Dataset Information

Characterization of Transcriptional Expression and Regulation of Carotenoid Cleavage Dioxygenase 4b in Grapes.

ABSTRACT: Norisoprenoids are important aromatic volatiles contributing to the pleasant floral/fruity odor in grapes and wine. They are produced from carotenoids through the cleavage of carotenoid cleavage dioxygenases (CCDs). However, the underlying mechanisms regulating VvCCD expression remain poorly understood. In this study, we showed that VvCCD4b expression was positively correlated with the accumulation of ?-damascenone, ?-ionone, 6-methyl-5-hepten-2-one, geranylacetone, dihydroedulan I, and total norisoprenoids in developing grapes in two vintages from two regions. VvCCD4b was found to be principally expressed in flowers, mature leaves, and berries. Abscisic acid strongly induced the expression of this gene. Additionally, the present study preliminarily indicated that the activity of the VvCCD4b promoter was dropped under 37°C treatment and also responded to the illumination change. VvCCD4b was expressed in parallel with VvMADS4 in developing grape berries. The latter is a MADS family transcription factor and nucleus-localized protein that was captured by yeast one-hybrid. A dual-luciferase reporter assay in tobacco leaves revealed that VvMADS4 downregulated the activity of the VvCCD4b promoter. VvMADS4 overexpression in grape calli and Vitis quinquangularis Rehd. leaves repressed the VvCCD4b expression. In summary, this work demonstrates that VvCCD4b expression is positively correlated with the accumulation of norisoprenoids, and VvMADS4 is a potential negative regulator of VvCCD4b. Our results provide a new perspective for understanding the regulation of VvCCD4b expression and norisoprenoid accumulation in grapes.

SUBMITTER: Meng N

PROVIDER: S-EPMC7227400 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Characterization of Transcriptional Expression and Regulation of Carotenoid Cleavage Dioxygenase 4b in Grapes.

Meng Nan N Wei Yi Y Gao Yuan Y Yu Keji K Cheng Jing J Li Xiang-Yi XY Duan Chang-Qing CQ Pan Qiu-Hong QH

Frontiers in plant science 20200508

Norisoprenoids are important aromatic volatiles contributing to the pleasant floral/fruity odor in grapes and wine. They are produced from carotenoids through the cleavage of carotenoid cleavage dioxygenases (CCDs). However, the underlying mechanisms regulating <i>VvCCD</i> expression remain poorly understood. In this study, we showed that <i>VvCCD4b</i> expression was positively correlated with the accumulation of β-damascenone, β-ionone, 6-methyl-5-hepten-2-one, geranylacetone, dihydroedulan I ...[more]

PMID: 32457771

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Project description:The dietary needs of humans for provitamin A carotenoids arise from their inability to synthesize vitamin A de novo. To improve the status of this essential micronutrient, special attention has been given to biofortification of staple foods, such as wheat grains, which are consumed in large quantities but contain low levels of provitamin A carotenoids. However, there remains an unclear contribution of metabolic genes and homoeologs to the turnover of carotenoids in wheat grains. To better understand carotenoid catabolism in tetraploid wheat, Targeting Induced Local Lesions in Genomes (TILLING) mutants of CCD4, encoding a Carotenoid Cleavage Dioxygenase (CCD) that cleaves carotenoids into smaller apocarotenoid molecules, were isolated and characterized. Our analysis showed that ccd4 mutations co-segregated with Poltergeist-like (pll) mutations in the TILLING mutants of A and B subgenomes, hence the ccd-A4 pll-A, ccd-B4 pll-B, and ccd-A4 ccd-B4 pll-A pll-B mutants were analyzed in this study. Carotenoid profiles are comparable in mature grains of the mutant and control plants, indicating that CCD4 homoeologs do not have a major impact on carotenoid accumulation in grains. However, the neoxanthin content was increased in leaves of ccd-A4 ccd-B4 pll-A pll-B relative to the control. In addition, four unidentified carotenoids showed a unique presence in leaves of ccd-A4 ccd-B4 pll-A pll-B plants. These results suggested that CCD4 homoeologs may contribute to the turnover of neoxanthin and the unidentified carotenoids in leaves. Interestingly, abnormal spike, grain, and seminal root phenotypes were also observed for ccd-A4 pll-A, ccd-B4 pll-B, and ccd-A4 ccd-B4 pll-A pll-B plants, suggesting that CCD4 and/or PLL homoeologs could function toward these traits. Overall, this study not only reveals the role of CCD4 in cleavage of carotenoids in leaves and grains, but also uncovers several critical growth traits that are controlled by CCD4, PLL, or the CCD4-PLL interaction.

Project description:BackgroundIn plants, carotenoids serve as the precursors to C13-norisoprenoids, a group of apocarotenoid compounds with diverse biological functions. Enzymatic cleavage of carotenoids catalysed by members of the carotenoid cleavage dioxygenase (CCD) family has been shown to produce a number of industrially important volatile flavour and aroma apocarotenoids including β-ionone, geranylacetone, pseudoionone, α-ionone and 3-hydroxy-β-ionone in a range of plant species. Apocarotenoids contribute to the floral and fruity attributes of many wine cultivars and are thereby, at least partly, responsible for the "varietal character". Despite their importance in grapes and wine; carotenoid cleavage activity has only been described for VvCCD1 and the mechanism(s) and regulation of carotenoid catabolism remains largely unknown.ResultsThree grapevine-derived CCD-encoding genes have been isolated and shown to be functional with unique substrate cleavage capacities. Our results demonstrate that the VvCCD4a and VvCCD4b catalyse the cleavage of both linear and cyclic carotenoid substrates. The expression of VvCCD1, VvCCD4a and VvCCD4b was detected in leaf, flower and throughout berry development. VvCCD1 expression was constitutive, whereas VvCCD4a expression was predominant in leaves and VvCCD4b in berries. A transgenic population with a 12-fold range of VvCCD1 expression exhibited a lack of correlation between VvCCD1 expression and carotenoid substrates and/or apocarotenoid products in leaves, providing proof that the in planta function(s) of VvCCD1 in photosynthetically active tissue is distinct from the in vitro activities demonstrated. The isolation and functional characterisation of VvCCD4a and VvCCD4b identify two additional CCDs that are functional in grapevine.ConclusionsTaken together, our results indicate that the three CCDs are under various levels of control that include gene expression (spatial and temporal), substrate specificity and compartmentalisation that act individually and/or co-ordinately to maintain carotenoid and volatile apocarotenoid levels in plants. Altering the expression of VvCCD1 in a transgenic grapevine population illustrated the divergence between the in vitro enzyme activity and the in planta activity of this enzyme, thereby contributing to the efforts to understand how enzymatic degradation of carotenoids involved in photosynthesis occurs. The identification and functional characterisation of VvCCD4a and VvCCD4b suggest that these enzymes are primarily responsible for catalysing the cleavage of plastidial carotenoids.

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Characterization of Transcriptional Expression and Regulation of Carotenoid Cleavage Dioxygenase 4b in Grapes.

Publications

Characterization of Transcriptional Expression and Regulation of Carotenoid Cleavage Dioxygenase 4b in Grapes.

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