Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis

Post-endosymbiotic evolution of chloroplasts was characterized by a massive transfer of cyanobacterial genes to the nucleus, followed by re-routing of many of their encoded proteins. In consequence, most plastid proteins are nucleus-encoded, enabling an anterograde (nucleus-to-plastid) control of the organelle. The regulation of chloroplast functions includes also cross-talk between chloroplasts and mitochondria, as well as retrograde (plastid-to-nucleus) signalling. Genetic analyses reveal that redox state, flux through the chlorophyll biosynthetic pathway, sugar sensing and reactive oxygen species contribute to retrograde signalling. However, the identity of the messenger molecule(s) remains largely unknown. Novel facets of the chloroplast-mitochondrion cross-talk have been revealed by the characterization of mitochondrial mutants affected in chloroplast properties. Studies of the nuclear chloroplast transcriptome imply the existence of at least three distinct types of transcriptional regulation: a master switch, acting in a binary mode by either inducing or repressing the same large set of genes; a “mixed response” with about equal numbers of up- and down-regulated genes; and mechanisms supporting the specific co-regulation of nuclear genes for photosynthesis and for plastid gene expression. The recent discovery of the latter mode of control highlights a possibly ancient route to co-ordinate chloroplast and nuclear genome expression.