cis-carotene biosynthesis, evolution and regulation in plants: The emergence of novel signaling metabolites

Abstract Carotenoids are isoprenoid pigments synthesised by plants, algae, photosynthetic bacteria as well as some non-photosynthetic bacteria, fungi and insects. Abundant carotenoids found in nature are synthesised via a linear route from phytoene to lycopene after which the pathway bifurcates into cyclised α- and β-carotenes. Plants evolved additional steps to generate a diversity of cis -carotene intermediates, which can accumulate in fruits or tissues exposed to an extended period of darkness. Enzymatic or oxidative cleavage, light-mediated photoisomerization and histone modifications can affect cis -carotene accumulation. cis -carotene accumulation has been linked to the production of signaling metabolites that feedback and forward to regulate nuclear gene expression. When cis -carotenes accumulate, plastid biogenesis and operational control can become impaired. Carotenoid derived metabolites and phytohormones such as abscisic acid and strigolactones can fine-tune cellular homeostasis. There is a hunt to identify a novel cis -carotene derived apocarotenoid signal and to elucidate the molecular mechanism by which it facilitates communication between the plastid and nucleus. In this review, we describe the biosynthesis and evolution of cis -carotenes and their links to regulatory switches, as well as highlight how cis -carotene derived apocarotenoid signals might control organelle communication, physiological and developmental processes in response to environmental change.