Asymmetric expression of homoeologous genes contributes to dietary adaption of an allodiploid hybrid fish derived from Megalobrama amblycephala (♀) × Culter alburnus (♂)

Abstract Background Hybridization, which can quickly merge two or more divergent genomes and form new allopolyploids, is an important technique in fish genetic breeding. However, the merged subgenomes must adjust and coexist with one another in a single nucleus, which may cause subgenome interaction and dominance at the gene expression level and has been observed in some allopolyploid plants. In our previous studies, newly formed allodiploid hybrid fish derived from herbivorous Megalobrama amblycephala (♀) × carnivorous Culter alburnus (♂) had herbivorous characteristic. It is thus interesting to further characterize whether the subgenome interaction and dominance derive dietary adaptation of this hybrid fish. Results Differential expression, homoeolog expression silencing and bias were investigated in the hybrid fish after 70 days of adaptation to carnivorous and herbivorous diets. A total of 2.65 × 108 clean reads (74.06 Gb) from the liver and intestinal transcriptomes were mapped to the two parent genomes based on specific SNPs. A total of 2538 and 4385 differentially expressed homoeologous genes (DEHs) were identified in the liver and intestinal tissues between the two groups of fish, respectively, and these DEHs were highly enriched in fat digestion and carbon metabolism, amino acid metabolism and steroid biosynthesis. Furthermore, subgenome dominance were observed in tissues, with paternal subgenome was more dominant than maternal subgenome. Moreover, subgenome expression dominance controlled functional pathways in metabolism, disease, cellular processes, environment and genetic information processing during the two dietary adaptation processes. In addition, few but sturdy villi in the intestine, significant fat accumulation and a higher concentration of malondialdehyde in the liver were observed in fish fed carnivorous diet compared with fish fed herbivorous diet. Conclusions Our results indicated that diet drives phenotypic and genetic variation, and the asymmetric expression of homoeologous genes (including differential expression, expression silencing and bias) may play key roles in dietary adaptation of hybrid fish. Subgenome expression dominance may contribute to uncovering the mechanistic basis of heterosis and also provide perspectives for fish genetic breeding and application.

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The subgenomes show asymmetric expression of alleles in hybrid lineages of Megalobrama amblycephala × Culter alburnus

Genome Research ◽

10.1101/gr.249805.119 ◽

2019 ◽

Vol 29 (11) ◽

pp. 1805-1815 ◽

Cited By ~ 13

Author(s):

Li Ren ◽

Wuhui Li ◽

Qinbo Qin ◽

He Dai ◽

Fengming Han ◽

...

Keyword(s):

Megalobrama Amblycephala ◽

Culter Alburnus ◽

Asymmetric Expression

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Maternal effects shape the alternative splicing of parental alleles in reciprocal cross hybrids of Megalobrama amblycephala ´ Culter alburnus

10.21203/rs.2.10581/v5 ◽

2020 ◽

Author(s):

Li Ren ◽

Xiaojing Yan ◽

Xin Gao ◽

Jialin Cui ◽

Pengcheng Yan ◽

...

Keyword(s):

Alternative Splicing ◽

Mrna Expression ◽

Maternal Effects ◽

Reciprocal Cross ◽

Differentially Expressed ◽

Megalobrama Amblycephala ◽

Homoeologous Genes ◽

Morphogenetic Protein ◽

Illumina Data ◽

Culter Alburnus

Abstract Background : Maternal effects contribute to adaptive significance for shaping various phenotypes of many traits. Potential implications of maternal effects are the cause of expression diversity, but these effects on mRNA expression and alternative splicing (AS) have not been fully elucidated in hybrid animals. Results: Two reciprocal cross hybrids following hybridization of Megalobrama amblycephala (blunt snout bream, BSB) and Culter alburnus (topmouth culter, TC) were used as a model to investigate maternal effects. In a comparison of BSB- and TC- homoeolog expression from the two reciprocal cross hybrids, we identified 49–348 differentially expressed BSB-homoeologous genes and 54–354 differentially expressed TC-homoeologous genes. 2402, 2959, and 3418 AS events between the two reciprocal cross hybrids were detected in Illumina data of muscle, liver, and gonads, respectively. Moreover, 21,577 (TC-homoeologs) and 30,007 (BSB-homoeologs) AS events were found in the 20,131 homoeologous gene pairs of TBF3 based on PacBio data, while 30,561 (TC-homoeologs) and 30,305 (BSB-homoeologs) AS events were found in BTF3. These results further improve AS prediction at the homoeolog level. The various AS patterns in bmpr2a belonged to the bone morphogenetic protein family were selected as an AS model to investigate expression diversity and their potential effects to body shape traits.Conclusions: The distribution of differentially expressed genes and AS in BSB- and TC-subgenomes exhibited various changes between the two reciprocal cross hybrids, suggesting that maternal effects were the cause of expression diversity. These findings provide a novel insight into mRNA expression changes and AS under maternal effects in lower vertebrates.

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Maternal effects shape the alternative splicing of parental alleles in reciprocal cross hybrids of Megalobrama amblycephala x Culter alburnus

10.21203/rs.2.10581/v4 ◽

2020 ◽

Author(s):

Li Ren ◽

Xiaojing Yan ◽

Xin Gao ◽

Jialin Cui ◽

Pengcheng Yan ◽

...

Keyword(s):

Alternative Splicing ◽

Mrna Expression ◽

Maternal Effects ◽

Reciprocal Cross ◽

Differentially Expressed ◽

Megalobrama Amblycephala ◽

Homoeologous Genes ◽

Morphogenetic Protein ◽

Illumina Data ◽

Culter Alburnus

Abstract Background Maternal effects contribute to adaptive significance for shaping various phenotypes of many traits. Potential implications of maternal effects are the cause of expression diversity, but these effects on mRNA expression and alternative splicing (AS) have not been fully elucidated in hybrid animals. Results Two reciprocal cross hybrids following hybridization of Megalobrama amblycephala (blunt snout bream, BSB) and Culter alburnus (topmouth culter, TC) were used as a model to investigate maternal effects. In a comparison of BSB- and TC- homoeolog expression from the two reciprocal cross hybrids, we identified 49–348 differentially expressed BSB-homoeologous genes and 54–354 differentially expressed TC-homoeologous genes. 2402, 2959, and 3418 AS events between the two reciprocal cross hybrids were detected in Illumina data of muscle, liver, and gonads, respectively. Moreover, 21,577 (TC-homoeologs) and 30,007 (BSB-homoeologs) AS events were found in the 20,131 homoeologous gene pairs of TBF3 based on PacBio data, while 30,561 (TC-homoeologs) and 30,305 (BSB-homoeologs) AS events were found in BTF3. These results further improve AS prediction at the homoeolog level. The various AS patterns in bmpr2a belonged to the bone morphogenetic protein family were selected as an AS model to investigate expression diversity and their potential effects to body shape traits.Conclusions The distribution of differentially expressed genes and AS in BSB- and TC-subgenomes exhibited various changes between the two reciprocal cross hybrids, suggesting that maternal effects were the cause of expression diversity. These findings provide a novel insight into mRNA expression changes and AS under maternal effects in lower vertebrates.

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Maternal effects shape the alternative splicing of parental alleles in reciprocal cross hybrids of Megalobrama amblycephala x Culter alburnus

10.21203/rs.2.10581/v1 ◽

2019 ◽

Author(s):

Li Ren ◽

Xiaojing Yan ◽

Xin Gao ◽

Jialin Cui ◽

Pengcheng Yan ◽

...

Keyword(s):

Alternative Splicing ◽

Mrna Expression ◽

Maternal Effects ◽

Reciprocal Cross ◽

Differentially Expressed ◽

Megalobrama Amblycephala ◽

Homoeologous Gene ◽

Gene Pairs ◽

Homoeologous Genes ◽

Culter Alburnus

Abstract Background Maternal effects contribute to adaptive significance for shaping various phenotypes of many traits. Potential implications of maternal effects are the cause of expression diversity, but these effects on mRNA expression and alternative splicing (AS) have not been fully elucidated in hybrid animal. Results Two reciprocal cross hybrids following hybridization of Megalobrama amblycephala (blunt snout bream, BSB) and Culter alburnus (topmouth culter, TC) were used as a model to investigate maternal effects. In a comparison of BSB and TC homoeolog expression from the two reciprocal cross hybrids, we identified 49–347 differentially expressed BSB-homoeologous genes and 54–354 TC-homoeologous genes. 2402, 2959, and 3418 AS events between the two reciprocal cross hybrids were detected in Illumina data of muscle, liver, and gonads, respectively. Moreover, 21,577 (TC-homoeologs) and 30,007 (BSB-homoeologs) AS events were found in the 20,131 homoeologous gene pairs of TB F3 based on PacBio data, while 30,561 (TC-homoeologs) and 30,305 (BSB-homoeologs) AS events were found in BT F3 homoeologous gene pairs. These results further improve AS prediction at the homoeolog level. To analyze body shape traits, bmpr2a of the bone morphogenetic protein family was selected as an AS model to investigate expression diversity. Conclusions The distribution of differentially expressed genes and AS in BSB- and TC-subgenomes exhibited various changes between the two reciprocal cross hybrids, suggesting that maternal effects are the cause of expression diversity. These findings provide a novel insight into mRNA expression changes and AS under maternal effects in lower vertebrates.

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Diploid hybrid fish derived from the cross between female Bleeker’s yellow tail and male topmouth culter, two cyprinid fishes belonging to different subfamilies

BMC Genetics ◽

10.1186/s12863-019-0781-5 ◽

2019 ◽

Vol 20 (1) ◽

Cited By ~ 3

Author(s):

Shengnan Li ◽

Lihua Xie ◽

Jun Xiao ◽

Liujiao Yuan ◽

Tian Zhou ◽

...

Keyword(s):

5S Rdna ◽

Reproductive Traits ◽

Gonadal Development ◽

Diploid Hybrid ◽

Distant Hybridization ◽

High Quality ◽

Genetic Breeding ◽

Fertile Female ◽

Hybrid Fish ◽

Fish Genetic Breeding

Abstract Background Bleeker’s yellow tail (Xenocypris davidi Bleeker, YT) and topmouth culter (Culter alburnus Basilewsky, TC) are both famous and important economic freshwater fish in China. YT, a kind of omnivorous fish, has strong resistance. TC, a kind of carnivorous fish, has high-quality meat but poor resistance. Distant hybridization can integrate the advantages of both parents. There has been no previous report regarding hybrid fish derived from female YT × male TC. It is expected that hybridization of these two kinds of fish will result in F1 hybrids with improved characteristics, such as faster growth rate, stronger resistance, and high-quality meat, which are of great significance in fish genetic breeding. Results In this study, we investigated the main biological characteristics of diploid hybrid fish derived from female YT × male TC. The hybrids had an intermediate number of upper lateral line scales between those for YT and TC. The hybrids were diploids with 48 chromosomes and had the same karyotype formula as their parents. The hybrids generated variations in 5S rDNA (designated class IV: 212 bp) and lost specific 5S rDNA derived from the maternal parent (designated class II: 221 bp), which might be related to hybridization. In terms of reproductive traits, all the tested female hybrids exhibited normal gonadal development, and the two-year-old F1 females produced mature eggs. However, all the tested testes of the male hybrids could not produce mature sperm. It is possible that the hybrid lineage will be established by back-crossing the fertile female hybrids and their parents. Conclusions Obtaining a fertile female hybrid fish made the creation of a new type of fish possible, which was significant in fish genetic breeding.

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Maternal effects shape the alternative splicing of parental alleles in reciprocal cross hybrids of Megalobrama amblycephala x Culter alburnus

10.21203/rs.2.10581/v2 ◽

2019 ◽

Author(s):

Li Ren ◽

Xiaojing Yan ◽

Xin Gao ◽

Jialin Cui ◽

Wuhui Li ◽

...

Keyword(s):

Alternative Splicing ◽

Mrna Expression ◽

Maternal Effects ◽

Reciprocal Cross ◽

Differentially Expressed ◽

Megalobrama Amblycephala ◽

Homoeologous Gene ◽

Gene Pairs ◽

Homoeologous Genes ◽

Culter Alburnus

Abstract Abstract Background Maternal effects contribute to adaptive significance for shaping various phenotypes of many traits. Potential implications of maternal effects are the cause of expression diversity, but these effects on mRNA expression and alternative splicing (AS) have not been fully elucidated in hybrid animal. Results Two reciprocal cross hybrids following hybridization of Megalobrama amblycephala (blunt snout bream, BSB) and Culter alburnus (topmouth culter, TC) were used as a model to investigate maternal effects. In a comparison of BSB and TC homoeolog expression from the two reciprocal cross hybrids, we identified 49–347 differentially expressed BSB-homoeologous genes and 54–354 TC-homoeologous genes. 2402, 2959, and 3418 AS events between the two reciprocal cross hybrids were detected in Illumina data of muscle, liver, and gonads, respectively. Moreover, 21,577 (TC-homoeologs) and 30,007 (BSB-homoeologs) AS events were found in the 20,131 homoeologous gene pairs of TBF 3 based on PacBio data, while 30,561 (TC-homoeologs) and 30,305 (BSB-homoeologs) AS events were found in BTF 3 homoeologous gene pairs. These results further improve AS prediction at the homoeolog level. The various AS patterns in bmpr2a with belonged to the bone morphogenetic protein family was selected as an AS model to investigate expression diversity and their potential effects to body shape traits. Conclusions The distribution of differentially expressed genes and AS in BSB- and TC-subgenomes exhibited various changes between the two reciprocal cross hybrids, suggesting that maternal effects are the cause of expression diversity. These findings provide a novel insight into mRNA expression changes and AS under maternal effects in lower vertebrates.

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Maternal effects shape the alternative splicing of parental alleles in reciprocal cross hybrids of Megalobrama amblycephala x Culter alburnus

10.21203/rs.2.10581/v3 ◽

2020 ◽

Author(s):

Li Ren ◽

Xiaojing Yan ◽

Xin Gao ◽

Jialin Cui ◽

Pengcheng Yan ◽

...

Keyword(s):

Alternative Splicing ◽

Mrna Expression ◽

Maternal Effects ◽

Reciprocal Cross ◽

Differentially Expressed ◽

Megalobrama Amblycephala ◽

Homoeologous Genes ◽

Morphogenetic Protein ◽

Illumina Data ◽

Culter Alburnus

Abstract Background Maternal effects contribute to adaptive significance for shaping various phenotypes of many traits. Potential implications of maternal effects are the cause of expression diversity, but these effects on mRNA expression and alternative splicing (AS) have not been fully elucidated in hybrid animals. Results Two reciprocal cross hybrids following hybridization of Megalobrama amblycephala (blunt snout bream, BSB) and Culter alburnus (topmouth culter, TC) were used as a model to investigate maternal effects. In a comparison of BSB- and TC- homoeolog expression from the two reciprocal cross hybrids, we identified 49–348 differentially expressed BSB-homoeologous genes and 54–354 differentially expressed TC-homoeologous genes. 2402, 2959, and 3418 AS events between the two reciprocal cross hybrids were detected in Illumina data of muscle, liver, and gonads, respectively. Moreover, 21,577 (TC-homoeologs) and 30,007 (BSB-homoeologs) AS events were found in the 20,131 homoeologous gene pairs of TBF 3 based on PacBio data, while 30,561 (TC-homoeologs) and 30,305 (BSB-homoeologs) AS events were found in BTF 3 . These results further improve AS prediction at the homoeolog level. The various AS patterns in bmpr2a belonged to the bone morphogenetic protein family were selected as an AS model to investigate expression diversity and their potential effects to body shape traits. Conclusions The distribution of differentially expressed genes and AS in BSB- and TC-subgenomes exhibited various changes between the two reciprocal cross hybrids, suggesting that maternal effects were the cause of expression diversity. These findings provide a novel insight into mRNA expression changes and AS under maternal effects in lower vertebrates.

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