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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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Fluorescence (A, G, H, I) and Nomarski/fluorescence (insert in G) microscopy, electron micrographs (B, C, D) and diagrammatic representations of cell division (E, F, J). A. A human cell stained with acridine orange. Only the cell nucleus (red) was visualized. B. The mitochondrion in Chlamydomonas reinhardtii is composed of many cristae around an electron transparent region. C and D. In Physarum polycephalum, the mitochondria contain electron dense rod-shaped mitochondrial nuclei (mt-nuclei) and mitochondriokinesis occurs using a small ring (indicated by an arrow in the enlarged image of D) after mt-nuclear division (mn in C). E and F. Change of concept of the cell. In addition to the cell nucleus (n), the DNAs in organelles (mitochondria and plastids) that are regard as ancestors of bacteria can be visualized as organellar nuclei (on in F). G, H, and I. The fluorescence images demonstrate mt-nuclei, pt-nuclei (rod-shaped or small spots) and the cell nucleus (n) in P. polycephalum (G), Nicotiana tabacum (H), and Homo sapiens (I). J. Organellar dynamics during life cycle of eukaryotes with non-sexual and sexual reproduction stages. Scale bars: 10 µm (A, H), 5 µm (I), 1 µm (G), and 0.1 µm (B,C). C and D are from Ref. 6, H is from Ref. 13, I is from Dr. Sasaki-Higashiyama, N.
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fig01: Fluorescence (A, G, H, I) and Nomarski/fluorescence (insert in G) microscopy, electron micrographs (B, C, D) and diagrammatic representations of cell division (E, F, J). A. A human cell stained with acridine orange. Only the cell nucleus (red) was visualized. B. The mitochondrion in Chlamydomonas reinhardtii is composed of many cristae around an electron transparent region. C and D. In Physarum polycephalum, the mitochondria contain electron dense rod-shaped mitochondrial nuclei (mt-nuclei) and mitochondriokinesis occurs using a small ring (indicated by an arrow in the enlarged image of D) after mt-nuclear division (mn in C). E and F. Change of concept of the cell. In addition to the cell nucleus (n), the DNAs in organelles (mitochondria and plastids) that are regard as ancestors of bacteria can be visualized as organellar nuclei (on in F). G, H, and I. The fluorescence images demonstrate mt-nuclei, pt-nuclei (rod-shaped or small spots) and the cell nucleus (n) in P. polycephalum (G), Nicotiana tabacum (H), and Homo sapiens (I). J. Organellar dynamics during life cycle of eukaryotes with non-sexual and sexual reproduction stages. Scale bars: 10 µm (A, H), 5 µm (I), 1 µm (G), and 0.1 µm (B,C). C and D are from Ref. 6, H is from Ref. 13, I is from Dr. Sasaki-Higashiyama, N.

Mentions: The discovery of mitochondrial (mt-) and plastidal (pt-) nuclei was important for the study of organelle division and inheritance. After the discovery of non-Mendelian phenotypes, a new phase in the study of traits inherited in a non-Mendelian manner began with genetic studies of microorganisms. However, these studies could not identify the non-Mendelian factor in the heredity of the cells. Electron microscopy demonstrated that plastids of alga5) and the mitochondria of animals contained DNA-like fibrils in electron transparent regions.6) Although molecular biological studies on the structure of organellar DNA and the sequencing of organelle genomes has progressed,7) it has proved difficult to observe DNA in mitochondria and plastids in vivo (Fig. 1A, B). Thus, it was thought that organelle DNAs, as well as bacterial DNAs, were naked in cells. In 1973–1974, we discovered that mitochondria in the slime mould Physarum polycephalum contained a large amount of mt-DNA, which was organized with proteins to form a rod-shaped electron dense mt-nucleus (Fig. 1C, D).6,8) The mitochondria divided according to a simple sequence, including spherule-, ovoid- and dumbbell-shaped structures, along with mt-nuclear division (Fig. 1C, D).6,9) The process of mt-division can be clearly classified into two main events: mt-nuclear division and mitochondriokinesis (also called mitochondrial division). These events in the division of the Physarum mitochondria seemed to be similar to those in the division of Rickettsiella melolonthae,9) suggesting that mitochondria could be regarded as descendants of endosymbiotic prokaryotes (Fig. 1E, F). The hypothesis is confirmed by the genome sequencing of Rickettsiella.10)


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)

Fluorescence (A, G, H, I) and Nomarski/fluorescence (insert in G) microscopy, electron micrographs (B, C, D) and diagrammatic representations of cell division (E, F, J). A. A human cell stained with acridine orange. Only the cell nucleus (red) was visualized. B. The mitochondrion in Chlamydomonas reinhardtii is composed of many cristae around an electron transparent region. C and D. In Physarum polycephalum, the mitochondria contain electron dense rod-shaped mitochondrial nuclei (mt-nuclei) and mitochondriokinesis occurs using a small ring (indicated by an arrow in the enlarged image of D) after mt-nuclear division (mn in C). E and F. Change of concept of the cell. In addition to the cell nucleus (n), the DNAs in organelles (mitochondria and plastids) that are regard as ancestors of bacteria can be visualized as organellar nuclei (on in F). G, H, and I. The fluorescence images demonstrate mt-nuclei, pt-nuclei (rod-shaped or small spots) and the cell nucleus (n) in P. polycephalum (G), Nicotiana tabacum (H), and Homo sapiens (I). J. Organellar dynamics during life cycle of eukaryotes with non-sexual and sexual reproduction stages. Scale bars: 10 µm (A, H), 5 µm (I), 1 µm (G), and 0.1 µm (B,C). C and D are from Ref. 6, H is from Ref. 13, I is from Dr. Sasaki-Higashiyama, N.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig01: Fluorescence (A, G, H, I) and Nomarski/fluorescence (insert in G) microscopy, electron micrographs (B, C, D) and diagrammatic representations of cell division (E, F, J). A. A human cell stained with acridine orange. Only the cell nucleus (red) was visualized. B. The mitochondrion in Chlamydomonas reinhardtii is composed of many cristae around an electron transparent region. C and D. In Physarum polycephalum, the mitochondria contain electron dense rod-shaped mitochondrial nuclei (mt-nuclei) and mitochondriokinesis occurs using a small ring (indicated by an arrow in the enlarged image of D) after mt-nuclear division (mn in C). E and F. Change of concept of the cell. In addition to the cell nucleus (n), the DNAs in organelles (mitochondria and plastids) that are regard as ancestors of bacteria can be visualized as organellar nuclei (on in F). G, H, and I. The fluorescence images demonstrate mt-nuclei, pt-nuclei (rod-shaped or small spots) and the cell nucleus (n) in P. polycephalum (G), Nicotiana tabacum (H), and Homo sapiens (I). J. Organellar dynamics during life cycle of eukaryotes with non-sexual and sexual reproduction stages. Scale bars: 10 µm (A, H), 5 µm (I), 1 µm (G), and 0.1 µm (B,C). C and D are from Ref. 6, H is from Ref. 13, I is from Dr. Sasaki-Higashiyama, N.
Mentions: The discovery of mitochondrial (mt-) and plastidal (pt-) nuclei was important for the study of organelle division and inheritance. After the discovery of non-Mendelian phenotypes, a new phase in the study of traits inherited in a non-Mendelian manner began with genetic studies of microorganisms. However, these studies could not identify the non-Mendelian factor in the heredity of the cells. Electron microscopy demonstrated that plastids of alga5) and the mitochondria of animals contained DNA-like fibrils in electron transparent regions.6) Although molecular biological studies on the structure of organellar DNA and the sequencing of organelle genomes has progressed,7) it has proved difficult to observe DNA in mitochondria and plastids in vivo (Fig. 1A, B). Thus, it was thought that organelle DNAs, as well as bacterial DNAs, were naked in cells. In 1973–1974, we discovered that mitochondria in the slime mould Physarum polycephalum contained a large amount of mt-DNA, which was organized with proteins to form a rod-shaped electron dense mt-nucleus (Fig. 1C, D).6,8) The mitochondria divided according to a simple sequence, including spherule-, ovoid- and dumbbell-shaped structures, along with mt-nuclear division (Fig. 1C, D).6,9) The process of mt-division can be clearly classified into two main events: mt-nuclear division and mitochondriokinesis (also called mitochondrial division). These events in the division of the Physarum mitochondria seemed to be similar to those in the division of Rickettsiella melolonthae,9) suggesting that mitochondria could be regarded as descendants of endosymbiotic prokaryotes (Fig. 1E, F). The hypothesis is confirmed by the genome sequencing of Rickettsiella.10)

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