Evidence for somatic transcription of male-transmitted mitochondrial genome in the DUI species Ruditapes philippinarum (Bivalvia: Veneridae)

Abstract

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.