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Maternal dominance contributes to subgenome differentiation in allopolyploid fishes.

ABSTRACT: Teleost fishes, which are the largest and most diverse group of living vertebrates, have a rich history of ancient and recent polyploidy. Previous studies of allotetraploid common carp and goldfish (cyprinids) reported a dominant subgenome, which is more expressed and exhibits biased gene retention. However, the underlying mechanisms contributing to observed 'subgenome dominance' remains poorly understood. Here we report high-quality genomes of twenty-one cyprinids to investigate the origin and subsequent subgenome evolution patterns following three independent allopolyploidy events. We identify the closest extant relatives of the diploid progenitor species, investigate genetic and epigenetic differences among subgenomes, and conclude that observed subgenome dominance patterns are likely due to a combination of maternal dominance and transposable element densities in each polyploid. These findings provide an important foundation to understanding subgenome dominance patterns observed in teleost fishes, and ultimately the role of polyploidy in contributing to evolutionary innovations.

SUBMITTER: Xu MR

PROVIDER: S-EPMC10724154 | biostudies-literature | 2023 Dec

REPOSITORIES: biostudies-literature

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Maternal dominance contributes to subgenome differentiation in allopolyploid fishes.

Xu Min-Rui-Xuan MR Liao Zhen-Yang ZY Brock Jordan R JR Du Kang K Li Guo-Yin GY Chen Zhi-Qiang ZQ Wang Ying-Hao YH Gao Zhong-Nan ZN Agarwal Gaurav G Wei Kevin H-C KH Shao Feng F Pang Shuai S Platts Adrian E AE van de Velde Jozefien J Lin Hong-Min HM Teresi Scott J SJ Bird Kevin K Niederhuth Chad E CE Xu Jin-Gen JG Yu Guo-Hua GH Yang Jian-Yuan JY Dai Si-Fa SF Nelson Andrew A Braasch Ingo I Zhang Xiao-Gu XG Schartl Manfred M Edger Patrick P PP Han Min-Jin MJ Zhang Hua-Hao HH

Nature communications 20231215 1

Teleost fishes, which are the largest and most diverse group of living vertebrates, have a rich history of ancient and recent polyploidy. Previous studies of allotetraploid common carp and goldfish (cyprinids) reported a dominant subgenome, which is more expressed and exhibits biased gene retention. However, the underlying mechanisms contributing to observed 'subgenome dominance' remains poorly understood. Here we report high-quality genomes of twenty-one cyprinids to investigate the origin and ...[more]

PMID: 38102128

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Project description: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.

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Maternal dominance contributes to subgenome differentiation in allopolyploid fishes.

Publications

Maternal dominance contributes to subgenome differentiation in allopolyploid fishes.

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