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Eight new mtDNA sequences of glass sponges reveal an extensive usage of +1 frameshifting in mitochondrial translation.
Gene. 2014 Feb 10; 535(2):336-44.GENE

Abstract

Three previously studied mitochondrial genomes of glass sponges (phylum Porifera, class Hexactinellida) contained single nucleotide insertions in protein coding genes inferred as sites of +1 translational frameshifting. To investigate the distribution and evolution of these sites and to help elucidate the mechanism of frameshifting, we determined eight new complete or nearly complete mtDNA sequences from glass sponges and examined individual mitochondrial genes from three others. We found nine new instances of single nucleotide insertions in these sequences and analyzed them both comparatively and phylogenetically. The base insertions appear to have been gained and lost repeatedly in hexactinellid mt protein genes, suggesting no functional significance for the frameshifting sites. A high degree of sequence conservation, the presence of unusual tRNAs, and a distinct pattern of codon usage suggest the "out-of-frame pairing" model of translational frameshifting. Additionally, we provide evidence that relaxed selection pressure on glass sponge mtDNA - possibly a result of their low growth rates and deep-water lifestyle - has allowed frameshift insertions to be tolerated for hundreds of millions of years. Our study provides the first example of a phylogenetically diverse and extensive usage of translational frameshifting in animal mitochondrial coding sequences.

Authors+Show Affiliations

Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011, USA. Electronic address: khaen@iastate.edu.Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA 50011, USA.Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA 50011, USA.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

24177232

Citation

Haen, Karri M., et al. "Eight New mtDNA Sequences of Glass Sponges Reveal an Extensive Usage of +1 Frameshifting in Mitochondrial Translation." Gene, vol. 535, no. 2, 2014, pp. 336-44.
Haen KM, Pett W, Lavrov DV. Eight new mtDNA sequences of glass sponges reveal an extensive usage of +1 frameshifting in mitochondrial translation. Gene. 2014;535(2):336-44.
Haen, K. M., Pett, W., & Lavrov, D. V. (2014). Eight new mtDNA sequences of glass sponges reveal an extensive usage of +1 frameshifting in mitochondrial translation. Gene, 535(2), 336-44. https://doi.org/10.1016/j.gene.2013.10.041
Haen KM, Pett W, Lavrov DV. Eight New mtDNA Sequences of Glass Sponges Reveal an Extensive Usage of +1 Frameshifting in Mitochondrial Translation. Gene. 2014 Feb 10;535(2):336-44. PubMed PMID: 24177232.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Eight new mtDNA sequences of glass sponges reveal an extensive usage of +1 frameshifting in mitochondrial translation. AU - Haen,Karri M, AU - Pett,Walker, AU - Lavrov,Dennis V, Y1 - 2013/10/28/ PY - 2013/05/28/received PY - 2013/10/17/revised PY - 2013/10/21/accepted PY - 2013/11/2/entrez PY - 2013/11/2/pubmed PY - 2014/3/13/medline KW - ATP synthase F0 subunit 6 KW - ATP synthase F0 subunit 8 KW - Codon usage KW - Hexactinellida KW - Mitochondrial frameshift KW - Mitochondrial genome KW - NADH dehydrogenase subunit 1 KW - NADH dehydrogenase subunit 2 KW - NADH dehydrogenase subunit 3 KW - NADH dehydrogenase subunit 4 KW - NADH dehydrogenase subunit 4l KW - NADH dehydrogenase subunit 5 KW - NADH dehydrogenase subunit 6 KW - OXPHOS KW - Oxidative phosphorylation KW - Programmed translational frameshift KW - atp6 KW - atp8 KW - cob KW - cox1 KW - cox2 KW - cox3 KW - cytochrome b KW - cytochrome c oxidase subunit 1 KW - cytochrome c oxidase subunit 2 KW - cytochrome c oxidase subunit 3 KW - mitochondrial 12s ribosomal RNA KW - mitochondrial 16s ribosomal RNA KW - nad1 KW - nad2 KW - nad3 KW - nad4 KW - nad4L KW - nad5 KW - nad6 KW - oxidative phosphorylation KW - rnl KW - rns SP - 336 EP - 44 JF - Gene JO - Gene VL - 535 IS - 2 N2 - Three previously studied mitochondrial genomes of glass sponges (phylum Porifera, class Hexactinellida) contained single nucleotide insertions in protein coding genes inferred as sites of +1 translational frameshifting. To investigate the distribution and evolution of these sites and to help elucidate the mechanism of frameshifting, we determined eight new complete or nearly complete mtDNA sequences from glass sponges and examined individual mitochondrial genes from three others. We found nine new instances of single nucleotide insertions in these sequences and analyzed them both comparatively and phylogenetically. The base insertions appear to have been gained and lost repeatedly in hexactinellid mt protein genes, suggesting no functional significance for the frameshifting sites. A high degree of sequence conservation, the presence of unusual tRNAs, and a distinct pattern of codon usage suggest the "out-of-frame pairing" model of translational frameshifting. Additionally, we provide evidence that relaxed selection pressure on glass sponge mtDNA - possibly a result of their low growth rates and deep-water lifestyle - has allowed frameshift insertions to be tolerated for hundreds of millions of years. Our study provides the first example of a phylogenetically diverse and extensive usage of translational frameshifting in animal mitochondrial coding sequences. SN - 1879-0038 UR - https://www.unboundmedicine.com/medline/citation/24177232/Eight_new_mtDNA_sequences_of_glass_sponges_reveal_an_extensive_usage_of_+1_frameshifting_in_mitochondrial_translation_ DB - PRIME DP - Unbound Medicine ER -