Early replication dynamics of sex-linked mitochondrial DNAs in the doubly uniparental inheritance species Ruditapes philippinarum (Bivalvia Veneridae)

Abstract

Mitochondrial homoplasmy, which is maintained by strictly maternal inheritance and a series of bottlenecks, is thought to be an adaptive condition for metazoans. Doubly uniparental inheritance (DUI) is a unique mode of mitochondrial transmission found in bivalve species, in which two distinct mitochondrial genome (mtDNA) lines are present, one inherited through eggs (F) and one through sperm (M). During development, the two lines segregate in a sex-and tissue-specific manner: females lose M during embryogenesis, whereas males actively segregate it in the germ line. These two pivotal events are still poorly characterized. Here we investigated mtDNA replication dynamics during embryogenesis and pre-adulthood of the venerid Ruditapes philippinarum using real-time quantitative PCR. We found that both mtDNAs do not detectably replicate during early embryogenesis, and that the M line might be lost from females around 24 h of age. A rise in mtDNA copy number was observed before the first reproductive season in both sexes, with the M mitochondrial genome replicating more than the F in males, and we associate these boosts to the early phase of gonad production. As evidence indicates that DUI relies on the same molecular machine of mitochondrial maternal inheritance that is common in most animals, our data are relevant not only to DUI but also to shed light on how differential segregations of mtDNA variants, in the same nuclear background, may be controlled during development.

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

“…Three consecutive “checkpoints” have been proposed as the main steps of the DUI mechanism [ 14 , 32 ]: checkpoint #1 takes place shortly after fertilization when sperm mitochondria enter the egg and are maintained as an aggregate in male embryos, whereas they disperse in females (this phenomenon has been studied in Mytilus and Ruditapes but not in unionids yet); checkpoint #2 concerns the disappearance of the M mtDNA only from females, following the dilution and/or degradation of sperm mitochondria; and checkpoint #3 implies the segregation of M mtDNA in the male germ line and the F mtDNA in the female one, becoming the dominant mtDNA in the gonad and the only mitochondrial line transmitted by sperms and eggs, respectively. From the above data, it appears that checkpoints #2 and #3 can sometimes fail in species with DUI, leading to intra-tissular heteroplasmy in both male and female individuals.…”

Gender-Associated Mitochondrial DNA Heteroplasmy in Somatic Tissues of the Endangered Freshwater MusselUnio crassus(Bivalvia: Unionidae): Implications for Sex Identification and Phylogeographical Studies

“…In addition, usefulness of microscopic examination of gonads is also limited, namely in the case of archival materials (e.g., specimens preserved in museum collections or dried tissue samples). Sex identification of individuals that are immature or infertile or castrated by trematodes is also problematic (Guerra et al., ). Moreover, it is relatively straightforward to identify adult females by analyzing their oocytes, in contrast to the more difficult identification of adult males, due to the small size of spermatocytes.…”

“…in which M‐type mtDNA was detected not only in somatic tissues of males but also in female nongonadal tissues (Garrido‐Ramos et al., ; Dalziel and Stewart, ; Venetis et al., ; Obata et al., ; Kyriakou et al., ). The presence of M‐type mtDNA in somatic tissues has also been investigated in marine clam Ruditapes philippinarum (Ghiselli et al., ; Milani et al., ; Guerra et al., ). The distribution of M‐type mtDNA in tissues of DUI freshwater mussels, including the most specious family the Unionidae, has not been widely studied as in Mytilus and R. philippinarum .…”

The dynamics of mito-nuclear coevolution: A perspective from bivalve species with two different mechanisms of mitochondrial inheritance

“…In DUI species, two mitochondrial lineages are present: the F-type, inherited through eggs, and the M-type, inherited through sperm; as a result, female somatic tissues are generally homoplasmic for the F-type, male somatic tissues are heteroplasmic, and gametes carry only the sex-specific mitochondrial lineage. Therefore, in contrast to all other Metazoa, in DUI bivalves, the same nuclear background has to coevolve with two distinct mtDNA lineages which present a high nucleotide divergence (up to 40%; Zouros, 2013) and different replication and transcription dynamics (Ghiselli, Milani, & Passamonti, 2011;Obata, Sano, & Komaru, 2011;Milani & Ghiselli, 2015;Ghiselli et al, 2013;Milani, Ghiselli, Iannello, & Passamonti, 2014;Milani & Ghiselli, 2015;Guerra, Ghiselli, Milani, Breton, & Passamonti, 2016). Therefore, DUI species offer a unique opportunity to investigate the coevolution between nuclear and mitochondrial genomes and the effects of heteroplasmy.…”