Structural variation during dog domestication: insights from gray wolf and dhole genomes
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摘要
Several processes like phenotypic evolution, disease susceptibility and environmental adaptations, which fashion the domestication of animals, are largely attributable to structural variations(SVs) in the genome.Here, we present high-quality draft genomes of the gray wolf(Canis lupus) and dhole(Cuon alpinus) with scaffold N50 of 6.04 Mb and 3.96 Mb, respectively. Sequence alignment comprising genomes of three canid species reveals SVs specific to the dog, particularly 16 315 insertions, 2565 deletions, 443 repeats, 16 inversions and 15 translocations. Functional annotation of the dog SVs associated with genes indicates their enrichments in energy metabolisms, neurological processes and immune systems. Interestingly, we identify and verify at population level an insertion fully covering a copy of the AKR1 B1(Aldo-Keto Reductase Family 1 Member B) transcript. Transcriptome analysis reveals a high level of expression of the new AKR1 B1 copy in the small intestine and liver, implying an increase in de novo fatty acid synthesis and antioxidant ability in dog compared to gray wolf, likely in response to dietary shifts during the agricultural revolution. For the first time, we report a comprehensive analysis of the evolutionary dynamics of SVs during the domestication step of dogs. Our findings demonstrate that retroposition can birth new genes to facilitate domestication, and affirm the importance of large-scale genomic variants in domestication studies.
Several processes like phenotypic evolution, disease susceptibility and environmental adaptations, which fashion the domestication of animals, are largely attributable to structural variations(SVs) in the genome.Here, we present high-quality draft genomes of the gray wolf(Canis lupus) and dhole(Cuon alpinus) with scaffold N50 of 6.04 Mb and 3.96 Mb, respectively. Sequence alignment comprising genomes of three canid species reveals SVs specific to the dog, particularly 16 315 insertions, 2565 deletions, 443 repeats, 16 inversions and 15 translocations. Functional annotation of the dog SVs associated with genes indicates their enrichments in energy metabolisms, neurological processes and immune systems. Interestingly, we identify and verify at population level an insertion fully covering a copy of the AKR1 B1(Aldo-Keto Reductase Family 1 Member B) transcript. Transcriptome analysis reveals a high level of expression of the new AKR1 B1 copy in the small intestine and liver, implying an increase in de novo fatty acid synthesis and antioxidant ability in dog compared to gray wolf, likely in response to dietary shifts during the agricultural revolution. For the first time, we report a comprehensive analysis of the evolutionary dynamics of SVs during the domestication step of dogs. Our findings demonstrate that retroposition can birth new genes to facilitate domestication, and affirm the importance of large-scale genomic variants in domestication studies.
Several processes like phenotypic evolution, disease susceptibility and environmental adaptations, which fashion the domestication of animals, are largely attributable to structural variations(SVs) in the genome.Here, we present high-quality draft genomes of the gray wolf(Canis lupus) and dhole(Cuon alpinus) with scaffold N50 of 6.04 Mb and 3.96 Mb, respectively. Sequence alignment comprising genomes of three canid species reveals SVs specific to the dog, particularly 16 315 insertions, 2565 deletions, 443 repeats, 16 inversions and 15 translocations. Functional annotation of the dog SVs associated with genes indicates their enrichments in energy metabolisms, neurological processes and immune systems. Interestingly, we identify and verify at population level an insertion fully covering a copy of the AKR1 B1(Aldo-Keto Reductase Family 1 Member B) transcript. Transcriptome analysis reveals a high level of expression of the new AKR1 B1 copy in the small intestine and liver, implying an increase in de novo fatty acid synthesis and antioxidant ability in dog compared to gray wolf, likely in response to dietary shifts during the agricultural revolution. For the first time, we report a comprehensive analysis of the evolutionary dynamics of SVs during the domestication step of dogs. Our findings demonstrate that retroposition can birth new genes to facilitate domestication, and affirm the importance of large-scale genomic variants in domestication studies.
引文
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3.Marquesbonet T,Girirajan S and Eichler EE.The origins and impact of primate segmental duplications.Trends Genet 2009;25:443-54.
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5.Lin T,Xu X and Ruan J et al.Genome analysis of Taraxacum kok-saghyz Rodin provides new insights into rubber biosynthesis.Natl Sci Rev 2018;5:78-87.
6.Xu SH,He ZW and Zhang Z et al.The origin,diversification and adaptation of a major mangrove clade(Rhizophoreae)revealed by whole-genome sequencing.Natl Sci Rev 2017;4:721-34.
7.Zhang X,Wang K and Wang L et al.Genome-wide patterns of copy number variation in the Chinese yak genome.BMC Genomics 2016;17:379.
8.Paudel Y,Madsen O and Megens H et al.Evolutionary dynamics of copy number variation in pig genomes in the context of adaptation and domestication.BMC Genomics 2013;14:449.
9.Axelsson E,Ratnakumar A and Arendt M et al.The genomic signature of dog domestication reveals adaptation to a starchrich diet.Nature 2013;495:360-4.
10.Norris BJ and Whan V.A gene duplication affecting expression of the ovine ASIP gene is responsible for white and black sheep.Genome Res 2008;18:1282-93.
11.Pielberg G,Olsson C and Syvanen A et al.Unexpectedly high allelic diversity at the KIT locus causing dominant white color in the domestic pig.Genetics 2002;160:305-11.
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13.Larson G,Karlsson EK and Perri AR et al.Rethinking dog domestication by integrating genetics,archeology,and biogeography.Proc Natl Acad Sci USA 2012;109:8878-83.
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15.Wang L,Ma YP and Zhou QJ et al.The geographical distribution of grey wolves(Canis lupus)in China:a systematic review.Zool Res 2016;37:315-26.
16.Lindblad-Toh K,Wade CM and Mikkelsen TS et al.Genome sequence,comparative analysis and haplotype structure of the domestic dog.Nature 2005;438:803-19.
17.Nicholas TJ,Baker C and Eichler EE et al.A high-resolution integrated map of copy number polymorphisms within and between breeds of the modern domesticated dog.BMC Genomics 2011;12:414.
18.Akey JM,Ruhe AL and Akey DT et al.Tracking footprints of artificial selection in the dog genome.Proc Natl Acad Sci USA2010;107:1160-5.
19.Ostrander EA,Wayne RK and Freedman AH et al.Demographic history,selection and functional diversity of the canine genome.Nat Rev Genet 2017;18:705-20.
20.Fan Z,Silva P and Gronau I et al.Worldwide patterns of genomic variation and admixture in gray wolves.Genome Res.2016;26:163-73.
21.Zhang W,Fan Z and Han E et al.Hypoxia adaptations in the Grey Wolf(Canis lupus chanco)from Qinghai-Tibet Plateau.PLo S Genet 2014;10:e1004466.
22.Liu YH,Wang L and Xu T et al.Whole-genome sequencing of African dogs provides insights into adaptations against tropical parasites.Mole Biol Evol 2018;35:287-98.
23.Wang GD,Fan RX and Zhai W et al.Genetic convergence in the adaptation of dogs and humans to the high-altitude environment of the Tibetan plateau.Genome Biol Evol 2014;6:2122-8.
24.Alvarez CE and Akey JM.Copy number variation in the domestic dog.Mamm Genome 2012;23:144-63.
25.Serres-Armero A,Povolotskaya IS and Quilez J et al.Similar genomic proportions of copy number variation within gray wolves and modern dog breeds inferred from whole genome sequencing.BMC Genomics 2017;18:977.
26.Newman TL,Tuzun E and Morrison VA et al.A genome-wide survey of structural variation between human and chimpanzee.Genome Res 2005;15:1344-56.
27.Yalcin B,Wong K and Agam A et al.Sequence-based characterization of structural variation in the mouse genome.Nature 2011;477:326-9.
28.Zhang H and Chen L.The complete mitochondrial genome of dhole Cuon alpinus:phylogenetic analysis and dating evolutionary divergence within canidae.Mol Biol Rep 2011;38:1651-60.
29.Wayne RK and Ostrander EA.Lessons learned from the dog genome.Trends Genet 2007;23:557-67.
30.Wang W and Kirkness EF.Short interspersed elements(SINEs)are a major source of canine genomic diversity.Genome Res 2005;15:1798-808.
31.Simao FA,Waterhouse RM and Ioannidis P et al.BUSCO:assessing genome assembly and annotation completeness with single-copy orthologs.Bioinformatics 2015;31:3210-2.
32.Larkin J,Johnson HM and Subramaniam PS.Differential nuclear localization of the IFNGR-1 and IFNGR-2 subunits of the IFN-γreceptor complex following activation by IFN-γ.J Interferon Cytokine Res 2000;20:565-76.
33.Lanier LL and Bakker ABH.The ITAM-bearing transmembrane adaptor DAP12in lymphoid and myeloid cell function.Immunol Today 2000;21:611-4.
34.Laplana M,Royo JL and Garcia LF et al.SIRPB1 copy-number polymorphism as candidate quantitative trait locus for impulsive-disinhibited personality.Genes Brain Behav 2014;13:653-62.
35.Weydt P,Pineda VV and Torrence AE et al.Thermoregulatory and metabolic defects in Huntington’s disease transgenic mice implicate PGC-1αin Huntington’s disease neurodegeneration.Cell Metab 2006;4:349-62.
36.Ahir VB,Panchal MT and Tripathi AK et al.Genetic polymorphism in the aldoketo reductase family 1 member b1(AKR1B1)gene of murrah buffalo bulls(Bubalus bubalis).Buffalo Bull 2010;29:274-8.
37.Xing J,Zhang Y and Han K et al.Mobile elements create structural variation:analysis of a complete human genome.Genome Res 2009;19:1516-26.
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