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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Veröffentlicht in:PloS one 2011-08, Vol.6 (8), p.e24251
Hauptverfasser: Kim, Eun-Deok, Chen, Z Jeffery
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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. 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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. 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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
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