Skip to main content
Log in

The influence of the Or and Carotene Hydroxylase genes on carotenoid accumulation in orange carrots [Daucus carota (L.)]

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

The Or and CH genes are necessary for the accumulation of high amounts of β-carotene and other carotenoid pigments in carrot roots, in addition to the Y and Y2 genes.

Abstract

Carrot taproot color results from the accumulation of various carotenoid and anthocyanin pigments. Recently, the Or gene was identified as a candidate gene associated with the accumulation of β-carotene and other provitamin A carotenoids in roots. The specific molecular mechanisms involved with this process, as well as the interactions between Or and the other genes involved in this process are not well understood. In order to better characterize the effect that Or alleles have on conditioning the accumulation of carotenoids in roots, we analyzed an F3 family fixed homozygous recessive for y and y2, derived from a cross between an orange carrot and a white wild carrot, segregating for the two known Or alleles, which we name Orc and Orw. QTL mapping across three different environments revealed that the accumulation of several carotenoids was associated with the Orc allele, with consistent patterns across environments. A second QTL on chromosome 7, harboring a carotene hydroxylase gene homologous to Lut5 in Arabidopsis, was also associated with the accumulation of several carotenoids. Two alleles for this gene, which we name CHc and CHw, were discovered to be segregating in this population. Our study provides further evidence that Or and CH are likely involved with controlling the accumulation of β-carotene and may be involved with modulating carotenoid flux in carrot, demonstrating that both were important domestication genes in carrot.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Availability of data and material

All phenotypic and genotypic data necessary to confirm the conclusions presented in this article are available as supplementary material. The unfiltered VCF file is available at https://doi.org/10.6084/m9.figshare.14067131.v1.

References

  • Arango J, Jourdan M, Geoffriau E, Beyer P, Welsch R (2014) Carotene hydroxylase activity determines the levels of both α-carotene and total carotenoids in orange carrots. Plant Cell 26:2223–2233. https://doi.org/10.1105/tpc.113.122127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowman MJ, Willis DK, Simon PW (2014) Transcript abundance of phytoene synthase 1 and phytoene synthase 2 is associated with natural variation of storage root carotenoid pigmentation in carrot. J Amer Soc Hort Sci 139:63–68

    Article  CAS  Google Scholar 

  • Broman KW, Wu H, Sen Ś, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890. https://doi.org/10.1093/bioinformatics/btg112

    Article  CAS  PubMed  Google Scholar 

  • Buishand J, Gabelman W (1979) Investigations on the inheritance of color and carotenoid content in phloem and xylem of carrot roots (Daucus carota L.). Euphytica 28:611–632. https://doi.org/10.1007/BF00038928

    Article  CAS  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971. https://doi.org/10.1093/genetics/138.3.963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellison S, Senalik D, Bostan H, Iorizzo M, Simon P (2017) Fine mapping, transcriptome analysis, and marker development for Y2, the gene that conditions βcarotene accumulation in carrot (Daucus carota L.). G3 (Bethesda) 7:2665–2675

    Article  CAS  Google Scholar 

  • Ellison SL, Luby CH, Corak KE, Coe KM, Senalik D, Iorizzo M, Goldman IL, Simon PW, Dawson JC (2018) Carotenoid presence is associated with the Or gene in domesticated carrot. Genetics 210:1497–1508. https://doi.org/10.1534/genetics.118.301299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ichikawa T, Nakazawa M, Kawashima M, Iizumi H, Kuroda H, Kondou Y, Tsuhara Y, Suzuki K, Ishikawa A, Seki M (2006) The FOX hunting system: an alternative gain-of-function gene hunting technique. The Plant J 48:974–985

    Article  CAS  Google Scholar 

  • Iorizzo M, Ellison S, Senalik D, Zeng P, Satapoomin P, Huang J, Bowman M, Iovene M, Sanseverino W, Cavagnaro P (2016) A high-quality carrot genome assembly provides new insights into carotenoid accumulation and asterid genome evolution. Nat Genet 48:657

    Article  CAS  Google Scholar 

  • Jansen RC, Stam P (1994) High resolution of quantitative traits into multiple loci via interval mapping. Genetics 136:1447–1455

    Article  CAS  Google Scholar 

  • Just B, Santos C, Fonseca M, Boiteux L, Oloizia B, Simon P (2007) Carotenoid biosynthesis structural genes in carrot (Daucus carota): isolation, sequence-characterization, single nucleotide polymorphism (SNP) markers and genome mapping. Theor Appl Genet 114:693–704

    Article  CAS  Google Scholar 

  • Just BJ, Santos CA, Yandell BS, Simon PW (2009) Major QTL for carrot color are positionally associated with carotenoid biosynthetic genes and interact epistatically in a domesticated × wild carrot cross. Theor Appl Genet 119:1155–1169

    Article  Google Scholar 

  • Kim J, DellaPenna D (2006) Defining the primary route for lutein synthesis in plants: the role of Arabidopsis carotenoid β-ring hydroxylase CYP97A3. Proc Natl Ac Sci (USA) 103:3474–3479

    Article  CAS  Google Scholar 

  • Laferriere L, Gabelman W (1968) Inheritance of color, total carotenoids, alpha-carotene, and beta-carotene in carrots, Daucus carota. L Proc Amer Soc Hort Sci 93:408–418

    Google Scholar 

  • Macko-Podgórni A, Machaj G, Stelmach K, Senalik D, Grzebelus E, Iorizzo M, Simon PW, Grzebelus D (2017) Characterization of a genomic region under selection in cultivated carrot (Daucus carota subsp. sativus) reveals a candidate domestication gene. Front Plant Sci 8:12

    Article  Google Scholar 

  • Oleszkiewicz T, Klimek-Chodacka M, Milewska-Hendel A, Zubko M, Stróż D, Kurczyńska E, Boba A, Szopa J, Baranski R (2018) Unique chromoplast organisation and carotenoid gene expression in carotenoid-rich carrot callus. Planta 248:1455–1471

    Article  CAS  Google Scholar 

  • Ouellette LA, Reid RW, Blanchard SG, Brouwer CR (2018) LinkageMapView—rendering high-resolution linkage and QTL maps. Bioinformatics 34:306–307

    Article  CAS  Google Scholar 

  • Park S, Kim HS, Jung YJ, Kim SH, Ji CY, Wang Z, Jeong JC, Lee H-S, Lee SY, Kwak S-S (2016) Orange protein has a role in phytoene synthase stabilization in sweetpotato. Sci Rep 6:33563

    Article  CAS  Google Scholar 

  • R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/

  • Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative genomics viewer. Nat Biotechnol 29:24–26

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Santos CAF, Simon PW (2006) Heritabilities and minimum gene number estimates of carrot carotenoids. Euphytica 151:79–86

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Simon PW, Pollak LM, Clevidence BA, Holden JM, Haytowitz DB (2009) Plant breeding for human nutritional quality. Plant Breed Rev 31:325–392

    CAS  Google Scholar 

  • Taylor J, Butler D (2017) R package ASMap efficient genetic linkage map construction and diagnosis. J Stat Soft. https://doi.org/10.18637/jss.v079.i06

    Article  Google Scholar 

  • Turner SD, Ellison SL, Senalik DA, Simon PW, Spalding EP, Miller ND (2018) An automated image analysis pipeline enables genetic studies of shoot and root morphology in carrot (Daucus carota L.). Front Plant Sci 9:1703. https://doi.org/10.3389/fpls.2018.01703

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang H, Ou C-G, Zhuang F-Y, Ma Z-G (2014) The dual role of phytoene synthase genes in carotenogenesis in carrot roots and leaves. Mol Breed 34:2065–2079

    Article  CAS  Google Scholar 

  • Wu Y, Bhat PR, Close TJ, Lonardi S (2008) Efficient and accurate construction of genetic linkage maps from the minimum spanning tree of a graph. PLoS Genet 4(10):e1000212

    Article  Google Scholar 

  • Zeng Z-B, Kao C-h, Basten CJ (1999) Estimating the genetic architecture of quantitative traits. Genet Res 74:279–289

    Article  CAS  Google Scholar 

  • Zhou J, Wang X, Lee J-Y, Lee J-Y (2013) Cell-to-cell movement of two interacting AT-hook factors in arabidopsis root vascular tissue patterning. Plant Cell 25:187–201

    Article  CAS  Google Scholar 

  • Zhou X, Welsch R, Yang Y, Álvarez D, Riediger M, Yuan H, Fish T, Liu J, Thannhauser TW, Li L (2015) Arabidopsis OR proteins are the major posttranscriptional regulators of phytoene synthase in controlling carotenoid biosynthesis. Proc Natl Acad Sci 112:3558–3563

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dr. Tom Horejsi for field assistance, Dr. Jeffrey Endelman for providing code for marker binning, as well as Nathan Bosch, Elise Leeder, Priya Beejan, and Erin Lalor for assistance with sample collection and preparation for HPLC phenotyping. The authors would also like to thank the University of Wisconsin Biotechnology center DNA sequencing facility for providing genotyping-by-sequencing library preparation and sequencing services.

Funding

This study was funded by the National Institute of Food and Agriculture, U. S. Department of Agriculture (NIFA-USDA), under award number 2016–51181-25400. K.C. was supported by a University of Wisconsin–Madison Science and Medicine Graduate Research Scholars Fellowship and NIFA-USDA under award number 2016–51181-25400. S.E. was supported by NIFA-USDA under award number 2016–51181-25400.

Author information

Authors and Affiliations

Authors

Contributions

KC, SE, JD, and PS conceived and designed this study. KC and SE collected phenotypic and genotypic data, KC, SE, JD, and DS ran analyses. KC, JD, and PS wrote the paper. JD, SE, DS, and PS provided comments about the paper.

Corresponding author

Correspondence to Philipp Simon.

Ethics declarations

Conflicts of interest

The authors declare that they do not have any conflict of interest.

Additional information

Communicated by Richard G. F. Visser.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 391 KB)

Supplementary file2 (XLSX 3770 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Coe, K.M., Ellison, S., Senalik, D. et al. The influence of the Or and Carotene Hydroxylase genes on carotenoid accumulation in orange carrots [Daucus carota (L.)]. Theor Appl Genet 134, 3351–3362 (2021). https://doi.org/10.1007/s00122-021-03901-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-021-03901-3

Keywords

Navigation