Ribosome profiling reveals dynamic translational landscape in maize seedlings under drought stress
Summary Plants can respond to environmental changes with various mechanisms occurred at transcriptional and translational levels. Thus far, there have been relatively extensive understandings of stress responses of plants on transcriptional level, while little information is known about that on tran...
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Veröffentlicht in: | The Plant journal : for cell and molecular biology 2015-12, Vol.84 (6), p.1206-1218 |
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creator | Lei, Lei Shi, Junpeng Chen, Jian Zhang, Mei Sun, Silong Xie, Shaojun Li, Xiaojie Zeng, Biao Peng, Lizeng Hauck, Andrew Zhao, Haiming Song, Weibin Fan, Zaifeng Lai, Jinsheng |
description | Summary
Plants can respond to environmental changes with various mechanisms occurred at transcriptional and translational levels. Thus far, there have been relatively extensive understandings of stress responses of plants on transcriptional level, while little information is known about that on translational level. To uncover the landscape of translation in plants in response to drought stress, we performed the recently developed ribosome profiling assay with maize seedlings growing under normal and drought conditions. Comparative analysis of the ribosome profiling data and the RNA‐seq data showed that the fold changes of gene expression at transcriptional level were moderately correlated with that of translational level globally (R2 = 0.69). However, less than half of the responsive genes were shared by transcription and translation under drought condition, suggesting that drought stress can introduce transcriptional and translational responses independently. We found that the translational efficiencies of 931 genes were changed significantly in response to drought stress. Further analysis revealed that the translational efficiencies of genes were highly influenced by their sequence features including GC content, length of coding sequences and normalized minimal free energy. In addition, we detected potential translation of 3063 upstream open reading frames (uORFs) on 2558 genes and these uORFs may affect the translational efficiency of downstream main open reading frames (ORFs). Our study indicates that plant can respond to drought stress with highly dynamic translational mechanism, that acting synergistically with that of transcription.
Significance Statement
Transcriptional changes upon drought stress are well known, but relatively few studies have considered translational changes. Here comparative analyses show that plants can respond to drought stress with highly dynamic translational changes, which function independently and synergistically with the transcriptional response. |
doi_str_mv | 10.1111/tpj.13073 |
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Plants can respond to environmental changes with various mechanisms occurred at transcriptional and translational levels. Thus far, there have been relatively extensive understandings of stress responses of plants on transcriptional level, while little information is known about that on translational level. To uncover the landscape of translation in plants in response to drought stress, we performed the recently developed ribosome profiling assay with maize seedlings growing under normal and drought conditions. Comparative analysis of the ribosome profiling data and the RNA‐seq data showed that the fold changes of gene expression at transcriptional level were moderately correlated with that of translational level globally (R2 = 0.69). However, less than half of the responsive genes were shared by transcription and translation under drought condition, suggesting that drought stress can introduce transcriptional and translational responses independently. We found that the translational efficiencies of 931 genes were changed significantly in response to drought stress. Further analysis revealed that the translational efficiencies of genes were highly influenced by their sequence features including GC content, length of coding sequences and normalized minimal free energy. In addition, we detected potential translation of 3063 upstream open reading frames (uORFs) on 2558 genes and these uORFs may affect the translational efficiency of downstream main open reading frames (ORFs). Our study indicates that plant can respond to drought stress with highly dynamic translational mechanism, that acting synergistically with that of transcription.
Significance Statement
Transcriptional changes upon drought stress are well known, but relatively few studies have considered translational changes. Here comparative analyses show that plants can respond to drought stress with highly dynamic translational changes, which function independently and synergistically with the transcriptional response.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.13073</identifier><identifier>PMID: 26568274</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Botany ; Corn ; Drought ; drought stress ; Environmental changes ; Gene Expression Regulation, Plant - physiology ; maize ; Protein Biosynthesis ; ribosome profiling ; Ribosomes - genetics ; Ribosomes - metabolism ; RNA‐seq ; Seedlings ; Seedlings - genetics ; Seedlings - metabolism ; Transcription factors ; Transcription, Genetic ; Transcriptome ; translational efficiency ; uORFs ; Water ; Zea mays - genetics ; Zea mays - metabolism</subject><ispartof>The Plant journal : for cell and molecular biology, 2015-12, Vol.84 (6), p.1206-1218</ispartof><rights>2015 The Authors. published by Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>2015 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>Copyright © 2015 John Wiley & Sons Ltd and the Society for Experimental Biology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5243-c76a06d7a197974de7e499fded89562c067c53e3176b43e188a698b03de1eef83</citedby><cites>FETCH-LOGICAL-c5243-c76a06d7a197974de7e499fded89562c067c53e3176b43e188a698b03de1eef83</cites></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.13073$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.13073$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>315,781,785,1418,1434,27928,27929,45578,45579,46413,46837</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26568274$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lei, Lei</creatorcontrib><creatorcontrib>Shi, Junpeng</creatorcontrib><creatorcontrib>Chen, Jian</creatorcontrib><creatorcontrib>Zhang, Mei</creatorcontrib><creatorcontrib>Sun, Silong</creatorcontrib><creatorcontrib>Xie, Shaojun</creatorcontrib><creatorcontrib>Li, Xiaojie</creatorcontrib><creatorcontrib>Zeng, Biao</creatorcontrib><creatorcontrib>Peng, Lizeng</creatorcontrib><creatorcontrib>Hauck, Andrew</creatorcontrib><creatorcontrib>Zhao, Haiming</creatorcontrib><creatorcontrib>Song, Weibin</creatorcontrib><creatorcontrib>Fan, Zaifeng</creatorcontrib><creatorcontrib>Lai, Jinsheng</creatorcontrib><title>Ribosome profiling reveals dynamic translational landscape in maize seedlings under drought stress</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>Summary
Plants can respond to environmental changes with various mechanisms occurred at transcriptional and translational levels. Thus far, there have been relatively extensive understandings of stress responses of plants on transcriptional level, while little information is known about that on translational level. To uncover the landscape of translation in plants in response to drought stress, we performed the recently developed ribosome profiling assay with maize seedlings growing under normal and drought conditions. Comparative analysis of the ribosome profiling data and the RNA‐seq data showed that the fold changes of gene expression at transcriptional level were moderately correlated with that of translational level globally (R2 = 0.69). However, less than half of the responsive genes were shared by transcription and translation under drought condition, suggesting that drought stress can introduce transcriptional and translational responses independently. We found that the translational efficiencies of 931 genes were changed significantly in response to drought stress. Further analysis revealed that the translational efficiencies of genes were highly influenced by their sequence features including GC content, length of coding sequences and normalized minimal free energy. In addition, we detected potential translation of 3063 upstream open reading frames (uORFs) on 2558 genes and these uORFs may affect the translational efficiency of downstream main open reading frames (ORFs). Our study indicates that plant can respond to drought stress with highly dynamic translational mechanism, that acting synergistically with that of transcription.
Significance Statement
Transcriptional changes upon drought stress are well known, but relatively few studies have considered translational changes. Here comparative analyses show that plants can respond to drought stress with highly dynamic translational changes, which function independently and synergistically with the transcriptional response.</description><subject>Botany</subject><subject>Corn</subject><subject>Drought</subject><subject>drought stress</subject><subject>Environmental changes</subject><subject>Gene Expression Regulation, Plant - physiology</subject><subject>maize</subject><subject>Protein Biosynthesis</subject><subject>ribosome profiling</subject><subject>Ribosomes - genetics</subject><subject>Ribosomes - metabolism</subject><subject>RNA‐seq</subject><subject>Seedlings</subject><subject>Seedlings - genetics</subject><subject>Seedlings - metabolism</subject><subject>Transcription factors</subject><subject>Transcription, Genetic</subject><subject>Transcriptome</subject><subject>translational efficiency</subject><subject>uORFs</subject><subject>Water</subject><subject>Zea mays - genetics</subject><subject>Zea mays - metabolism</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp1kE1LxDAQhoMouq4e_AMS8KKH7iZNm7RHWfxkQZEVvIW0ma5Z-mXSKuuvN2tXD4JzmcvzPsy8CJ1QMqF-pl27mlBGBNtBI8p4HDDKXnbRiKScBCKi4QE6dG5FCBWMR_voIOQxT0IRjVD2ZLLGNRXg1jaFKU29xBbeQZUO63WtKpPjzqralaozTa1KXKpau1y1gE2NK2U-ATsAvUk63NcaLNa26ZevHXadBeeO0F7hdXC83WP0fH21mN0G84ebu9nlPMjjMGJBLrgiXAtFU5GKSIOAKE0LDTpJYx7mhIs8ZsCo4FnEgCaJ4mmSEaaBAhQJG6Pzwes_eevBdbIyLofSHwxN76QPkiQWlIYePfuDrpre-u82VCxEmDJ_0hhdDFRuG-csFLK1plJ2LSmRm-KlL15-F-_Z062xzyrQv-RP0x6YDsCHKWH9v0kuHu8H5RfsI43I</recordid><startdate>201512</startdate><enddate>201512</enddate><creator>Lei, Lei</creator><creator>Shi, Junpeng</creator><creator>Chen, Jian</creator><creator>Zhang, Mei</creator><creator>Sun, Silong</creator><creator>Xie, Shaojun</creator><creator>Li, Xiaojie</creator><creator>Zeng, Biao</creator><creator>Peng, Lizeng</creator><creator>Hauck, Andrew</creator><creator>Zhao, Haiming</creator><creator>Song, Weibin</creator><creator>Fan, Zaifeng</creator><creator>Lai, Jinsheng</creator><general>Blackwell Publishing Ltd</general><scope>24P</scope><scope>WIN</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>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><scope>7X8</scope></search><sort><creationdate>201512</creationdate><title>Ribosome profiling reveals dynamic translational landscape in maize seedlings under drought stress</title><author>Lei, Lei ; Shi, Junpeng ; Chen, Jian ; Zhang, Mei ; Sun, Silong ; Xie, Shaojun ; Li, Xiaojie ; Zeng, Biao ; Peng, Lizeng ; Hauck, Andrew ; Zhao, Haiming ; Song, Weibin ; Fan, Zaifeng ; Lai, Jinsheng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5243-c76a06d7a197974de7e499fded89562c067c53e3176b43e188a698b03de1eef83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Botany</topic><topic>Corn</topic><topic>Drought</topic><topic>drought stress</topic><topic>Environmental changes</topic><topic>Gene Expression Regulation, Plant - physiology</topic><topic>maize</topic><topic>Protein Biosynthesis</topic><topic>ribosome profiling</topic><topic>Ribosomes - genetics</topic><topic>Ribosomes - metabolism</topic><topic>RNA‐seq</topic><topic>Seedlings</topic><topic>Seedlings - genetics</topic><topic>Seedlings - metabolism</topic><topic>Transcription factors</topic><topic>Transcription, Genetic</topic><topic>Transcriptome</topic><topic>translational efficiency</topic><topic>uORFs</topic><topic>Water</topic><topic>Zea mays - genetics</topic><topic>Zea mays - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lei, Lei</creatorcontrib><creatorcontrib>Shi, Junpeng</creatorcontrib><creatorcontrib>Chen, Jian</creatorcontrib><creatorcontrib>Zhang, Mei</creatorcontrib><creatorcontrib>Sun, Silong</creatorcontrib><creatorcontrib>Xie, Shaojun</creatorcontrib><creatorcontrib>Li, Xiaojie</creatorcontrib><creatorcontrib>Zeng, Biao</creatorcontrib><creatorcontrib>Peng, Lizeng</creatorcontrib><creatorcontrib>Hauck, Andrew</creatorcontrib><creatorcontrib>Zhao, Haiming</creatorcontrib><creatorcontrib>Song, Weibin</creatorcontrib><creatorcontrib>Fan, Zaifeng</creatorcontrib><creatorcontrib>Lai, Jinsheng</creatorcontrib><collection>Wiley Online Library (Open Access Collection)</collection><collection>Wiley Online Library (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>Biotechnology Research Abstracts</collection><collection>Calcium & 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><collection>MEDLINE - Academic</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lei, Lei</au><au>Shi, Junpeng</au><au>Chen, Jian</au><au>Zhang, Mei</au><au>Sun, Silong</au><au>Xie, Shaojun</au><au>Li, Xiaojie</au><au>Zeng, Biao</au><au>Peng, Lizeng</au><au>Hauck, Andrew</au><au>Zhao, Haiming</au><au>Song, Weibin</au><au>Fan, Zaifeng</au><au>Lai, Jinsheng</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ribosome profiling reveals dynamic translational landscape in maize seedlings under drought stress</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2015-12</date><risdate>2015</risdate><volume>84</volume><issue>6</issue><spage>1206</spage><epage>1218</epage><pages>1206-1218</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>Summary
Plants can respond to environmental changes with various mechanisms occurred at transcriptional and translational levels. Thus far, there have been relatively extensive understandings of stress responses of plants on transcriptional level, while little information is known about that on translational level. To uncover the landscape of translation in plants in response to drought stress, we performed the recently developed ribosome profiling assay with maize seedlings growing under normal and drought conditions. Comparative analysis of the ribosome profiling data and the RNA‐seq data showed that the fold changes of gene expression at transcriptional level were moderately correlated with that of translational level globally (R2 = 0.69). However, less than half of the responsive genes were shared by transcription and translation under drought condition, suggesting that drought stress can introduce transcriptional and translational responses independently. We found that the translational efficiencies of 931 genes were changed significantly in response to drought stress. Further analysis revealed that the translational efficiencies of genes were highly influenced by their sequence features including GC content, length of coding sequences and normalized minimal free energy. In addition, we detected potential translation of 3063 upstream open reading frames (uORFs) on 2558 genes and these uORFs may affect the translational efficiency of downstream main open reading frames (ORFs). Our study indicates that plant can respond to drought stress with highly dynamic translational mechanism, that acting synergistically with that of transcription.
Significance Statement
Transcriptional changes upon drought stress are well known, but relatively few studies have considered translational changes. Here comparative analyses show that plants can respond to drought stress with highly dynamic translational changes, which function independently and synergistically with the transcriptional response.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>26568274</pmid><doi>10.1111/tpj.13073</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Botany Corn Drought drought stress Environmental changes Gene Expression Regulation, Plant - physiology maize Protein Biosynthesis ribosome profiling Ribosomes - genetics Ribosomes - metabolism RNA‐seq Seedlings Seedlings - genetics Seedlings - metabolism Transcription factors Transcription, Genetic Transcriptome translational efficiency uORFs Water Zea mays - genetics Zea mays - metabolism |
title | Ribosome profiling reveals dynamic translational landscape in maize seedlings under drought stress |
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