Parallel subgenome structure and divergent expression evolution of allo-tetraploid common carp and goldfish

• Published in: Nature genetics Vol. 53; no. 10; pp. 1493 - 1503
• Main Authors: Li, Jiong-Tang, Wang, Qi, Huang Yang, Mei-Di, Li, Qing-Song, Cui, Ming-Shu, Dong, Zai-Jie, Wang, Hong-Wei, Yu, Ju-Hua, Zhao, Yu-Jie, Yang, Chen-Ru, Wang, Ya-Xin, Sun, Xiao-Qing, Zhang, Yan, Zhao, Ran, Jia, Zhi-Ying, Wang, Xi-Yin
• Format: Journal Article
• Language: English
• Published: New York Nature Publishing Group US 01.10.2021; Nature Publishing Group
• Subjects: 38; 45; 631/208/199; 631/208/212; 631/601; Agriculture; Allopolyploid; Alternative Splicing - genetics; Animal Genetics and Genomics; Animals; Annotations; Base Sequence; Biomedical and Life Sciences; Biomedicine; Cancer Research; Carassius auratus; Carp; Carps - genetics; Chromosomes; Coexistence; Compensation; Cyprinus carpio; Diploids; Divergence; Divergent evolution; Dosage compensation; Ecotypes; Evolution; Evolution, Molecular; Gene Expression Regulation; Gene Function; Genes; Genetic aspects; Genetic research; Genetic Variation; Genome; Genomes; Goldfish; Goldfish - genetics; Homogeneity; Human Genetics; Karyotype; Likelihood Functions; Molecular Sequence Annotation; Natural history; Phylogenetics; Phylogeny; Proteins; Selection, Genetic; Species Specificity; Splicing; Structure; Survival; Synteny; Synteny - genetics; Tetraploidy; Zebrafish; China
• ISSN: 1061-4036; 1546-1718; 1546-1718
• DOI: 10.1038/s41588-021-00933-9

How two subgenomes in allo-tetraploids adapt to coexistence and coordinate through structure and expression evolution requires extensive studies. In the present study, we report an improved genome assembly of allo-tetraploid common carp, an updated genome annotation of allo-tetraploid goldfish and the chromosome-scale assemblies of a progenitor-like diploid Puntius tetrazona and an outgroup diploid Paracanthobrama guichenoti . Parallel subgenome structure evolution in the allo-tetraploids was featured with equivalent chromosome components, higher protein identities, similar transposon divergence and contents, homoeologous exchanges, better synteny level, strong sequence compensation and symmetric purifying selection. Furthermore, we observed subgenome expression divergence processes in the allo-tetraploids, including inter-/intrasubgenome trans- splicing events, expression dominance, decreased expression levels, dosage compensation, stronger expression correlation, dynamic functionalization and balancing of differential expression. The potential disorders introduced by different progenitors in the allo-tetraploids were hypothesized to be alleviated by increasing structural homogeneity and performing versatile expression processes. Resequencing three common carp strains revealed two major ecotypes and uncovered candidate genes relevant to growth and survival rate. Genomic analysis of allo-tetraploid common carp and goldfish identifies parallel subgenome structure and divergent expression processes.