Coding palindromes in mitochondrial genes of Nematomorpha
Inverted repeats are common DNA elements, but they rarely overlap with protein-coding sequences due to the ensuing conflict with the structure and function of the encoded protein. We discovered numerous perfect inverted repeats of considerable length (up to 284 bp) embedded within the protein-coding...
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Veröffentlicht in: | Nucleic acids research 2019-07, Vol.47 (13), p.6858-6870 |
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creator | Mikhailov, Kirill V Efeykin, Boris D Panchin, Alexander Y Knorre, Dmitry A Logacheva, Maria D Penin, Aleksey A Muntyan, Maria S Nikitin, Mikhail A Popova, Olga V Zanegina, Olga N Vyssokikh, Mikhail Y Spiridonov, Sergei E Aleoshin, Vladimir V Panchin, Yuri V |
description | Inverted repeats are common DNA elements, but they rarely overlap with protein-coding sequences due to the ensuing conflict with the structure and function of the encoded protein. We discovered numerous perfect inverted repeats of considerable length (up to 284 bp) embedded within the protein-coding genes in mitochondrial genomes of four Nematomorpha species. Strikingly, both arms of the inverted repeats encode conserved regions of the amino acid sequence. We confirmed enzymatic activity of the respiratory complex I encoded by inverted repeat-containing genes. The nucleotide composition of inverted repeats suggests strong selection at the amino acid level in these regions. We conclude that the inverted repeat-containing genes are transcribed and translated into functional proteins. The survey of available mitochondrial genomes reveals that several other organisms possess similar albeit shorter embedded repeats. Mitochondrial genomes of Nematomorpha demonstrate an extraordinary evolutionary compromise where protein function and stringent secondary structure elements within the coding regions are preserved simultaneously. |
doi_str_mv | 10.1093/nar/gkz517 |
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We discovered numerous perfect inverted repeats of considerable length (up to 284 bp) embedded within the protein-coding genes in mitochondrial genomes of four Nematomorpha species. Strikingly, both arms of the inverted repeats encode conserved regions of the amino acid sequence. We confirmed enzymatic activity of the respiratory complex I encoded by inverted repeat-containing genes. The nucleotide composition of inverted repeats suggests strong selection at the amino acid level in these regions. We conclude that the inverted repeat-containing genes are transcribed and translated into functional proteins. The survey of available mitochondrial genomes reveals that several other organisms possess similar albeit shorter embedded repeats. Mitochondrial genomes of Nematomorpha demonstrate an extraordinary evolutionary compromise where protein function and stringent secondary structure elements within the coding regions are preserved simultaneously.</description><identifier>ISSN: 0305-1048</identifier><identifier>EISSN: 1362-4962</identifier><identifier>DOI: 10.1093/nar/gkz517</identifier><identifier>PMID: 31194871</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Amino Acid Sequence ; Animals ; Base Composition ; Base Sequence ; DNA, Helminth - genetics ; DNA, Ribosomal - genetics ; Electron Transport Complex I - genetics ; Evolution, Molecular ; Female ; Genes, Helminth - genetics ; Genes, Mitochondrial - genetics ; Genetic Code ; Genome, Mitochondrial ; Genomics ; Helminth Proteins - genetics ; Helminths - genetics ; Inverted Repeat Sequences - genetics ; Male ; Oxygen Consumption ; RNA, Helminth - genetics ; RNA, Ribosomal, 18S - genetics ; Selection, Genetic ; Sequence Alignment ; Sequence Homology, Amino Acid ; Species Specificity</subject><ispartof>Nucleic acids research, 2019-07, Vol.47 (13), p.6858-6870</ispartof><rights>The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research.</rights><rights>The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research. 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c444t-1dc2a7076e1bbc590ff861c6b694c8205335c8f1878f1fed6c0a11d90a6551503</citedby><cites>FETCH-LOGICAL-c444t-1dc2a7076e1bbc590ff861c6b694c8205335c8f1878f1fed6c0a11d90a6551503</cites><orcidid>0000-0002-0457-9625</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6649704/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6649704/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31194871$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mikhailov, Kirill V</creatorcontrib><creatorcontrib>Efeykin, Boris D</creatorcontrib><creatorcontrib>Panchin, Alexander Y</creatorcontrib><creatorcontrib>Knorre, Dmitry A</creatorcontrib><creatorcontrib>Logacheva, Maria D</creatorcontrib><creatorcontrib>Penin, Aleksey A</creatorcontrib><creatorcontrib>Muntyan, Maria S</creatorcontrib><creatorcontrib>Nikitin, Mikhail A</creatorcontrib><creatorcontrib>Popova, Olga V</creatorcontrib><creatorcontrib>Zanegina, Olga N</creatorcontrib><creatorcontrib>Vyssokikh, Mikhail Y</creatorcontrib><creatorcontrib>Spiridonov, Sergei E</creatorcontrib><creatorcontrib>Aleoshin, Vladimir V</creatorcontrib><creatorcontrib>Panchin, Yuri V</creatorcontrib><title>Coding palindromes in mitochondrial genes of Nematomorpha</title><title>Nucleic acids research</title><addtitle>Nucleic Acids Res</addtitle><description>Inverted repeats are common DNA elements, but they rarely overlap with protein-coding sequences due to the ensuing conflict with the structure and function of the encoded protein. We discovered numerous perfect inverted repeats of considerable length (up to 284 bp) embedded within the protein-coding genes in mitochondrial genomes of four Nematomorpha species. Strikingly, both arms of the inverted repeats encode conserved regions of the amino acid sequence. We confirmed enzymatic activity of the respiratory complex I encoded by inverted repeat-containing genes. The nucleotide composition of inverted repeats suggests strong selection at the amino acid level in these regions. We conclude that the inverted repeat-containing genes are transcribed and translated into functional proteins. The survey of available mitochondrial genomes reveals that several other organisms possess similar albeit shorter embedded repeats. Mitochondrial genomes of Nematomorpha demonstrate an extraordinary evolutionary compromise where protein function and stringent secondary structure elements within the coding regions are preserved simultaneously.</description><subject>Amino Acid Sequence</subject><subject>Animals</subject><subject>Base Composition</subject><subject>Base Sequence</subject><subject>DNA, Helminth - genetics</subject><subject>DNA, Ribosomal - genetics</subject><subject>Electron Transport Complex I - genetics</subject><subject>Evolution, Molecular</subject><subject>Female</subject><subject>Genes, Helminth - genetics</subject><subject>Genes, Mitochondrial - genetics</subject><subject>Genetic Code</subject><subject>Genome, Mitochondrial</subject><subject>Genomics</subject><subject>Helminth Proteins - genetics</subject><subject>Helminths - genetics</subject><subject>Inverted Repeat Sequences - genetics</subject><subject>Male</subject><subject>Oxygen Consumption</subject><subject>RNA, Helminth - genetics</subject><subject>RNA, Ribosomal, 18S - genetics</subject><subject>Selection, Genetic</subject><subject>Sequence Alignment</subject><subject>Sequence Homology, Amino Acid</subject><subject>Species Specificity</subject><issn>0305-1048</issn><issn>1362-4962</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkE1LxDAQhoMo7rp68QdIjyLUzTQfbS6CLH7Bohc9hzRNu9E2qUlX0F9vZddFLzMw8_DO8CB0CvgSsCBzp8K8eftikO-hKRCepVTwbB9NMcEsBUyLCTqK8RVjoMDoIZoQAEGLHKZILHxlXZP0qrWuCr4zMbEu6ezg9cqPE6vapDFuHPs6eTSdGnznQ79Sx-igVm00J9s-Qy-3N8-L-3T5dPewuF6mmlI6pFDpTOU45wbKUjOB67rgoHnJBdVFhhkhTBc1FPlYalNxjRVAJbDijAHDZIauNrn9uuxMpY0bgmplH2ynwqf0ysr_G2dXsvEfknMqckzHgPNtQPDvaxMH2dmoTdsqZ_w6yizj-WiGAR_Riw2qg48xmHp3BrD8cS1H13LjeoTP_j62Q3_lkm_IM3vf</recordid><startdate>20190726</startdate><enddate>20190726</enddate><creator>Mikhailov, Kirill V</creator><creator>Efeykin, Boris D</creator><creator>Panchin, Alexander Y</creator><creator>Knorre, Dmitry A</creator><creator>Logacheva, Maria D</creator><creator>Penin, Aleksey A</creator><creator>Muntyan, Maria S</creator><creator>Nikitin, Mikhail A</creator><creator>Popova, Olga V</creator><creator>Zanegina, Olga N</creator><creator>Vyssokikh, Mikhail Y</creator><creator>Spiridonov, Sergei E</creator><creator>Aleoshin, Vladimir V</creator><creator>Panchin, Yuri V</creator><general>Oxford University Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0457-9625</orcidid></search><sort><creationdate>20190726</creationdate><title>Coding palindromes in mitochondrial genes of Nematomorpha</title><author>Mikhailov, Kirill V ; Efeykin, Boris D ; Panchin, Alexander Y ; Knorre, Dmitry A ; Logacheva, Maria D ; Penin, Aleksey A ; Muntyan, Maria S ; Nikitin, Mikhail A ; Popova, Olga V ; Zanegina, Olga N ; Vyssokikh, Mikhail Y ; Spiridonov, Sergei E ; Aleoshin, Vladimir V ; Panchin, Yuri V</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c444t-1dc2a7076e1bbc590ff861c6b694c8205335c8f1878f1fed6c0a11d90a6551503</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Amino Acid Sequence</topic><topic>Animals</topic><topic>Base Composition</topic><topic>Base Sequence</topic><topic>DNA, Helminth - genetics</topic><topic>DNA, Ribosomal - genetics</topic><topic>Electron Transport Complex I - genetics</topic><topic>Evolution, Molecular</topic><topic>Female</topic><topic>Genes, Helminth - genetics</topic><topic>Genes, Mitochondrial - genetics</topic><topic>Genetic Code</topic><topic>Genome, Mitochondrial</topic><topic>Genomics</topic><topic>Helminth Proteins - genetics</topic><topic>Helminths - genetics</topic><topic>Inverted Repeat Sequences - genetics</topic><topic>Male</topic><topic>Oxygen Consumption</topic><topic>RNA, Helminth - genetics</topic><topic>RNA, Ribosomal, 18S - genetics</topic><topic>Selection, Genetic</topic><topic>Sequence Alignment</topic><topic>Sequence Homology, Amino Acid</topic><topic>Species Specificity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mikhailov, Kirill V</creatorcontrib><creatorcontrib>Efeykin, Boris D</creatorcontrib><creatorcontrib>Panchin, Alexander Y</creatorcontrib><creatorcontrib>Knorre, Dmitry A</creatorcontrib><creatorcontrib>Logacheva, Maria D</creatorcontrib><creatorcontrib>Penin, Aleksey A</creatorcontrib><creatorcontrib>Muntyan, Maria S</creatorcontrib><creatorcontrib>Nikitin, Mikhail A</creatorcontrib><creatorcontrib>Popova, Olga V</creatorcontrib><creatorcontrib>Zanegina, Olga N</creatorcontrib><creatorcontrib>Vyssokikh, Mikhail Y</creatorcontrib><creatorcontrib>Spiridonov, Sergei E</creatorcontrib><creatorcontrib>Aleoshin, Vladimir V</creatorcontrib><creatorcontrib>Panchin, Yuri V</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nucleic acids research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mikhailov, Kirill V</au><au>Efeykin, Boris D</au><au>Panchin, Alexander Y</au><au>Knorre, Dmitry A</au><au>Logacheva, Maria D</au><au>Penin, Aleksey A</au><au>Muntyan, Maria S</au><au>Nikitin, Mikhail A</au><au>Popova, Olga V</au><au>Zanegina, Olga N</au><au>Vyssokikh, Mikhail Y</au><au>Spiridonov, Sergei E</au><au>Aleoshin, Vladimir V</au><au>Panchin, Yuri V</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Coding palindromes in mitochondrial genes of Nematomorpha</atitle><jtitle>Nucleic acids research</jtitle><addtitle>Nucleic Acids Res</addtitle><date>2019-07-26</date><risdate>2019</risdate><volume>47</volume><issue>13</issue><spage>6858</spage><epage>6870</epage><pages>6858-6870</pages><issn>0305-1048</issn><eissn>1362-4962</eissn><abstract>Inverted repeats are common DNA elements, but they rarely overlap with protein-coding sequences due to the ensuing conflict with the structure and function of the encoded protein. We discovered numerous perfect inverted repeats of considerable length (up to 284 bp) embedded within the protein-coding genes in mitochondrial genomes of four Nematomorpha species. Strikingly, both arms of the inverted repeats encode conserved regions of the amino acid sequence. We confirmed enzymatic activity of the respiratory complex I encoded by inverted repeat-containing genes. The nucleotide composition of inverted repeats suggests strong selection at the amino acid level in these regions. We conclude that the inverted repeat-containing genes are transcribed and translated into functional proteins. The survey of available mitochondrial genomes reveals that several other organisms possess similar albeit shorter embedded repeats. Mitochondrial genomes of Nematomorpha demonstrate an extraordinary evolutionary compromise where protein function and stringent secondary structure elements within the coding regions are preserved simultaneously.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>31194871</pmid><doi>10.1093/nar/gkz517</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-0457-9625</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Amino Acid Sequence Animals Base Composition Base Sequence DNA, Helminth - genetics DNA, Ribosomal - genetics Electron Transport Complex I - genetics Evolution, Molecular Female Genes, Helminth - genetics Genes, Mitochondrial - genetics Genetic Code Genome, Mitochondrial Genomics Helminth Proteins - genetics Helminths - genetics Inverted Repeat Sequences - genetics Male Oxygen Consumption RNA, Helminth - genetics RNA, Ribosomal, 18S - genetics Selection, Genetic Sequence Alignment Sequence Homology, Amino Acid Species Specificity |
title | Coding palindromes in mitochondrial genes of Nematomorpha |
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