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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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Related in: MedlinePlus

Models of mitochondrial division by mt-division machinery (A) and molecular model of mt-division machinery (enlarged image in A) and plastid division by pt-division machinery (B) and molecular model of pt-division machinery (enlarged image in B). A. In the positioning phase, the inner MD ring and FtsZ ring are formed on the matrix side, and the division site is determined. In the constriction phase, the Mda1 ring and outer MD ring appear on the cytoplasmic side of the outer membrane. The inner MD, FtsZ, Mda1, and outer MD rings begin to constrict the equator of the dividing mitochondrion. When the mitochondrion has constricted at the division site, dynamin is recruited from the patches in the cytoplasm to form the mt-division machinery, with Mda1 and the outer MD ring, and finally migrates to a space inside the thickened outer MD ring and outside the outer membrane. In the pinching-off phase, the inner MD ring and the FtsZ ring are split to form a patch in each matrix. The dynamin ring pinches off the membrane of the bridge between the daughter mitochondria. The remnants of the mt-division machineries are broken into small patches. Putative molecular model of pinching-off at the bridge between daughter mitochondria. Inner MD and FtsZ rings are split to form two divided matrices and then the dynamin ring pinches off the outer and inner membranes simultaneously, at the center of the bridge, by a biochemical reaction between the PH domain and the double membranes under the control of Mda1 and the outer MD ring. B. Events similar to the mt-division machineries occur in the pt-division machineries. mn, mitochondrial nuclei; pt, plastid nuclei. Dynamin molecules is improved from Ref. 33, A is from Ref. 3.
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fig05: Models of mitochondrial division by mt-division machinery (A) and molecular model of mt-division machinery (enlarged image in A) and plastid division by pt-division machinery (B) and molecular model of pt-division machinery (enlarged image in B). A. In the positioning phase, the inner MD ring and FtsZ ring are formed on the matrix side, and the division site is determined. In the constriction phase, the Mda1 ring and outer MD ring appear on the cytoplasmic side of the outer membrane. The inner MD, FtsZ, Mda1, and outer MD rings begin to constrict the equator of the dividing mitochondrion. When the mitochondrion has constricted at the division site, dynamin is recruited from the patches in the cytoplasm to form the mt-division machinery, with Mda1 and the outer MD ring, and finally migrates to a space inside the thickened outer MD ring and outside the outer membrane. In the pinching-off phase, the inner MD ring and the FtsZ ring are split to form a patch in each matrix. The dynamin ring pinches off the membrane of the bridge between the daughter mitochondria. The remnants of the mt-division machineries are broken into small patches. Putative molecular model of pinching-off at the bridge between daughter mitochondria. Inner MD and FtsZ rings are split to form two divided matrices and then the dynamin ring pinches off the outer and inner membranes simultaneously, at the center of the bridge, by a biochemical reaction between the PH domain and the double membranes under the control of Mda1 and the outer MD ring. B. Events similar to the mt-division machineries occur in the pt-division machineries. mn, mitochondrial nuclei; pt, plastid nuclei. Dynamin molecules is improved from Ref. 33, A is from Ref. 3.

Mentions: Mt- and pt-division machineries have very precise architectures at the nanolevel, although they appear very smooth and simple. Fig. 5A shows a model of mt-division by the mt-division machinery.3) In the positioning phase of the mt-division machineries, the inner ZED ring, inner MD ring and FtsZ ring are formed on the matrix side, under the control of FtsH, and the division site is determined. The electron dense outer MD ring is located at the cytoplasmic side and then the dynamin ring is located around the MD ring in the cytoplasm. Finally, the outer membrane mt-division machinery is composed of the Mda1 ring, the outer MD ring, the dynamin ring, and unknown rings. The inner membrane mt-division machinery is composed of the ZED ring, the FtsZ ring, the inner MD ring and unknown rings. The existence of membrane-free mt-division machineries suggests that there is a linking structure through the membrane between the inner and outer mt-division machineries.30) In the constriction phase, dynamin is recruited from patches in the cytoplasm to form the outer membrane mt-division machinery, with Mda1 and the outer MD ring.30) Then dynamin drives the sliding of the MD ring fine filaments and causes the contraction required for mitochondrial division. At the late phase of mitochondrial division, the dynamin molecules move from the surface of the outer membrane mt-division machinery to the inside of the machinery (Fig. 5A).30) Praefcke and McMahon (2004) reviewed the superfamily of dynamins and the domain structure and function.33) Classical dynamins contain a GTPase domain, middle domain, pleckstrin-homology (PH) domain, GTPase effector doman (GED) and proline-rich domain. Dynamin probably pinches off the membranes at the bridge between the daughter plastids by a biochemical reaction between the PH domain and the double membrane. After mitochondrial division, the remnants of the mt-division machinery then adhere to one side of the daughter mitochondria and the dynamin ring is broken into small patches.26)


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)

Models of mitochondrial division by mt-division machinery (A) and molecular model of mt-division machinery (enlarged image in A) and plastid division by pt-division machinery (B) and molecular model of pt-division machinery (enlarged image in B). A. In the positioning phase, the inner MD ring and FtsZ ring are formed on the matrix side, and the division site is determined. In the constriction phase, the Mda1 ring and outer MD ring appear on the cytoplasmic side of the outer membrane. The inner MD, FtsZ, Mda1, and outer MD rings begin to constrict the equator of the dividing mitochondrion. When the mitochondrion has constricted at the division site, dynamin is recruited from the patches in the cytoplasm to form the mt-division machinery, with Mda1 and the outer MD ring, and finally migrates to a space inside the thickened outer MD ring and outside the outer membrane. In the pinching-off phase, the inner MD ring and the FtsZ ring are split to form a patch in each matrix. The dynamin ring pinches off the membrane of the bridge between the daughter mitochondria. The remnants of the mt-division machineries are broken into small patches. Putative molecular model of pinching-off at the bridge between daughter mitochondria. Inner MD and FtsZ rings are split to form two divided matrices and then the dynamin ring pinches off the outer and inner membranes simultaneously, at the center of the bridge, by a biochemical reaction between the PH domain and the double membranes under the control of Mda1 and the outer MD ring. B. Events similar to the mt-division machineries occur in the pt-division machineries. mn, mitochondrial nuclei; pt, plastid nuclei. Dynamin molecules is improved from Ref. 33, A is from Ref. 3.
© Copyright Policy - open-access
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3108297&req=5

fig05: Models of mitochondrial division by mt-division machinery (A) and molecular model of mt-division machinery (enlarged image in A) and plastid division by pt-division machinery (B) and molecular model of pt-division machinery (enlarged image in B). A. In the positioning phase, the inner MD ring and FtsZ ring are formed on the matrix side, and the division site is determined. In the constriction phase, the Mda1 ring and outer MD ring appear on the cytoplasmic side of the outer membrane. The inner MD, FtsZ, Mda1, and outer MD rings begin to constrict the equator of the dividing mitochondrion. When the mitochondrion has constricted at the division site, dynamin is recruited from the patches in the cytoplasm to form the mt-division machinery, with Mda1 and the outer MD ring, and finally migrates to a space inside the thickened outer MD ring and outside the outer membrane. In the pinching-off phase, the inner MD ring and the FtsZ ring are split to form a patch in each matrix. The dynamin ring pinches off the membrane of the bridge between the daughter mitochondria. The remnants of the mt-division machineries are broken into small patches. Putative molecular model of pinching-off at the bridge between daughter mitochondria. Inner MD and FtsZ rings are split to form two divided matrices and then the dynamin ring pinches off the outer and inner membranes simultaneously, at the center of the bridge, by a biochemical reaction between the PH domain and the double membranes under the control of Mda1 and the outer MD ring. B. Events similar to the mt-division machineries occur in the pt-division machineries. mn, mitochondrial nuclei; pt, plastid nuclei. Dynamin molecules is improved from Ref. 33, A is from Ref. 3.
Mentions: Mt- and pt-division machineries have very precise architectures at the nanolevel, although they appear very smooth and simple. Fig. 5A shows a model of mt-division by the mt-division machinery.3) In the positioning phase of the mt-division machineries, the inner ZED ring, inner MD ring and FtsZ ring are formed on the matrix side, under the control of FtsH, and the division site is determined. The electron dense outer MD ring is located at the cytoplasmic side and then the dynamin ring is located around the MD ring in the cytoplasm. Finally, the outer membrane mt-division machinery is composed of the Mda1 ring, the outer MD ring, the dynamin ring, and unknown rings. The inner membrane mt-division machinery is composed of the ZED ring, the FtsZ ring, the inner MD ring and unknown rings. The existence of membrane-free mt-division machineries suggests that there is a linking structure through the membrane between the inner and outer mt-division machineries.30) In the constriction phase, dynamin is recruited from patches in the cytoplasm to form the outer membrane mt-division machinery, with Mda1 and the outer MD ring.30) Then dynamin drives the sliding of the MD ring fine filaments and causes the contraction required for mitochondrial division. At the late phase of mitochondrial division, the dynamin molecules move from the surface of the outer membrane mt-division machinery to the inside of the machinery (Fig. 5A).30) Praefcke and McMahon (2004) reviewed the superfamily of dynamins and the domain structure and function.33) Classical dynamins contain a GTPase domain, middle domain, pleckstrin-homology (PH) domain, GTPase effector doman (GED) and proline-rich domain. Dynamin probably pinches off the membranes at the bridge between the daughter plastids by a biochemical reaction between the PH domain and the double membrane. After mitochondrial division, the remnants of the mt-division machinery then adhere to one side of the daughter mitochondria and the dynamin ring is broken into small patches.26)

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