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A novel mitochondrial genome architecture in thrips (Insecta: Thysanoptera): extreme size asymmetry among chromosomes and possible recent control region duplication.

ABSTRACT: Multipartite mitochondrial genomes are very rare in animals but have been found previously in two insect orders with highly rearranged genomes, the Phthiraptera (parasitic lice), and the Psocoptera (booklice/barklice).We provide the first report of a multipartite mitochondrial genome architecture in a third order with highly rearranged genomes: Thysanoptera (thrips). We sequenced the complete mitochondrial genomes of two divergent members of the Scirtothrips dorsalis cryptic species complex. The East Asia 1 species has the single circular chromosome common to animals while the South Asia 1 species has a genome consisting of two circular chromosomes. The fragmented South Asia 1 genome exhibits extreme chromosome size asymmetry with the majority of genes on the large, 14.28 kb, chromosome and only nad6 and trnC on the 0.92 kb mini-circle chromosome. This genome also features paralogous control regions with high similarity suggesting a very recent origin of the nad6 mini-circle chromosome in the South Asia 1 cryptic species.Thysanoptera, along with the other minor paraenopteran insect orders should be considered models for rapid mitochondrial genome evolution, including fragmentation. Continued use of these models will facilitate a greater understanding of recombination and other mitochondrial genome evolutionary processes across eukaryotes.

SUBMITTER: Dickey AM

PROVIDER: S-EPMC4460840 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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A novel mitochondrial genome architecture in thrips (Insecta: Thysanoptera): extreme size asymmetry among chromosomes and possible recent control region duplication.

Dickey Aaron M AM Kumar Vivek V Morgan J Kent JK Jara-Cavieres Antonella A Shatters Robert G RG McKenzie Cindy L CL Osborne Lance S LS

BMC genomics 20150609

<h4>Background</h4>Multipartite mitochondrial genomes are very rare in animals but have been found previously in two insect orders with highly rearranged genomes, the Phthiraptera (parasitic lice), and the Psocoptera (booklice/barklice).<h4>Results</h4>We provide the first report of a multipartite mitochondrial genome architecture in a third order with highly rearranged genomes: Thysanoptera (thrips). We sequenced the complete mitochondrial genomes of two divergent members of the Scirtothrips do ...[more]

PMID: 26055161

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Project description:Simple Summary Aeolothrips, commonly known as banded thrips, is the largest genus of the family Aeolothripidae (predatory thrips). In the current study, we sequenced the mitochondrial genome (mitogenome) of the banded thrip species Aeolothrips xinjiangensis. We found a novel gene arrangement in this mitogenome that has not been reported in Thysanoptera. By comparing the gene order and rearrangement patterns, we found seven identical gene blocks and three identical rearrangement events in two mitogenomes of banded thrips. There was marked variation in the mitochondrial gene order across thrip species, with only two conserved gene blocks shared by all 14 thrips. In addition, we found a positive correlation between the degree of gene rearrangement and evolutionary rate. Our results suggested that the mitogenomes of thrips have tended to be stable since their massive rearrangement. Abstract Extensive gene rearrangement is characteristic in the mitogenomes of thrips (Thysanoptera), but the historical process giving rise to the contemporary gene rearrangement pattern remains unclear. To better understand the evolutionary processes of gene rearrangement in the mitogenomes of thrips, we sequenced the mitogenome of the banded thrip species Aeolothrips xinjiangensis. First, we found a novel mitochondrial gene order in this species. This mitogenome is 16,947 bp in length and encodes the typical 37 coding genes (13 protein-coding genes, 22 tRNA genes, and two rRNA genes) of insects. The gene arrangement was dramatically different from the putative ancestral mitogenome, with 26 genes being translocated, eight of which were inverted. Moreover, we found a novel, conserved gene block, trnC-trnY, which has not been previously reported in the mitogenomes of thrips. With this newly assembled mitogenome, we compared mitogenome sequences across Thysanoptera to assess the evolutionary processes giving rise to the current gene rearrangement pattern in thrips. Seven identical gene blocks were shared by two sequenced banded thrip mitogenomes, while the reversal of ND2 combined with TDRL events resulted in the different gene orders of these two species. In phylogenetic analysis, the monophyly of the suborders and families of Thysanoptera was well supported. Across the gene orders of 14 thrips, only two conserved gene blocks, ATP8-ATP6 and ND4-ND4L, could be found. Correlation analysis showed that the degree of gene rearrangement was positively correlated with the non-synonymous substitution rate in thrips. Our study suggests that the mitogenomes of thrips remain stable over long evolutionary timescales after massive rearrangement during early diversification.

Dataset Information

A novel mitochondrial genome architecture in thrips (Insecta: Thysanoptera): extreme size asymmetry among chromosomes and possible recent control region duplication.

Publications

A novel mitochondrial genome architecture in thrips (Insecta: Thysanoptera): extreme size asymmetry among chromosomes and possible recent control region duplication.

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