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High-density single nucleotide polymorphism (SNP) array mapping in Brassica oleracea: identification of QTL associated with carotenoid variation in broccoli florets

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A high-resolution genetic linkage map of B. oleracea was developed from a B. napus SNP array. The work will facilitate genetic and evolutionary studies in Brassicaceae.

Abstract

A broccoli population, VI-158 × BNC, consisting of 150 F2:3 families was used to create a saturated Brassica oleracea (diploid: CC) linkage map using a recently developed rapeseed (Brassica napus) (tetraploid: AACC) Illumina Infinium single nucleotide polymorphism (SNP) array. The map consisted of 547 non-redundant SNP markers spanning 948.1 cM across nine chromosomes with an average interval size of 1.7 cM. As the SNPs are anchored to the genomic reference sequence of the rapid cycling B. oleracea TO1000, we were able to estimate that the map provides 96 % coverage of the diploid genome. Carotenoid analysis of 2 years data identified 3 QTLs on two chromosomes that are associated with up to half of the phenotypic variation associated with the accumulation of total or individual compounds. By searching the genome sequences of the two related diploid species (B. oleracea and B. rapa), we further identified putative carotenoid candidate genes in the region of these QTLs. This is the first description of the use of a B. napus SNP array to rapidly construct high-density genetic linkage maps of one of the constituent diploid species. The unambiguous nature of these markers with regard to genomic sequences provides evidence to the nature of genes underlying the QTL, and demonstrates the value and impact this resource will have on Brassica research.

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References

  • Arias T, Beilstein MA, Tang M, McKain MR, Pires JC (2014) Diversification times among Brassica (Brassicaceae) crops suggest hybrid formation after 20 million years of divergence. Am J Bot 101:86–91

    Article  PubMed  Google Scholar 

  • Ayele M, Haas BJ, Kumar N, Wu H, Xiao Y, Van Aken S, Utterback TR, Wortman JR, White OR, Town CD (2005) Whole genome shotgun sequencing of Brassica oleracea and its application to gene discovery and annotation in Arabidopsis. Genome Res 15:487–495

    Article  PubMed Central  PubMed  Google Scholar 

  • Babula D, Kaczmarek M, Barakat A, Delseny M, Quiros CF, Sadowski J (2003) Chromosomal mapping of Brassica oleracea based on ESTs from Arabidopsis thaliana: complexity of the comparative map. Mol Genet Genomics 268:656–665

    CAS  PubMed  Google Scholar 

  • Bohuon EJR, Keith DJ, Parkin IAP, Sharpe AG, Lydiate DJ (1996) Alignment of the conserved C genomes of Brassica oleracea and Brassica napus. Theor Appl Genet 93:833–839

    Article  CAS  PubMed  Google Scholar 

  • Brown AF, Yousef GG, Jeffery EH, Klein PB, Wallig MA, Kushad MM, Juvik JA (2002) Glucosinolate profiles in broccoli: variation in levels and implications in breeding for cancer chemoprotection. J Am Soc Hortic Sci 127:807

    CAS  Google Scholar 

  • Brown AF, Jeffery EH, Juvik JA (2007) A polymerase chain reaction-based linkage map of broccoli and identification of quantitative trait loci associated with harvest date and head weight. J Am Soc Hortic Sci 132:507–513

    CAS  Google Scholar 

  • Camargo LEA, Savides L, Jung G, Nienhuis J, Osborn TC (1997) Location of the self-incompatibility locus in an RFLP and RAPD map of Brassica oleracea. J Hered 88:57

    Article  CAS  PubMed  Google Scholar 

  • Cárdenas P, Gajardo H, Huebert T, Parkin I, Iniguez-Luy F, Federico M (2012) Retention of triplicated phytoene synthase (PSY) genes in Brassica napus L. and its diploid progenitors during the evolution of the Brassiceae. Theor Appl Genet 124:1215–1228

    Article  PubMed  Google Scholar 

  • Cazzonelli IC, Pogson BJ (2010) Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci 15:266–274

    Article  CAS  PubMed  Google Scholar 

  • de Sá MC, Rodriguez-Amaya DB (2004) Optimization of HPLC quantification of carotenoids in cooked green vegetables—comparison of analytical and calculated data. J Food Compos Anal 17:37–51

    Article  Google Scholar 

  • DellaPenna D, Pogson BJ (2006) Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol 57:711–738

    Article  CAS  PubMed  Google Scholar 

  • Eberhardt VM, Kobira K, Keck AS, Juvik AJ, Jeffery EH (2005) Correlation analyses of phytochemical composition, chemical, and cellular measures of antioxidant activity of broccoli (Brassica oleracea L. Var. italica). J Agric Food Chem 53:7421–7431

    Article  CAS  PubMed  Google Scholar 

  • Farnham MW, Kopsell DA (2009) Importance of genotype on carotenoid and chlorophyll levels in broccoli heads. HortScience 44:1248–1253

    Google Scholar 

  • Gao M, Li G, Yang B, Qui D, Farnham M, Quiros C (2007) High-density Brassica oleracea linkage map: identification of useful new linkages. Theor Appl Genet 115:277–287

    Article  CAS  PubMed  Google Scholar 

  • García-Plazaola JI, Matsubara S, Osmond CB (2007) The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions. Funct Plant Biol 34:759–773

    Article  Google Scholar 

  • Guzman I, Yousef GG, Brown AF (2012) Simultaneous extraction and quantitation of carotenoids, chlorophylls, and tocopherols in Brassica vegetables. J Agric Food Chem 60:7238–7244

    Article  CAS  PubMed  Google Scholar 

  • Heinonen MI, Ollilainen V, Linkola EK, Varo PT, Koivistoinen PE (1989) Carotenoids in Finnish foods: vegetables, fruits, and berries. J Agric Food Chem 10:655–659

    Article  Google Scholar 

  • Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4:210–218

    Article  CAS  PubMed  Google Scholar 

  • Holden JM, Eldridge AL, Beecher GR, Buzzard IM, Bhagwat S, Davis CS, Douglass LW, Gebhardt S, Haytowitz D, Schakel S (1999) Carotenoid content of U.S. foods: an update of the database. J Food Compos Anal 12:169–196

    Article  CAS  Google Scholar 

  • Hu J, Sadowski J, Osborn TC, Landry BS, Quiros CF (1998) Linkage group alignment from four independent Brassica oleracea RFLP maps. Genome 41:226–235

    Article  CAS  Google Scholar 

  • Iniguez-Luy F, Lukens L, Farnham M, Amasino R, Osborn T (2009) Development of public immortal mapping populations, molecular markers and linkage maps for rapid cycling Brassica rapa and B. oleracea. Theor Appl Genet 120:31–43

    Article  CAS  PubMed  Google Scholar 

  • Kianian SF, Quiros CF (1992) Generation of a Brassica oleracea composite RFLP map: linkage arrangements among various populations and evolutionary implications. Theor Appl Genet 84:544–554

    CAS  PubMed  Google Scholar 

  • Kidwell KK, Osborn TC (1992) Simple plant DNA isolation procedures. In: Beckman JS, Osborn TC (eds) Plant genomes: methods for genetic and physical mapping, pp 1–13 Kluwer Academic, Netherlands

  • Kurilich AC, Tsau GJ, Brown AF, Howard L, Klein PB, Jeffery EH, Kushad M, Wallig MA, Juvik JA (1999) Carotene, tocopherol, and ascorbate contents in subspecies of Brassica oleracea. J Agric Food Chem 47:1576–1581

    Article  CAS  PubMed  Google Scholar 

  • Kushad M, Brown AF, Kurilich A, Juvik JA, Klein PP, Wallig M, Jeffery E (1999) Variation of glucosinolates in vegetable crops of Brassica oleracea. J Agric Food Chem 47:1541–1548

    Article  CAS  PubMed  Google Scholar 

  • Lan TH, Paterson AH (2000) Comparative mapping of quantitative trait loci sculpting the curd of Brassica oleracea. Genetics 155:1927

    CAS  PubMed Central  PubMed  Google Scholar 

  • Landry BS, Hubert N, Crete R, Chang MS, Lincoln SE, Etoh T (1992) A genetic map for Brassica oleracea based on RFLP markers detected with expressed DNA sequences and mapping of resistance genes to race 2 of Plasmodiophora brassicae (Woronin). Genome 35:409–420

    Article  CAS  Google Scholar 

  • Lefsrud MG, Kopsell DA, Kopsell DE, Randle WM (2006) Kale carotenoids Are unaffected by, whereas biomass production, elemental concentrations, and selenium accumulation respond to, changes in selenium fertility. J Agric Food Chem 54:1764–1771

    Article  CAS  PubMed  Google Scholar 

  • Li G, Quiros CF (2003) In planta side-chain glucosinolate modification in Arabidopsis by introduction of dioxygenase Brassica homolog BoGSL-ALK. Theor Appl Genet 106:1116–1121

    CAS  PubMed  Google Scholar 

  • Müller H (1997) Determination of the carotenoid content in selected vegetables and fruit by HPLC and photodiode array detection. Z Lebensm Unters F A 204:88–94

    Article  Google Scholar 

  • Murkovic M, Gams K, Draxl S, Pfannhauser W (2000) Development of an Austrian Carotenoid Database. J Food Compos Anal 13:435–440

    Article  CAS  Google Scholar 

  • Nagaoka T, Doullah MAU, Matsumoto S, Kawasaki S, Ishikawa T, Hori H, Okazaki K (2010) Identification of QTLs that control clubroot resistance in Brassica oleracea and comparative analysis of clubroot resistance genes between B. rapa and B. oleracea. Theor Appl Genet 120:1335–1346

    Article  CAS  PubMed  Google Scholar 

  • Ooijin VJW (2009) MapQTL® 6. Kyazma, Netherlands

    Google Scholar 

  • Parkin I, Magrath R, Keith D, Sharpe A, Mithen R, Lydiate D (1994) Genetics of aliphatic glucosinolates. II. Hydroxylation of alkenyl glucosinolates in Brassica napus. Heredity 72:594–598

    Article  CAS  Google Scholar 

  • Parkin IAP, Gulden SM, Sharpe AG, Lukens L, Trick M, Osborn TC, Lydiate DJ (2005) Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 171:765–781

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pink D, Bailey L, McClement S, Hand P, Mathas E, Buchanan WV, Astley D, King G, Teakle G (2008) Double haploids, markers and QTL analysis in vegetable brassicas. Euphytica 164:509–514

    Article  CAS  Google Scholar 

  • Qiu D, Gao M, Li G, Quiros C (2009) Comparative sequence analysis for Brassica oleracea with similar sequences in B. rapa and Arabidopsis thaliana. Plant Cell Rep 28:649–661

    Article  CAS  PubMed  Google Scholar 

  • Ramsay LD, Jennings DE, Kearsey MJ, Marshall DF, Bohuon EJ, Arthur AE, Lydiate DJ (1996) The construction of a substitution library of recombinant backcross lines in Brassica oleracea for the precision mapping of quantitative trait loci. Genome 39:558–567

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Sola MÁ, Rodríguez-Concepción M (2012) Carotenoid biosynthesis in arabidopsis: a colorful pathway. The Arabidopsis Book 10:e0158

  • Schranz ME, Song BH, Windsor AJ, Mitchell-Olds T (2007) Comparative genomics in the Brassicaceae: a family-wide perspective. Curr Opin Plant Biol 10:168–175

    Article  CAS  PubMed  Google Scholar 

  • Sebastian RL, Howell EC, King GJ, Marshall DF, Kearsey MJ (2000) An integrated AFLP and RFLP Brassica oleracea linkage map from two morphologically distinct doubled-haploid mapping populations. Theor Appl Genet 100:75–81

    Article  CAS  Google Scholar 

  • Slater G, Birney E (2005) Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 6:31

    Article  PubMed Central  PubMed  Google Scholar 

  • Slocum MK, Figdore SS, Kennard WC, Suzuki JY, Osborn TC (1990) Linkage arrangement of restriction fragment length polymorphism loci in Brassica oleracea. Theor Appl Genet 80:57–64

    CAS  PubMed  Google Scholar 

  • Sujak A, Gabrielska J, Grudziński W, Borc R, Mazurek P, Gruszecki WI (1999) Lutein and zeaxanthin as protectors of lipid membranes against oxidative damage: the structural aspects. Arch Biochem Biophys 371:301–307

    Article  CAS  PubMed  Google Scholar 

  • Thompson MJ, Thompson HJ (2009) Biomedical agriculture: a systematic approach to food crop improvement for chronic disease prevention. Adv Agron 102:1–54

    Article  Google Scholar 

  • Town CD, Cheung F, Maiti R, Crabtree J, Haas BJ, Wortman JR, Hine EE, Althoff R, Arbogast TS, Tallon LJ, Vigouroux M, Trick M, Bancroft I (2006) Comparative genomics of Brassica oleracea and Arabidopsis thaliana reveal gene loss, fragmentation, and dispersal after polyploidy. Plant Cell 18:1348–1359

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang D, Hamauzu Y (2004) Phenolics, ascorbic acid, carotenoids and antioxidant activity of broccoli and their changes during conventional and microwave cooking. Food Chem 88:503–509

    Article  CAS  Google Scholar 

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Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The experiment conducted complies with the laws of the United States and Canada.

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Authors and Affiliations

  1. Department of Horticultural Science, Plants for Human Health Institute, North Carolina State University, Kannapolis, NC, 28081, USA

    Allan F. Brown, Gad G. Yousef, Kranthi K. Chebrolu, Robert W. Byrd, Koyt W. Everhart, Aswathy Thomas & Ivette Guzman

  2. Agriculture and Agri-Food Canada, 107 Science Place, Saskatoon, SK, S7N0X2, Canada

    Isobel A. P. Parkin

  3. National Research Council Canada, 110 Gymnasium Place, Saskatoon, SK, S7N0W9, Canada

    Andrew G. Sharpe

  4. General Mills Crop Biosciences, Kannapolis, NC, 28081, USA

    Rebekah Oliver & Eric W. Jackson

  5. UNC Charlotte Bioinformatics Services Division, University of North Carolina-Charlotte, 150 Research Campus Dr., Kannapolis, NC, 28081, USA

    Robert W. Reid

Authors
  1. Allan F. Brown
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  2. Gad G. Yousef
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  3. Kranthi K. Chebrolu
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  4. Robert W. Byrd
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  5. Koyt W. Everhart
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  6. Aswathy Thomas
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  7. Robert W. Reid
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  8. Isobel A. P. Parkin
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  9. Andrew G. Sharpe
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  10. Rebekah Oliver
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  11. Ivette Guzman
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  12. Eric W. Jackson
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Corresponding author

Correspondence to Allan F. Brown.

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Communicated by Maria Laura Federico.

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Brown, A.F., Yousef, G.G., Chebrolu, K.K. et al. High-density single nucleotide polymorphism (SNP) array mapping in Brassica oleracea: identification of QTL associated with carotenoid variation in broccoli florets. Theor Appl Genet 127, 2051–2064 (2014). https://doi.org/10.1007/s00122-014-2360-5

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  • DOI: https://doi.org/10.1007/s00122-014-2360-5

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