Abstract
The profile of secondary metabolites in plants reflects the balance of biosynthesis, degradation and storage, including the availability of precursors and products that affect the metabolic equilibrium. We investigated the impact of the precursor-product balance on the carotenoid pathway in the endosperm of intact rice plants because this tissue does not normally accumulate carotenoids, allowing us to control each component of the pathway. We generated transgenic plants expressing the maize phytoene synthase gene (ZmPSY1) and the bacterial phytoene desaturase gene (PaCRTI), which are sufficient to produce β-carotene in the presence of endogenous lycopene β-cyclase. We combined this mini-pathway with the Arabidopsis thaliana genes AtDXS (encoding 1-deoxy-D-xylulose 5-phosphate synthase, which supplies metabolic precursors) or AtOR (the ORANGE gene, which promotes the formation of a metabolic sink). Analysis of the resulting transgenic plants suggested that the supply of isoprenoid precursors from the MEP pathway is one of the key factors limiting carotenoid accumulation in the endosperm and that the overexpression of AtOR increased the accumulation of carotenoids in part by up-regulating a series of endogenous carotenogenic genes. The identification of metabolic bottlenecks in the pathway will help to refine strategies for the creation of engineered plants with specific carotenoid profiles.
Highlights
Plants synthesize a wide variety of natural products via complex secondary metabolic pathways (Miralpeix et al, 2013; Rischer et al, 2013)
The hpt gene was expressed constitutively, whereas Arabidopsis thaliana 1-deoxy-D-xylulose-5-phosphate synthase (AtDXS), ZmPSY1 and Pantoea ananatis CRTI (PaCRTI) were controlled by the endosperm-specific rice RP5 prolamin, wheat low-molecular-weight glutenin and barley D-hordein promoters, respectively
Our experiments revealed that AtDXS and A. thaliana ORANGE (AtOR) regulate different sets of endogenous carotenogenic genes, suggesting they boost carotenoid accumulation via distinct mechanisms
Summary
Plants synthesize a wide variety of natural products via complex secondary metabolic pathways (Miralpeix et al, 2013; Rischer et al, 2013). Many technical challenges must be overcome before multistep secondary metabolic pathways can be engineered effectively in heterologous plants. The endosperm of cereal seeds is a major food staple, but it is deficient in many vitamins and minerals, including carotenoids (Zhu et al, 2007, 2008). Rice (Oryza sativa) is an important food staple in developing countries, but carotenoids do not accumulate in the endosperm, so its consumption as part of a nondiverse diet is often associated with vitamin A deficiency (Farre et al, 2010; Underwood and Arthur, 1996)
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