The Grapevine Expression Atlas Reveals a Deep Transcriptome Shift Driving the Entire Plant into a Maturation Program[W][OA]

The authors developed a comprehensive transcriptome atlas in grapevine by comparing the genes expressed in 54 diverse samples accounting for ∼91% of all known grapevine genes. Using a panel of different statistical techniques, they found that the whole plant undergoes transcriptomic reprogramming, driving it towards maturity. We developed a genome-wide transcriptomic atlas of grapevine (Vitis vinifera) based on 54 samples representing green and woody tissues and organs at different developmental stages as well as specialized tissues such as pollen and senescent leaves. Together, these samples expressed ∼91% of the predicted grapevine genes. Pollen and senescent leaves had unique transcriptomes reflecting their specialized functions and physiological status. However, microarray and RNA-seq analysis grouped all the other samples into two major classes based on maturity rather than organ identity, namely, the vegetative/green and mature/woody categories. This division represents a fundamental transcriptomic reprogramming during the maturation process and was highlighted by three statistical approaches identifying the transcriptional relationships among samples (correlation analysis), putative biomarkers (O2PLS-DA approach), and sets of strongly and consistently expressed genes that define groups (topics) of similar samples (biclustering analysis). Gene coexpression analysis indicated that the mature/woody developmental program results from the reiterative coactivation of pathways that are largely inactive in vegetative/green tissues, often involving the coregulation of clusters of neighboring genes and global regulation based on codon preference. This global transcriptomic reprogramming during maturation has not been observed in herbaceous annual species and may be a defining characteristic of perennial woody plants.

[1]  M. Delledonne,et al.  Transcriptomics and Metabolomics for the Analysis of Grape Berry Development , 2012 .

[2]  G. Bryan,et al.  The Transcriptome of the Reference Potato Genome Solanum tuberosum Group Phureja Clone DM1-3 516R44 , 2011, PloS one.

[3]  L. Beltramini,et al.  Osmotin from Calotropis procera latex: new insights into structure and antifungal properties. , 2011, Biochimica et biophysica acta.

[4]  M. Ventura,et al.  Analysis of high-identity segmental duplications in the grapevine genome , 2011, BMC Genomics.

[5]  Wei Li,et al.  Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis , 2011, Proceedings of the National Academy of Sciences.

[6]  G. Domont,et al.  Osmotin purified from the latex of Calotropis procera: biochemical characterization, biological activity and role in plant defense. , 2011, Plant physiology and biochemistry : PPB.

[7]  M. Moshelion,et al.  Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA? , 2011, The Plant journal : for cell and molecular biology.

[8]  Jeff H. Chang,et al.  Effector-triggered immunity blocks pathogen degradation of an immunity-associated vesicle traffic regulator in Arabidopsis , 2011, Proceedings of the National Academy of Sciences.

[9]  R. Sekhon,et al.  Genome-wide atlas of transcription during maize development. , 2011, The Plant journal : for cell and molecular biology.

[10]  R. Jetter,et al.  A Member of the PLEIOTROPIC DRUG RESISTANCE Family of ATP Binding Cassette Transporters Is Required for the Formation of a Functional Cuticle in Arabidopsis[W] , 2011, Plant Cell.

[11]  W. Peng,et al.  The Jasmonate-ZIM-Domain Proteins Interact with the WD-Repeat/bHLH/MYB Complexes to Regulate Jasmonate-Mediated Anthocyanin Accumulation and Trichome Initiation in Arabidopsis thaliana[C][W] , 2011, Plant Cell.

[12]  Claudia C Weber,et al.  Support for multiple classes of local expression clusters in Drosophila melanogaster, but no evidence for gene order conservation , 2011, Genome Biology.

[13]  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.

[14]  Yanbin Yin,et al.  Molecular Analysis of a Family of Arabidopsis Genes Related to Galacturonosyltransferases1[W][OA] , 2011, Plant Physiology.

[15]  L. Ponnala,et al.  Tissue- and Cell-Type Specific Transcriptome Profiling of Expanding Tomato Fruit Provides Insights into Metabolic and Regulatory Specialization and Cuticle Formation , 2011 .

[16]  M. S. Grando,et al.  A candidate gene association study on muscat flavor in grapevine (Vitis vinifera L.) , 2010, BMC Plant Biology.

[17]  Diane M. Martin,et al.  Functional Annotation, Genome Organization and Phylogeny of the Grapevine (Vitis vinifera) Terpene Synthase Gene Family Based on Genome Assembly, FLcDNA Cloning, and Enzyme Assays , 2010, BMC Plant Biology.

[18]  K. Lilley,et al.  Identification of Putative Stage-Specific Grapevine Berry Biomarkers and Omics Data Integration into Networks1[C][W][OA] , 2010, Plant Physiology.

[19]  Manuele Bicego,et al.  Biclustering of Expression Microarray Data with Topic Models , 2010, 2010 20th International Conference on Pattern Recognition.

[20]  Rex T. Nelson,et al.  RNA-Seq Atlas of Glycine max: A guide to the soybean transcriptome , 2010, BMC Plant Biology.

[21]  A. Covarrubias,et al.  Functional Analysis of the Group 4 Late Embryogenesis Abundant Proteins Reveals Their Relevance in the Adaptive Response during Water Deficit in Arabidopsis1[C][W][OA] , 2010, Plant Physiology.

[22]  A. Burlingame,et al.  Plant L10 Ribosomal Proteins Have Different Roles during Development and Translation under Ultraviolet-B Stress1[C][W][OA] , 2010, Plant Physiology.

[23]  Cole Trapnell,et al.  Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. , 2010, Nature biotechnology.

[24]  L. Altschmied,et al.  Promoters of the Barley Germin-Like GER4 Gene Cluster Enable Strong Transgene Expression in Response to Pathogen Attack[W][OA] , 2010, Plant Cell.

[25]  G. Malerba,et al.  Characterization of Transcriptional Complexity during Berry Development in Vitis vinifera Using RNA-Seq1[W] , 2010, Plant Physiology.

[26]  B. Ambrose,et al.  The Arabidopsis B-sister MADS-box protein, GORDITA, represses fruit growth and contributes to integument development. , 2010, The Plant journal : for cell and molecular biology.

[27]  Nozomu Sakurai,et al.  Large-scale analysis of full-length cDNAs from the tomato (Solanum lycopersicum) cultivar Micro-Tom, a reference system for the Solanaceae genomics , 2010, BMC Genomics.

[28]  Aureliano Bombarely,et al.  TobEA: an atlas of tobacco gene expression from seed to senescence , 2010, BMC Genomics.

[29]  Reza Salavati,et al.  Universal function-specificity of codon usage , 2009, Nucleic acids research.

[30]  D. Preuss,et al.  The extracellular lipase EXL4 is required for efficient hydration of Arabidopsis pollen , 2009, Sexual Plant Reproduction.

[31]  Lior Pachter,et al.  Sequence Analysis , 2020, Definitions.

[32]  Hongyu Zhao,et al.  A transcriptome atlas of rice cell types uncovers cellular, functional and developmental hierarchies , 2009, Nature Genetics.

[33]  F. Denoeud,et al.  Annotating genomes with massive-scale RNA sequencing , 2008, Genome Biology.

[34]  M. Delledonne,et al.  Molecular analysis of post-harvest withering in grape by AFLP transcriptional profiling , 2008, Journal of experimental botany.

[35]  C. Bailey,et al.  Plant Systematics: A Phylogenetic Approach , 2008 .

[36]  M. Hanana,et al.  Identification et caractérisation d'un gène de réponse à la déshydratation « rd22 » chez la vigne (Vitis vinifera L.) , 2008 .

[37]  J. T. Matus,et al.  Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes , 2008, BMC Plant Biology.

[38]  S. Chakraborty,et al.  Proteomics Approach to Identify Dehydration Responsive Nuclear Proteins from Chickpea (Cicer arietinum L.)*S , 2008, Molecular & Cellular Proteomics.

[39]  U. Edlund,et al.  Visualization of GC/TOF-MS-based metabolomics data for identification of biochemically interesting compounds using OPLS class models. , 2008, Analytical chemistry.

[40]  S. Song,et al.  Overexpression of AtMYB 44 Enhances Stomatal Closure to Confer Abiotic Stress Tolerance in Transgenic Arabidopsis 1 [ C ] [ W ] [ OA ] , 2008 .

[41]  F. Barrieu,et al.  [Identification and characterization of "rd22" dehydration responsive gene in grapevine (Vitis vinifera L.)]. , 2008, Comptes rendus biologies.

[42]  S. Song,et al.  Overexpression of AtMYB44 Enhances Stomatal Closure to Confer Abiotic Stress Tolerance in Transgenic Arabidopsis1[C][W][OA] , 2007, Plant Physiology.

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

[44]  N. Slonim,et al.  A universal framework for regulatory element discovery across all genomes and data types. , 2007, Molecular cell.

[45]  J. Poulain,et al.  The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla , 2007, Nature.

[46]  J. Martínez-Zapater,et al.  The FT/TFL1 gene family in grapevine , 2007, Plant Molecular Biology.

[47]  Gynheung An,et al.  Wax-deficient anther1 Is Involved in Cuticle and Wax Production in Rice Anther Walls and Is Required for Pollen Development[W] , 2006, The Plant Cell Online.

[48]  Byoung-Tak Zhang,et al.  Identification of regulatory modules by co-clustering latent variable models: stem cell differentiation , 2006, Bioinform..

[49]  Lothar Thiele,et al.  A systematic comparison and evaluation of biclustering methods for gene expression data , 2006, Bioinform..

[50]  Ute Baumann,et al.  An atlas of gene expression from seed to seed through barley development , 2006, Functional & Integrative Genomics.

[51]  Jun Wang,et al.  Genome-wide transcription analyses in rice using tiling microarrays , 2006, Nature Genetics.

[52]  Peter K Hepler,et al.  Pectin Methylesterases and Pectin Dynamics in Pollen Tubes , 2005, The Plant Cell Online.

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

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

[55]  A. Baudry,et al.  TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. , 2004, The Plant journal : for cell and molecular biology.

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

[57]  Arlindo L. Oliveira,et al.  Biclustering algorithms for biological data analysis: a survey , 2004, IEEE/ACM Transactions on Computational Biology and Bioinformatics.

[58]  Thomas Hofmann,et al.  Unsupervised Learning by Probabilistic Latent Semantic Analysis , 2004, Machine Learning.

[59]  J. Trygg.  O2‐PLS for qualitative and quantitative analysis in multivariate calibration , 2002 .

[60]  A. Versari,et al.  Stilbene compounds and stilbene synthase expression during ripening, wilting, and UV treatment in grape cv. Corvina. , 2001, Journal of agricultural and food chemistry.

[61]  S. Robinson,et al.  Differential screening indicates a dramatic change in mRNA profiles during grape berry ripening. Cloning and characterization of cDNAs encoding putative cell wall and stress response proteins. , 2000, Plant physiology.

[62]  Ronald S. Jackson,et al.  Wine Science: Principles, Practice, Perception , 2000 .

[63]  X. Deng,et al.  Role of a COP1 Interactive Protein in Mediating Light-Regulated Gene Expression in Arabidopsis , 1998, Plant Cell.

[64]  Zhi-Yong Wang,et al.  Constitutive Expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) Gene Disrupts Circadian Rhythms and Suppresses Its Own Expression , 1998, Cell.

[65]  J. Bohlmann,et al.  Plant terpenoid synthases: molecular biology and phylogenetic analysis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[66]  A. Stead,et al.  Abscission of flowers and floral parts , 1997 .

[67]  Y Hochberg,et al.  Mathematical formulae for the prediction of the residual beta cell function during the first two years of disease in children and adolescents with insulin-dependent diabetes mellitus. , 1995, Medical hypotheses.

[68]  Alain Bouquet,et al.  Biology of the Grapevine , 1992 .

[69]  G. Schwarz.  Estimating the Dimension of a Model , 1978 .