Chloroplast Division

Abstract

Chloroplasts are descendants of cyanobacteria and divide by binary fission. Several components of the division apparatus have been identified in the past several years and we are beginning to appreciate the plastid division process at a mechanistic level. In this review, we attempt to summarize the most recent developments in the field and assemble these observations into a working model of plastid division in plants. Plastids: Characteristics, Origins and DistributionWithout chloroplasts, plant and animal life would not exist. Plastids have been studied most extensively with regard to their role in photosynthesis, and are essential to the plant itself, being required for a select of amino acid and lipid metabolism, assimilation of nitrogen and sulfur into organic compounds, signaling in response to environmental cues and biosynthesis of plant hormones (1)(2)(3)(4)(5). Despite all we have learned over the past century regarding this organelle, we still know relatively little about its replication-which, superficially, seems a simple process of binary fission. Because plastid division and biogenesis are an integral part of plant growth and development, understanding of the division process is paramount to our understanding of plant and organelle biology.Plastids arose from an endosymbiotic relationship between a primitive biciliate protozoan and an ancient cyanobacterium that began 1.2-1.5 billion years ago (Figure 1) (6,7). Initially, each partner derived some mutual benefit: the cyanobacterium occupied and exploited an untapped protective niche and the host extracted reduced carbon and other nutrients from its new tenant. Time, selective pressure and mutation bring us to the present day where the chloroplast is a prisoner in its own home, having lost more than 90% of the gene content present in its free-living ancestor. Most of the plastid division genes identified to date are cyanobacterial in origin and encode division proteins localized inside the organelle. These are directed to the plastid post-translationally by N-terminal transit peptides that are cleaved upon import. A few components of the division complex were invented by the host after endosymbiosis and function on the surface of the organelle in contact with the cytosol; the mechanisms targeting these proteins to the chloroplast surface are unknown. In land plants, all known plastid division genes reside in the nucleus-none are found in the plastid genome-although in at least one unicellular green alga two plastid division genes remain associated with the plastid genome (8).The terms chloroplast and plastid are often used interchangeably, but in vascular plants chloroplasts are actually a subset of plastids, each of which is specialized for a given set of functions within a specific cell type. All plastids are surrounded by two envelope membranes and are derived by division from a population of proplastids within the meristematic (stem) cells of the plant. Beyond land plants, red algae, green algae and diatoms also contain plastids. Even apicomplex...

Two Mechanosensitive Channel Homologs Influence Division Ring Placement in Arabidopsis Chloroplasts

“…Most wild-type chloroplasts contained only one Z-ring, though occasionally more were observed ( Figure 1C). By contrast, msl2 msl3 mutant chloroplasts frequently contained multiple Z-rings, some with a disorganized, forked appearance, similar to those observed in the arc11, arc3, mcd1, and parc6 mutants but distinct from those observed in other plastid division mutants, such as arc5, plastid division1 plastid division2 (pdv1 pdv2), or arc2 (Vitha et al, 2003;Miyagishima et al, 2006;Glynn et al, 2007Glynn et al, , 2009Fujiwara et al, 2008;Nakanishi et al, 2009a;Suzuki et al, 2009).…”

“…Conversely, At-MinE antisense suppression lines and two mutant alleles of At-MinE, minE1 and arc12, exhibit grossly enlarged chloroplasts containing numerous short FtsZ filaments (Glynn et al, 2007;Fujiwara et al, 2008). In summary, multiple lines of evidence indicate that, similar to their bacterial homologs, At-MinD and At-MinE antagonistically regulate Z-ring assembly (Itoh et al, 2001;Maple et al, 2002;Reddy et al, 2002;Fujiwara et al, 2004;Glynn et al, 2007;Maple and Møller, 2007b;Fujiwara et al, 2008).…”

“…Arabidopsis ARC3, a stromal protein that contains an incomplete FtsZ-like region, has been reported to interact directly with MinD, MinE, and FtsZ and copurify with FtsZ1, FtsZ2, and ARC6 Maple et al, 2007;McAndrew et al, 2008). arc3 mutants resemble arc11 mutants in that they exhibit enlarged chloroplasts and multiple FtsZ rings Shimada et al, 2004;Glynn et al, 2007;Maple et al, 2007). No MinC homolog has been identified in plants, though FtsZ assembly is sensitive to overexpression of E. coli MinC, suggesting that the system is capable of responding to MinC activity (Tavva et al, 2006).…”

“…Arabidopsis MinD antisense lines and a lossof-function allele of MinD, accumulation and replication of chloroplasts11 (arc11), exhibit enlarged chloroplasts with multiple Z-rings, suggesting that At-MinD behaves as a Z-ring assembly inhibitor (Colletti et al, 2000;Kanamaru et al, 2000;Vitha et al, 2003;Fujiwara et al, 2004). Conversely, At-MinE antisense suppression lines and two mutant alleles of At-MinE, minE1 and arc12, exhibit grossly enlarged chloroplasts containing numerous short FtsZ filaments (Glynn et al, 2007;Fujiwara et al, 2008). In summary, multiple lines of evidence indicate that, similar to their bacterial homologs, At-MinD and At-MinE antagonistically regulate Z-ring assembly (Itoh et al, 2001;Maple et al, 2002;Reddy et al, 2002;Fujiwara et al, 2004;Glynn et al, 2007;Maple and Møller, 2007b;Fujiwara et al, 2008).…”

GTP-dependent Heteropolymer Formation and Bundling of Chloroplast FtsZ1 and FtsZ2

“…This would further imply that chloroplast Z ring dynamics should be regulated in part by factors that inhibit protofilament bundling. One candidate for such a factor is the chloroplast division protein ARC3, a proposed functional replacement for bacterial MinC (46,54), which was recently shown to inhibit lateral interactions between EcFtsZ protofilaments assembled in vitro (55).…”