Skip to main content
Log in

Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Water deficits consistently promote higher concentrations of anthocyanins in red winegrapes and their wines. However, controversy remains as to whether there is any direct effect on berry metabolism other than inhibition of growth. Early (ED) and late (LD) season water deficits, applied before or after the onset of ripening (veraison), were imposed on field grown Vitis vinifera “Cabernet Sauvignon”, and the responses of gene expression in the flavonoid pathway and their corresponding metabolites were determined. ED accelerated sugar accumulation and the onset of anthocyanin synthesis. Both ED and LD increased anthocyanin accumulation after veraison. Expression profiling revealed that the increased anthocyanin accumulation resulted from earlier and greater expression of the genes controlling flux through the anthocyanin biosynthetic pathway, including F3H, DFR, UFGT and GST. Increases in total anthocyanins resulted predominantly from an increase of 3′4′5′-hydroxylated forms through the differential regulation of F3′H and F3′5′H. There were limited effects on proanthocyanidin, other flavonols, and on expression of genes committed to their synthesis. These results demonstrate that manipulation of abiotic stress through applied water deficits not only modulates compositional changes during berry ripening, but also alters the timing of particular aspects of the ripening process.

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

Access this article

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
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

C:

Control(s)

ED:

Early deficit

LD:

Late deficit

DAA:

Days after anthesis

References

  • Acevedo C, Ortega-Farias S, Moreno Y, Cordova F (2004) Effects of different levels of water application in pre- and post-veraison on must composition and wine color (cv. Cabernet Sauvignon). Acta Hortic 664:483–489

    Google Scholar 

  • Ageorges A, Fernandez L, Vialet S, Merdinoglu D, Terrier N, Romieu C (2006) Four specific isogenes of the anthocyanin metabolic pathway are systematically co-expressed with the red colour of grape berries. Plant Sci 170:372–383

    Article  CAS  Google Scholar 

  • Bogs J, Downey MO, Harvey JS, Ashton AR, Tanner GJ, Robinson SP (2005) Proanthocyanidin synthesis and expression of genes encoding leucoanthocyanidin reductase and anthocyanidin reductase in developing grape berries and grapevine leaves. Plant Physiol 139:652–663

    Article  PubMed  CAS  Google Scholar 

  • Bogs J, Ebadi A, McDavid D, Robinson SP (2006) Identification of the flavonoid hydroxylases from grapevine and their regulation during fruit development. Plant Physiol 140:279–291

    Article  PubMed  CAS  Google Scholar 

  • Bondada BR, Matthews MA, Shackel KA (2005) Functional xylem in the post-veraison grape berry. J Exp Bot 56:2949–2957

    Article  PubMed  CAS  Google Scholar 

  • Cakir 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 15:2165–80

    Article  PubMed  CAS  Google Scholar 

  • Castellarin SD, Di Gaspero G, Marconi R, Nonis A, Peterlunger E, Paillard S, Adam-Blondon AF, Testolin R (2006) Colour variation in red grapevines (Vitis vinifera L.): genomic organisation, expression of flavonoid 3′-hydroxylase, flavonoid 3′,5′-hydroxylase genes and related metabolite profiling of red cyanidin-/blue delphinidin-based anthocyanins in berry skin. BMC Genomics 7:12

    Article  PubMed  CAS  Google Scholar 

  • Castellarin SD, Pfeiffer A, Sivilotti P, Degan M, Peterlunger E, Di Gaspero G (2007) Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant Cell Environ (in press)

  • Coombe BG (1976) The development of fleshy fruits. Annu Rev Plant Physiol Plant Mol Biol 27:207–228

    CAS  Google Scholar 

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

    Google Scholar 

  • Cos P, De Bruyne T, Hermans N, Apers S, Berghe DV, Vlietinck AJ (2004) Proanthocyanidins in health care: current and new trends. Curr Med Chem 11:1345–59

    PubMed  CAS  Google Scholar 

  • Dokoozlian NK, Kliewer WM (1996) Influence of light on grape berry growth and composition varies during fruit development. J Am Soc Hortic Sci 121:869–874

    Google Scholar 

  • Downey MO, Harvey JS, Robinson SP (2003) Synthesis of flavonols and expression of flavonol synthase genes in developing grape berries of Shiraz and Chardonnay (Vitis vinifera L.). Aust J Grape Wine Res 9:110–121

    CAS  Google Scholar 

  • Gollop R, Even S, Colova-Tsolova V, Perl A (2002) Expression of the grape dihydroflavonol reductase gene and analysis of its promoter region. J Exp Bot 53:1397–1409

    Article  PubMed  CAS  Google Scholar 

  • Goto-Yamamoto N, Wan GH, Masaki K, Kobayashi S (2002) Structure and transcription of three chalcone synthase genes of grapevine (Vitis vinifera). Plant Sci 162:867–872

    Article  CAS  Google Scholar 

  • Greenspan MD, Schultz HR, Matthews MA (1996) Field evaluation of water transport in grape berries during water deficits. Physiol Plant 97:55–62

    Article  CAS  Google Scholar 

  • Greenspan MD, Shackel KA, Matthews MA (1994) Developmental changes in the diurnal water budget of the grape berry exposed to water deficits. Plant Cell Environ 17:811–820

    Article  Google Scholar 

  • Harbertson JF, Kennedy JA, Adams DO (2002) Tannin in skin and seeds of Cabernet Sauvignon, Syrah, and Pinot noir berries during ripening. Am J Enol Vitic 53:54–59

    CAS  Google Scholar 

  • Iandolino AB, da Silva FG, Lim H, Choi H, Williams LE, Cook DR (2004) High-quality RNA, cDNA, and derived EST libraries from grapevine (Vitis vinifera L.). Plant Mol Biol Rep 22:269–278

    CAS  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

    Article  CAS  Google Scholar 

  • Jeong ST, Goto-Yamamoto N, Hashizume K, Esaka M (2006) Expression of the flavonoid 3′-hydroxylase and flavonoid 3′,5′-hydroxylase genes and flavonoid composition in grape (Vitis vinifera). Plant Sci 170:61–69

    Article  CAS  Google Scholar 

  • Keller M (2005) Deficit irrigation and vine mineral nutrition. Am J Enol Vitic 56:267–283

    CAS  Google Scholar 

  • Kennedy JA, Matthews MA, Waterhouse AL (2002) Effect of maturity and vine water status on grape skin and wine flavonoids. Am J Enol Vitic 53:268–274

    CAS  Google Scholar 

  • Kitamura S, Shikazono N, Tanaka A (2004) Trasparent testa 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. Plant J 37:104–114

    Article  PubMed  CAS  Google Scholar 

  • Marrs KA, Alfenito MR, Lloyd AM, Walbot V (1995) A glutathione S-transferase involved in vacuolar transfer encoded by the maize gene bronze-2. Nature 375:397–400

    Article  PubMed  CAS  Google Scholar 

  • Matthews MA, Anderson MM (1988) Fruit ripening in Vitis vinifera L.: responses to seasonal water defits. Am J Enol Vitic 39:313–320

    Google Scholar 

  • Matthews MA, Anderson MM (1989) Reproductive development in grape (Vitis vinifera L.): responses to seasonal water deficits. Am J Enol Vitic 40:52–60

    Google Scholar 

  • Matthews MA, Anderson MM, Schultz HR (1987a) Phenologic and growth responses to early and late season water deficits in Cabernet franc. Vitis 26:147–160

    Google Scholar 

  • Matthews MA, Cheng GW, Weinbaum S (1987b) Changes in water potential and dermal extensibility during grape berry development. J Am Soc Hortic Sci 112:314–319

    Google Scholar 

  • Matthews MA, Ishii R, Anderson MM, O’Mahony M (1990) Dependence of wine sensory attributes on vine water status. J Sci Food Agric 51:321–335

    Article  CAS  Google Scholar 

  • Matthews MA, Shackel KA (2005) Growth and water transport in fleshy fruit. In: Vascular transport in plants. Elsevier, Boston, pp 181–197

  • Mueller LA, Goodman CD, Silady RA,Walbot V (2000) AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid-binding protein. Plant Physiol 123:1561–1570

    Article  PubMed  CAS  Google Scholar 

  • Ojeda H, Andary C, Kraeva E, Carbonneau A, Deloire A (2002) Influence of pre- and post-veraison water deficit on synthesis and concentration of skin phenolic compounds during berry growth of Vitis vinifera cv Shiraz. Am J Enol Vitic 53:261–267

    CAS  Google Scholar 

  • Pan QH, Li MJ, Peng CC, Zhang N, Zou X, Zou KQ, Wang XL, Yu XC, Wang XF, Zhang DP (2005) Abscisic acid activates acid invertases in developing grape berry. Physiol Plant 125:157–170

    Article  CAS  Google Scholar 

  • Patrick CW (1997) Phloem unloading: sieve element unloading and post-sieve element transport. Annu Rev Plant Physiol Plant Mol Biol 48:191–222

    Article  PubMed  CAS  Google Scholar 

  • Roby G, Harbetson JF, Adams DA, Matthews MA (2004) Berry size and vine water deficits as factors in winegrape composition: anthocyanins and tannins. Aust J Grape Wine Res 10:100–107

    Article  CAS  Google Scholar 

  • Sarni P, Fulcrand H, Souillol V, Souquet JM, Cheynier V (1995) Mechanisms of anthocyanin degredation in grape must-like solutions. J Sci Food Agric 69:385–391

    Article  CAS  Google Scholar 

  • Sipiora MJ, Gutiérrez Granda MJ (1998) Effects of pre- veraison irrigation cutoff and skin contact time on the composition, color, phenolic content of young Cabernet sauvignon wines in Spain. Am J Enol Vitic 49:152–162

    CAS  Google Scholar 

  • Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140:637–646

    Article  PubMed  CAS  Google Scholar 

  • Sparvoli F, Martin C, Scienza A, Gavazzi G, Tonelli C (1994) Cloning and molecular analysis of structural genes involved in flavonoid and stilbene biosynthesis in grape (Vitis vinifera L.). Plant Mol Biol 24:743–755

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Tanner GJ, Francki KT, Abrahams S, Watson JM, Larkin PJ, Ashton AR (2003) Proanthocyanidin biosynthesis in plants: Purification of legume leucoanthocyanidin reductase and molecular cloning of its cDNA. J Biol Chem 278:31647–31656

    Article  PubMed  CAS  Google Scholar 

  • Terrier N, Glissant D, Grimplet J, Barrieu F, Abbal P, Couture C, Ageorges A, Atanassova R, Leon C, Renaudin JP, Dedaldechamp F, Romieu C, Delrot S, Hamdi S (2005) Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development. Planta 222:832–847

    Article  PubMed  CAS  Google Scholar 

  • Thole JM, Kraft TF, Sueiro LA, Kang YH, Gills JJ, Cuendet M, Pezzuto JM, Seigler DS, Lila MA (2006) A comparative evaluation of the anticancer properties of European and american elderberry fruits. J Med Food 9:498–504

    Article  PubMed  CAS  Google Scholar 

  • Thomas TR, Shackel KA, Matthews MA (2006) Direct in-situ measurement of cell turgor in grape (Vitis vinifera L.) berries during development and in response to plant water deficits. Plant Cell Environ 29:993–1001

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank R.H. Phillips for cooperation and access to vineyard, Mark Krasnow for field assistance, Greg Giguere for water management, and Mark Downey for advice in HPLC analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gregory A. Gambetta.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Castellarin, S.D., Matthews, M.A., Di Gaspero, G. et al. Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries. Planta 227, 101–112 (2007). https://doi.org/10.1007/s00425-007-0598-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-007-0598-8

Keywords

Navigation