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ANTHOCYANIN1 from Solanum chilense is more efficient in accumulating anthocyanin metabolites than its Solanum lycopersicum counterpart in association with the ANTHOCYANIN FRUIT phenotype of tomato

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Abstract

Anthocyanins are flavonoid metabolites contributing attractive colors and antioxidant qualities to the human diet. Accordingly, there is a growing interest in developing crops enriched with these compounds. Fruits of the cultivated tomato, Solanum (S.) lycopersicum, do not normally produce high levels of anthocyanins. However, several wild tomato species yield anthocyanin-pigmented fruits, and this trait has been introgressed into the cultivated tomato. Two genes encoding homologous R2R3 MYB transcription factors, termed ANT1 and AN2, were previously genetically implicated in anthocyanin accumulation in tomato fruit peels of the ANTHOCYANIN FRUIT (AFT) genotype originating from S. chilense. Here we compared transgenic tomato plants constitutively over-expressing the S. lycopersicum (35S::ANT1 L ) or the S. chilense (35S::ANT1 C) allele, and show that each displayed variable levels of purple pigmentation in vegetative as well as reproductive tissues. However, 35S::ANT1 C was significantly more efficient in producing anthocyanin pigments, attributed to its gene coding-sequence rather than to its transcript levels. These results expand the potential of enhancing anthocyanin levels through engineering coding-sequence polymorphisms in addition to the transcriptional alterations commonly used. In addition, a segregating population obtained from a recombinant genotype revealed that the native ANT1, and not AN2, is fully associated with the AFT phenotype and that ANT1 alone can generate the characteristic phenotype of anthocyanin accumulation in AFT fruits. Our results therefore provide further support to the hypothesis that ANT1 is the gene responsible for anthocyanin accumulation in fruits of the AFT genotype.

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References

  • Adato A, Mandel T, Mintz-Oron S, Venger I, Levy D, Yativ M, Domínguez E, Wang Z, De Vos RC, Jetter R, Schreiber L, Heredia A, Rogachev I, Aharoni A (2009) Fruit-surface flavonoid accumulation in tomato is controlled by a SlMYB12-regulated transcriptional network. PLoS Genet 5:e1000777

    Article  PubMed  Google Scholar 

  • Ballester AR, Molthoff J, de Vos R, Hekkert BL, Orzaez D, Fernández-Moreno JP, Tripodi P, Grandillo S, Martin C, Heldens J, Ykema M, Granell A, Bovy A (2010) Biochemical and molecular analysis of pink tomatoes: deregulated expression of the gene encoding transcription factor SlMYB12 leads to pink tomato fruit color. Plant Physiol 152:71–84

    Article  PubMed  CAS  Google Scholar 

  • Boches P (2009) Breeding tomato for increased fruit phenolics. Ph.D. thesis submitted to the senate of Oregon State University

  • Bohm BA (1998) Chemistry and biochemistry of organic natural products. In: Introduction to Flavonoids. Harwood Academic Publishers, Amsterdam

    Google Scholar 

  • Borovsky Y, Oren-Shamir M, Ovadia R, De Jong W, Paran I (2004) The A locus that controls anthocyanin accumulation in pepper encodes a MYB transcription factor homologous to Anthocyanin2 of Petunia. Theor Appl Genet 109:23–29

    Article  PubMed  CAS  Google Scholar 

  • Bovy AG, Gomez-Roldan V, Hall RD (2010) Strategies to optimize the flavonoid content of tomato fruit. In: Santos-Buelga C, Escribano-Bailon MT, Lattanzio V (eds) Recent Advances in Polyphenols Research, Vol II. Wiley, Oxford, pp 138–162

    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  PubMed  CAS  Google Scholar 

  • Butelli E, Titta L, Giorgio M, Mock HP, Matros A, Peterek S, Schijlen EG, Hall RD, Bovy AG, Luo J, 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 

  • Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Rep 13:207–209

    Article  CAS  Google Scholar 

  • Giorgiev C (1972) Anthocyanin fruit tomato. Rep Tomato Genet Coop 22:10

    Google Scholar 

  • Goldsbrough AP, Tong Y, Yoder JI (1996) Lc as a non-destructive visual reporter and transposition excision marker gene for tomato. Plant J 9:927–933

    Article  CAS  Google Scholar 

  • Harborne JB (1994) The flavonoids: advances in research since 1986. Chapman and Hall, London

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jones CM, Mes P, Myers JR (2003) Characterization and inheritance of the Anthocyanin fruit (Aft) tomato. J Hered 94:449–456

    Article  PubMed  CAS  Google Scholar 

  • Kramer CY (1956) Extension of multiple range tests to group means with unequal number of replications. Biometrics 12:309–310

    Article  Google Scholar 

  • Levin I (2009) Regulating phytonutrient levels in plants—toward modification of plant metabolism for human health. In: Kaufman PB, Kirakosyan A (eds) Recent Advances in Plant Biotechnology. Springer, Dordrecht, pp 289–330

    Chapter  Google Scholar 

  • Luo J, Butelli E, Hill L, Parr A, Niggeweg R, Bailey P, Weisshaar B, Martin C (2008) AtMYB12 regulates caffeoyl quinic acid and flavonol synthesis in tomato: expression in fruit results in very high levels of both types of polyphenol. Plant J 56:316–326

    Article  PubMed  CAS  Google Scholar 

  • Mahjoub A, Hernould M, Joubès J, Decendit A, Mars M, Barrieu F, Hamdi S, Delrot S (2009) Overexpression of a grapevine R2R3-MYB factor in tomato affects vegetative development, flower morphology and flavonoid and terpenoid metabolism. Plant Physiol Biochem 47:551–561

    Article  PubMed  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 

  • 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  PubMed  CAS  Google Scholar 

  • McCormick S (1991) Transformation of tomato with Agrobacterium tumefaciens. In: Lindsey K (ed) Plant tissue culture manual: fundamentals and applications. Kluwer, Dordecht, pp 1–9

    Google Scholar 

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

    Google Scholar 

  • Rick CM, Cisneros P, Chetelat RT, DeVerna JW (1994) Abg—a gene on chromosome 10 for purple fruit derived from S. lycopersicoides. Rep Tomato Genet Coop 44:29–30

    Google Scholar 

  • Sapir M, Oren-Shamir M, Ovadia R, Reuveni M, Evenor D, Tadmor Y, Nahon S, Shlomo H, Chen L, Meir A, Levin I (2008) Molecular aspects of Anthocyanin fruit tomato in relation to high pigment-1. J Hered 99:292–303

    Article  PubMed  CAS  Google Scholar 

  • Schijlen EG, Ric de Vos CH, van Tunen AJ, Bovy AG (2004) Modification of flavonoid biosynthesis in crop plants. Phytochemistry 65:2631–2648

    Article  PubMed  CAS  Google Scholar 

  • Schijlen E (2007) Genetic engineering of flavonoid biosynthesis in tomato. Ph.D. thesis submitted to the senate of wageningen UR, The Netherlands

  • van Tuinen A, de Vos CHR, Hall RD, Linus HW, van der Plas LHW, Bowler C, Bino RJ (2006) Use of metabolomics for identification of tomato genotypes with enhanced nutritional value derived from natural light-hypersensitive mutants. In: Jaiwal PK (ed) Plant genetic engineering, vol 7: metabolic engineering and molecular farming-1. Studium Press, LLC. Huston, pp 240–256

  • 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 

  • Zuluaga DL, Gonzali S, Loreti E, Pucciariello C, Degl’Innocenti E, 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

Financial support was provided by the chief scientist of the Israeli ministry of agriculture and rural development. Contribution 125/2010 from the ARO, Volcani Center, Bet Dagan, Israel.

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Authors and Affiliations

  1. Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, P.O. Box 6, Bet Dagan, 50250, Israel

    Gali Schreiber, Moshe Reuveni, Dalia Evenor, Michal Oren-Shamir, Rinat Ovadia, Maya Sapir-Mir, Amir Bootbool-Man, Sahadia Nahon, Haviva Shlomo, Lea Chen & Ilan Levin

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  1. Gali Schreiber
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  2. Moshe Reuveni
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  3. Dalia Evenor
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  4. Michal Oren-Shamir
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  5. Rinat Ovadia
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  6. Maya Sapir-Mir
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  7. Amir Bootbool-Man
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  8. Sahadia Nahon
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  9. Haviva Shlomo
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  10. Lea Chen
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  11. Ilan Levin
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Correspondence to Ilan Levin.

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Communicated by G. Bryan.

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Schreiber, G., Reuveni, M., Evenor, D. et al. ANTHOCYANIN1 from Solanum chilense is more efficient in accumulating anthocyanin metabolites than its Solanum lycopersicum counterpart in association with the ANTHOCYANIN FRUIT phenotype of tomato. Theor Appl Genet 124, 295–307 (2012). https://doi.org/10.1007/s00122-011-1705-6

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