Unstable transcripts in Arabidopsis allotetraploids are associated with nonadditive gene expression in response to abiotic and biotic stresses
Genome-wide analysis has documented differential gene expression between closely related species in plants and animals and nonadditive gene expression in hybrids and allopolyploids compared to the parents. In Arabidopsis, 15-43% of genes are expressed differently between the related species, Arabido...
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description | Genome-wide analysis has documented differential gene expression between closely related species in plants and animals and nonadditive gene expression in hybrids and allopolyploids compared to the parents. In Arabidopsis, 15-43% of genes are expressed differently between the related species, Arabidopsis thaliana and Arabidopsis arenosa, the majority of which are nonadditively expressed (differently from mid-parent value) in allotetraploids. Nonadditive gene expression can be caused by transcriptional regulation through chromatin modifications, but the role of posttranscriptional regulation in nonadditive gene expression is largely unknown. Here we reported genome-wide analysis of mRNA decay in resynthesized Arabidopsis allotetraploids. Among ∼26,000 annotated genes, over 1% of gene transcripts showed rapid decay with an estimated half-life of less than 60 minutes, and they are called allotetraploid genes with unstable transcripts (AlloGUTs). Remarkably, 30% of alloGUTs matched the nonadditively expressed genes, and their expression levels were negatively correlated with the decay rate. Compared to all genes, these nonadditively expressed alloGUTs were overrepresented 2-6-fold in the Gene Ontology (GOSlim) classifications in response to abiotic and biotic stresses, signal transduction, and transcription. Interestingly, the AlloGUTs include transcription factor genes that are highly inducible under stress conditions and circadian clock regulators that regulate growth in A. thaliana. These data suggest a role of mRNA stability in homoeologous gene expression in Arabidopsis allopolyploids. The enrichment of nonadditively expressed genes in stress-related pathways were commonly observed in Arabidopsis and other allopolyploids such as wheat and cotton, which may suggest a role for stress-mediated growth vigor in hybrids and allopolyploids. |
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In Arabidopsis, 15-43% of genes are expressed differently between the related species, Arabidopsis thaliana and Arabidopsis arenosa, the majority of which are nonadditively expressed (differently from mid-parent value) in allotetraploids. Nonadditive gene expression can be caused by transcriptional regulation through chromatin modifications, but the role of posttranscriptional regulation in nonadditive gene expression is largely unknown. Here we reported genome-wide analysis of mRNA decay in resynthesized Arabidopsis allotetraploids. Among ∼26,000 annotated genes, over 1% of gene transcripts showed rapid decay with an estimated half-life of less than 60 minutes, and they are called allotetraploid genes with unstable transcripts (AlloGUTs). Remarkably, 30% of alloGUTs matched the nonadditively expressed genes, and their expression levels were negatively correlated with the decay rate. Compared to all genes, these nonadditively expressed alloGUTs were overrepresented 2-6-fold in the Gene Ontology (GOSlim) classifications in response to abiotic and biotic stresses, signal transduction, and transcription. Interestingly, the AlloGUTs include transcription factor genes that are highly inducible under stress conditions and circadian clock regulators that regulate growth in A. thaliana. These data suggest a role of mRNA stability in homoeologous gene expression in Arabidopsis allopolyploids. The enrichment of nonadditively expressed genes in stress-related pathways were commonly observed in Arabidopsis and other allopolyploids such as wheat and cotton, which may suggest a role for stress-mediated growth vigor in hybrids and allopolyploids.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0024251</identifier><identifier>PMID: 21897874</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Arabidopsis ; Arabidopsis - drug effects ; Arabidopsis - genetics ; Arabidopsis - physiology ; Arabidopsis thaliana ; Barley ; Bioinformatics ; Biology ; Cellular signal transduction ; Chromatin ; Circadian Clocks - genetics ; Circadian rhythm ; Circadian rhythms ; Comparative analysis ; Cotton ; Decay ; Decay rate ; Developmental biology ; Gene expression ; Gene Expression Regulation - drug effects ; Gene Expression Regulation - genetics ; Gene regulation ; Genes ; Genetic aspects ; Genomes ; Genomics ; Hybrids ; Kinetics ; Mammals ; Messenger RNA ; Molecular biology ; mRNA stability ; mRNA turnover ; Oligonucleotide Array Sequence Analysis ; Parents ; Plant growth ; Plant Growth Regulators - pharmacology ; Polyploidy ; Post-transcription ; Regulators ; RNA Stability - drug effects ; RNA, Messenger - chemistry ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Stress ; Stress, Physiological - drug effects ; Stress, Physiological - genetics ; Stresses ; Tetraploidy ; Transcription (Genetics) ; Transduction ; Vigor ; Wheat ; Yeast</subject><ispartof>PloS one, 2011-08, Vol.6 (8), p.e24251</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>2011 Kim, Chen. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Kim, Chen. 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c691t-967ab0f0ae243fe7baefbd7d49523ee9c5cc271036173c63dc5c0fb96db2cea83</citedby><cites>FETCH-LOGICAL-c691t-967ab0f0ae243fe7baefbd7d49523ee9c5cc271036173c63dc5c0fb96db2cea83</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3163679/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3163679/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,2926,23864,27922,27923,53789,53791,79370,79371</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21897874$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Hazen, Samuel P.</contributor><creatorcontrib>Kim, Eun-Deok</creatorcontrib><creatorcontrib>Chen, Z Jeffery</creatorcontrib><title>Unstable transcripts in Arabidopsis allotetraploids are associated with nonadditive gene expression in response to abiotic and biotic stresses</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Genome-wide analysis has documented differential gene expression between closely related species in plants and animals and nonadditive gene expression in hybrids and allopolyploids compared to the parents. In Arabidopsis, 15-43% of genes are expressed differently between the related species, Arabidopsis thaliana and Arabidopsis arenosa, the majority of which are nonadditively expressed (differently from mid-parent value) in allotetraploids. Nonadditive gene expression can be caused by transcriptional regulation through chromatin modifications, but the role of posttranscriptional regulation in nonadditive gene expression is largely unknown. Here we reported genome-wide analysis of mRNA decay in resynthesized Arabidopsis allotetraploids. Among ∼26,000 annotated genes, over 1% of gene transcripts showed rapid decay with an estimated half-life of less than 60 minutes, and they are called allotetraploid genes with unstable transcripts (AlloGUTs). Remarkably, 30% of alloGUTs matched the nonadditively expressed genes, and their expression levels were negatively correlated with the decay rate. Compared to all genes, these nonadditively expressed alloGUTs were overrepresented 2-6-fold in the Gene Ontology (GOSlim) classifications in response to abiotic and biotic stresses, signal transduction, and transcription. Interestingly, the AlloGUTs include transcription factor genes that are highly inducible under stress conditions and circadian clock regulators that regulate growth in A. thaliana. These data suggest a role of mRNA stability in homoeologous gene expression in Arabidopsis allopolyploids. The enrichment of nonadditively expressed genes in stress-related pathways were commonly observed in Arabidopsis and other allopolyploids such as wheat and cotton, which may suggest a role for stress-mediated growth vigor in hybrids and allopolyploids.</description><subject>Arabidopsis</subject><subject>Arabidopsis - drug effects</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis thaliana</subject><subject>Barley</subject><subject>Bioinformatics</subject><subject>Biology</subject><subject>Cellular signal transduction</subject><subject>Chromatin</subject><subject>Circadian Clocks - genetics</subject><subject>Circadian rhythm</subject><subject>Circadian rhythms</subject><subject>Comparative analysis</subject><subject>Cotton</subject><subject>Decay</subject><subject>Decay rate</subject><subject>Developmental biology</subject><subject>Gene expression</subject><subject>Gene Expression Regulation - drug effects</subject><subject>Gene Expression Regulation - genetics</subject><subject>Gene regulation</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Hybrids</subject><subject>Kinetics</subject><subject>Mammals</subject><subject>Messenger RNA</subject><subject>Molecular biology</subject><subject>mRNA stability</subject><subject>mRNA turnover</subject><subject>Oligonucleotide Array Sequence Analysis</subject><subject>Parents</subject><subject>Plant growth</subject><subject>Plant Growth Regulators - pharmacology</subject><subject>Polyploidy</subject><subject>Post-transcription</subject><subject>Regulators</subject><subject>RNA Stability - drug effects</subject><subject>RNA, Messenger - chemistry</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Stress</subject><subject>Stress, Physiological - drug effects</subject><subject>Stress, Physiological - genetics</subject><subject>Stresses</subject><subject>Tetraploidy</subject><subject>Transcription (Genetics)</subject><subject>Transduction</subject><subject>Vigor</subject><subject>Wheat</subject><subject>Yeast</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk2-L1DAQxoso3nn6DUQDguCLXZOmm7RvhOXwz8LBgXq-DWky3c3RTWome55fws9s1u0dW1CQvuhk-ptnpg-TonjO6Jxxyd5eh130up8PwcOc0rIqF-xBccoaXs5ESfnDo_ikeIJ4TemC10I8Lk5KVjeyltVp8evKY9JtDyRF7dFENyQkzpNl1K2zYUCHRPd9SJCBoQ_O5nMEohGDcTqBJT9c2hAfvLbWJXcDZA0eCNwOERBd8Hu5HOZBMbcJJAuH5AzR3pIxxLRnAZ8WjzrdIzwb32fF1Yf3X88_zS4uP67OlxczIxqWZo2QuqUd1VBWvAPZauhaK23VLEoO0JiFMaVklAsmuRHc5gTt2kbYtjSga35WvDzo5j9CNVqJinEqszNUlplYHQgb9LUaotvq-FMF7dSfRIhrpWMevQdlOy0rbSTnwlZdx1pRQVuVIAxrS2323d6N3XbtFqwBn73sJ6LTL95t1DrcKM4EF7LJAq9GgRi-7wDTP0YeqbXOUznfhSxmtg6NWlZS1DXLfmRq_hcqPxa2zuRl6lzOTwreTAoyk-A2rfUOUa2-fP5_9vLblH19xG5A92mDod-lvDI4BasDaGJAjNDdO8eo2t-FOzfU_i6o8S7kshfHrt8X3S0__w0E_Qny</recordid><startdate>20110829</startdate><enddate>20110829</enddate><creator>Kim, Eun-Deok</creator><creator>Chen, Z Jeffery</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20110829</creationdate><title>Unstable transcripts in Arabidopsis allotetraploids are associated with nonadditive gene expression in response to abiotic and biotic stresses</title><author>Kim, Eun-Deok ; Chen, Z Jeffery</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c691t-967ab0f0ae243fe7baefbd7d49523ee9c5cc271036173c63dc5c0fb96db2cea83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - drug effects</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis thaliana</topic><topic>Barley</topic><topic>Bioinformatics</topic><topic>Biology</topic><topic>Cellular signal transduction</topic><topic>Chromatin</topic><topic>Circadian Clocks - genetics</topic><topic>Circadian rhythm</topic><topic>Circadian rhythms</topic><topic>Comparative analysis</topic><topic>Cotton</topic><topic>Decay</topic><topic>Decay rate</topic><topic>Developmental biology</topic><topic>Gene expression</topic><topic>Gene Expression Regulation - drug effects</topic><topic>Gene Expression Regulation - genetics</topic><topic>Gene regulation</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Hybrids</topic><topic>Kinetics</topic><topic>Mammals</topic><topic>Messenger RNA</topic><topic>Molecular biology</topic><topic>mRNA stability</topic><topic>mRNA turnover</topic><topic>Oligonucleotide Array Sequence Analysis</topic><topic>Parents</topic><topic>Plant growth</topic><topic>Plant Growth Regulators - pharmacology</topic><topic>Polyploidy</topic><topic>Post-transcription</topic><topic>Regulators</topic><topic>RNA Stability - drug effects</topic><topic>RNA, Messenger - chemistry</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>Stress</topic><topic>Stress, Physiological - drug effects</topic><topic>Stress, Physiological - genetics</topic><topic>Stresses</topic><topic>Tetraploidy</topic><topic>Transcription (Genetics)</topic><topic>Transduction</topic><topic>Vigor</topic><topic>Wheat</topic><topic>Yeast</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kim, Eun-Deok</creatorcontrib><creatorcontrib>Chen, Z Jeffery</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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In Arabidopsis, 15-43% of genes are expressed differently between the related species, Arabidopsis thaliana and Arabidopsis arenosa, the majority of which are nonadditively expressed (differently from mid-parent value) in allotetraploids. Nonadditive gene expression can be caused by transcriptional regulation through chromatin modifications, but the role of posttranscriptional regulation in nonadditive gene expression is largely unknown. Here we reported genome-wide analysis of mRNA decay in resynthesized Arabidopsis allotetraploids. Among ∼26,000 annotated genes, over 1% of gene transcripts showed rapid decay with an estimated half-life of less than 60 minutes, and they are called allotetraploid genes with unstable transcripts (AlloGUTs). Remarkably, 30% of alloGUTs matched the nonadditively expressed genes, and their expression levels were negatively correlated with the decay rate. Compared to all genes, these nonadditively expressed alloGUTs were overrepresented 2-6-fold in the Gene Ontology (GOSlim) classifications in response to abiotic and biotic stresses, signal transduction, and transcription. Interestingly, the AlloGUTs include transcription factor genes that are highly inducible under stress conditions and circadian clock regulators that regulate growth in A. thaliana. These data suggest a role of mRNA stability in homoeologous gene expression in Arabidopsis allopolyploids. The enrichment of nonadditively expressed genes in stress-related pathways were commonly observed in Arabidopsis and other allopolyploids such as wheat and cotton, which may suggest a role for stress-mediated growth vigor in hybrids and allopolyploids.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21897874</pmid><doi>10.1371/journal.pone.0024251</doi><tpages>e24251</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis Arabidopsis - drug effects Arabidopsis - genetics Arabidopsis - physiology Arabidopsis thaliana Barley Bioinformatics Biology Cellular signal transduction Chromatin Circadian Clocks - genetics Circadian rhythm Circadian rhythms Comparative analysis Cotton Decay Decay rate Developmental biology Gene expression Gene Expression Regulation - drug effects Gene Expression Regulation - genetics Gene regulation Genes Genetic aspects Genomes Genomics Hybrids Kinetics Mammals Messenger RNA Molecular biology mRNA stability mRNA turnover Oligonucleotide Array Sequence Analysis Parents Plant growth Plant Growth Regulators - pharmacology Polyploidy Post-transcription Regulators RNA Stability - drug effects RNA, Messenger - chemistry RNA, Messenger - genetics RNA, Messenger - metabolism Stress Stress, Physiological - drug effects Stress, Physiological - genetics Stresses Tetraploidy Transcription (Genetics) Transduction Vigor Wheat Yeast |
title | Unstable transcripts in Arabidopsis allotetraploids are associated with nonadditive gene expression in response to abiotic and biotic stresses |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-09T22%3A33%3A36IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Unstable%20transcripts%20in%20Arabidopsis%20allotetraploids%20are%20associated%20with%20nonadditive%20gene%20expression%20in%20response%20to%20abiotic%20and%20biotic%20stresses&rft.jtitle=PloS%20one&rft.au=Kim,%20Eun-Deok&rft.date=2011-08-29&rft.volume=6&rft.issue=8&rft.spage=e24251&rft.pages=e24251-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0024251&rft_dat=%3Cgale_plos_%3EA476881361%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1307897072&rft_id=info:pmid/21897874&rft_galeid=A476881361&rft_doaj_id=oai_doaj_org_article_dfa74ac7336d4ff1b64eb42e6c1b2ac8&rfr_iscdi=true |