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QTL involved in the modification of cyanidin compounds in black and red raspberry fruit

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Abstract

Fruit from Rubus species are highly valued for their flavor and nutritive qualities. Anthocyanin content contributes to these qualities, and although many studies have been conducted to identify and quantify the major anthocyanin compounds from various Rubus species, the genetic control of the accumulation of these complex traits in Rubus is not yet well understood. The identification of the regions of the genome involved in the production of anthocyanins is an important first step in identifying the genes underlying their expression. In this study, ultra and high-performance liquid chromatography (UHPLC and HPLC) and two newly developed Rubus linkage maps were used to conduct QTL analyses to explore the presence of associations between concentrations of five anthocyanins in fruit and genotype. In total, 27 QTL were identified on the Rubus linkage maps, four of which are associated with molecular markers designed from transcription factors and three of which are associated with molecular markers designed from anthocyanin biosynthetic pathway candidate genes. The results of this study suggest that, while QTL for anthocyanin accumulation have been identified on six of seven Rubus linkage groups (RLG), the QTL on RLG2 and RLG7 may be very important for genetic control of cyanidin modification in Rubus.

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References

  • Allan AC, Hellens RP, Laing WA (2008) MYB transcription factors that colour our fruit. Trends Plant Sci 13:99–102

    Article  PubMed  CAS  Google Scholar 

  • Ash MM, Wolford KA, Carden TJ, Hwang KT, Carr TP (2011) Unrefined and refined black raspberry seed oils significantly lower triglycerides and moderately affect cholesterol metabolism in male Syrian hamsters. J Med Food 14:1032–1038

    Article  PubMed  CAS  Google Scholar 

  • Baudry A, Heim M, Dubreucq B, Caboche M, Weisshaar B, Lepiniec L (2004) TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J 39:366–380

    Article  PubMed  CAS  Google Scholar 

  • Bushakra J, Stephens M, Atmadjaja A, Lewers K, Symonds V, Udall J, Chagné D, Buck E, Gardiner S (2012) Construction of black (Rubus occidentalis) and red (R. idaeus) raspberry linkage maps and their comparison to the genomes of strawberry, apple, and peach. Theor Appl Genet 125(2):311–327

    Article  PubMed  CAS  Google Scholar 

  • Cabrera A, Kozik A, Howad W, Arús P, Iezzoni A, van der Knaap E (2009) Development and bin mapping of a Rosaceae Conserved Ortholog Set (COS) of markers. BMC Genom 10:562

    Article  Google Scholar 

  • Chen HS, Liu M, Shi LJ, Zhao JL, Zhang CP, Lin LQ, Liu Y, Zhang SJ, Jin JC, Wang L, Shen BZ, Liu JR (2011) Effects of raspberry phytochemical extract on cell proliferation, apoptosis, and serum proteomics in a rat model. J Food Sci 76:T192–T198

    Article  PubMed  CAS  Google Scholar 

  • Connor AM, Finn CE, McGhie TK, Alspach PA (2005) Genetic and environmental variation in anthocyanins and their relationship to antioxidant activity in blackberry and hybridberry cultivars. J Am Soc Hortic Sci 130:680–687

    CAS  Google Scholar 

  • Cooney JM, Jensen DJ, McGhie TK (2004) LC-MS identification of anthocyanins in boysenberry extract and anthocyanin metabolites in human urine following dosing. J Sci Food Agric 84:237–245

    Article  CAS  Google Scholar 

  • Dobson P, Graham J, Stewart D, Brennan R, Hackett CA, McDougall GJ (2012) Over-seasons analysis of quantitative trait loci affecting phenolic content and antioxidant capacity in raspberry. J Agric Food Chem 60:5360–5366

    Article  PubMed  CAS  Google Scholar 

  • Dossett M, Lee J, Finn CE (2010) Variation in anthocyanins and total phenolics of black raspberry populations. J Funct Foods 2:292–297

    Article  CAS  Google Scholar 

  • Dossett M, Lee J, Finn CE (2011) Characterization of a novel anthocyanin profile in wild black raspberry mutants: an opportunity for studying the genetic control of pigment and color. J Funct Foods 3:207–214

    Article  CAS  Google Scholar 

  • Draborg H, Villadsen D, Hamborg Nielsen T (1999) Cloning, characterization and expression of a bifunctional fructose-6-phosphate, 2-kinase/fructose-2,6-bisphosphatase from potato. Plant Mol Biol 39:709–720

    Article  PubMed  CAS  Google Scholar 

  • Espín JC, García-Conesa MT, Tomás-Barberán FA (2007) Nutraceuticals: facts and fiction. Phytochemistry 68:2986–3008

    Article  PubMed  Google Scholar 

  • Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, Allan AC (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J 49:414–427

    Article  PubMed  CAS  Google Scholar 

  • Finley JW, Kong A-N, Hintze KJ, Jeffery EH, Ji LL, Lei XG (2011) Antioxidants in foods: State of the science important to the food industry. J Agric Food Chem 59(13):6837–6846

    Article  PubMed  CAS  Google Scholar 

  • Graham J, Smith K, MacKenzie K, Jorgenson L, Hackett C, Powell W (2004) The construction of a genetic linkage map of red raspberry (Rubus idaeus subsp. idaeus) based on AFLPs, genomic-SSR and EST-SSR markers. Theor Appl Genet 109:740–749

    Article  PubMed  CAS  Google Scholar 

  • Graham J, Hackett C, Smith K, Woodhead M, Hein I, McCallum S (2009) Mapping QTLs for developmental traits in raspberry from bud break to ripe fruit. Theor Appl Genet 118:1143–1155

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hummer KE (2010) Rubus pharmacology: antiquity to the present. HortSci 45:1587–1591

    Google Scholar 

  • Jennings DL, Carmichael E (1980) Anthocyanin variation in the genus Rubus. New Phytol 84:505–513

    Article  CAS  Google Scholar 

  • Kafkas E, Özgen M, Özoğui Y, Türemiş N (2008) Phytochemical and fatty acid profile of selected red raspberry cultivars: a comparative study. J Food Quality 31:67–78

    Article  CAS  Google Scholar 

  • Kassim A, Poette J, Paterson A, Zait D, McCallum S, Woodhead M, Smith K, Hackett C, Graham J (2009) Environmental and seasonal influences on red raspberry anthocyanin antioxidant contents and identification of quantitative traits loci (QTL). Mol Nutrit Food Res 53:625–634

    Article  CAS  Google Scholar 

  • Keniry A, Hopkins CJ, Jewell E, Morrison B, Spangenberg GC, Edwards D, Batley J (2006) Identification and characterization of simple sequence repeat (SSR) markers from Fragaria × ananassa expressed sequences. Mol Ecol Notes 6:319–322

    Article  CAS  Google Scholar 

  • Kuhn DN, Chappell J, Boudet A, Hahlbrock K (1984) Induction of phenylalanine ammonia-lyase and 4-coumarate: CoA ligase mRNAs in cultured plant cells by UV light or fungal elicitor. Proc Nat Acad Sci 81:1102–1106

    Article  PubMed  CAS  Google Scholar 

  • Liang XW, Dron M, Cramer CL, Dixon RA, Lamb CJ (1989) Differential regulation of phenylalanine ammonia-lyase genes during plant development and by environmental cues. J Biol Chem 264:14486–14492

    PubMed  CAS  Google Scholar 

  • Lim E-K, Ashford DA, Hou B, Jackson RG, Bowles DJ (2004) Arabidopsis glycosyltransferases as biocatalysts in fermentation for regioselective synthesis of diverse quercetin glucosides. Biotechnol Bioeng 87:623–631

    Article  PubMed  CAS  Google Scholar 

  • Lin-Wang K, Bolitho K, Grafton K, Kortstee A, Karunairetnam S, McGhie T, Espley R, Hellens R, Allan A (2010) An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biol 10:50

    Article  PubMed  Google Scholar 

  • Määttä-Riihinen KR, Kamal-Eldin A, Törrönen AR (2004) Identification and quantification of phenolic compounds in berries of Fragaria and Rubus species (Family Rosaceae). J Agric Food Chem 52:6178–6187

    Article  PubMed  Google Scholar 

  • McCallum S, Woodhead M, Hackett C, Kassim A, Paterson A, Graham J (2010) Genetic and environmental effects influencing fruit colour and QTL analysis in raspberry. Theor Appl Genet 121:611–627

    Article  PubMed  CAS  Google Scholar 

  • McGhie TK, Hall HK, Ainge GD, Mowat AD (2002) Breeding Rubus cultivars for high anthocyanin content and high antioxidant capacity. Acta Hort (ISHS) 585:495–500

    CAS  Google Scholar 

  • Montrose DC, Horelik NA, Madigan JP, Stoner GD, Wang L-S, Bruno RS, Park HJ, Giardina C, Rosenberg DW (2011) Anti-inflammatory effects of freeze-dried black raspberry powder in ulcerative colitis. Carcinogenesis 32:343–350

    Article  PubMed  CAS  Google Scholar 

  • Mullen W, Yokota T, Lean MEJ, Crozier A (2003) Analysis of ellagitannins and conjugates of ellagic acid and quercetin in raspberry fruit by LC-MSn. Phytochemistry 64:617–624

    Article  PubMed  CAS  Google Scholar 

  • Ozgen M, Wyzgoski FJ, Tulio AZ, Gazula A, Miller AR, Scheerens JC, Reese RN, Wright SR (2008) Antioxidant capacity and phenolic antioxidants of midwestern black raspberries grown for direct markets are influenced by production site. HortSci 43:2039–2047

    Google Scholar 

  • Pelletier MK, Shirley BW (1996) Analysis of flavanone 3-hydroxylase in Arabidopsis seedlings (coordinate regulation with chalcone synthase and chalcone isomerase). Plant Physiol 111:339–345

    Article  PubMed  CAS  Google Scholar 

  • Sargent D, Rys A, Nier S, Simpson D, Tobutt K (2007) The development and mapping of functional markers in Fragaria and their transferability and potential for mapping in other genera. Theor Appl Genet 114:373–384

    Article  PubMed  CAS  Google Scholar 

  • Scalzo J, Currie A, Stephens J, McGhie T, Alspach P (2008) The anthocyanin composition of different Vaccinium, Ribes, and Rubus genotypes. BioFactors 34:13–21

    Article  PubMed  Google Scholar 

  • Seeram NP, Momin RA, Nair MG, Bourquin LD (2001) Cyclooxygenase inhibitory and antioxidant cyanidin glycosides in cherries and berries. Phytomedicine 8:362–369

    Article  PubMed  CAS  Google Scholar 

  • Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O, Delcher AL, Jaiswal P, Mockaitis K, Liston A, Mane SP, Burns P, Davis TM, Slovin JP, Bassil N, Hellens RP, Evans C, Harkins T, Kodira C, Desany B, Crasta OR, Jensen RV, Allan AC, Michael TP, Setubal JC, Celton J-M, Rees DJG, Williams KP, Holt SH, Rojas JJR, Chatterjee M, Liu B, Silva H, Meisel L, Adato A, Filichkin SA, Troggio M, Viola R, Ashman T-L, Wang H, Dharmawardhana P, Elser J, Raja R, Priest HD, Bryant DW, Fox SE, Givan SA, Wilhelm LJ, Naithani S, Christoffels A, Salama DY, Carter J, Girona EL, Zdepski A, Wang W, Kerstetter RA, Schwab W, Korban SS, Davik J, Monfort A, Denoyes-Rothan B, Arús P, Mittler R, Flinn B, Aharoni A, Bennetzen JL, Salzberg SL, Dickerman AW, Velasco R, Borodovsky M, Veilleux RE, Folta KM (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–116

    Article  PubMed  CAS  Google Scholar 

  • Sooriyapathirana S, Khan A, Sebolt A, Wang D, Bushakra J, Lin-Wang K, Allan A, Gardiner S, Chagné D, Iezzoni A (2010) QTL analysis and candidate gene mapping for skin and flesh color in sweet cherry fruit (Prunus avium L.). Tree Genet Genomes 6:821–832

    Article  Google Scholar 

  • Takos AM, Ubi BE, Robinson SP, Walker AR (2006) Condensed tannin biosynthesis genes are regulated separately from other flavonoid biosynthesis genes in apple fruit skin. Plant Sci 170:487–499

    Article  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 

  • Thompson MM (1995) Chromosome numbers of Rubus species at the National Clonal Germplasm Repository. HortSci 30:1447–1452

    Google Scholar 

  • Tohge T, Nishiyama Y, Hirai M, Yano M, Nakajima J, Awazuhara M, Inoue E, Takahashi H, Goodenowe D, Kitayama M, Noji M, Yamazaki M, Saito K (2005) Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant J 42:218–235

    Article  PubMed  CAS  Google Scholar 

  • Torre LC, Barritt BH (1977) Quantitative evaluation of Rubus fruit anthocyanin pigments. J Food Sci 42:488–490

    Article  CAS  Google Scholar 

  • Tulio AZ, Reese RN, Wyzgoski FJ, Rinaldi PL, Fu R, Scheerens JC, Miller AR (2008) Cyanidin 3-rutinoside and cyanidin 3-xylosylrutinoside as primary phenolic antioxidants in black raspberry. J Agric Food Chem 56:1880–1888

    Article  PubMed  CAS  Google Scholar 

  • van Ooijen JW (1992) Accuracy of mapping quantitative trait loci in autogamous species. Theor Appl Genet 84:803–811

    Article  Google Scholar 

  • van Ooijen JW (2004) MapQTL® 5, Software for the mapping of quantitative trait loci in experimental populations. Kyazma, B.V., Wageningen, The Netherlands

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagne D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouze P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel C-E, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839

    Article  PubMed  CAS  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  PubMed  CAS  Google Scholar 

  • VSN International L (2010) GenStat 12.2.0.3717 edn

  • Woodhead M, Weir A, Smith K, McCallum S, MacKenzie K, Graham J (2010) Functional markers for red raspberry. J Am Soc Hortic Sci 135:418–427

    Google Scholar 

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Acknowledgments

This work was completed as part of a Ph.D. thesis and supported in part by the PFR Excellence Program (JMB) and the “New Berries” FRST Programme (CO6XO807) (EJB). The authors would like to thank Andrew McLachlan (PFR) for help with the statistics; Peter Alspach (PFR) for help with the epistasis analysis; the Editor and three anonymous reviewers for helpful suggestions on the original manuscript.

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Correspondence to D. Chagné.

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Communicated by H. Nybom.

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Bushakra, J.M., Krieger, C., Deng, D. et al. QTL involved in the modification of cyanidin compounds in black and red raspberry fruit. Theor Appl Genet 126, 847–865 (2013). https://doi.org/10.1007/s00122-012-2022-4

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