Identification of putative stage-specific grapevine berry biomarkers and omics data integration into networks

TitoloIdentification of putative stage-specific grapevine berry biomarkers and omics data integration into networks
Tipo di pubblicazioneArticolo su Rivista peer-reviewed
Anno di Pubblicazione2010
AutoriZamboni, A., Di Carli Mariasole, Guzzo F., Stocchero M., Zenoni S., Ferrarini A., Tononi P., Toffali K., Desiderio Angiola, Lilley K.S., Pè M.E., Benvenuto Eugenio, Delledonne M., and Pezzotti M.
RivistaPlant Physiology
Volume154
Paginazione1439 - 1459
Data di pubblicazione2010
ISBN Number00320889 (ISSN)
Parole chiavearticle, biological marker, Biological Markers, cluster analysis, DNA microarray, fruit, gene expression profiling, gene expression regulation, genetics, Genomics, grape, metabolomics, Oligonucleotide Array Sequence Analysis, Plant, plant RNA, Proteomics, RNA, Vitis, Vitis vinifera
Astratto

The analysis of grapevine (Vitis vinifera) berries at the transcriptomic, proteomic, and metabolomic levels can provide great insight into the molecular events underlying berry development and postharvest drying (withering). However, the large and very different data sets produced by such investigations are difficult to integrate. Here, we report the identification of putative stage-specific biomarkers for berry development and withering and, to our knowledge, the first integrated systems-level study of these processes. Transcriptomic, proteomic, and metabolomic data were integrated using two different strategies, one hypothesis free and the other hypothesis driven. A multistep hypothesis-free approach was applied to data from four developmental stages and three withering intervals, with integration achieved using a hierarchical clustering strategy based on the multivariate bidirectional orthogonal projections to latent structures technique. This identified stage-specific functional networks of linked transcripts, proteins, and metabolites, providing important insights into the key molecular processes that determine the quality characteristics of wine. The hypothesis-driven approach was used to integrate data from three withering intervals, starting with subdata sets of transcripts, proteins, and metabolites. We identified transcripts and proteins that were modulated during withering as well as specific classes of metabolites that accumulated at the same time and used these to select subdata sets of variables. The multivariate bidirectional orthogonal projections to latent structures technique was then used to integrate the subdata sets, identifying variables representing selected molecular processes that take place specifically during berry withering. The impact of this holistic approach on our knowledge of grapevine berry development and withering is discussed. © 2010 American Society of Plant Biologists.

Note

Cited By :51Export Date: 16 July 2015CODEN: PLPHACorrespondence Address: Pezzotti, M.; Department of Biotechnology, University of Verona, 37134 Verona, Italy; email: mario.pezzotti@univr.itMolecular Sequence Numbers: GENBANK: GSE20511;Chemicals/CAS: Biological Markers; RNA, PlantReferences: Adrian, M., Jeandet, P., Veneau, J., Weston, L.A., Bessis, R., Biological activity of resveratrol, stilbenic compound from grapevine, against Botrytis cinerea, the causal agent for gray mold (1997) J Chem Ecol, 23, pp. 1689-1702;Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., Lipman, D.J., Gapped BLAST and PSI-BLAST: A new generation of protein database search programs (1997) Nucleic Acids Res, 25, pp. 3389-3402; Arnholdt-Schmitt, B., Stress-induced cell reprogramming: A role for global genome regulation? (2004) Plant Physiol, 136, pp. 2579-2586; Belkhadir, Y., Wang, X., Chory, J., Arabidopsis brassinosteroid signaling pathway (2006) Sci STKE, 2006, pp. cm5; Bellincontro, A., de Santis, D., Botondi, R., Villa, I., Mencarelli, F., Different post-harvest dehydration rates affect quality characteristics and volatile compounds of Malvasia, Trebbiano and Sangiovese grape for wine production (2004) J Sci Food Agric, 84, pp. 1791-1800; Bellincontro, A., Fardelli, A., de Santis, D., Botondi, R., Mencarelli, F., Postharvest ethylene and 1-MCP treatments both affect phenols, anthocyanins, and aromatic quality of Aleatico grapes and wine (2006) Aust J Grape Wine Res, 12, pp. 141-149; Bonello, P., Blodgett, J., Pinus nigra-Sphaeropsis sapinea as a model pathosystem to investigate local and systemic effects of fungal infection of pines (2003) Physiol Mol Plant Pathol, 63, pp. 249-261; Braidot, E., Zancani, M., Petrussa, E., Peresson, C., Bertolini, A., Patui, S., MacRi, F., Vianello, A., Transport and accumulation of flavonoids in grapevine (Vitis vinifera L.) (2008) Plant Signal Behav, 3, pp. 626-632; Breuil, A.C., Jeandet, P., Adrian, M., Chopin, F., Pirio, N., Meunier, P., Bessis, R., Characterization of pterostilbene dehydrodimer produced by laccase of Botrytis cinerea (1999) Phytopathology, 89, pp. 298-302; Bylesjö, M., Eriksson, D., Kusano, M., Moritz, T., Trygg, J., Data integration in plant biology: The O2PLS method for combined modeling of transcript and metabolite data (2007) Plant J, 52, pp. 1181-1191; Bylesjö, M., Nilsson, R., Srivastava, V., Johansson, A.I., Jansson, S., Karlsson, J., Moritz, T., Trygg, J., Integrated analysis of transcript, protein and metabolite data to study lignin biosynthesis in hybrid aspen (2009) J Proteome Res, 8, pp. 199-210; Carmona, M.J., Thomas, M.R., A molecular genetic perspective of reproductive development in grapevine (2008) J Exp Bot, 59, pp. 2579-2596; Cavaliere, C., Foglia, P., Gubbiotti, R., Sacchetti, P., Samperi, R., Laganà, A., Rapid-resolution liquid chromatography/mass spectrometry for determination and quantitation of polyphenols in grape berries (2008) Rapid Commun Mass Spectrom, 22, pp. 3089-3099; Chen, M., Markham, J.E., Dietrich, C.R., Jaworski, J.G., Cahoon, E.B., Sphingolipid long-chain base hydroxylation is important for growth and regulation of sphingolipid content and composition in Arabidopsis (2008) Plant Cell, 20, pp. 1862-1878; Chkaiban, L., Botondi, R., Bellincontro, A., de Santis, D., Kefalas, P., Mencarelli, F., Influence of postharvest water stress on lipoxygenase and alcohol dehydrogenase activities, and on the composition of some volatile compounds of Gewü rztraminer grapes dehydrated under controlled and uncontrolled thermohygrometric conditions (2007) Aust J Grape Wine Res, 13, pp. 142-147; Conde, C., Silva, P., Fontes, N., Dias, A.C.P., Tavares, R.M., Sousa, M.J., Agasse, A., Geros, H., Biochemical changes throughout grape berry development and fruit and wine quality (2007) Food, 1, pp. 1-22; Coombe, B.G., Adoption of a system for identifying grapevine growth stages (1995) Aust J Grape Wine Res, 1, pp. 100-110; Coombe, B.G., McCarthy, M.G., Dynamics of grape berry growth and physiology of ripening (2000) Aust J Grape Wine Res, 6, pp. 131-135; Costantini, V., Bellincontro, A., de Santis, D., Botondi, R., Mencarelli, F., Metabolic changes of Malvasia grapes for wine production during postharvest drying (2006) J Agric Food Chem, 54, pp. 3334-3340; Czemmel, S., Stracke, R., Weisshaar, B., Cordon, N., Harris, N.N., Walker, A.R., Robinson, S.P., Bogs, J., The grapevine R2R3-MYB transcription factor VvMYBF1 regulates flavonol synthesis in developing grape berries (2009) Plant Physiol, 151, pp. 1513-1530; Davies, C., Bottcher, C., Hormonal control of grapevine berry ripening (2009) Grapevine Molecular Physiology and Biotechnology, pp. 229-261. , In KA Roubelakis-Angelakis, ed, Ed 2. Springer, Dordrecht, The Netherlands; Deery, M.J., Maywood, E.S., Chesham, J.E., Sládek, M., Karp, N.A., Green, E.W., Charles, P.D., Lilley, K.S., Proteomic analysis reveals the role of synaptic vesicle cycling in sustaining the suprachiasmatic circadian clock (2009) Curr Biol, 19, pp. 2031-2036; de Lozanne, A., The role of BEACH proteins in Dictyostelium (2003) Traffic, 4, pp. 6-12; Deluc, L.G., Grimplet, J., Wheatley, M.D., Tillett, R.L., Quilici, D.R., Osborne, C., Schlauch, K.A., Cramer, G.R., Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development (2007) BMC Genomics, 8, p. 429; Dercks, W., Creasy, L.L., The significance of stilbene phytoalexins in the Plasmopara viticola grapevine interaction (1989) Physiol Mol Plant Pathol, 34, pp. 189-202; Deytieux-Belleau, C., Gagne, S., L’Hyvernay, A., Doneche, B., Geny, L., Possible roles of both abscisic acid and indol-acetic acid in controlling grape berry ripening process (2007) J Int Sci Vigne Vin, 41, pp. 141-148; di Carli, M., Villani, M.E., Renzone, G., Nardi, L., Pasquo, A., Franconi, R., Scaloni, A., Desiderio, A., Leaf proteome analysis of transgenic plants expressing antiviral antibodies (2009) J Proteome Res, 8, pp. 838-848; Dry, I.B., Robinson, S.P., Molecular cloning and characterisation of grape berry polyphenol oxidase (1994) Plant Mol Biol, 26, pp. 495-502; Garg, A.K., Kim, J.K., Owens, T.G., Ranwala, A.P., Choi, Y.D., Kochian, L.V., Wu, R.J., Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses (2002) Proc Natl Acad Sci USA, 99, pp. 15898-15903; Gerald, N.J., Siano, M., de Lozanne, A., The Dictyostelium LvsA protein is localized on the contractile vacuole and is required for osmoregulation (2002) Traffic, 3, pp. 50-60; Ghirardi, M.L., Lutton, T.W., Seibert, M., Interactions between diphenylcarbazide, zinc, cobalt, and manganese on the oxidizing side of photosystem II (1996) Biochemistry, 35, pp. 1820-1828; Giribaldi, M., Perugini, I., Sauvage, F.X., Schubert, A., Analysis of protein changes during grape berry ripening by 2-DE and MALDI-TOF (2007) Proteomics, 7, pp. 3154-3170; Glissant, D., Dedaldechamp, F., Delrot, S., Transcriptomic analysis of grape berry softening during ripening (2008) J Int Sci Vigne Vin, 42, pp. 1-13; Grimplet, J., Cramer, G.R., Dickerson, J.A., Mathiason, K., van Hemert, J., Fennell, A.Y., VitisNet: "omics" integration through grapevine molecular networks (2009) PLoS ONE, 4, pp. e8365; Grimplet, J., Deluc, L.G., Tillett, R.L., Wheatley, M.D., Schlauch, K.A., Cramer, G.R., Cushman, J.C., Tissue-specific mRNA expression profiling in grape berry tissues (2007) BMC Genomics, 8, p. 187; Grimplet, J., Wheatley, M.D., Jouira, H.B., Deluc, L.G., Cramer, G.R., Cushman, J.C., Proteomic and selected metabolite analysis of grape berry tissues under well-watered and water-deficit stress conditions (2009) Proteomics, 9, pp. 2503-2528; Hanana, M., Deluc, L., Fouquet, R., Daldoul, S., Barrieu, F., Ghorbel, A., Mliki, A., Hamdi, S., Identification and characterization of "rd22" dehydration responsive gene in grapevine (Vitis vinifera L.) (2008) C R Biol, 331, pp. 569-578; Hichri, I., Heppel, S.C., Pillet, J., Czemmel, S., Delrot, S., Lauvergeat, V., Bogs, J., The basic helix-loop-helix transcription factor MYC1 is involved in the regulation of the flavonoid biosynthesis pathway in grapevine (2010) Mol Plant, 3, pp. 509-523; Hood, L., Rowen, L., Galas, D.J., Aitchison, J.D., Systems biology at the Institute for Systems Biology (2008) Brief Funct Genomics Proteomics, 7, pp. 239-248; Iriti, M., Faoro, F., Bioactivity of grape chemicals for human health (2009) Nat Prod Commun, 4, pp. 611-634; Iriti, M., Rossoni, M., Borgo, M., Faoro, F., Benzothiadiazole enhances resveratrol and anthocyanin biosynthesis in grapevine, meanwhile improving resistance to Botrytis cinerea (2004) J Agric Food Chem, 52, pp. 4406-4413; Jaillon, O., Aury, J.M., Noel, B., Policriti, A., Clepet, C., Casagrande, A., Choisne, N., Jubin, C., The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla (2007) Nature, pp. 463-467. , French-Italian Public Consortium for Grapevine Genome Characterization; Josè-Estanyol, M., Puigdoménech, P., Rapid changes induced in developmental programmes of the maize embryo detected by analysis of the expression of genes encoding proline-rich proteins (1998) FEBS Lett, 422, pp. 400-402; Kedzierska, S., Structure, function and mechanisms of action of ATPases from the AAA superfamily of proteins (2006) Postepy Biochem, 52, pp. 330-338; Kell, D.B., Oliver, S.G., Here is the evidence, now what is the hypothesis? The complementary roles of inductive and hypothesis-driven science in the post-genomic era (2004) Bioessays, 26, pp. 99-105; Khodosh, R., Augsburger, A., Schwarz, T.L., Garrity, P.A., Bchs, a BEACH domain protein, antagonizes Rab11 in synapse morphogenesis and other developmental events (2006) Development, 133, pp. 4655-4665; Kuwabara, T., The 60-kDa precursor to the dithiothreitol-sensitive tetrameric protease of spinach thylakoids: Structural similarities between the protease and polyphenol oxidase (1995) FEBS Lett, 371, pp. 195-198; Kypri, E., Schmauch, C., Maniak, M., de Lozanne, A., The BEACH protein LvsB is localized on lysosomes and postlysosomes and limits their fusion with early endosomes (2007) Traffic, 8, pp. 774-783; Langcake, P., Pryce, R.J., Production of resveratrol by Vitis vinifera and other members of Vitaceae as a response to infection or injury (1976) Physiol Plant Pathol, 9, pp. 77-86; Li, F., Asami, T., Wu, X., Tsang, E.W., Cutler, A.J., A putative hydroxysteroid dehydrogenase involved in regulating plant growth and development (2007) Plant Physiol, 145, pp. 87-97; Liepman, A.H., Wilkerson, C.G., Keegstra, K., Expression of cellulose synthase-like (Csl) genes in insect cells reveals that CslA family members encode mannan synthases (2005) Proc Natl Acad Sci USA, 102, pp. 2221-2226; Lurin, C., Andrés, C., Aubourg, S., Bellaoui, M., Bitton, F., Bruyère, C., Caboche, M., Hoffmann, B., Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis (2004) Plant Cell, 16, pp. 2089-2103; Mahjoub, A., Hernould, M., Joubès, J., Decendit, A., Mars, M., Barrieu, F., Hamdi, S., Delrot, S., Overexpression of a grapevine R2R3-MYB factor in tomato affects vegetative development, flower morphology and flavonoid and terpenoid metabolism (2009) Plant Physiol Biochem, 47, pp. 551-561; Majeau, N., Coleman, J.R., Isolation and characterization of a cDNA coding for pea chloroplastic carbonic anhydrase (1991) Plant Physiol, 95, pp. 264-268; Mattivi, F., Guzzon, R., Vrhovsek, U., Stefanini, M., Velasco, R., Metabolite profiling of grape: Flavonols and anthocyanins (2006) J Agric Food Chem, 54, pp. 7692-7702; Matus, J.T., Aquea, F., Arce-Johnson, P., 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 Biol, 8, p. 83; Matus, J.T., Poupin, M.J., Cañón, P., Bordeu, E., Alcalde, J.A., Arce-Johnson, P., Isolation of WDR and bHLH genes related to flavonoid synthesis in grapevine (Vitis vinifera L.) (2010) Plant Mol Biol, 72, pp. 607-620; Mayer, A.M., Staples, R.C., Laccase: New functions for an old enzyme (2002) Phytochemistry, 60, pp. 551-565; Mayer, U., Jürgens, G., Microtubule cytoskeleton: A track record (2002) Curr Opin Plant Biol, 5, pp. 494-501; Nabel, G.J., Philosophy of science: The coordinates of truth (2009) Science, 326, pp. 53-54; Negri, A.S., Prinsi, B., Rossoni, M., Failla, O., Scienza, A., Cocucci, M., Espen, L., Proteome changes in the skin of the grape cultivar Barbera among different stages of ripening (2008) BMC Genomics, 9, p. 378; Ng, T.B., Antifungal proteins and peptides of leguminous and nonleguminous origins (2004) Peptides, 25, pp. 1215-1222; Nunan, K.J., Davies, C., Robinson, S.P., Fincher, G.B., Expression patterns of cell wall-modifying enzymes during grape berry development (2001) Planta, 214, pp. 257-264; Oh, M.H., Wang, X., Kota, U., Goshe, M.B., Clouse, S.D., Huber, S.C., Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassinosteroid signaling in Arabidopsis (2009) Proc Natl Acad Sci USA, 106, pp. 658-663; Oltvai, Z.N., Barabási, A.L., Systems biology: Life’s complexity pyramid (2002) Science, 298, pp. 763-764; Pandey, A., Chakraborty, S., Datta, A., Chakraborty, N., Proteomics approach to identify dehydration responsive nuclear proteins from chickpea (Cicer arietinum L.) (2008) Mol Cell Proteomics, 7, pp. 88-107; Pandey, S.P., Somssich, I.E., The role of WRKY transcription factors in plant immunity (2009) Plant Physiol, 150, pp. 1648-1655; Pezet, R., Perret, C., Jean-Denis, J.B., Tabacchi, R., Gindro, K., Viret, O., d-Viniferin, a resveratrol dehydrodimer: One of the major stilbenes synthesized by stressed grapevine leaves (2003) J Agric Food Chem, 51, pp. 5488-5492; Pilati, S., Perazzolli, M., Malossini, A., Cestaro, A., Demattè, L., Fontana, P., Dal Ri, A., Moser, C., Genome-wide transcriptional analysis of grapevine berry ripening reveals a set of genes similarly modulated during three seasons and the occurrence of an oxidative burst at vèraison (2007) BMC Genomics, 8, p. 428; Qureshi, M.I., Qadir, S., Zolla, L., Proteomics-based dissection of stressresponsive pathways in plants (2007) J Plant Physiol, 164, pp. 1239-1260; Rezaian, M.A., Krake, L.R., Nucleic acid extraction and virus detection in grapevine (1987) J Virol Methods, 17, pp. 277-285; Risseeuw, E.P., Daskalchuk, T.E., Banks, T.W., Liu, E., Cotelesage, J., Hellmann, H., Estelle, M., Crosby, W.L., Protein interaction analysis of SCF ubiquitin E3 ligase subunits from Arabidopsis (2003) Plant J, 34, pp. 753-767; Rizzini, F.M., Bonghi, C., Tonutti, P., Postharvest water loss induced marked changes in transcript profiling in skin of wine grape berry (2009) Postharvest Biol Technol, 52, pp. 247-253; Rouillard, J.M., Zuker, M., Gulari, E., OligoArray 2.0: Design of oligonucleotide probes for DNA microarrays using a thermodynamic approach (2003) Nucleic Acids Res, 31, pp. 3057-3062; Saedler, R., Jakoby, M., Marin, B., Galiana-Jaime, E., Hülskamp, M., The cell morphogenesis gene SPIRRIG in Arabidopsis encodes a WD/ BEACH domain protein (2009) Plant J, 59, pp. 612-621; Saha, D., Prasad, A.M., Srinivasan, R., Pentatricopeptide repeat proteins and their emerging roles in plants (2007) Plant Physiol Biochem, 45, pp. 521-534; Saito, K., Matsuda, F., Metabolomics for functional genomics, systems biology, and biotechnology (2010) Annu Rev Plant Biol, 61, pp. 463-489; Sarnowski, T.J., Ríos, G., Jásik, J., Swiezewski, S., Kaczanowski, S., Li, Y., Kwiatkowska, A., Koźbiał, P., SWI3 subunits of putative SWI/SNF chromatin-remodeling complexes play distinct roles during Arabidopsis development (2005) Plant Cell, 17, pp. 2454-2472; Sarry, J.E., Sommerer, N., Sauvage, F.X., Bergoin, A., Rossignol, M., Albagnac, G., Romieu, C., Grape berry biochemistry revisited upon proteomic analysis of the mesocarp (2004) Proteomics, 4, pp. 201-215; Shingu, Y., Kudo, T., Ohsato, S., Kimura, M., Ono, Y., Yamaguchi, I., Hamamoto, H., Characterization of genes encoding metal tolerance proteins isolated from Nicotiana glauca and Nicotiana tabacum (2005) Biochem Biophys Res Commun, 331, pp. 675-680; Smyth, G.K., Speed, T.P., Normalization of cDNA microarray data (2003) Methods, 31, pp. 265-273; Sugawara, H., Inoue, T., Li, C., Gotowda, M., Hibino, T., Takabe, T., Kai, Y., Crystal structures of wild-type and mutant plastocyanins from a higher plant, Silene (1999) J Biochem, 125, pp. 899-903; Sugihara, K., Hanagata, N., Dubinsky, Z., Baba, S., Karube, I., Molecular characterization of cDNA encoding oxygen evolving enhancer protein 1 increased by salt treatment in the mangrove Bruguiera gymnorrhiza (2000) Plant Cell Physiol, 41, pp. 1279-1285; Sweetman, C., Deluc, L.G., Cramer, G.R., Ford, C.M., Soole, K.L., Regulation of malate metabolism in grape berry and other developing fruits (2009) Phytochemistry, 70, pp. 1329-1344; Symons, G.M., Davies, C., Shavrukov, Y., Dry, I.B., Reid, J.B., Thomas, M.R., Grapes on steroids: Brassinosteroids are involved in grape berry ripening (2006) Plant Physiol, 140, pp. 150-158; Takeda, S., Sato, F., Ida, K., Yamada, Y., Nucleotide sequence of a cDNA for osmotin-like protein from cultured tobacco cells (1991) Plant Physiol, 97, pp. 844-846; Terrier, N., Glissant, D., Grimplet, J., Barrieu, F., Abbal, P., Couture, C., Ageorges, A., Renaudin, J.P., Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development (2005) Planta, 222, pp. 832-847; Terrier, N., Torregrosa, L., Ageorges, A., Vialet, S., Verriès, C., Cheynier, V., Romieu, C., Ectopic expression of VvMybPA2 promotes proanthocyanidin biosynthesis in grapevine and suggests additional targets in the pathway (2009) Plant Physiol, 149, pp. 1028-1041; Trygg, J., O2-PLS for qualitative and quantitative analysis in multivariate calibration (2002) J Chemometr, 16, pp. 283-293; Trygg, J., Wold, S., O2-PLS, a two-block (X-Y) latent variable regression (LVR) method with an integral OSC filter (2003) J Chemometr, 17, pp. 53-64; Tsugita, A., Kamo, M., 2-D electrophoresis of plant proteins (1999) Methods Mol Biol, 112, pp. 95-97; Versari, A., Parpinello, G.P., Tornielli, G.B., Ferrarini, R., Giulivo, C., Stilbene compounds and stilbene synthase expression during ripening, wilting, and UV treatment in grape cv. Corvina (2001) J Agric Food Chem, 49, pp. 5531-5536; Vicens, A., Fournand, D., Williams, P., Sidhoum, L., Moutounet, M., Doco, T., Changes in polysaccharide and protein composition of cell walls in grape berry skin (cv. Shiraz) during ripening and over-ripening (2009) J Agric Food Chem, 57, pp. 2955-2960; Viitanen, P.V., Schmidt, M., Buchner, J., Suzuki, T., Vierling, E., Dickson, R., Lorimer, G.H., Soll, J., Functional characterization of the higher plant chloroplast chaperonins (1995) J Biol Chem, 270, pp. 18158-18164; Waters, D.L.E., Holton, T.A., Ablett, E.M., Lee, L.S., Henry, R.J., cDNA microarray analysis of developing grape (Vitis vinifera cv. Shiraz) berry skin (2005) Funct Integr Genomics, 5, pp. 40-58; Wiklund, S., Johansson, E., Sjöström, L., Mellerowicz, E.J., Edlund, U., Shockcor, J.P., Gottfries, J., Trygg, J., Visualization of GC/TOF-MSbased metabolomics data for identification of biochemically interesting compounds using OPLS class models (2008) Anal Chem, 80, pp. 115-122; Yadav, M., Jain, S., Bhardwaj, A., Nagpal, R., Puniya, M., Tomar, R., Singh, V., Marotta, F., Biological and medicinal properties of grapes and their bioactive constituents: An update (2009) J Med Food, 12, pp. 473-484; Yoshimoto, M., Okuno, S., Yamaguchi, M., Yamakawa, O., Antimutagenicity of deacylated anthocyanins in purple-fleshed sweetpotato (2001) Biosci Biotechnol Biochem, 65, pp. 1652-1655; Yudin, D., Fainzilber, M., Ran on tracks: Cytoplasmic roles for a nuclear regulator (2009) J Cell Sci, 122, pp. 587-593; Zamboni, A., Minoia, L., Ferrarini, A., Tornielli, G.B., Zago, E., Delledonne, M., Pezzotti, M., Molecular analysis of post-harvest withering in grape by AFLP transcriptional profiling (2008) J Exp Bot, 59, pp. 4145-4159; Zhang, D., Hrmova, M., Wan, C.H., Wu, C., Balzen, J., Cai, W., Wang, J., Zhang, H., Members of a new group of chitinase-like genes are expressed preferentially in cotton cells with secondary walls (2004) Plant Mol Biol, 54, pp. 353-372; Zhang, J., Ma, H., Feng, J., Zeng, L., Wang, Z., Chen, S., Grape berry plasma membrane proteome analysis and its differential expression during ripening (2008) J Exp Bot, 59, pp. 2979-2990; Zhang, X.C., Cannon, S.B., Stacey, G., Evolutionary genomics of LysM genes in land plants (2009) BMC Evol Biol, 9, p. 183; Zsigmond, L., Rigó, G., Szarka, A., Székely, G., Otvös, K., Darula, Z., Medzihradszky, K.F., Szabados, L., Arabidopsis PPR40 connects abiotic stress responses to mitochondrial electron transport (2008) Plant Physiol, 146, pp. 1721-1737; Zurbriggen, M.D., Tognetti, V.B., Carrillo, N., Stress-inducible flavodoxin from photosynthetic microorganisms: The mystery of flavodoxin loss from the plant genome (2007) IUBMB Life, 59, pp. 355-360

URLhttp://www.scopus.com/inward/record.url?eid=2-s2.0-78249266582&partnerID=40&md5=456a9e9860a2f2c2e43dfdbb2fe0f931