A genome scale metabolic network for rice and accompanying analysis of tryptophan, auxin and serotonin biosynthesis regulation under biotic stress

BackgroundFunctional annotations of large plant genome projects mostly provide information on gene function and gene families based on the presence of protein domains and gene homology, but not necessarily in association with gene expression or metabolic and regulatory networks. These additional annotations are necessary to understand the physiology, development and adaptation of a plant and its interaction with the environment.ResultsRiceCyc is a metabolic pathway networks database for rice. It is a snapshot of the substrates, metabolites, enzymes, reactions and pathways of primary and intermediary metabolism in rice. RiceCyc version 3.3 features 316 pathways and 6,643 peptide-coding genes mapped to 2,103 enzyme-catalyzed and 87 protein-mediated transport reactions. The initial functional annotations of rice genes with InterPro, Gene Ontology, MetaCyc, and Enzyme Commission (EC) numbers were enriched with annotations provided by KEGG and Gramene databases. The pathway inferences and the network diagrams were first predicted based on MetaCyc reference networks and plant pathways from the Plant Metabolic Network, using the Pathologic module of Pathway Tools. This was enriched by manually adding metabolic pathways and gene functions specifically reported for rice. The RiceCyc database is hierarchically browsable from pathway diagrams to the associated genes, metabolites and chemical structures. Through the integrated tool OMICs Viewer, users can upload transcriptomic, proteomic and metabolomic data to visualize expression patterns in a virtual cell. RiceCyc, along with additional species-specific pathway databases hosted in the Gramene project, facilitates comparative pathway analysis.ConclusionsHere we describe the RiceCyc network development and discuss its contribution to rice genome annotations. As a case study to demonstrate the use of RiceCyc network as a discovery environment we carried out an integrated bioinformatic analysis of rice metabolic genes that are differentially regulated under diurnal photoperiod and biotic stress treatments. The analysis of publicly available rice transcriptome datasets led to the hypothesis that the complete tryptophan biosynthesis and its dependent metabolic pathways including serotonin biosynthesis are induced by taxonomically diverse pathogens while also being under diurnal regulation. The RiceCyc database is available online for free access at http://www.gramene.org/pathway/.

[1]  Robert D. Finn,et al.  InterPro: the integrative protein signature database , 2008, Nucleic Acids Res..

[2]  P. Saxena,et al.  Melatonin and serotonin in flowers and fruits of Datura metel L. , 2009, Journal of pineal research.

[3]  Li-li Chen,et al.  A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21 , 1995, Science.

[4]  Tai Wang,et al.  Comparative proteomic study reveals the involvement of diurnal cycle in cell division, enlargement, and starch accumulation in developing endosperm of Oryza sativa. , 2012, Journal of proteome research.

[5]  D. Svergun,et al.  Studies on structure-function relationships of indolepyruvate decarboxylase from Enterobacter cloacae, a key enzyme of the indole acetic acid pathway. , 2003, European journal of biochemistry.

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

[7]  Wei Zhu,et al.  The Institute for Genomic Research Osa1 Rice Genome Annotation Database1 , 2005, Plant Physiology.

[8]  Ethalinda K. S. Cannon,et al.  Maize Metabolic Network Construction and Transcriptome Analysis , 2013 .

[9]  Lloyd W. Sumner,et al.  MedicCyc: a biochemical pathway database for Medicago truncatula , 2007, Bioinform..

[10]  Melissa D. Lehti-Shiu,et al.  Importance of Lineage-Specific Expansion of Plant Tandem Duplicates in the Adaptive Response to Environmental Stimuli1[W][OA] , 2008, Plant Physiology.

[11]  H. Kawaide,et al.  The main auxin biosynthesis pathway in Arabidopsis , 2011, Proceedings of the National Academy of Sciences.

[12]  Peter G Zhang,et al.  Extensive divergence in alternative splicing patterns after gene and genome duplication during the evolutionary history of Arabidopsis. , 2010, Molecular biology and evolution.

[13]  Efrain C Azmitia,et al.  Modern views on an ancient chemical: serotonin effects on cell proliferation, maturation, and apoptosis , 2001, Brain Research Bulletin.

[14]  Pankaj Jaiswal,et al.  Biological ontologies in rice databases. An introduction to the activities in Gramene and Oryzabase. , 2005, Plant & cell physiology.

[15]  Peter D. Karp,et al.  MetaCyc: a multiorganism database of metabolic pathways and enzymes. , 2004, Nucleic acids research.

[16]  Peter D. Karp,et al.  The MetaCyc Database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases , 2007, Nucleic Acids Res..

[17]  E. Marcotte,et al.  Genetic dissection of the biotic stress response using a genome-scale gene network for rice , 2011, Proceedings of the National Academy of Sciences.

[18]  Peter D. Karp,et al.  The Pathway Tools software , 2002, ISMB.

[19]  L. Romero,et al.  Cysteine homeostasis plays an essential role in plant immunity. , 2012, The New phytologist.

[20]  P. Saxena,et al.  Mammalian neurohormones: potential significance in reproductive physiology of St. John's wort (Hypericum perforatum L.)? , 2002, Naturwissenschaften.

[21]  K. San,et al.  Expression of the Arabidopsis feedback-insensitive anthranilate synthase holoenzyme and tryptophan decarboxylase genes in Catharanthus roseus hairy roots. , 2006, Journal of biotechnology.

[22]  H. Miyagawa,et al.  Characterization of tryptophan-overproducing potato transgenic for a mutant rice anthranilate synthase α-subunit gene (OASA1D) , 2005, Planta.

[23]  J. Chory,et al.  Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis , 2011, Proceedings of the National Academy of Sciences.

[24]  John Boyle,et al.  Cytoscape: a community-based framework for network modeling. , 2009, Methods in molecular biology.

[25]  Kevin L. Childs,et al.  Gene Coexpression Network Analysis as a Source of Functional Annotation for Rice Genes , 2011, PloS one.

[26]  Y. Charng,et al.  Recent Gene Duplication and Subfunctionalization Produced a Mitochondrial GrpE, the Nucleotide Exchange Factor of the Hsp70 Complex, Specialized in Thermotolerance to Chronic Heat Stress in Arabidopsis1[W][OA] , 2011, Plant Physiology.

[27]  Reuben J. Peters,et al.  Identification of Syn-Pimara-7,15-Diene Synthase Reveals Functional Clustering of Terpene Synthases Involved in Rice Phytoalexin/Allelochemical Biosynthesis1 , 2004, Plant Physiology.

[28]  M. Yano,et al.  Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Suzanne M. Paley,et al.  Browsing metabolic and regulatory networks with BioCyc. , 2012, Methods in molecular biology.

[30]  J. Slovin,et al.  Two genetically discrete pathways convert tryptophan to auxin: more redundancy in auxin biosynthesis. , 2003, Trends in plant science.

[31]  K. Back,et al.  Production of serotonin by dual expression of tryptophan decarboxylase and tryptamine 5-hydroxylase in Escherichia coli , 2011, Applied Microbiology and Biotechnology.

[32]  M. Freeling,et al.  The evolutionary position of subfunctionalization, downgraded. , 2008, Genome dynamics.

[33]  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.

[34]  Wenying Xu,et al.  Transcriptome Phase Distribution Analysis Reveals Diurnal Regulated Biological Processes and Key Pathways in Rice Flag Leaves and Seedling Leaves , 2011, PloS one.

[35]  Yunde Zhao.  Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. , 2012, Molecular plant.

[36]  J. Kyozuka,et al.  Direct control of shoot meristem activity by a cytokinin-activating enzyme , 2007, Nature.

[37]  Insuk Lee,et al.  Towards Establishment of a Rice Stress Response Interactome , 2011, PLoS genetics.

[38]  Pankaj Jaiswal,et al.  Gramene database: a hub for comparative plant genomics. , 2011, Methods in molecular biology.

[39]  A. K. Grennan.  Genevestigator. Facilitating Web-Based Gene-Expression Analysis , 2006, Plant Physiology.

[40]  F. Legeai,et al.  Predotar: A tool for rapidly screening proteomes for N‐terminal targeting sequences , 2004, Proteomics.

[41]  P. Karp,et al.  Creation of a Genome-Wide Metabolic Pathway Database for Populus trichocarpa Using a New Approach for Reconstruction and Curation of Metabolic Pathways for Plants1[W][OA] , 2010, Plant Physiology.

[42]  Joanne Chory,et al.  Rapid Synthesis of Auxin via a New Tryptophan-Dependent Pathway Is Required for Shade Avoidance in Plants , 2008, Cell.

[43]  H. Fukuda,et al.  Functional Analyses of LONELY GUY Cytokinin-Activating Enzymes Reveal the Importance of the Direct Activation Pathway in Arabidopsis[W][OA] , 2009, The Plant Cell Online.

[44]  T. Kiba,et al.  Arabidopsis lonely guy (LOG) multiple mutants reveal a central role of the LOG-dependent pathway in cytokinin activation. , 2012, The Plant journal : for cell and molecular biology.

[45]  Pankaj Jaiswal,et al.  Global Profiling of Rice and Poplar Transcriptomes Highlights Key Conserved Circadian-Controlled Pathways and cis-Regulatory Modules , 2011, PloS one.

[46]  L. Quek,et al.  C4GEM, a Genome-Scale Metabolic Model to Study C4 Plant Metabolism1[W][OA] , 2010, Plant Physiology.

[47]  W. Martin,et al.  Purification and cDNA cloning of anthranilate synthase from Ruta graveolens: modes of expression and properties of native and recombinant enzymes. , 1995, The Plant journal : for cell and molecular biology.

[48]  Henry D. Priest,et al.  Genome-wide mapping of alternative splicing in Arabidopsis thaliana. , 2010, Genome research.

[49]  A. Hall,et al.  A Role for Multiple Circadian Clock Genes in the Response to Signals That Break Seed Dormancy in Arabidopsis[W] , 2009, The Plant Cell Online.

[50]  F. Matsuda,et al.  Integrated metabolomic and transcriptomic analyses of high-tryptophan rice expressing a mutant anthranilate synthase alpha subunit. , 2007, Journal of experimental botany.

[51]  P. Zimmermann,et al.  Gene-expression analysis and network discovery using Genevestigator. , 2005, Trends in plant science.

[52]  Fumio Matsuda,et al.  High-level tryptophan accumulation in seeds of transgenic rice and its limited effects on agronomic traits and seed metabolite profile. , 2006, Journal of experimental botany.

[53]  Edward S. Buckler,et al.  Gramene database in 2010: updates and extensions , 2010, Nucleic Acids Res..

[54]  C. Forst,et al.  Significance of two distinct types of tryptophan synthase beta chain in Bacteria, Archaea and higher plants , 2001, Genome Biology.

[55]  G. Galili,et al.  Principal Transcriptional Programs Regulating Plant Amino Acid Metabolism in Response to Abiotic Stresses1[W][OA] , 2008, Plant Physiology.

[56]  K. Back,et al.  Tryptamine 5‐hydroxylase‐deficient Sekiguchi rice induces synthesis of 5‐hydroxytryptophan and N‐acetyltryptamine but decreases melatonin biosynthesis during senescence process of detached leaves , 2012, Journal of pineal research.

[57]  R. Last,et al.  The Arabidopsis thaliana trp5 Mutant Has a Feedback-Resistant Anthranilate Synthase and Elevated Soluble Tryptophan , 1996, Plant physiology.

[58]  Xiang-Dong Fu,et al.  Timing of plant immune responses by a central circadian regulator , 2011, Nature.

[59]  Robert D. Finn,et al.  InterPro in 2011: new developments in the family and domain prediction database , 2011, Nucleic acids research.

[60]  R. Verpoorte,et al.  Purification and characterization of anthranilate synthase from Catharanthus roseus. , 1993, European journal of biochemistry.

[61]  K. Shimamoto,et al.  Sekiguchi Lesion Gene Encodes a Cytochrome P450 Monooxygenase That Catalyzes Conversion of Tryptamine to Serotonin in Rice* , 2010, The Journal of Biological Chemistry.

[62]  Susumu Goto,et al.  KEGG for integration and interpretation of large-scale molecular data sets , 2011, Nucleic Acids Res..

[63]  S. Sideris,et al.  The cloned gene, Xa21, confers resistance to multiple Xanthomonas oryzae pv. oryzae isolates in transgenic plants. , 1996, Molecular plant-microbe interactions : MPMI.

[64]  P. Zimmermann,et al.  GENEVESTIGATOR. Arabidopsis Microarray Database and Analysis Toolbox1[w] , 2004, Plant Physiology.

[65]  Young-soon Kim,et al.  Light‐regulated melatonin biosynthesis in rice during the senescence process in detached leaves , 2012, Journal of pineal research.

[66]  E. Tobin,et al.  A Role for Protein Kinase Casein Kinase2 α-Subunits in the Arabidopsis Circadian Clock1[W][OA] , 2011, Plant Physiology.

[67]  A. Ishihara,et al.  Induction of serotonin accumulation by feeding of rice striped stem borer in rice leaves , 2008, Plant signaling & behavior.

[68]  Kazunori Okada,et al.  Identification of a Biosynthetic Gene Cluster in Rice for Momilactones* , 2007, Journal of Biological Chemistry.

[69]  Erik L. L. Sonnhammer,et al.  A Hidden Markov Model for Predicting Transmembrane Helices in Protein Sequences , 1998, ISMB.

[70]  I. Lee,et al.  Characterization of the altered anthranilate synthase in 5-methyltryptophan-resistant rice mutants , 2005, Plant Cell Reports.

[71]  Arnab Roy,et al.  Functional characterization of the rice kaurene synthase-like gene family. , 2007, Phytochemistry.

[72]  F. Matsuda,et al.  The tryptophan pathway is involved in the defense responses of rice against pathogenic infection via serotonin production. , 2008, The Plant journal : for cell and molecular biology.

[73]  A. Ishihara,et al.  Probing the role of tryptophan-derived secondary metabolism in defense responses against Bipolaris oryzae infection in rice leaves by a suicide substrate of tryptophan decarboxylase. , 2011, Phytochemistry.

[74]  R. Last,et al.  Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. , 1995, The Plant cell.

[75]  Vladimir B Bajic,et al.  Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of japonica rice to chilling stress , 2010, BMC Plant Biology.

[76]  Anna N. Stepanova,et al.  TAA1-Mediated Auxin Biosynthesis Is Essential for Hormone Crosstalk and Plant Development , 2008, Cell.

[77]  H. Miyagawa,et al.  Metabolic flux analysis in plants using dynamic labeling technique: application to tryptophan biosynthesis in cultured rice cells. , 2007, Phytochemistry.

[78]  P. Kaiser,et al.  Protein degradation and the stress response. , 2012, Seminars in cell & developmental biology.

[79]  Yunde Zhao.  Auxin biosynthesis and its role in plant development. , 2010, Annual review of plant biology.

[80]  V. V. Roshchina,et al.  Neurotransmitters in Plant Life , 2001 .

[81]  C. Maranas,et al.  Zea mays iRS1563: A Comprehensive Genome-Scale Metabolic Reconstruction of Maize Metabolism , 2011, PloS one.

[82]  D. Choi,et al.  Induction of serotonin biosynthesis is uncoupled from the coordinated induction of tryptophan biosynthesis in pepper fruits (Capsicum annuum) upon pathogen infection , 2009, Planta.

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

[84]  Hur-Song Chang,et al.  Transcriptional Profiling Reveals Novel Interactions between Wounding, Pathogen, Abiotic Stress, and Hormonal Responses in Arabidopsis1,212 , 2002, Plant Physiology.

[85]  Ali Masoudi-Nejad,et al.  EGENES: Transcriptome-Based Plant Database of Genes with Metabolic Pathway Information and Expressed Sequence Tag Indices in KEGG1[C][W][OA] , 2007, Plant Physiology.

[86]  S. Brunak,et al.  Locating proteins in the cell using TargetP, SignalP and related tools , 2007, Nature Protocols.

[87]  Peter D. Karp,et al.  MetaCyc: a multiorganism database of metabolic pathways and enzymes , 2005, Nucleic Acids Res..

[88]  Chien-Chen Lai,et al.  Serotonin accumulation in transgenic rice by over-expressing tryptophan decarboxlyase results in a dark brown phenotype and stunted growth , 2012, Plant Molecular Biology.

[89]  Young-soon Kim,et al.  Senescence-Induced Serotonin Biosynthesis and Its Role in Delaying Senescence in Rice Leaves1[C][W][OA] , 2009, Plant Physiology.

[90]  Patrick Lambrix,et al.  Representations of molecular pathways: an evaluation of SBML, PSI MI and BioPAX , 2005, Bioinform..

[91]  Y. Benjamini,et al.  More powerful procedures for multiple significance testing. , 1990, Statistics in medicine.

[92]  Connor W. McEntee,et al.  Network Discovery Pipeline Elucidates Conserved Time-of-Day–Specific cis-Regulatory Modules , 2007, PLoS genetics.

[93]  Meimei Xu,et al.  Functional identification of rice syn-copalyl diphosphate synthase and its role in initiating biosynthesis of diterpenoid phytoalexin/allelopathic natural products. , 2004, The Plant journal : for cell and molecular biology.

[94]  Peter D. Karp,et al.  MetaCyc and AraCyc. Metabolic Pathway Databases for Plant Research1[w] , 2005, Plant Physiology.

[95]  K. Wakasa,et al.  In vitro reconstitution of rice anthranilate synthase: distinct functional properties of the α subunits OASA1 and OASA2 , 2004, Plant Molecular Biology.

[96]  R. Last,et al.  Coordinate regulation of the tryptophan biosynthetic pathway and indolic phytoalexin accumulation in Arabidopsis. , 1996, The Plant cell.

[97]  J. Phillipson,et al.  Anthranilate synthase in microorganisms and plants. , 1995, Phytochemistry.