Comparative Network Analysis Reveals That Tissue Specificity and Gene Function Are Important Factors Influencing the Mode of Expression Evolution in Arabidopsis and Rice1[W]

Microarray experiments have yielded massive amounts of expression information measured under various conditions for the model species Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa). Expression compendia grouping multiple experiments make it possible to define correlated gene expression patterns within one species and to study how expression has evolved between species. We developed a robust framework to measure expression context conservation (ECC) and found, by analyzing 4,630 pairs of orthologous Arabidopsis and rice genes, that 77% showed conserved coexpression. Examples of nonconserved ECC categories suggested a link between regulatory evolution and environmental adaptations and included genes involved in signal transduction, response to different abiotic stresses, and hormone stimuli. To identify genomic features that influence expression evolution, we analyzed the relationship between ECC, tissue specificity, and protein evolution. Tissue-specific genes showed higher expression conservation compared with broadly expressed genes but were fast evolving at the protein level. No significant correlation was found between protein and expression evolution, implying that both modes of gene evolution are not strongly coupled in plants. By integration of cis-regulatory elements, many ECC conserved genes were significantly enriched for shared DNA motifs, hinting at the conservation of ancestral regulatory interactions in both model species. Surprisingly, for several tissue-specific genes, patterns of concerted network evolution were observed, unveiling conserved coexpression in the absence of conservation of tissue specificity. These findings demonstrate that orthologs inferred through sequence similarity in many cases do not share similar biological functions and highlight the importance of incorporating expression information when comparing genes across species.

[1]  Mario Medvedovic,et al.  A new method to remove hybridization bias for interspecies comparison of global gene expression profiles uncovers an association between mRNA sequence divergence and differential gene expression in Xenopus , 2006, Nucleic acids research.

[2]  Eugene V Koonin,et al.  Evolutionary significance of gene expression divergence. , 2005, Gene.

[3]  Eduardo P C Rocha,et al.  An analysis of determinants of amino acids substitution rates in bacterial proteins. , 2004, Molecular biology and evolution.

[4]  Bernardo Lemos,et al.  Evolution of proteins and gene expression levels are coupled in Drosophila and are independently associated with mRNA abundance, protein length, and number of protein-protein interactions. , 2005, Molecular biology and evolution.

[5]  Jan-Peter Nap,et al.  Local Coexpression Domains of Two to Four Genes in the Genome of Arabidopsis1[w] , 2005, Plant Physiology.

[6]  Wen-Hsiung Li,et al.  External factors accelerate expression divergence between duplicate genes. , 2007, Trends in genetics : TIG.

[7]  J. Slate,et al.  Global patterns of gene expression in rice cultivars undergoing a susceptible or resistant interaction with the parasitic plant Striga hermonthica. , 2008, The New phytologist.

[8]  Dirk Inzé,et al.  CORNET: A User-Friendly Tool for Data Mining and Integration1[W] , 2010, Plant Physiology.

[9]  Stephane Rombauts,et al.  How many genes are there in plants (... and why are they there)? , 2007, Current opinion in plant biology.

[10]  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.

[11]  Klaas Vandepoele,et al.  Exploring the Plant Transcriptome through Phylogenetic Profiling1[w] , 2005, Plant Physiology.

[12]  Imre Vastrik,et al.  Arabidopsis Reactome: A Foundation Knowledgebase for Plant Systems Biology[W] , 2008, The Plant Cell Online.

[13]  Olga G. Troyanskaya,et al.  Accurate Quantification of Functional Analogy among Close Homologs , 2011, PLoS Comput. Biol..

[14]  A. Mustroph,et al.  Cross-Kingdom Comparison of Transcriptomic Adjustments to Low-Oxygen Stress Highlights Conserved and Plant-Specific Responses1[W][OA] , 2010, Plant Physiology.

[15]  L. MacNeil,et al.  Gene regulatory networks and the role of robustness and stochasticity in the control of gene expression. , 2011, Genome research.

[16]  A. Regev,et al.  Conservation and evolvability in regulatory networks: the evolution of ribosomal regulation in yeast. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[17]  L. Stein,et al.  Comparative genomics between rice and Arabidopsis shows scant collinearity in gene order. , 2001, Genome research.

[18]  Y. van de Peer,et al.  PLAZA: A Comparative Genomics Resource to Study Gene and Genome Evolution in Plants[W] , 2009, The Plant Cell Online.

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

[20]  Naama Barkai,et al.  Evolution of gene sequence and gene expression are not correlated in yeast. , 2008, Trends in genetics : TIG.

[21]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[22]  David G. Knowles,et al.  Functional Divergence of Duplicated Genes , 2011 .

[23]  Guillaume Blanc,et al.  Functional Divergence of Duplicated Genes Formed by Polyploidy during Arabidopsis Evolution , 2004, The Plant Cell Online.

[24]  S. Orzechowski.  Starch metabolism in leaves. , 2008, Acta biochimica Polonica.

[25]  Joshua M. Stuart,et al.  A Gene-Coexpression Network for Global Discovery of Conserved Genetic Modules , 2003, Science.

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

[27]  P. Bork,et al.  Co-evolution of transcriptional and post-translational cell-cycle regulation , 2006, Nature.

[28]  Pascal Condamine,et al.  Comparative Transcriptional Profiling of Two Contrasting Rice Genotypes under Salinity Stress during the Vegetative Growth Stage1[w] , 2005, Plant Physiology.

[29]  Ziheng Yang,et al.  PAML: a program package for phylogenetic analysis by maximum likelihood , 1997, Comput. Appl. Biosci..

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

[31]  G. Church,et al.  Identifying regulatory networks by combinatorial analysis of promoter elements , 2001, Nature Genetics.

[32]  J. Raes,et al.  The automatic detection of homologous regions (ADHoRe) and its application to microcolinearity between Arabidopsis and rice. , 2002, Genome research.

[33]  B. Usadel,et al.  PlaNet: Combined Sequence and Expression Comparisons across Plant Networks Derived from Seven Species[W][OA] , 2011, Plant Cell.

[34]  Fang-fang Fu,et al.  Coexpression Analysis Identifies Rice Starch Regulator1, a Rice AP2/EREBP Family Transcription Factor, as a Novel Rice Starch Biosynthesis Regulator1[W][OA] , 2010, Plant Physiology.

[35]  S. Rhee,et al.  MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. , 2004, The Plant journal : for cell and molecular biology.

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

[37]  Kengo Kinoshita,et al.  Coexpression landscape in ATTED-II: usage of gene list and gene network for various types of pathways , 2010, Journal of Plant Research.

[38]  Wei-Po Lee,et al.  Computational methods for discovering gene networks from expression data , 2009, Briefings Bioinform..

[39]  K. H. Wolfe,et al.  Divergence of spatial gene expression profiles following species-specific gene duplications in human and mouse. , 2004, Genome research.

[40]  Esther T. Chan,et al.  Conservation of core gene expression in vertebrate tissues , 2009, Journal of biology.

[41]  B. Snel,et al.  A global definition of expression context is conserved between orthologs, but does not correlate with sequence conservation , 2006, BMC Genomics.

[42]  Yoshiyuki Ogata,et al.  Approaches for extracting practical information from gene co-expression networks in plant biology. , 2007, Plant & cell physiology.

[43]  W. R. Whalley,et al.  A bioinformatic and transcriptomic approach to identifying positional candidate genes without fine mapping: an example using rice root-growth QTLs. , 2008, Genomics.

[44]  J. Nap,et al.  Local coexpression domains in the genome of rice show no microsynteny with Arabidopsis domains , 2007, Plant Molecular Biology.

[45]  Ziv Bar-Joseph,et al.  Cross species analysis of microarray expression data , 2009, Bioinform..

[46]  Yves Van de Peer,et al.  In situ analysis of cross-hybridisation on microarrays and the inference of expression correlation , 2007, BMC Bioinformatics.

[47]  K. Hastings.  Strong evolutionary conservation of broadly expressed protein isoforms in the troponin I gene family and other vertebrate gene families , 1996, Journal of Molecular Evolution.

[48]  M. Robinson‐Rechavi,et al.  How confident can we be that orthologs are similar, but paralogs differ? , 2009, Trends in genetics : TIG.

[49]  E. Bornberg-Bauer,et al.  The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. , 2007, The Plant journal : for cell and molecular biology.

[50]  Naama Barkai,et al.  Comparative biology: beyond sequence analysis. , 2007, Current opinion in biotechnology.

[51]  Wen-Hsiung Li,et al.  Divergence in the spatial pattern of gene expression between human duplicate genes. , 2003, Genome research.

[52]  Saranyan K. Palaniswamy,et al.  AGRIS and AtRegNet. A Platform to Link cis-Regulatory Elements and Transcription Factors into Regulatory Networks1[W][OA] , 2006, Plant Physiology.

[53]  Jianzhi Zhang,et al.  Evolutionary conservation of expression profiles between human and mouse orthologous genes. , 2006, Molecular biology and evolution.

[54]  John M. Walker,et al.  Comparative Genomics , 2007, Methods In Molecular Biology™.

[55]  A. Loraine,et al.  A regulon conserved in monocot and dicot plants defines a functional module in antifungal plant immunity , 2010, Proceedings of the National Academy of Sciences.

[56]  A. Loraine,et al.  Assembly of an Interactive Correlation Network for the Arabidopsis Genome Using a Novel Heuristic Clustering Algorithm1[W] , 2009, Plant Physiology.

[57]  Mukesh Jain,et al.  F-Box Proteins in Rice. Genome-Wide Analysis, Classification, Temporal and Spatial Gene Expression during Panicle and Seed Development, and Regulation by Light and Abiotic Stress1[W][OA] , 2007, Plant Physiology.

[58]  Klaas Vandepoele,et al.  Unraveling Transcriptional Control in Arabidopsis Using cis-Regulatory Elements and Coexpression Networks1[C][W] , 2009, Plant Physiology.

[59]  L. Duret,et al.  Determinants of substitution rates in mammalian genes: expression pattern affects selection intensity but not mutation rate. , 2000, Molecular biology and evolution.

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

[61]  Rafael A Irizarry,et al.  Exploration, normalization, and summaries of high density oligonucleotide array probe level data. , 2003, Biostatistics.

[62]  David Meinke,et al.  Identifying essential genes in Arabidopsis thaliana. , 2008, Trends in plant science.

[63]  J. Trygg,et al.  A cross-species transcriptomics approach to identify genes involved in leaf development , 2008, BMC Genomics.

[64]  T. Pham,et al.  RiceArrayNet: A Database for Correlating Gene Expression from Transcriptome Profiling, and Its Application to the Analysis of Coexpressed Genes in Rice1[C][W][OA] , 2009, Plant Physiology.

[65]  Julie D Thompson,et al.  Multiple Sequence Alignment Using ClustalW and ClustalX , 2003, Current protocols in bioinformatics.