Mechanism of plastid division: from a bacterium to an organelle.

Chloroplasts arose more than 1 billion years ago, when a free-living cyanobacterium became an endosymbiont in a eukaryotic host cell. Several lines of evidence indicate that all chloroplasts and their nonphotosynthetic relatives (plastids) are directly or indirectly derived from a single endosymbiotic event (Reyes-Prieto et al., 2007; Gould et al., 2008; Archibald, 2009; Fig. 1). The original endosymbiosis of the cyanobacterium gave rise to plastids (primary plastids) in the Archaeplastida, which are made up of the Glaucophya, Rhodophyta (red algae), and Viridiplantae (green algae and land plants). All other plastids, such as those found in kelps, dinoflagellates, malaria parasites (these three belong to the Chromalveolata), euglenids (Excavata), and chlorarachniophytes (Rhizaria), were established by subsequent endosymbiotic events in which eukaryotic algae had become integrated into other eukaryotes. Recent phylogenetic studies have classified eukaryotes into six supergroups: Amoebozoa, Opisthokonta (fungi and animals), Archaeplastida, Chromalveolata, Excavata, and Rhizaria. Thus, four of the six eukaryotic supergroups possess plastids (Reyes-Prieto et al., 2007; Gould et al., 2008; Archibald, 2009; Fig. 1). The conversion of a cyanobacterium to plastids required several steps (Reyes-Prieto et al., 2007; Gould et al., 2008; Archibald, 2009). Theoretically, a specific relationship developed between an endosymbiont and host, such as a predator-prey relationship. Subsequently, mechanisms controlling metabolic exchange between the two developed. Most of the genes that were once in the endosymbiont genomewere either lost or transferred into the host nuclear genome. As a result, the size of the plastid genome has been reduced to less than one-tenth that of the free-living cyanobacterial genome. Thus, the bulk of the plastid proteome consists of nucleus-encoded proteins that are translated on cytoplasmic ribosomes. In order to translocate proteins from the cytoplasm into chloroplasts, a protein import apparatus was developed at the envelope membrane. In addition, a mechanism that controls endosymbiotic cell division was developed such that each daughter cell would inherit the endosymbiont during cell division. Generally, algal cells contain either a single choloroplast or just a few chloroplasts. Thus, chloroplast division is synchronized with the host cell cycle such that the chloroplast divides before cytokinesis and is thus transmitted into each daughter cell. The requirement of division synchronization is supported by several other endosymbiotic relationships. For example, certain species of heterotrophic dinoflagellates engulf eukaryotic algae and use them as temporary chloroplasts (called “kleptoplasts”) for a period of days to weeks before digesting them. In contrast, a few dinoflagellate species maintain a eukaryotic algal unicell (i.e. containing the nucleus, mitochondria, Golgi apparatuses, etc.) as a permanent endosymbiont by synchronizing the endosymbiont cell division to the host cell cycle (Wouters et al., 2009; Imanian et al., 2010). A similar situation is also observed in other eukaryotic groups.Hatena arenicola has a transient green algal endosymbiont, and this photosynthetic endosymbiont is inherited by only one daughter cell during cell division. Daughter cells that have lost the endosymbiont again engulf the green alga (Okamoto and Inouye, 2005). H. arenicola (Katablepharidophyta) bears a close evolutionary relationship with cryptophytes, in which permanent chloroplasts of a red algal origin have been established by division synchronization (Fig. 1). There are also eukaryotes that possess permanent cyanobacterial endosymbionts, such as Paulinella chromatophora. This endosymbiont is consistently inherited by progeny cells as a consequence of tight synchronization of host and endosymbiotic cell cycles (Melkonian and Mollenhauer, 2005). Currently, it is largely unknown how endosymbiotic cell division is regulated by host cells in the diverse array of endosymbiotic relationships. However, studies over the last decade have rapidly provided information on the mechanism and the regulation of primary chloroplast division (Kuroiwa et al., 2008; Yang et al., 2008; Maple and Møller, 2010; Miyagishima and Kabeya, 2010; Pyke, 2010). In addition, several genome projects on the plastid-carrying eukaryotes have been initiated. These advances promise the eventual understanding of the mechanisms that coordinate the proliferation of both a host cell and an endosymbiont. The mechanism of primary plastid division, especially that of chloroplasts, has been summarized in 1 This work was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (grant no. 22687020). * E-mail [email protected]. www.plantphysiol.org/cgi/doi/10.1104/pp.110.170688