Different transcriptional ratios of male and female transmitted mitochondrial DNA and tissue-specific expression patterns in the blue mussel, Mytilus galloprovincialis

Abstract

In some bivalve species, paternal mitochondrial DNA (mtDNA) from sperm is transmitted to the offspring. This is called ''doubly uniparental inheritance'' (DUI). Under DUI, male offspring receive both paternal (M type) and maternal (F type) mtDNA. Females predominantly receive F type. Expression levels of M and F type mtDNA and mitochondrial RNA localization have not been studied extensively. In this study, we quantified M and F type mtDNA and their expression levels in male and female somatic tissues and gonads with real-time polymerase chain reaction (PCR) in the blue mussel, Mytilus galloprovincialis. M and F type expression patterns were studied with in situ hybridization, using probes specific to M and F type mtDNA in the cytochrome b region. We found that (i) F type mtDNA was expressed in somatic tissues and female gonads, while M type was not expressed in these tissues; (ii) M type expression in male gonads was limited, but strong expression was observed during early spermatogenesis; and (iii) F type expression ratios were significantly lower in female gonads than in somatic tissues and lower than both M and F type expression ratios in male gonads. We propose (i) different systems for M and F type tissue-specific transcriptional regulation; and (ii) different functions for F and M type mtDNA, with F type being functional in somatic tissues and female gonads and M type functioning only in spermatogenetic cells.

Co-expressed mitochondrial genomes: recently masculinized, recombinant mitochondrial genome is co-expressed with the female – transmitted mtDNA genome in a male Mytilus trossulus mussel from the Baltic Sea

“…Since the mantle consists of both generative and somatic tissues we expect one of the genomes to be the typical F genome, in line with the observed tissue-specific patterns of expression reported recently for the congeneric M. galloprovincialis [16]. Based on the comparative analysis we can conclude that the genome expressing the E S set of transcripts must be the typical F genome of this individual.…”

“…Further arguments supporting the masculinized status of the E L genome include its very expression in male generative tissues. All experimental and model approaches to DUI agree that the paternally transmitted genome should be present and expressed there [3,4,13,16,22]. The second argument is associated with the observed pattern of substitutions: the E L genome accumulated more non-synonymous substitutions than expected in the phylogenetic context.…”

“…Consequently, both genomes are present and expressed in the male germ line and only the paternal genome is present in sperm. Both genomes may also be present in the male somatic tissues, but primarily the F genome is expressed there [15,16]. The M genome evolves faster than the F genome and accumulates more non-synonymous substitutions.…”

Mitonuclear interactions: evolutionary consequences over multiple biological scales

“…In this system, heteroplasmy is the norm: a maternal haplotype is transmitted to all offspring, and a paternal haplotype is exclusively transmitted to male offspring. In males, the maternal haplotype is predominant in all somatic tissues, but is outweighed by the paternal haplotype in the gonads, a system that may have evolved in response to asymmetries in functional requirements of reproductive tissues [101,102]. Interestingly, sequence divergence between the two haplotypes can exceed 40%, yet mitochondrial function is maintained, suggesting that mtDNA-encoded components may be matched alongside sex-specific isoforms or duplicates of nuclear-encoded mitochondrial components [101,102].…”

Proteomic Analysis of Eggs from Mytilus edulis Females Differing in Mitochondrial DNA Transmission Mode

“…[22][23][24][25], a second copy of the cytochrome oxidase II (CoII gene) in the M genome of the mytilid Musculista senhousia (25), F and M specific open reading frames (26), and an M genome insertion extending the COII gene in unionid bivalves (27,28). In M. galloprovincialis, the M genome is transcribed in spermatogonia and spermatocytes, though not in somatic tissue (29). In unionids, the M genome COII protein is expressed on the outer sperm mitochondrial membrane (30).…”