In species with doubly uniparental inheritance (DUI), males are heteroplasmic for two sex-linked mitochondrial genomes (M- and F-mtDNA). While a role of M-mtDNA in male gametogenesis and sperm function is evident, there is an ongoing debate on whether it is transcribed or not in male soma. In this work we report a qPCR analysis in the DUI species Ruditapes philippinarum, showing that M-mtDNA is transcribed in somatic tissues. We observed a correlation between DNA copy numbers of the two analyzed genes, cytochrome b and a novel male-specific mitochondrial gene thought to be involved in DUI (orf21), and between their transcription levels. No correlation between a transcript and its DNA copy number was found, supporting the existence of complex regulatory mechanisms of mitochondrial transcription. We found the highest amount of mtDNA and mtRNA in gonads, likely due to the intense cell proliferation and high energy request for gametogenesis, while the observed variation among specimens is probably related to their different stages of gonad development. Finally, orf21 showed a highly variable transcription in advanced stages of gametogenesis. We hypothesize a differential storage of orf21 transcripts in spermatozoa, representing different paternal contributions to progeny, possibly leading to different developmental outcomes. A transcriptional activity does not necessarily imply the translation of M-mtDNA genes, and studies on mitochondrial proteins and their localization are needed to definitively assess the functioning of male-transmitted mitochondria in male soma. All that considered, the male soma of DUI species may represent an intriguing experimental model to study cytoplasmic genetic conflicts.
Comparative genomics has become a central tool for evolutionary biology, and a better knowledge of understudied taxa represents the foundation for future work. In this study, we characterized the transcriptome of male and female mature gonads in the European clam Ruditapes decussatus, compared with that in the Manila clam Ruditapes philippinarum providing, for the first time in bivalves, information about transcription dynamics and sequence evolution of sex-biased genes. In both the species, we found a relatively low number of sex-biased genes (1,284, corresponding to 41.3% of the orthologous genes between the two species), probably due to the absence of sexual dimorphism, and the transcriptional bias is maintained in only 33% of the orthologs. The dN/dS is generally low, indicating purifying selection, with genes where the female-biased transcription is maintained between the two species showing a significantly higher dN/dS. Genes involved in embryo development, cell proliferation, and maintenance of genome stability show a faster sequence evolution. Finally, we report a lack of clear correlation between transcription level and evolutionary rate in these species, in contrast with studies that reported a negative correlation. We discuss such discrepancy and call into question some methodological approaches and rationales generally used in this type of comparative studies.
In Metazoa, 4 out of 5 complexes involved in oxidative phosphorylation (OXPHOS) are formed by subunits encoded by both the mitochondrial (mtDNA) and nuclear (nuDNA) genomes, leading to the expectation of mito-nuclear coevolution. Previous studies have supported co-adaptation of mitochondria-encoded (mtOXPHOS) and nuclear-encoded OXPHOS (nuOXPHOS) subunits, often specifically interpreted with regard to the “nuclear compensation hypothesis”, a specific form of mitonuclear coevolution where nuclear genes compensate for deleterious mitochondrial mutations owing to less efficient mitochondrial selection. In this study we analysed patterns of sequence evolution of 79 OXPHOS subunits in 31 bivalve species, a taxon showing extraordinary mtDNA variability and including species with “doubly uniparental” mtDNA inheritance. Our data showed strong and clear signals of mitonuclear coevolution. NuOXPHOS subunits had concordant topologies with mtOXPHOS subunits, contrary to previous phylogenies based on nuclear genes lacking mt interactions. Evolutionary rates between mt and nuOXPHOS subunits were also highly correlated compared to non-OXPHOS-interacting nuclear genes. Nuclear subunits of chimeric OXPHOS complexes (I, III, IV, and V) also had higher dN/dS ratios than Complex II, which is formed exclusively by nuDNA-encoded subunits. However, we did not find evidence of nuclear compensation: mitochondria-encoded subunits showed similar dN/dS ratios compared to nuclear-encoded subunits, contrary to most previously studied bilaterian animals. Moreover, no site-specific signals of compensatory positive selection were detected in nuOXPHOS genes. Our analyses extend the evidence for mitonuclear coevolution to a new taxonomic group, but we propose a reconsideration of the nuclear compensation hypothesis.
Almost all eukaryotes rely on mitochondria and mitochondrial (mt)-encoded genes to generate cellular energy via oxidative phosphorylation (OXPHOS) (Karnkowska et al., 2016;Roger et al., 2017). Mt-encoded genes must coordinate with nuclear-encoded mt genes (i.e. N-mt genes) for OXPHOS. Coevolution and coadaptation between mt and N-mt genes are therefore essential and likely a ubiquitous feature of eukaryotes (Havird et al., 2019b;
Despite the large number of animal complete mitochondrial genomes currently available in public databases, knowledge about mitochondrial genomics in invertebrates is uneven. This paper reports, for the first time, the complete mitochondrial genome of the grooved carpet shell, Ruditapes decussatus, also known as the European clam. Ruditapes decussatus is morphologically and ecologically similar to the Manila clam Ruditapes philippinarum, which has been recently introduced for aquaculture in the very same habitats of Ruditapes decussatus, and that is replacing the native species. Currently the production of the European clam is almost insignificant, nonetheless it is considered a high value product, and therefore it is an economically important species, especially in Portugal, Spain and Italy. In this work we: (i) assembled Ruditapes decussatus mitochondrial genome from RNA-Seq data, and validated it by Sanger sequencing; (ii) analyzed and characterized the Ruditapes decussatus mitochondrial genome, comparing its features with those of other venerid bivalves; (iii) assessed mitochondrial sequence polymorphism (SP) and copy number variation (CNV) of tandem repeats across 26 samples. Despite using high-throughput approaches we did not find evidence for the presence of two sex-linked mitochondrial genomes, typical of the doubly uniparental inheritance of mitochondria, a phenomenon known in ∼100 bivalve species. According to our analyses, Ruditapes decussatus is more genetically similar to species of the Genus Paphia than to the congeneric Ruditapes philippinarum, a finding that bolsters the already-proposed need of a taxonomic revision. We also found a quite low genetic variability across the examined samples, with few SPs and little variability of the sequences flanking the control region (Largest Unassigned Regions (LURs). Strikingly, although we found low nucleotide variability along the entire mitochondrial genome, we observed high levels of length polymorphism in the LUR due to CNV of tandem repeats, and even a LUR length heteroplasmy in two samples. It is not clear if the lack of genetic variability in the mitochondrial genome of Ruditapes decussatus is a cause or an effect of the ongoing replacement of Ruditapes decussatus with the invasive Ruditapes philippinarum, and more analyses, especially on nuclear sequences, are required to assess this point.
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