Integrated metabolic and transcriptional analysis reveals the role of carotenoid cleavage dioxygenase 4 (IbCCD4) in carotenoid accumulation in sweetpotato tuberous roots

Abstract

Background Plant carotenoids are essential for human health, having wide uses in dietary supplements, food colorants, animal feed additives, and cosmetics. With the increasing demand for natural carotenoids, plant carotenoids have gained great interest in both academic and industry research worldwide. Orange-fleshed sweetpotato (Ipomoea batatas) enriched with carotenoids is an ideal feedstock for producing natural carotenoids. However, limited information is available regarding the molecular mechanism responsible for carotenoid metabolism in sweetpotato tuberous roots. Results In this study, metabolic profiling of carotenoids and gene expression analysis were conducted at six tuberous root developmental stages of three sweetpotato varieties with different flesh colors. The correlations between the expression of carotenoid metabolic genes and carotenoid levels suggested that the carotenoid cleavage dioxygenase 4 (IbCCD4) and 9-cis-epoxycarotenoid cleavage dioxygenases 3 (IbNCED3) play important roles in the regulation of carotenoid contents in sweetpotato. Transgenic experiments confirmed that the total carotenoid content decreased in the tuberous roots of IbCCD4-overexpressing sweetpotato. In addition, IbCCD4 may be regulated by two stress-related transcription factors, IbWRKY20 and IbCBF2, implying that the carotenoid accumulation in sweeetpotato is possibly fine-tuned in responses to stress signals. Conclusions A set of key genes were revealed to be responsible for carotenoid accumulation in sweetpotato, with IbCCD4 acts as a crucial player. Our findings provided new insights into carotenoid metabolism in sweetpotato tuberous roots and insinuated IbCCD4 to be a target gene in the development of new sweetpotato varieties with high carotenoid production.

Impact of steam cooking on the chemical profile of table-stock sweetpotatoes with different carotenoids content

“…The remaining cultivars exhibited no significant changes following the steaming process. The observed phenomenon is consistent with our previous findings, which might be attributed to the effective moisture retention in the sweetpotato flesh during the steaming process ( Zhang et al, 2023 ).

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“…Sweetpotato is an important source of carbohydrates, vitamins A and C, dietary fiber, iron, potassium, and protein, with its flesh color varying from white, yellow, and orange to purple ( Yan et al, 2022 ). There is evidence that the different color of flesh represents the richness of sweetpotato in terms of carotenoids, anthocyanins, phenolic compounds, etc., which have beneficial effects on the human body, such as anti-oxidation, anti-diabetes, and anti-cancer ( Zhang et al, 2023 ). Notably, the yellow and orange flesh sweetpotatoes are rich in carotenoids, which are important sources of antioxidants and vitamin A ( Laurie, Faber, & Claasen, 2018 ).…”

“…According to our previous research, except for streaming, which retained the most carotenoids content, different cooking methods could reduce the carotenoids contents of sweetpotato ( Yao, Zhang, Jia, Deng, & Wang, 2023 ). The carotenoids content of orange-fleshed sweetpotato (OFSP) was threefold higher than that of yellow-fleshed sweetpotato (YFSP), with YFSP experiencing a 50 % reduction after steaming, whereas OFSP retained nearly all of its carotenoids ( Yao et al, 2023 , Zhang et al, 2023 ). Additionally, the changes in the contents of starch, amylose, and soluble sugar in YFSP after steaming were significantly higher than those in OFSP ( Yao et al, 2023 , Zhang et al, 2023 ).…”

“…The carotenoids content of orange-fleshed sweetpotato (OFSP) was threefold higher than that of yellow-fleshed sweetpotato (YFSP), with YFSP experiencing a 50 % reduction after steaming, whereas OFSP retained nearly all of its carotenoids ( Yao et al, 2023 , Zhang et al, 2023 ). Additionally, the changes in the contents of starch, amylose, and soluble sugar in YFSP after steaming were significantly higher than those in OFSP ( Yao et al, 2023 , Zhang et al, 2023 ). During the steaming process, the starch and amylose content could significantly influence the sensory evaluation outcomes.…”

Verbascum species as a new source of saffron apocarotenoids and molecular tools for the biotechnological production of crocins and picrocrocin

“…Inside this subfamily, other CCD4 enzymes with a plastoglobuli localization are involved in the generation of aroma volatiles (Morote et al, 2023;Rubio et al, 2008;Wang et al, 2020), catalyzing the cleavage of 9,10;9 0 ,10 0 double bonds. However, these enzymes are also responsible for the degradation of carotenoids in different tissues and the loss of coloration of fruits and flowers (Awasthi et al, 2022;Brandi et al, 2011;Bruno et al, 2015;Gonzalez-Jorge et al, 2013;Morote et al, 2023;Ohmiya et al, 2006;Zhang et al, 2015Zhang et al, , 2023. Carotenoids, in particular b-carotene, can be sequentially cleaved by the activities of plastidic CCD7 (at positions 9,10 or 9 0 ,10 0 ) and CCD8 (at positions 13,14), resulting in carlactone as the precursor to strigolactone (Alder et al, 2008(Alder et al, , 2012.…”