The chimeric genes in the hybrid lineage of Carassius auratus cuvieri(♀)×Carassius auratus red var.(♂)
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摘要
Hybridization can combine the genomes of different strains or species, which leads to changes of genotype and phenotype in the hybrids. In this study, we aimed to investigate the genetic variations of hybrids(WR-F1 and WR-F2) derived from the intraspecific hybridization of white crucian carp(Carassius auratus cuvieri, WCC, ♀) and red crucian carp(Carassius auratus red var., RCC, ♂). Here, we compared the orthologous genes in the liver transcriptomes of hybrids with those of WCC and RCC, and classified the orthologous genes into eight gene patterns within three categories(chimera, mutant, and biparental origin genes).The results revealed 19.04%, 4.17% chimeric genes and 6.90%, 5.05% mutations of orthologous genes in WR-F1 and WR-F2 respectively. Seventeen of twenty-three characterized genes(77%) were confirmed to be the chimeras at the genomic DNA level.The GO classification discovered that some chimeric and mutant genes were related to metabolic process, immune system and developmental process in WR-F1. Our results provide the new evidence that hybridization can combine the parental genomes,leading to changes in the genotype of the resultant hybrids. This is the first report on the formation of chimeric genes from fish intraspecific hybridization, which is potentially interesting from the context of both evolution and the genetic breeding of fish.
Hybridization can combine the genomes of different strains or species, which leads to changes of genotype and phenotype in the hybrids. In this study, we aimed to investigate the genetic variations of hybrids(WR-F1 and WR-F2) derived from the intraspecific hybridization of white crucian carp(Carassius auratus cuvieri, WCC, ♀) and red crucian carp(Carassius auratus red var., RCC, ♂). Here, we compared the orthologous genes in the liver transcriptomes of hybrids with those of WCC and RCC, and classified the orthologous genes into eight gene patterns within three categories(chimera, mutant, and biparental origin genes).The results revealed 19.04%, 4.17% chimeric genes and 6.90%, 5.05% mutations of orthologous genes in WR-F1 and WR-F2 respectively. Seventeen of twenty-three characterized genes(77%) were confirmed to be the chimeras at the genomic DNA level.The GO classification discovered that some chimeric and mutant genes were related to metabolic process, immune system and developmental process in WR-F1. Our results provide the new evidence that hybridization can combine the parental genomes,leading to changes in the genotype of the resultant hybrids. This is the first report on the formation of chimeric genes from fish intraspecific hybridization, which is potentially interesting from the context of both evolution and the genetic breeding of fish.
Hybridization can combine the genomes of different strains or species, which leads to changes of genotype and phenotype in the hybrids. In this study, we aimed to investigate the genetic variations of hybrids(WR-F1 and WR-F2) derived from the intraspecific hybridization of white crucian carp(Carassius auratus cuvieri, WCC, ♀) and red crucian carp(Carassius auratus red var., RCC, ♂). Here, we compared the orthologous genes in the liver transcriptomes of hybrids with those of WCC and RCC, and classified the orthologous genes into eight gene patterns within three categories(chimera, mutant, and biparental origin genes).The results revealed 19.04%, 4.17% chimeric genes and 6.90%, 5.05% mutations of orthologous genes in WR-F1 and WR-F2 respectively. Seventeen of twenty-three characterized genes(77%) were confirmed to be the chimeras at the genomic DNA level.The GO classification discovered that some chimeric and mutant genes were related to metabolic process, immune system and developmental process in WR-F1. Our results provide the new evidence that hybridization can combine the parental genomes,leading to changes in the genotype of the resultant hybrids. This is the first report on the formation of chimeric genes from fish intraspecific hybridization, which is potentially interesting from the context of both evolution and the genetic breeding of fish.
引文
Adams,K.L.,and Wendel,J.F.(2005).Polyploidy and genome evolution in plants.Curr Opin Plant Biol 8,135-141.
Anders,S.,and Huber,W.(2010).Differential expression analysis for sequence count data.Genome Biol 11,R106.
Arnheim,N.,Krystal,M.,Schmickel,R.,Wilson,G.,Ryder,O.,and Zimmer,E.(1980).Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes.Proc Natl Acad Sci USA 77,7323-7327.
Bao,J.,and Yan,W.(2012).Male germline control of transposable elements.Biol Reproduct 86,1-14.
Bartley,D.M.,Rana,K.,and Immink,A.J.(2000).The use of inter-specific hybrids in aquaculture and fisheries reviews in Fish.Rev Fish Biol Fisheries 10,325-337.
Blanc,G.,and Wolfe,K.H.(2004).Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes.Plant Cell 16,1667-1678.
Brenchley,R.,Spannagl,M.,Pfeifer,M.,Barker,G.L.A.,D’Amore,R.,Allen,A.M.,McKenzie,N.,Kramer,M.,Kerhornou,A.,Bolser,D.,et al.(2012).Analysis of the bread wheat genome using whole-genome shotgun sequencing.Nature 491,705-710.
Chen,Z.J.(2007).Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids.Annu Rev Plant Biol 58,377-406.
Collins,S.,and Bell,G.(2004).Phenotypic consequences of 1,000 generations of selection at elevated CO2in a green alga.Nature 431,566-569.
Cui,P.,Lin,Q.,Ding,F.,Hu,S.,and Yu,J.(2012).The transcript-centric mutations in human genomes.Genomics Proteomics Bioinformatics 10,11-22.
Danecek,P.,Auton,A.,Abecasis,G.,Albers,C.A.,Banks,E.,DePristo,M.A.,Handsaker,R.E.,Lunter,G.,Marth,G.T.,Sherry,S.T.,et al.(2011).The variant call format and VCFtools.Bioinformatics 27,2156-2158.
Delmas,S.,Shunburne,L.,Ngo,H.P.,and Allers,T.(2009).Mre11-Rad50promotes rapid repair of DNA damage in the polyploid archaeon Haloferax volcanii by restraining homologous recombination.PLoS Genet5,e1000552.
DePristo,M.A.,Banks,E.,Poplin,R.,Garimella,K.V.,Maguire,J.R.,Hartl,C.,Philippakis,A.A.,del Angel,G.,Rivas,M.A.,Hanna,M.,et al.(2011).A framework for variation discovery and genotyping using next-generation DNA sequencing data.Nat Genet 43,491-498.
Dion-C?té,A.M.,Renaut,S.,Normandeau,E.,and Bernatchez,L.(2014).RNA-seq reveals transcriptomic shock involving transposable elements reactivation in hybrids of young lake whitefish species.Mol Biol Evol31,1188-1199.
Fedoroff,N.V.(2012).Transposable elements,epigenetics,and genome evolution.Science 338,758-767.
Feldman,M.,Liu,B.,Segal,G.,Abbo,S.,Levy,A.A.,and Vega,J.M.(1997).Rapid elimination of low-copy DNA sequences in polyploid wheat:a possible mechanism for differentiation of homoeologous chromosomes.Genetics 147,1381-1387.
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Kenton,A.,Parokonny,A.S.,Gleba,Y.Y.,and Bennett,M.D.(1993).Characterization of the Nicotiana tabacum L.genome by molecular cytogenetics.Mol Genet Genomics 240,159-169.
Kobayashi,J.,Iwabuchi,K.,Miyagawa,K.,Sonoda,E.,Suzuki,K.,Takata,M.,and Tauchi,H.(2008).Current topics in DNA double-strand break repair.J Radiat Res 49,93-103.
Koyama,H.,Ito,T.,Nakanishi,T.,and Sekimizu,K.(2007).Stimulation of RNA polymerase II transcript cleavage activity contributes to maintain transcriptional fidelity in yeast.Genes Cells 12,547-559.
Levin,H.L.,and Moran,J.V.(2011).Dynamic interactions between transposable elements and their hosts.Nat Rev Genet 12,615-627.
Li,H.,and Durbin,R.(2009).Fast and accurate short read alignment with Burrows-Wheeler transform.Bioinformatics 25,1754-1760.
Li,H.,Handsaker,B.,Wysoker,A.,Fennell,T.,Ruan,J.,Homer,N.,Marth,G.,Abecasis,G.,Durbin,R.,and Durbin,R.(2009).The sequence alignment/map format and SAMtools.Bioinformatics 25,2078-2079.
Li,L.,Zhong,Z.Z.,Zeng,M.,Liu,S.J.,Zhou,Y.,Xiao,J.,Wang,J.,and Liu,Y.(2013).Comparative analysis of intermuscular bones in fish of different ploidies.Sci China Life Sci 56,341-350.
Liu,S.J.(2010).Distant hybridization leads to different ploidy fishes.Sci China Life Sci 53,416-425.
Liu,S.,Liu,Y.,Zhou,G.,Zhang,X.,Luo,C.,Feng,H.,He,X.,Zhu,G.,and Yang,H.(2001).The formation of tetraploid stocks of red crucian carp×common carp hybrids as an effect of interspecific hybridization.Aquaculture 192,171-186.
Liu,S.,Qin,Q.,Xiao,J.,Lu,W.,Shen,J.,Li,W.,Liu,J.,Duan,W.,Zhang,C.,Tao,M.,et al.(2007).The formation of the polyploid hybrids from different subfamily fish crossings and its evolutionary significance.Genetics 176,1023-1034.
Liu,S.,Luo,J.,Chai,J.,Ren,L.,Zhou,Y.,Huang,F.,Liu,X.,Chen,Y.,Zhang,C.,Tao,M.,et al.(2016).Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish×common carp cross.Proc Natl Acad Sci USA 113,1327-1332.
Lopez,F.,Estève,J.P.,Buscail,L.,Delesque,N.,Saint-Laurent,N.,Thé-veniau,M.,Nahmias,C.,Vaysse,N.,and Susini,C.(1997).The tyrosine phosphatase SHP-1 associates with the sst2 somatostatin receptor and is an essential component of sst2-mediated inhibitory growth signaling.J Biol Chem 272,24448-24454.
Madlung,A.,Tyagi,A.P.,Watson,B.,Jiang,H.,Kagochi,T.,Doerge,R.W.,Martienssen,R.,and Comai,L.(2005).Genomic changes in synthetic Arabidopsis polyploids.Plant J 41,221-230.
Mallet,J.(2007).Hybrid speciation.Nature 446,279-283.
McKenna,A.,Hanna,M.,Banks,E.,Sivachenko,A.,Cibulskis,K.,Kernytsky,A.,Garimella,K.,Altshuler,D.,Gabriel,S.,Daly,M.,et al.(2010).The Genome Analysis Toolkit:a MapReduce framework for analyzing next-generation DNA sequencing data.Genome Res 20,1-297-1303.
Nei,M.,and Nozawa,M.(2011).Roles of mutation and selection in speciation:from hugo de vries to the modern genomic era.Genome Biol Evol 3,812-829.
Ozkan,H.,Levy,A.A.,and Feldman,M.(2001).Allopolyploidy-induced rapid genome evolution in the wheat(Aegilops-Triticum)group.Plant Cell 13,1735-1747.
Qin,Q.,He,W.,Liu,S.,Wang,J.,Xiao,J.,and Liu,Y.(2010).Analysis of5S rDNA organization and variation in polyploid hybrids from crosses of different fish subfamilies Journal of experimental zoology Part B.Mol Dev Evol 314,403-411.
Qin,Q.,Wang,J.,Hu,M.,Huang,S.,and Liu,S.(2016).Autotriploid origin of Carassius auratus as revealed by chromosomal locus analysis.Sci China Life Sci 59,622-626.
Reeb,P.D.,and Steibel,J.P.(2013).Evaluating statistical analysis models for RNA sequencing experiments.Front Genet 4,178.
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Arnheim,N.,Krystal,M.,Schmickel,R.,Wilson,G.,Ryder,O.,and Zimmer,E.(1980).Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes.Proc Natl Acad Sci USA 77,7323-7327.
Bao,J.,and Yan,W.(2012).Male germline control of transposable elements.Biol Reproduct 86,1-14.
Bartley,D.M.,Rana,K.,and Immink,A.J.(2000).The use of inter-specific hybrids in aquaculture and fisheries reviews in Fish.Rev Fish Biol Fisheries 10,325-337.
Blanc,G.,and Wolfe,K.H.(2004).Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes.Plant Cell 16,1667-1678.
Brenchley,R.,Spannagl,M.,Pfeifer,M.,Barker,G.L.A.,D’Amore,R.,Allen,A.M.,McKenzie,N.,Kramer,M.,Kerhornou,A.,Bolser,D.,et al.(2012).Analysis of the bread wheat genome using whole-genome shotgun sequencing.Nature 491,705-710.
Chen,Z.J.(2007).Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids.Annu Rev Plant Biol 58,377-406.
Collins,S.,and Bell,G.(2004).Phenotypic consequences of 1,000 generations of selection at elevated CO2in a green alga.Nature 431,566-569.
Cui,P.,Lin,Q.,Ding,F.,Hu,S.,and Yu,J.(2012).The transcript-centric mutations in human genomes.Genomics Proteomics Bioinformatics 10,11-22.
Danecek,P.,Auton,A.,Abecasis,G.,Albers,C.A.,Banks,E.,DePristo,M.A.,Handsaker,R.E.,Lunter,G.,Marth,G.T.,Sherry,S.T.,et al.(2011).The variant call format and VCFtools.Bioinformatics 27,2156-2158.
Delmas,S.,Shunburne,L.,Ngo,H.P.,and Allers,T.(2009).Mre11-Rad50promotes rapid repair of DNA damage in the polyploid archaeon Haloferax volcanii by restraining homologous recombination.PLoS Genet5,e1000552.
DePristo,M.A.,Banks,E.,Poplin,R.,Garimella,K.V.,Maguire,J.R.,Hartl,C.,Philippakis,A.A.,del Angel,G.,Rivas,M.A.,Hanna,M.,et al.(2011).A framework for variation discovery and genotyping using next-generation DNA sequencing data.Nat Genet 43,491-498.
Dion-C?té,A.M.,Renaut,S.,Normandeau,E.,and Bernatchez,L.(2014).RNA-seq reveals transcriptomic shock involving transposable elements reactivation in hybrids of young lake whitefish species.Mol Biol Evol31,1188-1199.
Fedoroff,N.V.(2012).Transposable elements,epigenetics,and genome evolution.Science 338,758-767.
Feldman,M.,Liu,B.,Segal,G.,Abbo,S.,Levy,A.A.,and Vega,J.M.(1997).Rapid elimination of low-copy DNA sequences in polyploid wheat:a possible mechanism for differentiation of homoeologous chromosomes.Genetics 147,1381-1387.
Flicek,P.,Amode,MR.,Barrell,D.,Beal,K.,Billis K.,Brent,S.,CarvalhoSilva,D.,Clapham,P.,Coates,G.,Fitzgerald,S.,et al.(2013).Ensembl2014.Nucleic Acids Res 41,D49-D55.
Gaeta,R.T.,Pires,J.C.,Iniguez-Luy,F.,Leon,E.,and Osborn,T.C.(2007).Genomic changes in resynthesized brassica napus and their effect on gene expression and phenotype.Plant Cell 19,3403-3417.
Galili,G.,Levy,A.A.,and Feldman,M.(1986).Gene-dosage compensation of endosperm proteins in hexaploid wheat Triticum aestivum.Proc Natl Acad Sci USA 83,6524-6528.
Hall,T.A.(1999).BioEdit:a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT.Nucl Acids Symp Ser 41,95-98.
Hegarty,M.J.,Abbott,R.J.,and Hiscock,S.J.(2012).Allopolyploid Speciation in Action:The Origins and Origins and Evolution of Senecio cambrensis.(Berlin:Springer Berlin Heidelberg),pp.245-270.
Hu,W.,Timmermans,M.C.,and Messing,J.(1998).Interchromosomal recombination in Zea mays.Genetics 150,1229-1237.
Huang,J.,Huen,M.S.Y.,Kim,H.,Leung,C.C.Y.,Glover,J.N.M.,Yu,X.,and Chen,J.(2009).RAD18 transmits DNA damage signalling to elicit homologous recombination repair.Nat Cell Biol 11,592-603.
Kanehisa,M.,Araki,M.,Goto,S.,Hattori,M.,Hirakawa,M.,Itoh,M.,Katayama,T.,Kawashima,S.,Okuda,S.,Tokimatsu,T.,et al.(2008).KEGG for linking genomes to life and the environment.Nucleic Acids Res 36,D480-D484.
Kenton,A.,Parokonny,A.S.,Gleba,Y.Y.,and Bennett,M.D.(1993).Characterization of the Nicotiana tabacum L.genome by molecular cytogenetics.Mol Genet Genomics 240,159-169.
Kobayashi,J.,Iwabuchi,K.,Miyagawa,K.,Sonoda,E.,Suzuki,K.,Takata,M.,and Tauchi,H.(2008).Current topics in DNA double-strand break repair.J Radiat Res 49,93-103.
Koyama,H.,Ito,T.,Nakanishi,T.,and Sekimizu,K.(2007).Stimulation of RNA polymerase II transcript cleavage activity contributes to maintain transcriptional fidelity in yeast.Genes Cells 12,547-559.
Levin,H.L.,and Moran,J.V.(2011).Dynamic interactions between transposable elements and their hosts.Nat Rev Genet 12,615-627.
Li,H.,and Durbin,R.(2009).Fast and accurate short read alignment with Burrows-Wheeler transform.Bioinformatics 25,1754-1760.
Li,H.,Handsaker,B.,Wysoker,A.,Fennell,T.,Ruan,J.,Homer,N.,Marth,G.,Abecasis,G.,Durbin,R.,and Durbin,R.(2009).The sequence alignment/map format and SAMtools.Bioinformatics 25,2078-2079.
Li,L.,Zhong,Z.Z.,Zeng,M.,Liu,S.J.,Zhou,Y.,Xiao,J.,Wang,J.,and Liu,Y.(2013).Comparative analysis of intermuscular bones in fish of different ploidies.Sci China Life Sci 56,341-350.
Liu,S.J.(2010).Distant hybridization leads to different ploidy fishes.Sci China Life Sci 53,416-425.
Liu,S.,Liu,Y.,Zhou,G.,Zhang,X.,Luo,C.,Feng,H.,He,X.,Zhu,G.,and Yang,H.(2001).The formation of tetraploid stocks of red crucian carp×common carp hybrids as an effect of interspecific hybridization.Aquaculture 192,171-186.
Liu,S.,Qin,Q.,Xiao,J.,Lu,W.,Shen,J.,Li,W.,Liu,J.,Duan,W.,Zhang,C.,Tao,M.,et al.(2007).The formation of the polyploid hybrids from different subfamily fish crossings and its evolutionary significance.Genetics 176,1023-1034.
Liu,S.,Luo,J.,Chai,J.,Ren,L.,Zhou,Y.,Huang,F.,Liu,X.,Chen,Y.,Zhang,C.,Tao,M.,et al.(2016).Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish×common carp cross.Proc Natl Acad Sci USA 113,1327-1332.
Lopez,F.,Estève,J.P.,Buscail,L.,Delesque,N.,Saint-Laurent,N.,Thé-veniau,M.,Nahmias,C.,Vaysse,N.,and Susini,C.(1997).The tyrosine phosphatase SHP-1 associates with the sst2 somatostatin receptor and is an essential component of sst2-mediated inhibitory growth signaling.J Biol Chem 272,24448-24454.
Madlung,A.,Tyagi,A.P.,Watson,B.,Jiang,H.,Kagochi,T.,Doerge,R.W.,Martienssen,R.,and Comai,L.(2005).Genomic changes in synthetic Arabidopsis polyploids.Plant J 41,221-230.
Mallet,J.(2007).Hybrid speciation.Nature 446,279-283.
McKenna,A.,Hanna,M.,Banks,E.,Sivachenko,A.,Cibulskis,K.,Kernytsky,A.,Garimella,K.,Altshuler,D.,Gabriel,S.,Daly,M.,et al.(2010).The Genome Analysis Toolkit:a MapReduce framework for analyzing next-generation DNA sequencing data.Genome Res 20,1-297-1303.
Nei,M.,and Nozawa,M.(2011).Roles of mutation and selection in speciation:from hugo de vries to the modern genomic era.Genome Biol Evol 3,812-829.
Ozkan,H.,Levy,A.A.,and Feldman,M.(2001).Allopolyploidy-induced rapid genome evolution in the wheat(Aegilops-Triticum)group.Plant Cell 13,1735-1747.
Qin,Q.,He,W.,Liu,S.,Wang,J.,Xiao,J.,and Liu,Y.(2010).Analysis of5S rDNA organization and variation in polyploid hybrids from crosses of different fish subfamilies Journal of experimental zoology Part B.Mol Dev Evol 314,403-411.
Qin,Q.,Wang,J.,Hu,M.,Huang,S.,and Liu,S.(2016).Autotriploid origin of Carassius auratus as revealed by chromosomal locus analysis.Sci China Life Sci 59,622-626.
Reeb,P.D.,and Steibel,J.P.(2013).Evaluating statistical analysis models for RNA sequencing experiments.Front Genet 4,178.
Rieseberg,L.H.(2001).Chromosomal rearrangements and speciation.Trends Ecol Evol 16,351-358.
Rogers,R.L.,Bedford,T.,and Hartl,D.L.(2009).Formation and longevity of chimeric and duplicate genes in Drosophila melanogaster.Genetics181,313-322.
Schnable,J.C.,Springer,N.M.,and Freeling,M.(2011).Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss.Proc Natl Acad Sci USA 108,4069-4074.
Shapiro,J.A.(2005).A 21st century view of evolution:genome system architecture,repetitive DNA,and natural genetic engineering.Gene345,91-100.
Soltis,D.E.,and Soltis,P.S.(1995).The dynamic nature of polyploid genomes.Proc Natl Acad Sci USA 92,8089-8091.
Stelkens,R.,and Seehausen,O.(2009).Genetic distance between species predicts novel trait expression in their hybrids.Evolution 63,884-897.
Van,G.A.,Carneiro,M.O.,Hartl,C.,et al.(2013).From FastQ data to high confidence variant calls:the Genome Analysis Toolkit best practices pipeline.Curr Protocols Bioinform 43,11-33.
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