The Rate of Cell Differentiation Controls the Arabidopsis Root Meristem Growth Phase

Upon seed germination, apical meristems grow as cell division prevails over differentiation and reach their final size when division and differentiation reach a balance. In the Arabidopsis root meristem, this balance results from the interaction between cytokinin (promoting differentiation) and auxin (promoting division) through a regulatory circuit whereby the ARR1 cytokinin-responsive transcription factor activates the gene SHY2, which negatively regulates the PIN genes encoding auxin transport facilitators. However, it remains unknown how the final meristem size is set, i.e., how a change in the relative rates of cell division and differentiation is brought about to cause meristem growth to stop. Here, we show that during meristem growth, expression of SHY2 is driven by another cytokinin-response factor, ARR12, and that completion of growth is brought about by the upregulation of SHY2 caused by both ARR12 and ARR1: this leads to an increase in cell differentiation rate that balances it with division, thus setting root meristem size. We also show that gibberellins selectively repress expression of ARR1 at early stages of meristem development, and that the DELLA protein REPRESSOR OF GA 1-3 (RGA) mediates this negative control.

[1]  M. Bennett,et al.  Gibberellin Signaling in the Endodermis Controls Arabidopsis Root Meristem Size , 2009, Current Biology.

[2]  Xiangdong Fu,et al.  Auxin promotes Arabidopsis root growth by modulating gibberellin response , 2003, Nature.

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

[4]  T. Sun,et al.  The DELLA motif is essential for gibberellin-induced degradation of RGA , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[5]  O. Leyser,et al.  AXR3 and SHY2 interact to regulate root hair development , 2003, Development.

[6]  D. Alabadí,et al.  Transcriptional Regulation of Gibberellin Metabolism Genes by Auxin Signaling in Arabidopsis1[W] , 2006, Plant Physiology.

[7]  J. Peng,et al.  The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. , 1997, Genes & development.

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

[9]  Shinjiro Yamaguchi,et al.  Gibberellin metabolism and its regulation. , 2008, Annual review of plant biology.

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

[11]  T. Sun,et al.  The Arabidopsis F-Box Protein SLEEPY1 Targets Gibberellin Signaling Repressors for Gibberellin-Induced Degradation , 2004, The Plant Cell Online.

[12]  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.

[13]  I. Hwang,et al.  Isolation of the Arabidopsis GA4 locus. , 1995, The Plant cell.

[14]  Thorsten Hamann,et al.  Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators , 2005, The EMBO journal.

[15]  S. Prat,et al.  Transcriptional factor interaction: a central step in DELLA function. , 2008, Current opinion in genetics & development.

[16]  Rishikesh Bhalerao,et al.  Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis , 2008, Nature Cell Biology.

[17]  Tai-Ping Sun,et al.  Gibberellin signaling: biosynthesis, catabolism, and response pathways. , 2002, The Plant cell.

[18]  Takashi Aoyama,et al.  ARR1 directly activates cytokinin response genes that encode proteins with diverse regulatory functions. , 2007, Plant & cell physiology.

[19]  P. Hedden,et al.  Isolation and Expression of Three Gibberellin 20-Oxidase cDNA Clones from Arabidopsis , 1995, Plant physiology.

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

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

[22]  M. Koornneef,et al.  Gibberellin requirement for Arabidopsis seed germination is determined both by testa characteristics and embryonic abscisic acid. , 2000, Plant physiology.

[23]  L. Lopez-Molina,et al.  The Gibberellic Acid Signaling Repressor RGL2 Inhibits Arabidopsis Seed Germination by Stimulating Abscisic Acid Synthesis and ABI5 Activity[W] , 2008, The Plant Cell Online.

[24]  T. Sun,et al.  The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis. , 1994, The Plant cell.

[25]  S. Dhondt,et al.  Gibberellin Signaling Controls Cell Proliferation Rate in Arabidopsis , 2009, Current Biology.

[26]  T. Sun,et al.  Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. , 2001, Genetics.

[27]  T. Sun,et al.  The Arabidopsis RGA Gene Encodes a Transcriptional Regulator Repressing the Gibberellin Signal Transduction Pathway , 1998, Plant Cell.

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

[29]  G. Sandberg,et al.  Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis , 2006, Proceedings of the National Academy of Sciences.