A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus

Colletti, Kelly; Tattersall, Elizabeth A. R.; Pyke, Kevin; Froelich, John E.; Stokes, Kevin D.; Osteryoung, Katherine W.

doi:10.1016/s0960-9822(00)00466-8

Cited by 193 publications

(201 citation statements)

References 59 publications

(98 reference statements)

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“…However, mitochondrial and chloroplast division are not equivalent processes. Chloroplast division requires the activity of several prokaryotically derived proteins in the chloroplast stroma, including FtsZ1, FtsZ2, MinD, MinE, and ARTEMIS (6,7,(11)(12)(13)(14)49), whereas related molecules are lacking in the mitochondria of animals, plants, and fungi, and no matrix-localized mitochondrial division proteins have been identified in these organisms.…”

Section: Discussionmentioning

confidence: 99%

“…This scenario describes the origin of the five previously identified plastid division proteins in plants, all of which evolved from related cell division proteins in cyanobacteria, are encoded in the nucleus, and are localized inside the chloroplast. These include FtsZ1 and FtsZ2, tubulin-like proteins that localize to a ring at the site of plastid constriction (3-10), MinD and MinE, which regulate placement of the plastid division site (11)(12)(13), and ARTEMIS, which appears to mediate constriction of the envelope membranes (14).…”

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ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery

Gao

Kadirjan-Kalbach

Froehlich

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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Chloroplast division in plant cells is orchestrated by a complex macromolecular machine with components positioned on both the inner and outer envelope surfaces. The only plastid division proteins identified to date are of endosymbiotic origin and are localized inside the organelle. Employing positional cloning methods in Arabidopsis in conjunction with a novel strategy for pinpointing the mutant locus, we have identified a gene encoding a new chloroplast division protein, ARC5. Mutants of ARC5 exhibit defects in chloroplast constriction, have enlarged, dumbbellshaped chloroplasts, and are rescued by a wild-type copy of ARC5. The ARC5 gene product shares similarity with the dynamin family of GTPases, which mediate endocytosis, mitochondrial division, and other organellar fission and fusion events in eukaryotes. Phylogenetic analysis showed that ARC5 is related to a group of dynamin-like proteins unique to plants. A GFP-ARC5 fusion protein localizes to a ring at the chloroplast division site. Chloroplast import and protease protection assays indicate that the ARC5 ring is positioned on the outer surface of the chloroplast. Thus, ARC5 is the first cytosolic component of the chloroplast division complex to be identified. ARC5 has no obvious counterparts in prokaryotes, suggesting that it evolved from a dynamin-related protein present in the eukaryotic ancestor of plants. These results indicate that the chloroplast division apparatus is of mixed evolutionary origin and that it shares structural and mechanistic similarities with both the cell division machinery of bacteria and the dynamin-mediated organellar fission machineries of eukaryotes.T he chloroplasts of plants and algae are widely believed to have evolved only once from a free-living cyanobacterial endosymbiont (1). Over evolutionary time, many of the genes once present in the endosymbiont have been transferred to the nuclear genome where they have acquired sequences encoding transit peptides that direct their gene products back to the chloroplast (1, 2). This scenario describes the origin of the five previously identified plastid division proteins in plants, all of which evolved from related cell division proteins in cyanobacteria, are encoded in the nucleus, and are localized inside the chloroplast. These include FtsZ1 and FtsZ2, tubulin-like proteins that localize to a ring at the site of plastid constriction (3-10), MinD and MinE, which regulate placement of the plastid division site (11-13), and ARTEMIS, which appears to mediate constriction of the envelope membranes (14).Despite localization of the previously identified plastid division proteins inside the chloroplasts in plant cells, ultrastructural studies have shown that plastid division entails the coordinated activity of components localized outside as well as inside the organelle. In plants, the chloroplast division complex comprises electron-dense structures situated both on the stromal surface of the inner envelope membrane and on the cytosolic surface of the outer membrane (15). These structur...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery

Gao

Kadirjan-Kalbach

Froehlich

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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253

254

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“…An additional homologue of FtsZ that is distinct from FtsZ1 and FtsZ2, but is still related to cyanobacterial FtsZs, is also present in plastids of primitive algae. Homologues of cyanobacterial MinD and MinE proteins are found in plants, and are required for the proper localization of plastid Z rings in Arabidopsis thaliana 108,109 , which indicates that the function of MinD and MinE in the spatial regulation of plastid Z rings has been conserved. Nevertheless, no homologues of MinC have been found in plants, so the factor that negatively regulates FtsZ assembly through MinD in plastids is not yet known.…”

Section: Ftsz and Organelle Division Plastid Divisionmentioning

confidence: 99%

FtsZ and the division of prokaryotic cells and organelles

Margolin

2005

Nat Rev Mol Cell Biol

560

484

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Binary fission of many prokaryotes as well as some eukaryotic organelles depends on the FtsZ protein, which self-assembles into a membrane-associated ring structure early in the division process. FtsZ is homologous to tubulin, the building block of the microtubule cytoskeleton in eukaryotes. Recent advances in genomics and cell-imaging techniques have paved the way for the remarkable progress in our understanding of fission in bacteria and organelles.Duplication of cells occurs by the division of a mother cell into two daughter cells. This process, known as cytokinesis, provides the force to split cells and is spatially regulated to faithfully partition the genetic material. The cytoskeleton has a crucial role in cytokinesis. In animal and fungal cells, a medial ring of actin and myosin, helped by other proteins, contracts to divide the cell. Plant cells use a cell plate, and are guided by actin filaments and microtubules. Prokaryotes, which include bacteria and archaea, possess homologues of eukaryotic cytoskeletal proteins. Most prokaryotes use a tubulin homologue, a protein known as FtsZ, to divide. Eukaryotic organelles such as chloroplasts and mitochondria evolved from bacteria, and all chloroplasts and some mitochondria use FtsZ to divide.FtsZ is thought to be the first protein to localize to the site of future division in bacteria 1 , and it assembles into what is known as the Z ring (FIG. 1). In Escherichia coli, the Z ring recruits at least ten other proteins, all of which are required for the progression and completion of cytokinesis 2 , as will be discussed below. Whereas the cytokinetic apparatus in eukaryotic cells and even organelles can be observed directly in stained thin sections by transmission electron microscopy, the Z ring and its associated factors are not detectable by these methods. This is probably because the protein machinery is largely membrane bound and resides in a densely populated cytoplasmic environment. However, the development of green fluorescent protein (GFP) fusion and improved immunofluorescence techniques over the past 10 years have been crucial in allowing the first direct visualization of many cellular components and their dynamics. For example, using GFP fusions, the dynamics of the Z ring and other components of the cell-division protein machinery can now be visualized in living bacterial cells. The combination of these new cytological tools with genomics and the Competing interests statementThe author declares no competing financial interests. HHS Public Access Author Manuscript Author ManuscriptAuthor ManuscriptAuthor Manuscript already powerful genetics of several model systems have spurred rapid progress in our understanding of the molecular cell biology of bacteria and eukaryotic organelles. This review will discuss how the recent revolutions in genomics and cell biology have provided new evolutionary and mechanistic insights into how bacterial cells and organelles divide. The FtsZ family of proteins Conservation of FtsZFtsZ is a highly conserved protein ...

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“…The first step seems to be the polymerization of AtFtsZ at the division site, forming the Z-ring , probably stabilized by ARC6, a DnaJ domain protein (Vitha et al, 2003). Like in bacteria (Justice et al, 2000), establishment of the proper division site is mediated by AtMinD and AtMinE (Colletti et al, 2000;Itoh et al, 2001). Then, sequential assembly of the inner and outer plastid division rings (PD ring) follows.…”

Section: Introductionmentioning

confidence: 99%

An Arabidopsis Homolog of the Bacterial Cell Division Inhibitor SulA Is Involved in Plastid Division[W]

et al. 2004

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Plastids have evolved from an endosymbiosis between a cyanobacterial symbiont and a eukaryotic host cell. Their division is mediated both by proteins of the host cell and conserved bacterial division proteins. Here, we identified a new component of the plastid division machinery, Arabidopsis thaliana SulA. Disruption of its cyanobacterial homolog (SSulA) in Synechocystis and overexpression of an AtSulA-green fluorescent protein fusion in Arabidopsis demonstrate that these genes are involved in cell and plastid division, respectively. Overexpression of AtSulA inhibits plastid division in planta but rescues plastid division defects caused by overexpression of AtFtsZ1-1 and AtFtsZ2-1, demonstrating that its role in plastid division may involve an interaction with AtFtsZ1-1 and AtFtsZ2-1.

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A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus

Cited by 193 publications

References 59 publications

ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery

ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery

FtsZ and the division of prokaryotic cells and organelles

An Arabidopsis Homolog of the Bacterial Cell Division Inhibitor SulA Is Involved in Plastid Division[W]

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