The Division Apparatus of Plastids and Mitochondria

Kuroiwa, Tsuneyoshi; Kuroiwa, Haruko; Sakai, Atsushi; Takahashi, Hidenori; Toda, Kyoko; Itoh, Ryuuichi

doi:10.1016/s0074-7696(08)60415-5

Cited by 201 publications

(181 citation statements)

References 61 publications

Supporting

Mentioning

170

Contrasting

Unclassified

Order By: Relevance

“…Previously, it was suggested that actin could be involved in the outer PD ring (summarized in Kuroiwa et al, 1998). However, in this study, any helical structure similar to F-actin could not be detected around the outer PD ring.…”

Section: Filaments Of the Plastid Division Apparatus 717contrasting

confidence: 72%

“…It has been detected in several species of Chlorophyta (green algae and terrestrial plants) (Hashimoto, 1986;Tewinkel and Volkmann, 1987;Hashimoto and Possingham, 1989;Oross and Possingham, 1989;Chida and Ueda, 1991;Duckett andLigrone, 1993a, 1993b;Ogawa et al, 1995;Robertson et al, 1996), Rhodophyta (Mita et al, 1986;Suzuki et al, 1994), and Chromophyta (Hashimoto, 1997;Beech and Gilson, 2000) and is thought to be ubiquitous in the plant kingdom (summarized in Kuroiwa, 1998;Kuroiwa et al, 1998). In most organisms, the PD ring consists of a double ring structure, with one ring on the cytosolic face of the outer envelope (outer ring) and one on the stromal face of the inner envelope (inner ring).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

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

Miyagishima¹,

Takahara²,

Kuroiwa³

2001

The Plant Cell

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

Section: Filaments Of the Plastid Division Apparatus 717contrasting

confidence: 72%

Section: Introductionmentioning

confidence: 99%

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

Miyagishima¹,

Takahara²,

Kuroiwa³

2001

The Plant Cell

Self Cite

View full text Add to dashboard Cite

show abstract

“…Evidence that division is altered in other tissues comes from our finding that overexpression of GNC and CGA1 results in increased numbers of chloroplasts in epidermal and cortical cells of the hypocotyl as well as the finding that GNC/CGA1 mutants alter the numbers of chloroplasts in leaves (Hudson et al, 2011). Chloroplasts multiply by binary fission (Possingham and Lawrence, 1983;Kuroiwa et al, 1998), and thus an increase in chloroplast number indicates an acceleration of chloroplast division.…”

Section: Key Role Of the Gnc/cga1 Family In Chloroplast Biogenesismentioning

confidence: 97%

Functional Characterization of the GATA Transcription Factors GNC and CGA1 Reveals Their Key Role in Chloroplast Development, Growth, and Division in Arabidopsis

et al. 2012

View full text Add to dashboard Cite

Chloroplasts develop from proplastids in a process that requires the interplay of nuclear and chloroplast genomes, but key steps in this developmental process have yet to be elucidated. Here, we show that the nucleus-localized transcription factors GATA NITRATE-INDUCIBLE CARBON-METABOLISM-INVOLVED (GNC) and CYTOKININ-RESPONSIVE GATA1 (CGA1) regulate chloroplast development, growth, and division in Arabidopsis (Arabidopsis thaliana). GNC and CGA1 are highly expressed in green tissues, and the phytohormone cytokinin regulates their expression. A gnc cga1 mutant exhibits a reduction in overall chlorophyll levels as well as in chloroplast size in the hypocotyl. Ectopic overexpression of either GNC or CGA1 promotes chloroplast biogenesis in hypocotyl cortex and root pericycle cells, based on increases in the number and size of the chloroplasts, and also results in expanded zones of chloroplast production into the epidermis of hypocotyls and cotyledons and into the cortex of roots. Ectopic overexpression also promotes the development of etioplasts from proplastids in dark-grown seedlings, subsequently enhancing the deetiolation process. Inducible expression of GNC demonstrates that GNCmediated chloroplast biogenesis can be regulated postembryonically, notably so for chloroplast production in cotyledon epidermal cells. Analysis of the gnc cga1 loss-of-function and overexpression lines supports a role for these transcription factors in regulating the effects of cytokinin on chloroplast division. These data support a model in which GNC and CGA1 serve as two of the master transcriptional regulators of chloroplast biogenesis, acting downstream of cytokinin and mediating the development of chloroplasts from proplastids and enhancing chloroplast growth and division in specific tissues.

show abstract

“…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 structures have been termed the inner and outer plastid-dividing (PD) rings, respectively.…”

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.

253

254

View full text Add to dashboard Cite

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...

show abstract

The Division Apparatus of Plastids and Mitochondria

Cited by 201 publications

References 61 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

Functional Characterization of the GATA Transcription Factors GNC and CGA1 Reveals Their Key Role in Chloroplast Development, Growth, and Division in Arabidopsis

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

Contact Info

Product

Resources

About