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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 micrographs of living young zygotes of C. reinhardtii (A), gametes and a zygote of P. polycephalum (D), sperm mitochondria of Oryzias latipes (G, H), patterns of nested PCR after mating (fertilization) of C. reinhardtii (B) and O. latipes (I) and models of active digestion of male plastid DNA (C), fertilization of vertebrate (E) and process of microinjection and the development of injected eggs (F). A. Preferential disappearance of male plastid nuclei (yellow) visualized in a SYBR Green I stained living zygote 50 min after mating. B. Male gamete plastid DNA is digested within 90 min after mating. C. During gametogenesis, nuclease C is synthesized or activated only in female (mt+) cells. At the same time, female plastid DNA becomes resistant to the action of nuclease C. During gamete fusion, nuclease C obtains access to unprotected male plastids and digests the male plastid DNA, leading to maternal inheritance of plastid DNA. Several factors might mediate the successful digestion of male plastid DNA after zygote formation. D. Each amoeba contained about 12 mitochondria and each mitochondrion was characterized by the rod shaped mt-nucleus at its center (blue in D). 1 hr after nuclear fusion, mt-nucleus fluorescence completely disappeared in about half of the mitochondria in the zygote (arrows). E. A large egg fertilizes with a sperm. F. After injection, the eggs remained intact and progressed through normal developmental stages. G and H. Phase-contrast and SYBR green I-MitoTracker double-stained images showed mitochondria (red) in sperm before (G) and sperms in fertilized egg (H) after fertilization. Sperm mitochondrial nuclei (yellow) disappeared completely 60 min after fertilization (right). I. Single sperm with or without mitochondrial nuclei was selectively extracted from fertilized eggs using optical tweezers and analyzed by nested PCR. Sperm and eggs were derived from AA2, and the HNI PCR product was added to each reaction as an internal control. Active digestion of sperm mitochondrial DNA (AA2) occurred 60 min after injection into eggs (right). N and n, cell nuclei. Scale bars: 0.5 mm (F), 5 µm (A, D), and 1 µm (G). Scale bars = 1 µm. A and B are from Ref. 36, C is from Ref. 37, D is from Ref. 39, F-I are from Ref. 40.
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fig06: Fluorescence micrographs of living young zygotes of C. reinhardtii (A), gametes and a zygote of P. polycephalum (D), sperm mitochondria of Oryzias latipes (G, H), patterns of nested PCR after mating (fertilization) of C. reinhardtii (B) and O. latipes (I) and models of active digestion of male plastid DNA (C), fertilization of vertebrate (E) and process of microinjection and the development of injected eggs (F). A. Preferential disappearance of male plastid nuclei (yellow) visualized in a SYBR Green I stained living zygote 50 min after mating. B. Male gamete plastid DNA is digested within 90 min after mating. C. During gametogenesis, nuclease C is synthesized or activated only in female (mt+) cells. At the same time, female plastid DNA becomes resistant to the action of nuclease C. During gamete fusion, nuclease C obtains access to unprotected male plastids and digests the male plastid DNA, leading to maternal inheritance of plastid DNA. Several factors might mediate the successful digestion of male plastid DNA after zygote formation. D. Each amoeba contained about 12 mitochondria and each mitochondrion was characterized by the rod shaped mt-nucleus at its center (blue in D). 1 hr after nuclear fusion, mt-nucleus fluorescence completely disappeared in about half of the mitochondria in the zygote (arrows). E. A large egg fertilizes with a sperm. F. After injection, the eggs remained intact and progressed through normal developmental stages. G and H. Phase-contrast and SYBR green I-MitoTracker double-stained images showed mitochondria (red) in sperm before (G) and sperms in fertilized egg (H) after fertilization. Sperm mitochondrial nuclei (yellow) disappeared completely 60 min after fertilization (right). I. Single sperm with or without mitochondrial nuclei was selectively extracted from fertilized eggs using optical tweezers and analyzed by nested PCR. Sperm and eggs were derived from AA2, and the HNI PCR product was added to each reaction as an internal control. Active digestion of sperm mitochondrial DNA (AA2) occurred 60 min after injection into eggs (right). N and n, cell nuclei. Scale bars: 0.5 mm (F), 5 µm (A, D), and 1 µm (G). Scale bars = 1 µm. A and B are from Ref. 36, C is from Ref. 37, D is from Ref. 39, F-I are from Ref. 40.

Mentions: Maternal inheritance of organelle genomes was thought to result from dilution of the paternal contribution. This is because the paternal gametes (sperm) are much smaller than maternal gametes (egg) and contribute only a small amount of cytoplasm to the progeny. However, if this idea is correct, maternal transmission of organelle DNA should not occur in isogamous organisms where there are no size differences between male and female gametes. Therefore, to obtain direct evidence for sexual transmission of organelle DNAs, we examined their behaviors in gametes and young zygotes of the isogamous alga Chlamydomonas reinhardtii using high resolution fluorescence microscopy. The preferential digestion of male (mt−) gamete-originated plastid (pt-) DNA occurred, while pt-DNA originating from female (mt+) gametes remained 50 min after mating of female and male gametes (Fig. 6A, B).35,36) They were observed in living cells (Fig. 6A) and confirmed by nested PCR (Fig. 6B). Thereafter, the maternal (uniparental) transmission of organelles that resulted from “the active digestion of male organelle nuclei (genomes) in young zygotes” was observed in almost all algae and land plants.4,13,37) The mechanism was analyzed by molecular and cellular biological techniques (Fig. 6C). A model for the molecular mechanism of uniparental inheritance in C. reinhardtii was proposed on the basis of the active digestion of male plastid DNA by the Ca2+-dependent nuclease MDN (mt+-specific DNase, 140 kDa).4,37) In vegetative cells, MDN is absent or inactivated in both mating types. During gametogenesis, MDN is synthesized or activated only in female cells.36) At the same time, female pt-DNA becomes resistant to the action of MDN. During gamete fusion, MDN obtains access to unprotected male plastids and digests the male pt-DNA, leading to the uniparental inheritance of pt-DNA. Several factors might mediate the successful digestion of male plastid DNA after zygote formation: (1) entry of MDN into male plastids; (2) efficient access of MDN to plastid DNA molecules; and (3) an increase in Ca2+ concentration inside male plastids. Zygote-specific gene expression might be crucial to these processes (Fig. 6C).37)


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 micrographs of living young zygotes of C. reinhardtii (A), gametes and a zygote of P. polycephalum (D), sperm mitochondria of Oryzias latipes (G, H), patterns of nested PCR after mating (fertilization) of C. reinhardtii (B) and O. latipes (I) and models of active digestion of male plastid DNA (C), fertilization of vertebrate (E) and process of microinjection and the development of injected eggs (F). A. Preferential disappearance of male plastid nuclei (yellow) visualized in a SYBR Green I stained living zygote 50 min after mating. B. Male gamete plastid DNA is digested within 90 min after mating. C. During gametogenesis, nuclease C is synthesized or activated only in female (mt+) cells. At the same time, female plastid DNA becomes resistant to the action of nuclease C. During gamete fusion, nuclease C obtains access to unprotected male plastids and digests the male plastid DNA, leading to maternal inheritance of plastid DNA. Several factors might mediate the successful digestion of male plastid DNA after zygote formation. D. Each amoeba contained about 12 mitochondria and each mitochondrion was characterized by the rod shaped mt-nucleus at its center (blue in D). 1 hr after nuclear fusion, mt-nucleus fluorescence completely disappeared in about half of the mitochondria in the zygote (arrows). E. A large egg fertilizes with a sperm. F. After injection, the eggs remained intact and progressed through normal developmental stages. G and H. Phase-contrast and SYBR green I-MitoTracker double-stained images showed mitochondria (red) in sperm before (G) and sperms in fertilized egg (H) after fertilization. Sperm mitochondrial nuclei (yellow) disappeared completely 60 min after fertilization (right). I. Single sperm with or without mitochondrial nuclei was selectively extracted from fertilized eggs using optical tweezers and analyzed by nested PCR. Sperm and eggs were derived from AA2, and the HNI PCR product was added to each reaction as an internal control. Active digestion of sperm mitochondrial DNA (AA2) occurred 60 min after injection into eggs (right). N and n, cell nuclei. Scale bars: 0.5 mm (F), 5 µm (A, D), and 1 µm (G). Scale bars = 1 µm. A and B are from Ref. 36, C is from Ref. 37, D is from Ref. 39, F-I are from Ref. 40.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig06: Fluorescence micrographs of living young zygotes of C. reinhardtii (A), gametes and a zygote of P. polycephalum (D), sperm mitochondria of Oryzias latipes (G, H), patterns of nested PCR after mating (fertilization) of C. reinhardtii (B) and O. latipes (I) and models of active digestion of male plastid DNA (C), fertilization of vertebrate (E) and process of microinjection and the development of injected eggs (F). A. Preferential disappearance of male plastid nuclei (yellow) visualized in a SYBR Green I stained living zygote 50 min after mating. B. Male gamete plastid DNA is digested within 90 min after mating. C. During gametogenesis, nuclease C is synthesized or activated only in female (mt+) cells. At the same time, female plastid DNA becomes resistant to the action of nuclease C. During gamete fusion, nuclease C obtains access to unprotected male plastids and digests the male plastid DNA, leading to maternal inheritance of plastid DNA. Several factors might mediate the successful digestion of male plastid DNA after zygote formation. D. Each amoeba contained about 12 mitochondria and each mitochondrion was characterized by the rod shaped mt-nucleus at its center (blue in D). 1 hr after nuclear fusion, mt-nucleus fluorescence completely disappeared in about half of the mitochondria in the zygote (arrows). E. A large egg fertilizes with a sperm. F. After injection, the eggs remained intact and progressed through normal developmental stages. G and H. Phase-contrast and SYBR green I-MitoTracker double-stained images showed mitochondria (red) in sperm before (G) and sperms in fertilized egg (H) after fertilization. Sperm mitochondrial nuclei (yellow) disappeared completely 60 min after fertilization (right). I. Single sperm with or without mitochondrial nuclei was selectively extracted from fertilized eggs using optical tweezers and analyzed by nested PCR. Sperm and eggs were derived from AA2, and the HNI PCR product was added to each reaction as an internal control. Active digestion of sperm mitochondrial DNA (AA2) occurred 60 min after injection into eggs (right). N and n, cell nuclei. Scale bars: 0.5 mm (F), 5 µm (A, D), and 1 µm (G). Scale bars = 1 µm. A and B are from Ref. 36, C is from Ref. 37, D is from Ref. 39, F-I are from Ref. 40.
Mentions: Maternal inheritance of organelle genomes was thought to result from dilution of the paternal contribution. This is because the paternal gametes (sperm) are much smaller than maternal gametes (egg) and contribute only a small amount of cytoplasm to the progeny. However, if this idea is correct, maternal transmission of organelle DNA should not occur in isogamous organisms where there are no size differences between male and female gametes. Therefore, to obtain direct evidence for sexual transmission of organelle DNAs, we examined their behaviors in gametes and young zygotes of the isogamous alga Chlamydomonas reinhardtii using high resolution fluorescence microscopy. The preferential digestion of male (mt−) gamete-originated plastid (pt-) DNA occurred, while pt-DNA originating from female (mt+) gametes remained 50 min after mating of female and male gametes (Fig. 6A, B).35,36) They were observed in living cells (Fig. 6A) and confirmed by nested PCR (Fig. 6B). Thereafter, the maternal (uniparental) transmission of organelles that resulted from “the active digestion of male organelle nuclei (genomes) in young zygotes” was observed in almost all algae and land plants.4,13,37) The mechanism was analyzed by molecular and cellular biological techniques (Fig. 6C). A model for the molecular mechanism of uniparental inheritance in C. reinhardtii was proposed on the basis of the active digestion of male plastid DNA by the Ca2+-dependent nuclease MDN (mt+-specific DNase, 140 kDa).4,37) In vegetative cells, MDN is absent or inactivated in both mating types. During gametogenesis, MDN is synthesized or activated only in female cells.36) At the same time, female pt-DNA becomes resistant to the action of MDN. During gamete fusion, MDN obtains access to unprotected male plastids and digests the male pt-DNA, leading to the uniparental inheritance of pt-DNA. Several factors might mediate the successful digestion of male plastid DNA after zygote formation: (1) entry of MDN into male plastids; (2) efficient access of MDN to plastid DNA molecules; and (3) an increase in Ca2+ concentration inside male plastids. Zygote-specific gene expression might be crucial to these processes (Fig. 6C).37)

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