Reciprocal regulation of chloroplast protein synthesis and carbon metabolism for thylakoid membrane biogenesis

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Thylakoid membranes represent highly developed sites for photosynthetic energy transduction. Their biogenesis requires the synthesis of both lipids as well as proteins. However, little is known regarding if and how these two biosynthetic pathways are interconnected at the molecular level. The chloroplast pyruvate dehydrogenase complex is well-known to produce activated di-carbon precursor molecules (acetyl-CoA) for fatty acid - and as a consequence - lipid synthesis. Our prework shows that the DLA2 subunit of this enzyme is additionally a component of a ribonculeoprotein complex and as this has a function in the spatial organization of chloroplast mRNA translation in the green algal model system Chlamydomonas reinhardtii. Conversely, RNA binding affects pyruvate dehydrogenase activity. These findings provide a first clue regarding how intraplastidic metabolic signaling and chloroplast gene expression could be reciprocally connected for thylakoid membrane biogenesis. In addition, our data provide first hints that these dual roles of the protein might exist in evolutionary distant organisms ranging from cyanobacteria to humans.In this project, we aim at elucidating the precise molecular working mode of this regulatory principle involving metabolic control of gene expression. By following molecular, genetical, and biochemical approaches in C. reinhardtii, we will use in vivo and in vitro techniques to characterize both the RNA binding and the enzymatic forms of DLA2 which appears to shuttle between different protein sub-complexes. A special focus will be on the dynamics and composition of these complexes and the role of acetate/acetyl-CoA for balancing both functions of DLA2. This work will be complemented by related analyses in cyanobacteria and higher plants, to test for an evolutionary conservation of such a regulatory switch.