Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross

Abstract

Polyploidy is much rarer in animals than in plants but it is not known why. The outcome of combining two genomes in vertebrates remains unpredictable, especially because polyploidization seldom shows positive effects and more often results in lethal consequences because viable gametes fail to form during meiosis. Fortunately, the goldfish (maternal) × common carp (paternal) hybrids have reproduced successfully up to generation 22, and this hybrid lineage permits an investigation into the genomics of hybridization and tetraploidization. The first two generations of these hybrids are diploids, and subsequent generations are tetraploids. Liver transcriptomes from four generations and their progenitors reveal chimeric genes (>9%) and mutations of orthologous genes. Characterizations of 18 randomly chosen genes from genomic DNA and cDNA confirm the chimera. Some of the chimeric and differentially expressed genes relate to mutagenesis, repair, and cancer-related pathways in 2nF 1 . Erroneous DNA excision between homologous parental genes may drive the high percentage of chimeric genes, or even more potential mechanisms may result in this phenomenon. Meanwhile, diploid offspring show paternal-biased expression, yet tetraploids show maternal-biased expression. These discoveries reveal that fast and unstable changes are mainly deleterious at the level of transcriptomes although some offspring still survive their genomic abnormalities. In addition, the synthetic effect of genome shock might have resulted in greatly reduced viability of 2nF 2 hybrid offspring. The goldfish × common carp hybrids constitute an ideal system for unveiling the consequences of intergenomic interactions in hybrid vertebrate genomes and their fertility.allopolyploidization | chimeric genes | transcriptomes | sequence validation | vertebrate P olyploidization is much rarer in vertebrates than in plants, and the reasons for this difference remain a mystery (1-3). Traditional explanations include barriers to sex determination, physiological and developmental constraints (especially nuclearcytoplasmic interactions and related factors) (2, 3), and genome shock or dramatic genomic restructuring (2-4). One type of polyploidization, allopolyploidization, involves the genomes of two species. Hybridization, accompanied by polyploidization, triggers vast genetic and genomic imbalances, including abnormal quadrivalent chromosomal groups, dosage imbalances, a high rate of DNA mutations and combinations, and other non-Mendelian phenomena (5-7). The effects of these imbalances are usually deleterious and are rarely advantageous. Imbalances in many plant crops determine the fate of the allopolyploid offspring. Genomic changes immediately follow allopolyploidization. Various and SignificanceWhy is polyploidization rarer in animals than in plants? This question remains unanswered due to the absence of a suitable system in animals for studying instantaneous polyploidization and the crucial changes that immediately follow hybridization. RNA-seq analyses discover exte...

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

“…There was apparently only one autotetraploidization event that occurred at the common ancestor of salmonids approximate 80 Mya, while polypoloidization evolved independently on multiple occasions in Cyprinids, of which the common carp (Cyprinus carpio) and goldfish (Carassius sp.) appear to have experienced the latest allotetraploidization event before their divergence [13][14][15] , thus providing an excellent model system for investigating the initial allopolyploidization event in teleosts and understanding the evolutionary Green, yellow and red circles represent the teleost-specific whole genome duplication (Ts3R), salmonid-specific whole genome duplication (Ss4R) and carp-specific whole genome duplication (Cs4R), respectively. benefits for phenotypic plasticity, environmental adaptations and species radiation post the latest WGD.…”

Differential expression of HPG‐axis genes in autotetraploids derived from red crucian carp Carassius auratus red var., ♀ × blunt snout bream Megalobrama amblycephala, ♂

“…These results indicated that there was sequence divergence after autotetraploidization. Previous studies suggested that polyploid formation could induce various types of genomic changes (Chen & Pikaard, 1997;Ha et al, 2009;Kashkush et al, 2003;Leitch & Leitch, 2008;Liu et al, 2016a;Ozkan et al, 2001;Parisod et al, 2010;Qin et al, 2010Qin et al, , 2016aSong et al, 1995;Tate et al, 2006). Importantly, a variety of genomic changes has been shown to result in diploid-like chromosome pairing (Paterson et al, 2004;Soltis et al, 2009;Wendel, 2000;Wolfe, 2001).…”

Genetic identification of a newly synthetic allopolyploid strain with 206 chromosomes in polyploid gibel carp

“…Several types of allotetraploid gibel carp with over 200 chromosomes have been created in the past thirty years (Gui et al., a; Zhu & Gui, ; Xiao et al., ; Li, Liang et al., ; Liu, Sun, Zhang, Luo & Liu, ; Liu et al., ). In this study, a newly synthetic allopolyploid strain was identified to have 206 chromosomes, and the morphological and growth traits were evaluated (Figure ).…”