Dorcus C. Gemenet, Guilherme da Silva Pereira, Bert De Boeck, Joshua C. Wood, Marcelo Mollinari, Bode A. Olukolu, Federico Diaz, Veronica Mosquera, Reuben T. Ssali, Maria David, Mercy N. Kitavi, Gabriela Burgos, Thomas Zum Felde, Marc Ghislain, Edward Carey, Jolien Swanckaert, Lachlan J. M. Coin, Zhangjun Fei, John P. Hamilton, Benard Yada, G. Craig Yencho, Zhao-Bang Zeng, Robert O. M. Mwanga, Awais Khan, Wolfgang J. Gruneberg, C. Robin Buell

Theoretical and Applied Genetics; January 2020, Volume 133, Issue 1, pp 23–36| Cite as

Key message

β-Carotene content in sweetpotato is associated with the Orange and phytoene synthase genes; due to physical linkage of phytoene synthase with sucrose synthase, β-carotene and starch content are negatively correlated.

Abstract

In populations depending on sweetpotato for food security, starch is an important source of calories, while β-carotene is an important source of provitamin A. The negative association between the two traits contributes to the low nutritional quality of sweetpotato consumed, especially in sub-Saharan Africa. Using a biparental mapping population of 315 F₁ progeny generated from a cross between an orange-fleshed and a non-orange-fleshed sweetpotato variety, we identified two major quantitative trait loci (QTL) on linkage group (LG) three (LG3) and twelve (LG12) affecting starch, β-carotene, and their correlated traits, dry matter and flesh color. Analysis of parental haplotypes indicated that these two regions acted pleiotropically to reduce starch content and increase β-carotene in genotypes carrying the orange-fleshed parental haplotype at the LG3 locus. Phytoene synthase and sucrose synthase, the rate-limiting and linked genes located within the QTL on LG3 involved in the carotenoid and starch biosynthesis, respectively, were differentially expressed in Beauregard versus Tanzania storage roots. The Orange gene, the molecular switch for chromoplast biogenesis, located within the QTL on LG12 while not differentially expressed was expressed in developing roots of the parental genotypes. We conclude that these two QTL regions act together in a cis and trans manner to inhibit starch biosynthesis in amyloplasts and enhance chromoplast biogenesis, carotenoid biosynthesis, and accumulation in orange-fleshed sweetpotato. Understanding the genetic basis of this negative association between starch and β-carotene will inform future sweetpotato breeding strategies targeting sweetpotato for food and nutritional security.

See https://link.springer.com/article/10.1007/s00122-019-03437-7

Figure 4: Characterization of the QTL on LG3 underlying starch and β-carotene. a Genes are noted by arrows: Homeodomain-like superfamily protein (green); sucrose synthase (aqua), phytoene synthase (lt. orange), glutathione S-transferase (burgundy), AMP-dependent synthetase and ligase family protein (lilac), RAB homolog (gray), polyamine oxidase (magenta), P-loop containing nucleoside triphosphate hydrolase superfamily protein (Lt. blue), and conserved hypothetical (black). Black arrowhead denotes marker S3_3185578. b Left panel: Expression abundances (log2 fragments per kilobase per exon model per million mapped reads (FPKM)) of candidate genes involved in carotenoid metabolism are shown in the heat map below each gene for Beauregard (B) and Tanzania (T) for storage roots (SR) and fibrous roots (RF) at 30, 40, and 50 days after transplanting (DAT). Key code value indicates log2 FPKM and count indicates the number of samples (sample = one gene per sampling) with that FPKM value shown as a histogram. Gene identifiers and gene name abbreviations are listed to the right of the heat map. BCH, β-carotene hydrolase; CCD, carotenoid cleavage dioxygenases; CRTISO, carotene isomerase; LUT, lutein deficient; LYCB, lycopene b-cyclase; NCED, 9-cis-epoxycarotenoid dioxygenase; NXS, neoxanthin synthase; OR, ORANGE protein; PDS, phytoene desaturase; PSY, phytoene synthase; VDE, violaxanthin de-epoxidase; ZEP, zeaxanthin epoxidase; ZDS, zeta-carotene desaturase; Z-ISO, z-carotene isomerase. Right panel: Differentially expressed genes based on the comparison of Beauregard versus Tanzania storage roots (color figure online)