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Increased accumulation and decreased catabolism of anthocyanins in red grape cell suspension culture following magnesium treatment

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Abstract

Anthocyanins are the largest and best studied group of plant pigments. However, not very much is known about the fate of these phenolic pigments after they have accumulated in the cell vacuoles of plant tissues. We have previously shown that magnesium treatment of ornamentals during the synthesis of anthocyanins in the flowers or foliage caused an increase in the pigment concentration. In this study, we characterized the effect of magnesium on the accumulation of anthocyanin in red cell suspension originating from Vitis vinifera cv. Gamay Red grapes. Magnesium treatment of the cells caused a 2.5- to 4.5-fold increase in anthocyanin concentration, with no substantial induction of the biosynthetic genes. This treatment inhibited the degradation of anthocyanins occurring in the cells, and changed the ratio between different anthocyanins determining cell color, with an increase in the relative concentration of the less stable pigment molecules. The process by which magnesium treatment affects anthocyanin accumulation is still not clear. However, the results presented suggest at least part of its effect on anthocyanin accumulation stems from inhibition of the pigments’ catabolism. When anthocyanin biosynthesis was inhibited, magnesium treatments prevented the constant degradation of anthocyanins in the cell suspension. Future understanding of the catabolic processes undergone by anthocyanins in plants may enable more efficient inhibition of this process and increased accumulation of these pigments, and possibly of additional phenolic compounds.

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Abbreviations

MS:

Murashige and Skoog

NAA:

Naphthaleneacetic acid

PAL:

Phenylalanine ammonia-lyase

CHS:

Chalcone synthase

DFR:

Dihydroflavonol 4-reductase

F3′H:

Flavonoid 3′-hydroxylase

F3′5′H:

Flavonoid 3′5′-hydroxylase

ANS:

Anthocyanidin synthase

DMSO:

Dimethyl sulfoxide

LC–MS:

Liquid chromatography–mass spectrometry

ULPC:

Ultra performance liquid chromatography

QTOF:

Quadrupole time of flight

References

  • Bailly C, Cormier F, Do CB (1997) Characterization and activities of S-adenosyl-l-methionine:cyanidin 3-glucoside 3′-O-methyltransferase in relation to anthocyanin accumulation in Vitis vinifera cell suspension cultures. Plant Sci 122:81–89

    Article  CAS  Google Scholar 

  • Bar-Akiva A, Ovadia R, Rogachev I, Bar-Or C, Bar E, Freiman Z, Nissim-Levi A, Gollop N, Lewinsohn E, Aharoni A, Weiss D, Koltai H, Oren-Shamir M (2010) Metabolic networking in Brunfelsia calycina petals after flower opening. J Exp Bot 61:1393–1403

    Article  PubMed  CAS  Google Scholar 

  • Ben Zvi MM, Florence NZ, Masci T, Ovadis M, Shklarman E, Ben-Meir H, Tzfira T, Dudareva N, Vainstein A (2008) Interlinking showy traits: co-engineering of scent and colour biosynthesis in flowers. Plant Biotechnol J 6:403–415

    Article  PubMed  CAS  Google Scholar 

  • Bradley JM, Rains SR, Manson JL, Davies KM (2000) Flower pattern stability in genetically modified lisianthus (Eustoma grandiflorum) under commercial growing conditions. N Z J Crop Hortic Sci 28:175–184

    Article  CAS  Google Scholar 

  • Brunner AM, Yakovlev IA, Strauss SH (2004) Validating internal controls for quantitative plant gene expression. BMC Plant Biol 4:14–20

    Google Scholar 

  • Butelli E, Titta L, Giorgio M, Mock HP, Matros A, Peterek S, Schijlen EGWM, Hall RD, Bovy AG, Jie L, Martin C (2008) Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat Biotechnol 26:1301–1308

    Article  PubMed  CAS  Google Scholar 

  • Castillo-Muñoz 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 57:7883–7891

    Google Scholar 

  • Curtin C, Zhang W, Franco C (2003) Manipulating anthocyanin composition in Vitis vinifera suspension cultures by elicitation with jasmonic acid and light irradiation. Biotechnol Lett 25:1131–1135

    Article  PubMed  CAS  Google Scholar 

  • Davies KM, Schwinn KE, Deroles SC, Manson DG, Lewis DH, Bloor SJ, Bradley JM (2003) Enhancing anthocyanin production by altering competition for substrate between flavonol synthase and dihydroflavonol 4-reductase. Euphytica 131:259–268

    Article  CAS  Google Scholar 

  • Decendit A, Merillon JM (1996) Condensed tannin and anthocyanin production in Vitis vinifera cell suspension cultures. Plant Cell Rep 15:762–765

    Article  CAS  Google Scholar 

  • Deroles S (2009) Anthocyanin biosynthesis in plant cell cultures: a potential source of natural colourants. In: Gould K, Davies K, Winefield C (eds) Anthocyanins: biosynthesis, functions, and applications. Springer, New York, pp 118–126

    Google Scholar 

  • Do CB, Cormier F (1990) Accumulation of anthocyanins enhanced by a high osmotic potential in grape (Vitis vinifera L.) cell suspensions. Plant Cell Rep 9:143–146

    Article  CAS  Google Scholar 

  • Do CB, Cormier F (1991a) Accumulation of peonidin 3-glucoside enhanced by osmotic stress in grape (Vitis vinifera L.) cell suspension. Cell Tissue Organ Cult 24:49–54

    Article  CAS  Google Scholar 

  • Do CB, Cormier F (1991b) Effects of low nitrate and high sugar concentrations on anthocyanin content and composition of grape (Vitis vinifera L.) cell suspension. Plant Cell Rep 9:500–504

    CAS  Google Scholar 

  • Flamini R (2003) Mass spectrometry in grape and wine chemistry. Part I: Polyphenols. Mass Spectrom Rev 22:218–250

    Google Scholar 

  • Flores FB, Oosterhaven J, Martinez-Madrid MC, Romojaro F (2005) Possible regulatory role of phenylalanine ammonia-lyase in the production of anthocyanins in asparagus (Asparagus officinalis L.). J Sci Food Agric 85:925–930

    Article  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 

  • Grotewold E (2006) The genetics and biochemistry of floral pigments. Annu Rev Plant Biol 57:761–780

    Article  PubMed  CAS  Google Scholar 

  • Huysamer M (1998) Report of the blushed pear workgroup: perceptions, facts and questions. Proceedings of Cape Pomological Association Technical Symposium, Cape Town, South Africa, 2–3 June, pp 187–192

  • 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

    Article  CAS  Google Scholar 

  • Jonsson LMV, Donker Koopman WE, Schram AW (1984) Turnover of anthocyanins and tissue compartmentation of anthocyanin biosynthesis in flowers of Petunia hybrida. J Plant Physiol 115:29–37

    CAS  Google Scholar 

  • Kondo T, Yoshida K, Nakagawa A, Kawai T, Tamura H, Goto T (1992) Structural basis of blue-colour development in flower petals from Commelina communis. Nature 358:515–518

    Article  CAS  Google Scholar 

  • Markham KR, Ofman DJ (1993) Lisianthus flavonoid pigments and factors influencing their expression in flower colour. Phytochemistry 34:679–685

    Article  PubMed  CAS  Google Scholar 

  • Mazza G, Miniati E (1993) Color stabilization and intensification. In: Mazza G, Miniati E (eds) Anthocyanins in fruits vegetables and grains. CRC Press, Boca Raton, pp 1–20

    Google Scholar 

  • Mori K, Goto-Yamamoto N, Kitayama M, Hashizume K (2007) Loss of anthocyanins in red-wine grape under high temperature. J Exp Bot 58:1935–1945

    Article  PubMed  CAS  Google Scholar 

  • Nissim-Levi A, Ovadia R, Foreer I, Oren-Shamir M (2007) Increased anthocyanin accumulation in ornamental plants due to magnesium treatment. J Hortic Sci Biotechnol 82:481–487

    CAS  Google Scholar 

  • Oosterhaven K, Poolman B, Smid EJ (1995) S-Carvone as a natural potato sprout inhibiting, fungistatic and bacteristatic compound. Ind Crops Prod 4:23–31

    Article  CAS  Google Scholar 

  • Oren-Shamir M (2009) Does anthocyanin degradation play a significant role in determining pigment concentration in plants? Plant Sci 177:310–316

    Article  CAS  Google Scholar 

  • Quattrocchio F, Wing JF, van der Woude K, Mol JNM, Koes R (1998) Analysis of bHLH and MYB domain proteins: species-specific regulatory differences are caused by divergent evolution of target anthocyanin genes. Plant J 13:475–488

    Article  PubMed  CAS  Google Scholar 

  • Shaked-Sachray L, Weiss D, Reuveni M, Nissim-Levi A, Oren-Shamir M (2002) Increased anthocyanin accumulation in aster flowers at elevated temperatures due to magnesium treatment. Physiol Plant 114:559–565

    Article  PubMed  CAS  Google Scholar 

  • Steyn WJ, Holcroft DM, Wand SJE, Jacobs G (2004) Anthocyanin degradation in detached pome fruit with reference to preharvest red color loss and pigmentation patterns of blushed and fully red pears. J Am Soc Hortic Sci 129:13–19

    CAS  Google Scholar 

  • Takeda K, Yanagisawa M, Kifune T, Kinoshita T, Timberlake CF (1994) A blue pigment complex in flowers of Salvia patens. Phytochemistry 29:1089–1091

    Article  Google Scholar 

  • Tanaka Y, Ohmiya A (2008) Seeing is believing: engineering anthocyanin and carotenoid biosynthetic pathways. Curr Opin Biotechnol 19:190–197

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J 54:733–749

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Brugliera F, Chandler S (2009) Recent progress of flower colour modification by biotechnology. Int J Mol Sci 10:5350–5369

    Article  PubMed  CAS  Google Scholar 

  • Vaknin H, Bar-Akiva A, Ovadia R, Nissim-Levi A, Forer I, Weiss D, Oren-Shamir M (2005) Active anthocyanin degradation in Brunfelsia calycina (yesterday-today-tomorrow) flowers. Planta 222:19–26

    Article  PubMed  CAS  Google Scholar 

  • van Tunen AJ, Mol JNM (1991) Control of flavonoids synthesis and manipulation of flower color. Plant Biotechnol 2:94–125

    Google Scholar 

  • Wang H, Race EJ, Shrikhande AJ (2003) Characterization of anthocyanins in grape juices by ion trap liquid chromatography-mass spectrometry. J Agric Food Chem 51:1839–1844

    Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

    Article  PubMed  CAS  Google Scholar 

  • Yoshida K, Mori M, Kondo T (2009) Blue flower color development by anthocyanins: from chemical structure to cell physiology. Nat Prod Rep 26:884–915

    Article  PubMed  CAS  Google Scholar 

  • Zenner K, Bopp M (1987) Anthocyanin turnover in Sinapis-alba L. J Plant Physiol 126:475–482

    CAS  Google Scholar 

  • Zhang W, Curtin C, Kikuchi M, Franco C (2002) Integration of jasmonic acid and light irradiation for enhancement of anthocyanin biosynthesis in Vitis vinifera suspension cultures. Plant Sci 162:459–468

    Article  Google Scholar 

  • Zhang W, Franco C, Curtin C, Conn S (2004) To stretch the boundary of secondary metabolite production in plant cell-based bioprocessing: anthocyanin as a case study. J Biomed Biotechnol 264–271

  • Zhang ZQ, Pang XQ, Duan XW, Ji ZL, Jiang YM (2005) Role of peroxidase in anthocyanin degradation in litchi fruit pericarp. Food Chem 90:47–52

    Article  Google Scholar 

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Correspondence to Michal Oren-Shamir.

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Sinilal, B., Ovadia, R., Nissim-Levi, A. et al. Increased accumulation and decreased catabolism of anthocyanins in red grape cell suspension culture following magnesium treatment. Planta 234, 61–71 (2011). https://doi.org/10.1007/s00425-011-1377-0

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  • DOI: https://doi.org/10.1007/s00425-011-1377-0

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