Carotenoid Cleavage Oxygenases from Microbes and Photosynthetic Organisms: Features and Functions
Abstract
:1. Introduction
2. Bacterial Carotenoid Oxygenases
2.1. Structural Studies
2.2. Substrate Specificity
2.2.1. Apocarotenoid Cleavage Oxygenases (ACO)
2.2.2. CCDs with Symmetrical Mode of Action
2.2.3. Carotenoid Oxygenases Cleaving at Different Positions
3. Fungal Carotenoid Oxygenases
3.1. Fungal CCDs Involved in Retinal Production
3.2. Fungal CCDs Involved in Trisporic Acid Production
3.3. Fungal CCDs Involved in Neurosporaxanthin Production
4. Plant CCDs
4.1. CCD1 and CCD2 Subfamilies
4.1.1. Mode of Action and Functional Implications
4.1.2. CCD1 Gene Family and Genomic Organization
4.1.3. Mode of Action of CCD2
4.1.4. Structure of CCD1 and CCD2 Enzymes
4.1.5. Regulation of CCD1 and CCD2 Enzymes
4.2. The CCD4 Subfamily
4.2.1. Enzyme Structure and Functional Implications
4.2.2. Gene Family and Genomic Organization
4.2.3. CCD4 Activity: Carotenoid Substrates and Cleavage Products
4.2.4. Expression Pattern in Plant Tissues
4.3. The CCD7 and CCD8 Subfamilies
5. CCDs in Algae
6. Conclusions
Supplementary Materials
Acknowledgments
Author Contributions
Conflicts of Interest
References
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Substrates | Diox1 Synechocystis sp. PCC 6803 | NosAco Nostoc sp. PCC 7120 |
---|---|---|
β-apo-4′-carotenal | Retinal | Not detected |
β-apo-8′-carotenal | Retinal | Retinal |
β-apo-10′-carotenal | Retinal | Retinal |
β-apo-12′-carotenal | Retinal | Not detected |
(3R)-3-OH-β-apo-8′-carotenal | 3-OH-retinal | 3R-3-OH-retinal |
(3R)-3-OH-β-apo-12′-carotenal | 3-OH-retinal | 3R-3-OH-retinal |
Apo-8′-lycopenal | Acycloretinal (slow) | Acycloretinal |
Apo-10′-lycopenal | No information | Acycloretinal |
β-apo-8′-carotenol | Retinal | Retinal |
(3R)-3-OH-β-apo-8′-carotenol | 3-OH-retinal | 3-OH-retinal |
Apo-8′-lycopenol | No information | Acycloretinal |
4-oxo-β-apo-8′-carotenal | 4-oxo-retinal (slow) | Not tested |
References | [29] | [32] |
Assayed Substrates | Enzymes and Products | ||||||
---|---|---|---|---|---|---|---|
β-carotene-oxygenase Microcystis PCC 7806 | NosCCD (NSC1) Nostoc sp. PCC 7120 | MtCCO Mycobacterium tuberculosis | NSC3 Nostoc sp. PCC 7120 | NACOX1 Novosphingobium | SaCCO Sphingopyxis alaskensis | PpCCO Plesiocystis pacifica | |
β-apo-8′-carotenal | β-ionone ( Other minority products ( | β-apo-13-carotenone ( Retinal ( | β-apo-13-carotenone ( β-apo-14′-carotenal Transretinal ( | β-apo-13-carotenone ( | Apo-12′-carotenal ( Apo-10′-carotenal ( | ||
β-apo-10′-carotenal | β-ionone ( | β-apo-13-carotenone ( Retinal ( | |||||
3-OH-β-apo-8′-carotenal | 3-OH-β-ionone ( | 3-OH-β-apo-13-carotenone ( 3-OH-retinal ( | |||||
3-OH-β-apo-10′-carotenal | 3-OH-β-ionone ( | 3-OH-β-apo-13-carotenone ( 3-OH-retinal ( | |||||
γ-carotene | β-ionone ( | β-apo-13-carotenone ( | |||||
β-carotene | 2 × β-cyclocitral ( Crocetindial ( | Apo-10,10′-apocarotene-dial ( | β-apo-13-carotenone ( Retinal ( β-apo-14′-carotenal ( | No | No | No (in vitro) | No |
Zeaxanthin | 2 × hydroxi-β-cyclocitral ( Crocetindial ( | 3-OH-β-ionone ( Apo-10,10′-apocarotene-dial ( | 3-OH-β-apo-13-carotenone ( 3-OH-β-apo-14′-carotenal ( 3-OH-retinal ( 3-OH-β-apo-11-carotenal? | No | No | No (in vitro) | Apo-13′-zeaxanthinone ( Apo-14′-zeaxanthinal ( Apo-12′-zeaxanthinal ( |
Lycopene | No | No | poorly | Yes (in vivo) Unknown product | |||
Lutein | 3-OH-β-apo-13-carotenone ( 3-OH-β-apo-14′-carotenal ( 3-OH-retinal ( 3-OH-α-apo-15′-carotenal( | No | |||||
Echinenone | No | 4-oxo-β-ionone ( Apo-10,10′-apocarotene-dial ( β-ionone ( | |||||
Canthaxantin | 2 x 4-oxo-β-ionone ( Apo-10,10′-apocarotene-dial ( | Apo-13′-canta-xanthinone ( Apo-14′-cantaxanthinal ( Apo-12′-cantaxanthinal ( | |||||
Astaxanthin | 3-OH-β-ionone ( 3-OH, 4-oxo-β-inone ( Apo-10,10′-apocarotene-dial ( | Apo-13′-astaxanthinone ( Apo-14′-astaxanthinal ( | |||||
References | [19] | [30,33] | [36] | [31] | [37] | [38] | [38] |
Substrates | Oxygenase | Products |
---|---|---|
β-apo-4′-carotenal | NACOX1 | β-apo-13-carotenone ( |
3,3′-dihydroxy-isorenieratene | MtCCO | 3-OH-β-apo-13-carotenone ( 3-OH-β-apo-15′-carotenal ( 3-OH-β-apo-14′-carotenal ( |
Echinenone | NosCCD | Apo-10,10′-apocarotenoid ( 2 × C13 ( |
Nostoxanthin | PpCCO | Apo-14′-nostoxanthinal ( Apo-12′-nostoxanthinal ( |
Hydroxylycopene | PpCCO | Unknown |
Dihydroxylycopene | PpCCO | Unknown |
Torulene | NSC3 | Transretinal ( |
4,4′-diapotorulene | NSC3 | Apo-14′-diapotorulenal ( |
4,4′-diapotorulene-4-al | NSC3 | Apo-10′-diapotorulenal ( |
4,4′-diaponeurosporene | NSC3 | Apo-14′-diaponeurosporenal ( |
4,4′-diaponeurosporen-4′-al | NSC3 | Apo-14′-diaponeurosporenal ( Apo-10′-diaponeurosporenal ( |
4,4′-diaponeurosporen-4′-oic acid | NSC3 | Apo-10′-diaponeurosporenal ( |
Myxol | NosCCD | 3-OH-β-ionone ( Apo-8′-10-apocarotenedial ( |
Myxol-2′-fucoside | NosCCD | 3-OH-β-ionone ( Apo-8′-10-apocarotenedial ( acetate adduct C10 |
4-ketomyxol-2′-fucoside | NosCCD | 3-OH-4-oxo-β-ionone ( Apo-8′-10-apocarotenedial ( |
4-hydroxymyxol-2′-fucoside | NosCCD | 3, 4-OH-β-ionone ( Apo-8′-10-apocarotenedial ( |
Species | Protein | Assay a | Parent Carotenoid | Cleavage Position | Product Detected | References |
---|---|---|---|---|---|---|
Arabidopsis thaliana | CCD4 | in planta | β-carotene, Violaxanthin | n.d. | n.d. | [107] |
in planta | Phytofluene, ζ-carotene | n.d. | n.d. | [135] | ||
in planta (leaf) | Epoxy-β-xanthophylls | C9–C10 or C9′–C10′ | C13-glycosids | [134] | ||
in planta (root) | β-carotene | n.d. | long-chain free apocarotenals (C15 to C30) | [134] | ||
in vitro | Apo-β-caroten-8′-al | C9–C10 | β-ionone | [96] | ||
Brassica napus | CCD4_C3 | in planta | α-carotene, δ-carotene | C9–C10 | α-ionone | [152] |
Chrysantemum morifolium | CCD4a | in vivo and in vitro | β-carotene | C9–C10 (C9′–C10′) | β-ionone | [96] |
Citrus clementina | CCD4b1 | in vitro | β-carotene, β-cryptoxanthin, Zeaxanthin, Lutein, α-carotene | C7–C8 or C7′–C8′ | 3-OH-apo-β-8-carotenal, apo-β-8-carotenal (C30); β-cyclocitral and 3-OH-β-cyclocitral (C10) | [133] |
Citrus unshiu | CCD4 | in vitro and in vivo | β-cryptoxanthin, Zeaxanthin | C7–C8 or C7′–C8′ | 3-OH-apo-β-8-carotenal | [131] |
Crocus sativus | CCD4a/b | in vivo | β-carotene, Zeaxanthin | C9–C10 (C9′–C10′) | β-ionone, β-OH-ionone | [89,147] |
CCD4c | in vivo | β-carotene | C9–C10 or C9′–C10′ | β-ionone, β-cyclocitral | [130] | |
in planta | C7–C8 or C7′–C8′ | |||||
in planta | Lutein | C9–C10 | Megastigma-4,6,8-triene (derived from 3-OH-α-ionone) | [130] | ||
Malus domestica | CCD4 | in vivo | β-carotene | C9–C10 (C9′–C10′) | β-ionone | [96] |
Osmanthus fragans | CCD4 | in vivo | β-carotene | C9–C10 (C9′–C10′) | β-ionone | [96] |
Rosa damascena | CCD4 | in vivo | β-carotene | C9–C10 (C9′–C10′) | β-ionone | [96] |
in vitro | apo-β-8-carotenal | C9–C10 | β-ionone | [96] | ||
Solanum tuberosum | CCD4 | in planta | Violaxanthin | n.d. | n.d. | [150] |
in vitro and in vivo | β-carotene | C9–C10 or C9′–C10′ | Apo-β-caroten-10′-al; β-ionone | [153] | ||
in vitro | α-carotene, Lutein, Zeaxanthin, β-cryptoxanthin | C9–C10 or C9′–C10′ | 3-OH-β-apo-10′-carotenal, β-apo-10′-carotenal3-OH-ε-apo-10´-carotenal | [153] | ||
Vitis vinifera | CCD4a/b | in vivo | ε-carotene, | C9–C10 (C9′–C10′) | α-ionone, | [98] |
CCD4a/b | in vivo | Neurosporene | C9′–C10′ | Geranylacetone | [98] | |
CCD4a/b | in vivo | Lycopene | C5–C6 (C5′–C6′) | 6-methyl-5-hepten-2-one | [98] | |
CCD4b | in vivo | ζ-carotene | C9–C10 (C9′–C10′) | α-ionone, Geranylacetone | [98] |
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Ahrazem, O.; Gómez-Gómez, L.; Rodrigo, M.J.; Avalos, J.; Limón, M.C. Carotenoid Cleavage Oxygenases from Microbes and Photosynthetic Organisms: Features and Functions. Int. J. Mol. Sci. 2016, 17, 1781. https://doi.org/10.3390/ijms17111781
Ahrazem O, Gómez-Gómez L, Rodrigo MJ, Avalos J, Limón MC. Carotenoid Cleavage Oxygenases from Microbes and Photosynthetic Organisms: Features and Functions. International Journal of Molecular Sciences. 2016; 17(11):1781. https://doi.org/10.3390/ijms17111781
Chicago/Turabian StyleAhrazem, Oussama, Lourdes Gómez-Gómez, María J. Rodrigo, Javier Avalos, and María Carmen Limón. 2016. "Carotenoid Cleavage Oxygenases from Microbes and Photosynthetic Organisms: Features and Functions" International Journal of Molecular Sciences 17, no. 11: 1781. https://doi.org/10.3390/ijms17111781
APA StyleAhrazem, O., Gómez-Gómez, L., Rodrigo, M. J., Avalos, J., & Limón, M. C. (2016). Carotenoid Cleavage Oxygenases from Microbes and Photosynthetic Organisms: Features and Functions. International Journal of Molecular Sciences, 17(11), 1781. https://doi.org/10.3390/ijms17111781