Dissecting the genetic control of root and leaf tissue-specific anthocyanin pigmentation in carrot (Daucus carota L.)

Authors: BANNOUD, FLORENCIA - Consejo Nacional De Investigaciones Científicas Y Técnicas(CONICET); ELLISON, SHELBY - Former ARS Employee; PAOLINELLI, MARCOS - Consejo Nacional De Investigaciones Científicas Y Técnicas(CONICET); Horejsi, Thomas; Senalik, Douglas; FANZONE, MARTIN - Instituto Nacional De Tecnologia Agropecuaria; IORIZZO, MASSIMO - North Carolina State University; Simon, Philipp; CAVAGNARO, PABLO - Consejo Nacional De Investigaciones Científicas Y Técnicas(CONICET)

Submitted to: Theoretical and Applied Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/17/2019
Publication Date: 5/29/2019
Citation: Bannoud, F., Ellison, S., Paolinelli, M., Horejsi, T.F., Senalik, D.A., Fanzone, M., Iorizzo, M., Simon, P.W., Cavagnaro, P. 2019. Dissecting the genetic control of root and leaf tissue-specific anthocyanin pigmentation in carrot (Daucus carota L.). Theoretical and Applied Genetics. 132:2485–2507. https://doi.org/10.1007/s00122-019-03366-5.
DOI: https://doi.org/10.1007/s00122-019-03366-5

Interpretive Summary: Purple was one of the original colors of carrots 1100 years ago in Central Asia. Anthocyanin pigments account for this color but the molecular biosynthetic mechanisms that explain the accumulation of anthocyanins in purple carrots have not been elucidated. In this study we evaluated the genetic basis for individual pigments and then followed the messenger RNA gene products of these genes to identify a messenger that triggers the biosynthesis of anthocyanins in purple carrots. These results provide a foundation for better understanding molecular control mechanisms that stimulate anthocyanin in not only carrots but also other vegetables and fruits. This research is of interest to plant geneticists and molecular biologists, and also to nutritionists since anthocyanins have a significant positive health impact as antioxidants that alleviate several cardiopulmonary disorders.

Technical Abstract: Purple carrots can accumulate large quantities of anthocyanins in their roots, as well as in other plant organs. In order to investigate the genetic control underlying tissue-specific anthocyanin pigmentation in the root phloem and xylem, and in leaf petioles, we scored purple color visually in these three tissues in segregating F2 and F4 populations, and quantified anthocyanin pigments in phloem and xylem tissues, individually, by high performance liquid chromatography in two of these populations, to map QTL and simply-inherited loci for anthocyanin pigmentation onto linkage maps constructed with genotyping-by-sequencing (GBS) markers. In the F2, a total of 41 and 10 QTL for phloem and xylem anthocyanins, respectively, were mapped across 5 linkage groups. Two regions in chromosome 3, called regions A and B, harboring co-localized QTL and simply-inherited loci for tissue-specific anthocyanins, largely condition pigmentation in the three tissues. Regions A and B both condition pigmentation in the phloem, with region B also conditioning pigmentation in the xylem and petioles. By means of linkage mapping, phylogenetic analysis, and comparative transcriptome (RNA-Seq) analysis among carrot roots with different purple-pigmentation phenotypes, we identified candidate genes conditioning pigmentation in the phloem, the main tissue influencing total anthocyanin levels in the root. Among them, a MYB transcription factor, DcMYB7, and two cytochrome CYP450 genes with putative flavone synthase activity seem to regulate both the presence/absence of pigmentation and the concentration of anthocyanins in the root phloem. Another MYB transcription factor, DcMYB6, was upregulated in the purple-colored samples of some of the transcriptome comparisons, suggesting a genotype-specific regulatory activity for this gene. These data contribute to the understanding of anthocyanin regulation in the carrot root at a tissue-specific level, and may be instrumental for improving carrot nutritional value.