Carotenoids in nature: insights from plants and beyond

Carotenoids are natural isoprenoid pigments that provide leaves, fruits, vegetables and flowers with distinctive yellow, orange and some reddish colours as well as several aromas in plants. Their bright colours serve as attractants for pollination and seed dispersal.Carotenoids comprise a large family ofC40 polyenes and are synthesised by all photosynthetic organisms, aphids, some bacteria and fungi alike. In animals carotenoid derivatives promote health, improve sexual behaviour and are essential for reproduction. As such, carotenoids are commercially important in agriculture, food, health and the cosmetic industries. In plants, carotenoids are essential components required for photosynthesis, photoprotection and the production of carotenoid-derived phytohormones, including ABA and strigolactone. The carotenoid biosynthetic pathway has been extensively studied in a range of organisms providing an almost complete pathway for carotenogenesis. A new wave in carotenoid biology has revealed implications for epigenetic and metabolic feedback control of carotenogenesis. Developmental and environmental signals can regulate carotenoid gene expression thereby affecting carotenoid accumulation. This review highlights mechanisms controlling (1) the first committed step in phytoene biosynthesis, (2) flux through the branch to synthesis of aand b-carotenes and (3) metabolic feedback signalling within and between the carotenoid, MEP and ABA pathways. Additional keywords: abscisic acid, apocarotenoids, carotenoid, chloroplast, chromatin, epigenetic, hormones, isoprenoid, metabolic feedback, plant, photoisomerisation, regulation, signal molecule, strigolactone. Received 19 August 2011, accepted 30 August 2011, published online 18 October 2011 Functions for carotenoids in nature Vitamins, antioxidants and spices Animals are generally unable to synthesise carotenoids and require a dietary intake of plant products to meet daily health demands. There are exceptions such as the synthesis of carotenoids in human protist parasites (e.g. Plasmodium and Toxoplasma) and aphids, which can be explained by the existence of a remnant plastid and lateral gene transfer of carotenoid biosynthesis genes from a fungus, respectively (Tonhosolo et al. 2009; Moran and Jarvik 2010). In most animals, dietary carotenoids are cleaved to provide precursors for vitamin A biosynthesis (of which a deficiency leads to blindness) and are valuable for many physiological functions and thus promote human health (e.g. antioxidant activity, immunostimulants, yolk nourishment to embryos, photoprotection, visual tuning as well as limiting agerelated macular degeneration of the eye) (Johnson 2002; Krinsky and Johnson 2005). A deficiency in vitamin A is responsible for child (and maternal) mortality and it is estimated that a 23–34% reduction in preschool mortality can be expected from vitamin A program reaching children in undernourished settings (The State of the World’s Children, UNICEF, www.un.org/en/mdg/ summit2010, accessed 19 August 2011). The development of high yielding b-carotene crops such as ‘golden rice’ could provide close to the recommended daily allowance of vitamin A for malnourished children and help combat vitamin A deficiency-induced mortality and morbidity (Fig. 1) (www. goldenrice.org, accessed 19 August 2011). The nutraceutical industry synthetically manufactures five major carotenoids on an industrial scale (e.g. lycopene, b-carotene, canthaxanthin, zeaxanthin and astaxanthin) for use in a range of food products and cosmetics, such as vitamin supplements and health products and as feed additives for poultry, livestock, fish and crustaceans (reviewed by Del Campo et al. 2007; Jackson et al. 2008). One of the most commercially valuable pigments, astaxanthin, is primarily synthesised by marine microorganisms, such as the green alga Haematococcus pluvialis and accumulates in fish such as salmon, thus, colouring their flesh red. Astaxanthin has been implicated as a potential therapeutic agent treating cardiovascular disease and prostatic cancer (Fassett and Coombes 2011). CSIRO PUBLISHING Goldacre Review Functional Plant Biology, 2011, 38, 833–847 www.publish.csiro.au/journals/fpb This compilation CSIRO 2011 http://dx.doi.org/10.1071/FP11192 Carotenoids accumulate in light exposed tissues, such as skin and as such have gained increased value in the cosmetic industries as suitable compounds for photoprotection due to their scavenging action on reactive oxygen species (ROS) and antiinflammatory properties (Stahl and Sies 2007). Photo-oxidative damage affects cellular lipids, proteins and DNA and is involved in the patho-biochemistry of erythema formation, premature aging of the skin, development of photodermatoses and skin cancer. Evidence shows that b-Carotene, lutein and perhaps even lycopene, can prevent UV-induced erythema formation and contribute to life-long protection against exposure to harmful affects of sunlight (Stahl and Sies 2007). Apocarotenoids are also highly valued as additives in the food industry. Spices such as bixin (annatto), a red-collared, dicarboxylic monomethyl ester apocarotenoid is traditionally derived from the plant Bixa orellana (also known as achiote). Saffron comes from the thread-like reddish coloured female reproductive organs of the Crocus sativa flower (petals are coloured light purple), which is considered one of the worlds most expensive spices andwidely used as a natural colourant. The OH O Retonic Acid CH3 H3C CH3 CH3 CH3 Nutrition and human health Behavior, reproduction and survival Photosynthesis and photoprotection Hormones and signaling molecules COOH O OH