WSL5, a pentatricopeptide repeat protein, is essential for chloroplast biogenesis in rice under cold stress

WSL5 is crucial for the splicing of the chloroplast genes rpl2 and rps12 under cold stress, and affects the retrograde signaling from plastids to the nucleus. Abstract Chloroplasts play an essential role in plant growth and development, and cold conditions affect chloroplast development. Although ma...

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Veröffentlicht in:Journal of experimental botany 2018-07, Vol.69 (16), p.3949-3961
Hauptverfasser: Liu, Xi, Lan, Jie, Huang, Yunshuai, Cao, Penghui, Zhou, Chunlei, Ren, Yaken, He, Niqing, Liu, Shijia, Tian, Yunlu, Nguyen, Thanhliem, Jiang, Ling, Wan, Jianmin
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container_end_page 3961
container_issue 16
container_start_page 3949
container_title Journal of experimental botany
container_volume 69
creator Liu, Xi
Lan, Jie
Huang, Yunshuai
Cao, Penghui
Zhou, Chunlei
Ren, Yaken
He, Niqing
Liu, Shijia
Tian, Yunlu
Nguyen, Thanhliem
Jiang, Ling
Wan, Jianmin
description WSL5 is crucial for the splicing of the chloroplast genes rpl2 and rps12 under cold stress, and affects the retrograde signaling from plastids to the nucleus. Abstract Chloroplasts play an essential role in plant growth and development, and cold conditions affect chloroplast development. Although many genes or regulators involved in chloroplast biogenesis and development have been isolated and characterized, many other components affecting chloroplast biogenesis under cold conditions have not been characterized. Here, we report the functional characterization of a white stripe leaf 5 (wsl5) mutant in rice. The mutant develops white-striped leaves during early leaf development and is albinic when planted under cold stress. Genetic and molecular analysis revealed that WSL5 encodes a novel chloroplast-targeted pentatricopeptide repeat protein. RNA sequencing analysis showed that expression of nuclear-encoded photosynthetic genes in the mutant was significantly repressed, and expression of many chloroplast-encoded genes was also significantly changed. Notably, the wsl5 mutation causes defects in editing of rpl2 and atpA, and splicing of rpl2 and rps12. wsl5 was impaired in chloroplast ribosome biogenesis under cold stress. We propose that the WSL5 allele is required for normal chloroplast development in maintaining retrograde signaling from plastids to the nucleus under cold stress.
doi_str_mv 10.1093/jxb/ery214
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Abstract Chloroplasts play an essential role in plant growth and development, and cold conditions affect chloroplast development. Although many genes or regulators involved in chloroplast biogenesis and development have been isolated and characterized, many other components affecting chloroplast biogenesis under cold conditions have not been characterized. Here, we report the functional characterization of a white stripe leaf 5 (wsl5) mutant in rice. The mutant develops white-striped leaves during early leaf development and is albinic when planted under cold stress. Genetic and molecular analysis revealed that WSL5 encodes a novel chloroplast-targeted pentatricopeptide repeat protein. RNA sequencing analysis showed that expression of nuclear-encoded photosynthetic genes in the mutant was significantly repressed, and expression of many chloroplast-encoded genes was also significantly changed. Notably, the wsl5 mutation causes defects in editing of rpl2 and atpA, and splicing of rpl2 and rps12. wsl5 was impaired in chloroplast ribosome biogenesis under cold stress. We propose that the WSL5 allele is required for normal chloroplast development in maintaining retrograde signaling from plastids to the nucleus under cold stress.</description><identifier>ISSN: 0022-0957</identifier><identifier>EISSN: 1460-2431</identifier><identifier>DOI: 10.1093/jxb/ery214</identifier><identifier>PMID: 29893948</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Alleles ; Chloroplasts - metabolism ; Cloning, Molecular ; Cold-Shock Response ; Down-Regulation ; Genes, Plant ; Introns ; Oryza - genetics ; Oryza - metabolism ; Oryza - physiology ; Photosynthesis - genetics ; Plant Proteins - genetics ; Plant Proteins - physiology ; Plastids - genetics ; Research Papers ; RNA Editing ; RNA Splicing ; Signal Transduction ; Stress, Physiological</subject><ispartof>Journal of experimental botany, 2018-07, Vol.69 (16), p.3949-3961</ispartof><rights>The Author(s) 2018. 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Abstract Chloroplasts play an essential role in plant growth and development, and cold conditions affect chloroplast development. Although many genes or regulators involved in chloroplast biogenesis and development have been isolated and characterized, many other components affecting chloroplast biogenesis under cold conditions have not been characterized. Here, we report the functional characterization of a white stripe leaf 5 (wsl5) mutant in rice. The mutant develops white-striped leaves during early leaf development and is albinic when planted under cold stress. Genetic and molecular analysis revealed that WSL5 encodes a novel chloroplast-targeted pentatricopeptide repeat protein. RNA sequencing analysis showed that expression of nuclear-encoded photosynthetic genes in the mutant was significantly repressed, and expression of many chloroplast-encoded genes was also significantly changed. Notably, the wsl5 mutation causes defects in editing of rpl2 and atpA, and splicing of rpl2 and rps12. wsl5 was impaired in chloroplast ribosome biogenesis under cold stress. We propose that the WSL5 allele is required for normal chloroplast development in maintaining retrograde signaling from plastids to the nucleus under cold stress.</description><subject>Alleles</subject><subject>Chloroplasts - metabolism</subject><subject>Cloning, Molecular</subject><subject>Cold-Shock Response</subject><subject>Down-Regulation</subject><subject>Genes, Plant</subject><subject>Introns</subject><subject>Oryza - genetics</subject><subject>Oryza - metabolism</subject><subject>Oryza - physiology</subject><subject>Photosynthesis - genetics</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - physiology</subject><subject>Plastids - genetics</subject><subject>Research Papers</subject><subject>RNA Editing</subject><subject>RNA Splicing</subject><subject>Signal Transduction</subject><subject>Stress, Physiological</subject><issn>0022-0957</issn><issn>1460-2431</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNp90U1LHTEUBuAgFb1-bPwBkk2hiKNJJpm5sxGK2Fa44KKKy3BuckZj507SJFP035tyVXTj6izy5D0HXkIOODvhrKtPHx6XpxifBJcbZMZlwyoha_6FzBgTomKdarfJTkoPjDHFlNoi26Kbd3Un5zPy5_b3Qh1ToAHHDDk64wOG7CzSiAEh0xB9RjceU5coplSYg4H2PlJzP_jowwAp06XzdzhiKsiNtMQgnUaLBfnB0pRj-bpHNnsYEu6_zF1y8-Pi-vxXtbj6eXn-fVEZyea5gp7V0tjeWABp1LJXom4a27RCAsrWiL41BmrRtE2LrQTLDQODKOu-QytUvUvO1rlhWq7QmnJyhEGH6FYQn7QHpz--jO5e3_l_umFKcsVLwLeXgOj_TpiyXrlkcBhgRD8lLYrrhFRtU-jRmproU4rYv63hTP9vR5d29Lqdgg_fH_ZGX-so4Osa-Cl8FvQM-06cew</recordid><startdate>20180718</startdate><enddate>20180718</enddate><creator>Liu, Xi</creator><creator>Lan, Jie</creator><creator>Huang, Yunshuai</creator><creator>Cao, Penghui</creator><creator>Zhou, Chunlei</creator><creator>Ren, Yaken</creator><creator>He, Niqing</creator><creator>Liu, Shijia</creator><creator>Tian, Yunlu</creator><creator>Nguyen, Thanhliem</creator><creator>Jiang, Ling</creator><creator>Wan, Jianmin</creator><general>Oxford University Press</general><scope>TOX</scope><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/0000-0003-1464-5881</orcidid><orcidid>https://orcid.org/0000-0002-7813-4362</orcidid></search><sort><creationdate>20180718</creationdate><title>WSL5, a pentatricopeptide repeat protein, is essential for chloroplast biogenesis in rice under cold stress</title><author>Liu, Xi ; Lan, Jie ; Huang, Yunshuai ; Cao, Penghui ; Zhou, Chunlei ; Ren, Yaken ; He, Niqing ; Liu, Shijia ; Tian, Yunlu ; Nguyen, Thanhliem ; Jiang, Ling ; Wan, Jianmin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c408t-af034cdfcdaa4c5bf52366d6724ae47c2f7cca326767e74ad1c0acee43f9ed253</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Alleles</topic><topic>Chloroplasts - metabolism</topic><topic>Cloning, Molecular</topic><topic>Cold-Shock Response</topic><topic>Down-Regulation</topic><topic>Genes, Plant</topic><topic>Introns</topic><topic>Oryza - genetics</topic><topic>Oryza - metabolism</topic><topic>Oryza - physiology</topic><topic>Photosynthesis - genetics</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - physiology</topic><topic>Plastids - genetics</topic><topic>Research Papers</topic><topic>RNA Editing</topic><topic>RNA Splicing</topic><topic>Signal Transduction</topic><topic>Stress, Physiological</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Xi</creatorcontrib><creatorcontrib>Lan, Jie</creatorcontrib><creatorcontrib>Huang, Yunshuai</creatorcontrib><creatorcontrib>Cao, Penghui</creatorcontrib><creatorcontrib>Zhou, Chunlei</creatorcontrib><creatorcontrib>Ren, Yaken</creatorcontrib><creatorcontrib>He, Niqing</creatorcontrib><creatorcontrib>Liu, Shijia</creatorcontrib><creatorcontrib>Tian, Yunlu</creatorcontrib><creatorcontrib>Nguyen, Thanhliem</creatorcontrib><creatorcontrib>Jiang, Ling</creatorcontrib><creatorcontrib>Wan, Jianmin</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><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>Journal of experimental botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Xi</au><au>Lan, Jie</au><au>Huang, Yunshuai</au><au>Cao, Penghui</au><au>Zhou, Chunlei</au><au>Ren, Yaken</au><au>He, Niqing</au><au>Liu, Shijia</au><au>Tian, Yunlu</au><au>Nguyen, Thanhliem</au><au>Jiang, Ling</au><au>Wan, Jianmin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>WSL5, a pentatricopeptide repeat protein, is essential for chloroplast biogenesis in rice under cold stress</atitle><jtitle>Journal of experimental botany</jtitle><addtitle>J Exp Bot</addtitle><date>2018-07-18</date><risdate>2018</risdate><volume>69</volume><issue>16</issue><spage>3949</spage><epage>3961</epage><pages>3949-3961</pages><issn>0022-0957</issn><eissn>1460-2431</eissn><abstract>WSL5 is crucial for the splicing of the chloroplast genes rpl2 and rps12 under cold stress, and affects the retrograde signaling from plastids to the nucleus. Abstract Chloroplasts play an essential role in plant growth and development, and cold conditions affect chloroplast development. Although many genes or regulators involved in chloroplast biogenesis and development have been isolated and characterized, many other components affecting chloroplast biogenesis under cold conditions have not been characterized. Here, we report the functional characterization of a white stripe leaf 5 (wsl5) mutant in rice. The mutant develops white-striped leaves during early leaf development and is albinic when planted under cold stress. Genetic and molecular analysis revealed that WSL5 encodes a novel chloroplast-targeted pentatricopeptide repeat protein. RNA sequencing analysis showed that expression of nuclear-encoded photosynthetic genes in the mutant was significantly repressed, and expression of many chloroplast-encoded genes was also significantly changed. Notably, the wsl5 mutation causes defects in editing of rpl2 and atpA, and splicing of rpl2 and rps12. wsl5 was impaired in chloroplast ribosome biogenesis under cold stress. We propose that the WSL5 allele is required for normal chloroplast development in maintaining retrograde signaling from plastids to the nucleus under cold stress.</abstract><cop>UK</cop><pub>Oxford University Press</pub><pmid>29893948</pmid><doi>10.1093/jxb/ery214</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-1464-5881</orcidid><orcidid>https://orcid.org/0000-0002-7813-4362</orcidid><oa>free_for_read</oa></addata></record>
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subjects Alleles
Chloroplasts - metabolism
Cloning, Molecular
Cold-Shock Response
Down-Regulation
Genes, Plant
Introns
Oryza - genetics
Oryza - metabolism
Oryza - physiology
Photosynthesis - genetics
Plant Proteins - genetics
Plant Proteins - physiology
Plastids - genetics
Research Papers
RNA Editing
RNA Splicing
Signal Transduction
Stress, Physiological
title WSL5, a pentatricopeptide repeat protein, is essential for chloroplast biogenesis in rice under cold stress
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