The timing and manner of disassembly of the apparatuses for chloroplast and mitochondrial division in the red alga Cyanidioschyzon merolae

Miyagishima, Shin-ya; Kuroiwa, Haruko; Kuroiwa, Tsuneyoshi

doi:10.1007/s004250000426

“…Some of these morphological changes have been reported in Chlorophyta (Chida and Ueda, 1991;Ogawa et al, 1995). The differences among the three rings suggest that the protein compositions of the rings are different (Miyagishima et al, 2001). …”

mentioning

confidence: 73%

“…The inner and middle rings disassemble in parallel as they contract and disappear just before the completion of chloroplast division. In contrast, the outer rings remain in the cytosol after chloroplast division (Miyagishima et al, 2001). Some of these morphological changes have been reported in Chlorophyta (Chida and Ueda, 1991;Ogawa et al, 1995).…”

mentioning

confidence: 81%

“…The Plant Cell Filaments of the Plastid Division Apparatus 715 study of the PD ring in C. merolae suggested that the proteins composing the PD rings exist on the envelopes only in the dividing phase (Miyagishima et al, 2001). Therefore, candidate proteins should be bound to the envelopes only during the dividing phase and enriched in the insoluble fraction of Nonidet P-40 treatment.…”

mentioning

confidence: 99%

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Novel Filaments 5 nm in Diameter Constitute the Cytosolic Ring of the Plastid Division Apparatus

Miyagishima

¹

,

Takahara

²

,

Kuroiwa

³

2001

Self Cite

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The plastid division apparatus (called the plastid-dividing ring) has been detected in several plant and algal species at the constricted region of plastids by transmission electron microscopy. The apparatus is composed of two or three rings: an outer ring in the cytosol, an inner ring in the stroma, and a middle ring in the intermembrane space. The components of these rings are not clear. FtsZ, which forms the bacterial cytokinetic ring, has been proposed as a component of both the inner and outer rings. Here, we present the ultrastructure of the outer ring at high resolution. To visualize the outer ring by negative staining, we isolated dividing chloroplasts from a synchronized culture of a red alga, Cyanidioschyzon merolae , and lysed them with nonionic detergent Nonidet P-40. Nonidet P-40 extracted primarily stroma, thylakoids, and the inner and middle rings, leaving the envelope and outer ring largely intact. Negative staining revealed that the outer ring consists of a bundle of 5-nm filaments in which globular proteins are spaced 4.8 nm apart. Immunoblotting using an FtsZ-specific antibody failed to show immunoreactivity in the fraction containing the filament. Moreover, the filament structure and properties are unlike those of known cytoskeletal filaments. The bundle of filaments forms a very rigid structure and does not disassemble in 2 M urea. We also identified a dividing phase-specific 56-kD protein of chloroplasts as a candidate component of the ring. Our results suggest that the main architecture of the outer ring did not descend from cyanobacteria during the course of endosymbiosis but was added by the host cell early in plant evolution. INTRODUCTIONEukaryotic cells contain organelles that are duplicated and inherited by daughter cells during cell division. Among these organelles, mitochondria and plastids are unique in that they contain DNA-protein complexes (nucleoids) and machinery sufficient for protein synthesis. It is generally believed that mitochondria and plastids arose from prokaryotic endosymbionts during eukaryotic evolution. The endosymbiotic theory states that the progenitor of mitochondria was an ␣ -proteobacterium and that the plastid ancestor was a cyanobacterium (Gray, 1992). Mitochondria and plastids multiply by the division of preexisting organelles, as do bacteria (Leech et al., 1981;Kuroiwa, 1982Kuroiwa, , 1991Possingham and Lawrence, 1983; Boffey and Lloyd, 1988). Of the characterized mitochondrial and plastid genomes, however, none has a complete set of genes sufficient for self-replication. Mitochondria that cannot synthesize proteins as a result of large genome deletions (petite mutant) (Attardi and Schatz, 1988) and plastids that lack ribosomes (Hashimoto and Possingham, 1989) still can proliferate. Therefore, it is believed that products from the host (nuclear) genomes perform mitochondrial and plastid division. Nuclear regulation of organelle division remains poorly understood, but in plastid division both the plastid-dividing ring (PD ring) (summarized in Kuroiwa et ...

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“…These structures have been termed the inner and outer plastid-dividing (PD) rings, respectively. A middle PD ring positioned in the intermembrane space has also been described in the red alga Cyanidioschyzon merolae (16), and the dynamics of assembly and disassembly of the three PD rings have been investigated in detail in this organism (17,18). Although it was previously hypothesized that the PD rings might contain FtsZ (4), recent evidence showing that the FtsZ ring assembles before and is separable from the PD rings in both C. merolae and plants (19,20) indicate that this is not the case.…”

mentioning

confidence: 99%

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

Gao

¹

,

Kadirjan-Kalbach

²

,

Froehlich

³

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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“…The Plant Cell the outer PD ring disassembles and disappears from the surface inward over 1 to 2 hr (Miyagishima et al, 2001). It will be interesting to determine how the cytosol disassembles the ring after chloroplast division and how such a rigid bundle of filaments contracts.…”

mentioning

confidence: 99%

Novel Filaments 5 nm in Diameter Constitute the Cytosolic Ring of the Plastid Division Apparatus

Miyagishima¹,

Takahara²,

Kuroiwa³

2001

Self Cite

View full text Add to dashboard Cite

The plastid division apparatus (called the plastid-dividing ring) has been detected in several plant and algal species at the constricted region of plastids by transmission electron microscopy. The apparatus is composed of two or three rings: an outer ring in the cytosol, an inner ring in the stroma, and a middle ring in the intermembrane space. The components of these rings are not clear. FtsZ, which forms the bacterial cytokinetic ring, has been proposed as a component of both the inner and outer rings. Here, we present the ultrastructure of the outer ring at high resolution. To visualize the outer ring by negative staining, we isolated dividing chloroplasts from a synchronized culture of a red alga, Cyanidioschyzon merolae , and lysed them with nonionic detergent Nonidet P-40. Nonidet P-40 extracted primarily stroma, thylakoids, and the inner and middle rings, leaving the envelope and outer ring largely intact. Negative staining revealed that the outer ring consists of a bundle of 5-nm filaments in which globular proteins are spaced 4.8 nm apart. Immunoblotting using an FtsZ-specific antibody failed to show immunoreactivity in the fraction containing the filament. Moreover, the filament structure and properties are unlike those of known cytoskeletal filaments. The bundle of filaments forms a very rigid structure and does not disassemble in 2 M urea. We also identified a dividing phase-specific 56-kD protein of chloroplasts as a candidate component of the ring. Our results suggest that the main architecture of the outer ring did not descend from cyanobacteria during the course of endosymbiosis but was added by the host cell early in plant evolution. INTRODUCTIONEukaryotic cells contain organelles that are duplicated and inherited by daughter cells during cell division. Among these organelles, mitochondria and plastids are unique in that they contain DNA-protein complexes (nucleoids) and machinery sufficient for protein synthesis. It is generally believed that mitochondria and plastids arose from prokaryotic endosymbionts during eukaryotic evolution. The endosymbiotic theory states that the progenitor of mitochondria was an ␣ -proteobacterium and that the plastid ancestor was a cyanobacterium (Gray, 1992). Mitochondria and plastids multiply by the division of preexisting organelles, as do bacteria (Leech et al., 1981;Kuroiwa, 1982Kuroiwa, , 1991Possingham and Lawrence, 1983; Boffey and Lloyd, 1988). Of the characterized mitochondrial and plastid genomes, however, none has a complete set of genes sufficient for self-replication. Mitochondria that cannot synthesize proteins as a result of large genome deletions (petite mutant) (Attardi and Schatz, 1988) and plastids that lack ribosomes (Hashimoto and Possingham, 1989) still can proliferate. Therefore, it is believed that products from the host (nuclear) genomes perform mitochondrial and plastid division. Nuclear regulation of organelle division remains poorly understood, but in plastid division both the plastid-dividing ring (PD ring) (summarized in Kuroiwa et ...

show abstract

The timing and manner of disassembly of the apparatuses for chloroplast and mitochondrial division in the red alga Cyanidioschyzon merolae

Cited by 50 publications

References 43 publications

Novel Filaments 5 nm in Diameter Constitute the Cytosolic Ring of the Plastid Division Apparatus

Novel Filaments 5 nm in Diameter Constitute the Cytosolic Ring of the Plastid Division Apparatus

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

Novel Filaments 5 nm in Diameter Constitute the Cytosolic Ring of the Plastid Division Apparatus

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