Stem cell homeostasis in the Arabidopsis shoot meristem is regulated by intercellular movement of CLAVATA3 and its sequestration by CLAVATA1

Stem cell maintenance in the Arabidopsis shoot meristem is regulated by communication between the apical stem cells and the underlying organizing centre. Expression of the homeobox gene WUSCHEL in the organizing centre induces stem cell identity in the overlying neighbours, which then express the CLAVATA3 gene whose activity in turn restricts the size of the WUSCHEL expression domain. We have analyzed how the stem cells and the organizing centre communicate, by studying the mode of action of CLAVATA3 protein. We provide direct evidence that CLAVATA3 protein functions as a mobile intercellular signal in the shoot apical meristem that spreads laterally from the stem cells and acts both on their lateral neighbours and on the stem cells themselves to repress WUSCHEL transcription. We also show that the spread and range of action of CLAVATA3 can be limited by binding to its receptor CLAVATA1, which offers an explanation for how CLAVATA3 is prevented from entering the organizing centre and repressing WUSCHEL transcription there. This regulated spread of a secreted signalling molecule enables the shoot meristem to permit the onset of cell differentiation in the periphery, but at the same time to maintain a stable niche for its stem cells in the center.

[1]  Robert W. Williams,et al.  The CLAVATA1 Gene Encodes a Putative Receptor Kinase That Controls Shoot and Floral Meristem Size in Arabidopsis , 1997, Cell.

[2]  D. Prasher,et al.  Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[3]  M. Lenhard,et al.  The WUSCHEL and SHOOTMERISTEMLESS genes fulfil complementary roles in Arabidopsis shoot meristem regulation. , 2002, Development.

[4]  I. Raskin,et al.  Characterization of Arabidopsis acid phosphatase promoter and regulation of acid phosphatase expression. , 2000, Plant physiology.

[5]  N. Raikhel,et al.  CLV3 Is Localized to the Extracellular Space, Where It Activates the Arabidopsis CLAVATA Stem Cell Signaling Pathway Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.002196. , 2002, The Plant Cell Online.

[6]  M. Hobe,et al.  Regulation of CLV 3 Expression by Two Homeobox Genes in Arabidopsis 1 , 2002 .

[7]  M. Lenhard,et al.  WUSCHEL signaling functions in interregional communication during Arabidopsis ovule development. , 2002, Genes & development.

[8]  G. Jürgens,et al.  The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. , 1996, Development.

[9]  J. Long,et al.  The development of apical embryonic pattern in Arabidopsis. , 1998, Development.

[10]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[11]  L. Gälweiler,et al.  A transcription activation system for regulated gene expression in transgenic plants. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[12]  S. Clark,et al.  The Arabidopsis CLAVATA2 Gene Encodes a Receptor-like Protein Required for the Stability of the CLAVATA1 Receptor-like Kinase , 1999, Plant Cell.

[13]  C. Koncz,et al.  The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector , 1986, Molecular and General Genetics MGG.

[14]  R. Porat,et al.  Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. , 1996, The Plant cell.

[15]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[16]  M. Hobe,et al.  Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. , 2000, Science.

[17]  Steven M. Clark,et al.  CLAVATA3 IS A SPECIFIC REGULATOR OF SHOOT AND FLORAL MERISTEM DEVELOPMENT AFFECTING THE SAME PROCESSES AS CLAVATA1 , 1995 .

[18]  Zhenbiao Yang,et al.  The CLAVATA1 Receptor-like Kinase Requires CLAVATA3 for Its Assembly into a Signaling Complex That Includes KAPP and a Rho-Related Protein , 1999, Plant Cell.

[19]  Heiko Schoof,et al.  The Stem Cell Population of Arabidopsis Shoot Meristems Is Maintained by a Regulatory Loop between the CLAVATA and WUSCHEL Genes , 2000, Cell.

[20]  S. Brunak,et al.  Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. , 2000, Journal of molecular biology.

[21]  Heiko Schoof,et al.  Role of WUSCHEL in Regulating Stem Cell Fate in the Arabidopsis Shoot Meristem , 1998, Cell.

[22]  E. Meyerowitz,et al.  CLAVATA 3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA 1 , 1995 .

[23]  E. Meyerowitz,et al.  CLAVATA1, a regulator of meristem and flower development in Arabidopsis. , 1993, Development.

[24]  R. Simon,et al.  Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. , 1999, Science.

[25]  M. Hobe,et al.  Regulation of CLV3 Expression by Two Homeobox Genes in Arabidopsis1 , 2002, Plant Physiology.

[26]  D. Weigel,et al.  The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia. , 1999, The Plant journal : for cell and molecular biology.

[27]  T. Steeves,et al.  Patterns in plant development: Subject index , 1972 .