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Biparental Inheritance Through Uniparental Transmission: The Doubly Uniparental Inheritance (DUI) of Mitochondrial DNA

Abstract

Many bivalvian mollusks have a sperm-transmitted mitochondrial genome (M), along with the standard egg-transmitted one (F). The phenomenon, known as doubly uniparental inheritance (DUI) of mtDNA, is the only known case in which biparental inheritance of a cytoplasmic genome is the rule rather than the exception. In the mussel Mytilus sperm mitochondria disperse randomly among blastomeres in female embryos, but form an aggregate and stay in the same blastomere in male embryos. In adults, somatic tissues of both sexes are dominated by the F genome. Sperm contains only the M genome and eggs the F (and perhaps traces of M). A female produces mostly daughters, mostly sons, or both sexes in about equal numbers, irrespective of its mate. Thus maleness and M mtDNA fate are tightly linked and under maternal control. Hybridization and triploidization affect the former but not the latter, which suggests that the two are not causally linked. Gene content and arrangement are the same in conspecific F and M genomes, but primary sequence has diverged from 20 % to 40 %, depending on species. The two genomes differ at the control region (CR). Synonymous substitutions accumulate faster in the M than the F genome and non-synonymous even faster. Expression studies indicate that the M genome is active only at spermatogenesis. These observations suggest that the M genome is under a more relaxed selective constraint than the F. Some mytilid species carry, in low frequencies, sperm-transmitted mtDNAs whose primary sequence is of the F type and the CR is an F/M mosaic (“masculinized” genomes). In venerids sperm mitochondria behavior, M genome fate and sex determination are as in mytilids. In unionids the M genome also evolves faster than the F and F/M sequence divergence reaches 50 %. The identification of F-specific and M-specific open reading frames in non-coding regions of unionids and mytilids, in conjunction with the CR’s mosaic structure of masculinized genomes, suggest that the mitochondrial genomes of species with DUI carry sequences that affect their transmission route. A model that incorporates these findings is presented in this review.

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Acknowledgments

Practically everybody who has worked on the topic of this review was asked if he or she wanted to see an early version of it. Most responded positively and offered valuable comments and encouragement. The list includes F. Batista, A. Beaumont, S. Breton, A. Burzynski, L. Cao, A. Diz, H. Doucet-Beaupré, F. Ghiselli, J. Hilbish, E. Kenchington, A. Kousathanas, E. Ladoukakis, B. Ort, M. Passamonti, G. Pogson, H. Quesada, P. Rawson, C. Riginos, G. Rodakis, C. Saavedra, D. Skibinski, J. Theologidis and Y. Yusa. I thank all of them warmly and assume the responsibility if the final version does not completely address their comments. I also thank the anonymous reviewers for valuable comments. My special thanks go to E. Kyriakou who patiently compiled all references she could find about DUI and to G. Rodakis who drew the figures. But my deepest debt goes to D. Skibinski. He identified a serious mistake in a previous version of the DUI model, a drastic revision of which is presented here, and read the entire first and second versions of the review. This review owes much of what is worth to his deep insight of the phenomenon of DUI and his unselfishness to share it with others. In a way, he is a co-author of it.

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Zouros, E. Biparental Inheritance Through Uniparental Transmission: The Doubly Uniparental Inheritance (DUI) of Mitochondrial DNA. Evol Biol 40, 1–31 (2013). https://doi.org/10.1007/s11692-012-9195-2

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Keywords

  • Mitochondrial DNA
  • Doubly uniparental inheritance (DUI)
  • MtDNA recombination
  • Bivalvian mollusks