Novel Insights into the Contribution of Plastoglobules and Reactive Oxygen Species to Chromoplast Differentiation

Enriching plant tissues in phytonutrients can be done by stimulating their biosynthesis but also by providing appropriate sink structures for their sequestering and storage. Chromoplasts are plastids specialized in the production and accumulation of carotenoids that are naturally formed in non-photosynthetic tissues such as flower petals and ripe fruit. Chromoplasts can also be artificially differentiated from leaf chloroplasts by boosting the production of phytoene (the first committed intermediate of the carotenoid pathway) with the bacterial phytoene synthase crtB. Here we show that crtB-induced leaf chromoplasts develop plastoglobules harboring high levels of carotenoids (mainly phytoene and pro-vitamin A β-carotene) but also other nutritionally-relevant isoprenoids such as tocopherols (vitamin E) and phylloquinone (vitamin K1). Further promoting plastoglobule proliferation by exposure to intense (high) light resulted in a higher accumulation of these health-related metabolites but also an acceleration of the chloroplast-to-chromoplast conversion. We further show that production of reactive oxygen species (ROS) stimulates chromoplastogenesis. Our data suggest that, similar to that already described for decreased photosynthesis and enhanced carotenoid biosynthesis, ROS production is not just a consequence but a promoter of the chromoplast differentiation process.