The Control Region of Maternally and Paternally Inherited Mitochondrial Genomes of Three Species of the Sea Mussel Genus Mytilus

Abstract

Species of the mussel genus Mytilus possess maternally and paternally transmitted mitochondrial genomes. In the interbreeding taxa Mytilus edulis and M. galloprovincialis, several genomes of both types have been fully sequenced. The genome consists of the coding part (which, in addition to protein and RNA genes, contains several small noncoding sequences) and the main control region (CR), which in turn consists of three distinct parts: the first variable (VD1), the conserved (CD), and the second variable (VD2) domain. The maternal and paternal genomes are very similar in gene content and organization, even though they differ by .20% in primary sequence. They differ even more at VD1 and VD2, yet they are remarkably similar at CD. The complete sequence of a genome from the closely related species M. trossulus was previously reported and found to consist of a maternal-like coding part and a paternal-like and a maternal-like CR. From this and from the fact that it was extracted from a male individual, it was inferred that this is a genome that switched from maternal to paternal transmission. Here we provide clear evidence that this genome is the maternal genome of M. trossulus. We have found that in this genome the tRNA Gln in the coding region is apparently defective and that an intact copy of this tRNA occurs in the CR, that one of the two conserved domains is missing essential motifs, and that one of the two first variable domains has a high rate of divergence. These features may explain the large size and mosaic structure of the CR of the maternal genome of M. trossulus. We have also obtained CR sequences of the maternal and paternal genomes of M. californianus, a more distantly related species. We compare the control regions from all three species, focusing on the divergence among genomes of different species origin and among genomes of different transmission routes.

Comparative Mitochondrial Genomics of Freshwater Mussels (Bivalvia: Unionoida) With Doubly Uniparental Inheritance of mtDNA: Gender-Specific Open Reading Frames and Putative Origins of Replication

“…In contrast, the first and last domains are among the most divergent parts of the M and F genomes. It has been suggested that this tripartite structure, which is also a characteristic of the mammalian control region, demonstrates that different parts of the control region evolve under different selective constraints (Cao et al 2004a(Cao et al , 2009). In freshwater mussels (Unionoida), the high degree of sequence divergence observed among species and also between intraspecific F and M genomes presents a challenge for characterizing the structure of any of the shared unassigned regions.…”

“…For the more distantly related species, pairwise comparisons within each gender revealed, as expected, higher levels of nucleotide sequence divergence (.45%). Identification of conserved motifs or regions with high similarity to the other DUI-species control regions: Previous analyses of the mytiloid mussel Mytilus have shown that the F and M main control regions can be divided into three domains on the basis of indels and patterns of nucleotide variation (Cao et al 2004a(Cao et al , 2009). The middle domain of the control region encodes a hairpin structure and is the most slowly evolving part of the mitochondrial genome.…”

“…Overall, these studies have shown (i) a high level of nucleotide sequence divergence but nearly identical gene content between F and M genomes within each species, (ii) an accelerated rate of molecular evolution of both the M and the F genomes compared to other animal mitochondrial genomes, (iii) an accelerated rate of molecular evolution of M genomes compared to F genomes, (iv) an absence of atp8 in mytiloid mussels, (v) the presence of a second trnM (i.e., transfer RNA gene for methionine) in mytiloid and veneroid bivalves, (vi) recombination between M and F genomes in mytiloid mussels, (vii) periodic ''role reversals'' (masculinization) of female-transmitted mtDNA in mytiloid mussels that are subsequently transmitted through sperm, (viii) different gene order between F and M genomes in unionoids, and (ix) the presence of a unique extension of the cytochrome c oxidase subunit II gene in the M (but not the F) genome in unionoids (reviewed in Breton et al 2007; see also Chapman et al 2008). An important hypothesis that has emerged from sequencing studies of species with DUI is that genderspecific sequences and/or sequences that exhibit the highest level of nucleotide divergence between the F and M genomes (i.e., regions that are under different, potentially gender-specific selective constraints and could, therefore, have different roles in either genome) are the most likely candidates for determining whether a mitochondrial genome will be transmitted maternally or paternally (Zouros 2000;Burzyń ski et al 2003;Cao et al 2004a;Breton et al 2006Breton et al , 2007Theologidis et al 2007;Venetis et al 2007;Cao et al 2009). For example, it has been demonstrated in marine mussels that masculinized type genomes (i.e., an F genome that ''masculinizes'' and takes on the role of the previous M genome) are essentially recombinants composed of an F genome's coding and control regions, with an additional standard M-type control region (Burzyń ski et al 2003;Breton et al 2006;Venetis et al 2007).…”

“…Identifying the unionoid F and M control regions is essential for a more complete understanding of DUI. Studies of mytiloid genomes that have switched from maternal to paternal transmission have provided evidence that specific sequences of the mtDNA genome that control the mode of inheritance (i.e., male or female transmission) are located in the control region (Burzyński et al 2003;Breton et al 2006;Venetis et al 2007;Cao et al 2009). It is therefore critical that the control region in unionoids be confirmed to facilitate comparative studies of the developmental control of the F and M genomes across all bivalve species that possess DUI.…”

Comparative mitogenomic analysis reveals cryptic species: A case study in Mactridae (Mollusca: Bivalvia)

“…In the class Bivalvia, there are five genera which have at least two complete genomes reported, hongkongensis, C. iredalei, C. nippona, C. sikamea and C. virginica) were obtained from GenBank Breton et al, 2006;Cao et al, 2009;He et al, 2011;Milbury and Gaffney, 2005;Mizi et al, 2005;Ren et al, 2009a;Ren et al, 2009b;Wang et al, 2010;Wang et al, 2011;Wu et al, 2010;Xu et al, 2012;Yu and Li, 2011;Yuan et al, 2012). In addition to the mitochondrial genome sequence of M. chinensis from this study, the three recent reported mitochondrial genomes from Mactra veneriformis and Coelomactra antiquata (two genomes from the latter with specimens from Ri Zhao, Shandong Province in northern China and Zhang Zhou, Fujian Province in southern China) (Meng et al, 2013a;Meng et al, 2012;Meng et al, 2013c) were included in the phylogenetic analysis which includes a total of 25 bivalve mitochondrial genomes.…”