Epidermal patterning in Arabidopsis: models make a difference.

The leaf and root epidermis in Arabidopsis provide ideal systems in which to explore the mechanisms that underlie the patterned assignment of cell fates during development. Extensive experimental studies have uncovered a complex interlocked feedback network that operates within the epidermis to coordinate the choice between hair and nonhair fates. A number of recent studies using mathematical models have begun to study this network, highlighting new mechanisms that have subsequently been confirmed in model-directed experiments. These studies illustrate the potential of integrated modeling and experimentation to shed new light on developmental processes. Moreover, these models enable systems-level comparative analyses that may help understand the origin and role of properties, such as robustness and redundancy in developmental systems and, concomitantly, the evolution of development itself.

[1]  Mariana Benítez,et al.  Dynamic-module redundancy confers robustness to the gene regulatory network involved in hair patterning of Arabidopsis epidermis , 2010, Biosyst..

[2]  Arezki Boudaoud,et al.  An introduction to the mechanics of morphogenesis for plant biologists. , 2010, Trends in plant science.

[3]  Stuart A. Newman,et al.  Bare Bones Pattern Formation: A Core Regulatory Network in Varying Geometries Reproduces Major Features of Vertebrate Limb Development and Evolution , 2010, PloS one.

[4]  Ben Scheres,et al.  JACKDAW controls epidermal patterning in the Arabidopsis root meristem through a non-cell-autonomous mechanism , 2010, Development.

[5]  Isaac Salazar-Ciudad,et al.  A computational model of teeth and the developmental origins of morphological variation , 2010, Nature.

[6]  Henrik Jönsson,et al.  Modeling plant growth and pattern formation. , 2010, Current opinion in plant biology.

[7]  Martin Hülskamp,et al.  One, two, three...models for trichome patterning in Arabidopsis? , 2009, Current opinion in plant biology.

[8]  V. Grieneisen,et al.  Back to the future: evolution of computational models in plant morphogenesis. , 2009, Current opinion in plant biology.

[9]  Andrew C. Oates,et al.  Quantitative approaches in developmental biology , 2009, Nature Reviews Genetics.

[10]  J. Timmer,et al.  Functional diversity of R3 single-repeat genes in trichome development , 2009, Development.

[11]  Y. Kang,et al.  The MYB23 Gene Provides a Positive Feedback Loop for Cell Fate Specification in the Arabidopsis Root Epidermis[C][W] , 2009, The Plant Cell Online.

[12]  Angela Bruex,et al.  The gene regulatory network for root epidermal cell-type pattern formation in Arabidopsis. , 2009, Journal of experimental botany.

[13]  T. Wada,et al.  Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis , 2009, Development.

[14]  Shigeru Kondo,et al.  Theoretical analysis of mechanisms that generate the pigmentation pattern of animals. , 2009, Seminars in cell & developmental biology.

[15]  K. Morohashi,et al.  A Systems Approach Reveals Regulatory Circuitry for Arabidopsis Trichome Initiation by the GL3 and GL1 Selectors , 2009, PLoS genetics.

[16]  J. Schiefelbein,et al.  A Feedback Mechanism Controlling SCRAMBLED Receptor Accumulation and Cell-Type Pattern in Arabidopsis , 2008, Current Biology.

[17]  Ricard V. Solé,et al.  Neutrality and Robustness in Evo-Devo: Emergence of Lateral Inhibition , 2008, PLoS Comput. Biol..

[18]  N. Monk,et al.  Regulative feedback in pattern formation: towards a general relativistic theory of positional information , 2008, Development.

[19]  J. Timmer,et al.  A competitive complex formation mechanism underlies trichome patterning on Arabidopsis leaves , 2008, Molecular systems biology.

[20]  John Schiefelbein,et al.  A Mutual Support Mechanism through Intercellular Movement of CAPRICE and GLABRA3 Can Pattern the Arabidopsis Root Epidermis , 2008, PLoS biology.

[21]  J. Schiefelbein,et al.  Comprehensive analysis of single-repeat R3 MYB proteins in epidermal cell patterning and their transcriptional regulation in Arabidopsis , 2008, BMC Plant Biology.

[22]  Jens Timmer,et al.  Two-Dimensional Patterning by a Trapping/Depletion Mechanism: The Role of TTG1 and GL3 in Arabidopsis Trichome Formation , 2008, PLoS biology.

[23]  K. Morohashi,et al.  The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci , 2008, Development.

[24]  Jim Haseloff,et al.  A system for modelling cell-cell interactions during plant morphogenesis. , 2008, Annals of botany.

[25]  Kiyotaka Okada,et al.  A genetic regulatory network in the development of trichomes and root hairs. , 2008, Annual review of plant biology.

[26]  J. Fisahn,et al.  Gene expression profiling of the different stages of Arabidopsis thaliana trichome development on the single cell level. , 2008, Plant physiology and biochemistry : PPB.

[27]  J. Schiefelbein,et al.  Distinct and overlapping roles of single-repeat MYB genes in root epidermal patterning. , 2007, Developmental biology.

[28]  K. Morohashi,et al.  Participation of the Arabidopsis bHLH Factor GL3 in Trichome Initiation Regulatory Events1[W][OA] , 2007, Plant Physiology.

[29]  Daisuke Shibata,et al.  Arabidopsis TRANSPARENT TESTA GLABRA2 Is Directly Regulated by R2R3 MYB Transcription Factors and Is Involved in Regulation of GLABRA2 Transcription in Epidermal Differentiation[W] , 2007, The Plant Cell Online.

[30]  E. Almaas.  Biological impacts and context of network theory , 2007, Journal of Experimental Biology.

[31]  Mariana Benítez,et al.  Gene regulatory network models for plant development. , 2007, Current opinion in plant biology.

[32]  J. Schiefelbein,et al.  The role of the SCRAMBLED receptor-like kinase in patterning the Arabidopsis root epidermis. , 2007, Developmental biology.

[33]  M. Hülskamp,et al.  Epidermal pattern formation in the root and shoot of Arabidopsis. , 2007, Biochemical Society transactions.

[34]  Gregory T. Reeves,et al.  Quantitative models of developmental pattern formation. , 2006, Developmental cell.

[35]  Satoshi Tabata,et al.  Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation , 2005, Development.

[36]  Y. Kang,et al.  The WEREWOLF MYB protein directly regulates CAPRICE transcription during cell fate specification in the Arabidopsis root epidermis , 2005, Development.

[37]  L. Serna.  Epidermal cell patterning and differentiation throughout the apical-basal axis of the seedling. , 2005, Journal of experimental botany.

[38]  T. Wada,et al.  Regulation of CAPRICE transcription by MYB proteins for root epidermis differentiation in Arabidopsis. , 2005, Plant & cell physiology.

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

[40]  C. Bernhardt,et al.  The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis , 2005, Development.

[41]  M. D. Marks,et al.  Comparison of TRY and the closely related At1g01380 gene in controlling Arabidopsis trichome patterning. , 2004, The Plant journal : for cell and molecular biology.

[42]  Martin Hülskamp,et al.  Creating a two-dimensional pattern de novo during Arabidopsis trichome and root hair initiation. , 2004, Current opinion in genetics & development.

[43]  J. Schiefelbein,et al.  ENHANCER of TRYand CPC 2(ETC2) reveals redundancy in the region-specific control of trichome development of Arabidopsis , 2004, Plant Molecular Biology.

[44]  J. Schiefelbein,et al.  The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. , 2004, Developmental biology.

[45]  W. Schmidt,et al.  Environmentally Induced Plasticity of Root Hair Development in Arabidopsis1 , 2004, Plant Physiology.

[46]  C. Bernhardt,et al.  The bHLH genes GLABRA3 (GL3) andENHANCER OF GLABRA3 (EGL3) specify epidermal cell fate in the Arabidopsis root , 2003, Development.

[47]  J. Bergelson,et al.  Interactive Effects of Jasmonic Acid, Salicylic Acid, and Gibberellin on Induction of Trichomes in Arabidopsis1 , 2003, Plant Physiology.

[48]  L. Herrera-Estrella,et al.  The role of nutrient availability in regulating root architecture. , 2003, Current opinion in plant biology.

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

[50]  Gregory A. Wray,et al.  Evolution of the Gene Network Underlying Wing Polyphenism in Ants , 2002, Science.

[51]  G. Odell,et al.  Robustness, Flexibility, and the Role of Lateral Inhibition in the Neurogenic Network , 2002, Current Biology.

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

[53]  Elliot M Meyerowitz,et al.  Plants Compared to Animals: The Broadest Comparative Study of Development , 2002, Science.

[54]  J. Schiefelbein,et al.  Developmentally distinct MYB genes encode functionally equivalent proteins in Arabidopsis. , 2001, Development.

[55]  Fan Zhang,et al.  GL3 encodes a bHLH protein that regulates trichome development in arabidopsis through interaction with GL1 and TTG1. , 2000, Genetics.

[56]  G. Odell,et al.  The segment polarity network is a robust developmental module , 2000, Nature.

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

[58]  E. Álvarez-Buylla,et al.  Genetic regulation of root hair development in Arabidopsis thaliana: a network model. , 2000, Journal of theoretical biology.

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

[60]  G. Jürgens,et al.  Generation of a Spacing Pattern: The Role of TRIPTYCHON in Trichome Patterning in Arabidopsis , 1999, Plant Cell.

[61]  J. Gray,et al.  Allele-specific interactions between ttg and gl1 during trichome development in Arabidopsis thaliana. , 1999, Genetics.

[62]  D. Szymanski,et al.  GLABROUS1 Overexpression and TRIPTYCHON Alter the Cell Cycle and Trichome Cell Fate in Arabidopsis , 1998, Plant Cell.

[63]  G. Jürgens,et al.  Tissue layer and organ specificity of trichome formation are regulated by GLABRA1 and TRIPTYCHON in Arabidopsis. , 1998, Development.

[64]  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.

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

[66]  B. Scheres,et al.  Root pattern: shooting in the dark? , 1998, Seminars in cell & developmental biology.

[67]  F. Sack,et al.  Epidermal cell fate and patterning in leaves. , 1997, The Plant cell.

[68]  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.

[69]  L. Dolan.  Pattern in the Root Epidermis: An Interplay of Diffusible Signals and Cellular Geometry , 1996 .

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

[71]  N. Young,et al.  The control of trichome spacing and number in Arabidopsis. , 1996, Development.

[72]  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.

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

[74]  Susan Pollock,et al.  Arabidopsis GLABROUS1 Gene Requires Downstream Sequences for Function. , 1993, The Plant cell.

[75]  J. Schnakenberg,et al.  Simple chemical reaction systems with limit cycle behaviour. , 1979, Journal of theoretical biology.

[76]  H. Meinhardt,et al.  A theory of biological pattern formation , 1972, Kybernetik.

[77]  A. M. Turing,et al.  The chemical basis of morphogenesis , 1952, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[78]  W. Schmidt,et al.  From priming to plasticity: the changing fate of rhizodermic cells. , 2008, BioEssays : news and reviews in molecular, cellular and developmental biology.

[79]  C. Espinosa-Soto,et al.  Equivalent genetic regulatory networks in different contexts recover contrasting spatial cell patterns that resemble those in Arabidopsis root and leaf epidermis: a dynamic model. , 2007, The International journal of developmental biology.

[80]  M. Hülskamp,et al.  Epidermal differentiation: trichomes in Arabidopsis as a model system. , 2005, The International journal of developmental biology.