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ABA Initiates Anthocyanin Production in Grape Cell Cultures

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Abstract

Abscisic acid (ABA) has a well-known positive impact on grape ripening, especially color development, but its role in the initiation of anthocyanin synthesis remains unclear. To elucidate this point, ABA treatment was applied to a simple Vitis vinifera model, consisting of Cabernet Sauvignon cell suspensions that do not spontaneously produce anthocyanins under laboratory conditions. Endogenous ABA levels, the expression of some genes in the upstream part of the anthocyanin pathway, and anthocyanin content were determined. Exogenous ABA treatment sharply increased cell ABA content and induced both structural and regulatory genes involved in anthocyanin production. These changes were promptly detected, as early as 6 h after ABA treatment, whereas anthocyanin production was observed only after 4 days in culture. These results demonstrate that ABA promotes anthocyanin synthesis in grape cell culture.

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References

  • Alleweldt G, Koch R (1977) Der äthylengehalt reifender Weinbeeren. Vitis 16:263–271

    CAS  Google Scholar 

  • Antolin MC, Baigorri H, De Luis I, Aguirrezabal F, Gény L, Broquedis M, Sanchez-Diaz M (2003) ABA during reproductive development in non-irrigated grapes (Vitis vinifera L. cv. Tempranillo). Austr J Grape Wine Res 9:169–176

    Article  CAS  Google Scholar 

  • Aroca R, Vernieri P, Ruiz-Lozano JM (2008) Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery. J Exp Bot 59:2029–2041

    Article  CAS  PubMed  Google Scholar 

  • Ban T, Ishimura M, Kobayashi S, Shiozaki S, Goto-Yamamoto N, Horiuchi S (2003) Abscisic acid and 2,4-dichlorophenoxyacetic acid affect the expression of anthocyanin biosynthetic pathway genes in “Kyoho” grape berries. J Hortic Sci Biotechnol 78:586–589

    CAS  Google Scholar 

  • Broquedis M (1987) Utilisation de la dialyse et de la chromatographie ultra-rapide pour le dosage de l’acide abscissique : Application à la vigne. Vitis 26:19–26

    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 15:2165–2180

    Article  CAS  PubMed  Google Scholar 

  • Carrari F, Fernie AR, Iusem ND (2004) Heard it through the grape? ABA and sugar cross-talk: the ASR-story. Trends Plant Sci 9:57–59

    Article  CAS  PubMed  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 grape under seasonal water deficit. Plant Cell Environ 30:1381–1399

    Article  CAS  PubMed  Google Scholar 

  • Chervin C, El-Kereamy A, Roustan JP, Latche A, Lamon J, Bouzayen M (2005) Ethylene seems required for the berry development and ripening in grape, a non-climacteric fruit. Plant Sci 167:1301–1305

    Article  Google Scholar 

  • Chervin C, Tira-Umphon A, Terrier N, Zouine M, Severac D, Roustan JP (2008) Stimulation of the grape berry expansion by ethylene and effects on related gene transcripts, over the ripening phase. Physiol Plant 134:534–546

    Article  CAS  PubMed  Google Scholar 

  • Chervin C, Tira-Umphon A, Chatelet P, Jauneau A, Boss PK, Tesniere C (2009) Ethylene and other stimuli affect expression of the UDP glucose-flavonoid 3-O-glucosyltransferase in a non-climacteric fruit. Vitis 48:11–16

    CAS  Google Scholar 

  • Coombe BG, Hale CR (1973) The hormone content of ripening grape berries and the effects of growth substance treatments. Plant Physiol 51:629–634

    Article  CAS  PubMed  Google Scholar 

  • De La Hera Orts ML, Martinez-Cutillas A, Lopez-Lorca JM, Perez-Prieto LJ, Gomez-Plaza E (2005) Effect of deficit irrigation on anthocyanin content of Monastrell grapes and wines. J Int Sci Vigne Vin 39:47–55

    CAS  Google Scholar 

  • Deluc LG, Grimplet J, Wheatley MD, Tillett RL, Quilici DR, Osborne C, Schooley DA, Schlauch KA, Cushman JC, Cramer GR (2007) Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development. BMC Genomics 8:429

    Article  PubMed  Google Scholar 

  • Deluc LG, Quilici DR, Decendit A, Grimplet J, Wheatley MD, Schlauch KA, Mérillon JM, Cushman JC, Cramer GR (2009) Water deficit alters differentially metabolic pathways affecting important flavor and quality traits in grape berries of Cabernet Sauvignon and Chardonnay. BMC Genomics 10:212

    Article  PubMed  Google Scholar 

  • Deytieux-Belleau C, Gagné S, L’hyvernay A, Donèche B, Gény L (2007) Possible roles of both abscisic acid and indol-acetic acid in controlling grape berry ripening process. J Int Sci Vigne Vin 41:141–148

    CAS  Google Scholar 

  • El Kereamy A, Chervin C, Roustan JP, Cheynier V, Souquet JM, Moutounet M, Raynal J, Ford C, Latché A, Pech JC, Bouzayen M (2003) Exogenous ethylene stimulates the long-term expression of genes related to anthocyanin biosynthesis in grape berries. Physiol Plant 119:175–182

    Article  CAS  Google Scholar 

  • Esteban MA, Villanueva MJ, Lissarrague JR (2001) Effect of irrigation on changes in the anthocyanin composition of the skin of cv. Tempranillo (Vitis vinifera L.) grape berries during ripening. J Sci Food Agric 81:409–420

    Article  CAS  Google Scholar 

  • Faurie B, Cluzet S, Mérillon J-M (2009) Implication of signaling pathways involving calcium, phosphorylation and active oxygen species in methyl jasmonate-induced defense responses in grape cell cultures. J Plant Physiol 166:1863–1877

    Article  CAS  PubMed  Google Scholar 

  • Fisher TC, Halbwirth H, Roemmelt S, Sabatini E, Schlangen K, Andreotti C, Spinelli F, Costa G, Forkmann G, Treutter D, Stich K (2006) Induction of polyphenol gene expression in apple (Malus × domestica) after the application of a dioxygenase inhibitor. Physiol Plant 128:604–617

    Article  Google Scholar 

  • Gagné S, Estève K, Deytieux C, Saucier C, Gény L (2006) Influence of abscisic acid in triggering “véraison” in grape berry skins of Vitis vinifera L. cv. Cabernet Sauvignon. J Int Sci Vigne Vin 40:7–14

    Google Scholar 

  • Gény L, Darrieumerlou A, Doneche B (2003) Conjugated polyamines and hydroxycinnamic acids in grape berries during Botrytis cinerea disease development: differences between “Noble rot” and “Grey mould”. Austr J Grape Wine Res 9:1–5

    Google Scholar 

  • Giribaldi M, Perugini I, Sauvage FX, Schubert A (2007) Analysis of protein changes during grape berry ripening by 2-DE and MALDI-TOF. Proteomics 7:3154–3170

    Article  CAS  PubMed  Google Scholar 

  • Guo D, Liang J, Li L (2009) Abscisic acid (ABA) inhibition of lateral root formation involves endogenous ABA biosynthesis in Arachis hypogaea L. Plant Growth Regul 58:173–179

    Article  CAS  Google Scholar 

  • Hale CR, Coombe BG (1974) Abscisic acid—an effect on the ripening of grapes. Bull R Soc NZ 12:831–836

    Google Scholar 

  • Hao G, Du X, Zhao F, Ji H (2010) Fungal endophytes-induced abscisic acid is required for flavonoid accumulation in suspension cells of Ginkgo biloba. Biotechnol Lett 32:305–314

    Article  CAS  PubMed  Google Scholar 

  • Hiratsuka S, Onodera H, Kawai Y, Kubo T, Itoh H, Wada R (2001a) ABA and sugar effects on anthocyanin formation in grape berry cultured in vitro. Sci Hortic 90:121–130

    Article  CAS  Google Scholar 

  • Hiratsuka S, Onodera H, Kawai Y, Kubo T, Itoh H, Wada R (2001b) Enzyme activity changes during anthocyanin synthesis in “Olympia” grape berries. Sci Hortic 90:255–264

    Article  CAS  Google Scholar 

  • Hung KT, Cheng DG, Hsu YT, Kao CH (2008) Abscisic acid-induced hydrogen peroxide is required for anthocyanin accumulation in leaves of rice seedlings. J Plant Physiol 165:1280–1287

    Article  CAS  PubMed  Google Scholar 

  • Jeong ST, Goto-Yamamoto ON, 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 

  • Jiang Y, Joyce DC (2003) ABA effects on ethylene production, PAL activity, anthocyanin and phenolic concentrations of strawberry fruit. Plant Growth Reg 39:171–174

    Article  Google Scholar 

  • Kataoka I, Sugiura A, Utsunomiya N, Tomana T (1982) Effect of abscisic acid and defoliation on anthocyanin accumulation in Kyoho grapes (Vitis vinifera L. × V. labruscana Bailey). Vitis 21:325–332

    CAS  Google Scholar 

  • Kim SK, Kim JT, Jeong SH, Nam YS, Kim SH (1998) Effects of ethephon and ABA application on coloration, content, and composition of anthocyanin in grapes. J Korean Soc Hortic Sci 39:547–554

    CAS  Google Scholar 

  • Kim JS, Lee BH, Kim SH, Oh KH, Yun Cho K (2006) Response to environmental and chemical signals for anthocyanin biosynthesis in nonchlorophyllous corn (Zea mays L.) leaf. J Plant Biol 49:16–25

    Article  CAS  Google Scholar 

  • Koussa T, Colin L, Broquedis M (2004) Endogenous levels of abscisic acid in various organs of Vitis vinifera L. (cv. Cabernet Sauvignon) between flower buds separated and grape closed stages. J Int Sci Vigne Vin 38:141–146

    CAS  Google Scholar 

  • Koyama K, Sadamatsu K, Goto-Yamamoto N (2009) Abscisic acid stimulated ripening and gene expression in berry skins of the Cabernet Sauvignon grape. Funct Integr Genomics. doi:10.1007/s10192-009-0145-8

  • Krisa S, Waffo-Téguo PW, Decendit A, Deffieux G, Vercauteren J, Mérillon JM (1999) Production of 13C-labelled anthocyanins by Vitis vinifera cell suspension cultures. Phytochemistry 51:651–656

    Article  CAS  PubMed  Google Scholar 

  • Lacampagne S, Gagné S, Gény L (2010) Involvement of abscisic acid in controlling the proanthocyanidin biosynthesis pathway in grape skin: new elements regarding the regulation of tannin composition and leucoanthocyanidin reductase (LAR) and anthocyanidin reductase (ANR) activities and expression. J Plant Growth Regul 29:81–90

    Article  CAS  Google Scholar 

  • Larronde F, Krisa S, Decendit A, Chèze C, Deffieux G, Mérillon JM (1998) Regulation of polyphenol production in Vitis vinifera cell suspension cultures by sugars. Plant Cell 17:946–950

    CAS  Google Scholar 

  • Lecourieux F, Lecourieux D, Vignault C, Delrot S (2010) A sugar-inducible protein kinase, VvSK1, regulates hexose transport and sugar accumulation in grape cells. Plant Physiol 152:1096–1106

    Article  CAS  PubMed  Google Scholar 

  • Lund ST, Peng FY, Nayar T, Reid KE, Schlosser J (2008) 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

    Article  CAS  PubMed  Google Scholar 

  • Matsushima J, Hiratsuka S, Taniguchi N, Wada R, Suzaki N (1989) Anthocyanin accumulation and sugar content in the skin of grape cultivar ‘Olympia’ treated with ABA. J Jpn Soc Hortic Sci 58:551–555

    Article  CAS  Google Scholar 

  • Nagira Y, Ozeki Y (2004) A system in which anthocyanin synthesis is induced in regenerated Torenia shoots. J Plant Res 117:377–383

    Article  CAS  PubMed  Google Scholar 

  • Nagira Y, Ikegami K, Koshiba T, Ozeki Y (2006) Effect of ABA upon anthocyanin synthesis in regenerated Torenia shoots. J Plant Res 119:137–144

    Article  CAS  PubMed  Google Scholar 

  • Owen SJ, Lafond MD, Bowen P, Bogdanoff C, Usher K, Abrams SR (2009) Profiles of abscisic acid and its catabolites in developing merlot grape (Vitis vinifera) berries. Am J Enol Viticult 60:277–284

    CAS  Google Scholar 

  • Paek NC, Lee BM, Bai DG, Cobb BG, Magill CW, Smith JD (1997) Regulatory roles of abscisic acid for anthocyanin synthesis in maize kernels. Maydica 42:385–391

    Google Scholar 

  • Palejwala VA, Parikh HR, Modi VV (1985) The role of abscisic acid in the ripening of grapes. Physiol Plant 65:498–502

    Article  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 

  • Peppi MC, Fidelibus MW, Dokoozlian N (2006) Abscisic acid application timing and concentration affect firmness, pigmentation, and color of “Flame seedless” grapes. Hortic Sci 42:1440–1445

    Google Scholar 

  • Pilati S, Perazzolli M, Malossini A, Cestaro A, Demattè L, Fontana P, Dal Ri A, Viola R, Velasco R, Moser C (2007) Genome-wide transcriptional analysis of grape berry ripening reveals a set of genes similarly modulated during three seasons and the occurrence of an oxidative burst at véraison. BMC Genomics 8:428

    Article  PubMed  Google Scholar 

  • Riberéau-Gayon P, Stonestreet E (1965) Le dosage des anthocyanes dans le vin rouge. Bull Soc Chim 9:2649–2652

    Google Scholar 

  • Shiozaki S, Kamata Y, Ogata T, Horiuchi S, Kawase K (1999) Localization of abscisic acid in grape berry by immunohistochemical techniques. J Jpn Soc Hortic Sci 68:1–9

    Article  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Szyjewicz E, Kliewer WM (1983) Influence of timing of ethephon application on yield and fruit composition of ‘Chenin blanc’ grapes. Am J Enol Viticult 34:53–56

    CAS  Google Scholar 

  • Tattersall EA, Ergul A, Alkayal F, Deluc L, Cushman JC, Cramer GR (2005) Comparison of methods for isolating high-quality RNA from leaves of grape. Am J Enol Viticult 56:400–407

    CAS  Google Scholar 

  • Vágner M, Vondráková Z, Strnadová Z, Eder J, Macháčková I (1998) Endogenous levels of plant growth hormones during early stages of somatic embryogenesis of Picea abies. Adv Hortic Sci 12:11–18

    Google Scholar 

  • Wheeler S, Loveys B, Ford C, Davies C (2009) The relationship between the expression of abscisic acid biosynthesis genes, accumulation of abscisic acid and the promotion of Vitis vinifera L. berry ripening by abscisic acid. Austr J Grape Wine Res 15:195–204

    Article  CAS  Google Scholar 

  • Yu XC, Li MJ, Gao GF, Feng HZ, Geng XQ, Peng CC, Zhu SY, Wang XJ, Shen YY, Zhang DP (2006) Abscisic acid stimulates a calcium-dependent protein kinase in grape berry. Plant Physiol 140:558–579

    Article  CAS  PubMed  Google Scholar 

  • Zeevaart JA, Creelman RA (1988) Metabolism and physiology of abscisic acid. Ann Rev Plant Physiol Plant Mol Biol 39:439–473

    Article  CAS  Google Scholar 

  • Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res 97:111–119

    Article  Google Scholar 

  • Zhang M, Leng P, Zhang G, Li X (2009a) Cloning and functional analysis of 9-cis-epoxycarotenoid dioxygenase (NCED) genes encoding a key enzyme during abscisic acid biosynthesis from peach and grape fruits. J Plant Physiol 166:1241–1252

    Article  CAS  PubMed  Google Scholar 

  • Zhang M, Yuan B, Leng P (2009b) The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. J Exp Bot 60:1579–1588

    Article  CAS  PubMed  Google Scholar 

  • Zheng Y, Tian L, Liu H, Pan Q, Zhan J, Huang W (2009) Sugars induce anthocyanin accumulation and flavanone 3-hydroxylase expression in grape berries. Plant Growth Regul 58:251–260

    Article  CAS  Google Scholar 

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Acknowledgments

The authors thank the CIVB (Conseil Interprofessionnel du Vin de Bordeaux—Bordeaux Wine Council) for financial support, Arthur Soriano for technical assistance, and Aquitaine Traduction for reviewing the English manuscript.

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Correspondence to Laurence Gény.

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Gagné, S., Cluzet, S., Mérillon, JM. et al. ABA Initiates Anthocyanin Production in Grape Cell Cultures. J Plant Growth Regul 30, 1–10 (2011). https://doi.org/10.1007/s00344-010-9165-9

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  • DOI: https://doi.org/10.1007/s00344-010-9165-9

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