The Multipartite Mitochondrial Genome of Liposcelis bostrychophila: Insights into the Evolution of Mitochondrial Genomes in Bilateral Animals

Abstract

Booklice (order Psocoptera) in the genus Liposcelis are major pests to stored grains worldwide and are closely related to parasitic lice (order Phthiraptera). We sequenced the mitochondrial (mt) genome of Liposcelis bostrychophila and found that the typical single mt chromosome of bilateral animals has fragmented into and been replaced by two medium-sized chromosomes in this booklouse; each of these chromosomes has about half of the genes of the typical mt chromosome of bilateral animals. These mt chromosomes are 8,530 bp (mt chromosome I) and 7,933 bp (mt chromosome II) in size. Intriguingly, mt chromosome I is twice as abundant as chromosome II. It appears that the selection pressure for compact mt genomes in bilateral animals favors small mt chromosomes when small mt chromosomes co-exist with the typical large mt chromosomes. Thus, small mt chromosomes may have selective advantages over large mt chromosomes in bilateral animals. Phylogenetic analyses of mt genome sequences of Psocodea (i.e. Psocoptera plus Phthiraptera) indicate that: 1) the order Psocoptera (booklice and barklice) is paraphyletic; and 2) the order Phthiraptera (the parasitic lice) is monophyletic. Within parasitic lice, however, the suborder Ischnocera is paraphyletic; this differs from the traditional view that each suborder of parasitic lice is monophyletic.

Maternal transmission, sex ratio distortion, and mitochondria

“…Draft assemblies for each line were generated with Ray v2.20 (k = 31) (98). We searched assemblies for mitochondrial genes using tblastx, with sequenced L. bostrychophila mitochondrial genomes as queries (82). Pieces of retrieved genes (400-800 bp) were then used as seeds in mitoBim (99) (proofreading mode) to corroborate and extend minicircles, before validation by PCR and Sanger sequencing (see Dataset S1 for primer sequence and PCR conditions).…”

“…Both distorter and normal individuals had multipartite mitochondrial genomes, consisting of at least five and seven minicircles, respectively. Minicircle mitochondrial genomes have been documented in a number of Psocodea (81), ranging from two in L. bostrychophila and two other Liposcelis species (82,83) [although another species, Liposcelis decolor, has a single "canonical" chromosome (84)], all the way to the extreme case in the human louse, Pediculus humanus, whose mitochondrial genome consists of 18 minicircles (85). Although many other mitochondria (and plastids) have evolved minicircle genome architecture (86,87), in arthropods this organization is apparently restricted to Psocodea.…”

The complete mitochondrial genome sequence of the western flower thrips Frankliniella occidentalis (Thysanoptera: Thripidae) contains triplicate putative control regions

“…Duplicated CRs are found in the snake Dinodon semicarinatus (Kumazawa et al, 1998), cephalopod Loligo bleekeri (Tomita et al, 2002), brown dog tick Rhipicephalus sanguineus (Black and Roehrdanz, 1998), plague thrips Thrips imagines (Shao and Barker, 2003), sea-firefly Vargula hilgendorfii (Ogoh and Ohmiya, 2004), Australasian Ixodes ticks (Shao et al, 2005), Leptotrombidium mites (Shao et al, 2006) and Liposcelis bostrychophila (Wei et al, 2012). Three CRs have been reported in Metaperipatus inae (Braband et al, 2010).…”

“…The mt genomes of most metazoa studied to date have only one CR. However, those of some snakes (Kumazawa et al, 1996), sea cucumbers (Arndt and Smith, 1998), metastriate ticks (Black and Roehrdanz, 1998;Campbell and Barker, 1999), Amazon parrots (Eberhard et al, 2001), a fish (Lee et al, 2001), a thrips (Shao and Barker, 2003), a sea firefly (Ogoh and Ohmiya, 2004), some ticks (Shao et al, 2005), some chigger mites (Shao et al, 2006) and a booklice (Wei et al, 2012) have duplicate CRs. Specifically, there are two separate CRs with identical or highly similar nucleotide sequences.…”

The Complete Mitochondrial Genome of Aleurocanthus camelliae: Insights into Gene Arrangement and Genome Organization within the Family Aleyrodidae

“…The animal ancestral genome organization is retained in most insects, although minor changes were observed in some species [14,17]. In several groups of insects, mt genome organizations are not conservative and contain a lot of gene absences and rearrangements, pseudogenes or have been fragmented [5,8,18,19]. …”