Transmission of Functional, Wild-Type Mitochondria and the Fittest mtDNA to the Next Generation: Bottleneck Phenomenon, Balbiani Body, and Mitophagy
Abstract
:1. Introduction
2. Categories (Types) of Animal Ovaries
3. Selection of Highly Active (“Healthy”) Mitochondria and the Balbiani Body—The High Energy Pathway
- The early germline cells receive mitochondria in various functional states. They are not selected but partitioned to the individual germline cells stochastically as assumed in the bottleneck phenomenon.
- As oogenesis progresses, the mitochondria present in each germline cell gather next to the nucleus and form the Bb. Within the Bb, mitochondria multiply and fuse forming an extensive local network.
- Dysfunctional mitochondrial units (containing mutated mtDNA) are separated from the network and eliminated by mitophagy.
- After dispersal of the Bb selected (healthy) mitochondria populate the ooplasm.
- Labelling with various antibodies and fluorescent probes showed that in the oocytes of a sea urchin, Paracentrotus lividus highly active mitochondria accumulate next to the germinal vesicle and here colocalize with vesicular acidic organelles (autophagosomes, autolysosomes) [35,36]. Thus, the arrangement of organelles in sea urchin oocytes mimics those in Thermobia.
- Autoradiographic studies revealed that in Xenopus Bb mtDNA is replicated synchronously “in neighboring mitochondria” [32] implying that in this species several smaller mitochondrial networks may coexist within single Bb.
- In murine oocytes the number of mitochondria remaining in physical contact has been estimated to increase from 21–58% during Bb formation [37]. Moreover, reevaluation of microphotographs published elsewhere (e.g., Figure 5B,F in [37]; 1E in [38]; 7B in [39]) suggests that the Bb mitochondria are also interconnected in mammals.
- It has been recently shown, using an allele-specific FISH approach, that mitochondrial fragmentation is responsible for the removal of mutated mtDNA in the female germline cells of Drosophila [40].
4. Silencing the Mitochondrial Activity—Low Energy Pathway
5. Can High Energy and Low Energy Pathways Coexist in Related Animal Lineages?
6. Conclusions and Future Perspectives
- On the basis of our EM studies, we suggest that the “high energy” and “low energy” pathways may operate even in closely related lineages of a given taxon. This, in turn, implies that these pathways are not evolutionary conserved and are rather related to morpho-functional characteristics of the ovaries as for instance: presence/absence of the nurse cells associated with the oocyte or presence of the Bb in the ooplasm.
- It is well known that in the ovaries of both vertebrates and invertebrates, a relatively large fraction of young germline cells is eliminated via apoptosis [53,54,55,56]. We believe, in this context that the selection of the mitochondria in oocytes is a two-step process: The first step operates at the cellular level and involves selection of mitochondria and mtDNA variants. In the second, all the germline cells that still (after the first step) contain large number of mutated mtDNA are eliminated via apoptosis. This idea is in line with our EM analyses showing that in apoptotic oocytes of Thermobia, the Bbs mitochondria reveal highly altered morphology (Figure 1C).
- The mechanisms responsible for mitochondrial inheritance obviously need further studies. There are at least two fundamental questions that should be answered:
- How replication of mtDNA (and consequent multiplication of mitochondria) located within the Bb is initiated? Is nuage material implicated in this initiation?
- Is recruitment of highly functional and healthy mitochondria to the Bb guaranteed by cytoskeleton (microtubules) as suggested by Milani [8] or it is an obvious consequence of a bottleneck phenomenon?
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Tworzydlo, W.; Sekula, M.; Bilinski, S.M. Transmission of Functional, Wild-Type Mitochondria and the Fittest mtDNA to the Next Generation: Bottleneck Phenomenon, Balbiani Body, and Mitophagy. Genes 2020, 11, 104. https://doi.org/10.3390/genes11010104
Tworzydlo W, Sekula M, Bilinski SM. Transmission of Functional, Wild-Type Mitochondria and the Fittest mtDNA to the Next Generation: Bottleneck Phenomenon, Balbiani Body, and Mitophagy. Genes. 2020; 11(1):104. https://doi.org/10.3390/genes11010104
Chicago/Turabian StyleTworzydlo, Waclaw, Malgorzata Sekula, and Szczepan M. Bilinski. 2020. "Transmission of Functional, Wild-Type Mitochondria and the Fittest mtDNA to the Next Generation: Bottleneck Phenomenon, Balbiani Body, and Mitophagy" Genes 11, no. 1: 104. https://doi.org/10.3390/genes11010104
APA StyleTworzydlo, W., Sekula, M., & Bilinski, S. M. (2020). Transmission of Functional, Wild-Type Mitochondria and the Fittest mtDNA to the Next Generation: Bottleneck Phenomenon, Balbiani Body, and Mitophagy. Genes, 11(1), 104. https://doi.org/10.3390/genes11010104