A vast pool of lineage-specific microproteins encoded by long non-coding RNAs in plants
Pervasive transcription of eukaryotic genomes results in expression of long non-coding RNAs (lncRNAs) most of which are poorly conserved in evolution and appear to be non-functional. However, some lncRNAs have been shown to perform specific functions, in particular, transcription regulation. Thousan...
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| Veröffentlicht in: | Nucleic acids research 2021-10, Vol.49 (18), p.10328-10346 |
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| creator | Fesenko, Igor Shabalina, Svetlana A Mamaeva, Anna Knyazev, Andrey Glushkevich, Anna Lyapina, Irina Ziganshin, Rustam Kovalchuk, Sergey Kharlampieva, Daria Lazarev, Vassili Taliansky, Michael Koonin, Eugene V |
| description | Pervasive transcription of eukaryotic genomes results in expression of long non-coding RNAs (lncRNAs) most of which are poorly conserved in evolution and appear to be non-functional. However, some lncRNAs have been shown to perform specific functions, in particular, transcription regulation. Thousands of small open reading frames (smORFs, |
| doi_str_mv | 10.1093/nar/gkab816 |
| format | Article |
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However, some lncRNAs have been shown to perform specific functions, in particular, transcription regulation. Thousands of small open reading frames (smORFs, <100 codons) located on lncRNAs potentially might be translated into peptides or microproteins. We report a comprehensive analysis of the conservation and evolutionary trajectories of lncRNAs-smORFs from the moss Physcomitrium patens across transcriptomes of 479 plant species. Although thousands of smORFs are subject to substantial purifying selection, the majority of the smORFs appear to be evolutionary young and could represent a major pool for functional innovation. Using nanopore RNA sequencing, we show that, on average, the transcriptional level of conserved smORFs is higher than that of non-conserved smORFs. Proteomic analysis confirmed translation of 82 novel species-specific smORFs. Numerous conserved smORFs containing low complexity regions (LCRs) or transmembrane domains were identified, the biological functions of a selected LCR-smORF were demonstrated experimentally. Thus, microproteins encoded by smORFs are a major, functionally diverse component of the plant proteome.</description><identifier>ISSN: 0305-1048</identifier><identifier>EISSN: 1362-4962</identifier><identifier>DOI: 10.1093/nar/gkab816</identifier><identifier>PMID: 34570232</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Bryopsida - genetics ; Computational Biology ; Open Reading Frames ; Proteome ; RNA, Long Noncoding ; Transcriptome</subject><ispartof>Nucleic acids research, 2021-10, Vol.49 (18), p.10328-10346</ispartof><rights>Published by Oxford University Press on behalf of Nucleic Acids Research 2021.</rights><rights>Published by Oxford University Press on behalf of Nucleic Acids Research 2021. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c381t-4029e8e97aa81f52ce6bed7d3db7db5dc86607c5e6ac0f962b685c32992f1d3b3</citedby><cites>FETCH-LOGICAL-c381t-4029e8e97aa81f52ce6bed7d3db7db5dc86607c5e6ac0f962b685c32992f1d3b3</cites><orcidid>0000-0002-5757-8271 ; 0000-0003-3943-8299 ; 0000-0002-3774-819X</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/PMC8501992/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8501992/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34570232$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Fesenko, Igor</creatorcontrib><creatorcontrib>Shabalina, Svetlana A</creatorcontrib><creatorcontrib>Mamaeva, Anna</creatorcontrib><creatorcontrib>Knyazev, Andrey</creatorcontrib><creatorcontrib>Glushkevich, Anna</creatorcontrib><creatorcontrib>Lyapina, Irina</creatorcontrib><creatorcontrib>Ziganshin, Rustam</creatorcontrib><creatorcontrib>Kovalchuk, Sergey</creatorcontrib><creatorcontrib>Kharlampieva, Daria</creatorcontrib><creatorcontrib>Lazarev, Vassili</creatorcontrib><creatorcontrib>Taliansky, Michael</creatorcontrib><creatorcontrib>Koonin, Eugene V</creatorcontrib><title>A vast pool of lineage-specific microproteins encoded by long non-coding RNAs in plants</title><title>Nucleic acids research</title><addtitle>Nucleic Acids Res</addtitle><description>Pervasive transcription of eukaryotic genomes results in expression of long non-coding RNAs (lncRNAs) most of which are poorly conserved in evolution and appear to be non-functional. However, some lncRNAs have been shown to perform specific functions, in particular, transcription regulation. Thousands of small open reading frames (smORFs, <100 codons) located on lncRNAs potentially might be translated into peptides or microproteins. We report a comprehensive analysis of the conservation and evolutionary trajectories of lncRNAs-smORFs from the moss Physcomitrium patens across transcriptomes of 479 plant species. Although thousands of smORFs are subject to substantial purifying selection, the majority of the smORFs appear to be evolutionary young and could represent a major pool for functional innovation. Using nanopore RNA sequencing, we show that, on average, the transcriptional level of conserved smORFs is higher than that of non-conserved smORFs. Proteomic analysis confirmed translation of 82 novel species-specific smORFs. Numerous conserved smORFs containing low complexity regions (LCRs) or transmembrane domains were identified, the biological functions of a selected LCR-smORF were demonstrated experimentally. Thus, microproteins encoded by smORFs are a major, functionally diverse component of the plant proteome.</description><subject>Bryopsida - genetics</subject><subject>Computational Biology</subject><subject>Open Reading Frames</subject><subject>Proteome</subject><subject>RNA, Long Noncoding</subject><subject>Transcriptome</subject><issn>0305-1048</issn><issn>1362-4962</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVUU1LxDAQDaK468fJu-QoSDUfTZpehEX8AlEQxWNIk-ka7Sa16Qr-eyO7ip5mmHm8mfceQgeUnFBS89NghtP5m2kUlRtoSrlkRVlLtommhBNRUFKqCdpJ6ZUQWlJRbqMJL0VFGGdT9DzDHyaNuI-xw7HFnQ9g5lCkHqxvvcULb4fYD3EEHxKGYKMDh5tP3MUwxyGGIk98bh_uZgn7gPvOhDHtoa3WdAn213UXPV1ePJ5fF7f3Vzfns9vCckXHoiSsBgV1ZYyirWAWZAOuctw1lWuEs0pKUlkB0ljSZlWNVMJyVtespY43fBedrXj7ZbMAZyGMg-l0P_iFGT51NF7_3wT_oufxQytBaGbJBEdrgiG-LyGNeuGThS6rgLhMmolK1lQIxTP0eAXNjqQ0QPt7hhL9HYXOUeh1FBl9-PezX-yP9_wL66WHwA</recordid><startdate>20211011</startdate><enddate>20211011</enddate><creator>Fesenko, Igor</creator><creator>Shabalina, Svetlana A</creator><creator>Mamaeva, Anna</creator><creator>Knyazev, Andrey</creator><creator>Glushkevich, Anna</creator><creator>Lyapina, Irina</creator><creator>Ziganshin, Rustam</creator><creator>Kovalchuk, Sergey</creator><creator>Kharlampieva, Daria</creator><creator>Lazarev, Vassili</creator><creator>Taliansky, Michael</creator><creator>Koonin, Eugene 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/0000-0002-5757-8271</orcidid><orcidid>https://orcid.org/0000-0003-3943-8299</orcidid><orcidid>https://orcid.org/0000-0002-3774-819X</orcidid></search><sort><creationdate>20211011</creationdate><title>A vast pool of lineage-specific microproteins encoded by long non-coding RNAs in plants</title><author>Fesenko, Igor ; Shabalina, Svetlana A ; Mamaeva, Anna ; Knyazev, Andrey ; Glushkevich, Anna ; Lyapina, Irina ; Ziganshin, Rustam ; Kovalchuk, Sergey ; Kharlampieva, Daria ; Lazarev, Vassili ; Taliansky, Michael ; Koonin, Eugene V</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c381t-4029e8e97aa81f52ce6bed7d3db7db5dc86607c5e6ac0f962b685c32992f1d3b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Bryopsida - genetics</topic><topic>Computational Biology</topic><topic>Open Reading Frames</topic><topic>Proteome</topic><topic>RNA, Long Noncoding</topic><topic>Transcriptome</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Fesenko, Igor</creatorcontrib><creatorcontrib>Shabalina, Svetlana A</creatorcontrib><creatorcontrib>Mamaeva, Anna</creatorcontrib><creatorcontrib>Knyazev, Andrey</creatorcontrib><creatorcontrib>Glushkevich, Anna</creatorcontrib><creatorcontrib>Lyapina, Irina</creatorcontrib><creatorcontrib>Ziganshin, Rustam</creatorcontrib><creatorcontrib>Kovalchuk, Sergey</creatorcontrib><creatorcontrib>Kharlampieva, Daria</creatorcontrib><creatorcontrib>Lazarev, Vassili</creatorcontrib><creatorcontrib>Taliansky, Michael</creatorcontrib><creatorcontrib>Koonin, Eugene 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>Fesenko, Igor</au><au>Shabalina, Svetlana A</au><au>Mamaeva, Anna</au><au>Knyazev, Andrey</au><au>Glushkevich, Anna</au><au>Lyapina, Irina</au><au>Ziganshin, Rustam</au><au>Kovalchuk, Sergey</au><au>Kharlampieva, Daria</au><au>Lazarev, Vassili</au><au>Taliansky, Michael</au><au>Koonin, Eugene V</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A vast pool of lineage-specific microproteins encoded by long non-coding RNAs in plants</atitle><jtitle>Nucleic acids research</jtitle><addtitle>Nucleic Acids Res</addtitle><date>2021-10-11</date><risdate>2021</risdate><volume>49</volume><issue>18</issue><spage>10328</spage><epage>10346</epage><pages>10328-10346</pages><issn>0305-1048</issn><eissn>1362-4962</eissn><abstract>Pervasive transcription of eukaryotic genomes results in expression of long non-coding RNAs (lncRNAs) most of which are poorly conserved in evolution and appear to be non-functional. However, some lncRNAs have been shown to perform specific functions, in particular, transcription regulation. Thousands of small open reading frames (smORFs, <100 codons) located on lncRNAs potentially might be translated into peptides or microproteins. We report a comprehensive analysis of the conservation and evolutionary trajectories of lncRNAs-smORFs from the moss Physcomitrium patens across transcriptomes of 479 plant species. Although thousands of smORFs are subject to substantial purifying selection, the majority of the smORFs appear to be evolutionary young and could represent a major pool for functional innovation. Using nanopore RNA sequencing, we show that, on average, the transcriptional level of conserved smORFs is higher than that of non-conserved smORFs. Proteomic analysis confirmed translation of 82 novel species-specific smORFs. 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| subjects | Bryopsida - genetics Computational Biology Open Reading Frames Proteome RNA, Long Noncoding Transcriptome |
| title | A vast pool of lineage-specific microproteins encoded by long non-coding RNAs in plants |
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