Mitochondrial Genes, Sex Determination and Hermaphroditism in Freshwater Mussels (Bivalvia: Unionoida)

Abstract

Many bivalves, including both marine and freshwater mussels, have an unusual system of “doubly uniparental inheritance” (DUI) of mitochondrial (mt) DNA. In species with DUI, males are heteroplasmic for a male-transmitted (M-type) mitochondrial genome that is dominant in sperm and a female-transmitted (F-type) mitochondrial genome. The F-type genome is found in somatic tissues of both sexes as well as in eggs. In unionoid freshwater mussels, dioecious species have been shown to have both M and F-type genomes. Sequence analysis of mt genomes has shown that there are gender-specific, novel, open reading frames (orfs) in the F- and M-type genomes, respectively, in all dioecious freshwater mussel species examined (i.e., an F-orf and an M-orf, respectively). In contrast, hermaphroditic freshwater mussels lose the M-type genome completely (and, concomitantly, the M-orf is lost as well) and the remaining F-type undergoes macromutations in the F-orf. We refer to this highly modified orf in hermaphrodites as the “H-orf”. The functions of the F-orf, M-orf, and H-orf genes and their protein products have not yet been determined. However, immunoelectron microscopy has demonstrated the F-ORF protein in mitochondria (which is consistent with a mitochondrial encoded protein) but also on the nuclear membrane and in the nucleoplasm (which is not thought normal for a mitochondrial encoded protein). The presence of this protein in extra-mitochondrial locations suggests a non-oxidative phosphorylation function for the F-ORF protein and has led to the hypothesis that this protein is involved in the genetic regulatory network specifying dioecy (separate males and females) in freshwater mussels. Future research should focus on the period of transitioning from dioecy to hermaphroditism to characterize key mutational changes in the orf gene(s) associated with this change in reproductive strategy.