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Unexpected consequences of a sudden and massive transposon amplification on rice gene expression
High-copy-number transposable elements comprise the majority of eukaryotic genomes where they are major contributors to gene and genome evolution. However, it remains unclear how a host genome can survive a rapid burst of hundreds or thousands of insertions because such bursts are exceedingly rare i...
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Published in: | Nature (London) 2009-10, Vol.461 (7267), p.1130-1134 |
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description | High-copy-number transposable elements comprise the majority of eukaryotic genomes where they are major contributors to gene and genome evolution. However, it remains unclear how a host genome can survive a rapid burst of hundreds or thousands of insertions because such bursts are exceedingly rare in nature and therefore difficult to observe in real time. In a previous study we reported that in a few rice strains the DNA transposon mPing was increasing its copy number by approximately 40 per plant per generation. Here we exploit the completely sequenced rice genome to determine 1,664 insertion sites using high-throughput sequencing of 24 individual rice plants and assess the impact of insertion on the expression of 710 genes by comparative microarray analysis. We find that the vast majority of transposable element insertions either upregulate or have no detectable effect on gene transcription. This modest impact reflects a surprising avoidance of exon insertions by mPing and a preference for insertion into 5' flanking sequences of genes. Furthermore, we document the generation of new regulatory networks by a subset of mPing insertions that render adjacent genes stress inducible. As such, this study provides evidence for models first proposed previously for the involvement of transposable elements and other repetitive sequences in genome restructuring and gene regulation. |
doi_str_mv | 10.1038/nature08479 |
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Here we exploit the completely sequenced rice genome to determine 1,664 insertion sites using high-throughput sequencing of 24 individual rice plants and assess the impact of insertion on the expression of 710 genes by comparative microarray analysis. We find that the vast majority of transposable element insertions either upregulate or have no detectable effect on gene transcription. This modest impact reflects a surprising avoidance of exon insertions by mPing and a preference for insertion into 5' flanking sequences of genes. Furthermore, we document the generation of new regulatory networks by a subset of mPing insertions that render adjacent genes stress inducible. As such, this study provides evidence for models first proposed previously for the involvement of transposable elements and other repetitive sequences in genome restructuring and gene regulation.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/nature08479</identifier><identifier>PMID: 19847266</identifier><identifier>CODEN: NATUAS</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>5' Flanking Region - genetics ; Agronomy. Soil science and plant productions ; Alleles ; Analysis ; Arabidopsis - genetics ; Biological and medical sciences ; Cold Temperature ; Comparative analysis ; DNA Copy Number Variations - genetics ; DNA Transposable Elements - genetics ; Exons ; Fundamental and applied biological sciences. Psychology ; gene amplification ; Gene Amplification - genetics ; gene dosage ; Gene Dosage - genetics ; Gene expression ; gene expression regulation ; Gene Expression Regulation, Plant ; genes ; Genetic aspects ; Genetic diversity ; Genetic transcription ; Genetics and breeding of economic plants ; Genomics ; Humanities and Social Sciences ; letter ; Life sciences ; messenger RNA ; microarray technology ; multidisciplinary ; Oligonucleotide Array Sequence Analysis ; Open Reading Frames - genetics ; Oryza - genetics ; Oryza sativa ; Preferences ; Promoter Regions, Genetic - genetics ; Rice ; Science ; Science (multidisciplinary) ; Stress, Physiological - genetics ; Transgenes - genetics ; transposon copy number ; transposon insertions ; Transposons</subject><ispartof>Nature (London), 2009-10, Vol.461 (7267), p.1130-1134</ispartof><rights>Macmillan Publishers Limited. All rights reserved 2009</rights><rights>2009 INIST-CNRS</rights><rights>COPYRIGHT 2009 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Oct 22, 2009</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c641t-c78a07237ff032073d1f4d9cd3ebd8957cc4ba9025ee689ecd2ea7a0b2416aa83</citedby><cites>FETCH-LOGICAL-c641t-c78a07237ff032073d1f4d9cd3ebd8957cc4ba9025ee689ecd2ea7a0b2416aa83</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27903,27904</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=22020614$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19847266$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Naito, Ken</creatorcontrib><creatorcontrib>Zhang, Feng</creatorcontrib><creatorcontrib>Tsukiyama, Takuji</creatorcontrib><creatorcontrib>Saito, Hiroki</creatorcontrib><creatorcontrib>Hancock, C. Nathan</creatorcontrib><creatorcontrib>Richardson, Aaron O</creatorcontrib><creatorcontrib>Okumoto, Yutaka</creatorcontrib><creatorcontrib>Tanisaka, Takatoshi</creatorcontrib><creatorcontrib>Wessler, Susan R</creatorcontrib><title>Unexpected consequences of a sudden and massive transposon amplification on rice gene expression</title><title>Nature (London)</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>High-copy-number transposable elements comprise the majority of eukaryotic genomes where they are major contributors to gene and genome evolution. However, it remains unclear how a host genome can survive a rapid burst of hundreds or thousands of insertions because such bursts are exceedingly rare in nature and therefore difficult to observe in real time. In a previous study we reported that in a few rice strains the DNA transposon mPing was increasing its copy number by approximately 40 per plant per generation. Here we exploit the completely sequenced rice genome to determine 1,664 insertion sites using high-throughput sequencing of 24 individual rice plants and assess the impact of insertion on the expression of 710 genes by comparative microarray analysis. We find that the vast majority of transposable element insertions either upregulate or have no detectable effect on gene transcription. This modest impact reflects a surprising avoidance of exon insertions by mPing and a preference for insertion into 5' flanking sequences of genes. Furthermore, we document the generation of new regulatory networks by a subset of mPing insertions that render adjacent genes stress inducible. As such, this study provides evidence for models first proposed previously for the involvement of transposable elements and other repetitive sequences in genome restructuring and gene regulation.</description><subject>5' Flanking Region - genetics</subject><subject>Agronomy. Soil science and plant productions</subject><subject>Alleles</subject><subject>Analysis</subject><subject>Arabidopsis - genetics</subject><subject>Biological and medical sciences</subject><subject>Cold Temperature</subject><subject>Comparative analysis</subject><subject>DNA Copy Number Variations - genetics</subject><subject>DNA Transposable Elements - genetics</subject><subject>Exons</subject><subject>Fundamental and applied biological sciences. 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Nathan</au><au>Richardson, Aaron O</au><au>Okumoto, Yutaka</au><au>Tanisaka, Takatoshi</au><au>Wessler, Susan R</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Unexpected consequences of a sudden and massive transposon amplification on rice gene expression</atitle><jtitle>Nature (London)</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2009-10-22</date><risdate>2009</risdate><volume>461</volume><issue>7267</issue><spage>1130</spage><epage>1134</epage><pages>1130-1134</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><coden>NATUAS</coden><abstract>High-copy-number transposable elements comprise the majority of eukaryotic genomes where they are major contributors to gene and genome evolution. However, it remains unclear how a host genome can survive a rapid burst of hundreds or thousands of insertions because such bursts are exceedingly rare in nature and therefore difficult to observe in real time. In a previous study we reported that in a few rice strains the DNA transposon mPing was increasing its copy number by approximately 40 per plant per generation. Here we exploit the completely sequenced rice genome to determine 1,664 insertion sites using high-throughput sequencing of 24 individual rice plants and assess the impact of insertion on the expression of 710 genes by comparative microarray analysis. We find that the vast majority of transposable element insertions either upregulate or have no detectable effect on gene transcription. This modest impact reflects a surprising avoidance of exon insertions by mPing and a preference for insertion into 5' flanking sequences of genes. Furthermore, we document the generation of new regulatory networks by a subset of mPing insertions that render adjacent genes stress inducible. As such, this study provides evidence for models first proposed previously for the involvement of transposable elements and other repetitive sequences in genome restructuring and gene regulation.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>19847266</pmid><doi>10.1038/nature08479</doi><tpages>5</tpages></addata></record> |
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subjects | 5' Flanking Region - genetics Agronomy. Soil science and plant productions Alleles Analysis Arabidopsis - genetics Biological and medical sciences Cold Temperature Comparative analysis DNA Copy Number Variations - genetics DNA Transposable Elements - genetics Exons Fundamental and applied biological sciences. Psychology gene amplification Gene Amplification - genetics gene dosage Gene Dosage - genetics Gene expression gene expression regulation Gene Expression Regulation, Plant genes Genetic aspects Genetic diversity Genetic transcription Genetics and breeding of economic plants Genomics Humanities and Social Sciences letter Life sciences messenger RNA microarray technology multidisciplinary Oligonucleotide Array Sequence Analysis Open Reading Frames - genetics Oryza - genetics Oryza sativa Preferences Promoter Regions, Genetic - genetics Rice Science Science (multidisciplinary) Stress, Physiological - genetics Transgenes - genetics transposon copy number transposon insertions Transposons |
title | Unexpected consequences of a sudden and massive transposon amplification on rice gene expression |
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