A protein binding site in the M mitochondrial genome of Mytilus galloprovincialis may be responsible for its paternal transmission

• Mussels (Mytilus) have a maternally (F) and a paternally (M) transmitted mtDNA (DUI).
• We have identified a region of M that forms a complex with protein extracts from male gonads.
• The reaction is limited to perinuclear mitochondria.
• We suggest that in spermatocytes mitochondria are destroyed except those involved in this reaction.
• This explains why the sperm carries only the M mtDNA.

Sea mussels (genus Mytilus) have two mitochondrial genomes in obligatory co-existence, one that is transmitted through the egg and the other through the sperm. The phenomenon, known as Doubly Uniparental Inheritance (DUI) of mitochondrial DNA (mtDNA), is presently known to occur in more than 40 molluscan bivalve species. Females and the somatic tissues of males contain mainly the maternal (F) genome. In contrast, the sperm contains only the paternal (M) genome. Through electrophoretic mobility shift assay (EMSA) experiments we have identified a sequence element in the control region (CR) of the M genome that acts as a binding site for the formation of a complex with a protein factor that occurs in the male gonad. An adenine tract upstream to the element is also essential for the formation of the complex. The reaction is highly specific. It does not occur with protein extracts from the female gonad or from a male or female somatic tissue. Further experiments showed that the interaction takes place in mitochondria surrounding the nucleus of the cells of male gonads, suggesting a distinct role of perinuclear mitochondria. We propose that at a certain point during spermatogenesis mitochondria are subject to degradation and that perinuclear mitochondria with the M mtDNA–protein complex are protected from this degradation with the result that mature spermatozoa contain only the paternal mitochondrial genome.