The unusual system of doubly uniparental inheritance of mtDNA: isn’t one enough?

doi:10.1016/j.tig.2007.05.011

Trends in Genetics

Volume 23, Issue 9, September 2007, Pages 465-474

https://doi.org/10.1016/j.tig.2007.05.011 Get rights and content

Mitochondria possess their own genetic material (mitochondrial DNA or mtDNA), whose gene products are involved in mitochondrial respiration and oxidative phosphorylation, transcription, and translation. In animals, mitochondrial DNA is typically transmitted to offspring by the mother alone. The discovery of ‘doubly uniparental inheritance’ (DUI) of mtDNA in some bivalves has challenged the paradigm of strict maternal inheritance (SMI). In this review, we survey recent advances in our understanding of DUI, which is a peculiar system of cytoplasmic DNA inheritance that involves distinct maternal and paternal routes of mtDNA transmission, a novel extension of a mitochondrial gene (cox2), recombination, and periodic ‘role-reversals’ of the normally male and female-transmitted mitochondrial genomes. DUI provides a unique opportunity for studying nuclear-cytoplasmic genome interactions and the evolutionary significance of different modes of mitochondrial inheritance.

Section snippets

Mitochondrial inheritance: rules for mussels

Mitochondria are multifunctional, DNA-bearing organelles found in eukaryotic cells. Animal mitochondrial DNA (mtDNA) is typically a circular molecule ∼16.5-kilobase long (but linear and longer mtDNAs exist across eukaryotes, see Ref. [1]) that normally encodes ∼37 genes [2]. Among them, 24 mitochondrial genes encode components involved in the mitochondrial translational machinery (22 tRNAs and two rRNAs). The remaining 13 genes encode protein subunits of the respiratory chain complexes and ATP

The DUI system unveiled

DUI was discovered in 1990 when a high frequency of heteroplasmic individuals was detected in a study of mtDNA variation in a hybrid zone between Mytilus edulis and M. galloprovincialis mussels in southwest England [26]. The occurrence of two divergent mtDNAs in the same individuals was subsequently confirmed in other mytilid populations 27, 28. These findings, combined with previous cytological studies showing retention of paternal mitochondria in early embryos [29], led the authors to suggest

Molecular evolution of M and F mitochondrial genomes

Genetic analyses using partial mtDNA sequences of M and F mitotypes in species with DUI 14, 15, 16, 17, 18, 20, 30, 31 indicated that (i) DUI appeared 200 million years ago, if not before; (ii) mussel mtDNA (both M and F lineages) has experienced an accelerated rate of mtDNA sequence divergence compared with that of other animal taxa; and (iii) the M genome evolves more quickly than the F genome. A leading interpretation explaining why M evolves faster than F, and why both of them evolve faster

When DUI breaks down: masculinization of F mtDNA

Phylogenetic analyses of cytochrome c oxidase subunit I (cox1) sequences have demonstrated that in marine (but not freshwater) mussels, the fidelity of DUI is sometimes compromised. Some males seem to lack a typical M genome 33, 49, 50, 51, and F genomes seem to occasionally invade the male route of inheritance such that they become transmitted from generation to generation only through sperm 33, 34, 38, 49. However, the reverse (i.e. an M genome invading the F genome route of transmission) has

Origin and evolution of DUI

Even if the occurrence of DUI in other taxa remains to be explored, the question persists why DUI evolved in bivalve mollusks 7, 61. Can the considerable variation of bivalve reproductive strategies provide a clue [62]? Although individuals of many bivalve species demonstrate stable gonochoric sexuality (i.e. once they become male or female, they remain that sex throughout their life), several species have simultaneous hermaphrodites that produce both male and female gametes in the ovotestis or

Potential adaptive evolution of M mtDNA

Currently, it is unclear whether a selective advantage favoured the retention of DUI in bivalves, but one possible mechanism could be related to the sex-antagonistic effects of mtDNA resulting from maternal inheritance 7, 8, 9. In SMI, natural selection on mtDNA operates only in females because males do not transmit their cytoplasmic genes 24, 25. Consequently, mtDNA genotypes that have positive (or neutral, or even slightly deleterious) fitness effects in females but potentially deleterious

Concluding remarks

Since its discovery in the early 1990s, much progress has been made in understanding the DUI system in bivalve species, in particular with regard to the mechanisms underlying the sex-specific behaviour of sperm mitochondria and the molecular evolution of M and F mitochondrial genomes. Future work will focus on unique features of the DUI system such as the potential adaptive evolution of the M genome on sperm motility, the role of recombination in masculinization events (and specifically the

Acknowledgements

We thank Gertraud Burger and the anonymous reviewers for suggestions that improved this article. This work was supported by research grants from the National Sciences and Engineering Research Council (NSERC) to P.U. Blier and D.T. Stewart, and from the National Science Foundation (NSF) to W.R. Hoeh. S. Breton and H. Doucet Beaupré were financially supported by the Fonds Québécois de la Recherche sur la Nature et les Technologies (FQRNT) and NSERC scholarships.

Glossary

Gonochoric: describes a sexually reproducing species in which there are two (at least) distinct sexes.
Heteroplasmy: the existence of two (or more) plastid variants (mitochondrial or chloroplast DNA) within an organelle, cell, tissue or individual.
Homoplasmy: the condition in which all plastid genomes (i.e. usually referring to genetic identity of mitochondria or chloroplasts) in an organelle, cell, tissue or individual are identical.
Hybrid zone: an area where two species come into contact and offspring

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The presence of doubly uniparental inheritance (DUI) in bivalves represents a unique mode of mitochondrial transmission, whereby paternal (male-transmitted M-type) and maternal (female-transmitted F-type) haplotypes are transmitted to offspring separately. Male embryos retain both haplotypes, but the M-type is selectively removed from females. Due to the presence of heteroplasmy in males, mtDNA can recombine resulting in a ‘masculinized’ haplotype referred to as M^f-type. While mtDNA recombination is usually rare, it has been recorded in multiple mussel species across the Northern Hemisphere. Given that mitochondria are the powerhouse of the cell, different mtDNA haplotypes may have different selective advantages under diverse environmental conditions. This may be particularly important for sperm fitness and fertilization success. In this study we aimed to i) determine the presence, prevalence of the M^f-type in Australian blue mussels (Mytilus sp.) and ii) investigate the effect of M^f-mtDNA on sperm performance (a fitness correlate). We found a high prevalence of recombined mtDNA (≈35 %) located within the control region of the mitochondrial genome, which occurred only in specimens that contained Southern Hemisphere mtDNA. The presence of two female mitotypes were identified in the studied mussels, one likely originating from the Northern Hemisphere, and the other either representing the endemic M. planulatus species or introduced genotypes from the Southern Hemisphere. Despite having recombination events present in a third of the studied population, analysis of sperm performance indicated no difference in fertilization success related to mitotype.
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^*: These authors contributed equally to this work.

View full text

Trends in Genetics

ReviewThe unusual system of doubly uniparental inheritance of mtDNA: isn’t one enough?

Section snippets

Mitochondrial inheritance: rules for mussels

The DUI system unveiled

Molecular evolution of M and F mitochondrial genomes

When DUI breaks down: masculinization of F mtDNA

Origin and evolution of DUI

Potential adaptive evolution of M mtDNA

Concluding remarks

Acknowledgements

Glossary

Trends Genet.

Trends Genet.

Trends Genet.

Trends Ecol. Evol.

FEBS Lett.

Mol. Cell. Endocrinol.

Trends Ecol. Evol.

Am. J. Hum. Genet.

Trends Ecol. Evol.

Trends Ecol. Evol.

Trends Genet.

Trends Ecol. Evol.

J. Biol. Chem.

J. Biol. Chem.

Animal mitochondrial genomes

Nucleic Acids Res.

The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models

Annu. Rev. Genet.

The inheritance of organelle genes and genomes: patterns and mechanisms

Genome

A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine

Annu. Rev. Genet.

Genes in Conflict

The units of selection on mitochondrial DNA

Annu. Rev. Ecol. Syst.

The incomplete natural history of mitochondria

Mol. Ecol.

Mitochondrial DNA inheritance

Nature

Mitochondrial-DNA inheritance

Nature

Sex-limited mitochondrial DNA transmission in the marine mussel Mytilus edulis

Genetics

An unusual type of mitochondrial-DNA inheritance in the blue mussel Mytilus

Proc. Natl. Acad. Sci. U. S. A.

Paternal mitochondrial DNA differentiation far exceeds maternal mitochondrial DNA and allozyme differentiation in the freshwater mussel, Anodonta grandis grandis

Evolution Int. J. Org. Evolution

Multiple origins of gender-associated mitochondrial DNA lineages in bivalves (Mollusca: Bivalvia)

Evolution Int. J. Org. Evolution

Gender-associated mitochondrial DNA heteroplasmy in the venerid clam Tapes philippinarum (Mollusca Bivalvia)

Curr. Genet.

Ancient sex-specific extension of the cytochrome c oxidase II gene in bivalves and the fidelity of doubly-uniparental inheritance

Mol. Biol. Evol.

Evolution of a unique mitotype-specific protein-coding extension of the cytochrome c oxidase II gene in freshwater mussels (Bivalvia: Unionoida)

J. Mol. Evol.

High fidelity of mitochondrial genome transmission under the doubly uniparental mode of inheritance in freshwater mussels (Bivalvia: Unionoidea)

Evolution Int. J. Org. Evolution

Molecular evolution and recombination in gender-associated mitochondrial DNAs of the manila clam Tapes philippinarum

Genetics

Taxonomic distribution and phylogenetic utility of gender-associated mitochondrial genomes in the Unionoida (Bivalvia)

Malacologia

Sperm mitochondrial DNA transmission to both male and female offspring in the blue mussel Mytilus galloprovincialis

Dev. Growth Differ.

Quantitation of the male and female types of mitochondrial DNA in a blue mussel, Mytilus galloprovincialis, using real-time polymerase chain reaction assay

Dev. Growth Differ.

Sexy sons: a dead end for cytoplasmic genes

Proc. R. Soc. Lond. B. Biol. Sci.

Sex-biased mitochondrial-DNA heteroplasmy in the marine mussel Mytilus

Proc. R. Soc. Lond. B. Biol. Sci.

Heteroplasmy suggests limited biparental inheritance of Mytilus mitochondrial-DNA

Science

Direct evidence for extensive paternal mitochondrial-DNA inheritance in the marine mussel Mytilus

Nature

Cytological aspects of fertilization in the lamellibranch, Mytilus edulis. II. Development of the male pronucleus and the association of the maternally and paternally derived chromosomes

J. Exp. Zool.

Evolutionary relationships among the male and female mitochondrial-DNA lineages in the Mytilus edulis species complex

Mol. Biol. Evol.

Male and female mitochondrial-DNA lineages in the blue mussel (Mytilus edulis) species group

Review
The unusual system of doubly uniparental inheritance of mtDNA: isn’t one enough?