Chromatin organization and cell fate switch respond to positional information in Arabidopsis

Many types of plant cell retain their developmental plasticity and have the capacity to switch fate when exposed to a new source of positional information. In the root epidermis of Arabidopsis, cells differentiate in alternating files of hair cells and non-hair cells, in response to positional information and the activity of the homoeodomain transcription factor GLABRA2 (GL2) in future non-hair cells. Here we show by three-dimensional fluorescence in situ hybridization on intact root epidermal tissue that alternative states of chromatin organization around the GL2 locus are required to control position-dependent cell-type specification. When, as a result of an atypical cell division, a cell is displaced from a hair file into a non-hair file, it switches fate. We show that during this event the chromatin state around the GL2 locus is not inherited, but is reorganized in the G1 phase of the cell cycle in response to local positional information. This ability to remodel chromatin organization may provide the basis for the plasticity in plant cell fate changes.

[1]  Claire S. Grierson,et al.  Clonal relationships and cell patterning in the root epidermis of Arabidopsis , 1994 .

[2]  T. Wada,et al.  Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. , 1997, Science.

[3]  Keith Roberts,et al.  Clonal analysis of the Arabidopsis root confirms that position, not lineage, determines cell fate , 2000, Planta.

[4]  T. Wada,et al.  Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation , 2002, Development.

[5]  J. Schiefelbein,et al.  Embryonic control of epidermal cell patterning in the root and hypocotyl of Arabidopsis. , 2001, Development.

[6]  M. D. Marks,et al.  A common position-dependent mechanism controls cell-type patterning and GLABRA2 regulation in the root and hypocotyl epidermis of Arabidopsis. , 1998, Plant physiology.

[7]  K. Okada,et al.  Signalling in cell type specification. , 1999, Seminars in cell & developmental biology.

[8]  L. Dolan,et al.  Epidermal patterning genes are active during embryogenesis in Arabidopsis , 2003, Development.

[9]  L. Wolpert Cell boundaries: knowing who to mix with and what to shout or whisper , 2003, Development.

[10]  L. Dolan,et al.  The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development. , 1996, The Plant journal : for cell and molecular biology.

[11]  I. Sussex,et al.  WHAT CHIMERAS CAN TELL US ABOUT PLANT DEVELOPMENT. , 1996, Annual review of plant physiology and plant molecular biology.

[12]  J. Schiefelbein,et al.  The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. , 1996, Development.

[13]  F. Berger,et al.  Positional information in root epidermis is defined during embryogenesis and acts in domains with strict boundaries , 1998, Current Biology.

[14]  Bruce Stillman,et al.  FASCIATA Genes for Chromatin Assembly Factor-1 in Arabidopsis Maintain the Cellular Organization of Apical Meristems , 2001, Cell.

[15]  J. Schiefelbein,et al.  Cell Pattern in the Arabidopsis Root Epidermis Determined by Lateral Inhibition with Feedback , 2002, The Plant Cell Online.

[16]  R. Shen,et al.  Positional Signaling Mediated by a Receptor-like Kinase in Arabidopsis , 2005, Science.

[17]  T. Laux The Stem Cell Concept in Plants A Matter of Debate , 2003, Cell.

[18]  J. Schiefelbein,et al.  WEREWOLF, a MYB-Related Protein in Arabidopsis, Is a Position-Dependent Regulator of Epidermal Cell Patterning , 1999, Cell.

[19]  Ronald W. Davis,et al.  The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. , 1994, Developmental biology.

[20]  R. Gupta A matter of debate , 2007, Nature Immunology.