Control of plant stem cell function by conserved interacting transcriptional regulators

• Published in: Nature (London) Vol. 517; no. 7534; pp. 377 - 380
• Main Authors: Zhou, Yun, Liu, Xing, Engstrom, Eric M., Nimchuk, Zachary L., Pruneda-Paz, Jose L., Tarr, Paul T., Yan, An, Kay, Steve A., Meyerowitz, Elliot M.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 15.01.2015; Nature Publishing Group
• Subjects: 13/51; 14/19; 147/135; 38/15; 38/22; 38/77; 631/449/2653/2657; 82/111; 82/80; 82/83; Arabidopsis - cytology; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - metabolism; Botanical research; Botany; Cell Proliferation; Development; Flowers & plants; Gene expression; Gene Expression Regulation, Plant; Genetic aspects; Genetic transcription; Histone Acetyltransferases - metabolism; Homeodomain Proteins - metabolism; Humanities and Social Sciences; letter; multidisciplinary; Physiological aspects; Plant cells and tissues; Plant Shoots - cytology; Plant Shoots - genetics; Plants; Properties; Protein Binding; Proteins; Science; Stem Cell Niche; Stem cells; Stem Cells - cytology; Stem Cells - metabolism; Transcription factors; Transcription, Genetic; Yeast; United States
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature13853

Here, plant HAM proteins are shown to physically interact with the transcription factor WUSCHEL and the related WOX proteins, with this interaction driving downstream transcriptional programs and determining the activities of stem cells. Regulation of plant stem cell function Postembryonic development of above-ground tissues and of roots of plants depends on stem cells in the shoot and root apical meristems, respectively. The transcription factor WUSCHEL (WUS) and the related WOX proteins are known to be involved in the specification and maintenance of stem cells within all meristems throughout the plant kingdom. The HAIRY MERISTEM (HAM) family of transcription regulators is known to contribute to shoot stem cell function in certain plant species. The present paper shows that WOX and HAM family proteins act together to control the production of all types of stem cells in diverse niches in Arabidopsis , and that WUS and HAM share some common targets in vivo . Differences in the combined expression patterns of WOX and HAM family members appear to determine the formation of diverse stem cell niche locations. These findings demonstrate how co-operative transcriptional regulators drive common regulatory pathways and point to mechanisms underlying the evolution of stem cell regulation in plants. 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 1 , 2 , 3 , 4 . 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 5 , 6 , and is thought to establish the shoot stem cell niche through a feedback circuit involving the CLAVATA3 (CLV3) peptide signalling pathway 7 . 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 8 . WOX4, expressed in Arabidopsis procambial cells, defines the vascular stem cell niche 9 , 10 , 11 . WUS/WOX family proteins are evolutionarily and functionally conserved throughout the plant kingdom 12 and emerge as key actors in the specification and maintenance of stem cells within all meristems 13 . 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.