In aphids, at least one of the carotenoid synthesis genes is active because a spontaneous point mutation in a copy of a phytoene desaturase is associated with loss of red body color ( 11). In fungi, cyclase/synthase fusion proteins and phytoene desaturases are required for the synthesis of carotenes, including β-carotene ( 21), a provitamin A carotenoid and a substrate for the biosynthesis of diverse xanthophylls ( 7, 22). The cyclase/synthase fusions suggested a fungal origin of the lateral transfer events, a conclusion confirmed by phylogenetic analyses ( 11, 18– 20). In all cases, the laterally transferred genes consisted of fused cyclase/synthases and phytoene desaturases. Subsequently, carotenoid biosynthetic genes were identified in other Hemiptera, the adelgids ( 17), and in two other arthropod lineages, gall midges (Insecta, Diptera) ( 18) and spider mites (in Tetranychus urticae, a member of Chelicerata, the sister taxon to the mandibulate arthropods) ( 19, 20). This thinking changed when Moran and Jarvik ( 11) discovered that the pea aphid ( Acyrthosiphon pisum) genome harbors carotenoid biosynthetic genes acquired by horizontal gene transfer. Until recently, all animals were thought to lack the ability to synthesize carotenoids de novo. Finally, carotenoids, such as lutein and zeaxanthin in human and keto-carotenoids like astaxanthin in other organisms, have been postulated to serve important roles as antioxidants ( 14, 15).ĭespite their ubiquity and essential functions, relatively little is known in animals about carotenoid uptake, transport, and metabolism ( 8), which contrasts with endogenously synthesized pigments like melanin, for which dozens of genes in the pathway for synthesis and distribution have been characterized ( 8, 16). ![]() Further, carotenoids, including β-carotene, are processed in animals to chromophores, including retinal (vitamin A), that, in complexes with opsins, are the chemical transducers in vision ( 2, 12, 13). Many animals are also able to modify carotenes to produce their own brightly colored xanthophylls, and, collectively, carotenoids underlie many of the striking yellows, oranges, and reds observed in the animal kingdom ( 8), including feather and beak colors in birds ( 9, 10), as well as body and cocoon colors in insects ( 8, 11). Most animals obtain carotenoids from their diet, including carotenes (hydrocarbon carotenoids), like β-carotene, and xanthophylls (carotenoids with oxygen, like lutein or astaxanthin) ( 7). In animals, carotenoids are widespread and have diverse roles, including signaling to conspecifics and protection from oxidative stress ( 2– 6). Over 700 structures are found in nature, reflecting modifications to the C 40 backbone, such as cyclization or the addition of oxygen-containing groups ( 1, 2). Carotenoid biosynthetic genes of fungal origin have therefore enabled some mites to forgo dietary carotenoids, with endogenous synthesis underlying their intense pigmentation and ability to enter diapause, a key to the global distribution of major spider mite pests of agriculture.Ĭarotenoids are isoprenoid compounds produced by photosynthetic organisms, like plants, as well as by some bacteria, Archaea, and fungi ( 1). urticae, consistent with a role for this enzyme in provisioning provitamin A carotenoids required for light perception. ![]() Further, we show that phytoene desaturase activity is essential for photoperiodic induction of diapause in an overwintering strain of T. Using a combination of genetic approaches, we show that mutations in a single horizontally transferred phytoene desaturase result in complete albinism in the two-spotted spider mite, Tetranychus urticae, as well as in the citrus red mite, Panonychus citri. Pigmentation in spider mites results solely from carotenoids. The finding of horizontal gene transfers of carotenoid biosynthetic genes to three arthropod lineages was unprecedented however, the relevance of the transfers for the arthropods that acquired them has remained largely speculative, which is especially true for spider mites that feed on plant cell contents, a known source of carotenoids. Recently, sequencing projects in aphids and adelgids, spider mites, and gall midges identified genes with homology to fungal sequences encoding de novo carotenoid biosynthetic proteins like phytoene desaturase. Most animals acquire carotenoids from their diets because de novo synthesis of carotenoids is primarily limited to plants and some bacteria and fungi. Carotenoids underlie many of the vibrant yellow, orange, and red colors in animals, and are involved in processes ranging from vision to protection from stresses.
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