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Expression and mapping of anthocyanin biosynthesis genes in carrot

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Abstract

Anthocyanin gene expression has been extensively studied in leaves, fruits and flowers of numerous plants. Little, however, is known about anthocyanin accumulation in roots of carrots or other species. We quantified expression of six anthocyanin biosynthetic genes [phenylalanine ammonia-lyase (PAL3), chalcone synthase (CHS1), flavanone 3-hydroxylase (F3H), dihydroflavonol 4-reductase (DFR1), leucoanthocyanidin dioxygenase (LDOX2), and UDP-glucose:flavonoid 3-O-glucosyltransferase (UFGT)] in three carrot inbreds with contrasting root color: solid purple (phloem and xylem); purple outer phloem/orange xylem; and orange phloem and xylem. Transcripts for five of these genes (CHS1, DFR1, F3H, LDOX2, PAL3) accumulated at high levels in solid purple carrots, less in purple-orange carrot, and low or no transcript in orange carrots. Gene expression coincided with anthocyanin accumulation. In contrast, UFGT expression was comparable in purple and orange carrots and relatively unchanged during root development. In addition, five anthocyanin biosynthesis genes [FLS1 (flavonol synthase), F3H, LDOX2, PAL3, and UFGT] and three anthocyanin transcription factors (DcEFR1, DcMYB3 and DcMYB5) were mapped in a population segregating for the P 1 locus that conditions purple root color. P 1 mapped to chromosome 3 and of the eight anthocyanin biosynthesis genes, only F3H and FLS1 were linked to P 1. The gene expression and mapping data suggest a coordinated regulatory control of anthocyanin expression in carrot root and establish a framework for studying the anthocyanin pathway in carrots, and they also suggest that none of the genes evaluated is a candidate for P 1.

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References

  • Alessandro MS, Galmarini CR, Iorizzo M, Simon PW (2013) Molecular mapping of vernalization requirement and fertility restoration genes in carrot. Theor Appl Genet 126:415–423

    Article  PubMed  Google Scholar 

  • Boiteux LS, Fonseca MEN, Simon PW (1999) Effects of plant tissue and DNA purification methods on randomly amplified polymorphic DNA-based genetic fingerprinting analysis in carrot. J Am Soc Hort Sci 124:32–38

    CAS  Google Scholar 

  • Buishand JG, Gabelman WH (1979) Investigations on the inheritance of color and carotenoid content in phloem and xylem of carrot roots (Daucus carota L.). Euphytica 28:611–632

    Article  CAS  Google Scholar 

  • Cavagnaro PF, Chung SM, Manin S, Yildiz M, Ali A, Alessandro MS, Iorizzo M, Senalik D, Simon PW (2011) Microsatellite isolation and marker development in carrot—genomic distribution, linkage mapping, genetic diversity analysis and marker transferability across Apiaceae. BMC Genomics 12:386

    Article  PubMed  CAS  Google Scholar 

  • Chalker-Scott L (1999) Elevated ultraviolet-B radiation induces cross protection to cold in leaves of rhododendron under field conditions. Photochem Photobiol 79:199–204

    Google Scholar 

  • Deng C, Davis TM (2001) Molecular identification of the yellow fruit color (c) locus in diploid strawberry: a candidate gene approach. Theor Appl Genet 103:316–322

    Article  CAS  Google Scholar 

  • Dixon RA, Palva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097

    PubMed  CAS  Google Scholar 

  • Dooner HK, Robbins TP, Jorgensen RA (1991) Genetic and developmental control of anthocyanin biosynthesis. Annu Rev Genet 25:173–199

    Article  PubMed  CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Durbin ML, McCaig B, Clegg MT (2000) Molecular evolution of chalcone synthase multigene family in the morning glory genome. Plant Mol Biol 42:79–92

    Article  PubMed  CAS  Google Scholar 

  • Forkmann G, de Vlaming P, Spribille R, Wiering H, Schramm AW (1986) Genetic and biochemical studies on the conversion of dihydroflavonols to flavonols in flowers of Petunia hybrida. Zeitschrift für Naturforschung 41c:179–186

    Google Scholar 

  • Harborne JB (1976) A unique pattern of anthocyanins in Daucus carota and other Umbelliferae. Biochem Syst Ecol 4:31–35

    Article  CAS  Google Scholar 

  • Hirner AA, Veit S, Seitz HU (2001) Regulation of anthocyanin biosynthesis in UV-A-irradiated cell cultures of carrot and in organs of intact carrot plants. Plant Sci 161:315–322

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Holton TA, Tanaka Y (1994) Blue roses a pigment of our imagination. Trends Biotechnol 12:40–42

    Article  Google Scholar 

  • Holton TA, Brugliera F, Tanaka Y (1993) Cloning and expression of flavonol synthase from Petunia hybrid. Plant J 4(6):1003–1010

    Article  PubMed  CAS  Google Scholar 

  • Iorizzo M, Senalik DA, Grzebelus D, Bowman M, Cavagnaro PF, Matvienko M, Ashrafi H, Van Deynze A, Simon PW (2011) De novo assembly and characterization of the carrot transcriptome reveals novel genes, new markers, and genetic diversity. BMC Genomics 12:389

    Article  PubMed  CAS  Google Scholar 

  • Iovene M, Cavagnaro PF, Senalik D, Buell CR, Jiang J, Simon P (2011) Comparative FISH mapping of Daucus species (Apiaceae family). Chromosome Res 19:493–506

    Article  PubMed  CAS  Google Scholar 

  • Jaakola L, Määtta K, Pirttilä AM, Törrönen R, Kärenlampi S, Hohtola A (2002) Expression of genes involved in anthocyanin biosynthesis in relation to anthocyanin, proanthocyanidin, and flavonol levels during bilberry fruit development. Plant Physiol 130:729–739

    Article  PubMed  CAS  Google Scholar 

  • Jung CS, Griffith HM, De Jong DM, Cheng S, Bodis M, De Jong WS (2005) The potato P locus codes for flavonoid 3′5′-hydroxylase. Theor Appl Genet 110:269–275

    Article  PubMed  CAS  Google Scholar 

  • Just BJ, Santos CAF, Fonseca MEN, Boiteux LS, Oloizia BB, Simon PW (2007) Carotenoid biosynthesis structural genes in carrot (Daucus carota): isolation, sequence-characterization, single nucleotide polymorphism (SNP) markers and genome mapping. Theor Apple Genet 114:693–704

    Article  CAS  Google Scholar 

  • Kimura S, Chikagawa Y, Kato M, Maeda K, Ozeki Y (2008) Upregulation of the promoter activity of the carrot (Daucus carota) phenylalanine ammonia-lyase gene (DcPAL3) is caused by new members of the transcriptional regulatory proteins, DcEFR1 and DcEFR2, which bind to the GCC-box homolog and act as an activator to the DcPAL3 promoter. J Plant Res 121:499–508

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi S, Ishimaro 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 160:543–550

    Article  PubMed  CAS  Google Scholar 

  • Koes RE, Quattrocchio F, Mol JNM (1993) The flavonoid biosynthetic pathway in plants: function and evolution. Bioessays 16:123–132

    Article  Google Scholar 

  • Kondo S, Hiraoka K, Kobayashi S, Honda C, Terahara N (2002) Changes in the expression of anthocyanin biosynthetic genes during apple development. J Am Soc Hort Sci 127:971–976

    CAS  Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombinant values. Annu Eugen 12:172–175

    Article  Google Scholar 

  • Kurilich AC, Clevidence BA, Britz SJ, Simon PW, Novotny JA (2005) Plasma and urine responses are lower for acylated vs nonacylated anthocyanins from raw and cooked purple carrots. J Agric Food Chem 5:6537–6542

    Article  Google Scholar 

  • Lalusin AG, Ohta M, Fujimura T (2006) Temporal and spatial expression of genes involved in anthocyanin biosynthesis during sweet potato (Ipomoea batatas (L.) Lam.) root development. Int J Plant Sci 167(2):249–256

    Article  CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  PubMed  CAS  Google Scholar 

  • Li J, Ou-Lee TM, Raba R, Amundson RG, Last RL (1993) Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. Plant Cell 5:171–179

    PubMed  CAS  Google Scholar 

  • Lu QN, Yang Q (2006) cDNA cloning and expression of anthocyanin biosynthetic genes in wild potato (Solanum pinnatisectum). Afr J Biotechnol 5(10):811–818

    CAS  Google Scholar 

  • Mano H, Ogasawara F, Sato K, Higo H, Minobe Y (2007) Isolation of a regulatory gene of anthocyanin biosynthesis in tuberous roots of purple-fleshed sweet potato. Plant Physiol 143:1252–1268

    Article  PubMed  CAS  Google Scholar 

  • McClure JW (1975) Physiology and function of flavonoids. In: Harborne JB, Mabry TJ (eds) The flavonoids. Academic Press, New York, pp 970–1055

    Google Scholar 

  • Mo Y, Nagel C, Taylor LP (1992) Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proc Natl Acad Sci USA 89:7213–7217

    Article  PubMed  CAS  Google Scholar 

  • Modolo LV, Blount JW, Achnine L, Naoumkina MA, Wang X, Dixon RA (2007) A functional genomics approach to (iso)flavonoid glycosylation in the model Legume Medicago truncatula. Plant Mol Biol 64:499–518

    Article  PubMed  CAS  Google Scholar 

  • Mol J, Jenkins GI, Schafer E, Weiss D (1996) Signal perception, transduction and gene expression involved in anthocyanin biosynthesis. Crit Rev Plant Sci 15:525–557

    CAS  Google Scholar 

  • Ozeki Y, Matui M, Sakuta M, Matsuoka M, Ohasi Y, Kano-Murakami Y, Yamamoto N, Tanaka Y (1990) Differential regulation of phenylalanine ammonia-lyase genes during anthocyanin synthesis and by transfer effect in carrot cell suspension cultures. Physiol Plant 80:379–387

    Article  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res 29:2002–2007

    Article  Google Scholar 

  • Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper—Excel-based tool using pair-wise correlations. Biotechnol Lett 26:509–515

    Article  PubMed  CAS  Google Scholar 

  • Quattrocchio F, Wing JF, Leppen HTC, Mol JNM, Koes RE (1993) Regulatory genes controlling anthocyanin pigmentation are functionally conserved among plant species and have distinct sets of target genes. Plant Cell 5:1497–1512

    PubMed  CAS  Google Scholar 

  • Rasmussen R (2001) Quantification on the LightCycler. In: Meuer S, Wittwer C, Nakagawara K (eds) Rapid cycle real-time PCR, methods and applications. Springer, Heidelberg, pp 21–34

    Chapter  Google Scholar 

  • Reddy AR (1996) Genetic and molecular analysis of the anthocyanin pigmentation pathway in rice. Rice Genetics, III. In: Proceedings of the Third International Rice Genetics Symposium, 16–20 Oct Manila (Philippines), pp 341–352

  • Ross JA, Kasum CM (2002) Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu Rev Nutr 22:19–34

    Article  PubMed  CAS  Google Scholar 

  • Rotenberg D, Thompson TS, German TL, Willis DK (2006) Methods for effective real-time RT-PCR analysis of virus-induced gene silencing. J Virol Methods 138:49–59

    Article  PubMed  CAS  Google Scholar 

  • Santos CAF, Simon PW (2002) QTL analyses reveal clustered loci for accumulation of major provitamin A carotenes and lycopene in carrot roots. Mol Genet Genomics 268:122–129

    Article  PubMed  CAS  Google Scholar 

  • Sharma M, Cortes-Cruz M, Ahern KR, McMullen M, Brutnell TP, Chopra S (2011) Identification of the Pr1 gene product completes the anthocyanin biosynthesis pathway of maize. Genetics 188:69–79

    Article  PubMed  CAS  Google Scholar 

  • Shirley BW (1996) Flavonoid biosynthesis: “new” functions for an “old” pathway. Trends Plant Sci 1:377–382

    Google Scholar 

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

    Article  Google Scholar 

  • Simon PW (1996) Inheritance and expression of purple and yellow storage root color in carrot. J Hered 87:63–66

    Article  Google Scholar 

  • Simon PW, Peterson CE, Gabelman WH (1990) B493 and B9304, carrot inbreds for use in breeding, genetics and tissue culture. HortScience 25:815

    Google Scholar 

  • Simon PW, Rubatzky V, Bassett MJ, Strandberg JO, White JM (1997) B7262 purple carrot inbred. HortScience 32:146–147

    Google Scholar 

  • Stommel JR, Lightbourn GJ, Winkel BS, Griesbach RJ (2009) Transcription factor families regulate the anthocyanin biosynthetic pathway in Capsicum annum. J Am Hort Sci 134:244–251

    Google Scholar 

  • Vivek BS, Simon PW (1999) Linkage relationship among molecular markers and storage root traits of carrot (Daucus carota L. ssp. sativus). Theor Appl Genet 99:58–64

    Article  CAS  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, Van De Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    Article  PubMed  CAS  Google Scholar 

  • Vuylsteke M, Mank R, Antosine R, Bastiaans E, Senior ML, Stuber CW, Melchinger AE, Lubbersted T, Xia XC, Stam P, Zabeau M, Kuiper M (1999) Two high-density AFLP linkage maps of Zea mays L.: analysis of distribution of AFLP markers. Theor Appl Genet 99:921–935

    Article  CAS  Google Scholar 

  • Wako T, Kimura S, Chikagawa Y, Ozeki Y (2010) Characterization of MYB proteins as transcriptional regulatory factors for carrot phenylalanine ammonia-lyase gene (DcPAL3). Plant Biotechnol 27:131–139

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This article includes parts of the doctoral thesis of the first author. The authors gratefully acknowledge support from the Initiative for Future Agriculture Food Systems Grant number 2000-4258 from the USDA Cooperative Research, Education, and Extension Service, the USDA, ARS; the University of Wisconsin-Madison; the California Fresh Carrot Advisory Board; and vegetable seed companies for their support of this research. The authors are also grateful for the proficient technical assistance of Drs. Megan Bowman and Douglas Senalik.

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Authors and Affiliations

  1. Department of Horticulture, University of Wisconsin-Madison, 1575 Linden Drive, Madison, WI, 53706, USA

    Mehtap Yildiz, Pablo F. Cavagnaro, Massimo Iorizzo & Philipp W. Simon

  2. Department of Agricultural Biotechnology, Faculty of Agriculture, Yuzuncu Yil University, 65080, Van, Turkey

    Mehtap Yildiz

  3. Department of Plant Pathology, University of Wisconsin-Madison, 1575 Linden Drive, Madison, WI, 53706, USA

    David K. Willis

  4. USDA-Agricultural Research Service, Vegetable Crops Unit, University of Wisconsin-Madison, 1575 Linden Drive, Madison, WI, 53706, USA

    David K. Willis & Philipp W. Simon

  5. Estación Experimental Agropecuaria La Consulta, Instituto Nacional de Tecnología Agropecuaria, Ex Ruta 40 km 96, La Consulta CC 8, 5567, Mendoza, Argentina

    Pablo F. Cavagnaro

  6. Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Buenos Aires, Argentina

    Pablo F. Cavagnaro

  7. Department of Horticulture Production and Marketing, Faculty of Agricultural Science and Technology, Lefke European University, TRNC, Mersin 10, Turkey

    Kazim Abak

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  1. Mehtap Yildiz
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  2. David K. Willis
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  6. Philipp W. Simon
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Correspondence to Philipp W. Simon.

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Communicated by I. Paran.

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Yildiz, M., Willis, D.K., Cavagnaro, P.F. et al. Expression and mapping of anthocyanin biosynthesis genes in carrot. Theor Appl Genet 126, 1689–1702 (2013). https://doi.org/10.1007/s00122-013-2084-y

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