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

Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing, China.
PLoS ONE (Impact Factor: 3.23). 03/2012; 7(3):e33973. DOI: 10.1371/journal.pone.0033973
Source: PubMed


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Liposcelis bostrychophila and found that the typical single mt chromosome of bilateral animals has fragmented into and been replaced by two medium-sized chromosomes in this booklouse; each of these chromosomes has about half of the genes of the typical mt chromosome of bilateral animals.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.

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    • "different species because different copies of tandemly repeated elements are usually present (Zhang and Hewitt, 1997). Besides the variation of the encoding genes and control region, the gene order of insect mt genome is also occasionally variable, e.g. in some species of Psocodea (Shao et al., 2001, 2003, 2009, 2012; Wei et al., 2012; Cameron et al., 2007, 2011; Covacin et al., 2006a, 2006b) although it is highly conserved in most insects (Boore, 1999; Wolstenholme, 1992). "
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    • "For instance, mt genomes that consist of multiple chromosomes have been reported in parasitic lice [7]–[9], booklice [3], rotifera [10] and nematodes [11]–[13]. Variations in mt genome organization may provide a novel perspective for understanding animal evolution [14]–[16], in addition to genome sequences [3], [17], RNA secondary structures [7], [18]–[20], and gene rearrangements [5], [18], [21], [22]. "
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    ABSTRACT: Booklice in the genus Liposcelis are pests of stored grain products. They pose a considerable economic threat to global food security and safety. To date, the complete mitochondrial genome has only been determined for a single booklouse species Liposcelis bostrychophila. Unlike most bilateral animals, which have their 37 mt genes on one circular chromosome, ≈15 kb in size, the mt genome of L. bostrychophila has two circular chromosomes, 8 and 8.5 kb in size. Here, we report the mt genome of another booklouse, Liposcelis decolor. The mt genome of L. decolor has the typical mt chromosome of bilateral animals, 14,405 bp long with 37 genes (13 PCGs, 22 tRNAs and 2 rRNAs). However, the arrangement of these genes in L. decolor differs substantially from that observed in L. bostrychophila and other insects. With the exception of atp8-atp6, L. decolor differs from L. bostrychophila in the arrangement of all of the other 35 genes. The variation in the mt genome organization and mt gene arrangement between the two Liposcelis species is unprecedented for closely related animals in the same genus. Furthermore, our results indicate that the two-chromosome mt genome organization observed in L. bostrychophila likely evolved recently after L. bostrychophila and L. decolor split from their most recent common ancestor.
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    • "The fragmented mitochondrial genomes of the human lice and the pig lice represent the most radical departure to date in bilateral animals from the typical, single-chromosome organization of mt genomes, although multipartite mt genomes have also been observed in the rotifer, Brachionus plicatilis, and the booklouse, Liposcelis bostrychophila, which have two mt chromosomes [13,14], and the potato cyst nematode, Globodera pallida, which has six chromosomes [15]. Outside bilateral animals, highly fragmented mt genomes were observed in ichthyosporean protists [16], diplonemid protists [17] and box jellyfish [18]. "
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