Conserved Noncoding Sequences Highlight Shared Components of Regulatory Networks in Dicotyledonous Plants[W][OA]

This study identifies regions of noncoding DNA in dicot plants that are likely to facilitate complex regulation of genes by binding multiple transcription factors. Regulatory mechanisms that the model organism Arabidopsis is likely to share with crop plants provide a focus for research that has real-world applications. Conserved noncoding sequences (CNSs) in DNA are reliable pointers to regulatory elements controlling gene expression. Using a comparative genomics approach with four dicotyledonous plant species (Arabidopsis thaliana, papaya [Carica papaya], poplar [Populus trichocarpa], and grape [Vitis vinifera]), we detected hundreds of CNSs upstream of Arabidopsis genes. Distinct positioning, length, and enrichment for transcription factor binding sites suggest these CNSs play a functional role in transcriptional regulation. The enrichment of transcription factors within the set of genes associated with CNS is consistent with the hypothesis that together they form part of a conserved transcriptional network whose function is to regulate other transcription factors and control development. We identified a set of promoters where regulatory mechanisms are likely to be shared between the model organism Arabidopsis and other dicots, providing areas of focus for further research.

[1]  Brent S. Pedersen,et al.  Screening synteny blocks in pairwise genome comparisons through integer programming , 2011, BMC Bioinformatics.

[2]  William Stafford Noble,et al.  Assessing computational tools for the discovery of transcription factor binding sites , 2005, Nature Biotechnology.

[3]  I. Albert,et al.  Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome , 2007, Nature.

[4]  D. Bastola,et al.  Alfin1, a novel zinc-finger protein in alfalfa roots that binds to promoter elements in the salt-inducible MsPRP2 gene , 1998, Plant Molecular Biology.

[5]  Alexander Tiskin,et al.  Semi-local String Comparison: Algorithmic Techniques and Applications , 2007, Math. Comput. Sci..

[6]  Steve A. Kay,et al.  Reciprocal Regulation Between TOC1 and LHY/CCA1 Within the Arabidopsis Circadian Clock , 2001, Science.

[7]  M. Gribskov,et al.  The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) , 2006, Science.

[8]  R. Tjian,et al.  Orchestrated response: a symphony of transcription factors for gene control. , 2000, Genes & development.

[9]  Alexander E. Kel,et al.  TRANSFAC® and its module TRANSCompel®: transcriptional gene regulation in eukaryotes , 2005, Nucleic Acids Res..

[10]  Nicholas L. Bray,et al.  AVID: A global alignment program. , 2003, Genome research.

[11]  F. Feltus,et al.  Evidence of function for conserved noncoding sequences in Arabidopsis thaliana. , 2012, The New phytologist.

[12]  Andrew M. Jenkinson,et al.  Ensembl 2009 , 2008, Nucleic Acids Res..

[13]  S. Moose,et al.  Conserved Noncoding Sequences among Cultivated Cereal Genomes Identify Candidate Regulatory Sequence Elements and Patterns of Promoter Evolution Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010181. , 2003, The Plant Cell Online.

[14]  U. Grossniklaus,et al.  Intronic regulatory elements determine the divergent expression patterns of AGAMOUS-LIKE6 subfamily members in Arabidopsis. , 2009, The Plant journal : for cell and molecular biology.

[15]  Christopher A. Penfold,et al.  High-Resolution Temporal Profiling of Transcripts during Arabidopsis Leaf Senescence Reveals a Distinct Chronology of Processes and Regulation[C][W][OA] , 2011, Plant Cell.

[16]  Curtis E. Dyreson,et al.  Genome analysis Athena : a resource for rapid visualization and systematic analysis of Arabidopsis promoter sequences , 2005 .

[17]  Stephen M. Mount,et al.  The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus) , 2008, Nature.

[18]  Dustin A. Cartwright,et al.  A High Quality Draft Consensus Sequence of the Genome of a Heterozygous Grapevine Variety , 2007, PloS one.

[19]  H. Liu,et al.  Evaluation of seed storage-protein gene 5′ untranslated regions in enhancing gene expression in transgenic rice seed , 2010, Theoretical and Applied Genetics.

[20]  Irene K. Moore,et al.  The DNA-encoded nucleosome organization of a eukaryotic genome , 2009, Nature.

[21]  A. Myburg,et al.  Comparative analysis of orthologous cellulose synthase promoters from Arabidopsis, Populus and Eucalyptus: evidence of conserved regulatory elements in angiosperms. , 2008, The New phytologist.

[22]  Brian C. Thomas,et al.  G-Boxes, Bigfoot Genes, and Environmental Response: Characterization of Intragenomic Conserved Noncoding Sequences in Arabidopsis[W] , 2007, The Plant Cell Online.

[23]  Liang Tang,et al.  PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database , 2010, Nucleic Acids Res..

[24]  E. Bornberg-Bauer,et al.  Evolutionary divergence and limits of conserved non-coding sequence detection in plant genomes , 2011, Nucleic acids research.

[25]  R. R. Samaha,et al.  Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. , 2000, Science.

[26]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[27]  T. Koshiba,et al.  Complex regulation of ABA biosynthesis in plants. , 2002, Trends in plant science.

[28]  Chuntao Wang,et al.  The 5'untranslated region of the FAD3 mRNA is required for its translational enhancement at low temperature in Arabidopsis roots , 2010 .

[29]  Y. van de Peer,et al.  Identification of novel regulatory modules in dicotyledonous plants using expression data and comparative genomics , 2006, Genome Biology.

[30]  Martin Kuiper,et al.  BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks , 2005, Bioinform..

[31]  M. Goodman,et al.  Embryonic epsilon and gamma globin genes of a prosimian primate (Galago crassicaudatus). Nucleotide and amino acid sequences, developmental regulation and phylogenetic footprints. , 1988, Journal of molecular biology.

[32]  Jun S. Song,et al.  High-throughput mapping of the chromatin structure of human promoters , 2007, Nature Biotechnology.

[33]  Alexander Tiskin,et al.  Evolutionary analysis of regulatory sequences (EARS) in plants. , 2010, The Plant journal : for cell and molecular biology.

[34]  Tanya Vavouri,et al.  Tuning in to the signals: noncoding sequence conservation in vertebrate genomes. , 2008, Trends in genetics : TIG.

[35]  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.

[36]  David N Arnosti,et al.  Transcriptional enhancers: Intelligent enhanceosomes or flexible billboards? , 2005, Journal of cellular biochemistry.

[37]  Gabriel Moreno-Hagelsieb,et al.  Choosing BLAST options for better detection of orthologs as reciprocal best hits , 2008, Bioinform..

[38]  Wyeth W. Wasserman,et al.  TFBS: Computational framework for transcription factor binding site analysis , 2002, Bioinform..

[39]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[40]  Yoshihiro Ugawa,et al.  Plant cis-acting regulatory DNA elements (PLACE) database: 1999 , 1999, Nucleic Acids Res..

[41]  K. Vandepoele,et al.  Systematic Identification of Functional Plant Modules through the Integration of Complementary Data Sources1[W][OA] , 2012, Plant Physiology.

[42]  Cizhong Jiang,et al.  Nucleosome positioning and gene regulation: advances through genomics , 2009, Nature Reviews Genetics.

[43]  Joel Dudley,et al.  TimeTree: a public knowledge-base of divergence times among organisms , 2006, Bioinform..

[44]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[45]  Klaus Harter,et al.  Cis-motifs upstream of the transcription and translation initiation sites are effectively revealed by their positional disequilibrium in eukaryote genomes using frequency distribution curves , 2006, BMC Bioinformatics.

[46]  Erik L. L. Sonnhammer,et al.  InParanoid 7: new algorithms and tools for eukaryotic orthology analysis , 2009, Nucleic Acids Res..

[47]  S. Goff,et al.  Utility and distribution of conserved noncoding sequences in the grasses , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[48]  P. Benfey,et al.  Using Cauliflower to Find Conserved Non-Coding Regions in Arabidopsis1 , 2002, Plant Physiology.

[49]  Ole Winther,et al.  JASPAR, the open access database of transcription factor-binding profiles: new content and tools in the 2008 update , 2007, Nucleic Acids Res..

[50]  D. Church,et al.  Cross-species sequence comparisons: a review of methods and available resources. , 2003, Genome research.

[51]  L. Mirny,et al.  Nucleosome-mediated cooperativity between transcription factors , 2009, Proceedings of the National Academy of Sciences.

[52]  M. Goodman,et al.  Embryonic ε and γ globin genes of a prosimian primate (Galago crassicaudatus): Nucleotide and amino acid sequences, developmental regulation and phylogenetic footprints , 1988 .

[53]  A. Bashir,et al.  Conserved noncoding sequences in the grasses. , 2003, Genome research.

[54]  Sascha Ott,et al.  An alignment-free model for comparison of regulatory sequences , 2010, Bioinform..

[55]  Xin Chen,et al.  TRANSFAC: an integrated system for gene expression regulation , 2000, Nucleic Acids Res..

[56]  David A. Nix,et al.  Large-Scale Turnover of Functional Transcription Factor Binding Sites in Drosophila , 2006, PLoS Comput. Biol..

[57]  MarkSpensley,et al.  Evolutionarily Conserved Regulatory Motifs in the Promoter of the Arabidopsis Clock Gene LATE ELONGATED HYPOCOTYL , 2009 .

[58]  D. Weigel,et al.  A genetic framework for floral patterning , 1998, Nature.

[59]  Alexander Tiskin,et al.  Computing alignment plots efficiently , 2009, PARCO.

[60]  Taichi E. Takasuka,et al.  Are nucleosome positions in vivo primarily determined by histone–DNA sequence preferences? , 2009, Nucleic acids research.

[61]  E. Grotewold,et al.  Genome wide analysis of Arabidopsis core promoters , 2005, BMC Genomics.

[62]  Chris M. Brown,et al.  Effect of 5'UTR introns on gene expression in Arabidopsis thaliana , 2006, BMC Genomics.

[63]  Brian C. Thomas,et al.  Arabidopsis intragenomic conserved noncoding sequence , 2007, Proceedings of the National Academy of Sciences.

[64]  P. Bucher,et al.  Searching for regulatory elements in human noncoding sequences. , 1997, Current opinion in structural biology.

[65]  Matthew R. Pocock,et al.  The Bioperl toolkit: Perl modules for the life sciences. , 2002, Genome research.