Spatial coordination between stem cell activity and cell differentiation in the root meristem.

A critical issue in development is the coordination of the activity of stem cell niches with differentiation of their progeny to ensure coherent organ growth. In the plant root, these processes take place at opposite ends of the meristem and must be coordinated with each other at a distance. Here, we show that in Arabidopsis, the gene SCR presides over this spatial coordination. In the organizing center of the root stem cell niche, SCR directly represses the expression of the cytokinin-response transcription factor ARR1, which promotes cell differentiation, controlling auxin production via the ASB1 gene and sustaining stem cell activity. This allows SCR to regulate, via auxin, the level of ARR1 expression in the transition zone where the stem cell progeny leaves the meristem, thus controlling the rate of differentiation. In this way, SCR simultaneously controls stem cell division and differentiation, ensuring coherent root growth.

[1]  Ottoline Leyser,et al.  An Auxin-Dependent Distal Organizer of Pattern and Polarity in the Arabidopsis Root , 1999, Cell.

[2]  A. Spradling,et al.  Stem cells find their niche , 2001, Nature.

[3]  B. Sundberg,et al.  A Microscale Technique for Gas Chromatography-Mass Spectrometry Measurements of Picogram Amounts of Indole-3-Acetic Acid in Plant Tissues , 1995, Plant physiology.

[4]  S. Sabatini,et al.  Analysis of root meristem size development. , 2010, Methods in molecular biology.

[5]  M. Evans,et al.  Gravity-regulated differential auxin transport from columella to lateral root cap cells , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Daniel L. Mace,et al.  A High-Resolution Root Spatiotemporal Map Reveals Dominant Expression Patterns , 2007, Science.

[7]  Tal Nawy,et al.  Transcriptional Profile of the Arabidopsis Root Quiescent Centerw⃞ , 2005, The Plant Cell Online.

[8]  Teva Vernoux,et al.  An Evolutionarily Conserved Mechanism Delimiting SHR Movement Defines a Single Layer of Endodermis in Plants , 2007, Science.

[9]  Lewis Wolpert,et al.  Principles of Development , 1997 .

[10]  P. Benfey,et al.  Transcriptional Regulation of ROS Controls Transition from Proliferation to Differentiation in the Root , 2010, Cell.

[11]  Sang-Kee Song,et al.  Large-scale analysis of the GRAS gene family in Arabidopsis thaliana , 2008, Plant Molecular Biology.

[12]  B. Scheres,et al.  Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division. , 2004, Genes & development.

[13]  Bruno Müller,et al.  Cytokinin signaling networks. , 2012, Annual review of plant biology.

[14]  K. Palme,et al.  Arabidopsis ASA1 Is Important for Jasmonate-Mediated Regulation of Auxin Biosynthesis and Transport during Lateral Root Formation[W][OA] , 2009, The Plant Cell Online.

[15]  T. Mukherjee,et al.  Interaction between Differentiating Cell- and Niche-Derived Signals in Hematopoietic Progenitor Maintenance , 2011, Cell.

[16]  M. Lenhard,et al.  Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers , 2007, Nature.

[17]  P. Benfey,et al.  Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[18]  P. Benfey,et al.  The SCARECROW Gene Regulates an Asymmetric Cell Division That Is Essential for Generating the Radial Organization of the Arabidopsis Root , 1996, Cell.

[19]  Claudia van den Berg,et al.  Short-range control of cell differentiation in the Arabidopsis root meristem , 1997, Nature.

[20]  Sean May,et al.  Cytokinin Regulation of Auxin Synthesis in Arabidopsis Involves a Homeostatic Feedback Loop Regulated via Auxin and Cytokinin Signal Transduction[W][OA] , 2010, Plant Cell.

[21]  Laila Moubayidin,et al.  The molecular basis of cytokinin function. , 2010, Current opinion in plant biology.

[22]  J. Friml Subcellular trafficking of PIN auxin efflux carriers in auxin transport. , 2010, European journal of cell biology.

[23]  Laila Moubayidin,et al.  The Rate of Cell Differentiation Controls the Arabidopsis Root Meristem Growth Phase , 2010, Current Biology.

[24]  Klaus Palme,et al.  The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots , 2005, Nature.

[25]  G. Fink,et al.  Differential regulation of an auxin-producing nitrilase gene family in Arabidopsis thaliana. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[26]  James A.H. Murray,et al.  A Bistable Circuit Involving SCARECROW-RETINOBLASTOMA Integrates Cues to Inform Asymmetric Stem Cell Division , 2012, Cell.

[27]  Alexander G. Fletcher,et al.  A PHABULOSA/Cytokinin Feedback Loop Controls Root Growth in Arabidopsis , 2012, Current Biology.

[28]  N. Perrimon,et al.  Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. , 1993, Development.

[29]  Anna N. Stepanova,et al.  A Link between Ethylene and Auxin Uncovered by the Characterization of Two Root-Specific Ethylene-Insensitive Mutants in Arabidopsis , 2005, The Plant Cell Online.

[30]  J. Friml,et al.  Auxin regulates distal stem cell differentiation in Arabidopsis roots , 2010, Proceedings of the National Academy of Sciences.

[31]  Renze Heidstra,et al.  Cytokinins Determine Arabidopsis Root-Meristem Size by Controlling Cell Differentiation , 2007, Current Biology.

[32]  James A. Cuff,et al.  A Bivalent Chromatin Structure Marks Key Developmental Genes in Embryonic Stem Cells , 2006, Cell.

[33]  Takashi Aoyama,et al.  A Genetic Framework for the Control of Cell Division and Differentiation in the Root Meristem , 2008, Science.

[34]  Ben Scheres,et al.  Auxin: the looping star in plant development. , 2008, Annual review of plant biology.

[35]  P. Rubery,et al.  Naturally Occurring Auxin Transport Regulators , 1988, Science.

[36]  Ben Scheres,et al.  Stem-cell niches: nursery rhymes across kingdoms , 2007, Nature Reviews Molecular Cell Biology.

[37]  P. Benfey,et al.  Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. , 2000, Development.

[38]  K. Ljung,et al.  The Arabidopsis YUCCA1 Flavin Monooxygenase Functions in the Indole-3-Pyruvic Acid Branch of Auxin Biosynthesis[W] , 2011, Plant Cell.

[39]  Masashi Yamada,et al.  Sites and Regulation of Auxin Biosynthesis in Arabidopsis Roots , 2005, The Plant Cell Online.

[40]  Ykä Helariutta,et al.  Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate , 2010, Nature.

[41]  J. Reed,et al.  Arabidopsis SHY2/IAA3 Inhibits Auxin-Regulated Gene Expression Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010283. , 2002, The Plant Cell Online.

[42]  P. Benfey,et al.  Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth , 2010, Nature.

[43]  Laila Moubayidin,et al.  Cytokinin-auxin crosstalk. , 2009, Trends in plant science.

[44]  T. Mikkelsen,et al.  Genome-wide maps of chromatin state in pluripotent and lineage-committed cells , 2007, Nature.

[45]  Anna N. Stepanova,et al.  TAA1-Mediated Auxin Biosynthesis Is Essential for Hormone Crosstalk and Plant Development , 2008, Cell.

[46]  P. Benfey,et al.  The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. , 1999, The Plant journal : for cell and molecular biology.

[47]  R. Sablowski,et al.  Plant stem cell niches: from signalling to execution. , 2011, Current opinion in plant biology.

[48]  S. Sabatini,et al.  SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. , 2003, Genes & development.