Beyond Genomics: Studying Evolution with Gene Coexpression Networks.

Understanding how genomes change as organisms become more complex is a central question in evolution. Molecular evolutionary studies typically correlate the appearance of genes and gene families with the emergence of biological pathways and morphological features. While such approaches are of great importance to understand how organisms evolve, they are also limited, as functionally related genes work together in contexts of dynamic gene networks. Since functionally related genes are often transcriptionally coregulated, gene coexpression networks present a resource to study the evolution of biological pathways. In this opinion article, we discuss recent developments in this field and how coexpression analyses can be merged with existing genomic approaches to transfer functional knowledge between species to study the appearance or extension of pathways.

[1]  Christophe Périn,et al.  GreenPhylDB: a database for plant comparative genomics , 2007, Nucleic Acids Res..

[2]  J. Petrášek,et al.  Evolution and Structural Diversification of PILS Putative Auxin Carriers in Plants , 2012, Front. Plant Sci..

[3]  G. Jürgens,et al.  Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation , 2003, Cell.

[4]  K. H. Wolfe,et al.  Functional Partitioning of Yeast Co-Expression Networks after Genome Duplication , 2006, PLoS biology.

[5]  C. Kuhlemeier,et al.  Auxin Regulates the Initiation and Radial Position of Plant Lateral Organs , 2000, Plant Cell.

[6]  Y. van de Peer,et al.  Dissecting Plant Genomes with the PLAZA Comparative Genomics Platform1[W] , 2011, Plant Physiology.

[7]  Fumiko Ohta,et al.  Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D , 2004, Nature.

[8]  Royston Goodacre,et al.  Identification of Novel Genes in Arabidopsis Involved in Secondary Cell Wall Formation Using Expression Profiling and Reverse Genetics , 2005, The Plant Cell Online.

[9]  S. Carroll,et al.  Gene co-option in physiological and morphological evolution. , 2002, Annual review of cell and developmental biology.

[10]  D. Goring,et al.  The diversity of plant U-box E3 ubiquitin ligases: from upstream activators to downstream target substrates. , 2009, Journal of experimental botany.

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

[12]  J. Bowman,et al.  Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation , 2010, Development.

[13]  R. Zhong,et al.  Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. , 2010, Trends in plant science.

[14]  R. Tsien,et al.  Specificity and Stability in Topology of Protein Networks , 2022 .

[15]  S. Pongor,et al.  The quest for orthologs: finding the corresponding gene across genomes. , 2008, Trends in genetics : TIG.

[16]  Takuji Sasaki,et al.  The map-based sequence of the rice genome , 2005, Nature.

[17]  Kengo Kinoshita,et al.  ATTED-II in 2016: A Plant Coexpression Database Towards Lineage-Specific Coexpression , 2015, Plant & cell physiology.

[18]  Jan Petrásek,et al.  Auxin transport routes in plant development , 2009, Development.

[19]  Casey S. Greene,et al.  Functional Knowledge Transfer for High-accuracy Prediction of Under-studied Biological Processes , 2013, PLoS Comput. Biol..

[20]  Staffan Persson,et al.  Co-expression tools for plant biology: opportunities for hypothesis generation and caveats. , 2009, Plant, cell & environment.

[21]  A. Murphy,et al.  Arabidopsis PIS1 encodes the ABCG37 transporter of auxinic compounds including the auxin precursor indole-3-butyric acid , 2010, Proceedings of the National Academy of Sciences.

[22]  M. Mutwil,et al.  Tools of the trade: studying molecular networks in plants. , 2016, Current opinion in plant biology.

[23]  M. Mutwil,et al.  Elucidating gene function and function evolution through comparison of co-expression networks of plants , 2014, Front. Plant Sci..

[24]  Stuart A. Casson,et al.  KNAT6 gene of Arabidopsis is expressed in roots and is required for correct lateral root formation , 2004, Plant Molecular Biology.

[25]  Dirk Inzé,et al.  CORNET 2.0: integrating plant coexpression, protein-protein interactions, regulatory interactions, gene associations and functional annotations. , 2012, The New phytologist.

[26]  Klaas Vandepoele,et al.  Comparative Network Analysis Reveals That Tissue Specificity and Gene Function Are Important Factors Influencing the Mode of Expression Evolution in Arabidopsis and Rice1[W] , 2011, Plant Physiology.

[27]  K. Vandepoele,et al.  Comparative co-expression analysis in plant biology. , 2012, Plant, cell & environment.

[28]  Kenneth D. Birnbaum,et al.  The potential of single-cell profiling in plants , 2016, Genome Biology.

[29]  C. Lapierre,et al.  Evolution of a Novel Phenolic Pathway for Pollen Development , 2009, Science.

[30]  J. Bennetzen,et al.  The Physcomitrella Genome Reveals Evolutionary Insights into the Conquest of Land by Plants , 2008, Science.

[31]  Staffan Persson,et al.  Large-Scale Co-Expression Approach to Dissect Secondary Cell Wall Formation Across Plant Species , 2011, Front. Plant Sci..

[32]  David M. Goodstein,et al.  Phytozome: a comparative platform for green plant genomics , 2011, Nucleic Acids Res..

[33]  Loren H Rieseberg,et al.  Reconstructing patterns of reticulate evolution in plants. , 2004, American journal of botany.

[34]  Klaas Vandepoele,et al.  CoExpNetViz: Comparative Co-Expression Networks Construction and Visualization Tool , 2016, Front. Plant Sci..

[35]  Riet De Smet,et al.  Redundancy and rewiring of genetic networks following genome-wide duplication events. , 2012, Current opinion in plant biology.

[36]  Douglas G. Scofield,et al.  The Norway spruce genome sequence and conifer genome evolution , 2013, Nature.

[37]  Elliot M. Meyerowitz,et al.  Antagonistic Regulation of PIN Phosphorylation by PP2A and PINOID Directs Auxin Flux , 2007, Cell.

[38]  Marcel Dicke,et al.  Rewiring of the Jasmonate Signaling Pathway in Arabidopsis during Insect Herbivory , 2011, Front. Plant Sci..

[39]  Sandrine Dudoit,et al.  Polygenic and directional regulatory evolution across pathways in Saccharomyces , 2010, Proceedings of the National Academy of Sciences.

[40]  Ondřej Novák,et al.  Arabidopsis WAT1 is a vacuolar auxin transport facilitator required for auxin homoeostasis , 2013, Nature Communications.

[41]  Sara L. Zimmer,et al.  The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions , 2007, Science.

[42]  Kevin Vanneste,et al.  Inference of genome duplications from age distributions revisited. , 2013, Molecular biology and evolution.

[43]  C. Pál,et al.  Dosage sensitivity and the evolution of gene families in yeast , 2003, Nature.

[44]  C. Hardtke,et al.  Vascular continuity and auxin signals. , 2000, Trends in plant science.

[45]  B. Honig,et al.  Structure-based prediction of protein-protein interactions on a genome-wide scale , 2012, Nature.

[46]  N. Friedman,et al.  Natural history and evolutionary principles of gene duplication in fungi , 2007, Nature.

[47]  M. Estelle,et al.  Constitutive auxin response in Physcomitrella reveals complex interactions between Aux/IAA and ARF proteins , 2016, eLife.

[48]  J. Bowman,et al.  Radial Patterning of Arabidopsis Shoots by Class III HD-ZIP and KANADI Genes , 2003, Current Biology.

[49]  Sarah A Teichmann,et al.  Novel specificities emerge by stepwise duplication of functional modules. , 2005, Genome research.

[50]  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.

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

[52]  S. Shabala,et al.  Linking stomatal traits and expression of slow anion channel genes HvSLAH1 and HvSLAC1 with grain yield for increasing salinity tolerance in barley , 2014, Front. Plant Sci..

[53]  Daniel W. A. Buchan,et al.  A large-scale evaluation of computational protein function prediction , 2013, Nature Methods.

[54]  Klaus Palme,et al.  Auxin transport inhibitors block PIN1 cycling and vesicle trafficking , 2001, Nature.

[55]  Elise A. R. Serin,et al.  Learning from Co-expression Networks: Possibilities and Challenges , 2016, Front. Plant Sci..

[56]  T. Kakimoto CKI1, a Histidine Kinase Homolog Implicated in Cytokinin Signal Transduction , 1996, Science.

[57]  Peter J. Bickel,et al.  Comparative Analysis of the Transcriptome across Distant Species , 2014, Nature.

[58]  Hyojin Kim,et al.  AraNet v2: an improved database of co-functional gene networks for the study of Arabidopsis thaliana and 27 other nonmodel plant species , 2014, Nucleic Acids Res..

[59]  Matthew D. Wilkerson,et al.  PlantGDB: a resource for comparative plant genomics , 2007, Nucleic Acids Res..

[60]  Rachel B. Brem,et al.  Polygenic evolution of a sugar specialization trade-off in yeast , 2016, Nature.

[61]  S. Turner,et al.  PXY, a Receptor-like Kinase Essential for Maintaining Polarity during Plant Vascular-Tissue Development , 2007, Current Biology.

[62]  H. Lehrach,et al.  A Human Protein-Protein Interaction Network: A Resource for Annotating the Proteome , 2005, Cell.

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

[64]  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.

[65]  R. Shamir,et al.  The MORPH Algorithm: Ranking Candidate Genes for Membership in Arabidopsis and Tomato Pathways[C][W] , 2012, Plant Cell.

[66]  M. Strnad,et al.  Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins , 2014, Nature Communications.

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

[68]  A. Fernie,et al.  FamNet: A Framework to Identify Multiplied Modules Driving Pathway Expansion in Plants1 , 2016, Plant Physiology.

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

[70]  H. Doddapaneni,et al.  Cyanophora paradoxa Genome Elucidates Origin of Photosynthesis in Algae and Plants , 2012, Science.

[71]  Tomislav Domazet-Loso,et al.  A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages. , 2007, Trends in genetics : TIG.

[72]  N. Provart,et al.  BAR expressolog identification: expression profile similarity ranking of homologous genes in plant species. , 2012, The Plant journal : for cell and molecular biology.

[73]  F. Feltus,et al.  Gene Coexpression Network Alignment and Conservation of Gene Modules between Two Grass Species: Maize and Rice[C][W][OA] , 2011, Plant Physiology.

[74]  T. Ghosh,et al.  Expression Pattern Similarities Support the Prediction of Orthologs Retaining Common Functions after Gene Duplication Events1[OPEN] , 2016, Plant Physiology.

[75]  T. Greb,et al.  MOL1 is required for cambium homeostasis in Arabidopsis , 2016, The Plant journal : for cell and molecular biology.

[76]  K. Marchal,et al.  Genome-Scale Co-Expression Network Comparison across Escherichia coli and Salmonella enterica Serovar Typhimurium Reveals Significant Conservation at the Regulon Level of Local Regulators Despite Their Dissimilar Lifestyles , 2014, PloS one.

[77]  Kengo Kinoshita,et al.  ATTED-II Updates: Condition-Specific Gene Coexpression to Extend Coexpression Analyses and Applications to a Broad Range of Flowering Plants , 2011, Plant & cell physiology.

[78]  Hideyuki Suzuki,et al.  CoP: a database for characterizing co-expressed gene modules with biological information in plants , 2010, Bioinform..

[79]  Ari Pekka Mähönen,et al.  A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. , 2000, Genes & development.

[80]  Luis Serrano,et al.  Correlation of mRNA and protein in complex biological samples , 2009, FEBS letters.

[81]  S. Rhee,et al.  Towards revealing the functions of all genes in plants. , 2014, Trends in plant science.

[82]  Michael S. Barker,et al.  The Selaginella Genome Identifies Genetic Changes Associated with the Evolution of Vascular Plants , 2011, Science.

[83]  Staffan Persson,et al.  Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[84]  N. Provart,et al.  An extensive (co-)expression analysis tool for the cytochrome P450 superfamily in Arabidopsis thaliana , 2008, BMC Plant Biology.

[85]  Amborella Genome The Amborella Genome and the Evolution of Flowering Plants , 2013, Science.

[86]  Hailin Chen,et al.  STARNET 2: a web-based tool for accelerating discovery of gene regulatory networks using microarray co-expression data , 2009, BMC Bioinformatics.

[87]  M. Ikeuchi,et al.  Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation , 2014, Nature Communications.

[88]  Jonathan D. G. Jones,et al.  Evidence for Network Evolution in an Arabidopsis Interactome Map , 2011, Science.

[89]  Aaron R. Sharp,et al.  Genome Mapping in Plant Comparative Genomics. , 2016, Trends in plant science.

[90]  A. Theologis,et al.  Early Genes and Auxin Action , 1996, Plant physiology.