The extremely divergent maternally- and paternally-transmitted mitochondrial genomes are co-expressed in somatic tissues of two freshwater mussel species with doubly uniparental inheritance of mtDNA

Abstract

Freshwater mussel species with doubly uniparental inheritance (DUI) of mtDNA are unique because they are naturally heteroplasmic for two extremely divergent mtDNAs with ~50% amino acid differences for protein-coding genes. The paternally-transmitted mtDNA (or M mtDNA) clearly functions in sperm in these species, but it is still unknown whether it is transcribed when present in male or female soma. In the present study, we used PCR and RT-PCR to detect the presence and expression of the M mtDNA in male and female somatic and gonadal tissues of the freshwater mussel species Venustaconcha ellipsiformis and Utterbackia peninsularis (Unionidae). This is the first study demonstrating that the M mtDNA is transcribed not only in male gonads, but also in male and female soma in freshwater mussels with DUI. Because of the potentially deleterious nature of heteroplasmy, we suggest the existence of different mechanisms in DUI species to deal with this possibly harmful situation, such as silencing mechanisms for the M mtDNA at the transcriptional, post-transcriptional and/or post-translational levels. These hypotheses will necessitate additional studies in distantly-related DUI species that could possess different mechanisms of action to deal with heteroplasmy.

Metabolic remodelling associated with mtDNA: insights into the adaptive value of doubly uniparental inheritance of mitochondria

“…In recent years, the vision of selective neutrality of mtDNA has been challenged, and our results add to the growing body of evidence showing that cytoplasmic genetic variation can influence fitness [2,6,7,12,14]. They are also in line with the Father's curse hypothesis [30], as DUI allows selection to act directly on the M-mtDNA, which can accumulate mutations that are beneficial or neutral in sperm, but potentially harmful when present and expressed in somatic tissues or in eggs. Since the OXPHOS capacity in heteroplasmic Mytilus male gills does not digress much from homoplasmic female gills, it is plausible that the amount of M-mtDNA does not reach the threshold required to produce a strong effect in male soma [39].…”

“…As mentioned above, in these species, females are usually homoplasmic, whereas males possess sperm with paternal mitochondria and soma with maternal mitochondria [27]. That said, some studies have also shown that both parental haplotypes can coexist and be expressed in somatic tissues, mostly in male individuals [30]. In M. edulis, the genetic divergence between the two parental haplotypes reaches 10 -22% [27 -29], whereas it reaches 8% in A. islandica [38].…”

“…Eggs transmit their mitochondria to daughters and sons, and sperm only to sons, and females are usually homoplasmic for the F-type mtDNA whereas males possess the F-type mtDNA in their somatic tissues and the M-type mtDNA in their sperm [27 -29]. Some cases where both haplotypes have been detected in male and sometimes in female somatic tissues have, however, been reported [30]. The naturally heteroplasmic DUI system represents a unique model to assess the adaptive value of mtDNA variations, and their potential evolutionary implications.…”

Unorthodox features in two venerid bivalves with doubly uniparental inheritance of mitochondria

“…An even more extreme departure from the norm in bivalve mitochondrial genomes is their mode of doubly uniparental inheritance (DUI) -both egg and sperm mitochondria are transmitted from generation to generation in several bivalve species, but only male offspring retain paternally-transmitted mitochondria (with male or M mtDNA) in their gametes [10][11][12] . Adult females of DUI-exhibiting species usually possess only the female-transmitted mtDNA (F mtDNA) in their soma and gametes whereas males possess F mtDNA in their soma and M mtDNA in their gametes [10][11][12][13] . The DNA divergence between F and M mtDNAs usually vary from about 8% to 40% depending on the species 12,14 .…”

“…One factor explaining this observation may be that the M genome is subject to weaker selective pressures than the F genome due to an unequal "division of labor" in the DUI system 16 . Typical animal mtDNA functions in gonads and somatic tissues of both sexes whereas under DUI, F mtDNA functions in female gonads and the soma of both sexes, while M mtDNAs functions primarily in spermatozoa of male gonads and only partially in the male soma 13,16,18 . As opposed to SMI that promotes homoplasmy, a state in which all mtDNA copies are typically genetically identical in each cell, thus preventing potentially harmful genomic conflicts, DUI is a naturally heteroplasmic system in which two highly divergent mitochondrial lineages coexist in the same nuclear background, enabling the analysis of the consequences of tissue heteroplamy 13 .…”