Skip to main content
Log in

Root restriction affected anthocyanin composition and up-regulated the transcription of their biosynthetic genes during berry development in ‘Summer Black’ grape

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Root restriction was applied to ‘Summer black’ grape (Vitis vinifera L. × Vitis labrusca L.) to investigate its effect on anthocyanin biosynthesis in grape berry during development. Anthocyanin composition and expression patterns of 16 genes in anthocyanin pathway were thus analyzed. The results showed that the anthocyanin levels in berry skin were significantly increased and the anthocyanin profile was enriched. Gene expression pattern revealed that the increased anthocyanins coincide with the up-regulated expression of all 16 genes investigated, including phenylalanine ammonia-lyase, 4-coumarate CoA ligase, chalcone synthase 1, chalcone synthase 2, chalcone synthase 3, chalcone isomerase, flavanone 3-hydroxylase 1, flavanone 3-hydroxylase 2, flavonoid 3′-hydroxylase (F3′H), flavonoid 3′,5′-hydroxylase (F3′5′H), di-hydroflavonol 4-reductase, leucoanthocyanidin dioxygenase, O-methyltransferases (OMT), UDP-glucose:flavonoid 3-O-glucosyl-transferase (3GT), UDP-glucose:flavonoid 5-O-glucosyl-transferase (5GT) and glutathione S-transferase (GST). The increased total anthocyanins predominantly resulted from the increase of tri-hydroxylated, methoxylated and mono-glycosylated rather than di-hydroxylated, non-methoxylated, and di-glycosylated forms, which might be due to the differential regulation of F3′5′H/F3′H, OMT and 3GT, respectively.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

Abbreviations

TSS:

Total soluble solid

TA:

Titratable acid

Cy:

Cyanidin

Pn:

Peonidin

Dp:

Delphinidin

Pt:

Petunidin

Mv:

Malvidin

Pg:

Pelargonidin

PAL:

Phenylalanine ammonia-lyase

C4H:

Cinnamate-4-hydroxylase

4CL:

4-Coumarate CoA ligase

CHS:

Chalcone synthase

CHI:

Chalcone isomerase

F3H:

Flavanone 3β-hydroxylase

F3′H:

Flavonoid 3′-hydroxylase

F3′5′H:

Flavonoid 3′,5′-hydroxylase

DFR:

Di-hydroflavonol 4-reductase

LDOX:

Leucoanthocyanidin dioxygenase

OMT:

O-Methyltransferase

3GT:

UDP-Glucose:flavonoid 3-O-glucosyltransferase

5GT:

UDP-Glucose:flavonoid 5-O-glucosyltransferase

ACT:

Anthocyanin acyltransferase

Glu:

Glucoside

GST:

Glutathione S-transferase

DAA:

Days after anthesis

References

  • Antolin MC, Ayari M, Sanchez-Diaz M (2006) Effects of partial rootzone drying on yield, ripening and berry ABA in potted Tempranillo grapevines with split roots. Aust J Grape Wine Res 12(1):13–20

    Article  CAS  Google Scholar 

  • Bindon K, Dry P, Loveys B (2008) Influence of partial rootzone drying on the composition and accumulation of anthocyanins in grape berries (Vitis vinifera cv. Cabernet Sauvignon). Aust J Grape Wine Res 14(2):91–103

    Article  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(1):279–291

    Article  PubMed  CAS  Google Scholar 

  • Boland AM, Jerie PH, Mitchell PD, Goodwin I (2000a) Long-term effects of restricted root volume and regulated deficit irrigation on peach: I. Growth and mineral nutrition. J Am Soc Hortic Sci 125(1):135–142

    Google Scholar 

  • Boland AM, Jerie PH, Mitchell PD, Goodwin I, Connor DJ (2000b) Long-term effects of restricted root volume and regulated deficit irrigation con peach: II. Productivity and water use. J Am Soc Hortic Sci 125(1):143–148

    Google Scholar 

  • Castellarin S, Di Gaspero G (2007) Transcriptional control of anthocyanin biosynthetic genes in extreme phenotypes for berry pigmentation of naturally occurring grapevines. BMC Plant Biol 7(1):1–10

    Article  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  Google Scholar 

  • Castellarin S, Matthews M, Di Gaspero G, Gambetta G (2007a) Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries. Planta 227(1):101–112

    Article  PubMed  CAS  Google Scholar 

  • Castellarin SD, Pfeiffer A, Sivilotti P, Degan M, Peterlunger E, Di Gaspero G (2007b) Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant Cell Environ 30(11):1381–1399

    Article  PubMed  CAS  Google Scholar 

  • Castillo-Munoz N, Fernandez-Gonzalez M, Gomez-Alonso S, Garcia-Romero E, Hermosin-Gutierrez I (2009) Red-color related phenolic composition of Garnacha Tintorera (Vitis vinifera L.) grapes and red wines. J Agric Food Chem 57(17):7883–7891

    Article  PubMed  CAS  Google Scholar 

  • Chorti E, Guidoni S, Ferrandino A, Novello V (2010) Effect of different cluster sunlight exposure levels on ripening and anthocyanin accumulation in Nebbiolo grapes. Am J Enol Vitic 61(1):23–30

    CAS  Google Scholar 

  • Christie PJ, Alfenito MR, Walbot V (1994) Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta 194(4):541–549

    Article  CAS  Google Scholar 

  • Conn S, Curtin C, Bézier A, Franco C, Zhang W (2008) Purification, molecular cloning, and characterization of glutathione S-transferases (GSTs) from pigmented Vitis vinifera L. cell suspension cultures as putative anthocyanin transport proteins. J Exp Bot 59(13):3621

    Article  PubMed  CAS  Google Scholar 

  • Conn S, Franco C, Zhang W (2010) Characterization of anthocyanic vacuolar inclusions in Vitis vinifera L. cell suspension cultures. Planta 231(6):1–18

    Google Scholar 

  • Cortell JM, Halbleib M, Gallagher AV, Righetti TL, Kennedy JA (2007) Influence of vine vigor on grape (Vitis vinifera L. cv. Pinot Noir) anthocyanins. 1. Anthocyanin concentration and composition in fruit. J Agric Food Chem 55(16):6575–6584

    Article  PubMed  CAS  Google Scholar 

  • Dixon DP, Cole DJ, Edwards R (1998) Purification, regulation and cloning of a glutathione transferase (GST) from maize resembling the auxin-inducible type-III GSTs. Plant Mol Biol 36(1):75–87

    Article  PubMed  CAS  Google Scholar 

  • Downey MO, Harvey JS, Robinson SP (2004) The effect of bunch shading on berry development and flavonoid accumulation in Shiraz grapes. Aust J Grape Wine Res 10(1):55–73

    Article  CAS  Google Scholar 

  • Dry PR, Loveys BR (1998) Factors influencing grapevine vigour and the potential for control with partial rootzone drying. Aust J Grape Wine Res 4(3):140–148

    Article  Google Scholar 

  • Falginella L, Di Gaspero G, Castellarin SD (2012) Expression of flavonoid genes in the red grape berry of ‘Alicante Bouschet’ varies with the histological distribution of anthocyanins and their chemical composition. Planta 236(4):1–15

    Google Scholar 

  • Gueffroy DE, Kepner RE, Webb AD (1971) Acylated anthocyanin pigments in Vitis vinifera grapes: identification of malvidin-3-(6-p-coumaroyl) glucoside. Phytochemistry 10(4):813–819

    Article  CAS  Google Scholar 

  • Guidoni S, Allara P, Schubert A (2002) Effect of cluster thinning on berry skin anthocyanin composition of Vitis vinifera cv. Nebbiolo. Am J Enol Vitic 53(3):224–226

    CAS  Google Scholar 

  • He F, Mu L, Yan G-L, Liang N-N, Pan Q-H, Wang J, Reeves MJ, Duan C-Q (2010) Biosynthesis of anthocyanins and their regulation in colored grapes. Molecules 15(12):9057–9091

    Article  PubMed  CAS  Google Scholar 

  • Holton TA, Cornish EC (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7(7):1071–1083

    PubMed  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 (Amsterdam, Neth) 167(2):247–252

    CAS  Google Scholar 

  • Jing P, Bomser JA, Schwartz SJ, He J, Magnuson BA, Giusti MM (2008) Structure–function relationships of anthocyanins from various anthocyanin-rich extracts on the inhibition of colon cancer cell growth. J Agric Food Chem 56(20):9391–9398

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi S (2009) Regulation of anthocyanin biosynthesis in grapes. J Jpn Soc Hortic Sci 78(4):387–393

    Article  CAS  Google Scholar 

  • Kobayashi S, Ishimaru M, Ding CK, Yakushiji H, Goto N (2001) Comparison of UDP-glucose:flavonoid 3-O-glucosyltransferase (UFGT) gene sequences between white grapes (Vitis vinifera) and their sports with red skin. Plant Sci (Amsterdam, Neth) 160(3):543–550

    CAS  Google Scholar 

  • Kobayashi S, Ishimaru M, Hiraoka K, Honda C (2002) Myb-related genes of the Kyoho grape (Vitis labruscana) regulate anthocyanin biosynthesis. Planta 215(6):924–933

    Article  PubMed  CAS  Google Scholar 

  • Liang ZC, Wu BH, Fan PG, Yang CX, Duan W, Zheng XB, Liu CY, Li SH (2008) Anthocyanin composition and content in grape berry skin in Vitis germplasm. Food Chem 111(4):837–844

    Article  CAS  Google Scholar 

  • Manach C, Mazur A, Scalbert A (2005) Polyphenols and prevention of cardiovascular diseases. Curr Opin Lipidol 16(1):77–84

    Article  PubMed  CAS  Google Scholar 

  • Mataa M, Tominaga S (1998) Effects of root restriction on tree development in Ponkan mandarin (Citrus reticulata Blanco). J Am Soc Hortic Sci 123(4):651–655

    Google Scholar 

  • McCloskey LP, Yengoyan L (1981) Analysis of anthocyanins in Vitis vinifera wines and red color versus aging by HPLC and spectrophotometry. Am J Enol Vitic 32(4):257–261

    CAS  Google Scholar 

  • Mertens-Talcott SU, Rios J, Jilma-Stohlawetz P, Pacheco-Palencia LA, Meibohm B, Talcott ST, Derendorf H (2008) Pharmacokinetics of anthocyanins and antioxidant effects after the consumption of anthocyanin-rich acai juice and pulp (Euterpe oleracea Mart.) in human healthy volunteers. J Agric Food Chem 56(17):7796–7802

    Article  PubMed  CAS  Google Scholar 

  • Mori K, Sugaya S, Gemma H (2005) Decreased anthocyanin biosynthesis in grape berries grown under elevated night temperature condition. Sci Hortic 105(3):319–330

    Article  CAS  Google Scholar 

  • Myers S (1992) Root restriction of apple and peach with in-ground fabric containers. Acta Hortic 322:215–219

    Google Scholar 

  • Nadal M, Lampreave M (2004) The effects of irrigation on the water relations of the grapevine, yield, grape and wine composition of tempranillo CV in mediterranean climate. J Int Sci Vigne Vin 38(1):75–80

    Google Scholar 

  • Naor A, Gal Y, Bravdo B (2002) Shoot and cluster thinning influence vegetative growth, fruit yield, and wine quality of ‘Sauvignon blanc’ grapevines. J Am Soc Hortic Sci 127(4):628–634

    Google Scholar 

  • Ojeda H, Andary C, Kraeva E, Carbonneau A, Deloire A (2002) Influence of pre- and postveraison water deficit on synthesis and concentration of skin phenolic compounds during berry growth of Vitis vinifera cv. Shiraz. Am J Enol Vitic 53(4):261–267

    CAS  Google Scholar 

  • Ozden M, Vardin H, Simsek M, Karaaslan M (2010) Effects of rootstocks and irrigation levels on grape quality of Vitis vinifera L. cv. Shiraz. Afr J Biotechnol 9(25):3801–3807

    CAS  Google Scholar 

  • Pomar F, Novo M, Masa A (2005) Varietal differences among the anthocyanin profiles of 50 red table grape cultivars studied by high performance liquid chromatography. J Chromatogr A 1094(1–2):34–41

    PubMed  CAS  Google Scholar 

  • Prior RL (2003) Fruits and vegetables in the prevention of cellular oxidative damage. Am J Clin Nutr 78(3):570–578

    Google Scholar 

  • Sarma AD, Sharma R (1999) Anthocyanin-DNA copigmentation complex: mutual protection against oxidative damage. Phytochemistry 52(7):1313–1318

    Article  CAS  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protocols 3(6):1101–1108

    Article  CAS  Google Scholar 

  • Seitz C, Eder C, Deiml B, Kellner S, Martens S, Forkmann G (2006) Cloning, functional identification and sequence analysis of flavonoid 3′-hydroxylase and flavonoid 3′,5′-hydroxylase cDNAs reveals independent evolution of flavonoid 3′,5′-hydroxylase in the Asteraceae family. Plant Mol Biol 61(3):365–381

    Article  PubMed  CAS  Google Scholar 

  • Terrier N, Glissant D, Grimplet J, Barrieu F, Abbal P, Couture C, Ageorges A, Atanassova R, Léon C, Renaudin J-P, Dédaldéchamp 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(5):832–847

    Article  PubMed  CAS  Google Scholar 

  • Vian MA, Tomao V, Coulomb PO, Lacombe JM, Dangles O (2006) Comparison of the anthocyanin composition during ripening of Syrah grapes grown using organic or conventional agricultural practices. J Agric Food Chem 54(15):5230–5235

    Article  PubMed  CAS  Google Scholar 

  • Wang SP, Okamoto G, Hirano K (1997) Vine growth and fruit development of ‘Pione’ grapes planted in root-restricted buried and raised beds. J Jpn Soc Hortic Sci 66(2):253–259

    Article  CAS  Google Scholar 

  • Wang SP, Okamoto G, Hirano K (1998) Effects of rooting-zone restriction on the changes in carbohydrates and nitrogenous compounds in ‘Kyoho’ grapevines during winter dormancy and early shoot growth. J Jpn Soc Hortic Sci 67(4):577–582

    Article  CAS  Google Scholar 

  • Wang S, Okamoto G, Hirano K, Lu J, Zhang C (2001) Effects of restricted rooting volume on vine growth and berry development of Kyoho grapevines. Am J Enol Vitic 52(3):248–253

    Google Scholar 

  • Wang B, He J, Duan C, Yu X, Zhu L, Xie Z, Zhang C, Xu W, Wang S (2012) Root restriction affects anthocyanin accumulation and composition in berry skin of Kyoho grape (Vitis vinifera L. × Vitis labrusca L.) during ripening. Sci Hortic 137:20–28

    Article  CAS  Google Scholar 

  • Webster AD, Atkinson CJ, Vaughan SJ, Lucas AS, Mallling E, Mallling W (1997) Controlling the shoot growth and cropping of sweet cherry trees using root pruning or root restriction techniques. Acta Hortic 451:643–652

    Google Scholar 

  • Wen P-F, Chen J-Y, Kong W-F, Pan Q-H, Wan S-B, Huang W-D (2005) Salicylic acid induced the expression of phenylalanine ammonia-lyase gene in grape berry. Plant Sci (Amsterdam, Neth) 169(5):928–934

    CAS  Google Scholar 

  • Wulf LW, Nagel CW (1978) High-pressure liquid chromatographic separation of anthocyanins of Vitis vinifera. Am J Enol Vitic 29(1):42–49

    CAS  Google Scholar 

  • Xie ZS, Li B, Forney CF, Xu WP, Wang SP (2009) Changes in sugar content and relative enzyme activity in grape berry in response to root restriction. Sci Hortic 123(1):39–45

    Article  CAS  Google Scholar 

  • Yamane T, Jeong ST, Goto-Yamamoto N, Koshita Y, Kobayashi S (2006) Effects of temperature on anthocyanin biosynthesis in grape berry skins. Am J Enol Vitic 57(1):54–59

    CAS  Google Scholar 

  • Yang TY, Zhu LN, Wang SP, Gu WJ, Huang DF, Xu WP, Jiang AL, Li SC (2007) Nitrate uptake kinetics of grapevine under root restriction. Sci Hortic 111(4):358–364

    Article  CAS  Google Scholar 

  • Zhu L, Wang S, Yang T, Zhang C, Xu W (2006) Vine growth and nitrogen metabolism of ‘Fujiminori’ grapevines in response to root restriction. Sci Hortic 107(2):143–149

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by the Special Funds of Modern Industrial Technology System for Agriculture (CARS-30) and National Natural Science Foundation of China (31201580/C150101). We wish to thank Dr. Juan Xu from National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, for her comments and corrections.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shiping Wang.

Additional information

Communicated by L. Bavaresco.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table S1 (DOC 35 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, B., He, J., Bai, Y. et al. Root restriction affected anthocyanin composition and up-regulated the transcription of their biosynthetic genes during berry development in ‘Summer Black’ grape. Acta Physiol Plant 35, 2205–2217 (2013). https://doi.org/10.1007/s11738-013-1257-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-013-1257-2

Keywords

Navigation