Home LiteratureArticle Details
PMID: 20826702 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

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

Plant physiology ·Vol. 154 ·No. 3 ·2010-11-00 ·Pages 1439-59

Zamboni A, Di Carli M, Guzzo F, Stocchero M, Zenoni S, Ferrarini A, Tononi P, Toffali K, Desiderio A, Lilley KS, Pè ME, Benvenuto E, Delledonne M, Pezzotti M

Abstract

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.

MeSH Terms
Biomarkers Cluster Analysis Fruit/genetics Gene Expression Profiling Gene Expression Regulation, Plant Genomics Metabolomics Oligonucleotide Array Sequence Analysis Proteomics RNA, Plant/genetics Vitis/genetics
Chemicals
Biomarkers RNA, Plant
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Zamboni Anita
Department of Biotechnology, University of Verona, Verona, Italy.
Di Carli Mariasole
Guzzo Flavia
Stocchero Matteo
Zenoni Sara
Ferrarini Alberto
Tononi Paola
Toffali Ketti
Desiderio Angiola
Lilley Kathryn S
Pè M Enrico
Benvenuto Eugenio
Delledonne Massimo
Pezzotti Mario
References (89)
89 references, click to expand
  1. A molecular genetic perspective of reproductive development in grapevine.
    J Exp Bot. 2008;59(10):2579-96 PMID: 18596111
  2. The grapevine R2R3-MYB transcription factor VvMYBF1 regulates flavonol synthesis in developing grape berries.
    Plant Physiol. 2009 Nov;151(3):1513-30 PMID: 19741049
  3. Systems biology at the Institute for Systems Biology.
    Brief Funct Genomic Proteomic. 2008 Jul;7(4):239-48 PMID: 18579616
  4. Benzothiadiazole enhances resveratrol and anthocyanin biosynthesis in grapevine, meanwhile improving resistance to Botrytis cinerea.
    J Agric Food Chem. 2004 Jul 14;52(14):4406-13 PMID: 15237944
  5. Sphingolipid long-chain base hydroxylation is important for growth and regulation of sphingolipid content and composition in Arabidopsis.
    Plant Cell. 2008 Jul;20(7):1862-78 PMID: 18612100
  6. Proteomics-based dissection of stress-responsive pathways in plants.
    J Plant Physiol. 2007 Oct;164(10):1239-60 PMID: 17662502
  7. The cell morphogenesis gene SPIRRIG in Arabidopsis encodes a WD/BEACH domain protein.
    Plant J. 2009 Aug;59(4):612-21 PMID: 19392685
  8. Antimutagenicity of deacylated anthocyanins in purple-fleshed sweetpotato.
    Biosci Biotechnol Biochem. 2001 Jul;65(7):1652-5 PMID: 11515552
  9. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla.
    Nature. 2007 Sep 27;449(7161):463-7 PMID: 17721507
  10. Expression of cellulose synthase-like (Csl) genes in insect cells reveals that CslA family members encode mannan synthases.
    Proc Natl Acad Sci U S A. 2005 Feb 8;102(6):2221-6 PMID: 15647349
  11. A putative hydroxysteroid dehydrogenase involved in regulating plant growth and development.
    Plant Physiol. 2007 Sep;145(1):87-97 PMID: 17616511
  12. Tissue-specific mRNA expression profiling in grape berry tissues.
    BMC Genomics. 2007 Jun 21;8:187 PMID: 17584945
  13. Nucleotide sequence of a cDNA for osmotin-like protein from cultured tobacco cells.
    Plant Physiol. 1991 Oct;97(2):844-6 PMID: 16668481
  14. Nucleic acid extraction and virus detection in grapevine.
    J Virol Methods. 1987 Sep;17(3-4):277-85 PMID: 2824545
  15. Molecular analysis of post-harvest withering in grape by AFLP transcriptional profiling.
    J Exp Bot. 2008;59(15):4145-59 PMID: 19010774
  16. Metabolomics for functional genomics, systems biology, and biotechnology.
    Annu Rev Plant Biol. 2010;61:463-89 PMID: 19152489
  17. Ectopic expression of VvMybPA2 promotes proanthocyanidin biosynthesis in grapevine and suggests additional targets in the pathway.
    Plant Physiol. 2009 Feb;149(2):1028-41 PMID: 19098092
  18. Characterization of a Pterostilbene Dehydrodimer Produced by Laccase of Botrytis cinerea.
    Phytopathology. 1999 Apr;89(4):298-302 PMID: 18944774
  19. Overexpression of a grapevine R2R3-MYB factor in tomato affects vegetative development, flower morphology and flavonoid and terpenoid metabolism.
    Plant Physiol Biochem. 2009 Jul;47(7):551-61 PMID: 19375343
  20. The role of BEACH proteins in Dictyostelium.
    Traffic. 2003 Jan;4(1):6-12 PMID: 12535270
  21. Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development.
    Planta. 2005 Nov;222(5):832-47 PMID: 16151847
  22. Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):15898-903 PMID: 12456878
  23. Here is the evidence, now what is the hypothesis? The complementary roles of inductive and hypothesis-driven science in the post-genomic era.
    Bioessays. 2004 Jan;26(1):99-105 PMID: 14696046
  24. [Identification and characterization of "rd22" dehydration responsive gene in grapevine (Vitis vinifera L.)].
    C R Biol. 2008 Aug;331(8):569-78 PMID: 18606386
  25. [Structure, function and mechanisms of action of ATPases from the AAA superfamily of proteins].
    Postepy Biochem. 2006;52(3):330-8 PMID: 17201069
  26. Grape berry biochemistry revisited upon proteomic analysis of the mesocarp.
    Proteomics. 2004 Jan;4(1):201-15 PMID: 14730682
  27. Grapes on steroids. Brassinosteroids are involved in grape berry ripening.
    Plant Physiol. 2006 Jan;140(1):150-8 PMID: 16361521
  28. Members of a new group of chitinase-like genes are expressed preferentially in cotton cells with secondary walls.
    Plant Mol Biol. 2004 Feb;54(3):353-72 PMID: 15284492
  29. Stress-inducible flavodoxin from photosynthetic microorganisms. The mystery of flavodoxin loss from the plant genome.
    IUBMB Life. 2007 Apr-May;59(4-5):355-60 PMID: 17505975
  30. Bchs, a BEACH domain protein, antagonizes Rab11 in synapse morphogenesis and other developmental events.
    Development. 2006 Dec;133(23):4655-65 PMID: 17079274
  31. 2-D electrophoresis of plant proteins.
    Methods Mol Biol. 1999;112:95-7 PMID: 10027232
  32. Biological and medicinal properties of grapes and their bioactive constituents: an update.
    J Med Food. 2009 Jun;12(3):473-84 PMID: 19627194
  33. Isolation and characterization of a cDNA coding for pea chloroplastic carbonic anhydrase.
    Plant Physiol. 1991 Jan;95(1):264-8 PMID: 16667962
  34. Arabidopsis brassinosteroid signaling pathway.
    Sci STKE. 2006 Dec 05;2006(364):cm5 PMID: 17148786
  35. Stress-induced cell reprogramming. A role for global genome regulation?
    Plant Physiol. 2004 Sep;136(1):2579-86 PMID: 15375206
  36. Antifungal proteins and peptides of leguminous and non-leguminous origins.
    Peptides. 2004 Jul;25(7):1215-22 PMID: 15245883
  37. Integrated analysis of transcript, protein and metabolite data to study lignin biosynthesis in hybrid aspen.
    J Proteome Res. 2009 Jan;8(1):199-210 PMID: 19053836
  38. Analysis of protein changes during grape berry ripening by 2-DE and MALDI-TOF.
    Proteomics. 2007 Sep;7(17):3154-70 PMID: 17683049
  39. Molecular cloning and characterisation of grape berry polyphenol oxidase.
    Plant Mol Biol. 1994 Oct;26(1):495-502 PMID: 7948897
  40. Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development.
    BMC Genomics. 2007 Nov 22;8:429 PMID: 18034876
  41. Data integration in plant biology: the O2PLS method for combined modeling of transcript and metabolite data.
    Plant J. 2007 Dec;52(6):1181-91 PMID: 17931352
  42. Leaf proteome analysis of transgenic plants expressing antiviral antibodies.
    J Proteome Res. 2009 Feb;8(2):838-48 PMID: 19099506
  43. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis.
    Plant Cell. 2004 Aug;16(8):2089-103 PMID: 15269332
  44. Characterization of genes encoding metal tolerance proteins isolated from Nicotiana glauca and Nicotiana tabacum.
    Biochem Biophys Res Commun. 2005 Jun 3;331(2):675-80 PMID: 15850811
  45. Stilbene compounds and stilbene synthase expression during ripening, wilting, and UV treatment in grape cv. Corvina.
    J Agric Food Chem. 2001 Nov;49(11):5531-6 PMID: 11714355
  46. cDNA microarray analysis of developing grape (Vitis vinifera cv. Shiraz) berry skin.
    Funct Integr Genomics. 2005 Jan;5(1):40-58 PMID: 15480888
  47. Arabidopsis PPR40 connects abiotic stress responses to mitochondrial electron transport.
    Plant Physiol. 2008 Apr;146(4):1721-37 PMID: 18305213
  48. Protein interaction analysis of SCF ubiquitin E3 ligase subunits from Arabidopsis.
    Plant J. 2003 Jun;34(6):753-67 PMID: 12795696
  49. Proteomic and selected metabolite analysis of grape berry tissues under well-watered and water-deficit stress conditions.
    Proteomics. 2009 May;9(9):2503-28 PMID: 19343710
  50. Changes in polysaccharide and protein composition of cell walls in grape berry skin (Cv. Shiraz) during ripening and over-ripening.
    J Agric Food Chem. 2009 Apr 8;57(7):2955-60 PMID: 19334762
  51. Isolation of WDR and bHLH genes related to flavonoid synthesis in grapevine (Vitis vinifera L.).
    Plant Mol Biol. 2010 Apr;72(6):607-20 PMID: 20112051
  52. Proteome changes in the skin of the grape cultivar Barbera among different stages of ripening.
    BMC Genomics. 2008 Aug 08;9:378 PMID: 18691399
  53. Delta-viniferin, a resveratrol dehydrodimer: one of the major stilbenes synthesized by stressed grapevine leaves.
    J Agric Food Chem. 2003 Aug 27;51(18):5488-92 PMID: 12926902
  54. The BEACH protein LvsB is localized on lysosomes and postlysosomes and limits their fusion with early endosomes.
    Traffic. 2007 Jun;8(6):774-83 PMID: 17488289
  55. Visualization of GC/TOF-MS-based metabolomics data for identification of biochemically interesting compounds using OPLS class models.
    Anal Chem. 2008 Jan 1;80(1):115-22 PMID: 18027910
  56. Functional characterization of the higher plant chloroplast chaperonins.
    J Biol Chem. 1995 Jul 28;270(30):18158-64 PMID: 7629128
  57. SWI3 subunits of putative SWI/SNF chromatin-remodeling complexes play distinct roles during Arabidopsis development.
    Plant Cell. 2005 Sep;17(9):2454-72 PMID: 16055636
  58. The role of WRKY transcription factors in plant immunity.
    Plant Physiol. 2009 Aug;150(4):1648-55 PMID: 19420325
  59. The 60-kDa precursor to the dithiothreitol-sensitive tetrameric protease of spinach thylakoids: structural similarities between the protease and polyphenol oxidase.
    FEBS Lett. 1995 Sep 4;371(2):195-8 PMID: 7672127
  60. The basic helix-loop-helix transcription factor MYC1 is involved in the regulation of the flavonoid biosynthesis pathway in grapevine.
    Mol Plant. 2010 May;3(3):509-23 PMID: 20118183
  61. The Dictyostelium LvsA protein is localized on the contractile vacuole and is required for osmoregulation.
    Traffic. 2002 Jan;3(1):50-60 PMID: 11872142
  62. Transport and accumulation of flavonoids in grapevine (Vitis vinifera L.).
    Plant Signal Behav. 2008 Sep;3(9):626-32 PMID: 19513253
  63. Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassinosteroid signaling in Arabidopsis.
    Proc Natl Acad Sci U S A. 2009 Jan 13;106(2):658-63 PMID: 19124768
  64. Pentatricopeptide repeat proteins and their emerging roles in plants.
    Plant Physiol Biochem. 2007 Aug;45(8):521-34 PMID: 17560114
  65. Proteomic analysis reveals the role of synaptic vesicle cycling in sustaining the suprachiasmatic circadian clock.
    Curr Biol. 2009 Dec 15;19(23):2031-6 PMID: 19913422
  66. Metabolite profiling of grape: Flavonols and anthocyanins.
    J Agric Food Chem. 2006 Oct 4;54(20):7692-702 PMID: 17002441
  67. Grape berry plasma membrane proteome analysis and its differential expression during ripening.
    J Exp Bot. 2008;59(11):2979-90 PMID: 18550598
  68. Ran on tracks--cytoplasmic roles for a nuclear regulator.
    J Cell Sci. 2009 Mar 1;122(Pt 5):587-93 PMID: 19225125
  69. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  70. Microtubule cytoskeleton: a track record.
    Curr Opin Plant Biol. 2002 Dec;5(6):494-501 PMID: 12393011
  71. Regulation of malate metabolism in grape berry and other developing fruits.
    Phytochemistry. 2009 Jul-Aug;70(11-12):1329-44 PMID: 19762054
  72. Systems biology. Life's complexity pyramid.
    Science. 2002 Oct 25;298(5594):763-4 PMID: 12399572
  73. Expression patterns of cell wall-modifying enzymes during grape berry development.
    Planta. 2001 Dec;214(2):257-64 PMID: 11800390
  74. OligoArray 2.0: design of oligonucleotide probes for DNA microarrays using a thermodynamic approach.
    Nucleic Acids Res. 2003 Jun 15;31(12):3057-62 PMID: 12799432
  75. 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.
    BMC Genomics. 2007 Nov 22;8:428 PMID: 18034875
  76. Crystal structures of wild-type and mutant plastocyanins from a higher plant, Silene.
    J Biochem. 1999 May;125(5):899-903 PMID: 10220581
  77. Laccase: new functions for an old enzyme.
    Phytochemistry. 2002 Jul;60(6):551-65 PMID: 12126701
  78. Bioactivity of grape chemicals for human health.
    Nat Prod Commun. 2009 May;4(5):611-34 PMID: 19445314
  79. VitisNet: "Omics" integration through grapevine molecular networks.
    PLoS One. 2009 Dec 21;4(12):e8365 PMID: 20027228
  80. Evolutionary genomics of LysM genes in land plants.
    BMC Evol Biol. 2009 Aug 03;9:183 PMID: 19650916
  81. Rapid-resolution liquid chromatography/mass spectrometry for determination and quantitation of polyphenols in grape berries.
    Rapid Commun Mass Spectrom. 2008 Oct;22(20):3089-99 PMID: 18819110
  82. Molecular characterization of cDNA encoding oxygen evolving enhancer protein 1 increased by salt treatment in the mangrove Bruguiera gymnorrhiza.
    Plant Cell Physiol. 2000 Nov;41(11):1279-85 PMID: 11092914
  83. Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes.
    BMC Plant Biol. 2008 Jul 22;8:83 PMID: 18647406
  84. Normalization of cDNA microarray data.
    Methods. 2003 Dec;31(4):265-73 PMID: 14597310
  85. Proteomics approach to identify dehydration responsive nuclear proteins from chickpea (Cicer arietinum L.).
    Mol Cell Proteomics. 2008 Jan;7(1):88-107 PMID: 17921517
  86. Philosophy of science. The coordinates of truth.
    Science. 2009 Oct 2;326(5949):53-4 PMID: 19797647
  87. Rapid changes induced in developmental programmes of the maize embryo detected by analysis of the expression of genes encoding proline-rich proteins.
    FEBS Lett. 1998 Feb 6;422(3):400-2 PMID: 9498825
  88. Interactions between diphenylcarbazide, zinc, cobalt, and manganese on the oxidizing side of photosystem II.
    Biochemistry. 1996 Feb 13;35(6):1820-8 PMID: 8639663
  89. Metabolic changes of Malvasia grapes for wine production during postharvest drying.
    J Agric Food Chem. 2006 May 3;54(9):3334-40 PMID: 16637693
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
Published
2010-11-00
Epub
2010-00-08
Pages
1439-59
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC2971619
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com