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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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Phase contrast/fluorescence (A, D, J). phase-contrast (J), fluorescence micrographs (B, E. F, G, J) of isolated mitochondria (A), pt-division machineries (B), complexes of mt- and pt-division machineries (D, E, F), mt-division machinery (G), mitochondria and ZED (J), contraction model of pt-division machineries (C), an electron micrograph of the complex of isolated mt- and pt-division machineries (H), and SDS-PAGE (I). A. Physarum mitochondria with m-nuclei (bright rods) were drawn up in a “Y” image using optical tweezers. B. Manipulation of intact PD division machinery of C. merolae (a) and a dynamin-released PD division machinery (b) with the optical tweezer. The base line of one end of each of the pt-division machineries is fixed to the cover glass (yellow lines), while the other end is trapped by the optical tweezers (arrowheads) and an infrared laser (red lines). C. The schema shows a contraction model of pt-division machineries. In the first step, the dynamin molecules (red) drive the sliding of the fine filaments. In the second step, dynamin moves from the surface to the inside and pinches off the narrow bridge between daughter plastids. D. Mt-division machinery (yellow) is associated with pt-division machinery (red) in intact dividing cells. E and F. The bulk of isolated mt-division machinery (green) adheres to the pt-division machinery (red). G. Isolated mt-division machinery is a small ring. H. Immuno-electron micrograph showing the distributions of Mda1 and dynamin (Dnm2) in isolated mt- (large gold particles) and pt- (small gold particles) division machineries after negative staining. I. SDS-PAGE images of isolated PD machineries were compared with the interphase fraction (right). Proteins of isolated mitochondrial and plastid division machineries from cells in early M-phase (left), later M-phase (middle), and inter-phase (right) were separated by SDS-PAGE. J. In cells with transient DNA introduction and expression of ZED promoter without antisense-ZED, mitochondrial division (red) occurred normally (control). Plastid division occurred normally (phase contrast, PC), but mitochondrial division did not occur in ZED (blue)-downregulated cells (ZED antisense). Scale bars: 1 µm (A, B, G, J), 0.2 µm (H). B and C are from Ref. 28, D–J are from Ref. 30.
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fig04: Phase contrast/fluorescence (A, D, J). phase-contrast (J), fluorescence micrographs (B, E. F, G, J) of isolated mitochondria (A), pt-division machineries (B), complexes of mt- and pt-division machineries (D, E, F), mt-division machinery (G), mitochondria and ZED (J), contraction model of pt-division machineries (C), an electron micrograph of the complex of isolated mt- and pt-division machineries (H), and SDS-PAGE (I). A. Physarum mitochondria with m-nuclei (bright rods) were drawn up in a “Y” image using optical tweezers. B. Manipulation of intact PD division machinery of C. merolae (a) and a dynamin-released PD division machinery (b) with the optical tweezer. The base line of one end of each of the pt-division machineries is fixed to the cover glass (yellow lines), while the other end is trapped by the optical tweezers (arrowheads) and an infrared laser (red lines). C. The schema shows a contraction model of pt-division machineries. In the first step, the dynamin molecules (red) drive the sliding of the fine filaments. In the second step, dynamin moves from the surface to the inside and pinches off the narrow bridge between daughter plastids. D. Mt-division machinery (yellow) is associated with pt-division machinery (red) in intact dividing cells. E and F. The bulk of isolated mt-division machinery (green) adheres to the pt-division machinery (red). G. Isolated mt-division machinery is a small ring. H. Immuno-electron micrograph showing the distributions of Mda1 and dynamin (Dnm2) in isolated mt- (large gold particles) and pt- (small gold particles) division machineries after negative staining. I. SDS-PAGE images of isolated PD machineries were compared with the interphase fraction (right). Proteins of isolated mitochondrial and plastid division machineries from cells in early M-phase (left), later M-phase (middle), and inter-phase (right) were separated by SDS-PAGE. J. In cells with transient DNA introduction and expression of ZED promoter without antisense-ZED, mitochondrial division (red) occurred normally (control). Plastid division occurred normally (phase contrast, PC), but mitochondrial division did not occur in ZED (blue)-downregulated cells (ZED antisense). Scale bars: 1 µm (A, B, G, J), 0.2 µm (H). B and C are from Ref. 28, D–J are from Ref. 30.

Mentions: To identify further novel proteins in the pt-division machineries, we improved the method for isolating intact pt-division machineries. The outer membrane (associating dynamin and PD rings) of the plastids could not be completely solved by high concentrations of NP-40 (Fig. 3A–C).28) Instead, dividing plastids were obtained from synchronized cells and treated with n-octyl-β-D-glucopyranoside (OG) after Nonidet P-40 treatment. The purity of the isolated pt-division machineries was examined by fluorescent and electron microscopy, SDS-polyacrylamide gel electrophoresis, MALDI-TOF MS, and immunoblotting. The isolated division machineries showed super twist, spiral, and ring structures (Fig. 3D–F),28) suggesting that pt-division machineries included structures and molecules that generate motive force for contraction at the dividing site. The isolated pt-division machinery was smooth, and comprised a bundle of fine filaments 5–7 nm in diameter (Fig. 3F) that was composed of an FtsZ ring (inside) and the PD ring and dynamin rings (outside) through the membranes (Fig. 3F).28) The existence of membrane-free pt-machineries suggested that there is a linking structure through the membrane between the inner (FtsZ and inner PD) and outer (outer PD and dynamin) rings (Fig. 4C).


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)

Phase contrast/fluorescence (A, D, J). phase-contrast (J), fluorescence micrographs (B, E. F, G, J) of isolated mitochondria (A), pt-division machineries (B), complexes of mt- and pt-division machineries (D, E, F), mt-division machinery (G), mitochondria and ZED (J), contraction model of pt-division machineries (C), an electron micrograph of the complex of isolated mt- and pt-division machineries (H), and SDS-PAGE (I). A. Physarum mitochondria with m-nuclei (bright rods) were drawn up in a “Y” image using optical tweezers. B. Manipulation of intact PD division machinery of C. merolae (a) and a dynamin-released PD division machinery (b) with the optical tweezer. The base line of one end of each of the pt-division machineries is fixed to the cover glass (yellow lines), while the other end is trapped by the optical tweezers (arrowheads) and an infrared laser (red lines). C. The schema shows a contraction model of pt-division machineries. In the first step, the dynamin molecules (red) drive the sliding of the fine filaments. In the second step, dynamin moves from the surface to the inside and pinches off the narrow bridge between daughter plastids. D. Mt-division machinery (yellow) is associated with pt-division machinery (red) in intact dividing cells. E and F. The bulk of isolated mt-division machinery (green) adheres to the pt-division machinery (red). G. Isolated mt-division machinery is a small ring. H. Immuno-electron micrograph showing the distributions of Mda1 and dynamin (Dnm2) in isolated mt- (large gold particles) and pt- (small gold particles) division machineries after negative staining. I. SDS-PAGE images of isolated PD machineries were compared with the interphase fraction (right). Proteins of isolated mitochondrial and plastid division machineries from cells in early M-phase (left), later M-phase (middle), and inter-phase (right) were separated by SDS-PAGE. J. In cells with transient DNA introduction and expression of ZED promoter without antisense-ZED, mitochondrial division (red) occurred normally (control). Plastid division occurred normally (phase contrast, PC), but mitochondrial division did not occur in ZED (blue)-downregulated cells (ZED antisense). Scale bars: 1 µm (A, B, G, J), 0.2 µm (H). B and C are from Ref. 28, D–J are from Ref. 30.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig04: Phase contrast/fluorescence (A, D, J). phase-contrast (J), fluorescence micrographs (B, E. F, G, J) of isolated mitochondria (A), pt-division machineries (B), complexes of mt- and pt-division machineries (D, E, F), mt-division machinery (G), mitochondria and ZED (J), contraction model of pt-division machineries (C), an electron micrograph of the complex of isolated mt- and pt-division machineries (H), and SDS-PAGE (I). A. Physarum mitochondria with m-nuclei (bright rods) were drawn up in a “Y” image using optical tweezers. B. Manipulation of intact PD division machinery of C. merolae (a) and a dynamin-released PD division machinery (b) with the optical tweezer. The base line of one end of each of the pt-division machineries is fixed to the cover glass (yellow lines), while the other end is trapped by the optical tweezers (arrowheads) and an infrared laser (red lines). C. The schema shows a contraction model of pt-division machineries. In the first step, the dynamin molecules (red) drive the sliding of the fine filaments. In the second step, dynamin moves from the surface to the inside and pinches off the narrow bridge between daughter plastids. D. Mt-division machinery (yellow) is associated with pt-division machinery (red) in intact dividing cells. E and F. The bulk of isolated mt-division machinery (green) adheres to the pt-division machinery (red). G. Isolated mt-division machinery is a small ring. H. Immuno-electron micrograph showing the distributions of Mda1 and dynamin (Dnm2) in isolated mt- (large gold particles) and pt- (small gold particles) division machineries after negative staining. I. SDS-PAGE images of isolated PD machineries were compared with the interphase fraction (right). Proteins of isolated mitochondrial and plastid division machineries from cells in early M-phase (left), later M-phase (middle), and inter-phase (right) were separated by SDS-PAGE. J. In cells with transient DNA introduction and expression of ZED promoter without antisense-ZED, mitochondrial division (red) occurred normally (control). Plastid division occurred normally (phase contrast, PC), but mitochondrial division did not occur in ZED (blue)-downregulated cells (ZED antisense). Scale bars: 1 µm (A, B, G, J), 0.2 µm (H). B and C are from Ref. 28, D–J are from Ref. 30.
Mentions: To identify further novel proteins in the pt-division machineries, we improved the method for isolating intact pt-division machineries. The outer membrane (associating dynamin and PD rings) of the plastids could not be completely solved by high concentrations of NP-40 (Fig. 3A–C).28) Instead, dividing plastids were obtained from synchronized cells and treated with n-octyl-β-D-glucopyranoside (OG) after Nonidet P-40 treatment. The purity of the isolated pt-division machineries was examined by fluorescent and electron microscopy, SDS-polyacrylamide gel electrophoresis, MALDI-TOF MS, and immunoblotting. The isolated division machineries showed super twist, spiral, and ring structures (Fig. 3D–F),28) suggesting that pt-division machineries included structures and molecules that generate motive force for contraction at the dividing site. The isolated pt-division machinery was smooth, and comprised a bundle of fine filaments 5–7 nm in diameter (Fig. 3F) that was composed of an FtsZ ring (inside) and the PD ring and dynamin rings (outside) through the membranes (Fig. 3F).28) The existence of membrane-free pt-machineries suggested that there is a linking structure through the membrane between the inner (FtsZ and inner PD) and outer (outer PD and dynamin) rings (Fig. 4C).

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