Abstract

BackgroundDoubly Uniparental Inheritance (DUI) is a fascinating exception to matrilinear inheritance of mitochondrial DNA (mtDNA). Species with DUI are characterized by two distinct mtDNAs that are inherited either through females (F-mtDNA) or through males (M-mtDNA). DUI sex-linked mitochondrial genomes share several unusual features, such as additional protein coding genes and unusual gene duplications/structures, which have been related to the functionality of DUI. Recently, new evidence for DUI was found in the mytilid bivalve Musculista senhousia. This paper describes the complete sex-linked mitochondrial genomes of this species.ResultsOur analysis highlights that both M and F mtDNAs share roughly the same gene content and order, but with some remarkable differences. The Musculista sex-linked mtDNAs have differently organized putative control regions (CR), which include repeats and palindromic motifs, thought to provide sites for DNA-binding proteins involved in the transcriptional machinery. Moreover, in male mtDNA, two cox2 genes were found, one (M-cox2b) 123bp longer.ConclusionsThe complete mtDNA genome characterization of DUI bivalves is the first step to unravel the complex genetic signals allowing Doubly Uniparental Inheritance, and the evolutionary implications of such an unusual transmission route in mitochondrial genome evolution in Bivalvia. The observed redundancy of the palindromic motifs in Musculista M-mtDNA may have a role on the process by which sperm mtDNA becomes dominant or exclusive of the male germline of DUI species. Moreover, the duplicated M-COX2b gene may have a different, still unknown, function related to DUI, in accordance to what has been already proposed for other DUI species in which a similar cox2 extension has been hypothesized to be a tag for male mitochondria.

Highlights

  • Uniparental Inheritance (DUI) is a fascinating exception to matrilinear inheritance of mitochondrial DNA

  • The size of both F and M mitochondrial genomes are within the size range of mollusk mitochondrial DNA (mtDNA) sequenced to date, i.e. from 7808 bp in Batilaria cumingi to 32,115 bp in Placopecten magellanicus

  • When compared to other Mytilidae, only four gene boundaries are shared with Mytilus, i.e. rrnS-nad6, nad2-cox3, nad4L-nad5 and nad3-cox1, while the rest of the genome is different, highlighting that gene arrangement evolves rapidly within the family

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Summary

Introduction

Uniparental Inheritance (DUI) is a fascinating exception to matrilinear inheritance of mitochondrial DNA (mtDNA). DUI sex-linked mitochondrial genomes share several unusual features, such as additional protein coding genes and unusual gene duplications/structures, which have been related to the functionality of DUI. Metazoan mitochondrial DNA (mtDNA) is generally a small molecule (15-20 kb), and much larger mitochondrial genomes have occasionally been found, they are often products of duplications of mtDNA portions, rather than variations in gene content [1,2]. ‘Control Region’, CR), but it is unclear whether it is homologous among distantly related animals or, alternatively, it independently arose from various non-coding sequences. This difficulty in establishing homology is because CRs share sequence similarity only among closely related taxa. All metazoan mitochondrial genes have homologs in plants, fungi and/or protists [6,7,8,9]

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