The allotetraploid origin and asymmetrical genome evolution of the common carp Cyprinus carpio

Xu, Peng; Xu, Jian; Liu, Guangjian; Chen, Lin; Zhou, Zhixiong; Peng, Wenzhu; Jiang, Yanliang; Zhao, Zixia; Jia, Zhiying; Sun, Yuhan; Wu, Yidi; Chen, Baohua; Pu, Fei; Feng, Jianxin; Luo, Jing; Chai, Jing; Zhang, Hanyuan; Wang, Hui; Dong, Chuanju; Jiang, Wenkai; Sun, Xiaowen

doi:10.1038/s41467-019-12644-1

Cited by 172 publications

(151 citation statements)

References 68 publications

Supporting

Mentioning

119

Contrasting

Order By: Relevance

“…This could lead to uneven ohnolog loss rates, a process that is referred to as biased fractionation [ 27 ]. In line with previous studies on teleosts [ 28 , 29 ], we found significant biases in local gene loss, albeit only in 9 of 47 syntenic duplicate blocks. However, we did not find equivalent large-scale biases in expression loss (Additional file 1 : Figure S9), thus rendering regional differences in selection constraints an unlikely explanation for the large number of ohnologs experiencing loss of expression in one copy.…”

Section: Resultssupporting

confidence: 92%

Comparative regulomics supports pervasive selection on gene dosage following whole genome duplication

et al. 2021

View full text Add to dashboard Cite

Background Whole genome duplication (WGD) events have played a major role in eukaryotic genome evolution, but the consequence of these extreme events in adaptive genome evolution is still not well understood. To address this knowledge gap, we used a comparative phylogenetic model and transcriptomic data from seven species to infer selection on gene expression in duplicated genes (ohnologs) following the salmonid WGD 80–100 million years ago. Results We find rare cases of tissue-specific expression evolution but pervasive expression evolution affecting many tissues, reflecting strong selection on maintenance of genome stability following genome doubling. Ohnolog expression levels have evolved mostly asymmetrically, by diverting one ohnolog copy down a path towards lower expression and possible pseudogenization. Loss of expression in one ohnolog is significantly associated with transposable element insertions in promoters and likely driven by selection on gene dosage including selection on stoichiometric balance. We also find symmetric expression shifts, and these are associated with genes under strong evolutionary constraints such as ribosome subunit genes. This possibly reflects selection operating to achieve a gene dose reduction while avoiding accumulation of “toxic mutations”. Mechanistically, ohnolog regulatory divergence is dictated by the number of bound transcription factors in promoters, with transposable elements being one likely source of novel binding sites driving tissue-specific gains in expression. Conclusions Our results imply pervasive adaptive expression evolution following WGD to overcome the immediate challenges posed by genome doubling and to exploit the long-term genetic opportunities for novel phenotype evolution.

show abstract

Section: Resultssupporting

confidence: 92%

Comparative regulomics supports pervasive selection on gene dosage following whole genome duplication

et al. 2021

View full text Add to dashboard Cite

show abstract

“…Although Cyprinidae contains more polyploid species than any other vertebrate groups, the origin of polyploidy in cyprinid species is still unknown. C. carpio, the most studied species, is reported to be allotetraploid according to cytogenetic [44] and genomic [25,45] evidence. Tor species in Torini is also speculated to be allotetraploid based on ohnologue genealogy of Sox genes [33].…”

Section: (B) Genetic Basis Of Adaptive Potential In Polyploid Cyprinidaementioning

confidence: 99%

Substantially adaptive potential in polyploid cyprinid fishes: evidence from biogeographic, phylogenetic and genomic studies

Guo

2020

Proc. R. Soc. B.

View full text Add to dashboard Cite

Whole genome duplication (WGD) is commonly believed to play key roles in vertebrate evolution. However, nowadays polyploidy exists in a few fish, amphibian and reptile groups only, and seems to be an evolutionary dead end in vertebrates. We investigate the evolutionary significance of polyploidization in Cyprinidae—a fish family that contains more polyploid species than any other vertebrate group—with integrated biogeographic, phylogenetic and genomic analyses. First, polyploid species are found to be significantly frequent in areas of higher altitude and lower mean annual temperature compared with diploid species in Cyprinidae. Second, a polyploidy-related diversification rate shift is observed in Cyprinidae. This increased net diversification rate is only seen in three polyploid lineages, and other polyploid lineages have similar net diversification rate as well as diploid lineages in Cyprinidae. Interestingly, significant ‘lag times’ existed between polyploidization and radiation in Cyprinidae. Multiple polyploid lineages were established approximately 15 Ma through recurrent allopolyploidization events, but the net diversification rate did not start to increase until approximately 5 Ma—long after polyploidization events. Environmental changes associated with the continuous uplift of the Tibetan Plateau and climate change have probably promoted the initial establishment and subsequent radiation of polyploidy in Cyprinidae. Finally, the unique retention of duplicated genes in polyploid cyprinids adapted to harsh environments is found. Taken together, our results suggest that polyploidy in Cyprinidae is far more than an evolutionary dead end, but rather shows substantially adaptive potential. Polyploid cyprinids thus constitute an ideal model system for unveiling largely unexplored consequences of WGD in vertebrates, from genomic evolution to species diversification.

show abstract

“…Another challenge is that some cyprinid species have experienced genome duplications and polyploidization (Yang et al, 2015). Polyploids usually harbour more complex genome organization and gene content than diploids (Xu et al, 2019).…”

mentioning

confidence: 99%

Chromosome‐level genome assembly of a cyprinid fish Onychostoma macrolepis by integration of nanopore sequencing, Bionano and Hi‐C technology

Sun

Gao

Wang

et al. 2020

Molecular Ecology Resources

View full text Add to dashboard Cite

Onychostoma macrolepis is an emerging commercial cyprinid fish species. It is a model system for studies of sexual dimorphism and genome evolution. Here, we report the chromosome‐level assembly of the O.macrolepis genome obtained from the integration of nanopore long‐read sequencing with physical maps produced using Bionano and Hi‐C technology. A total of 87.9 Gb of nanopore sequence provided approximately 100‐fold coverage of the genome. The preliminary genome assembly was 883.2 Mb in size with a contig N50 size of 11.2 Mb. The 969 corrected contigs obtained from Bionano optical mapping were assembled into 853 scaffolds and produced an assembly of 886.5 Mb with a scaffold N50 of 16.5 Mb. Finally, using the Hi‐C data, 881.3 Mb (99.4% of genome) in 526 scaffolds were anchored and oriented in 25 chromosomes ranging in size from 25.27 to 56.49 Mb. In total, 24,770 protein‐coding genes were predicted in the genome, and ~96.85% of the genes were functionally annotated. The annotated assembly contains 93.3% complete genes from the BUSCO reference set. In addition, we identified 409 Mb (46.23% of the genome) of repetitive sequence, and 11,213 non‐coding RNAs, in the genome. Evolutionary analysis revealed that O. macrolepis diverged from common carp approximately 24.25 million years ago. The chromosomes of O. macrolepis showed an unambiguous correspondence to the chromosomes of zebrafish. The high‐quality genome assembled in this work provides a valuable genomic resource for further biological and evolutionary studies of O. macrolepis.

show abstract

The allotetraploid origin and asymmetrical genome evolution of the common carp Cyprinus carpio

Cited by 172 publications

References 68 publications

Comparative regulomics supports pervasive selection on gene dosage following whole genome duplication

Comparative regulomics supports pervasive selection on gene dosage following whole genome duplication

Substantially adaptive potential in polyploid cyprinid fishes: evidence from biogeographic, phylogenetic and genomic studies

Chromosome‐level genome assembly of a cyprinid fish Onychostoma macrolepis by integration of nanopore sequencing, Bionano and Hi‐C technology

Contact Info

Product

Resources

About