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Homoeolog expression bias and expression level dominance in resynthesized allopolyploid Brassica napus

BACKGROUND: Allopolyploids require rapid genetic and epigenetic modifications to reconcile two or more sets of divergent genomes. To better understand the fate of duplicate genes following genomic mergers and doubling during allopolyploid formation, in this study, we explored the global gene express...

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Autores principales: Wu, Jian, Lin, Li, Xu, Meiling, Chen, Peipei, Liu, Dongxiao, Sun, Qinfu, Ran, Liping, Wang, Youping
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6080508/
https://www.ncbi.nlm.nih.gov/pubmed/30081834
http://dx.doi.org/10.1186/s12864-018-4966-5
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author Wu, Jian
Lin, Li
Xu, Meiling
Chen, Peipei
Liu, Dongxiao
Sun, Qinfu
Ran, Liping
Wang, Youping
author_facet Wu, Jian
Lin, Li
Xu, Meiling
Chen, Peipei
Liu, Dongxiao
Sun, Qinfu
Ran, Liping
Wang, Youping
author_sort Wu, Jian
collection PubMed
description BACKGROUND: Allopolyploids require rapid genetic and epigenetic modifications to reconcile two or more sets of divergent genomes. To better understand the fate of duplicate genes following genomic mergers and doubling during allopolyploid formation, in this study, we explored the global gene expression patterns in resynthesized allotetraploid Brassica napus (AACC) and its diploid parents B. rapa (AA) and B. oleracea (CC) using RNA sequencing of leaf transcriptomes. RESULTS: We found that allopolyploid B. napus formation was accompanied by extensive changes (approximately one-third of the expressed genes) in the parental gene expression patterns (‘transcriptome shock’). Interestingly, the majority (85%) of differentially expressed genes (DEGs) were downregulated in the allotetraploid. Moreover, the homoeolog expression bias (relative contribution of homoeologs to the transcriptome) and expression level dominance (total expression level of both homoeologs) were thoroughly investigated by monitoring the expression of 23,766 B. oleracea-B. rapa orthologous gene pairs. Approximately 36.5% of the expressed gene pairs displayed expression bias with a slight preference toward the A-genome. In addition, 39.6, 4.9 and 9.0% of the expressed gene pairs exhibited expression level dominance (ELD), additivity expression and transgressive expression, respectively. The genome-wide ELD was also biased toward the A-genome in the resynthesized B. napus. To explain the ELD phenomenon, we compared the individual homoeolog expression levels relative to those of the diploid parents and found that ELD in the direction of the higher-expression parent can be explained by the downregulation of homoeologs from the dominant parent or upregulation of homoeologs from the nondominant parent; however, ELD in the direction of the lower-expression parent can be explained only by the downregulation of the nondominant parent or both homoeologs. Furthermore, Gene Ontology (GO) enrichment analysis suggested that the alteration in the gene expression patterns could be a prominent cause of the phenotypic variation between the newly formed B. napus and its parental species. CONCLUSIONS: Collectively, our data provide insight into the rapid repatterning of gene expression at the beginning of Brassica allopolyploidization and enhance our knowledge of allopolyploidization processes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4966-5) contains supplementary material, which is available to authorized users.
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spelling pubmed-60805082018-08-09 Homoeolog expression bias and expression level dominance in resynthesized allopolyploid Brassica napus Wu, Jian Lin, Li Xu, Meiling Chen, Peipei Liu, Dongxiao Sun, Qinfu Ran, Liping Wang, Youping BMC Genomics Research Article BACKGROUND: Allopolyploids require rapid genetic and epigenetic modifications to reconcile two or more sets of divergent genomes. To better understand the fate of duplicate genes following genomic mergers and doubling during allopolyploid formation, in this study, we explored the global gene expression patterns in resynthesized allotetraploid Brassica napus (AACC) and its diploid parents B. rapa (AA) and B. oleracea (CC) using RNA sequencing of leaf transcriptomes. RESULTS: We found that allopolyploid B. napus formation was accompanied by extensive changes (approximately one-third of the expressed genes) in the parental gene expression patterns (‘transcriptome shock’). Interestingly, the majority (85%) of differentially expressed genes (DEGs) were downregulated in the allotetraploid. Moreover, the homoeolog expression bias (relative contribution of homoeologs to the transcriptome) and expression level dominance (total expression level of both homoeologs) were thoroughly investigated by monitoring the expression of 23,766 B. oleracea-B. rapa orthologous gene pairs. Approximately 36.5% of the expressed gene pairs displayed expression bias with a slight preference toward the A-genome. In addition, 39.6, 4.9 and 9.0% of the expressed gene pairs exhibited expression level dominance (ELD), additivity expression and transgressive expression, respectively. The genome-wide ELD was also biased toward the A-genome in the resynthesized B. napus. To explain the ELD phenomenon, we compared the individual homoeolog expression levels relative to those of the diploid parents and found that ELD in the direction of the higher-expression parent can be explained by the downregulation of homoeologs from the dominant parent or upregulation of homoeologs from the nondominant parent; however, ELD in the direction of the lower-expression parent can be explained only by the downregulation of the nondominant parent or both homoeologs. Furthermore, Gene Ontology (GO) enrichment analysis suggested that the alteration in the gene expression patterns could be a prominent cause of the phenotypic variation between the newly formed B. napus and its parental species. CONCLUSIONS: Collectively, our data provide insight into the rapid repatterning of gene expression at the beginning of Brassica allopolyploidization and enhance our knowledge of allopolyploidization processes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4966-5) contains supplementary material, which is available to authorized users. BioMed Central 2018-08-06 /pmc/articles/PMC6080508/ /pubmed/30081834 http://dx.doi.org/10.1186/s12864-018-4966-5 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Wu, Jian
Lin, Li
Xu, Meiling
Chen, Peipei
Liu, Dongxiao
Sun, Qinfu
Ran, Liping
Wang, Youping
Homoeolog expression bias and expression level dominance in resynthesized allopolyploid Brassica napus
title Homoeolog expression bias and expression level dominance in resynthesized allopolyploid Brassica napus
title_full Homoeolog expression bias and expression level dominance in resynthesized allopolyploid Brassica napus
title_fullStr Homoeolog expression bias and expression level dominance in resynthesized allopolyploid Brassica napus
title_full_unstemmed Homoeolog expression bias and expression level dominance in resynthesized allopolyploid Brassica napus
title_short Homoeolog expression bias and expression level dominance in resynthesized allopolyploid Brassica napus
title_sort homoeolog expression bias and expression level dominance in resynthesized allopolyploid brassica napus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6080508/
https://www.ncbi.nlm.nih.gov/pubmed/30081834
http://dx.doi.org/10.1186/s12864-018-4966-5
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