The plastid is a semiautonomous organelle essential in photosynthesis and other metabolic activities of plants and algae. Plastid DNA is organized into the nucleoid with various proteins and RNA, and the nucleoid is subject to dynamic changes during the development of plant cells. Characterization of the major DNA-binding proteins of nucleoids revealed essential differences in the two lineages of photosynthetic eukaryotes, namely nucleoids of green plants contain sulfite reductase as a major DNA-binding protein that represses the genomic activity, whereas the prokaryotic DNA-binding protein HU is abundant in plastid nucleoids of the rhodophyte lineage. In addition, current knowledge on DNA-binding proteins, as well as the replication and transcription systems of plastids, is reviewed from comparative and evolutionary points of view. A revised hypothesis on the discontinuous evolution of plastid genomic machinery is presented: despite the cyanobacterial origin of plastids, the genomic machinery of the plastid genome is fundamentally different from its counterpart in cyanobacteria.