Homoeolog expression bias and expression level dominance in resynthesized allopolyploid Brassica napus
Abstract 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...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2018-08-01
|
| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12864-018-4966-5 |
| _version_ | 1819027967028756480 |
|---|---|
| author | Jian Wu Li Lin Meiling Xu Peipei Chen Dongxiao Liu Qinfu Sun Liping Ran Youping Wang |
| author_facet | Jian Wu Li Lin Meiling Xu Peipei Chen Dongxiao Liu Qinfu Sun Liping Ran Youping Wang |
| author_sort | Jian Wu |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-12-21T05:50:52Z |
| format | Article |
| id | doaj.art-966c409623d74e469f35445f5d0a24dd |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-21T05:50:52Z |
| publishDate | 2018-08-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-966c409623d74e469f35445f5d0a24dd2022-12-21T19:13:58ZengBMCBMC Genomics1471-21642018-08-0119111310.1186/s12864-018-4966-5Homoeolog expression bias and expression level dominance in resynthesized allopolyploid Brassica napusJian Wu0Li Lin1Meiling Xu2Peipei Chen3Dongxiao Liu4Qinfu Sun5Liping Ran6Youping Wang7Jiangsu Provincial Key Laboratory of Crop Genetics and Physiology, Yangzhou UniversityJiangsu Provincial Key Laboratory of Crop Genetics and Physiology, Yangzhou UniversityJiangsu Provincial Key Laboratory of Crop Genetics and Physiology, Yangzhou UniversityJiangsu Provincial Key Laboratory of Crop Genetics and Physiology, Yangzhou UniversityJiangsu Provincial Key Laboratory of Crop Genetics and Physiology, Yangzhou UniversityJiangsu Provincial Key Laboratory of Crop Genetics and Physiology, Yangzhou UniversityJiangsu Provincial Key Laboratory of Crop Genetics and Physiology, Yangzhou UniversityJiangsu Provincial Key Laboratory of Crop Genetics and Physiology, Yangzhou UniversityAbstract 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.http://link.springer.com/article/10.1186/s12864-018-4966-5Oilseed rapeAllopolyploidizationGene expression patternsHomoeolog expression biasExpression level dominanceRNA sequencing |
| spellingShingle | Jian Wu Li Lin Meiling Xu Peipei Chen Dongxiao Liu Qinfu Sun Liping Ran Youping Wang Homoeolog expression bias and expression level dominance in resynthesized allopolyploid Brassica napus BMC Genomics Oilseed rape Allopolyploidization Gene expression patterns Homoeolog expression bias Expression level dominance RNA sequencing |
| 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 | Oilseed rape Allopolyploidization Gene expression patterns Homoeolog expression bias Expression level dominance RNA sequencing |
| url | http://link.springer.com/article/10.1186/s12864-018-4966-5 |
| work_keys_str_mv | AT jianwu homoeologexpressionbiasandexpressionleveldominanceinresynthesizedallopolyploidbrassicanapus AT lilin homoeologexpressionbiasandexpressionleveldominanceinresynthesizedallopolyploidbrassicanapus AT meilingxu homoeologexpressionbiasandexpressionleveldominanceinresynthesizedallopolyploidbrassicanapus AT peipeichen homoeologexpressionbiasandexpressionleveldominanceinresynthesizedallopolyploidbrassicanapus AT dongxiaoliu homoeologexpressionbiasandexpressionleveldominanceinresynthesizedallopolyploidbrassicanapus AT qinfusun homoeologexpressionbiasandexpressionleveldominanceinresynthesizedallopolyploidbrassicanapus AT lipingran homoeologexpressionbiasandexpressionleveldominanceinresynthesizedallopolyploidbrassicanapus AT youpingwang homoeologexpressionbiasandexpressionleveldominanceinresynthesizedallopolyploidbrassicanapus |