Carotene Hydroxylase Activity Determines the Levels of Both α-Carotene and Total Carotenoids in Orange Carrots

Arango, Jacobo; Jourdan, Matthieu; Geoffriau, Emmanuel; Beyer, Peter; Welsch, Ralf

doi:10.1105/tpc.113.122127

Cited by 128 publications

(96 citation statements)

References 62 publications

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“…In fact, this is observed in association with a widespread CYP97A3 deficiency in orange carrot cultivars (Arango et al, 2014) and favorable BCH alleles in maize (Zea mays; Yan et al, 2010) as well as in biotechnological approaches (e.g. in potato tubers; Diretto et al, 2007).…”

Section: Tissue-specific Differences In Carotenoid Degradationmentioning

confidence: 99%

Tissue-Specific Apocarotenoid Glycosylation Contributes to Carotenoid Homeostasis in Arabidopsis Leaves

et al. 2015

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Attaining defined steady-state carotenoid levels requires balancing of the rates governing their synthesis and metabolism. Phytoene formation mediated by phytoene synthase (PSY) is rate limiting in the biosynthesis of carotenoids, whereas carotenoid catabolism involves a multitude of nonenzymatic and enzymatic processes. We investigated carotenoid and apocarotenoid formation in Arabidopsis (Arabidopsis thaliana) in response to enhanced pathway flux upon PSY overexpression. This resulted in a dramatic accumulation of mainly b-carotene in roots and nongreen calli, whereas carotenoids remained unchanged in leaves. We show that, in chloroplasts, surplus PSY was partially soluble, localized in the stroma and, therefore, inactive, whereas the membrane-bound portion mediated a doubling of phytoene synthesis rates. Increased pathway flux was not compensated by enhanced generation of long-chain apocarotenals but resulted in higher levels of C 13 apocarotenoid glycosides (AGs). Using mutant lines deficient in carotenoid cleavage dioxygenases (CCDs), we identified CCD4 as being mainly responsible for the majority of AGs formed. Moreover, changed AG patterns in the carotene hydroxylase mutants lutein deficient1 (lut1) and lut5 exhibiting altered leaf carotenoids allowed us to define specific xanthophyll species as precursors for the apocarotenoid aglycons detected. In contrast to leaves, carotenoid hyperaccumulating roots contained higher levels of b-carotene-derived apocarotenals, whereas AGs were absent. These contrasting responses are associated with tissue-specific capacities to synthesize xanthophylls, which thus determine the modes of carotenoid accumulation and apocarotenoid formation.

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Section: Tissue-specific Differences In Carotenoid Degradationmentioning

confidence: 99%

Tissue-Specific Apocarotenoid Glycosylation Contributes to Carotenoid Homeostasis in Arabidopsis Leaves

et al. 2015

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“…However, additional, hitherto unidentified carotenoid-derived metabolites with signaling function have been reported as being involved in the feedback regulation of carotenogenic gene expression (Diretto et al, 2006;Bai et al, 2009;Kachanovsky et al, 2012;Galpaz et al, 2013) and in the control of developmental processes (Avendaño-Vázquez et al, 2014;Van Norman et al, 2014;Tian, 2015). Furthermore, altered carotenoid patterns, achieved by overexpressing a downstream carotene hydroxylase, reduced PSY protein amounts in cultivated carrots by a posttranscriptional mechanism (Arango et al, 2014). …”

Section: Flux-dependent Translational Control Of Psy Mediated By Thementioning

confidence: 99%

“…Moreover, PSY protein levels were recently found to be posttranslationally regulated by the ORANGE proteins in Arabidopsis (Zhou et al, 2015). Additionally, potential feedbackregulatory mechanisms involve translation, plastid import, protein-protein interaction, and protein turnover to achieve stoichiometrically defined carotenoid biosynthetic complexes (Cazzonelli and Pogson, 2010;Nogueira et al, 2013;Arango et al, 2014;Avendaño-Vázquez et al, 2014;Tian, 2015).…”

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Carotenogenesis Is Regulated by 5′UTR-Mediated Translation of Phytoene Synthase Splice Variants

et al. 2016

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Phytoene synthase (PSY) catalyzes the highly regulated, frequently rate-limiting synthesis of the first biosynthetically formed carotene. While PSY constitutes a small gene family in most plant taxa, the Brassicaceae, including Arabidopsis (Arabidopsis thaliana), predominantly possess a single PSY gene. This monogenic situation is compensated by the differential expression of two alternative splice variants (ASV), which differ in length and in the exon/intron retention of their 59UTRs. ASV1 contains a long 59UTR (untranslated region) and is involved in developmentally regulated carotenoid formation, such as during deetiolation. ASV2 contains a short 59UTR and is preferentially induced when an immediate increase in the carotenoid pathway flux is required, such as under salt stress or upon sudden light intensity changes. We show that the long 59UTR of ASV1 is capable of attenuating the translational activity in response to high carotenoid pathway fluxes. This function resides in a defined 59UTR stretch with two predicted interconvertible RNA conformations, as known from riboswitches, which might act as a flux sensor. The translation-inhibitory structure is absent from the short 59UTR of ASV2 allowing to bypass translational inhibition under conditions requiring rapidly increased pathway fluxes. The mechanism is not found in the rice (Oryza sativa) PSY1 59UTR, consistent with the prevalence of transcriptional control mechanisms in taxa with multiple PSY genes. The translational control mechanism identified is interpreted in terms of flux adjustments needed in response to retrograde signals stemming from intermediates of the plastid-localized carotenoid biosynthesis pathway.

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“…As PSY catalyzes the rate-limiting step in carotenoid biosynthesis (Arango et al, 2014), the reduction of PSY protein could account for the reduced carotenoid accumulation in low-b fruit. This was confirmed by the determination of phytoene accumulation in detached developing melon fruit tissues upon the inhibition of PDS activity by NF, an indicative assay for PSY activity (Beisel et al, 2011;Lätari et al, 2015).…”

Section: Facilitation Of the Active Psy Enzymementioning

confidence: 99%

Distinct Mechanisms of the ORANGE Protein in Controlling Carotenoid Flux

Chayut

Yuan

Ohali³

et al. 2016

Plant Physiol.

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b-Carotene adds nutritious value and determines the color of many fruits, including melon (Cucumis melo). In melon mesocarp, b-carotene accumulation is governed by the Orange gene (CmOr) golden single-nucleotide polymorphism (SNP) through a yet to be discovered mechanism. In Arabidopsis (Arabidopsis thaliana), OR increases carotenoid levels by posttranscriptionally regulating phytoene synthase (PSY). Here, we identified a CmOr nonsense mutation (Cmor-lowb) that lowered fruit b-carotene levels with impaired chromoplast biogenesis. Cmor-lowb exerted a minimal effect on PSY transcripts but dramatically decreased PSY protein levels and enzymatic activity, leading to reduced carotenoid metabolic flux and accumulation. However, the golden SNP was discovered to not affect PSY protein levels and carotenoid metabolic flux in melon fruit, as shown by carotenoid and immunoblot analyses of selected melon genotypes and by using chemical pathway inhibitors. The high b-carotene accumulation in golden SNP melons was found to be due to a reduced further metabolism of b-carotene. This was revealed by genetic studies with double mutants including carotenoid isomerase (yofi), a carotenoid-isomerase nonsense mutant, which arrests the turnover of prolycopene. The yofi F2 segregants accumulated prolycopene independently of the golden SNP. Moreover, Cmor-lowb was found to inhibit chromoplast formation and chloroplast disintegration in fruits from 30 d after anthesis until ripening, suggesting that CmOr regulates the chloroplast-to-chromoplast transition. Taken together, our results demonstrate that CmOr is required to achieve PSY protein levels to maintain carotenoid biosynthesis metabolic flux but that the mechanism of the CmOr golden SNP involves an inhibited metabolism downstream of b-carotene to dramatically affect both carotenoid content and plastid fate.b-Carotene, a C-40 isoprenoid molecule, is the major source of vitamin A in the human diet (Maiani et al., 2009). Lack of dietary vitamin A is a common cause of premature death and child blindness in developing countries. b-Carotene is abundant in diverse edible plant tissues such as pumpkin (Cucurbita pepo) fruits, sweet potato (Ipomoea batatas) tubers, carrot (Daucus carota) roots, kale (Brassica oleracea) leaves, mango (Mangifera indica), and orange-fleshed melon (Cucumis melo) fruits (Howitt and Pogson, 2006;Yuan et al., 2015b). In green tissues, two b-carotene molecules are located in each PSII reaction center to facilitate electron transfer and to provide photoprotection by quenching singlet oxygen products (Telfer, 2002). In many fruits and flowers, b-carotene serves as a yellow-orange colorant and as a precursor for aromatic molecules to attract pollinators and seed dispersers (Walter and Strack, 2011).b-Carotene is a metabolite in the carotenoid biosynthesis pathway that receives its precursors from the plastid-localized methyl-erythritol phosphate pathway. Carotenoid biosynthesis starts with the condensation of two geranylgeranyl diphosphate molecules, yielding the color...

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Carotene Hydroxylase Activity Determines the Levels of Both α-Carotene and Total Carotenoids in Orange Carrots

Cited by 128 publications

References 62 publications

Tissue-Specific Apocarotenoid Glycosylation Contributes to Carotenoid Homeostasis in Arabidopsis Leaves

Tissue-Specific Apocarotenoid Glycosylation Contributes to Carotenoid Homeostasis in Arabidopsis Leaves

Carotenogenesis Is Regulated by 5′UTR-Mediated Translation of Phytoene Synthase Splice Variants

Distinct Mechanisms of the ORANGE Protein in Controlling Carotenoid Flux

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