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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 origin of eukaryotic cells (A) and dynamic events of bacterial division machineries and mitochondria during endosymbiosis with phagocytosis and vesicle-division machineries (B). A. Origin and evolution of eukaryotic cells with emphasis on mt- and pt-division machineries, including plasma membrane vesicle division, and cytoplasmic vesicle division. Basic eukaryotic cells are composed of double-membrane-bound organelles (cell nucleus, mitochondrion and plastid and single-membrane-bound organelles (ER, Golgi apparatus, lysosomes (vacuoles), microbodies). With phagocytosis, microbodies, mitochondria, and plastids are generated from Eubacteria. The formation of eukaryotic cell organelles consists of two phases: before and after mitochondria and plastids are generated from phagocytosis. B. Schematic representation of the bacterial division machinery, the vesicle division machinery, the inner membrane mt-division machinery and the outer membrane mt-division machinery. Eubacteria divided using bacterial division proteins. Almost all bacterial proteins were lost during endosymbiosis and FtsZ and ZED remained in inner mt-division machineries in eukaryotes. A is from Ref. 3.
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fig07: Schematic representation of the origin of eukaryotic cells (A) and dynamic events of bacterial division machineries and mitochondria during endosymbiosis with phagocytosis and vesicle-division machineries (B). A. Origin and evolution of eukaryotic cells with emphasis on mt- and pt-division machineries, including plasma membrane vesicle division, and cytoplasmic vesicle division. Basic eukaryotic cells are composed of double-membrane-bound organelles (cell nucleus, mitochondrion and plastid and single-membrane-bound organelles (ER, Golgi apparatus, lysosomes (vacuoles), microbodies). With phagocytosis, microbodies, mitochondria, and plastids are generated from Eubacteria. The formation of eukaryotic cell organelles consists of two phases: before and after mitochondria and plastids are generated from phagocytosis. B. Schematic representation of the bacterial division machinery, the vesicle division machinery, the inner membrane mt-division machinery and the outer membrane mt-division machinery. Eubacteria divided using bacterial division proteins. Almost all bacterial proteins were lost during endosymbiosis and FtsZ and ZED remained in inner mt-division machineries in eukaryotes. A is from Ref. 3.

Mentions: The first two steps are particularly interesting. Vesicle division rings around the neck of vesicle buds seem to play a role in phagocytosis (Fig. 7A, B).3,43) The formation of clathrin-coated vesicles could serve as a guide, as the use of dynamin-related proteins during the severing of vesicles at the plasma membrane and during division of the mitochondrial outer membrane suggests a common evolutionary origin.3,4,43) van del Bliek (2000) imagined that the first endosymbiotic bacteria used dynamin of the host cell during the entry at the plasma membrane and used it again during division of its outer membrane, before eventually giving rise to modern day mitochondria.43) A small (40 nm diameter) electron-dense ring was observed around the neck of vesicle buds formed from the plasma membrane.44) Since then, it has been generally believed that this electron-dense ring, or spiral, consists of dynamin recruited to the vesicle necks. This hypothesis was supported by the fact that the endocytic protein, GTPase dynamin, binds directly to liposomes, deforming them into tubules in vitro, and plays critical roles in membrane fission and curvature during clathrin-mediated endocytosis. However, several problems remain to be solved.3,15) There is no direct in vivo evidence that the vesicle division rings contain dynamin. Using immunoelectron microscopy with antibodies to dynamin, gold particles indicating dynamin signals were not located directly on the filaments of the vesicle division ring in vivo, but only near the vesicle ring. The dynamin rings in mt- and pt-division machineries in C. merolae were 20 or 100 times larger in diameter and more than 1,000 times greater in volume than those of the vesicle division machinery. However, even when the dynamin rings were observed clearly by immunoelectron and immunofluorescent microscopy, they were never observed directly using electron microscopy. Thus, the vesicle division machineries were considered to be analogous to the mt- and pt-division machineries were considered: the collar is composed of vesicle division rings, dynamin rings, and putative rings, and is divided by a biochemical reaction between one domain in the vesicle division machinery and the constricted plasma membrane (Fig. 7A, B).3,15) It is presumed that the vesicle division ring is similar to prototypes of the outer mt- and pt-division machineries; therefore, it seemed logical to hypothesize that they evolved into these outer membrane organelle division machineries (Fig. 7A, B).3,15,43)


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 origin of eukaryotic cells (A) and dynamic events of bacterial division machineries and mitochondria during endosymbiosis with phagocytosis and vesicle-division machineries (B). A. Origin and evolution of eukaryotic cells with emphasis on mt- and pt-division machineries, including plasma membrane vesicle division, and cytoplasmic vesicle division. Basic eukaryotic cells are composed of double-membrane-bound organelles (cell nucleus, mitochondrion and plastid and single-membrane-bound organelles (ER, Golgi apparatus, lysosomes (vacuoles), microbodies). With phagocytosis, microbodies, mitochondria, and plastids are generated from Eubacteria. The formation of eukaryotic cell organelles consists of two phases: before and after mitochondria and plastids are generated from phagocytosis. B. Schematic representation of the bacterial division machinery, the vesicle division machinery, the inner membrane mt-division machinery and the outer membrane mt-division machinery. Eubacteria divided using bacterial division proteins. Almost all bacterial proteins were lost during endosymbiosis and FtsZ and ZED remained in inner mt-division machineries in eukaryotes. A is from Ref. 3.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig07: Schematic representation of the origin of eukaryotic cells (A) and dynamic events of bacterial division machineries and mitochondria during endosymbiosis with phagocytosis and vesicle-division machineries (B). A. Origin and evolution of eukaryotic cells with emphasis on mt- and pt-division machineries, including plasma membrane vesicle division, and cytoplasmic vesicle division. Basic eukaryotic cells are composed of double-membrane-bound organelles (cell nucleus, mitochondrion and plastid and single-membrane-bound organelles (ER, Golgi apparatus, lysosomes (vacuoles), microbodies). With phagocytosis, microbodies, mitochondria, and plastids are generated from Eubacteria. The formation of eukaryotic cell organelles consists of two phases: before and after mitochondria and plastids are generated from phagocytosis. B. Schematic representation of the bacterial division machinery, the vesicle division machinery, the inner membrane mt-division machinery and the outer membrane mt-division machinery. Eubacteria divided using bacterial division proteins. Almost all bacterial proteins were lost during endosymbiosis and FtsZ and ZED remained in inner mt-division machineries in eukaryotes. A is from Ref. 3.
Mentions: The first two steps are particularly interesting. Vesicle division rings around the neck of vesicle buds seem to play a role in phagocytosis (Fig. 7A, B).3,43) The formation of clathrin-coated vesicles could serve as a guide, as the use of dynamin-related proteins during the severing of vesicles at the plasma membrane and during division of the mitochondrial outer membrane suggests a common evolutionary origin.3,4,43) van del Bliek (2000) imagined that the first endosymbiotic bacteria used dynamin of the host cell during the entry at the plasma membrane and used it again during division of its outer membrane, before eventually giving rise to modern day mitochondria.43) A small (40 nm diameter) electron-dense ring was observed around the neck of vesicle buds formed from the plasma membrane.44) Since then, it has been generally believed that this electron-dense ring, or spiral, consists of dynamin recruited to the vesicle necks. This hypothesis was supported by the fact that the endocytic protein, GTPase dynamin, binds directly to liposomes, deforming them into tubules in vitro, and plays critical roles in membrane fission and curvature during clathrin-mediated endocytosis. However, several problems remain to be solved.3,15) There is no direct in vivo evidence that the vesicle division rings contain dynamin. Using immunoelectron microscopy with antibodies to dynamin, gold particles indicating dynamin signals were not located directly on the filaments of the vesicle division ring in vivo, but only near the vesicle ring. The dynamin rings in mt- and pt-division machineries in C. merolae were 20 or 100 times larger in diameter and more than 1,000 times greater in volume than those of the vesicle division machinery. However, even when the dynamin rings were observed clearly by immunoelectron and immunofluorescent microscopy, they were never observed directly using electron microscopy. Thus, the vesicle division machineries were considered to be analogous to the mt- and pt-division machineries were considered: the collar is composed of vesicle division rings, dynamin rings, and putative rings, and is divided by a biochemical reaction between one domain in the vesicle division machinery and the constricted plasma membrane (Fig. 7A, B).3,15) It is presumed that the vesicle division ring is similar to prototypes of the outer mt- and pt-division machineries; therefore, it seemed logical to hypothesize that they evolved into these outer membrane organelle division machineries (Fig. 7A, B).3,15,43)

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