Mutant-Based Model of Two Independent Pathways for Carotenoid-Mediated Chloroplast Biogenesis in Arabidopsis Embryos

Chloroplasts are essential for autonomous plant growth, and their biogenesis is a complex process requiring both plastid and nuclear genome. One of the essential factors required for chloroplast biogenesis are carotenoids. Carotenoids are synthesized in plastids, and it was shown that plastid localized methylerythritol 4-phosphate (MEP) pathway provides substrates for their biosynthesis. Here, we propose a model, using results of our own mutant analysis combined with the results of others, that a MEP-independent pathway, likely a mevalonate (MVA)-dependent pathway, provides intermediates for chloroplast biogenesis in Arabidopsis embryos. The pattern of this chloroplast biogenesis differs from the MEP-dependent chloroplast biogenesis. In MEP-dependent chloroplast biogenesis, chloroplasts are formed rather uniformly in the whole embryo, with stronger chlorophyll accumulation in cotyledons. In a MEP-independent pathway, chloroplasts are formed predominantly in the hypocotyl and in the embryonic root. We also show that this pattern of chlorophyll accumulation is common to MEP pathway mutants as well as to the mutant lacking geranylgeranyl diphosphate synthase 11 (GGPPS11) activity in plastids but expressing it in the cytosol (GGPPS11cyt). It was recently described that shorter GGPPS11 transcripts are present in Arabidopsis, and they can be translated into active cytosolic proteins. We therefore propose that the MEP-independent pathway for chloroplast biogenesis in Arabidopsis embryos is an MVA pathway that provides substrates for the synthesis of GGPP via GGPPS11cyt and this is then transported to plastids, where it is used for carotenoid biosynthesis and subsequently for chloroplast biogenesis mainly in the hypocotyl and in the embryonic root.