Lin Chen , Chengyu Li , Bijun Li , Xiaofan Zhou , Yulin Bai , Xiaoqing Zou , Zhixiong Zhou , Qian He , Baohua Chen , Mei Wang , Yaguo Xue , Zhou Jiang , Jianxin Feng , Tao Zhou , Zhanjiang Liu , Peng Xu
{"title":"Evolutionary divergence of subgenomes in common carp provides insights into speciation and allopolyploid success","authors":"Lin Chen , Chengyu Li , Bijun Li , Xiaofan Zhou , Yulin Bai , Xiaoqing Zou , Zhixiong Zhou , Qian He , Baohua Chen , Mei Wang , Yaguo Xue , Zhou Jiang , Jianxin Feng , Tao Zhou , Zhanjiang Liu , Peng Xu","doi":"10.1016/j.fmre.2023.06.011","DOIUrl":null,"url":null,"abstract":"<div><p>Hybridization and polyploidization have made great contributions to speciation, heterosis, and agricultural production within plants, but there is still limited understanding and utilization in animals. Subgenome structure and expression reorganization and cooperation post hybridization and polyploidization are essential for speciation and allopolyploid success. However, the mechanisms have not yet been comprehensively assessed in animals. Here, we produced a high-fidelity reference genome sequence for common carp, a typical allotetraploid fish species cultured worldwide. This genome enabled in-depth analysis of the evolution of subgenome architecture and expression responses. Most genes were expressed with subgenome biases, with a trend of transition from the expression of subgenome A during the early stages to that of subgenome B during the late stages of embryonic development. While subgenome A evolved more rapidly, subgenome B contributed to a greater level of expression during development and under stressful conditions. Stable dominant patterns for homoeologous gene pairs both during development and under thermal stress suggest a potential fixed heterosis in the allotetraploid genome. Preferentially expressing either copy of a homoeologous gene at higher levels to confer development and response to stress indicates the dominant effect of heterosis. The plasticity of subgenomes and their shifting of dominant expression during early development, and in response to stressful conditions, provide novel insights into the molecular basis of the successful speciation, evolution, and heterosis of the allotetraploid common carp.</p></div>","PeriodicalId":34602,"journal":{"name":"Fundamental Research","volume":null,"pages":null},"PeriodicalIF":6.2000,"publicationDate":"2024-05-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S2667325823001978/pdfft?md5=cb9ab4ed3299042173c1cac283a2419e&pid=1-s2.0-S2667325823001978-main.pdf","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Fundamental Research","FirstCategoryId":"1085","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S2667325823001978","RegionNum":3,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"Multidisciplinary","Score":null,"Total":0}
引用次数: 0
Abstract
Hybridization and polyploidization have made great contributions to speciation, heterosis, and agricultural production within plants, but there is still limited understanding and utilization in animals. Subgenome structure and expression reorganization and cooperation post hybridization and polyploidization are essential for speciation and allopolyploid success. However, the mechanisms have not yet been comprehensively assessed in animals. Here, we produced a high-fidelity reference genome sequence for common carp, a typical allotetraploid fish species cultured worldwide. This genome enabled in-depth analysis of the evolution of subgenome architecture and expression responses. Most genes were expressed with subgenome biases, with a trend of transition from the expression of subgenome A during the early stages to that of subgenome B during the late stages of embryonic development. While subgenome A evolved more rapidly, subgenome B contributed to a greater level of expression during development and under stressful conditions. Stable dominant patterns for homoeologous gene pairs both during development and under thermal stress suggest a potential fixed heterosis in the allotetraploid genome. Preferentially expressing either copy of a homoeologous gene at higher levels to confer development and response to stress indicates the dominant effect of heterosis. The plasticity of subgenomes and their shifting of dominant expression during early development, and in response to stressful conditions, provide novel insights into the molecular basis of the successful speciation, evolution, and heterosis of the allotetraploid common carp.
杂交和多倍体化对植物的物种演化、异交和农业生产做出了巨大贡献,但对动物的了解和利用仍然有限。杂交和多倍体化后的亚基因组结构和表达重组与合作对于物种演化和异源多倍体的成功至关重要。然而,这些机制尚未在动物中得到全面评估。在这里,我们为鲤鱼--一种典型的全球养殖的异源四倍体鱼类--制作了一个高保真参考基因组序列。通过该基因组可以深入分析亚基因组结构和表达反应的进化。大多数基因的表达具有亚基因组偏向,其表达趋势是从胚胎发育早期的亚基因组 A 过渡到晚期的亚基因组 B。虽然亚基因组 A 的进化更快,但亚基因组 B 在发育过程中和应激条件下的表达水平更高。同源基因对在发育过程中和热胁迫条件下的稳定显性模式表明,异源四倍体基因组中存在潜在的固定异质性。同源基因的任一拷贝在较高水平上的优先表达能促进发育并对胁迫做出反应,这表明异源基因的显性效应。亚基因组的可塑性及其在早期发育和应激条件下的优势表达转移,为了解异源四倍体鲤鱼成功的物种分化、进化和杂交的分子基础提供了新的视角。