Whole Genome Incorporation and Epigenetic Stability in a Newly Synthetic Allopolyploid of Gynogenetic Gibel Carp

Abstract

Allopolyploidization plays an important role in speciation, and some natural or synthetic allopolyploid fishes have been extensively applied to aquaculture. Although genetic and epigenetic inheritance and variation associated with plant allopolyploids have been well documented, the relative research in allopolyploid animals is scarce. In this study, the genome constitution and DNA methylation inheritance in a newly synthetic allopolyploid of gynogenetic gibel carp were analyzed. The incorporation of a whole genome of paternal common carp sperm in the allopolyploid was confirmed by genomic in situ hybridization, chromosome localization of 45S rDNAs, and sequence comparison. Pooled sample-based methylation sensitive amplified polymorphism (MSAP) revealed that an overwhelming majority (98.82%) of cytosine methylation patterns in the allopolyploid were inherited from its parents of hexaploid gibel carp clone D and common carp. Compared to its parents, 11 DNA fragments in the allopolyploid were proved to be caused by interindividual variation, recombination, deletion, and mutation through individual sample-based MSAP and sequencing. Contrast to the rapid and remarkable epigenetic changes in most of analyzed neopolyploids, no cytosine methylation variation was detected in the gynogenetic allopolyploid. Therefore, the newly synthetic allopolyploid of gynogenetic gibel carp combined genomes from its parents and maintained genetic and epigenetic stability after its formation and subsequently seven successive gynogenetic generations. Our current results provide a paradigm for recurrent polyploidy consequences in the gynogenetic allopolyploid animals.

Regain of sex determination system and sexual reproduction ability in a synthetic octoploid male fish

“…Polyploids are very rare but have been reported in vertebrates including fish, amphibians and reptiles. Unisexual reproduction, such as parthenogenesis, gynogenesis and hybridogenesis, are often associated with polyploids, because the alternative unisexual reproduction can help polyploids to pass through meiosis barrier and reproduction bottleneck after polyploidy (Vandepoele et al, 2004;Gui and Zhou, 2010;Choleva and Janko, 2013;Avise, 2015;Zhou and Gui, 2017;Shao et al, 2018;Chen et al, 2020). However, the direct consequences of polyploidy on sex determination system and reproduction mode transition remain unknown in natural polyploids as it is very difficult to return to the past polyploidy events.…”

“…Significantly, two rounds of polyploidy events have been revealed to occur in the polyploid complex of Carassius, in which an earlier allopolyploidy at about 18.5 million years ago (Mya) has led to ancestral allotetraploid C. auratus with 100 chromosomes, and a recurrent autotriploidy at about 0.5 Mya has produced the extant hexaploid C. gibelio with about 150 chromosomes (Li et al, 2014). The tetraploid C. auratus have returned to normal diploid status that can reproduce by sexual reproduction, whereas hexaploid C. gibelio has also evolved to reproduce successfully via unisexual gynogenesis (Gui and Zhou, 2010;Li and Gui, 2018). In this study, we synthesized a group of artificial octoploids by incorporating one genome (50 chromosomes) of tetraploid C. auratus with sexual reproduction ability into the unisexual gynogenetic hexaploid C. gibelio, and found that the X/Y sex determination system from tetraploid C. auratus has been transferred into the synthetic octoploids.…”

“…The fragments specific to sex chromosome B22 of C. auratus amplified by PCR (Tables S6 and S7 in Supporting Information) were labeled by DIG-Nick Translation Mix (Roche, Switzerland), and the green fluorescent signals were obtained with fluorescein isothiocyanate (FITC) conjugated-DIG antibody (Roche, Switzerland). As reported previously, genomic in situ hybridization can display heterochromatin regions with repetitive sequences, such as centromeres, telomere, and sex chromosomes (Zhu and Gui, 2007;Shao et al, 2018). The genomic DNA of tetraploid C. auratus was labeled by Biotin-Nick Labeling System (Roche, Switzerland), and red fluorescent signals were stained by ExtraAvidin-Cy3 antibody (Sigma-Aldrich, USA).…”

“…Compared with the prevalence in plants, polyploid species are very rare in ver-tebrates (Soltis et al, 2015), which are documented only in some taxonomic lineages of fishes, amphibians, and reptiles (Comai, 2005;Session et al, 2016;Zhou and Gui, 2017). Generally, polyploids pass through the reproduction bottleneck via unisexual reproduction modes including parthenogenesis, gynogenesis and hybridogenesis (Vandepoele et al, 2004;Gui and Zhou, 2010;Choleva and Janko, 2013;Avise, 2015;Shao et al, 2018;Zhou et al, 2019;Wang et al, 2020), and evolve to a stable polyploid biotype via the subsequent diploidization process as the long-term strategies (Soltis et al, 2015;Wendel, 2015;Zhou et al, 2018). However, the direct consequences immediately following polyploidy on reproduction mode transition remains unclear.…”

Biotechnological innovation in genetic breeding and sustainable green development in Chinese aquaculture

“…随着对银鲫独特的多重生殖方式 [69,70] 以及其六倍体遗传背景对其他鱼类精子染色体组或染 色体片段的包容性和整合性的认识 [71] , 银鲫新品种纷 至沓来. 2008年, 本研究组 [44] 通过对不同克隆系交配 的子代应用分子标记辅助育种技术培育出核质杂种异 育银鲫"中科3号"; 2015年, 与中国水产科学研究院长 江水产研究所合作, 参与培育出融入有鲤精子全部染 色体的"长丰鲫" [72,73] ; 2018年, 基于基因组reads测序 深度比较策略和分子模块筛选鉴定, 培育出异育银鲫 "中科5号" [45,46] . 在人工雌核生殖技术方面, 1986年, 吴 清江等人 [74] 应用该技术结合性反转, 培育出可规模化 养殖的全雌鲤.…”