Symmetric subgenomes and balanced homoeolog expression stabilize the establishment of allopolyploidy in cyprinid fish
Abstract Background Interspecific postzygotic reproduction isolation results from large genetic divergence between the subgenomes of established hybrids. Polyploidization immediately after hybridization may reset patterns of homologous chromosome pairing and ameliorate deleterious genomic incompatib...
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BMC
2022-09-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-022-01401-4 |
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| author | Li Ren Xin Gao Jialin Cui Chun Zhang He Dai Mengxue Luo Shaofang He Qinbo Qin Kaikun Luo Min Tao Jun Xiao Jing Wang Hong Zhang Xueyin Zhang Yi Zhou Jing Wang Xin Zhao Guiming Liu Guoliang Wang Linhe Huo Shi Wang Fangzhou Hu Rurong Zhao Rong Zhou Yude Wang Qinfeng Liu Xiaojing Yan Chang Wu Conghui Yang Chenchen Tang Wei Duan Shaojun Liu |
| author_facet | Li Ren Xin Gao Jialin Cui Chun Zhang He Dai Mengxue Luo Shaofang He Qinbo Qin Kaikun Luo Min Tao Jun Xiao Jing Wang Hong Zhang Xueyin Zhang Yi Zhou Jing Wang Xin Zhao Guiming Liu Guoliang Wang Linhe Huo Shi Wang Fangzhou Hu Rurong Zhao Rong Zhou Yude Wang Qinfeng Liu Xiaojing Yan Chang Wu Conghui Yang Chenchen Tang Wei Duan Shaojun Liu |
| author_sort | Li Ren |
| collection | DOAJ |
| description | Abstract Background Interspecific postzygotic reproduction isolation results from large genetic divergence between the subgenomes of established hybrids. Polyploidization immediately after hybridization may reset patterns of homologous chromosome pairing and ameliorate deleterious genomic incompatibility between the subgenomes of distinct parental species in plants and animals. However, the observation that polyploidy is less common in vertebrates raises the question of which factors restrict its emergence. Here, we perform analyses of the genome, epigenome, and gene expression in the nascent allotetraploid lineage (2.95 Gb) derived from the intergeneric hybridization of female goldfish (Carassius auratus, 1.49 Gb) and male common carp (Cyprinus carpio, 1.42 Gb), to shed light on the changes leading to the stabilization of hybrids. Results We firstly identify the two subgenomes derived from the parental lineages of goldfish and common carp. We find variable unequal homoeologous recombination in somatic and germ cells of the intergeneric F1 and allotetraploid (F22 and F24) populations, reflecting high plasticity between the subgenomes, and rapidly varying copy numbers between the homoeolog genes. We also find dynamic changes in transposable elements accompanied by genome merger and duplication in the allotetraploid lineage. Finally, we observe the gradual decreases in cis-regulatory effects and increases in trans-regulatory effects along with the allotetraploidization, which contribute to increases in the symmetrical homoeologous expression in different tissues and developmental stages, especially in early embryogenesis. Conclusions Our results reveal a series of changes in transposable elements, unequal homoeologous recombination, cis- and trans-regulations (e.g. DNA methylation), and homoeologous expression, suggesting their potential roles in mediating adaptive stabilization of regulatory systems of the nascent allotetraploid lineage. The symmetrical subgenomes and homoeologous expression provide a novel way of balancing genetic incompatibilities, providing a new insight into the early stages of allopolyploidization in vertebrate evolution. |
| first_indexed | 2024-04-11T21:13:24Z |
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| id | doaj.art-e53e170d80de457c89d8e20cfd3a9e10 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-11T21:13:24Z |
| publishDate | 2022-09-01 |
| publisher | BMC |
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| series | BMC Biology |
| spelling | doaj.art-e53e170d80de457c89d8e20cfd3a9e102022-12-22T04:02:57ZengBMCBMC Biology1741-70072022-09-0120111710.1186/s12915-022-01401-4Symmetric subgenomes and balanced homoeolog expression stabilize the establishment of allopolyploidy in cyprinid fishLi Ren0Xin Gao1Jialin Cui2Chun Zhang3He Dai4Mengxue Luo5Shaofang He6Qinbo Qin7Kaikun Luo8Min Tao9Jun Xiao10Jing Wang11Hong Zhang12Xueyin Zhang13Yi Zhou14Jing Wang15Xin Zhao16Guiming Liu17Guoliang Wang18Linhe Huo19Shi Wang20Fangzhou Hu21Rurong Zhao22Rong Zhou23Yude Wang24Qinfeng Liu25Xiaojing Yan26Chang Wu27Conghui Yang28Chenchen Tang29Wei Duan30Shaojun Liu31State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityBiomarker Technologies CorporationState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityWuhan Carbon Code Biotechnologies CorporationState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityBiomarker Technologies CorporationBeijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry SciencesBeijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry SciencesBeijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry SciencesBeijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry SciencesState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityAbstract Background Interspecific postzygotic reproduction isolation results from large genetic divergence between the subgenomes of established hybrids. Polyploidization immediately after hybridization may reset patterns of homologous chromosome pairing and ameliorate deleterious genomic incompatibility between the subgenomes of distinct parental species in plants and animals. However, the observation that polyploidy is less common in vertebrates raises the question of which factors restrict its emergence. Here, we perform analyses of the genome, epigenome, and gene expression in the nascent allotetraploid lineage (2.95 Gb) derived from the intergeneric hybridization of female goldfish (Carassius auratus, 1.49 Gb) and male common carp (Cyprinus carpio, 1.42 Gb), to shed light on the changes leading to the stabilization of hybrids. Results We firstly identify the two subgenomes derived from the parental lineages of goldfish and common carp. We find variable unequal homoeologous recombination in somatic and germ cells of the intergeneric F1 and allotetraploid (F22 and F24) populations, reflecting high plasticity between the subgenomes, and rapidly varying copy numbers between the homoeolog genes. We also find dynamic changes in transposable elements accompanied by genome merger and duplication in the allotetraploid lineage. Finally, we observe the gradual decreases in cis-regulatory effects and increases in trans-regulatory effects along with the allotetraploidization, which contribute to increases in the symmetrical homoeologous expression in different tissues and developmental stages, especially in early embryogenesis. Conclusions Our results reveal a series of changes in transposable elements, unequal homoeologous recombination, cis- and trans-regulations (e.g. DNA methylation), and homoeologous expression, suggesting their potential roles in mediating adaptive stabilization of regulatory systems of the nascent allotetraploid lineage. The symmetrical subgenomes and homoeologous expression provide a novel way of balancing genetic incompatibilities, providing a new insight into the early stages of allopolyploidization in vertebrate evolution.https://doi.org/10.1186/s12915-022-01401-4PolyploidHybridizationGenomic recombinationCis- and trans- regulationFish |
| spellingShingle | Li Ren Xin Gao Jialin Cui Chun Zhang He Dai Mengxue Luo Shaofang He Qinbo Qin Kaikun Luo Min Tao Jun Xiao Jing Wang Hong Zhang Xueyin Zhang Yi Zhou Jing Wang Xin Zhao Guiming Liu Guoliang Wang Linhe Huo Shi Wang Fangzhou Hu Rurong Zhao Rong Zhou Yude Wang Qinfeng Liu Xiaojing Yan Chang Wu Conghui Yang Chenchen Tang Wei Duan Shaojun Liu Symmetric subgenomes and balanced homoeolog expression stabilize the establishment of allopolyploidy in cyprinid fish BMC Biology Polyploid Hybridization Genomic recombination Cis- and trans- regulation Fish |
| title | Symmetric subgenomes and balanced homoeolog expression stabilize the establishment of allopolyploidy in cyprinid fish |
| title_full | Symmetric subgenomes and balanced homoeolog expression stabilize the establishment of allopolyploidy in cyprinid fish |
| title_fullStr | Symmetric subgenomes and balanced homoeolog expression stabilize the establishment of allopolyploidy in cyprinid fish |
| title_full_unstemmed | Symmetric subgenomes and balanced homoeolog expression stabilize the establishment of allopolyploidy in cyprinid fish |
| title_short | Symmetric subgenomes and balanced homoeolog expression stabilize the establishment of allopolyploidy in cyprinid fish |
| title_sort | symmetric subgenomes and balanced homoeolog expression stabilize the establishment of allopolyploidy in cyprinid fish |
| topic | Polyploid Hybridization Genomic recombination Cis- and trans- regulation Fish |
| url | https://doi.org/10.1186/s12915-022-01401-4 |
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