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Mechanisms of organelle division and inheritance and their implications regarding the origin of eukaryotic cells.

Kuroiwa T - Proc. Jpn. Acad., Ser. B, Phys. Biol. Sci. (2010)

Bottom Line: Mitochondria and plastids have their own DNAs and are regarded as descendants of endosymbiotic prokaryotes.Organellar DNAs are not naked in vivo but are associated with basic proteins to form DNA-protein complexes (called organelle nuclei).The maternal inheritance of organelles developed during sexual reproduction and it is also probably intimately related to the origin of organelles.

View Article: PubMed Central - PubMed

Affiliation: Research Information Center of Extremophile, Rikkyo (St. Paul's) University, Tokyo, Japan. tsune@rikkyo.ne.jp

ABSTRACT
Mitochondria and plastids have their own DNAs and are regarded as descendants of endosymbiotic prokaryotes. Organellar DNAs are not naked in vivo but are associated with basic proteins to form DNA-protein complexes (called organelle nuclei). The concept of organelle nuclei provides a new approach to explain the origin, division, and inheritance of organelles. Organelles divide using organelle division rings (machineries) after organelle-nuclear division. Organelle division machineries are a chimera of the FtsZ (filamentous temperature sensitive Z) ring of bacterial origin and the eukaryotic mechanochemical dynamin ring. Thus, organelle division machineries contain a key to solve the origin of organelles (eukaryotes). The maternal inheritance of organelles developed during sexual reproduction and it is also probably intimately related to the origin of organelles. The aims of this review are to describe the strategies used to reveal the dynamics of organelle division machineries, and the significance of the division machineries and maternal inheritance in the origin and evolution of eukaryotes.

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Electron micrograph (A: SEM, C, E, F: TEM) and phase contrast (PC in B) and fluorescence micrograph (cmFtsZ, cmDnm in B, D) of isolated plastids with pt-division machineries (A–C) and isolated pt-division machineries (D, E, F). A. The image shows a dividing plastid with pt-division machinery at the center of the plastid. B and C. The pt-division machineries with the outer membrane are a chimera of bacterial FtsZ (CmFtsZ), dynamin (CmDnm2), and PD rings (arrow head in C). D, E, and F. Isolated pt-division machineries are composed of a bundle of fine filaments (enlarged image in F) and contained dynamin (small gold particles in F) and FtsZ (large gold particles in F). Scale bars: 1 µm (B), 0.5 µm (A, C, E), and 0.1 µm (F). A is from Ref. 3, B, C, D and F are from Ref. 28, E is from Ref. 3.
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fig03: Electron micrograph (A: SEM, C, E, F: TEM) and phase contrast (PC in B) and fluorescence micrograph (cmFtsZ, cmDnm in B, D) of isolated plastids with pt-division machineries (A–C) and isolated pt-division machineries (D, E, F). A. The image shows a dividing plastid with pt-division machinery at the center of the plastid. B and C. The pt-division machineries with the outer membrane are a chimera of bacterial FtsZ (CmFtsZ), dynamin (CmDnm2), and PD rings (arrow head in C). D, E, and F. Isolated pt-division machineries are composed of a bundle of fine filaments (enlarged image in F) and contained dynamin (small gold particles in F) and FtsZ (large gold particles in F). Scale bars: 1 µm (B), 0.5 µm (A, C, E), and 0.1 µm (F). A is from Ref. 3, B, C, D and F are from Ref. 28, E is from Ref. 3.

Mentions: We isolated dividing plastids with their pt-division machineries from a synchronized culture of C. merolae (Figs. 2G and 3A) and treated them with nonionic detergent Nonidet P-40 to extract stroma and thylakoids.22) The inner rings and outer ring remained intact after the treatment. Negative staining revealed that the outer ring consists of a bundle of 5-nm filaments (Fig. 2G), in which globular proteins are spaced 4.8 nm apart.22) Sliding of the fine filaments seemed to generate the motive force for contraction of the machineries.13,22) Moreover, the structure and properties of the filaments are unlike those of known cytoskeletal filaments. We also examined dividing phase-specific proteins of plastids as candidate components of the rings. However, as the outer membranes could not be solved completely by NP-40 treatment and as the architectural proteins in the pt-division machineries were very small or were present in very low amounts, we could not determine the candidate proteins.


Mechanisms of organelle division and inheritance and their implications regarding the origin of eukaryotic cells.

Kuroiwa T - Proc. Jpn. Acad., Ser. B, Phys. Biol. Sci. (2010)

Electron micrograph (A: SEM, C, E, F: TEM) and phase contrast (PC in B) and fluorescence micrograph (cmFtsZ, cmDnm in B, D) of isolated plastids with pt-division machineries (A–C) and isolated pt-division machineries (D, E, F). A. The image shows a dividing plastid with pt-division machinery at the center of the plastid. B and C. The pt-division machineries with the outer membrane are a chimera of bacterial FtsZ (CmFtsZ), dynamin (CmDnm2), and PD rings (arrow head in C). D, E, and F. Isolated pt-division machineries are composed of a bundle of fine filaments (enlarged image in F) and contained dynamin (small gold particles in F) and FtsZ (large gold particles in F). Scale bars: 1 µm (B), 0.5 µm (A, C, E), and 0.1 µm (F). A is from Ref. 3, B, C, D and F are from Ref. 28, E is from Ref. 3.
© Copyright Policy - open-access
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3108297&req=5

fig03: Electron micrograph (A: SEM, C, E, F: TEM) and phase contrast (PC in B) and fluorescence micrograph (cmFtsZ, cmDnm in B, D) of isolated plastids with pt-division machineries (A–C) and isolated pt-division machineries (D, E, F). A. The image shows a dividing plastid with pt-division machinery at the center of the plastid. B and C. The pt-division machineries with the outer membrane are a chimera of bacterial FtsZ (CmFtsZ), dynamin (CmDnm2), and PD rings (arrow head in C). D, E, and F. Isolated pt-division machineries are composed of a bundle of fine filaments (enlarged image in F) and contained dynamin (small gold particles in F) and FtsZ (large gold particles in F). Scale bars: 1 µm (B), 0.5 µm (A, C, E), and 0.1 µm (F). A is from Ref. 3, B, C, D and F are from Ref. 28, E is from Ref. 3.
Mentions: We isolated dividing plastids with their pt-division machineries from a synchronized culture of C. merolae (Figs. 2G and 3A) and treated them with nonionic detergent Nonidet P-40 to extract stroma and thylakoids.22) The inner rings and outer ring remained intact after the treatment. Negative staining revealed that the outer ring consists of a bundle of 5-nm filaments (Fig. 2G), in which globular proteins are spaced 4.8 nm apart.22) Sliding of the fine filaments seemed to generate the motive force for contraction of the machineries.13,22) Moreover, the structure and properties of the filaments are unlike those of known cytoskeletal filaments. We also examined dividing phase-specific proteins of plastids as candidate components of the rings. However, as the outer membranes could not be solved completely by NP-40 treatment and as the architectural proteins in the pt-division machineries were very small or were present in very low amounts, we could not determine the candidate proteins.

Bottom Line: Mitochondria and plastids have their own DNAs and are regarded as descendants of endosymbiotic prokaryotes.Organellar DNAs are not naked in vivo but are associated with basic proteins to form DNA-protein complexes (called organelle nuclei).The maternal inheritance of organelles developed during sexual reproduction and it is also probably intimately related to the origin of organelles.

View Article: PubMed Central - PubMed

Affiliation: Research Information Center of Extremophile, Rikkyo (St. Paul's) University, Tokyo, Japan. tsune@rikkyo.ne.jp

ABSTRACT
Mitochondria and plastids have their own DNAs and are regarded as descendants of endosymbiotic prokaryotes. Organellar DNAs are not naked in vivo but are associated with basic proteins to form DNA-protein complexes (called organelle nuclei). The concept of organelle nuclei provides a new approach to explain the origin, division, and inheritance of organelles. Organelles divide using organelle division rings (machineries) after organelle-nuclear division. Organelle division machineries are a chimera of the FtsZ (filamentous temperature sensitive Z) ring of bacterial origin and the eukaryotic mechanochemical dynamin ring. Thus, organelle division machineries contain a key to solve the origin of organelles (eukaryotes). The maternal inheritance of organelles developed during sexual reproduction and it is also probably intimately related to the origin of organelles. The aims of this review are to describe the strategies used to reveal the dynamics of organelle division machineries, and the significance of the division machineries and maternal inheritance in the origin and evolution of eukaryotes.

Show MeSH
Related in: MedlinePlus