Mitochondrial genomes and Doubly Uniparental Inheritance: new insights from Musculista senhousia sex-linked mitochondrial DNAs (Bivalvia Mytilidae)

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.

A Comparative Analysis of Mitochondrial ORFans: New Clues on Their Origin and Role in Species with Doubly Uniparental Inheritance of Mitochondria

“…Long PCRs, using gamete DNA extractions as template, were performed to obtain a segment containing the whole Largest Unassigned Region (LUR) (i.e., in both mtDNAs, the region between rrnL and cob ); in the F-mtDNA, this region also contains the Female Unassigned Region 2 (FUR2) (see Passamonti et al 2011 for annotation details). Primers for long-PCRs are the same used in Passamonti et al (2011): M-mtDNA from sperm was amplified with primers M-16S103F and M-cob386R, whereas F-mtDNA from eggs with primers F-16S142F and F-cob383R (supplementary material S1, Supplementary Material online).…”

“…Primers for long-PCRs are the same used in Passamonti et al (2011): M-mtDNA from sperm was amplified with primers M-16S103F and M-cob386R, whereas F-mtDNA from eggs with primers F-16S142F and F-cob383R (supplementary material S1, Supplementary Material online). Both segments were amplified with Herculase II Fusion Enzyme kit (Stratagene) in a 50 µl reaction volume composed of 10 µl 5× Herculase II Run Buffer, 0.5 µl of 100 mM dNTP mix, 1.25 µl of 10 µM primers, 0.5 µl of Herculase II Fusion DNA Polymerase, 5 µl of total DNA, and 31.5 µl of Nuclease-free water (Ambion Inc.).…”

“…galloprovincialis , and Myt. trossulus ) (Bivalvia, Mytilidae) were checked to assess the conservation of the ORFs described in Passamonti et al (2011) and Breton et al (2011b) (last GenBank access: September 2012). The new sequences of M. senhousia LURs were also searched for the presence of novel ORFs (only the longest ORFs found in all sequences were considered).…”

“…For example, novel mitochondrial Open Reading Frames (ORFs) can arise from gene duplication. In bivalve molluscs, a cox2 duplication is found in the clam Ruditapes philippinarum (Bivalvia, Veneridae) (Okazaki M and Ueshima R, unpublished data; GenBank AB065375.1) and in the mussel Musculista senhousia (Bivalvia, Mytilidae) (Passamonti et al 2011). Moreover, nad2 duplication is at the origin of two novel ORFs in the oyster genus Crassostrea (Bivalvia, Ostreidae) (Wu et al 2012).…”

Proteomic Analysis of Eggs from Mytilus edulis Females Differing in Mitochondrial DNA Transmission Mode

“…Many candidate functional differences have been discovered including rearrangements in the control region (e.g. [22][23][24][25], a second copy of the cytochrome oxidase II (CoII gene) in the M genome of the mytilid Musculista senhousia (25), F and M specific open reading frames (26), and an M genome insertion extending the COII gene in unionid bivalves (27,28). In M. galloprovincialis, the M genome is transcribed in spermatogonia and spermatocytes, though not in somatic tissue (29).…”