Incompatibility between Nuclear and Mitochondrial Genomes Contributes to an Interspecies Reproductive Barrier

Hong Ma, Nuria Marti Gutierrez, Robert Morey, Crystal Van Dyken, Eunju Kang, Tomonari Hayama, Yeonmi Lee, Ying Li, Rebecca Tippner-Hedges, Don P. Wolf, Louise C. Laurent, Shoukhrat Mitalipov

Research output: Contribution to journalArticle

32 Citations (Scopus)

Abstract

Vertebrate cells carry two different genomes, nuclear (nDNA) and mitochondrial (mtDNA), both encoding proteins involved in oxidative phosphorylation. Because of the extensive interactions, adaptive coevolution of the two genomes must occur to ensure normal mitochondrial function. To investigate whether incompatibilities between these two genomes could contribute to interspecies reproductive barriers, we performed reciprocal mtDNA replacement (MR) in zygotes between widely divergent . Mus m. domesticus (B6) and conplastic . Mus m. musculus (PWD) mice. Transfer of MR1 cybrid embryos (B6nDNA-PWDmtDNA) supported normal development of F1 offspring with reduced male fertility but unaffected reproductive fitness in females. Furthermore, donor PWD mtDNA was faithfully transmitted through the germline into F2 and F3 generations. In contrast, reciprocal MR2 (PWDnDNA-B6mtDNA) produced high embryonic loss and stillborn rates, suggesting an association between mitochondrial function and infertility. These results strongly suggest that functional incompatibility between nuclear and mitochondrial genomes contributes to interspecies reproductive isolation in mammals. Compatibility between nuclear and mitochondrial genomes is important for normal reproductive fitness. Mitalipov and colleagues show that reciprocal mtDNA replacement in zygotes between two mouse strains (B6 and PWD) results in post-implantation embryonic lethality, suggesting that mtDNA sequence divergence between mammalian species contributes to a reproductive barrier.

Original languageEnglish (US)
JournalCell Metabolism
DOIs
StateAccepted/In press - Nov 12 2015

Fingerprint

Mitochondrial Genome
Mitochondrial DNA
Genetic Fitness
Zygote
Genome
Reproductive Isolation
Oxidative Phosphorylation
Infertility
Fertility
Vertebrates
Mammals
Embryonic Structures
Proteins

ASJC Scopus subject areas

  • Cell Biology
  • Molecular Biology
  • Physiology

Cite this

Incompatibility between Nuclear and Mitochondrial Genomes Contributes to an Interspecies Reproductive Barrier. / Ma, Hong; Marti Gutierrez, Nuria; Morey, Robert; Van Dyken, Crystal; Kang, Eunju; Hayama, Tomonari; Lee, Yeonmi; Li, Ying; Tippner-Hedges, Rebecca; Wolf, Don P.; Laurent, Louise C.; Mitalipov, Shoukhrat.

In: Cell Metabolism, 12.11.2015.

Research output: Contribution to journalArticle

Ma, H, Marti Gutierrez, N, Morey, R, Van Dyken, C, Kang, E, Hayama, T, Lee, Y, Li, Y, Tippner-Hedges, R, Wolf, DP, Laurent, LC & Mitalipov, S 2015, 'Incompatibility between Nuclear and Mitochondrial Genomes Contributes to an Interspecies Reproductive Barrier', Cell Metabolism. https://doi.org/10.1016/j.cmet.2016.06.012
Ma, Hong ; Marti Gutierrez, Nuria ; Morey, Robert ; Van Dyken, Crystal ; Kang, Eunju ; Hayama, Tomonari ; Lee, Yeonmi ; Li, Ying ; Tippner-Hedges, Rebecca ; Wolf, Don P. ; Laurent, Louise C. ; Mitalipov, Shoukhrat. / Incompatibility between Nuclear and Mitochondrial Genomes Contributes to an Interspecies Reproductive Barrier. In: Cell Metabolism. 2015.
@article{117e4d424fc142cb934ba3bbcd860830,
title = "Incompatibility between Nuclear and Mitochondrial Genomes Contributes to an Interspecies Reproductive Barrier",
abstract = "Vertebrate cells carry two different genomes, nuclear (nDNA) and mitochondrial (mtDNA), both encoding proteins involved in oxidative phosphorylation. Because of the extensive interactions, adaptive coevolution of the two genomes must occur to ensure normal mitochondrial function. To investigate whether incompatibilities between these two genomes could contribute to interspecies reproductive barriers, we performed reciprocal mtDNA replacement (MR) in zygotes between widely divergent . Mus m. domesticus (B6) and conplastic . Mus m. musculus (PWD) mice. Transfer of MR1 cybrid embryos (B6nDNA-PWDmtDNA) supported normal development of F1 offspring with reduced male fertility but unaffected reproductive fitness in females. Furthermore, donor PWD mtDNA was faithfully transmitted through the germline into F2 and F3 generations. In contrast, reciprocal MR2 (PWDnDNA-B6mtDNA) produced high embryonic loss and stillborn rates, suggesting an association between mitochondrial function and infertility. These results strongly suggest that functional incompatibility between nuclear and mitochondrial genomes contributes to interspecies reproductive isolation in mammals. Compatibility between nuclear and mitochondrial genomes is important for normal reproductive fitness. Mitalipov and colleagues show that reciprocal mtDNA replacement in zygotes between two mouse strains (B6 and PWD) results in post-implantation embryonic lethality, suggesting that mtDNA sequence divergence between mammalian species contributes to a reproductive barrier.",
author = "Hong Ma and {Marti Gutierrez}, Nuria and Robert Morey and {Van Dyken}, Crystal and Eunju Kang and Tomonari Hayama and Yeonmi Lee and Ying Li and Rebecca Tippner-Hedges and Wolf, {Don P.} and Laurent, {Louise C.} and Shoukhrat Mitalipov",
year = "2015",
month = "11",
day = "12",
doi = "10.1016/j.cmet.2016.06.012",
language = "English (US)",
journal = "Cell Metabolism",
issn = "1550-4131",
publisher = "Cell Press",

}

TY - JOUR

T1 - Incompatibility between Nuclear and Mitochondrial Genomes Contributes to an Interspecies Reproductive Barrier

AU - Ma, Hong

AU - Marti Gutierrez, Nuria

AU - Morey, Robert

AU - Van Dyken, Crystal

AU - Kang, Eunju

AU - Hayama, Tomonari

AU - Lee, Yeonmi

AU - Li, Ying

AU - Tippner-Hedges, Rebecca

AU - Wolf, Don P.

AU - Laurent, Louise C.

AU - Mitalipov, Shoukhrat

PY - 2015/11/12

Y1 - 2015/11/12

N2 - Vertebrate cells carry two different genomes, nuclear (nDNA) and mitochondrial (mtDNA), both encoding proteins involved in oxidative phosphorylation. Because of the extensive interactions, adaptive coevolution of the two genomes must occur to ensure normal mitochondrial function. To investigate whether incompatibilities between these two genomes could contribute to interspecies reproductive barriers, we performed reciprocal mtDNA replacement (MR) in zygotes between widely divergent . Mus m. domesticus (B6) and conplastic . Mus m. musculus (PWD) mice. Transfer of MR1 cybrid embryos (B6nDNA-PWDmtDNA) supported normal development of F1 offspring with reduced male fertility but unaffected reproductive fitness in females. Furthermore, donor PWD mtDNA was faithfully transmitted through the germline into F2 and F3 generations. In contrast, reciprocal MR2 (PWDnDNA-B6mtDNA) produced high embryonic loss and stillborn rates, suggesting an association between mitochondrial function and infertility. These results strongly suggest that functional incompatibility between nuclear and mitochondrial genomes contributes to interspecies reproductive isolation in mammals. Compatibility between nuclear and mitochondrial genomes is important for normal reproductive fitness. Mitalipov and colleagues show that reciprocal mtDNA replacement in zygotes between two mouse strains (B6 and PWD) results in post-implantation embryonic lethality, suggesting that mtDNA sequence divergence between mammalian species contributes to a reproductive barrier.

AB - Vertebrate cells carry two different genomes, nuclear (nDNA) and mitochondrial (mtDNA), both encoding proteins involved in oxidative phosphorylation. Because of the extensive interactions, adaptive coevolution of the two genomes must occur to ensure normal mitochondrial function. To investigate whether incompatibilities between these two genomes could contribute to interspecies reproductive barriers, we performed reciprocal mtDNA replacement (MR) in zygotes between widely divergent . Mus m. domesticus (B6) and conplastic . Mus m. musculus (PWD) mice. Transfer of MR1 cybrid embryos (B6nDNA-PWDmtDNA) supported normal development of F1 offspring with reduced male fertility but unaffected reproductive fitness in females. Furthermore, donor PWD mtDNA was faithfully transmitted through the germline into F2 and F3 generations. In contrast, reciprocal MR2 (PWDnDNA-B6mtDNA) produced high embryonic loss and stillborn rates, suggesting an association between mitochondrial function and infertility. These results strongly suggest that functional incompatibility between nuclear and mitochondrial genomes contributes to interspecies reproductive isolation in mammals. Compatibility between nuclear and mitochondrial genomes is important for normal reproductive fitness. Mitalipov and colleagues show that reciprocal mtDNA replacement in zygotes between two mouse strains (B6 and PWD) results in post-implantation embryonic lethality, suggesting that mtDNA sequence divergence between mammalian species contributes to a reproductive barrier.

UR - http://www.scopus.com/inward/record.url?scp=84978863319&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84978863319&partnerID=8YFLogxK

U2 - 10.1016/j.cmet.2016.06.012

DO - 10.1016/j.cmet.2016.06.012

M3 - Article

JO - Cell Metabolism

JF - Cell Metabolism

SN - 1550-4131

ER -