A Comprehensive Analysis of Carotenoid Cleavage Dioxygenases Genes in Solanum Lycopersicum

Abstract

Carotenoid cleavage dioxygenases (CCDs) in plant species is one of the most important enzymes in the carotenoid metabolism. In this study, we performed a comprehensive analysis for the CCDs family in Solanum lycopersicum based on the whole tomato genome sequences and explored their expression pattern. At least seven CCD genes were discovered in the tomato genome sequence. Two pairs of them were arranged in tandem. The tandem duplication events could be dating to approximately 14 and 21 Mya, and the tandem duplication genes experienced a purifying selection during the course of evolution after diversification. Additionally, subcellular localization revealed that four members were predicted to be cytoplasm-localized and the three remaining members plastids-localized. Subsequently, a number of cis-regulatory elements, which were involved in light responsiveness, hormone regulation, and abiotic and biotic stresses, were identified in the promoter sequences of SlCCD genes. Phylogenetic tree revealed that the CCDs from Solanaceae crops have a closer genetic relationship. The difference in abundance and distinct expression patterns during the vegetative and reproductive development suggests different functions for these seven SlCCDs. Our findings suggest that SlCCDs family play important roles throughout the whole life course and will lay the foundation for further elaborating the regulatory mechanism of each member in tomato.

Carotenoid Cleavage Oxygenases from Microbes and Photosynthetic Organisms: Features and Functions

“…The degree of protein sequence identity among CCD4 members is quite variable, ranging from 30% to 98%, with typical values around 50%–70% [115,130,133,147,148]. In multigene CCD4 families, a high degree of homology (85%–98% identity at the protein level) is usually found between the different members, frequently located in tandem on the same chromosome (i.e., tomato CCD4a and b , citrus CCD4b1 and b2 , chrysamthemum CCD4a-1 to a-4 , or Populus CCD4c to e ) [115,133].…”

“…Analysis of the carotenoid profile in tubers from RNAi CCD4 potato lines suggested violaxanthin as the main substrate [150]. However, in-depth biochemical characterization of potato CCD4a using in vitro and in vivo assays points to β-carotene as its main substrate, cleaved at C9–C10 or C9′–C10′ positions [148]. In saffron, in vivo assays showed that CCD4a and b cleave β-carotene and zeaxanthin most likely at the C9–C10 and C9′–C10′ double bonds, while CCD4c cleaves other xanthophylls such as lutein [89,130,151].…”

“…Usually at least one CCD4 member is highly or exclusively expressed in flowers, and its function has been related to the production of nor-isoprenoid aroma volatiles to attract pollinators [96,133,146,148,154,155]. In chrysantemum, Osmanthus , and cabbage, the expression of a specific CCD4 gene in petals is responsible for carotenoid degradation and a lack of flower coloration [136,145,152].…”

“…In saffron, the expression of CCD4a/b correlates with the production of the nor-isoprenoid β-ionone in flower tissues, while CCD4c is restricted to stigmas and shows a highly regulated expression pattern during flower development [89,130]. In other species, such as sweet orange, tomato, and potato, at least one CCD4 gene is expressed in flowers, but their involvement in carotenoid degradation has not been elucidated [133,148,150]. Expression of CCD4 genes has also been reported in many fruits and its role has been associated with the biosynthesis of nor-isoprenoid volatiles or apocarotenoids pigments, which may attract animals to facilitate seed dispersion.…”

“…It is interesting to note that, due to the intense orange-red color of these C 30 apocarotenoids, the citrus CCD4 activity enhances fruit pigmentation, in contrast to the other CCD4s described so far whose activity is associated with color loss. In other species, such as bitter melon, goji berry, and tomato, the expression of at least one CCD4 gene has been reported in ripened fruits, but no relationship has been established with carotenoid content [148,155,163]. In potato tubers, compared with the yellow ones, CCD4 activity regulates coloration, as indicated by the elevated CCD4 expression in mature white-fleshed tubers [150].…”