snRNA 3' End Processing by a CPSF73-Containing Complex Essential for Development in Arabidopsis
Uridine-rich small nuclear RNAs (snRNAs) are the basal components of the spliceosome and play essential roles in splicing. The biogenesis of the majority of snRNAs involves 3' end endonucleolytic cleavage of the nascent transcript from the elongating DNA-dependent RNA ploymerase II. However, th...
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| description | Uridine-rich small nuclear RNAs (snRNAs) are the basal components of the spliceosome and play essential roles in splicing. The biogenesis of the majority of snRNAs involves 3' end endonucleolytic cleavage of the nascent transcript from the elongating DNA-dependent RNA ploymerase II. However, the protein factors responsible for this process remain elusive in plants. Here, we show that DEFECTIVE in snRNA PROCESSING 1 (DSP1) is an essential protein for snRNA 3' end maturation in Arabidopsis. A hypomorphic dsp1-1 mutation causes pleiotropic developmental defects, impairs the 3' end processing of snRNAs, increases the levels of snRNA primary transcripts (pre-snRNAs), and alters the occupancy of Pol II at snRNA loci. In addition, DSP1 binds snRNA loci and interacts with Pol-II in a DNA/RNA-dependent manner. We further show that DSP1 forms a conserved complex, which contains at least four additional proteins, to catalyze snRNA 3' end maturation in Arabidopsis. The catalytic component of this complex is likely the cleavage and polyadenylation specificity factor 73 kDa-I (CSPF73-I), which is the nuclease cleaving the pre-mRNA 3' end. However, the DSP1 complex does not affect pre-mRNA 3' end cleavage, suggesting that plants may use different CPSF73-I-containing complexes to process snRNAs and pre-mRNAs. This study identifies a complex responsible for the snRNA 3' end maturation in plants and uncovers a previously unknown function of CPSF73 in snRNA maturation. |
| doi_str_mv | 10.1371/journal.pbio.1002571 |
| format | Article |
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The biogenesis of the majority of snRNAs involves 3' end endonucleolytic cleavage of the nascent transcript from the elongating DNA-dependent RNA ploymerase II. However, the protein factors responsible for this process remain elusive in plants. Here, we show that DEFECTIVE in snRNA PROCESSING 1 (DSP1) is an essential protein for snRNA 3' end maturation in Arabidopsis. A hypomorphic dsp1-1 mutation causes pleiotropic developmental defects, impairs the 3' end processing of snRNAs, increases the levels of snRNA primary transcripts (pre-snRNAs), and alters the occupancy of Pol II at snRNA loci. In addition, DSP1 binds snRNA loci and interacts with Pol-II in a DNA/RNA-dependent manner. We further show that DSP1 forms a conserved complex, which contains at least four additional proteins, to catalyze snRNA 3' end maturation in Arabidopsis. The catalytic component of this complex is likely the cleavage and polyadenylation specificity factor 73 kDa-I (CSPF73-I), which is the nuclease cleaving the pre-mRNA 3' end. However, the DSP1 complex does not affect pre-mRNA 3' end cleavage, suggesting that plants may use different CPSF73-I-containing complexes to process snRNAs and pre-mRNAs. This study identifies a complex responsible for the snRNA 3' end maturation in plants and uncovers a previously unknown function of CPSF73 in snRNA maturation.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.1002571</identifier><identifier>PMID: 27780203</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Biology and Life Sciences ; Cleavage And Polyadenylation Specificity Factor - metabolism ; Colleges & universities ; Deoxyribonucleic acid ; Development ; DNA ; Gene expression ; Genes, Plant ; Genetic aspects ; Methods ; Mutation ; Plant sciences ; Plants ; Pollen ; Proteins ; Research and Analysis Methods ; RNA Processing, Post-Transcriptional ; RNA sequencing ; RNA, Small Nuclear - genetics ; RNA, Small Nuclear - metabolism</subject><ispartof>PLoS biology, 2016-10, Vol.14 (10), p.e1002571-e1002571</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Biol 14(10): e1002571. doi:10.1371/journal.pbio.1002571</rights><rights>2016 Liu et al 2016 Liu et al</rights><rights>2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Biol 14(10): e1002571. doi:10.1371/journal.pbio.1002571</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c728t-10a180f10eb45f6b6df637d5ae758a3c5477903bb517ec5162ec734300edf55d3</citedby><cites>FETCH-LOGICAL-c728t-10a180f10eb45f6b6df637d5ae758a3c5477903bb517ec5162ec734300edf55d3</cites><orcidid>0000-0002-4166-9056</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/PMC5079582/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5079582/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27780203$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Yunfeng</creatorcontrib><creatorcontrib>Li, Shengjun</creatorcontrib><creatorcontrib>Chen, Yuan</creatorcontrib><creatorcontrib>Kimberlin, Athen N</creatorcontrib><creatorcontrib>Cahoon, Edgar B</creatorcontrib><creatorcontrib>Yu, Bin</creatorcontrib><title>snRNA 3' End Processing by a CPSF73-Containing Complex Essential for Development in Arabidopsis</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><description>Uridine-rich small nuclear RNAs (snRNAs) are the basal components of the spliceosome and play essential roles in splicing. The biogenesis of the majority of snRNAs involves 3' end endonucleolytic cleavage of the nascent transcript from the elongating DNA-dependent RNA ploymerase II. However, the protein factors responsible for this process remain elusive in plants. Here, we show that DEFECTIVE in snRNA PROCESSING 1 (DSP1) is an essential protein for snRNA 3' end maturation in Arabidopsis. A hypomorphic dsp1-1 mutation causes pleiotropic developmental defects, impairs the 3' end processing of snRNAs, increases the levels of snRNA primary transcripts (pre-snRNAs), and alters the occupancy of Pol II at snRNA loci. In addition, DSP1 binds snRNA loci and interacts with Pol-II in a DNA/RNA-dependent manner. We further show that DSP1 forms a conserved complex, which contains at least four additional proteins, to catalyze snRNA 3' end maturation in Arabidopsis. The catalytic component of this complex is likely the cleavage and polyadenylation specificity factor 73 kDa-I (CSPF73-I), which is the nuclease cleaving the pre-mRNA 3' end. However, the DSP1 complex does not affect pre-mRNA 3' end cleavage, suggesting that plants may use different CPSF73-I-containing complexes to process snRNAs and pre-mRNAs. This study identifies a complex responsible for the snRNA 3' end maturation in plants and uncovers a previously unknown function of CPSF73 in snRNA maturation.</description><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Biology and Life Sciences</subject><subject>Cleavage And Polyadenylation Specificity Factor - metabolism</subject><subject>Colleges & universities</subject><subject>Deoxyribonucleic acid</subject><subject>Development</subject><subject>DNA</subject><subject>Gene expression</subject><subject>Genes, Plant</subject><subject>Genetic aspects</subject><subject>Methods</subject><subject>Mutation</subject><subject>Plant sciences</subject><subject>Plants</subject><subject>Pollen</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>RNA Processing, Post-Transcriptional</subject><subject>RNA sequencing</subject><subject>RNA, Small Nuclear - 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genetics</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>Biology and Life Sciences</topic><topic>Cleavage And Polyadenylation Specificity Factor - metabolism</topic><topic>Colleges & universities</topic><topic>Deoxyribonucleic acid</topic><topic>Development</topic><topic>DNA</topic><topic>Gene expression</topic><topic>Genes, Plant</topic><topic>Genetic aspects</topic><topic>Methods</topic><topic>Mutation</topic><topic>Plant sciences</topic><topic>Plants</topic><topic>Pollen</topic><topic>Proteins</topic><topic>Research and Analysis Methods</topic><topic>RNA Processing, Post-Transcriptional</topic><topic>RNA sequencing</topic><topic>RNA, Small Nuclear - genetics</topic><topic>RNA, Small Nuclear - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Yunfeng</creatorcontrib><creatorcontrib>Li, Shengjun</creatorcontrib><creatorcontrib>Chen, Yuan</creatorcontrib><creatorcontrib>Kimberlin, Athen N</creatorcontrib><creatorcontrib>Cahoon, Edgar B</creatorcontrib><creatorcontrib>Yu, Bin</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Opposing Viewpoints in Context (Gale)</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><collection>PLoS Biology</collection><jtitle>PLoS biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Yunfeng</au><au>Li, Shengjun</au><au>Chen, Yuan</au><au>Kimberlin, Athen N</au><au>Cahoon, Edgar B</au><au>Yu, Bin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>snRNA 3' End Processing by a CPSF73-Containing Complex Essential for Development in Arabidopsis</atitle><jtitle>PLoS biology</jtitle><addtitle>PLoS Biol</addtitle><date>2016-10-25</date><risdate>2016</risdate><volume>14</volume><issue>10</issue><spage>e1002571</spage><epage>e1002571</epage><pages>e1002571-e1002571</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><abstract>Uridine-rich small nuclear RNAs (snRNAs) are the basal components of the spliceosome and play essential roles in splicing. The biogenesis of the majority of snRNAs involves 3' end endonucleolytic cleavage of the nascent transcript from the elongating DNA-dependent RNA ploymerase II. However, the protein factors responsible for this process remain elusive in plants. Here, we show that DEFECTIVE in snRNA PROCESSING 1 (DSP1) is an essential protein for snRNA 3' end maturation in Arabidopsis. A hypomorphic dsp1-1 mutation causes pleiotropic developmental defects, impairs the 3' end processing of snRNAs, increases the levels of snRNA primary transcripts (pre-snRNAs), and alters the occupancy of Pol II at snRNA loci. In addition, DSP1 binds snRNA loci and interacts with Pol-II in a DNA/RNA-dependent manner. We further show that DSP1 forms a conserved complex, which contains at least four additional proteins, to catalyze snRNA 3' end maturation in Arabidopsis. The catalytic component of this complex is likely the cleavage and polyadenylation specificity factor 73 kDa-I (CSPF73-I), which is the nuclease cleaving the pre-mRNA 3' end. However, the DSP1 complex does not affect pre-mRNA 3' end cleavage, suggesting that plants may use different CPSF73-I-containing complexes to process snRNAs and pre-mRNAs. This study identifies a complex responsible for the snRNA 3' end maturation in plants and uncovers a previously unknown function of CPSF73 in snRNA maturation.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27780203</pmid><doi>10.1371/journal.pbio.1002571</doi><orcidid>https://orcid.org/0000-0002-4166-9056</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Arabidopsis Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis Proteins - metabolism Arabidopsis thaliana Biology and Life Sciences Cleavage And Polyadenylation Specificity Factor - metabolism Colleges & universities Deoxyribonucleic acid Development DNA Gene expression Genes, Plant Genetic aspects Methods Mutation Plant sciences Plants Pollen Proteins Research and Analysis Methods RNA Processing, Post-Transcriptional RNA sequencing RNA, Small Nuclear - genetics RNA, Small Nuclear - metabolism |
| title | snRNA 3' End Processing by a CPSF73-Containing Complex Essential for Development in Arabidopsis |
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