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Rearrangement and evolution of mitochondrial genomes in Thysanoptera (Insecta)

Prior to this study, complete mitochondrial genomes from Order Thysanoptera were restricted to a single family, the Thripidae, resulting in a biased view of their evolution. Here we present the sequences for the mitochondrial genomes of four additional thrips species, adding three extra families and...

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Autores principales: Tyagi, Kaomud, Chakraborty, Rajasree, Cameron, Stephen L., Sweet, Andrew D., Chandra, Kailash, Kumar, Vikas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6971079/
https://www.ncbi.nlm.nih.gov/pubmed/31959910
http://dx.doi.org/10.1038/s41598-020-57705-4
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author Tyagi, Kaomud
Chakraborty, Rajasree
Cameron, Stephen L.
Sweet, Andrew D.
Chandra, Kailash
Kumar, Vikas
author_facet Tyagi, Kaomud
Chakraborty, Rajasree
Cameron, Stephen L.
Sweet, Andrew D.
Chandra, Kailash
Kumar, Vikas
author_sort Tyagi, Kaomud
collection PubMed
description Prior to this study, complete mitochondrial genomes from Order Thysanoptera were restricted to a single family, the Thripidae, resulting in a biased view of their evolution. Here we present the sequences for the mitochondrial genomes of four additional thrips species, adding three extra families and an additional subfamily, thus greatly improving taxonomic coverage. Thrips mitochondrial genomes are marked by high rates of gene rearrangement, duplications of the control region and tRNA mutations. Derived features of mitochondrial tRNAs in thrips include gene duplications, anticodon mutations, loss of secondary structures and high gene translocation rates. Duplicated control regions are found in the Aeolothripidae and the ‘core’ Thripinae clade but do not appear to promote gene rearrangement as previously proposed. Phylogenetic analysis of thrips mitochondrial sequence data supports the monophyly of two suborders, a sister-group relationship between Stenurothripidae and Thripidae, and suggests a novel set of relationships between thripid genera. Ancestral state reconstructions indicate that genome rearrangements are common, with just eight gene blocks conserved between any thrips species and the ancestral insect mitochondrial genome. Conversely, 71 derived rearrangements are shared between at least two species, and 24 of these are unambiguous synapomorphies for clades identified by phylogenetic analysis. While the reconstructed sequence of genome rearrangements among the protein-coding and ribosomal RNA genes could be inferred across the phylogeny, direct inference of phylogeny from rearrangement data in MLGO resulted in a highly discordant set of relationships inconsistent with both sequence-based phylogenies and previous morphological analysis. Given the demonstrated rates of genomic evolution within thrips, extensive sampling is needed to fully understand these phenomena across the order.
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spelling pubmed-69710792020-01-27 Rearrangement and evolution of mitochondrial genomes in Thysanoptera (Insecta) Tyagi, Kaomud Chakraborty, Rajasree Cameron, Stephen L. Sweet, Andrew D. Chandra, Kailash Kumar, Vikas Sci Rep Article Prior to this study, complete mitochondrial genomes from Order Thysanoptera were restricted to a single family, the Thripidae, resulting in a biased view of their evolution. Here we present the sequences for the mitochondrial genomes of four additional thrips species, adding three extra families and an additional subfamily, thus greatly improving taxonomic coverage. Thrips mitochondrial genomes are marked by high rates of gene rearrangement, duplications of the control region and tRNA mutations. Derived features of mitochondrial tRNAs in thrips include gene duplications, anticodon mutations, loss of secondary structures and high gene translocation rates. Duplicated control regions are found in the Aeolothripidae and the ‘core’ Thripinae clade but do not appear to promote gene rearrangement as previously proposed. Phylogenetic analysis of thrips mitochondrial sequence data supports the monophyly of two suborders, a sister-group relationship between Stenurothripidae and Thripidae, and suggests a novel set of relationships between thripid genera. Ancestral state reconstructions indicate that genome rearrangements are common, with just eight gene blocks conserved between any thrips species and the ancestral insect mitochondrial genome. Conversely, 71 derived rearrangements are shared between at least two species, and 24 of these are unambiguous synapomorphies for clades identified by phylogenetic analysis. While the reconstructed sequence of genome rearrangements among the protein-coding and ribosomal RNA genes could be inferred across the phylogeny, direct inference of phylogeny from rearrangement data in MLGO resulted in a highly discordant set of relationships inconsistent with both sequence-based phylogenies and previous morphological analysis. Given the demonstrated rates of genomic evolution within thrips, extensive sampling is needed to fully understand these phenomena across the order. Nature Publishing Group UK 2020-01-20 /pmc/articles/PMC6971079/ /pubmed/31959910 http://dx.doi.org/10.1038/s41598-020-57705-4 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Tyagi, Kaomud
Chakraborty, Rajasree
Cameron, Stephen L.
Sweet, Andrew D.
Chandra, Kailash
Kumar, Vikas
Rearrangement and evolution of mitochondrial genomes in Thysanoptera (Insecta)
title Rearrangement and evolution of mitochondrial genomes in Thysanoptera (Insecta)
title_full Rearrangement and evolution of mitochondrial genomes in Thysanoptera (Insecta)
title_fullStr Rearrangement and evolution of mitochondrial genomes in Thysanoptera (Insecta)
title_full_unstemmed Rearrangement and evolution of mitochondrial genomes in Thysanoptera (Insecta)
title_short Rearrangement and evolution of mitochondrial genomes in Thysanoptera (Insecta)
title_sort rearrangement and evolution of mitochondrial genomes in thysanoptera (insecta)
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6971079/
https://www.ncbi.nlm.nih.gov/pubmed/31959910
http://dx.doi.org/10.1038/s41598-020-57705-4
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