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Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis
H Kaneda1, J Hayashi, S Takahama
1Department of Laboratory Animal Science, Tokyo Metropolitan Institute of Medical Science, Japan.
Abstract:
To examine whether mtDNA is uni- or biparentally transmitted in mice, we developed an assay that can detect sperm mtDNA in a single mouse embryo. In intraspecific hybrids of Mus musculus, paternal mtDNA was detected only through the early pronucleus stage, and its disappearance co-incided with loss of membrane potential in sperm-derived mitochondria. By contrast, in interspecific hybrids between M. musculus and Mus spretus, paternal mtDNA was detected throughout development from pronucleus stage to neonates. We propose that oocyte cytoplasm has a species-specific mechanism that recognizes and eliminates sperm mitochondria and mtDNA. This mechanism must recognize nuclearly encoded proteins in the sperm midpiece, and not the mtDNA or the proteins it encodes, because sperm mitochondria from the congenic strain B6.mtspr, which carries M. spretus mtDNA on background of M. musculus (B6) nuclear genes, were eliminated early by B6 oocytes as in intraspecific crosses. We conclude that cytoplasmic genomes are transmitted uniparentally in intraspecific crosses in mammals as in Chlamydomonas and that leakage of parental mtDNA is limited to interspecific crosses, which rarely occur in nature.
Insights
Mitochondrial DNA (mtDNA) is usually uniparentally transmitted in mice. However, sperm mtDNA can persist in embryos during rare interspecific crosses, suggesting a species-specific oocyte mechanism for eliminating paternal mitochondria.
Area of Science:
- Genetics
- Cell Biology
- Reproductive Biology
Background:
- Mitochondrial DNA (mtDNA) inheritance patterns are crucial for understanding cellular and organismal biology.
- While often uniparental, exceptions to strict maternal inheritance of mtDNA exist in some species.
- Investigating paternal mtDNA transmission in mammals provides insights into reproductive barriers and evolutionary mechanisms.
Purpose of the Study:
- To determine if mitochondrial DNA (mtDNA) is transmitted uniparentally or biparentally in mice.
- To investigate the role of oocyte cytoplasm in the elimination of sperm mitochondria.
- To identify the factors responsible for the recognition and degradation of paternal mtDNA.
Main Methods:
- Development of a sensitive assay to detect sperm mtDNA in single mouse embryos.
- Analysis of paternal mtDNA transmission in intraspecific (Mus musculus) and interspecific (Mus musculus x Mus spretus) mouse hybrids.
- Utilizing congenic mouse strains (B6.mtspr) to differentiate between nuclear and mitochondrial genetic contributions.
Main Results:
- Paternal mtDNA was transiently detected in early embryos of intraspecific crosses, coinciding with mitochondrial membrane potential loss.
- Interspecific crosses showed sustained paternal mtDNA detection from the pronucleus stage to neonates.
- Oocytes eliminated sperm mitochondria from congenic strains carrying foreign mtDNA, indicating a nuclear-encoded recognition mechanism.
Conclusions:
- Mammalian mtDNA is uniparentally transmitted in intraspecific crosses, similar to Chlamydomonas.
- Oocyte cytoplasm possesses a species-specific mechanism to recognize and eliminate sperm mitochondria and mtDNA.
- The elimination mechanism targets nuclear-encoded proteins in sperm midpiece, not mtDNA itself.
- Paternal mtDNA leakage is primarily observed in rare interspecific crosses, not natural intraspecific reproduction.