Skip to main content
SpringerLink
Log in

Biochemical and genetic evidences of anthocyanin biosynthesis and accumulation in a selected tomato mutant

Rendiconti Lincei volume 26, pages 293–306 (2015)Cite this article

Abstract

Anthocyanins add significant nutritional value to the plant-derived foods that contain them because of their health-promoting effects. In tomato (Solanum lycopersicum L.), anthocyanins are normally synthesized only in vegetative tissues. Atroviolacium (atv) is a mutant characterized by intense anthocyanin pigmentation in the vegetative tissues. In this study, we investigated the anthocyanin biosynthetic pathway in this mutant and in its genetic background (Ailsa Craig, AC) in order to reveal the molecular regulation of anthocyanin biosynthesis in this line, and to find out where the anthocyanin biosynthesis is intensified. To our knowledge, this is the first report showing the sucrose-induced accumulation of anthocyanins in vegetative tissues of tomato, and demonstrating the molecular regulation of anthocyanin biosynthesis in atv mutant.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Abbreviations

F3′H:

Flavonoid 3′-hydroxylase

F3′5′H:

Flavonoid 3′5′-hydroxylase

DFR:

Dihydroflavonol 4-reductase

FLS:

Flavonols synthase

ANS:

Anthocyanidin synthase

3-GT:

Flavonoid 3-O-glucosyltransferase

5-GT:

Flavonoid 5-O-glucosyltransferase

RT:

Flavonoid 3-O-glucoside-rhamnosyltransferase

AAC:

Anthocyanin acyltransferase

GST:

Glutathione S-transferase

PAT:

Putative anthocyanin transporter

NAR:

Naringenin

DHK:

Dihydrokaempferol

References

  • Al Sane KO, Povero G, Perata P (2011) Anthocyanin tomato mutants: overview and characterization of an anthocyanin less somaclonal mutant. Plant Biosys 145:1–9

    Article  Google Scholar 

  • Andersen Q (2008) Recent advances in the field of anthocyanins-main focus on structures. In: Daayf F and Lattanzio V (eds). Recent Adv Polyphenol Res 1: 167-201

  • Andersen Q, Jordheim M (2006) The anthocyanins. In: Markham K (ed) Andersen Q., The flavonoids: chemistry, biochemistry, and applicationsTaylor & Francis Group, CRC Press, Boca Raton pp, pp 471–551

    Google Scholar 

  • Baier M, Hemmann G, Holman R, Corke F, Card R, Smith C, Rook F, Bevan M (2004) Characterization of mutants in Arabidopsis showing increased sugar specific gene expression, growth, and developmental responses. Plant Physiol 134:81–91

    Article  CAS  Google Scholar 

  • Bovy A, de Vos R, Kemper M, Schijlen E, Almenar Pertejo M, Muir S, Collins G, Robinson S, Verhoeyen M, Hughes S, Santos-Buelga C, van Tunen A (2002) High flavonol tomatoes resulting from the heterologous expression of the maize transcription factor genes LC and C1. Plant Cell 14:2509–2526

    Article  CAS  Google Scholar 

  • Bovy A, Schijlen E, Hall RD (2007) Metabolic engineering of flavonoids in tomato (Solanum lycopersicum L.); the potential for metabolomics. Metabolomics 3:399–412

    Article  CAS  Google Scholar 

  • Couée I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459

    Article  Google Scholar 

  • Davies K, Schwinn K, Deroles S, Manson D, Lewis D, Bloor S, Bradley J (2003) Enhancing anthocyanin production by altering competition for substrate between flavonol synthase and dihydroflavonol 4-reductase. Euphytica 131:259–268

    Article  CAS  Google Scholar 

  • Davies K, Zhang H, Schwinn K (2008) Recent advances in the molecular biology and metabolic engineering of flavonoid biosynthesis in ornamental plants. In: Daayf F, Lattanzio V (eds). Recent Adv Polyphenol Res 1: 139–166

  • De Jong WS, Eannetta NT, De Jong DM, Bodis M (2004) Candidate gene analysis of anthocyanin pigmentation loci in the Solanaceae. Theor Appl Genetics 108:423–432

    Article  Google Scholar 

  • Gibson S (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8:93–102

    Article  CAS  Google Scholar 

  • Giovanni P, Gonzali S, Bassolino L, Mazzucato A, Perata P (2011) Transcriptional analysis in high-anthocyanin tomatoes reveals synergistic effect of Aft and atv genes. J Plant Physiol 168:270–279

    Article  Google Scholar 

  • Gollop R, Farhi S, Peri A (2001) Regulation of the leucoanthocyanidin dioxygenase gene expression in Vitis vinifera. Plant Sci 161:579–588

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gonzali S, Mazzucato A, Perata P (2009) Purple as a tomato: towards high anthocyanin tomatoes. Trends Plant Sci 5:237–241

    Article  Google Scholar 

  • Gould K, Davies K, Winefield C (eds) (2009) Anthocyanins: biosynthesis, functions, and applications. Springer Science and Business Media, LLC, New York

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Grotewold E (ed) (2006b) The science of flavonoids. Springer Science and Business Media Inc, New York

    Google Scholar 

  • Hinderer W, Petersen M, Seitz H (1984) Inhibition of flavonoid biosynthesis by gibberellic acid in cell suspension cultures of Daucus carota L. Planta 160:544–549

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hughes N, Neufeld H, Burkey K (2005) Functional role of anthocyanins in high-light winter leaves of the evergreen herb Galax urceolata. New Phytol 168(3):575–587

    Article  CAS  Google Scholar 

  • Ilan A, Dougall DK (1994) Effects of gibberellic acid and uniconazole on the activities of some enzymes of anthocyanin biosynthesis in carrot cell cultures. J Plant Growth Reg 13:213–220

    Article  CAS  Google Scholar 

  • Ilan A, Zanewich KP, Rood SB, Dougall DK (1994) Gibberellic acid decreases anthocyanin accumulation in wild carrot cell suspension cultures but does not alter 3′-nucleotidase activity. Physiol Plant 92:47–52

    Article  CAS  Google Scholar 

  • Lattanzio V, Kroon Paul A, Quideau S, Treutter D (2008) Plant Phenolics: Secondary Metabolites with Diverse Functions. In: Daayf F, Lattanzio V (eds). Recent Adv Polyphenol Res 1: 1–35

  • Lewis M, Liu HW (2010) Comprehensive natural products II: chemistry and biology: 10 Volume Set vol 1. Secondary metabolites: organization and biosynthesis. Newnes Pub 7388

  • Lila MA (2004) Anthocyanins and human health: an in vitro investigative approach. J Biomed Biotechnol 5:306–313

    Article  Google Scholar 

  • Liu CJ, Blount JW, Steele CL, Dixon RA (2002) Bottlenecks for metabolic engineering of isoflavone glycoconjugates in Arabidopsis. Proc Nat Acad Sci USA 99:14578–14583

    Article  CAS  Google Scholar 

  • Loreti E, Povero G, Novi G, Solfanelli C, Alpi A, Perata P (2008) Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytol 179:1004 1016

    Google Scholar 

  • Mathews H, Clendennen SK, Caldwell CG, Liu XL, Connors K, Matheis N, Schuster DK, Menasco DJ, Wagoner W, Lightner J, Wagner DR (2003) Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport. Plant Cell 15:1689–1703

    Article  CAS  Google Scholar 

  • Mazza G and Kay C (2008) Bioactivity, absorption, and metabolism of anthocyanins. In: Daayf F, Lattanzio V (eds). Recent Adv Polyphenol Res 1: 228–262

  • Mes PJ, Boches P, Myers JR (2008) Characterization of tomatoes expressing anthocyanin in the fruit. J Am Soc Hort Sci 133(2):262–269

    Google Scholar 

  • Motohashi N, Sakagami H (2009) Anthocyanins as functional food colors. In: Motohashi N (ed) Bioactive heterocycles VII; flavonoids and anthocyanins in plants, and latest bioactive heterocycles II. Springer, Berlin Heidelberg, pp 1–41

    Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Perata P, Matsukura C, Vernieri P, Yamaguchi J (1997) Sugar repression of a gibberellin-dependent signaling pathway in barley embryos. Plant Cell 9:2197–2208

    Article  CAS  Google Scholar 

  • Pietta P (2000) Flavonoids as antioxidants. J Nat Prod 63:1035–1042

    Article  CAS  Google Scholar 

  • Rademacher W (2000) Growth retardants: effects on gibberellin biosynthesis and other metabolic pathways. Ann Rev Plant Physiol Plant Mol Biol 51:501–531

    Article  CAS  Google Scholar 

  • Roemmelt S, Zimmermann N, Rademacher W, Treutter D (2003) Formation of novel flavonoids in apple (Malusxdomestica) treated with the 2-oxoglutarate-dependent dioxygenase inhibitor prohexadione-Ca. Phytochemistry 64:709–716

    Article  CAS  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Ann Rev Plant Biol 57:675–709

    Article  CAS  Google Scholar 

  • Ronchi A, Farina G, Gozzo F, Tonelli C (1997) Effects of a triazolic fungicide on maize plant metabolism: modifications of transcript abundance in resistance related pathways. Plant Sci 130:51–62

    Article  CAS  Google Scholar 

  • Schijlen E, Ric de Vos C, van Tunen A, Bovy A (2004) Modification of flavonoid biosynthesis in crop plants. Phytochemistry 65:2631–2648

    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  Google Scholar 

  • Springob K, Nakajima JI, Yamazaki M, Saito K (2003) Recent advances in the biosynthesis and accumulation of anthocyanins. Natural Product Reports 20:288–303

    Article  CAS  Google Scholar 

  • Stafford H (1991) Flavonoid evolution: an enzymic approach. Plant Physiol 96:680–685

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tanaka Y, Katsumoto Y, Brugliera F, Mason J (2005) Genetic engineering in floriculture. Plant Cell, Tissue Organ Cult 80:1–24

    Article  CAS  Google Scholar 

  • Taylor LP, Grotewold E (2005) Flavonoids as developmental regulators. Curr Opin Plant Biol 8:317–323

    Article  CAS  Google Scholar 

  • Torres C, Davies N, Yanez J, Andrews P (2005) disposition of selected flavonoids in fruit tissues of various tomato (Solanum lycopersicum L.) genotypes. J Agric Food Chem 53:9536–9543

    Article  CAS  Google Scholar 

  • Tsuda S, Fukui Y, Nakamura N, Katsumoto Y, Sakakibara KY, Fukuchi-Mizutani M, Ohira K, Ueyama Y, Ohkawa H, Holton TA, Takaaki Kusumi T, Tanaka Y (2004) Flower color modification of Petunia hybrida commercial varieties by metabolic engineering. Plant Biotechnol 21:377–386

    Article  CAS  Google Scholar 

  • Verhoeyen M, Bovy A, Collins G, Muir S, Robinson S, de Vos C, Colliver S (2002) Increasing antioxidant levels in tomatoes through modification of the flavonoid biosynthetic pathway. J Exp Bot 53:2099–2106

    Article  CAS  Google Scholar 

  • Willits MG, Kramer CM, Prata RT, De Luca V, Potter BG, Steffens JC, Graser G (2005) Utilization of the genetic resources of wild species to create a nontransgenic high flavonoid tomato. J Agric Food Chem 53:1231–1236

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Zuluaga D, Gonzali S, Loreti E, Pucciariello C, Degl’Innocenti C, Guidi L, Alpi A, Perata P (2008) Arabidopsis thaliana MYB75/PAP1 transcription factor induces anthocyanin production in transgenic tomato plants. Funct Plant Biol 35:606–618

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Authors would like to thank Prof. Pierdomenico Perata and Giovanni povero (Scuola Superiore Sant’ Anna, Italy) for their valuable assistance, support and guidance throughout this research work. Thanks, also, to Prof. Gian Piero Soressi (Department of Agrobiology and Agrochemistry, University of Tuscia, Viterbo, Italy) for providing us with the seeds of atroviolacium (atv) and its genetic background (Ailsa Craig). This research was supported by the Italian Ministry of University and Research (MiUR), PRIN2006, TomANTHO Project.

Author information

Authors and Affiliations

  1. Department of Biology, College of Science, King Khalid University, Abha, Saudi Arabia

    Khaldoun O. Al Sane & Abd El-Latif Hesham

  2. Department of Genetics, Faculty of Agriculture, Assiut University, Assiut, Egypt

    Abd El-Latif Hesham

Authors
  1. Khaldoun O. Al Sane
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Abd El-Latif Hesham
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Khaldoun O. Al Sane.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Al Sane, K.O., Hesham, A.EL. Biochemical and genetic evidences of anthocyanin biosynthesis and accumulation in a selected tomato mutant. Rend. Fis. Acc. Lincei 26, 293–306 (2015). https://doi.org/10.1007/s12210-015-0446-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12210-015-0446-x

Keywords

search

Navigation