Conservation and Divergence of Light-Regulated Genome Expression Patterns during Seedling Development in Rice and Arabidopsis[W]

Genome-wide 70-mer oligonucleotide microarrays of rice (Oryza sativa) and Arabidopsis thaliana were used to profile genome expression changes during light-regulated seedling development. We estimate that the expression of ∼20% of the genome in both rice and Arabidopsis seedlings is regulated by white light. Qualitatively similar expression profiles from seedlings grown under different light qualities were observed in both species; however, a quantitatively weaker effect on genome expression was observed in rice. Most metabolic pathways exhibited qualitatively similar light regulation in both species with a few species-specific differences. Global comparison of expression profiles between rice and Arabidopsis reciprocal best-matched gene pairs revealed a higher correlation of genome expression patterns in constant light than in darkness, suggesting that the genome expression profile of photomorphogenesis is more conserved. Transcription factor gene expression under constant light exposure was poorly conserved between the two species, implying a faster-evolving rate of transcription factor gene expression in light-grown plants. Organ-specific expression profiles during seedling photomorphogenesis provide genome-level evidence for divergent light effects in different higher plant organs. Finally, overrepresentation of specific promoter motifs in root- and leaf-specific light-regulated genes in both species suggests that these cis-elements are important for gene expression responses to light.

[1]  J. Michael Cherry,et al.  Microarray data quality analysis: lessons from the AFGC project , 2004, Plant Molecular Biology.

[2]  Stephane Rombauts,et al.  PlantCARE, a plant cis-acting regulatory element database , 1999, Nucleic Acids Res..

[3]  Eberhard Schäfer,et al.  Phytochromes control photomorphogenesis by differentially regulated, interacting signaling pathways in higher plants. , 2002, Annual review of plant biology.

[4]  A. Cashmore,et al.  The G-box: a ubiquitous regulatory DNA element in plants bound by the GBF family of bZIP proteins. , 1995, Trends in biochemical sciences.

[5]  Scott A. Rifkin,et al.  Evolution of gene expression in the Drosophila melanogaster subgroup , 2003, Nature Genetics.

[6]  M B Wilkins,et al.  Light- and gravity-sensing guidance systems in plants , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[7]  P. Quail,et al.  Rapid transcriptional regulation by phytochrome of the genes for phytochrome and chlorophyll a/b-binding protein in Avena sativa , 1988, Molecular and cellular biology.

[8]  K. L. Poff,et al.  Altering the axial light gradient affects photomorphogenesis in emerging seedlings of Zea mays L. , 1986, Plant physiology.

[9]  N. Chua,et al.  Phytochrome A and phytochrome B mediate the hypocotyl-specific downregulation of TUB1 by light in arabidopsis. , 1995, The Plant cell.

[10]  Yoshikatsu Sato,et al.  Chloroplast movement. , 2003, Annual review of plant biology.

[11]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[12]  L. Hennig,et al.  Chromatin-Remodeling and Memory Factors. New Regulators of Plant Development , 2002, Plant Physiology.

[13]  Tong Zhu,et al.  Multiple transcription-factor genes are early targets of phytochrome A signaling , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[14]  R. Sharrock,et al.  Differential Patterns of Expression of the Arabidopsis PHYB, PHYD, and PHYE Phytochrome Genes , 1997, Plant physiology.

[15]  Kenichi Higo,et al.  PLACE: a database of plant cis-acting regulatory DNA elements , 1998, Nucleic Acids Res..

[16]  A. Paterson,et al.  Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Gerald M Rubin,et al.  Evidence for large domains of similarly expressed genes in the Drosophila genome , 2002, Journal of biology.

[18]  R. Amasino,et al.  Role of chromatin modification in flowering-time control. , 2005, Trends in plant science.

[19]  Hongyu Zhao,et al.  Analysis of far-red light-regulated genome expression profiles of phytochrome A pathway mutants in Arabidopsis. , 2002, The Plant journal : for cell and molecular biology.

[20]  K. Shinozaki,et al.  Identification of genes regulated by dark adaptation and far‐red light illumination in roots of Arabidopsis thaliana* , 2004 .

[21]  X. Deng,et al.  Arabidopsis bZIP Protein HY5 Directly Interacts with Light-Responsive Promoters in Mediating Light Control of Gene Expression , 1998, Plant Cell.

[22]  J. Torrey,et al.  The Reversible Inhibition by Red and Far-Red Light of Auxin-Induced Lateral Root Initiation in Isolated Pea Roots. , 1964, Plant physiology.

[23]  Mark Gerstein,et al.  ExpressYourself: a modular platform for processing and visualizing microarray data , 2003, Nucleic Acids Res..

[24]  S. Rhee,et al.  Functional Annotation of the Arabidopsis Genome Using Controlled Vocabularies1 , 2004, Plant Physiology.

[25]  Hongyu Zhao,et al.  A Tiling Microarray Expression Analysis of Rice Chromosome 4 Suggests a Chromosome-Level Regulation of Transcriptionw⃞ , 2005, The Plant Cell Online.

[26]  G. Khush.  Origin, dispersal, cultivation and variation of rice , 1997, Plant Molecular Biology.

[27]  E. Blancaflor,et al.  Plant Gravitropism. Unraveling the Ups and Downs of a Complex Process1 , 2003, Plant Physiology.

[28]  K. Shimamoto,et al.  Rice as a model for comparative genomics of plants. , 2002, Annual review of plant biology.

[29]  D. Basu,et al.  Rice PHYC gene: structure, expression, map position and evolution , 2000, Plant Molecular Biology.

[30]  G. Church,et al.  Computational identification of cis-regulatory elements associated with groups of functionally related genes in Saccharomyces cerevisiae. , 2000, Journal of molecular biology.

[31]  N. Wei,et al.  Arabidopsis COP8, COP10, and COP11 genes are involved in repression of photomorphogenic development in darkness. , 1994, The Plant cell.

[32]  H Niemann,et al.  Identification and analysis of eukaryotic promoters: recent computational approaches. , 2001, Trends in genetics : TIG.

[33]  John Quackenbush,et al.  Assessing unmodified 70-mer oligonucleotide probe performance on glass-slide microarrays , 2003, Genome Biology.

[34]  B. Burr,et al.  International Rice Genome Sequencing Project: the effort to completely sequence the rice genome. , 2000, Current opinion in plant biology.

[35]  Dawei Li,et al.  The Genomes of Oryza sativa: A History of Duplications , 2005, PLoS biology.

[36]  R. Sharrock,et al.  Patterns of Expression and Normalized Levels of the Five Arabidopsis Phytochromes1 , 2002, Plant Physiology.

[37]  K. Okada,et al.  Functional analysis of each blue light receptor, cry1, cry2, phot1, and phot2, by using combinatorial multiple mutants in Arabidopsis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[38]  E. Huq,et al.  PHYTOCHROME-INTERACTING FACTOR 1 Is a Critical bHLH Regulator of Chlorophyll Biosynthesis , 2004, Science.

[39]  H. Mohr.  Primary Effects of Light on Growth , 1962 .

[40]  J. Chory,et al.  Light: an indicator of time and place. , 2000, Genes & development.

[41]  Y. Ohno,et al.  PHOTOINHIBITION OF ELONGATION GROWTH OF ROOTS IN RICE SEEDLINGS , 1967 .

[42]  P. Quail,et al.  Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution, and differential expression of a plant regulatory photoreceptor family. , 1989, Genes & development.

[43]  S. Kay,et al.  The rice phytochrome gene: structure, autoregulated expression, and binding of GT-1 to a conserved site in the 5' upstream region. , 1989, The Plant cell.

[44]  L. Feldman,et al.  Light-regulated gravitropism in seedling roots of maize. , 1987, Plant physiology.

[45]  X. Deng,et al.  Multiple photoreceptors mediate the light-induced reduction of GUS-COP1 from Arabidopsis hypocotyl nuclei. , 1998, The Plant journal : for cell and molecular biology.

[46]  E. J. Williams,et al.  Coexpression of neighboring genes in the genome of Arabidopsis thaliana. , 2004, Genome research.

[47]  Masaki Furuya,et al.  Isolation and Characterization of Rice Phytochrome A Mutants , 2001, Plant Cell.

[48]  A. Cashmore,et al.  Cryptochromes: blue light receptors for plants and animals. , 1999, Science.

[49]  Huanming Yang,et al.  A Draft Sequence of the Rice Genome (Oryza sativa L. ssp. indica) , 2002, Science.

[50]  M. Koornneef,et al.  Genetic control of light-inhibited hypocotyl elongation in Arabidopsis thaliana (L.) , 1980 .

[51]  Philippe Reymond,et al.  A Conserved Transcript Pattern in Response to a Specialist and a Generalist Herbivorew⃞ , 2004, The Plant Cell Online.

[52]  J. B. Reid,et al.  DE1, a 12-Base Pair cis-Regulatory Element Sufficient to Confer Dark-inducible and Light Down-regulated Expression to a Minimal Promoter in Pea* , 2000, The Journal of Biological Chemistry.

[53]  K. Shimamoto,et al.  Phytochromes confer the photoperiodic control of flowering in rice (a short-day plant). , 1999, The Plant journal : for cell and molecular biology.

[54]  E. Liscum,et al.  Blue Light Signaling through the Cryptochromes and Phototropins. So That's What the Blues Is All About1 , 2003, Plant Physiology.

[55]  J. Ecker,et al.  The phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[56]  David Botstein,et al.  Diverse and specific gene expression responses to stresses in cultured human cells. , 2004, Molecular biology of the cell.

[57]  P. Quail.  Photosensory perception and signalling in plant cells: new paradigms? , 2002, Current opinion in cell biology.

[58]  K. Yeh,et al.  Eukaryotic phytochromes: light-regulated serine/threonine protein kinases with histidine kinase ancestry. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[59]  T. Brutnell,et al.  Photomorphogenic Responses in Maize Seedling Development1[w] , 2003, Plant Physiology.

[60]  R. Fischer,et al.  Biology of chromatin dynamics. , 2005, Annual review of plant biology.

[61]  Hongyu Zhao,et al.  Light Control of Arabidopsis Development Entails Coordinated Regulation of Genome Expression and Cellular Pathways , 2001, The Plant Cell Online.

[62]  Guillaume Blanc,et al.  Widespread Paleopolyploidy in Model Plant Species Inferred from Age Distributions of Duplicate Genes , 2004, The Plant Cell Online.

[63]  H. Fukuzawa,et al.  Photochemical Properties of the Flavin Mononucleotide-Binding Domains of the Phototropins from Arabidopsis, Rice, andChlamydomonas reinhardtii 1 , 2002, Plant Physiology.

[64]  Ning Sun,et al.  Organ-Specific Expression of Arabidopsis Genome during Development1[w] , 2005, Plant Physiology.

[65]  M. Gerstein,et al.  A Genome-Wide Analysis of Blue-Light Regulation of Arabidopsis Transcription Factor Gene Expression during Seedling Development , 2003 .

[66]  Cornelius S. Barry,et al.  Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[67]  D. E. Somers,et al.  Temporal and spatial expression patterns of PHYA and PHYB genes in Arabidopsis. , 1995, The Plant journal : for cell and molecular biology.

[68]  Chentao Lin.  Blue Light Receptors and Signal Transduction Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000646. , 2002, The Plant Cell Online.

[69]  M. Takano,et al.  The Rice COLEOPTILE PHOTOTROPISM1 Gene Encoding an Ortholog of Arabidopsis NPH3 Is Required for Phototropism of Coleoptiles and Lateral Translocation of Auxinw⃞ , 2005, The Plant Cell Online.

[70]  B. Weisshaar,et al.  Two distinct cis-acting elements are involved in light-dependent activation of the pea elip promoter , 1994, Molecular and General Genetics MGG.

[71]  T. Brutnell,et al.  Cereal phytochromes: targets of selection, targets for manipulation? , 2005, Trends in plant science.

[72]  Jian Wang,et al.  A microarray analysis of the rice transcriptome and its comparison to Arabidopsis. , 2005, Genome research.

[73]  T. G. Owens,et al.  Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[74]  C. Dean,et al.  Integrated Cytogenetic Map of Chromosome Arm 4S of A. thaliana Structural Organization of Heterochromatic Knob and Centromere Region , 2000, Cell.

[75]  D. Galbraith,et al.  Methods for Transcriptional Profiling in Plants. Be Fruitful and Replicate , 2004, Plant Physiology.

[76]  K. Devos,et al.  Comparative genetics in the grasses. , 1998, Plant molecular biology.

[77]  Mark Gerstein,et al.  Multi-species microarrays reveal the effect of sequence divergence on gene expression profiles. , 2005, Genome research.

[78]  M. Furuya,et al.  Phytochrome action in Oryza sativa L. , 1970, Planta.

[79]  E. Huq,et al.  Direct targeting of light signals to a promoter element-bound transcription factor. , 2000, Science.

[80]  Andreas Madlung,et al.  Sensitivity of 70-mer oligonucleotides and cDNAs for microarray analysis of gene expression in Arabidopsis and its related species. , 2004, Plant biotechnology journal.

[81]  P. Quail,et al.  phyB is evolutionarily conserved and constitutively expressed in rice seedling shoots , 1991, Molecular and General Genetics MGG.

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

[83]  C. Pál,et al.  The evolutionary dynamics of eukaryotic gene order , 2004, Nature Reviews Genetics.

[84]  N. Yamamoto,et al.  Functional Analysis and Intracellular Localization of Rice Cryptochromes , 2003, Plant Physiology.

[85]  S. D. Rider,et al.  Light induces phenylpropanoid metabolism in Arabidopsis roots. , 2004, The Plant journal : for cell and molecular biology.

[86]  Cornelia I Bargmann,et al.  Comparing genomic expression patterns across species identifies shared transcriptional profile in aging , 2004, Nature Genetics.

[87]  D. Botstein,et al.  Cluster analysis and display of genome-wide expression patterns. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[88]  R. Wing,et al.  Toward a cytological characterization of the rice genome. , 2001, Genome research.

[89]  Wen-Hsiung Li,et al.  Dating the Monocot–Dicot Divergence and the Origin of Core Eudicots Using Whole Chloroplast Genomes , 2004, Journal of Molecular Evolution.

[90]  Melanie J Correll,et al.  Phytochromes A and B Mediate Red-Light-Induced Positive Phototropism in Roots1 , 2003, Plant Physiology.

[91]  W. Briggs,et al.  Distribution of Phytochrome in Etiolated Seedlings. , 1965, Plant physiology.

[92]  John D. Storey,et al.  Statistical significance for genomewide studies , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[93]  Che-Jun Pjon,et al.  PHYTOCHROME ACTION IN ORYZA SATIVA L. I. GROWTH RESPONSES OF ETIOLATED COLEOPTILES TO RED, FAR-RED AND BLUE LIGHT , 1967 .

[94]  Stefan R. Henz,et al.  A gene expression map of Arabidopsis thaliana development , 2005, Nature Genetics.

[95]  B. Gaut,et al.  Does recombination shape the distribution and evolution of tandemly arrayed genes (TAGs) in the Arabidopsis thaliana genome? , 2003, Genome research.

[96]  J. Ohlrogge,et al.  Microarray analysis of developing Arabidopsis seeds. , 2000, Plant physiology.

[97]  E..  Dynamic Regulation of Chloroplast Transcription’ , 2002 .

[98]  Jian Wang,et al.  BGI-RIS: an integrated information resource and comparative analysis workbench for rice genomics , 2004, Nucleic Acids Res..

[99]  Matthew E. Hudson,et al.  Identification of Promoter Motifs Involved in the Network of Phytochrome A-Regulated Gene Expression by Combined Analysis of Genomic Sequence and Microarray Data1[w] , 2003, Plant Physiology.

[100]  W. Terzaghi,et al.  Light-Regulated Transcription , 1995 .

[101]  M. Delseny,et al.  The Arabidopsis thaliana genome project , 1997 .