Transcriptomic Analysis Suggests a Coordinated Regulation of Carotenoid Metabolism in Ripening Chili Pepper (Capsicum annuum var. conoides) Fruits

Abstract

Carotenoids are not only photosynthetic and photoprotective pigments in plants, but also essential antioxidative nutrients for human health. The fruit is the main plant organ that synthesizes and sequestrates carotenoids. Fruit ripening is a complicated developmental process, during which the rewiring of the metabolic network is tightly coordinated with the re-organization of cellular and organellular structures. Chili pepper (Capsicum annuum) is one of the major crops that accumulates a distinct level of carotenoids, especially capsanthin, in their ripened fruits. To elucidate how different metabolic and developmental scenarios are regulated in ripening chili pepper fruits, we analyzed the carotenoid profiles and transcriptomes of fruits at different ripening stages. Our pigment analysis indicated an opposite correlation between the contents of carotenoid species with β,β-structures (e.g., β-carotene, zeaxanthin, and capsanthin) and of lutein with the β,ε-structure, whereas lutein displayed a high correlation with chlorophylls during ripening. From the chili pepper Zunla-1 genome, a full repertoire of 38 homologous genes encoding enzymes in the carotenoid biosynthetic pathway was identified. The fluctuations in their transcript abundances during ripening suggested different involvement of these genes in the regulation of carotenoid biosynthesis. We further searched genes of which the expression showed high correlations with the accumulation of β-carotene during the ripening process. Moreover, from the transcriptomic analysis, a total of 17 transcription factors that co-expressed with different groups of carotenoid biosynthetic genes were identified.