Population genomics identifies genetic signatures of carrot domestication and improvement and uncovers the origin of high-carotenoid orange carrots

Authors: COE, KEVIN - North Carolina State University; BOSTAN, HAMED - North Carolina State University; Rolling, William; TURNER-HISSONG, SARAH - Bayer Cropscience; MACKO-PODGORNI, ALICJA - Agricultural University Of Poland; Senalik, Douglas; LIU, SU - North Carolina State University; SETH, ROMIT - North Carolina State University; CURABA, JULIEN - North Carolina State University; FENTIE MENGIST, MOLLA - North Carolina State University; GRZEBELUS, DARIUSZ - Agricultural University Of Poland; VAN DEYNZE, ALLEN - University Of California, Davis; DAWSON, JULIE - University Of Wisconsin; ELLISON, SHELBY - University Of Wisconsin; Simon, Philipp; IORIZZO, MASSIMO - North Carolina State University

Submitted to: Nature Plants
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/28/2023
Publication Date: 9/28/2023
Citation: Coe, K., Bostan, H., Rolling, W.R., Turner-Hissong, S., Macko-Podgorni, A., Senalik, D.A., Liu, S., Seth, R., Curaba, J., Fentie Mengist, M., Grzebelus, D., Van Deynze, A., Dawson, J., Ellison, S., Simon, P.W., Iorizzo, M. 2023. Population genomics identifies genetic signatures of carrot domestication and improvement and uncovers the origin of high-carotenoid orange carrots. Nature Plants. 9:1643–1658. https://doi.org/10.1038/s41477-023-01526-6.
DOI: https://doi.org/10.1038/s41477-023-01526-6

Interpretive Summary: The written history of carrot indicates that, relative to wild carrot, the first domesticated carrots 1100 years ago contained yellow carotenoid pigments and started to develop flowers later in the life cycle, while in the 1500's the first orange carrots were developed. In this study the genetic fingerprints of 630 wild and cultivated carrots from around the world were evaluated and new genetic variation was observed for genes controlling carotenoid pigment accumulation, flowering time, and plant growth in carrots in roughly the same time frame as written history. This study sheds light on the genetics of carrot domestication that confirms written history, and provides insights to genes controlling yellow and orange carrots that may have application in improving the nutritional value of other crops. It is of interest to carrot growers and researchers, seed companies, nutritional scientists, historians, and consumers.

Technical Abstract: Here an improved carrot reference genome and resequencing of 630 carrot accessions were used to investigate carrot domestication and improvement. The study demonstrated that carrot was domesticated during the Early Middle Age in the region spanning Western Asia to Central Asia, and orange carrot was selected during the early Renaissance period in Europe, likely in the Netherlands. A progressive reduction of genetic diversity accompanied this process. Genes controlling vernalization/flowering, plant development and morphology, carotenoid biosynthesis, photosynthesis/light responses were under selection during domestication and improvement. Three recessive genes, REC1, Or and EXECUTER1 homologs, were essential to select for the high a- and ß- carotene orange phenotype. The study highlighted that in carrot high a- and ß- carotene biosynthesis is controlled through molecular mechanisms that regulate the interaction between the carotenoid biosynthetic pathway, the photosynthetic systems and chloroplast biogenesis. Overall the study elucidated at molecular level carrot domestication/breeding history and carotenoid genetics.