members underlie the formation of diverse stem cell niche locations, and the HAM family is essential for all of these stem cell niches. These findings establish a new framework for the control of stem cell production during plant development.
© 2014 Macmillan Publishers Limited. Received 25 February 2014. Accepted 10 September 2014. Published online 26 October 2014. The authors are grateful to R. Deshaies for his support with the protein purification and pull-down experiments, to D. Rees for sharing the 96-well format luminometer, to T. Laux, T. Greb and X. Deng for sharing published reagents, to K. Sugimoto and A. Roeder for help with the histology experiments and critical reading of the manuscript, to A. Sampathkumar for the suggestion of confocal imaging, and to A. Garda and L. Wang for technical support. Scanning electron microscopy was performed at the Applied Research Center of the College of William and Mary with technical assistance from B. Robertson. This work was funded by National Institutes of Health (NIH) grant R01 GM104244 and by the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation (through grant GBMF3406) to E.M.M., by a Caltech Gosney Postdoctoral Fellowship to Y.Z., by NIH grants GM094212, GM056006 and GM067837 to S.A.K., and was aided by a grant from The Jane Coffin Childs (JCC) Memorial Fund for Medical Research to X.L., a JCC fellow.
Supplemental Material - nature13853-sv1.mov
Accepted Version - nihms627782.pdf