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Liposcelis bostrychophila and found that the typical single mt chromosome of bilateral animals has fragmented into and been replaced by two medium-sized chromosomes in this booklouse; each of these chromosomes has about half of the genes of the typical mt chromosome of bilateral animals.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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    ABSTRACT: The Plecoptera (stoneflies) is a hemimetabolous order of insects, whose larvae are usually used as indicators for fresh water biomonitoring. Herein, we describe the complete mitochondrial (mt) genome of a stonefly species, namely Acroneuria hainana Wu belonging to the family Perlidae. This mt genome contains 13 PCGs, 22 tRNA-coding genes and 2 rRNA-coding genes that are conserved in most insect mt genomes, and it also has the identical gene order with the insect ancestral gene order. However, there are three special initiation codons of ND1, ND5 and COI in PCGs: TTG, GTG and CGA, coding for L, V and R, respectively. Additionally, the 899-bp control region, with 73.30% A+T content, has two long repeated sequences which are found at the 3'-end closing to the tRNA(Ile) gene. Both of them can be folded into a stem-loop structure, whose adjacent upstream and downstream sequences can be also folded into stem-loop structures. It is presumed that the four special structures in series could be associated with the D-loop replication. It might be able to adjust the replication speed of two replicate directions. Copyright © 2014 Elsevier B.V. All rights reserved.
    Gene 12/2014; 557(1). DOI:10.1016/j.gene.2014.12.009 · 2.14 Impact Factor
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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.
    PLoS ONE 03/2014; 9(3):e91902. DOI:10.1371/journal.pone.0091902 · 3.23 Impact Factor
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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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    ABSTRACT: Blood-sucking lice (suborder Anoplura) parasitize eutherian mammals with 67% of the 540 described species found on rodents. The five species of blood-sucking lice that infest humans and pigs have fragmented mitochondrial genomes and differ substantially in the extent of fragmentation. To understand whether, or not, any life-history factors are linked to such variation, we sequenced the mt genomes of Polyplax asiatica and Polyplax spinulosa, collected from the greater bandicoot rat, Bandicota indica, and the Asian house rat, Rattus tanezumi, respectively. We identified all of the 37 mitochondrial genes common to animals in Polyplax asiatica and Polyplax spinulosa. The mitochondrial genes of these two rat lice are on 11 circular minichromosomes; each minichromosome is 2-4 kb long and has 2-7 genes. The two rat lice share the same pattern for the distribution of the protein-coding genes and ribosomal RNA genes over the minichromosomes, but differ in the pattern for the distribution of 8 of the 22 transfer RNA genes. The mitochondrial genomes of the Polyplax rat lice have 3.4 genes, on average, on each minichromosome and, thus, are less fragmented than those of the human lice (2.1 and 2.4 genes per minichromosome), but are more fragmented than those of the pig lice (4.1 genes per minichromosome). Our results revealed distinct patterns of mitochondrial genome fragmentation within the genus Polyplax and, furthermore, indicated a possible inverse link between the extent of mitochondrial genome fragmentation and the length of life cycle of the blood-sucking lice.
    BMC Genomics 01/2014; 15(1):44. DOI:10.1186/1471-2164-15-44 · 3.99 Impact Factor
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