The DYW-subgroup pentatricopeptide repeat protein PPR27 interacts with ZmMORF1 to facilitate mitochondrial RNA editing and seed development in maize

The PPR-DYW protein PPR27 interacts with ZmMORF1 to facilitate C-to-U editing of ccmFN-1357, which is essential for mitochondrial complex III assembly and seed development in maize. Abstract C-to-U RNA editing in plant mitochondria requires the participation of many nucleus-encoded factors, most of...

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Veröffentlicht in:Journal of experimental botany 2020-09, Vol.71 (18), p.5495-5505
Hauptverfasser: Liu, Rui, Cao, Shi-Kai, Sayyed, Aqib, Yang, Huan-Huan, Zhao, Jiao, Wang, Xiaomin, Jia, Ru-Xue, Sun, Feng, Tan, Bao-Cai
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container_issue 18
container_start_page 5495
container_title Journal of experimental botany
container_volume 71
creator Liu, Rui
Cao, Shi-Kai
Sayyed, Aqib
Yang, Huan-Huan
Zhao, Jiao
Wang, Xiaomin
Jia, Ru-Xue
Sun, Feng
Tan, Bao-Cai
description The PPR-DYW protein PPR27 interacts with ZmMORF1 to facilitate C-to-U editing of ccmFN-1357, which is essential for mitochondrial complex III assembly and seed development in maize. Abstract C-to-U RNA editing in plant mitochondria requires the participation of many nucleus-encoded factors, most of which are pentatricopeptide repeat (PPR) proteins. There is a large number of PPR proteins and the functions many of them are unknown. Here, we report a mitochondrion-localized DYW-subgroup PPR protein, PPR27, which functions in the editing of multiple mitochondrial transcripts in maize. The ppr27 mutant is completely deficient in C-to-U editing at the ccmFN-1357 and rps3-707 sites, and editing at six other sites is substantially reduced. The lack of editing at ccmFN-1357 causes a deficiency of CcmFN protein. As CcmFN functions in the maturation pathway of cytochrome proteins that are subunits of mitochondrial complex III, its deficiency results in an absence of cytochrome c1 and cytochrome c proteins. Consequently, the assembly of mitochondrial complex III and super-complex I+III2 is decreased, which impairs the electron transport chain and respiration, leading to arrests in embryogenesis and endosperm development in ppr27. In addition, PPR27 was found to physically interact with ZmMORF1, which interacts with ZmMORF8, suggesting that these three proteins may facilitate C-to-U RNA editing via the formation of a complex in maize mitochondria. This RNA editing is essential for complex III assembly and seed development in maize.
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Abstract C-to-U RNA editing in plant mitochondria requires the participation of many nucleus-encoded factors, most of which are pentatricopeptide repeat (PPR) proteins. There is a large number of PPR proteins and the functions many of them are unknown. Here, we report a mitochondrion-localized DYW-subgroup PPR protein, PPR27, which functions in the editing of multiple mitochondrial transcripts in maize. The ppr27 mutant is completely deficient in C-to-U editing at the ccmFN-1357 and rps3-707 sites, and editing at six other sites is substantially reduced. The lack of editing at ccmFN-1357 causes a deficiency of CcmFN protein. As CcmFN functions in the maturation pathway of cytochrome proteins that are subunits of mitochondrial complex III, its deficiency results in an absence of cytochrome c1 and cytochrome c proteins. Consequently, the assembly of mitochondrial complex III and super-complex I+III2 is decreased, which impairs the electron transport chain and respiration, leading to arrests in embryogenesis and endosperm development in ppr27. In addition, PPR27 was found to physically interact with ZmMORF1, which interacts with ZmMORF8, suggesting that these three proteins may facilitate C-to-U RNA editing via the formation of a complex in maize mitochondria. This RNA editing is essential for complex III assembly and seed development in maize.</description><identifier>ISSN: 0022-0957</identifier><identifier>EISSN: 1460-2431</identifier><identifier>DOI: 10.1093/jxb/eraa273</identifier><identifier>PMID: 32531050</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Mitochondrial Proteins - genetics ; Plant Proteins - genetics ; Plants, Genetically Modified - genetics ; RNA, Mitochondrial - genetics ; Seeds - genetics ; Zea mays - genetics</subject><ispartof>Journal of experimental botany, 2020-09, Vol.71 (18), p.5495-5505</ispartof><rights>The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com 2020</rights><rights>The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. 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Abstract C-to-U RNA editing in plant mitochondria requires the participation of many nucleus-encoded factors, most of which are pentatricopeptide repeat (PPR) proteins. There is a large number of PPR proteins and the functions many of them are unknown. Here, we report a mitochondrion-localized DYW-subgroup PPR protein, PPR27, which functions in the editing of multiple mitochondrial transcripts in maize. The ppr27 mutant is completely deficient in C-to-U editing at the ccmFN-1357 and rps3-707 sites, and editing at six other sites is substantially reduced. The lack of editing at ccmFN-1357 causes a deficiency of CcmFN protein. As CcmFN functions in the maturation pathway of cytochrome proteins that are subunits of mitochondrial complex III, its deficiency results in an absence of cytochrome c1 and cytochrome c proteins. Consequently, the assembly of mitochondrial complex III and super-complex I+III2 is decreased, which impairs the electron transport chain and respiration, leading to arrests in embryogenesis and endosperm development in ppr27. In addition, PPR27 was found to physically interact with ZmMORF1, which interacts with ZmMORF8, suggesting that these three proteins may facilitate C-to-U RNA editing via the formation of a complex in maize mitochondria. This RNA editing is essential for complex III assembly and seed development in maize.</description><subject>Mitochondrial Proteins - genetics</subject><subject>Plant Proteins - genetics</subject><subject>Plants, Genetically Modified - genetics</subject><subject>RNA, Mitochondrial - genetics</subject><subject>Seeds - genetics</subject><subject>Zea mays - genetics</subject><issn>0022-0957</issn><issn>1460-2431</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kU1v1DAQhi0EokvhxB3NCSGhUH_EcXysCgWkQqtVEYJL5DjjrqskDrbD1-_gB2O0C0dOo5EePa9mXkIeM_qCUS1Obr_3JxiN4UrcIRtWN7TitWB3yYZSziuqpToiD1K6pZRKKuV9ciS4FKwsG_Lreofw8tPHKq39TQzrAgvO2eTobVhwyX5AiLigybDEkNHPcHW15Qr8nEuozQm--byDz9O7y-05gxzAGetHXxwIk8_B7sI8RG9G2L4_BRx89vMNmHmAhDjAgF9xDMtUUosTJuN_4kNyz5kx4aPDPCYfzl9dn72pLi5fvz07vaiskCpXTguJvdTcaMOsUdw4y52oqW5lIzTVDtu20chZo5RVTrV1zzm1gyini8aJY_Js7y2nfVkx5W7yyeI4mhnDmjpeM67btta6oM_3qI0hpYiuW6KfTPzRMdr9qaErNXSHGgr95CBe-wmHf-zfvxfg6R4oH_-v6TdRnJKC</recordid><startdate>20200919</startdate><enddate>20200919</enddate><creator>Liu, Rui</creator><creator>Cao, Shi-Kai</creator><creator>Sayyed, Aqib</creator><creator>Yang, Huan-Huan</creator><creator>Zhao, Jiao</creator><creator>Wang, Xiaomin</creator><creator>Jia, Ru-Xue</creator><creator>Sun, Feng</creator><creator>Tan, Bao-Cai</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><orcidid>https://orcid.org/0000-0003-4861-0521</orcidid></search><sort><creationdate>20200919</creationdate><title>The DYW-subgroup pentatricopeptide repeat protein PPR27 interacts with ZmMORF1 to facilitate mitochondrial RNA editing and seed development in maize</title><author>Liu, Rui ; Cao, Shi-Kai ; Sayyed, Aqib ; Yang, Huan-Huan ; Zhao, Jiao ; Wang, Xiaomin ; Jia, Ru-Xue ; Sun, Feng ; Tan, Bao-Cai</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c357t-f935eb592a9a1ca72afc2f34098563909fe8869e21677c7f784b220cd305036f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Mitochondrial Proteins - genetics</topic><topic>Plant Proteins - genetics</topic><topic>Plants, Genetically Modified - genetics</topic><topic>RNA, Mitochondrial - genetics</topic><topic>Seeds - genetics</topic><topic>Zea mays - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Rui</creatorcontrib><creatorcontrib>Cao, Shi-Kai</creatorcontrib><creatorcontrib>Sayyed, Aqib</creatorcontrib><creatorcontrib>Yang, Huan-Huan</creatorcontrib><creatorcontrib>Zhao, Jiao</creatorcontrib><creatorcontrib>Wang, Xiaomin</creatorcontrib><creatorcontrib>Jia, Ru-Xue</creatorcontrib><creatorcontrib>Sun, Feng</creatorcontrib><creatorcontrib>Tan, Bao-Cai</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><jtitle>Journal of experimental botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Rui</au><au>Cao, Shi-Kai</au><au>Sayyed, Aqib</au><au>Yang, Huan-Huan</au><au>Zhao, Jiao</au><au>Wang, Xiaomin</au><au>Jia, Ru-Xue</au><au>Sun, Feng</au><au>Tan, Bao-Cai</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The DYW-subgroup pentatricopeptide repeat protein PPR27 interacts with ZmMORF1 to facilitate mitochondrial RNA editing and seed development in maize</atitle><jtitle>Journal of experimental botany</jtitle><addtitle>J Exp Bot</addtitle><date>2020-09-19</date><risdate>2020</risdate><volume>71</volume><issue>18</issue><spage>5495</spage><epage>5505</epage><pages>5495-5505</pages><issn>0022-0957</issn><eissn>1460-2431</eissn><abstract>The PPR-DYW protein PPR27 interacts with ZmMORF1 to facilitate C-to-U editing of ccmFN-1357, which is essential for mitochondrial complex III assembly and seed development in maize. Abstract C-to-U RNA editing in plant mitochondria requires the participation of many nucleus-encoded factors, most of which are pentatricopeptide repeat (PPR) proteins. There is a large number of PPR proteins and the functions many of them are unknown. Here, we report a mitochondrion-localized DYW-subgroup PPR protein, PPR27, which functions in the editing of multiple mitochondrial transcripts in maize. The ppr27 mutant is completely deficient in C-to-U editing at the ccmFN-1357 and rps3-707 sites, and editing at six other sites is substantially reduced. The lack of editing at ccmFN-1357 causes a deficiency of CcmFN protein. As CcmFN functions in the maturation pathway of cytochrome proteins that are subunits of mitochondrial complex III, its deficiency results in an absence of cytochrome c1 and cytochrome c proteins. 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subjects Mitochondrial Proteins - genetics
Plant Proteins - genetics
Plants, Genetically Modified - genetics
RNA, Mitochondrial - genetics
Seeds - genetics
Zea mays - genetics
title The DYW-subgroup pentatricopeptide repeat protein PPR27 interacts with ZmMORF1 to facilitate mitochondrial RNA editing and seed development in maize
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