Integrated Metabolomic and Transcriptomic Analyses Reveal the Basis for Carotenoid Biosynthesis in Sweet Potato (Ipomoea batatas (L.) Lam.) Storage Roots

Abstract

Carotenoids are important compounds of quality and coloration within sweet potato storage roots, but the mechanisms that govern the accumulation of these carotenoids remain poorly understood. In this study, metabolomic and transcriptomic analyses of carotenoids were performed using young storage roots (S2) and old storage roots (S4) from white-fleshed (variety S19) and yellow-fleshed (variety BS) sweet potato types. S19 storage roots exhibited significantly lower total carotenoid levels relative to BS storage roots, and different numbers of carotenoid types were detected in the BS-S2, BS-S4, S19-S2, and S19-S4 samples. β-cryptoxanthin was identified as a potential key driver of differences in root coloration between the S19 and BS types. Combined transcriptomic and metabolomic analyses revealed significant co-annotation of the carotenoid and abscisic acid (ABA) metabolic pathways, PSY (phytoene synthase), CHYB (β-carotene 3-hydroxylase), ZEP (zeaxanthin epoxidase), NCED3 (9-cis-epoxycarotenoid dioxygenase 3), ABA2 (xanthoxin dehydrogenase), and CYP707A (abscisic acid 8'-hydroxylase) genes were found to be closely associated with carotenoid and ABA content in these sweet potato storage roots. The expression patterns of the transcription factors OFP and FAR1 were associated with the ABA content in these two sweet potato types. Together, these results provide a valuable foundation for understanding the mechanisms governing carotenoid biosynthesis in storage roots, and offer a theoretical basis for sweet potato breeding and management.

Keywords: abscisic acid; carotenoid; metabolome; sweet potato; transcriptome.

Figure 1

Analyses of sweet potato storage root phenotypic characteristics and carotenoid content. (a) Storage root phenotypes were assessed for BS-S2, BS-S4, S19-S2, and S19-S4 samples. Scale bar = 200 μm. (b) Correlations between carotenoid content and color change. (c,d) Total carotenoid content (c) and color change (d) were analyzed in both sweet potato types at the analyzed time points. Data are means ± SEM (n = 3). *** p < 0.001, ** p < 0.01, * p < 0.05.

Figure 2

Analysis of carotenoid levels in sweet potato samples. The content of lutein (a–g), carotenoid esters (h–k), and carotene (l). Data are means ± SEM (n = 3). *** p < 0.001, ** p < 0.01, * p < 0.05.

Figure 3

Correlations between ABA levels and carotenoid content. (a) Total ABA-GE levels in the indicated samples (μg/g FW). (b) Total ABA levels in the indicated samples (μg/g FW). (c) The contents of ABA and ABA-GE were positively correlated with the contents of carotenoid-related components (graphic area is positively correlated with content.). Data are means ± SEM (n = 3). ** p < 0.01, * p < 0.05.

Figure 4

Analyses of DEGs identified in transcriptomic of sweet potato storage root samples and principal component analyses. (a) Sample repeatability and correlation analyses. (b) Heatmaps representing hierarchically clustered DEGs. (c) Statistical analyses of DEGs in the indicated groups. (d) PCA for samples included in transcriptomic analyses. (e) DEG cluster analyses.

Figure 5

The carotenoid and ABA metabolic pathways exhibiting DEG and DAM enrichment. (A: BS-S2; B: BS-S4; C: S19-S2; D: S19-S4.).

Figure 6

Differentially expressed genes encoding transcription factors in sweet potato samples. (a–d) The top 20 TF-encoding genes exhibiting the greatest fold-change in expression levels when comparing the BS-S2 and BS-S4 (a), S19-S2 and BS-S2 (b), S19-S2 and S19-S4 (c), and S19-S4 and BS-S4 (d) samples.

Figure 7

Correlation between DEGs and DAMs trends, with stronger correlations corresponding to a more consistent trend.

Figure 8

Expression analyses of structural genes and transcription factors associated with the carotenoid and ABA biosynthesis pathways. Data are means ± SEM (n = 3). *** p < 0.001, ** p < 0.01, * p < 0.05.