Molecular structure and evolution of chloroplast nucleoids

Abstract

Almost all life on earth depend on photosynthesis performed by chloroplasts of algae and land plants. Chloroplasts possess their own genomic DNA (cpDNA), which are considered as a relic of the endosymbiotic cyanobacterium. A copy of cpDNA encodes ~200 proteins essential for photosynthesis and biogenesis, and are packaged in DNA-protein complex called chloroplast nucleoids (CPNs), a counterpart of nuclear chromosome. However, little is known about the evolution of CPN structure and the molecular mechanism that regulates CPN morphology. To deduce the evolution of CPN structure, we analyzed CPNs of algae and liverwort, and proposed a model that the recurrent modification of CPN organization by eukaryotic factors originally related to chromatin organization likely have been the driving force for the diversification of CPNs since the early stage of plant evolution. We also investigated sulfite reductase (SiR), a major component of CPNs in land plants, to reveal the molecular basis to bind and bend cpDNA. The combination of in silico and in vivo analysis revealed that C-terminally region of SiR (~50 aa) plays a key role to interact and compact cpDNA. Furthermore, we identified the novel gene MOC1, which regulates the CPN morphology in algae and land plants. MOC1 encodes the chloroplast-targeted Holliday junction resolvase, suggesting that MOC1 untangles cpDNA tangled via Holliday junctions to segregate chloroplast genome faithfully.