The evolution of the regulatory mechanism of chloroplast division

Abstract

Chloroplasts arose from a cyanobacterial endosymbiont and multiply by division, reminiscent of their free-living ancestor. However, chloroplasts can not divide by themselves, and the division is performed and controlled by proteins that are encoded by the host nucleus. The continuity of chloroplasts was originally established by synchronization of endosymbiotic cell division with host cell division, as seen in existent algae. In contrast, land plant cells contain multiple chloroplasts, the division of which is not synchronized, even in the same cell. Land plants have evolved cell and chloroplast differentiation systems in which the size and number of chloroplasts (or other types of plastids) change along with their respective cellular function by changes in the division rate. We recently reported that PLASTID DIVISION (PDV) proteins, land-plant specific components of the chloroplast division apparatus, determined the rate of chloroplast division. The level of PDV protein is regulated by the cell differentiation program based on cytokinin, and the increase or decrease of the PDV level gives rise to an increase or decrease in the chloroplast division rate. Thus, the integration of PDV proteins into the chloroplast division machinery enabled land plant cells to change chloroplast size and number in accord with the fate of cell differentiation.

Figure 1

Evolution of the chloroplast division machinery. The division complex of algae and land plants include FtsZ and ARC 6, both of which are descended from the cell division machinery of cyanobacteria. DR P5B was added after endosymbiosis. PDV2 was acquired by a common ancestor of land plants. PDV1 and PARC 6 emerged by gene duplication of PDV2 and ARC 6, respectively, in a common ancestor of vascular plants (Ferns and seed plants). The site of the FtsZ ring formation is determined by the MinD and MinE proteins which are descended from cyanobacteria, the ARC 3 protein which is specific to green algae and land plants, and land-plant specific protein MCD1. The inset diagram shows the pathway of chloroplast division complex assembly in green algae and land plants.

Figure 2

Regulation of the chloroplast division in algae and land plants. (A) The chloroplast divides once per host cell cycle in algae. Components of the chloroplast division machinery are expressed in a specific phase of the host cell cycle. (B) The rate of the chloroplast division changes during cell differentiation in land plants. In angiosperms, proplastids actively divide in the meristematic cells, while the division rate slows down as leaves and chloroplasts mature. The PDV level, but not that of the other division components, decreases in parallel with the division rate.