Review of cytological studies on cellular and molecular mechanisms of uniparental (maternal or paternal) inheritance of plastid and mitochondrial genomes induced by active digestion of organelle nuclei (nucleoids)

Kuroiwa, Tsuneyoshi

doi:10.1007/s10265-009-0306-9

Cited by 38 publications

(39 citation statements)

References 108 publications

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“…ptDNAs (and also mitochondrial DNAs [mtDNAs]) are cytologically detectable as nucleoids by staining tissues with DNA fluorescent dye, such as 49,6-diamidino-2-phenylindole (DAPI) or SYBR green I (SYBR) (Kuroiwa, 1991(Kuroiwa, , 2010. The ptDNAs exist as a complex with proteins that constitute plastid nucleoids (Sato et al, 1998(Sato et al, , 2001(Sato et al, , 2003Murakami et al, 2000;Jeong et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

A Conserved, Mg2+-Dependent Exonuclease Degrades Organelle DNA duringArabidopsisPollen Development

et al. 2011

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In plant cells, mitochondria and plastids contain their own genomes derived from the ancestral bacteria endosymbiont. Despite their limited genetic capacity, these multicopy organelle genomes account for a substantial fraction of total cellular DNA, raising the question of whether organelle DNA quantity is controlled spatially or temporally. In this study, we genetically dissected the organelle DNA decrease in pollen, a phenomenon that appears to be common in most angiosperm species. By staining mature pollen grains with fluorescent DNA dye, we screened Arabidopsis thaliana for mutants in which extrachromosomal DNAs had accumulated. Such a recessive mutant, termed defective in pollen organelle DNA degradation1 (dpd1), showing elevated levels of DNAs in both plastids and mitochondria, was isolated and characterized. DPD1 encodes a protein belonging to the exonuclease family, whose homologs appear to be found in angiosperms. Indeed, DPD1 has Mg 2+ -dependent exonuclease activity when expressed as a fusion protein and when assayed in vitro and is highly active in developing pollen. Consistent with the dpd phenotype, DPD1 is dual-targeted to plastids and mitochondria. Therefore, we provide evidence of active organelle DNA degradation in the angiosperm male gametophyte, primarily independent of maternal inheritance; the biological function of organellar DNA degradation in pollen is currently unclear.

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Section: Introductionmentioning

confidence: 99%

A Conserved, Mg2+-Dependent Exonuclease Degrades Organelle DNA duringArabidopsisPollen Development

et al. 2011

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“…4),14) In this review, I describe the mechanisms and machineries of organelle division and briefly summarize the mechanism of organelle inheritance, as recently reviewed. 4) Finally, the implications of the mechanisms of organelle division and inheritance regarding the evolutionally origin of eukaryotic cells are discussed.…”

Section: )mentioning

confidence: 99%

“…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).…”

Section: Mechanisms Of Maternal Inheritance Of Mitochondrial and The mentioning

confidence: 99%

“…One hundred years ago, Correns and Baur (1909) independently discovered that different plastid phenotypes were inherited in a non-Mendelian fashion in higher plants. 4) If their discoveries are taken as the first step, the history of the study of the inheritance of mitochondria and plastid genomes can be classified into four steps. 1) the discovery of nonMendelian plastid phenotypes.…”

Section: Introductionmentioning

confidence: 99%

“…3) sequencing of entire genomes of mitochondria and plastids, and 4) the discovery of a nucleus in mitochondria and plastids (the nucleoid; a complex of DNA and proteins). 4) 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.…”

Section: Introductionmentioning

confidence: 99%

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Erratum to “Mechanisms of organelle division and inheritance and their implications regarding the origin of eukaryotic cells”

KUROIWA¹

2017

Proceedings of the Japan Academy. Ser. B: Physical and Biologic

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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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Why are most organelle genomes transmitted maternally?

2014

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Why the DNA-containing organelles, chloroplasts, and mitochondria, are inherited maternally is a long standing and unsolved question. However, recent years have seen a paradigm shift, in that the absoluteness of uniparental inheritance is increasingly questioned. Here, we review the field and propose a unifying model for organelle inheritance. We argue that the predominance of the maternal mode is a result of higher mutational load in the paternal gamete. Uniparental inheritance evolved from relaxed organelle inheritance patterns because it avoids the spread of selfish cytoplasmic elements. However, on evolutionary timescales, uniparentally inherited organelles are susceptible to mutational meltdown (Muller's ratchet). To prevent this, fall-back to relaxed inheritance patterns occurs, allowing low levels of sexual organelle recombination. Since sexual organelle recombination is insufficient to mitigate the effects of selfish cytoplasmic elements, various mechanisms for uniparental inheritance then evolve again independently. Organelle inheritance must therefore be seen as an evolutionary unstable trait, with a strong general bias to the uniparental, maternal, mode.

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Review of cytological studies on cellular and molecular mechanisms of uniparental (maternal or paternal) inheritance of plastid and mitochondrial genomes induced by active digestion of organelle nuclei (nucleoids)

Cited by 38 publications

References 108 publications

A Conserved, Mg2+-Dependent Exonuclease Degrades Organelle DNA duringArabidopsisPollen Development

A Conserved, Mg2+-Dependent Exonuclease Degrades Organelle DNA duringArabidopsisPollen Development

Erratum to “Mechanisms of organelle division and inheritance and their implications regarding the origin of eukaryotic cells”

Why are most organelle genomes transmitted maternally?

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