The coordinated action of PPR4 and EMB2654 on each intron half mediates trans‐splicing of rps12 transcripts in plant chloroplasts

Summary The pentatricopeptide repeat proteins PPR4 and EMB2654 have been shown to be required for the trans‐splicing of plastid rps12 transcripts in Zea mays (maize) and Arabidopsis, respectively, but their roles in this process are not well understood. We investigated the functions of the Arabidops...

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Veröffentlicht in:The Plant journal : for cell and molecular biology 2019-12, Vol.100 (6), p.1193-1207
Hauptverfasser: Lee, Kwanuk, Park, Su Jung, Colas des Francs‐Small, Catherine, Whitby, Michael, Small, Ian, Kang, Hunseung
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container_title The Plant journal : for cell and molecular biology
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creator Lee, Kwanuk
Park, Su Jung
Colas des Francs‐Small, Catherine
Whitby, Michael
Small, Ian
Kang, Hunseung
description Summary The pentatricopeptide repeat proteins PPR4 and EMB2654 have been shown to be required for the trans‐splicing of plastid rps12 transcripts in Zea mays (maize) and Arabidopsis, respectively, but their roles in this process are not well understood. We investigated the functions of the Arabidopsis and Oryza sativa (rice) orthologs of PPR4, designated AtPPR4 (At5g04810) and OsPPR4 (Os4g58780). Arabidopsis atppr4 and rice osppr4 mutants are embryo‐lethal and seedling‐lethal 3 weeks after germination, respectively, showing that PPR4 is essential in the development of both dicot and monocot plants. Artificial microRNA‐mediated mutants of AtPPR4 displayed a specific defect in rps12 trans‐splicing, with pale‐green, yellowish or albino phenotypes, according to the degree of knock‐down of AtPPR4 expression. Comparison of RNA footprints in atppr4 and emb2654 mutants showed a similar concordant loss of extensive footprints at the 3′ end of intron 1a and at the 5′ end of intron 1b in both cases. EMB2654 is known to bind within the footprint region in intron 1a and we show that AtPPR4 binds to the footprint region in intron 1b, via its PPR motifs. Binding of both PPR4 and EMB2654 is essential to juxtapose the two intron halves and to maintain the RNAs in a splicing‐competent structure for the efficient trans‐splicing of rps12 intron 1, which is crucial for chloroplast biogenesis and plant development. The similarity of EMB2654 and PPR4 orthologs and their respective binding sites across land plant phylogeny indicates that their coordinate function in rps12 trans‐splicing has probably been conserved for 500 million years. Significance Statement Despite the crucial role of pentatricopeptide repeat (PPR) proteins in organellar RNA metabolism and plant development, the functions of many PPR proteins remain unknown. Here, we show that the PPR4 and EMB2654 bind to the 5′ end of rps12 intron 1b and the 3′ end of rps12 intron 1a to juxtapose the two intron halves for the efficient trans‐splicing of rps12 intron 1, which is essential for chloroplast biogenesis and plant development.
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We investigated the functions of the Arabidopsis and Oryza sativa (rice) orthologs of PPR4, designated AtPPR4 (At5g04810) and OsPPR4 (Os4g58780). Arabidopsis atppr4 and rice osppr4 mutants are embryo‐lethal and seedling‐lethal 3 weeks after germination, respectively, showing that PPR4 is essential in the development of both dicot and monocot plants. Artificial microRNA‐mediated mutants of AtPPR4 displayed a specific defect in rps12 trans‐splicing, with pale‐green, yellowish or albino phenotypes, according to the degree of knock‐down of AtPPR4 expression. Comparison of RNA footprints in atppr4 and emb2654 mutants showed a similar concordant loss of extensive footprints at the 3′ end of intron 1a and at the 5′ end of intron 1b in both cases. EMB2654 is known to bind within the footprint region in intron 1a and we show that AtPPR4 binds to the footprint region in intron 1b, via its PPR motifs. Binding of both PPR4 and EMB2654 is essential to juxtapose the two intron halves and to maintain the RNAs in a splicing‐competent structure for the efficient trans‐splicing of rps12 intron 1, which is crucial for chloroplast biogenesis and plant development. The similarity of EMB2654 and PPR4 orthologs and their respective binding sites across land plant phylogeny indicates that their coordinate function in rps12 trans‐splicing has probably been conserved for 500 million years. Significance Statement Despite the crucial role of pentatricopeptide repeat (PPR) proteins in organellar RNA metabolism and plant development, the functions of many PPR proteins remain unknown. Here, we show that the PPR4 and EMB2654 bind to the 5′ end of rps12 intron 1b and the 3′ end of rps12 intron 1a to juxtapose the two intron halves for the efficient trans‐splicing of rps12 intron 1, which is essential for chloroplast biogenesis and plant development.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.14509</identifier><identifier>PMID: 31442349</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Arabidopsis ; Arabidopsis thaliana ; Binding sites ; chloroplast ; Chloroplasts ; Corn ; Embryos ; Footprints ; Gene expression ; Germination ; intron splicing ; miRNA ; Mutants ; Oryza sativa ; pentatricopeptide repeat ; Phenotypes ; Phylogeny ; Ribonucleic acid ; Rice ; RNA ; RNA metabolism ; Seedlings ; Splicing ; Zea mays</subject><ispartof>The Plant journal : for cell and molecular biology, 2019-12, Vol.100 (6), p.1193-1207</ispartof><rights>2019 The Authors The Plant Journal © 2019 John Wiley &amp; Sons Ltd</rights><rights>2019 The Authors The Plant Journal © 2019 John Wiley &amp; Sons Ltd.</rights><rights>Copyright © 2019 John Wiley &amp; Sons Ltd and the Society for Experimental Biology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><orcidid>0000-0001-5300-1216 ; 0000-0002-3532-7690</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Ftpj.14509$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.14509$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,778,782,1414,1430,27911,27912,45561,45562,46396,46820</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31442349$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lee, Kwanuk</creatorcontrib><creatorcontrib>Park, Su Jung</creatorcontrib><creatorcontrib>Colas des Francs‐Small, Catherine</creatorcontrib><creatorcontrib>Whitby, Michael</creatorcontrib><creatorcontrib>Small, Ian</creatorcontrib><creatorcontrib>Kang, Hunseung</creatorcontrib><title>The coordinated action of PPR4 and EMB2654 on each intron half mediates trans‐splicing of rps12 transcripts in plant chloroplasts</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>Summary The pentatricopeptide repeat proteins PPR4 and EMB2654 have been shown to be required for the trans‐splicing of plastid rps12 transcripts in Zea mays (maize) and Arabidopsis, respectively, but their roles in this process are not well understood. We investigated the functions of the Arabidopsis and Oryza sativa (rice) orthologs of PPR4, designated AtPPR4 (At5g04810) and OsPPR4 (Os4g58780). Arabidopsis atppr4 and rice osppr4 mutants are embryo‐lethal and seedling‐lethal 3 weeks after germination, respectively, showing that PPR4 is essential in the development of both dicot and monocot plants. Artificial microRNA‐mediated mutants of AtPPR4 displayed a specific defect in rps12 trans‐splicing, with pale‐green, yellowish or albino phenotypes, according to the degree of knock‐down of AtPPR4 expression. Comparison of RNA footprints in atppr4 and emb2654 mutants showed a similar concordant loss of extensive footprints at the 3′ end of intron 1a and at the 5′ end of intron 1b in both cases. EMB2654 is known to bind within the footprint region in intron 1a and we show that AtPPR4 binds to the footprint region in intron 1b, via its PPR motifs. 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Here, we show that the PPR4 and EMB2654 bind to the 5′ end of rps12 intron 1b and the 3′ end of rps12 intron 1a to juxtapose the two intron halves for the efficient trans‐splicing of rps12 intron 1, which is essential for chloroplast biogenesis and plant development.</description><subject>Arabidopsis</subject><subject>Arabidopsis thaliana</subject><subject>Binding sites</subject><subject>chloroplast</subject><subject>Chloroplasts</subject><subject>Corn</subject><subject>Embryos</subject><subject>Footprints</subject><subject>Gene expression</subject><subject>Germination</subject><subject>intron splicing</subject><subject>miRNA</subject><subject>Mutants</subject><subject>Oryza sativa</subject><subject>pentatricopeptide repeat</subject><subject>Phenotypes</subject><subject>Phylogeny</subject><subject>Ribonucleic acid</subject><subject>Rice</subject><subject>RNA</subject><subject>RNA metabolism</subject><subject>Seedlings</subject><subject>Splicing</subject><subject>Zea mays</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNo9UctOwzAQtBCIlsKBH0CWOKf1K3ZyhKq8VESFisQtcmKHuEqTYLtCvSHxA3wjX4L7gL3saHd2VrsDwDlGQxxi5LvFELMYpQegjymPI4rp6yHoo5SjSDBMeuDEuQVCWFDOjkGPYsYIZWkffM0rDYu2tco00msFZeFN28C2hLPZM4OyUXDyeE14zGAoa1lU0DTeBlzJuoRLrUyYc9Bb2bifz2_X1aYwzdtGwXYOk12nsKbzLozCrpaNh0VVt7YN2Hl3Co5KWTt9ts8D8HIzmY_vounT7f34ahotKIvTKM5ZmWtNhOaYJ0gIoRVCZS6kVISVKCWaqwShQknNWZLyQmJaChUzGctcJXQALne6nW3fV9r5bNGubBNWZoQSLnCMcBpYF3vWKg_XZZ01S2nX2d_PAmG0I3yYWq__-xhlGzOyYEa2NSObzx62gP4CkMx9aQ</recordid><startdate>201912</startdate><enddate>201912</enddate><creator>Lee, Kwanuk</creator><creator>Park, Su Jung</creator><creator>Colas des Francs‐Small, Catherine</creator><creator>Whitby, Michael</creator><creator>Small, Ian</creator><creator>Kang, Hunseung</creator><general>Blackwell Publishing Ltd</general><scope>NPM</scope><scope>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><orcidid>https://orcid.org/0000-0001-5300-1216</orcidid><orcidid>https://orcid.org/0000-0002-3532-7690</orcidid></search><sort><creationdate>201912</creationdate><title>The coordinated action of PPR4 and EMB2654 on each intron half mediates trans‐splicing of rps12 transcripts in plant chloroplasts</title><author>Lee, Kwanuk ; Park, Su Jung ; Colas des Francs‐Small, Catherine ; Whitby, Michael ; Small, Ian ; Kang, Hunseung</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-j3459-5b4fbee27e61680777ed00fb7aad24f092e6d800cdae64896ca13f7d54a5abd83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis thaliana</topic><topic>Binding sites</topic><topic>chloroplast</topic><topic>Chloroplasts</topic><topic>Corn</topic><topic>Embryos</topic><topic>Footprints</topic><topic>Gene expression</topic><topic>Germination</topic><topic>intron splicing</topic><topic>miRNA</topic><topic>Mutants</topic><topic>Oryza sativa</topic><topic>pentatricopeptide repeat</topic><topic>Phenotypes</topic><topic>Phylogeny</topic><topic>Ribonucleic acid</topic><topic>Rice</topic><topic>RNA</topic><topic>RNA metabolism</topic><topic>Seedlings</topic><topic>Splicing</topic><topic>Zea mays</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lee, Kwanuk</creatorcontrib><creatorcontrib>Park, Su Jung</creatorcontrib><creatorcontrib>Colas des Francs‐Small, Catherine</creatorcontrib><creatorcontrib>Whitby, Michael</creatorcontrib><creatorcontrib>Small, Ian</creatorcontrib><creatorcontrib>Kang, Hunseung</creatorcontrib><collection>PubMed</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lee, Kwanuk</au><au>Park, Su Jung</au><au>Colas des Francs‐Small, Catherine</au><au>Whitby, Michael</au><au>Small, Ian</au><au>Kang, Hunseung</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The coordinated action of PPR4 and EMB2654 on each intron half mediates trans‐splicing of rps12 transcripts in plant chloroplasts</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2019-12</date><risdate>2019</risdate><volume>100</volume><issue>6</issue><spage>1193</spage><epage>1207</epage><pages>1193-1207</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>Summary The pentatricopeptide repeat proteins PPR4 and EMB2654 have been shown to be required for the trans‐splicing of plastid rps12 transcripts in Zea mays (maize) and Arabidopsis, respectively, but their roles in this process are not well understood. We investigated the functions of the Arabidopsis and Oryza sativa (rice) orthologs of PPR4, designated AtPPR4 (At5g04810) and OsPPR4 (Os4g58780). Arabidopsis atppr4 and rice osppr4 mutants are embryo‐lethal and seedling‐lethal 3 weeks after germination, respectively, showing that PPR4 is essential in the development of both dicot and monocot plants. Artificial microRNA‐mediated mutants of AtPPR4 displayed a specific defect in rps12 trans‐splicing, with pale‐green, yellowish or albino phenotypes, according to the degree of knock‐down of AtPPR4 expression. Comparison of RNA footprints in atppr4 and emb2654 mutants showed a similar concordant loss of extensive footprints at the 3′ end of intron 1a and at the 5′ end of intron 1b in both cases. EMB2654 is known to bind within the footprint region in intron 1a and we show that AtPPR4 binds to the footprint region in intron 1b, via its PPR motifs. Binding of both PPR4 and EMB2654 is essential to juxtapose the two intron halves and to maintain the RNAs in a splicing‐competent structure for the efficient trans‐splicing of rps12 intron 1, which is crucial for chloroplast biogenesis and plant development. The similarity of EMB2654 and PPR4 orthologs and their respective binding sites across land plant phylogeny indicates that their coordinate function in rps12 trans‐splicing has probably been conserved for 500 million years. Significance Statement Despite the crucial role of pentatricopeptide repeat (PPR) proteins in organellar RNA metabolism and plant development, the functions of many PPR proteins remain unknown. Here, we show that the PPR4 and EMB2654 bind to the 5′ end of rps12 intron 1b and the 3′ end of rps12 intron 1a to juxtapose the two intron halves for the efficient trans‐splicing of rps12 intron 1, which is essential for chloroplast biogenesis and plant development.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>31442349</pmid><doi>10.1111/tpj.14509</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0001-5300-1216</orcidid><orcidid>https://orcid.org/0000-0002-3532-7690</orcidid><oa>free_for_read</oa></addata></record>
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subjects Arabidopsis
Arabidopsis thaliana
Binding sites
chloroplast
Chloroplasts
Corn
Embryos
Footprints
Gene expression
Germination
intron splicing
miRNA
Mutants
Oryza sativa
pentatricopeptide repeat
Phenotypes
Phylogeny
Ribonucleic acid
Rice
RNA
RNA metabolism
Seedlings
Splicing
Zea mays
title The coordinated action of PPR4 and EMB2654 on each intron half mediates trans‐splicing of rps12 transcripts in plant chloroplasts
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