New insights into mitochondrial segregation from the Doubly Uniparental Inheritance system in bivalves

While nuclear genome segregation is well characterized, mechanisms underlying mitochondrial partitioning remain partially obscure, even though its failure can cause developmental arrest or harmful mutations. This knowledge gap invokes the need for new, more suitable model systems to study such mechanisms. Doubly Uniparental Inheritance (DUI) of mitochondria in bivalves is a useful system for such studies. In DUI, sperm mitochondria in male embryos are actively transported across cell divisions to precursors of the germline, and this male-specific pattern depends on maternal factors stored in eggs. The presence of distinct mitochondrial segregation patterns in male and female embryos offers a unique opportunity to investigate the molecular bases of this process.

Here, we leveraged this system by (1) performing RNA-Seq on eggs producing male-biased versus female-biased progenies in the Mediterranean mussel Mytilus galloprovincialis to identify factors involved in differential mitochondrial segregation; and (2) inferring signatures of convergent evolutionary rate across DUI bivalve genomes to separate segregation-specific factors from those involved in sex determination. We show that differentially transcribed genes across eggs that give rise to either male- or female-biased progeny are predominantly associated with mitochondrial dynamics, cytoskeletal organization, and vesicular trafficking. We also identified multiple long noncoding RNAs-many derived from transposable elements-that might have roles in the regulation of other maternally supplied factors that shepherd paternal mitochondria.

By overlaying clues from expression and sequence evolution, we delineate a conserved protein-protein interaction network of factors that mediate mitochondrial segregation. This study reveals general principles of organelle selection in animals and unveils the contribution of new factors.