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

Abstract

BackgroundAllopolyploids 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.ResultsWe 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.ConclusionsCollectively, 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 materialThe online version of this article (10.1186/s12864-018-4966-5) contains supplementary material, which is available to authorized users.

Assessing the response of small RNA populations to allopolyploidy using resynthesized Brassica napus allotetraploids

“…The lower-accumulation of sRNAs involved in metabolism is in accordance with previous works performed on the same Brassica material that identified up-regulation of genes involved in metabolism and notably photosynthesis, in early allotetraploids (Marmagne et al 2010) as well as on other Brassica neoallotetraploids with diverse metabolic processes that were enriched in up-regulated genes in the first generation of selfing (Wu et al 2018). Other studies dealing with the outcome of allopolyploidy have demonstrated the higher photosynthetic capacity of allopolyploids compared to their diploid progenitors (e.g.…”

Replaying the evolutionary tape to investigate subgenome dominance in allopolyploid Brassica napus

“…Given that gene expression level dominance occurs instantly following the initial hybridization event (15) , resynthesized allopolyploids are the ideal system to investigate the establishment and escalation of subgenome dominance. Few studies have used multiple independently derived resynthesized allopolyploids to investigate the variability of subgenome dominance (21)(22)(23)(24)(25)(26) . Thus it remains unclear the extent to which the emergence of subgenome dominance is a result of pre-existing characteristics of the diploid progenitors or due to independent and non-recurrent events during polyploid formation.…”

Homoeolog expression bias and expression level dominance (ELD) in four tissues of natural allotetraploid Brassica napus

“…the world. This crop not only provides edible oil and important nutrients for human beings but also provides protein-rich food for animals [20]. The allotetraploid B. napus was formed by natural hybridization and polyploidization of two diploid progenitors, B. rapa (A r A r , 2n = 20) and B. oleracea (C o C o , 2n = 18), approximately 7,500 years ago [21].…”

“…To date, many genetic and epigenetic changes in the formation of allotetraploid B. napus have been studied, including chromosome pairings [23], chromosomal rearrangements [18,[24][25][26][27][28], transposon activation [29], gene expression changes [28,[30][31][32][33][34][35], alternative splicing pattern changes [36], epigenetic phenomena [28,37,38], and protein expression changes [39,40]. Moreover, only one study has focused on changes in expression level dominance (ELD) and homoeolog expression bias in newly synthesized allotetraploid B. napus and its diploid parents [20]. However, similar studies are limited in natural allotetraploid B. napus and its diploid progenitors.…”

“…High-throughput transcriptome sequencing technology can provide whole-genome gene expression information with low background signals but accurate quantification [41] and makes it possible to distinguish the expression of homologous genes [20,42]. In recent years, the genomes of B. napus [21,43,44] and its two diploid progenitors B. rapa [45] and B. oleracea [46] have been successfully sequenced, providing an unprecedented opportunity to explore the ELD and homologous expression bias of natural allotetraploid B. napus and its two diploid progenitors.…”