Gene network analysis in plant development by genomic technologies.

The analysis of the gene regulatory networks underlying development is of central importance for a better understanding of the mechanisms that control the formation of the different cell-types, tissues or organs of an organism. The recent invention of genomic technologies has opened the possibility of studying these networks at a global level. In this paper, we summarize some of the recent advances that have been made in the understanding of plant development by the application of genomic technologies. We focus on a few specific processes, namely flower and root development and the control of the cell cycle, but we also highlight landmark studies in other areas that opened new avenues of experimentation or analysis. We describe the methods and the strategies that are currently used for the analysis of plant development by genomic technologies, as well as some of the problems and limitations that hamper their application. Since many genomic technologies and concepts were first developed and tested in organisms other than plants, we make reference to work in non-plant species and compare the current state of network analysis in plants to that in other multicellular organisms.

[1]  R. Nishihama,et al.  Mitotic Cyclins Stimulate the Activity of c-Myb-like Factors for Transactivation of G2/M Phase-specific Genes in Tobacco* , 2004, Journal of Biological Chemistry.

[2]  Elliot M. Meyerowitz,et al.  Arabidopsis, a useful weed , 1989, Cell.

[3]  D. Wagner,et al.  Genomic identification of direct target genes of LEAFY. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[4]  H. Sommer,et al.  Characterization of Antirrhinum Petal Development and Identification of Target Genes of the Class B MADS Box Gene DEFICIENSw⃞ , 2004, The Plant Cell Online.

[5]  L. Hennig,et al.  Genome-wide gene expression in an Arabidopsis cell suspension , 2003, Plant Molecular Biology.

[6]  K. Helin,et al.  E2F7, a novel E2F featuring DP‐independent repression of a subset of E2F‐regulated genes , 2003, The EMBO journal.

[7]  S. Kosugi,et al.  E2Ls, E2F-like Repressors of Arabidopsis That Bind to E2F Sites in a Monomeric Form* , 2002, The Journal of Biological Chemistry.

[8]  Elliot M. Meyerowitz,et al.  Genome-Wide Analysis of Spatial Gene Expression in Arabidopsis Flowers , 2004, The Plant Cell Online.

[9]  D. Pe’er,et al.  Module networks: identifying regulatory modules and their condition-specific regulators from gene expression data , 2003, Nature Genetics.

[10]  C. Dean,et al.  Multiple Pathways in the Decision to Flower: Enabling, Promoting, and Resetting , 2004, The Plant Cell Online.

[11]  E. Meyerowitz,et al.  A Homolog of NO APICAL MERISTEM Is an Immediate Target of the Floral Homeotic Genes APETALA3/PISTILLATA , 1998, Cell.

[12]  Detlef Weigel,et al.  Dissection of floral induction pathways using global expression analysis , 2003, Development.

[13]  D. Inzé,et al.  Cell cycle: the key to plant growth control? , 2003, Trends in plant science.

[14]  James Z Zhang,et al.  Overexpression analysis of plant transcription factors. , 2003, Current opinion in plant biology.

[15]  Philip N Benfey,et al.  Network building: transcriptional circuits in the root. , 2004, Current opinion in plant biology.

[16]  J. Bowman,et al.  Promoter Bashing, microRNAs, and Knox Genes. New Insights, Regulators, and Targets-of-Regulation in the Establishment of Lateral Organ Polarity in Arabidopsis1 , 2004, Plant Physiology.

[17]  Georg Haberer,et al.  Transcriptional Similarities, Dissimilarities, and Conservation of cis-Elements in Duplicated Genes of Arabidopsis1[w] , 2004, Plant Physiology.

[18]  D. Shasha,et al.  A Gene Expression Map of the Arabidopsis Root , 2003, Science.

[19]  D. Inzé,et al.  Transcript profiling of early lateral root initiation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[20]  B. S. Baker,et al.  Gene Expression During the Life Cycle of Drosophila melanogaster , 2002, Science.

[21]  M. Scott.  Development The Natural History of Genes , 2000, Cell.

[22]  P. Schnable,et al.  Global expression profiling applied to plant development. , 2004, Current opinion in plant biology.

[23]  R. Macknight,et al.  It's time to flower: the genetic control of flowering time , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[24]  M. Gerstein,et al.  Genomic analysis of regulatory network dynamics reveals large topological changes , 2004, Nature.

[25]  M. Zik,et al.  Global Identification of Target Genes Regulated by APETALA3 and PISTILLATA Floral Homeotic Gene Action Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.006353. , 2003, The Plant Cell Online.

[26]  Utpal Nath,et al.  CINCINNATA Controls Both Cell Differentiation and Growth in Petal Lobes and Leaves of Antirrhinum1 , 2004, Plant Physiology.

[27]  K. White,et al.  Developmental genomic approaches in model organisms. , 2002, Annual review of genomics and human genetics.

[28]  Wenming Wang,et al.  HUA ENHANCER3 reveals a role for a cyclin-dependent protein kinase in the specification of floral organ identity in Arabidopsis , 2004, Development.

[29]  Mark Gerstein,et al.  Distribution of NF-kappaB-binding sites across human chromosome 22. , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[30]  W. Crosby,et al.  APETALA1 and SEPALLATA3 interact to promote flower development. , 2001, The Plant journal : for cell and molecular biology.

[31]  Nicola J. Rinaldi,et al.  Transcriptional regulatory code of a eukaryotic genome , 2004, Nature.

[32]  Huai Wang,et al.  The Embryo MADS Domain Protein AGAMOUS-Like 15 Directly Regulates Expression of a Gene Encoding an Enzyme Involved in Gibberellin Metabolism , 2004, The Plant Cell Online.

[33]  J. Chandler,et al.  Translational fusions with the engrailed repressor domain efficiently convert plant transcription factors into dominant-negative functions. , 2002, Nucleic acids research.

[34]  Y. Mizukami,et al.  A matter of size: developmental control of organ size in plants. , 2001, Current opinion in plant biology.

[35]  C. Gutiérrez,et al.  Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCF(AtSKP2) pathway in response to light. , 2002, The Plant cell.

[36]  Roger E Bumgarner,et al.  Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. , 2001, Science.

[37]  S. Cawley,et al.  Unbiased Mapping of Transcription Factor Binding Sites along Human Chromosomes 21 and 22 Points to Widespread Regulation of Noncoding RNAs , 2004, Cell.

[38]  W. Shen.  The plant E2F-Rb pathway and epigenetic control. , 2002, Trends in plant science.

[39]  John J. Wyrick,et al.  Genome-wide location and function of DNA binding proteins. , 2000, Science.

[40]  T. Payne,et al.  KNUCKLES (KNU) encodes a C2H2 zinc-finger protein that regulates development of basal pattern elements of the Arabidopsis gynoecium , 2004, Development.

[41]  C. Espinosa-Soto,et al.  A Gene Regulatory Network Model for Cell-Fate Determination during Arabidopsis thaliana Flower Development That Is Robust and Recovers Experimental Gene Expression Profilesw⃞ , 2004, The Plant Cell Online.

[42]  S. Hake,et al.  The knotted1-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulating metabolic pathways. , 2003, Genes & development.

[43]  Kathleen Marchal,et al.  PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences , 2002, Nucleic Acids Res..

[44]  Dirk Inzé,et al.  Plant cell cycle transitions. , 2003, Current opinion in plant biology.

[45]  J. Riechmann,et al.  Transcriptional Regulation: a Genomic Overview , 2002, The arabidopsis book.

[46]  W. Lukowitz,et al.  A MAPKK Kinase Gene Regulates Extra-Embryonic Cell Fate in Arabidopsis , 2004, Cell.

[47]  D. Weigel,et al.  Temporally and spatially controlled induction of gene expression in Arabidopsis thaliana. , 2004, The Plant journal : for cell and molecular biology.

[48]  K. Hiratsu,et al.  Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. , 2003, The Plant journal : for cell and molecular biology.

[49]  R. Simon,et al.  The ethanol switch: a tool for tissue-specific gene induction during plant development. , 2003, The Plant journal : for cell and molecular biology.

[50]  Wei Wang,et al.  Dissecting the transcription networks of a cell using computational genomics. , 2003, Current opinion in genetics & development.

[51]  Shailesh V. Date,et al.  A Probabilistic Functional Network of Yeast Genes , 2004, Science.

[52]  Kalika Prasad,et al.  A conserved function for Arabidopsis SUPERMAN in regulating floral-whorl cell proliferation in rice, a monocotyledonous plant , 2000, Current Biology.

[53]  T. Volkert,et al.  E2F integrates cell cycle progression with DNA repair, replication, and G(2)/M checkpoints. , 2002, Genes & development.

[54]  Nicola J. Rinaldi,et al.  Transcriptional Regulatory Networks in Saccharomyces cerevisiae , 2002, Science.

[55]  E. Álvarez-Buylla,et al.  Conversion of leaves into petals in Arabidopsis , 2001, Current Biology.

[56]  J. Arias,et al.  In vivo target promoter-binding activities of a xenobiotic stress-activated TGA factor. , 2001, The Plant journal : for cell and molecular biology.

[57]  Crisanto Gutierrez,et al.  A genome-wide identification of E2F-regulated genes in Arabidopsis. , 2003, The Plant journal : for cell and molecular biology.

[58]  Koji Goto,et al.  Complexes of MADS-box proteins are sufficient to convert leaves into floral organs , 2001, Nature.

[59]  Gudrun Wacker.  Similarities and Differences , 2005 .

[60]  P. Brown,et al.  Coordinate regulation of yeast ribosomal protein genes is associated with targeted recruitment of Esa1 histone acetylase. , 2000, Molecular cell.

[61]  P. Lio’,et al.  Periodic gene expression program of the fission yeast cell cycle , 2004, Nature Genetics.

[62]  L. Breeden,et al.  Periodic Transcription: A Cycle within a Cycle , 2003, Current Biology.

[63]  S. P. Fodor,et al.  Large-Scale Transcriptional Activity in Chromosomes 21 and 22 , 2002, Science.

[64]  S. Jacobsen,et al.  Regulation of SUP Expression Identifies Multiple Regulators Involved in Arabidopsis Floral Meristem Development , 2000, Plant Cell.

[65]  E. Winzeler,et al.  Treasures and traps in genome-wide data sets: case examples from yeast , 2002, Nature Reviews Genetics.

[66]  Claude W. dePamphilis,et al.  Genome-Wide Analysis of the Cyclin Family in Arabidopsis and Comparative Phylogenetic Analysis of Plant Cyclin-Like Proteins1[w] , 2004, Plant Physiology.

[67]  E. Davidson,et al.  Gene regulatory network controlling embryonic specification in the sea urchin. , 2004, Current opinion in genetics & development.

[68]  M. Busch,et al.  Molecular analysis of the , 1996 .

[69]  E. Coen,et al.  Genetic Control of Surface Curvature , 2003, Science.

[70]  Eric H Davidson,et al.  Developmental gene network analysis. , 2003, The International journal of developmental biology.

[71]  Harmen J. Bussemaker,et al.  REDUCE: an online tool for inferring cis-regulatory elements and transcriptional module activities from microarray data , 2003, Nucleic Acids Res..

[72]  A. de Bruin,et al.  Identification and Characterization of E2F7, a Novel Mammalian E2F Family Member Capable of Blocking Cellular Proliferation* , 2003, Journal of Biological Chemistry.

[73]  N. L. La Thangue,et al.  E2F and cell cycle control: a double-edged sword. , 2003, Archives of biochemistry and biophysics.

[74]  Matthew W. Hahn,et al.  The evolution of transcriptional regulation in eukaryotes. , 2003, Molecular biology and evolution.

[75]  Nicola J. Rinaldi,et al.  Serial Regulation of Transcriptional Regulators in the Yeast Cell Cycle , 2001, Cell.

[76]  J. Fak,et al.  Transcriptional Control in the Segmentation Gene Network of Drosophila , 2004, PLoS biology.

[77]  Tim Hui-Ming Huang,et al.  Isolating human transcription factor targets by coupling chromatin immunoprecipitation and CpG island microarray analysis. , 2002, Genes & development.

[78]  D. Weigel,et al.  LEAFY controls floral meristem identity in Arabidopsis , 1992, Cell.

[79]  K. Weston.  Myb proteins in life, death and differentiation. , 1998, Current opinion in genetics & development.

[80]  R. W. Davis,et al.  Epidermal cell fate determination in Arabidopsis: patterns defined by a steroid-inducible regulator. , 1994, Science.

[81]  G. Sumara,et al.  A Probabilistic Functional Network of Yeast Genes , 2004 .

[82]  S. Kay,et al.  Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. , 2000, Science.

[83]  R. Amasino,et al.  Vernalization and epigenetics: how plants remember winter. , 2004, Current opinion in plant biology.

[84]  E. Coen,et al.  The TCP domain: a motif found in proteins regulating plant growth and development. , 1999, The Plant journal : for cell and molecular biology.

[85]  Sven Bergmann,et al.  Defining transcription modules using large-scale gene expression data , 2004, Bioinform..

[86]  T. Jack.  Molecular and Genetic Mechanisms of Floral Control , 2004, The Plant Cell Online.

[87]  K. Okada,et al.  RABBIT EARS, encoding a SUPERMAN-like zinc finger protein, regulates petal development in Arabidopsis thaliana , 2003, Development.

[88]  Stephane Rombauts,et al.  Genome-Wide Analysis of Core Cell Cycle Genes in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010445. , 2002, The Plant Cell Online.

[89]  P. Brewer,et al.  PETAL LOSS, a trihelix transcription factor gene, regulates perianth architecture in the Arabidopsis flower , 2004, Development.

[90]  A. Fraser,et al.  A probabilistic view of gene function , 2004, Nature Genetics.

[91]  J. Doonan,et al.  G2/M-Phase–Specific Transcription during the Plant Cell Cycle Is Mediated by c-Myb–Like Transcription Factors , 2001, The Plant Cell Online.

[92]  M. Vidal.  A Biological Atlas of Functional Maps , 2001, Cell.

[93]  S. Bergmann,et al.  Similarities and Differences in Genome-Wide Expression Data of Six Organisms , 2003, PLoS biology.

[94]  L. Hood,et al.  A Genomic Regulatory Network for Development , 2002, Science.

[95]  C. Bergounioux,et al.  AtE2F-a and AtDP-a, members of the E2F family of transcription factors, induce Arabidopsis leaf cells to re-enter S phase , 2002, Molecular Genetics and Genomics.

[96]  E. Davidson.  Genomic Regulatory Systems: Development and Evolution , 2005 .

[97]  H. Bussemaker,et al.  Regulatory element detection using correlation with expression , 2001, Nature Genetics.

[98]  D. Inzé,et al.  Microarray analysis of E2Fa-DPa-overexpressing plants uncovers a cross-talking genetic network between DNA replication and nitrogen assimilation , 2003, Journal of Cell Science.

[99]  Kathleen Marchal,et al.  Computational Approaches to Identify Promoters and cis-Regulatory Elements in Plant Genomes1 , 2003, Plant Physiology.

[100]  I. Somssich,et al.  Stimulus-Dependent, Promoter-Specific Binding of Transcription Factor WRKY1 to Its Native Promoter and the Defense-Related Gene PcPR1-1 in Parsleyw⃞ , 2004, The Plant Cell Online.

[101]  D. Slonim,et al.  Composition and dynamics of the Caenorhabditis elegans early embryonic transcriptome , 2003, Development.

[102]  J. Murray,et al.  Altered Cell Cycle Distribution, Hyperplasia, and Inhibited Differentiation in Arabidopsis Caused by the D-Type Cyclin CYCD3 Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.004838. , 2003, The Plant Cell Online.

[103]  K. Schneitz,et al.  NOZZLE regulates proximal-distal pattern formation, cell proliferation and early sporogenesis during ovule development in Arabidopsis thaliana. , 2000, Development.

[104]  B. Frey,et al.  The functional landscape of mouse gene expression , 2004, Journal of biology.

[105]  M. Gerstein,et al.  Complex transcriptional circuitry at the G1/S transition in Saccharomyces cerevisiae. , 2002, Genes & development.

[106]  I. Henderson,et al.  Control of Arabidopsis flowering: the chill before the bloom , 2004, Development.

[107]  Hongyu Zhao,et al.  An Arabidopsis Promoter Microarray and its Initial Usage in the Identification of HY5 Binding Targets in Vitro , 2004, Plant Molecular Biology.

[108]  I. Sussex,et al.  Laser Capture Microdissection of Cells from Plant Tissues1 , 2003, Plant Physiology.

[109]  Thomas E. Royce,et al.  Global Identification of Human Transcribed Sequences with Genome Tiling Arrays , 2004, Science.

[110]  Nicola J. Rinaldi,et al.  Computational discovery of gene modules and regulatory networks , 2003, Nature Biotechnology.

[111]  D. Weigel,et al.  The role of JAGGED in shaping lateral organs , 2004, Development.

[112]  J. Bowman,et al.  Establishment of polarity in angiosperm lateral organs. , 2002, Trends in genetics : TIG.

[113]  D. Inzé,et al.  Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa–DPa transcription factor , 2002, The EMBO journal.

[114]  David Botstein,et al.  Promoter-specific binding of Rap1 revealed by genome-wide maps of protein–DNA association , 2001, Nature Genetics.

[115]  S. Cawley,et al.  Novel RNAs identified from an in-depth analysis of the transcriptome of human chromosomes 21 and 22. , 2004, Genome research.

[116]  J L Bowman,et al.  Genes directing flower development in Arabidopsis. , 1989, The Plant cell.

[117]  P. Sieber,et al.  Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[118]  J. Rinn,et al.  The transcriptional activity of human Chromosome 22. , 2003, Genes & development.

[119]  E. Meyerowitz,et al.  The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development , 2004, Development.

[120]  V. Sundaresan,et al.  The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. , 1999, Genes & development.

[121]  E. Meyerowitz,et al.  The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS , 2004, Nature.

[122]  Michael Q. Zhang,et al.  A global transcriptional regulatory role for c-Myc in Burkitt's lymphoma cells , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[123]  Pascal Gantet,et al.  Transcription Factor Networks. Pathways to the Knowledge of Root Development , 2004, Plant Physiology.

[124]  Yaniv Ziv,et al.  Revealing modular organization in the yeast transcriptional network , 2002, Nature Genetics.

[125]  D. Inzé,et al.  The Plant-Specific Cyclin-Dependent Kinase CDKB1;1 and Transcription Factor E2Fa-DPa Control the Balance of Mitotically Dividing and Endoreduplicating Cells in Arabidopsis , 2004, The Plant Cell Online.

[126]  Thomas E. Royce,et al.  Distribution of NF-κB-binding sites across human chromosome 22 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[127]  D. Weigel,et al.  Regulatory Elements of the Floral Homeotic Gene AGAMOUS Identified by Phylogenetic Footprinting and Shadowing Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009548. , 2003, The Plant Cell Online.

[128]  Nicola J. Rinaldi,et al.  Control of Pancreas and Liver Gene Expression by HNF Transcription Factors , 2004, Science.

[129]  C. Gutiérrez,et al.  G(1) to S transition: more than a cell cycle engine switch. , 2002, Current opinion in plant biology.

[130]  N. Chua,et al.  Chemical-inducible systems for regulated expression of plant genes. , 2000, Current opinion in biotechnology.

[131]  H. Nakagami,et al.  Phosphorylation of Retinoblastoma-Related Protein by the Cyclin D/Cyclin-Dependent Kinase Complex Is Activated at the G1/S-Phase Transition in Tobacco Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.0025 , 2002, The Plant Cell Online.

[132]  Detlef Weigel,et al.  Building beauty: the genetic control of floral patterning. , 2002, Developmental cell.

[133]  C. Gutiérrez,et al.  Role of an Atypical E2F Transcription Factor in the Control of Arabidopsis Cell Growth and Differentiation , 2004, The Plant Cell Online.

[134]  T. Ideker.  A systems approach to discovering signaling and regulatory pathways--or, how to digest large interaction networks into relevant pieces. , 2004, Advances in experimental medicine and biology.

[135]  D. Botstein,et al.  Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF , 2001, Nature.

[136]  Scott A. Rifkin,et al.  Microarray analysis of Drosophila development during metamorphosis. , 1999, Science.

[137]  Dominique C Bergmann,et al.  Stomatal Development and Pattern Controlled by a MAPKK Kinase , 2004, Science.

[138]  Scott A. Rifkin,et al.  A Gene Expression Map for the Euchromatic Genome of Drosophila melanogaster , 2004, Science.

[139]  K. White,et al.  Patterns of Gene Expression During Drosophila Mesoderm Development , 2001, Science.

[140]  D. Inzé,et al.  Genome-wide analysis of core cell cycle genes in the unicellular green alga Ostreococcus tauri. , 2005, Molecular biology and evolution.

[141]  Qi Xie,et al.  A chemical-regulated inducible RNAi system in plants. , 2003, The Plant journal : for cell and molecular biology.

[142]  G. Ditta,et al.  B and C floral organ identity functions require SEPALLATA MADS-box genes , 2000, Nature.

[143]  V. Reinke,et al.  Genome-wide analysis of developmental and sex-regulated gene expression profiles in Caenorhabditis elegans. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[144]  R. Young,et al.  A common set of gene regulatory networks links metabolism and growth inhibition. , 2004, Molecular cell.

[145]  Huai Wang,et al.  A chromatin immunoprecipitation (ChIP) approach to isolate genes regulated by AGL15, a MADS domain protein that preferentially accumulates in embryos. , 2002, The Plant journal : for cell and molecular biology.

[146]  Wilhelm Gruissem,et al.  Cell Cycle-regulated Gene Expression inArabidopsis * , 2002, The Journal of Biological Chemistry.

[147]  D. Wagner,et al.  Floral induction in tissue culture: a system for the analysis of LEAFY-dependent gene regulation. , 2004, The Plant journal : for cell and molecular biology.

[148]  T. Mockler,et al.  Interdependency of Brassinosteroid and Auxin Signaling in Arabidopsis , 2004, PLoS biology.

[149]  M. Gerstein,et al.  GATA-1 binding sites mapped in the β-globin locus by using mammalian chIp-chip analysis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[150]  Joseph M. Dale,et al.  Empirical Analysis of Transcriptional Activity in the Arabidopsis Genome , 2003, Science.

[151]  E. Brown,et al.  Genomic analysis of gene expression in C. elegans. , 2000, Science.

[152]  M. Mulisch,et al.  A putative iron regulatory protein (IRP)-encoding cDNA sequence in the ciliate Eufolliculina uhligi, and differential gene expression during the life cycle , 1999 .