Skip to main content
SpringerLink
Log in

Gene expression analyses in individual grape (Vitis vinifera L.) berries during ripening initiation reveal that pigmentation intensity is a valid indicator of developmental staging within the cluster

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Asynchronous ripening of individual grape berries within clusters can lead to inconsistent organoleptic characteristics for wine making. Ripening initiation in grape berries is non-climacteric and not well understood at the molecular level. Evidence is lacking for a single master switch controlling this process, such as the established role for ethylene in climacteric fruit ripening. We used Affymetrix microarray analyses of 32 individual Vitis vinifera cv. Cabernet Sauvignon berries sampled from two clusters at 50% ripening initiation. By delineating four developmental stages of ripening initiation, we demonstrate that pigmentation is a statistically significant indicator of transcriptional state during ripening initiation. We report on clustered gene expression patterns which were mined for genes annotated with signal transduction functions in order to advance regulatory network modeling of ripening initiation in grape berries. Abscisic acid has previously been demonstrated to be an important signaling component regulating ripening initiation in grapevine. We demonstrate via real-time RT-PCR analyses that up-regulation of a 9-cis-epoxycarotenoid gene family member, VvNCED2, in grape seed and pericarp and a putative ortholog to a reported abscisic acid receptor, VvGCR2, are correlated with ripening initiation. Our results suggest a role for these genes in abscisic acid signaling during ripening initiation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

CCD:

Carotenoid cleavage dioxygenase

FCM clustering:

Fuzzy c-means clustering

NCED:

9-cis-epoxycarotenoid cleavage dioxygenase

References

  • Auldridge ME, Block A, Vogel JT, Dabney-Smith C, Mila I, Bouzayen M et al (2006) Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J 45(6):982–993

    Article  PubMed  CAS  Google Scholar 

  • Çakir B, Agasse A, Gaillard C, Saumonneau A, Delrot S, Atanassova R (2003) A grape ASR protein involved in sugar and abscisic acid signaling. Plant Cell 15:2165–2180. doi:10.1105/tpc.013854

    Article  PubMed  CAS  Google Scholar 

  • Chervin C, El-Kereamy A, Roustan J-P, Latché A, Lamon J, Bouzayen M (2004) Ethylene seems required for the berry development and ripening in grape, a non-climacteric fruit. Plant Sci 167(6):1301–1305. doi:10.1016/j.plantsci.2004.06.026

    Article  CAS  Google Scholar 

  • Chevalier D, Batoux M, Fulton L, Pfister K, Yadav RK, Schellenberg M et al (2005) STRUBBELIG defines a receptor kinase-mediated signaling pathway regulating organ development in Arabidopsis. Proc Natl Acad Sci USA 102(25):9074–9079. doi:10.1073/pnas.0503526102

    Article  PubMed  CAS  Google Scholar 

  • Coombe BG (1980) Development of the grape berry. I. Effects of time of flowering and competition. Aust J Agric Res 31:125–131. doi:10.1071/AR9800125

    Article  Google Scholar 

  • Coombe BG (1992) Research on development and ripening of the grape berry. Am J Enol Vitic 43(1):101–110

    Google Scholar 

  • Coombe BG, Bishop GR (1980) Development of the grape berry. II. Changes in diameter and deformability during veraison. Aust J Agric Res 31:499–509. doi:10.1071/AR9800499

    Article  Google Scholar 

  • Davies C, Boss P, Robinson S (1997) Treatment of grape berries, a nonclimacteric fruit, with a synthetic auxin retards ripening and alters the expression of developmentally regulated genes. Plant Physiol 115:1155–1161

    PubMed  CAS  Google Scholar 

  • Deluc LG, Grimplet J, Wheatley MD, Tillett RL, Quilici DR, Osborne C et al (2007) Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development. BMC Genomics 8:429. doi:10.1186/1471-2164-8-429

    Article  PubMed  Google Scholar 

  • Fillion L, Ageorges A, Picaud S, Coutos-Thévenot P, Lemoine R, Romieu C et al (1999) Cloning and expression of a hexose transporter gene expressed during the ripening of grape berry. Plant Physiol 120:1083–1094. doi:10.1104/pp.120.4.1083

    Article  PubMed  CAS  Google Scholar 

  • Futschik ME, Carlisle B (2005) Noise-robust soft clustering of gene expression time-course data. J Bioinform Comput Biol 3(4):965–988. doi:10.1142/S0219720005001375

    Article  PubMed  CAS  Google Scholar 

  • Gagne S, Esteve K, Deytieux C, Saucier C, Geny L (2006) Influence of abscisic acid in triggering veraison in grape berry skins of Vitis vinifera L. cv. Cabernet Sauvignon. J Int Sci Vigne Vin 40:7–14

    CAS  Google Scholar 

  • Gao Y, Zeng Q, Guo J, Cheng J, Ellis BE, Chen J-G (2007) Genetic characterization reveals no role for the reported ABA receptor, GCR2, in ABA control of seed germination and early seedling development in Arabidopsis. Plant J 52(6):1001–1013

    Article  PubMed  CAS  Google Scholar 

  • Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S et al (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80. doi:10.1186/gb-2004-5-10-r80

    Article  PubMed  Google Scholar 

  • Giribaldi M, Perugini I, Sauvage F-X, Schubert A (2007) Analysis of protein changes during grape berry ripening by 2-DE and MALDI-TOF. Proteomics 7(17):3154–3170. doi:10.1002/pmic.200600974

    Article  PubMed  CAS  Google Scholar 

  • Goeman JJ, van de Geer SA, de Kort F, van Houwelingen HC (2004) A global test for groups of genes: Testing association with a clinical outcome. Bioinformatics 20:93–99. doi:10.1093/bioinformatics/btg382

    Article  PubMed  CAS  Google Scholar 

  • Goes de Silva F, Iandolino A, Al-Kayal F, Bohlmann MC, Cushman MA, Lim H et al (2005) Characterizing the grape transcriptome. Analysis of expressed sequence tags from multiple Vitis species and development of a compendium of gene expression during berry development. Plant Physiol 139:574–597. doi:10.1104/pp.105.065748

    Article  CAS  Google Scholar 

  • Grimplet J, Deluc LG, Tillett RL, Wheatley MD, Schlauch KA, Cramer GR et al (2007) Tissue-specific mRNA expression profiling in grape berry tissues. BMC Genomics 8:187. doi:10.1186/1471-2164-8-187

    Article  PubMed  CAS  Google Scholar 

  • Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U et al (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostat 4(2):249–264. doi:10.1093/biostatistics/4.2.249

    Article  Google Scholar 

  • Jeong ST, Goto-Yamamoto N, Kobayashi S, Esaka M (2004) Effects of plant hormones and shading on the accumulation of anthocyanins and the expression of anthocyanin biosynthetic genes in grape berry skins. Plant Sci 167:247–252. doi:10.1016/j.plantsci.2004.03.021

    Article  CAS  Google Scholar 

  • Josefsson LG, Rask L (1997) Cloning of a putative G protein-coupled receptor from Arabidopsis thaliana. Eur J Biochem 249:415–420. doi:10.1111/j.1432-1033.1997.t01-1-00415.x

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi S, Goto-Yamamoto N, Hirochika H (2004) Retrotransposon-induced mutations in grape skin color. Science 304(5673):982. doi:10.1126/science.1095011

    Article  PubMed  Google Scholar 

  • Li C, Wong WH (2001) Model-based analysis of oligonucleotide arrays: Expression index computation and outlier detection. Proc Natl Acad Sci USA 98:31–36. doi:10.1073/pnas.011404098

    Article  Google Scholar 

  • Liu X, Yue Y, Li B, Nie Y, Li W, Wu W-H et al (2007) A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid. Science 315(5819):1712–1716. doi:10.1126/science.1135882

    Article  PubMed  CAS  Google Scholar 

  • Lücker J, Bowen P, Bohlmann J (2004) Vitis vinifera terpenoid cyclases: functional identification of two sesquiterpene synthase cDNAs encoding (+)-valencene synthase and (−)-germacrene D synthase and expression of mono- and sesquiterpene synthases in grapevine flowers and berries. Phytochem 65:2649–2659. doi:10.1016/j.phytochem.2004.08.017

    Article  CAS  Google Scholar 

  • Lund ST, Bohlmann J (2006) The molecular basis for wine grape quality—a volatile subject. Science 311:804–805. doi:10.1126/science.1118962

    Article  PubMed  CAS  Google Scholar 

  • Mathieu S, Terrier N, Procureur J, Bigey F, Gunaha Z (2005) A carotenoid cleavage dioxygenase from Vitis vinifera L.: functional characterization and expression during grape berry development in relation to C-13-norisoprenoid accumulation. J Exp Bot 56(420):2721–2731. doi:10.1093/jxb/eri265

    Article  PubMed  CAS  Google Scholar 

  • Mathieu S, Bigey F, Procureur J, Terrier N, Gunaha Z (2007) Production of a recombinant carotenoid cleavage dioxygenase from grape and enzyme assay in water-miscible organic solvents. Biotechnol Lett 29(5):837–841. doi:10.1007/s10529-007-9315-8

    Article  PubMed  CAS  Google Scholar 

  • Mullins MG, Rajasekaran K (1981) Fruiting cuttings: Revised method for producing test-plants of grapevine cultivars. Am J Enol Vitic 32:35–40

    Google Scholar 

  • Nunan KJ, Sims IM, Bacic A, Robinson SP, Fincher GB (1998) Changes in cell wall composition during ripening of grape berries. Plant Physiol 118(3):783–792. doi:10.1104/pp.118.3.783

    Article  PubMed  CAS  Google Scholar 

  • Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, Mortensen P et al (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127:635–648. doi:10.1016/j.cell.2006.09.026

    Article  PubMed  CAS  Google Scholar 

  • Osakabe Y, Maruyama K, Seki M, Satou M, Shinozaki K, Yamaguchi-Shinozakia K (2005) Leucine-rich repeat receptor-like kinase1 is a key membrane-bound regulator of abscisic acid early signaling in Arabidopsis. Plant Cell 17:1105–1119. doi:10.1105/tpc.104.027474

    Article  PubMed  CAS  Google Scholar 

  • Pilati S, Perazzolli M, Malossini A, Cestaro A, Dematte L, Fontana P et al (2007) 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 veraison. BMC Genomics 8:428. doi:10.1186/1471-2164-8-428

    Article  PubMed  Google Scholar 

  • Pratt C (1971) Reproductive anatomy in cultivated grapes: a review. Am J Enol Vitic 22:92–109

    Google Scholar 

  • R Development Core Team (2006) R: a language and environment for statistical computing. Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org

  • Ramakers C, Ruijter JM, Deprez RHL, Moorman AFM (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66. doi:10.1016/S0304-3940(02)01423-4

    Article  PubMed  CAS  Google Scholar 

  • Razem FA, El-Kereamy A, Abrams SR, Hill RD (2006) The RNA-binding protein FCA is an abscisic acid receptor. Nature 439(7074):290–294. doi:10.1038/nature04373

    Article  PubMed  CAS  Google Scholar 

  • Reid KR, Olsson N, Schlosser J, Peng F, Lund ST (2006) An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol 6:27. doi:10.1186/1471-2229-6-27

    Article  PubMed  CAS  Google Scholar 

  • Rodrigo MJ, Alquezar B, Zacarias L (2006) Cloning and characterization of two 9-cis-epoxycarotenoid dioxygenase genes, differentially regulated during fruit maturation and under stress conditions, from orange (Citrus sinensis L. Osbeck). J Exp Bot 57(3):633–643. doi:10.1093/jxb/erj048

    Article  PubMed  CAS  Google Scholar 

  • Sarry J-E, Sommerer N, Sauvage F-X, Bergoin A, Rossignol M, Albagnac G et al (2003) Grape berry biochemistry revisited upon proteomic analysis of the mesocarp. Proteomics 4(1):201–215. doi:10.1002/pmic.200300499

    Article  CAS  Google Scholar 

  • Schlosser J, Olsson N, Weis M, Reid K, Peng F, Lund S et al (2008) Cellular expansion and gene expression in the developing grape (Vitis vinifera L.). Protoplasma 232:255–265. doi:10.1007/s00709-008-0280-9

    Article  CAS  PubMed  Google Scholar 

  • Scienza A, Miravalle R, Visai C, Fregoni M (1978) Relationship between seed number, gibberellin and abscisic acid levels and ripening in Cabernet Sauvignon grape berries. Vitis 17:361–368

    CAS  Google Scholar 

  • Shen Y-Y, Wang X-F, Wu F-Q, Du S-Y, Cao Z, Shang Y et al (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823–826. doi:10.1038/nature05176

    Article  PubMed  CAS  Google Scholar 

  • Simkin AJ, Schwartz SH, Auldridge M, Taylor MG, Klee HJ (2004) The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles beta-ionone, pseudoionone, and geranylacetone. Plant J 40(6):882–892. doi:10.1111/j.1365-313X.2004.02263.x

    Article  PubMed  CAS  Google Scholar 

  • Soar CJ, Speirs J, Maffei SM, Loveys BR (2004) Gradients in stomatal conductance, xylem sap ABA and bulk leaf ABA along canes of Vitis vinifera cv. Shiraz: Molecular and physiological studies investigating their source. Funct Plant Biol 31:659–669. doi:10.1071/FP03238

    Article  CAS  Google Scholar 

  • Srinivasan C, Mullins MG (1981) Physiology of flowering in the grapevine—a review. Am J Enol Vitic 32(1):47–63

    CAS  Google Scholar 

  • Symons GM, Davies C, Shavrukov Y, Dry IB, Reid JB, Thomas MR (2006) Grapes on steroids. Brassinosteroids are involved in grape berry ripening. Plant Physiol 140:150–158. doi:10.1104/pp.105.070706

    Article  PubMed  CAS  Google Scholar 

  • Terrier N, Glissant D, Grimplet J, Barrieu F, Abbal P, Couture C et al (2005) Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development. Planta 222(5):832–847. doi:10.1007/s00425-005-0017-y

    Article  PubMed  CAS  Google Scholar 

  • The French–Italian Public Consortium for Grapevine Genome Characterization (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–468. doi:10.1038/nature06148

    Article  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. doi:10.1093/nar/22.22.4673

    Article  PubMed  CAS  Google Scholar 

  • Thompson AJ, Thorne ET, Burbridge A, Jackson AC, Sharp RE, Taylor IB (2004) Complementation of notabilis, an abscisic acid-deficient mutant of tomato: importance of sequence context and utility of partial complementation. Plant Cell Environ 27(4):459–471. doi:10.1111/j.1365-3040.2003.01164.x

    Article  CAS  Google Scholar 

  • Valon C, Smalle J, Goodman HM, Giraudat J (1993) Characterization of an Arabidopsis thaliana gene (TMKL1) encoding a putative transmembrane protein with an unusual kinase-like domain. Plant Mol Biol 23:415–421. doi:10.1007/BF00029017

    Article  PubMed  CAS  Google Scholar 

  • Velasco R, Zharkikh A, Troggio M et al (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS One 12:e1326. doi:10.1371/journal.pone.0001326

    Article  CAS  Google Scholar 

  • Wilson CL, Miller CJ (2005) Simpleaffy: A Bioconductor package for Affymetrix quality control and data analysis. Bioinformatics 21(18):3683–3685. doi:10.1093/bioinformatics/bti605

    Article  PubMed  CAS  Google Scholar 

  • Wu ZJ, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F (2003) A model-based background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 99:909–917. doi:10.1198/016214504000000683

    Article  Google Scholar 

  • Yang YH, Xiao YY, Segal M (2005) Identifying differentially expressed genes from microarray experiments via statistic synthesis. Bioinformatics 21(7):1084–1093. doi:10.1093/bioinformatics/bti108

    Article  PubMed  CAS  Google Scholar 

  • Yu X-C, Li M-J, Gao G-F, Feng H-Z, Geng X-Q, Peng C-C et al (2006) Abscisic acid stimulates a calcium-dependent protein kinase in grape berry. Plant Physiol 140:558–579. doi:10.1104/pp.105.074971

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Dr. Jörg Bohlmann for his helpful comments in review of this manuscript. We also thank Dr. Jin-Gui Chen for helpful discussions regarding GCR2. We thank Merinda Deng and Tanya Pirogovskaia for assistance with real-time RT-PCR experiments. The authors gratefully acknowledge funding for this research from Genome Canada and project management support from Genome British Columbia as part of the Genome Canada-Genoma España collaborative research and development initiative. The authors also wish to thank the Province of British Columbia and the BC wine industry for their continued support of research activities in the University of British Columbia Wine Research Centre.

Author information

Authors and Affiliations

  1. Wine Research Centre, Faculty of Land and Food Systems, University of British Columbia, Vancouver, BC, Canada

    Steven T. Lund, Fred Y. Peng, Karen E. Reid & James Schlosser

  2. Bioinformatics Group, Canada’s Michael Smith Genome Sciences Centre, BC Cancer Agency, Vancouver, BC, Canada

    Tarun Nayar

Authors
  1. Steven T. Lund
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fred Y. Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tarun Nayar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Karen E. Reid
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. James Schlosser
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Steven T. Lund.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(DOC 38 kb)

(XLS 18 kb)

(XLS 26 kb)

(XLS 21 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lund, S.T., Peng, F.Y., Nayar, T. et al. Gene expression analyses in individual grape (Vitis vinifera L.) berries during ripening initiation reveal that pigmentation intensity is a valid indicator of developmental staging within the cluster. Plant Mol Biol 68, 301–315 (2008). https://doi.org/10.1007/s11103-008-9371-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-008-9371-z

Keywords

Search

Navigation