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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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Schematic representation of the eukaryotic phylogenic tree (A) and the model cell (E), fluorescence microscopy (B–D) and electron micrographs (F, G) of C. merolae cells. A. Mitochondria and plastids originated from α-proteobacteria and cyanobacteria of eubacteria, respectively, and increased in number during evolution. B and C. The photographs show a cell nucleus (top), mitochondrial nucleus (middle), and plastid nucleus (bottom) in interphase (B) and dividing cells (C) after staining with DAPI. The plastids emit red autofluorescence. D. The synchronized dividing plastids show a dumbbell-shape. E. Model of the dividing cell showing a spherical cell nucleus (blue), v-shaped mitochondrion with division machinery (green), and a dumbbell-shaped plastid with division machinery (red). F. Dividing cell shows cross sections of cell nucleus (n), mitochondrion (m), plastid (p), dividing electron dense mt- (short arrows in enlarged image) and pt-division machineries (long arrows in enlarged image) at the division sites. G. The contracted outer pt-division machinery looks like a bundle of fine filaments, 5–7 nm in diameter, after negative staining. Scale bars: 10 µm (D), 1 µm (B, C), and 0.1 µm (F). E is from Dr. Yoshida, Y., F is from Ref. 3, G is from Ref. 23.
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fig02: Schematic representation of the eukaryotic phylogenic tree (A) and the model cell (E), fluorescence microscopy (B–D) and electron micrographs (F, G) of C. merolae cells. A. Mitochondria and plastids originated from α-proteobacteria and cyanobacteria of eubacteria, respectively, and increased in number during evolution. B and C. The photographs show a cell nucleus (top), mitochondrial nucleus (middle), and plastid nucleus (bottom) in interphase (B) and dividing cells (C) after staining with DAPI. The plastids emit red autofluorescence. D. The synchronized dividing plastids show a dumbbell-shape. E. Model of the dividing cell showing a spherical cell nucleus (blue), v-shaped mitochondrion with division machinery (green), and a dumbbell-shaped plastid with division machinery (red). F. Dividing cell shows cross sections of cell nucleus (n), mitochondrion (m), plastid (p), dividing electron dense mt- (short arrows in enlarged image) and pt-division machineries (long arrows in enlarged image) at the division sites. G. The contracted outer pt-division machinery looks like a bundle of fine filaments, 5–7 nm in diameter, after negative staining. Scale bars: 10 µm (D), 1 µm (B, C), and 0.1 µm (F). E is from Dr. Yoshida, Y., F is from Ref. 3, G is from Ref. 23.

Mentions: The mitochondria and plastids in almost all eukaryotes divide after organelle-nuclear division, as in slime mould. When daughter mitochondria were pinched off at the final stage of division, a small ring-like structure (Fig. 1D) and a smooth bridge between daughter mitochondria were observed in P. polycephalum and Nitella flexilis,6) respectively. These structures have been found to be universal in eukaryotes.15) However, it proved very difficult to study the cellular and molecular mechanisms of organelle division in eukaryotes for the following reasons. In Bikonta (plantae), Opisthokonta (animalia and fungi) and Amoebozoa (amoebae, slime mould), 1) the cells contain a large number of mitochondria, 2) mitochondrial shapes are irregular, 3) mitochondrial division occurs randomly (sometimes mitochondrial fusion also occurs), and 4) mitochondria move actively in whole cells (Figs. 1J and 2A).


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)

Schematic representation of the eukaryotic phylogenic tree (A) and the model cell (E), fluorescence microscopy (B–D) and electron micrographs (F, G) of C. merolae cells. A. Mitochondria and plastids originated from α-proteobacteria and cyanobacteria of eubacteria, respectively, and increased in number during evolution. B and C. The photographs show a cell nucleus (top), mitochondrial nucleus (middle), and plastid nucleus (bottom) in interphase (B) and dividing cells (C) after staining with DAPI. The plastids emit red autofluorescence. D. The synchronized dividing plastids show a dumbbell-shape. E. Model of the dividing cell showing a spherical cell nucleus (blue), v-shaped mitochondrion with division machinery (green), and a dumbbell-shaped plastid with division machinery (red). F. Dividing cell shows cross sections of cell nucleus (n), mitochondrion (m), plastid (p), dividing electron dense mt- (short arrows in enlarged image) and pt-division machineries (long arrows in enlarged image) at the division sites. G. The contracted outer pt-division machinery looks like a bundle of fine filaments, 5–7 nm in diameter, after negative staining. Scale bars: 10 µm (D), 1 µm (B, C), and 0.1 µm (F). E is from Dr. Yoshida, Y., F is from Ref. 3, G is from Ref. 23.
© Copyright Policy - open-access
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3108297&req=5

fig02: Schematic representation of the eukaryotic phylogenic tree (A) and the model cell (E), fluorescence microscopy (B–D) and electron micrographs (F, G) of C. merolae cells. A. Mitochondria and plastids originated from α-proteobacteria and cyanobacteria of eubacteria, respectively, and increased in number during evolution. B and C. The photographs show a cell nucleus (top), mitochondrial nucleus (middle), and plastid nucleus (bottom) in interphase (B) and dividing cells (C) after staining with DAPI. The plastids emit red autofluorescence. D. The synchronized dividing plastids show a dumbbell-shape. E. Model of the dividing cell showing a spherical cell nucleus (blue), v-shaped mitochondrion with division machinery (green), and a dumbbell-shaped plastid with division machinery (red). F. Dividing cell shows cross sections of cell nucleus (n), mitochondrion (m), plastid (p), dividing electron dense mt- (short arrows in enlarged image) and pt-division machineries (long arrows in enlarged image) at the division sites. G. The contracted outer pt-division machinery looks like a bundle of fine filaments, 5–7 nm in diameter, after negative staining. Scale bars: 10 µm (D), 1 µm (B, C), and 0.1 µm (F). E is from Dr. Yoshida, Y., F is from Ref. 3, G is from Ref. 23.
Mentions: The mitochondria and plastids in almost all eukaryotes divide after organelle-nuclear division, as in slime mould. When daughter mitochondria were pinched off at the final stage of division, a small ring-like structure (Fig. 1D) and a smooth bridge between daughter mitochondria were observed in P. polycephalum and Nitella flexilis,6) respectively. These structures have been found to be universal in eukaryotes.15) However, it proved very difficult to study the cellular and molecular mechanisms of organelle division in eukaryotes for the following reasons. In Bikonta (plantae), Opisthokonta (animalia and fungi) and Amoebozoa (amoebae, slime mould), 1) the cells contain a large number of mitochondria, 2) mitochondrial shapes are irregular, 3) mitochondrial division occurs randomly (sometimes mitochondrial fusion also occurs), and 4) mitochondria move actively in whole cells (Figs. 1J and 2A).

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