Mitochondrial genome function and maternal inheritance

Allen, John F.; Paula, Wilson B. M. de

doi:10.1042/bst20130106

Cited by 26 publications

(31 citation statements)

References 65 publications

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“…Yet the observation is that females in active bilaterians invariably combine early germline sequestration with large oocytes, in the extreme packed with several orders of magnitude more mitochondria than are present in normal cells (10 6 versus ~10 3 ) [19]. The model seems at odds with these observations.…”

Section: Resultsmentioning

confidence: 99%

“…The model shows that the early sequestration of large oocytes is more likely to be favoured when accompanied by specific lowering of μ B (Fig 3 and S4 Fig). This is the case in the female germline of most [15,19] but not all [28,29] bilaterians. Even when mitochondria are active it is possible that other specific adaptations could suppress μ B , for example, through upregulating antioxidant or DNA repair enzymes [28].…”

Section: Discussionmentioning

confidence: 99%

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Selection for Mitochondrial Quality Drives Evolution of the Germline

et al. 2016

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The origin of the germline–soma distinction is a fundamental unsolved question. Plants and basal metazoans do not have a germline but generate gametes from pluripotent stem cells in somatic tissues (somatic gametogenesis). In contrast, most bilaterians sequester a dedicated germline early in development. We develop an evolutionary model which shows that selection for mitochondrial quality drives germline evolution. In organisms with low mitochondrial replication error rates, segregation of mutations over multiple cell divisions generates variation, allowing selection to optimize gamete quality through somatic gametogenesis. Higher mutation rates promote early germline sequestration. We also consider how oogamy (a large female gamete packed with mitochondria) alters selection on the germline. Oogamy is beneficial as it reduces mitochondrial segregation in early development, improving adult fitness by restricting variation between tissues. But it also limits variation between early-sequestered oocytes, undermining gamete quality. Oocyte variation is restored through proliferation of germline cells, producing more germ cells than strictly needed, explaining the random culling (atresia) of precursor cells in bilaterians. Unlike other models of germline evolution, selection for mitochondrial quality can explain the stability of somatic gametogenesis in plants and basal metazoans, the evolution of oogamy in all plants and animals with tissue differentiation, and the mutational forces driving early germline sequestration in active bilaterians. The origins of predation in motile bilaterians in the Cambrian explosion is likely to have increased rates of tissue turnover and mitochondrial replication errors, in turn driving germline evolution and the emergence of complex developmental processes.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Selection for Mitochondrial Quality Drives Evolution of the Germline

et al. 2016

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“…According to this view, separation of a line of quiescent, template mitochondria maintains the integrity of mtDNA through the female germ line and between generations (Allen 1996; Allen and de Paula 2013). This hypothesis appears to be consistent with observations reported for mitochondria of a cnidarian, the jellyfish Aurelia aurita (de Paula et al 2013).…”

Section: Introductionmentioning

confidence: 99%

Female and Male Gamete Mitochondria Are Distinct and Complementary in Transcription, Structure, and Genome Function

Paula

Agip

Missirlis

et al. 2013

Genome Biology and Evolution

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Respiratory electron transport in mitochondria is coupled to ATP synthesis while generating mutagenic oxygen free radicals. Mitochondrial DNA mutation then accumulates with age, and may set a limit to the lifespan of individual, multicellular organisms. Why is this mutation not inherited? Here we demonstrate that female gametes—oocytes—have unusually small and simple mitochondria that are suppressed for DNA transcription, electron transport, and free radical production. By contrast, male gametes—sperm—and somatic cells of both sexes transcribe mitochondrial genes for respiratory electron carriers and produce oxygen free radicals. This germ-line division between mitochondria of sperm and egg is observed in both the vinegar fruitfly and the zebrafish—species spanning a major evolutionary divide within the animal kingdom. We interpret these findings as an evidence that oocyte mitochondria serve primarily as genetic templates, giving rise, irreversibly and in each new generation, to the familiar energy-transducing mitochondria of somatic cells and male gametes. Suppressed mitochondrial metabolism in the female germ line may therefore constitute a mechanism for increasing the fidelity of mitochondrial DNA inheritance.

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“…Mitochondria in mammalian oocytes are spherical with little cristae [2]. These mitochondria are transcriptionally and bioenergetically silent and this functional state seems to be evolutionarily conserved [12,13], especially in immature eggs, which have slow ATP production [14]. This quiescent state is believed to be important to keep the number of mitochondrial DNA mutations to minimum, as these mutations will then be passed down to the embryo [13].…”

Section: The Role Of Mitochondria In Oocyte Biologymentioning

confidence: 99%

Oocyte mitochondrial function and reproduction

Babayev

Seli²

2015

Current Opinion in Obstetrics &Amp; Gynecology

257

179

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Purpose of review Mitochondria are cellular organelles that are required for energy production. Emerging evidence demonstrates their role in oocyte development and reproduction. In this review, we examine recent animal and clinical studies on the role of mitochondria in fertility. We also analyse the impact of assisted reproductive techniques (ARTs) on mitochondrial function and discuss the future clinical implications of mitochondrial nutrients and mitochondrial replacement. Recent findings Mitochondria affect all aspects of mammalian reproduction. They are essential for optimal oocyte maturation, fertilization and embryonic development. Mitochondrial dysfunction causes a decrease in oocyte quality and interferes with embryonic development. ART procedures affect mitochondrial function, while mitochondrial nutrients may increase mitochondrial performance in oocytes. New mitochondrial replacement procedures using mitochondria obtained from polar bodies or from the patient’s own oogonial stem cells are promising and may address concerns related to the induction of high-levels of heteroplasmy, which could potentially result in negative long-term health effects. Summary Optimal energy production is required for oocyte and embryo development, and mitochondrial abnormalities have devastating reproductive consequences. Improvement of oocyte mitochondrial function via intake of compounds that boost mitochondrial activity may have clinical benefits, and mitochondrial replacement could potentially be used for the prevention of mitochondrial diseases.

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Mitochondrial genome function and maternal inheritance

Cited by 26 publications

References 65 publications

Selection for Mitochondrial Quality Drives Evolution of the Germline

Selection for Mitochondrial Quality Drives Evolution of the Germline

Female and Male Gamete Mitochondria Are Distinct and Complementary in Transcription, Structure, and Genome Function

Oocyte mitochondrial function and reproduction

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