A novel carotenoid accumulation mechanism revealed through analysis of genetic structure and domestication in carrot (Daucus carota L.)

Authors: Ellison, Shelby; LUBY, CLAIRE - University Of Wisconsin; CORAK, KEO - University Of Wisconsin; COE, KEVIN - University Of Wisconsin; Senalik, Douglas; IORIZZO, MASSIMO - North Carolina State University; GOLDMAN, IRWIN - University Of Wisconsin; Simon, Philipp; DAWSON, JULIE - University Of Wisconsin

Submitted to: Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/15/2018
Publication Date: 12/1/2018
Citation: Ellison, S.L., Luby, C., Corak, K., Coe, K.M., Senalik, D.A., Iorizzo, M., Goldman, I., Simon, P.W., Dawson, J. 2018. A novel carotenoid accumulation mechanism revealed through analysis of genetic structure and domestication in carrot (Daucus carota L.). Genetics. 210(4):1497-1508. https://doi.org/10.1534/genetics.118.301299.
DOI: https://doi.org/10.1534/genetics.118.301299

Interpretive Summary: The first colors of carrot 1100 years ago were purple and yellow, not orange. There is some evidence for orange carrot earlier in history, but orange carrots did not appear consistently in the historical record until the 16th century when they quickly became the predominant color, as it is still today. The orange pigments in carrots, called carotenoids, contribute to their visual appeal and they provide 10-15% of the vitamin A to the U.S. diet. In past experiments we studied two of the genes that underlie the accumulation of high levels of carotenoids in carrot roots, but much of that biomolecular mechanism is largely unknown. Using a global collection of diverse carrots varying in color, in this study we provide the first evidence that the Or gene is involved in carrot carotenoid accumulation. The Or gene is known to be involved in carotenoid accumulation in other crops including cauliflower and sweet potato, but before this study, not carrot. Our analysis also enabled the identification of regions of the carrot genome that contain genes likely involved in carrot domestication that include not only the Or gene but also other traits such as carrot shape and flowering. This study will be of interest to plant geneticists, molecular biologists, breeders, nutritionists, vegetable growers, and agricultural historians.

Technical Abstract: Carrots accumulate more carotenoids than any other crop. Genetic variation in the carotenoid biosynthetic pathway does not fully explain the accumulation of such high levels of carotenoids in carrot roots. Using a diverse collection of modern and historic cultivated varieties and wild carrot accessions, an association analysis revealed a significant association with a region of the genome that contains the Or gene, advancing the Or gene as a candidate for carotenoid accumulation in carrots. This gene family has been demonstrated to control carotenoid accumulation in other crop families but has not previously been described in carrot. Our analysis also allowed us to more completely characterize the genetic structure of carrot, showing that the western domesticated carrot largely forms one genetic group, despite dramatic phenotypic differences among market classes within this group. Eastern domesticated and wild accessions form a second group, which reflects the more recent cultivation history of carrots in the specific eastern region of central Asia; and other wild accessions form distinct geographic groups, with a very well-defined group on the Iberian peninsula. Using genome-wide Fst, nucleotide diversity, and Tajima’s D statistics, we analyzed the genome for regions putatively under selection during domestication, and identified five regions that were significant for all three methods of detection, one of which includes the Or gene. This provides further support that Or was important in the early stages of carrot domestication and improvement and may explain why it has not been found with less genetically diverse mapping populations.