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

Abstract

Apocarotenoids are carotenoid-derived compounds widespread in all major taxonomic groups, where they play important roles in different physiological processes. In addition, apocarotenoids include compounds with high economic value in food and cosmetics industries. Apocarotenoid biosynthesis starts with the action of carotenoid cleavage dioxygenases (CCDs), a family of non-heme iron enzymes that catalyze the oxidative cleavage of carbon-carbon double bonds in carotenoid backbones through a similar molecular mechanism, generating aldehyde or ketone groups in the cleaving ends. From the identification of the first CCD enzyme in plants, an increasing number of CCDs have been identified in many other species, including microorganisms, proving to be a ubiquitously distributed and evolutionarily conserved enzymatic family. This review focuses on CCDs from plants, algae, fungi, and bacteria, describing recent progress in their functions and regulatory mechanisms in relation to the different roles played by the apocarotenoids in these organisms.

Keywords: algae; apocarotenoids; bacteria; carotenoid cleavage dioxygenase; fungi; plants.

Figure 1

Tridimensional models of 12 carotenoid-cleavage dioxygenases from all the subfamilies included in this review. The VP14 (PBD: 2biwA) structure from maize has been used as a template. (A) Side view of CCDs with β-strands shown in yellow, α-helices in magenta, and loops in grey; (B) Top view rotated 90° towards the viewer from (A); (C) Lateral and top views of CCD2, CCD8, and ACO showing Fe²⁺ ion in green and histidines in blue. Accession numbers are: VP14: O24592.2, ACOX, P74334; AtCCD1, O65572; AtCCD7, AEC10494.1; AtCCD8, Q8VY26; AtCCD4: O49675; Cao-2, XP001727958.1; CarS, ADU04395.1; CarX, CAH70723.1; CsCCD2L, ALM23547.1; CcCCD4b1, XP006424046; AcaA, 77754.

Figure 1

Tridimensional models of 12 carotenoid-cleavage dioxygenases from all the subfamilies included in this review. The VP14 (PBD: 2biwA) structure from maize has been used as a template. (A) Side view of CCDs with β-strands shown in yellow, α-helices in magenta, and loops in grey; (B) Top view rotated 90° towards the viewer from (A); (C) Lateral and top views of CCD2, CCD8, and ACO showing Fe²⁺ ion in green and histidines in blue. Accession numbers are: VP14: O24592.2, ACOX, P74334; AtCCD1, O65572; AtCCD7, AEC10494.1; AtCCD8, Q8VY26; AtCCD4: O49675; Cao-2, XP001727958.1; CarS, ADU04395.1; CarX, CAH70723.1; CsCCD2L, ALM23547.1; CcCCD4b1, XP006424046; AcaA, 77754.

Figure 2

Enzymatic reactions achieved by fungal CCDs. (A) Retinal production from β-carotene by the Cco1 (Ustilago maydis) and CarX (F. fujikuroi) CCDs; (B) β-apo-4′-carotenal production from torulene by the CarT (F. fujikuroi) and Cao-2 (N. crassa) CCDs; (C) β-apo-13-carotenone production from β-carotene by the sequential cleavage by the CarS and AcaA CCDs (P. blakesleeanus). Cleavage sites are shaded and indicated by an arrow.

Figure 3

Activity of plant CCD1 and CCD2 subfamilies, showing their divergence in substrate specificity and cleavage sites on the following substrates: (A) ζ-carotene and lycopene; (B) β-carotene; and (C) zeaxantine. Symbols indicate double bonds where oxygenases cleave. : C5–C6; : C7–C8; : C9–C10 and C9′–C10′; : C13–C14; : C13′–C14′; : C11′–C12′.

Figure 4

Biosynthetic pathway of strigolactones (SLs) from β-carotene.