Intercross population study reveals that co-mutation of mitfa genes in two subgenomes induces red skin color in common carp (Cyprinus carpio wuyuanensis)

Common carp are among the oldest domesticated fish in the world. As such, there are many food and ornamental carp strains with abundant phenotypic variations due to natural and artificial selection. Hebao red carp (HB, Cyprinus carpio wuyuanensis), an indigenous strain in China, is renowned for its unique body morphology and reddish skin. To reveal the genetic basis underlying the distinct skin color of HB, we constructed an improved high-fidelity (HiFi) HB genome with good contiguity, completeness, and correctness. Genome structure comparison was conducted between HB and a representative wild strain, Yellow River carp (YR, C. carpio haematopterus), to identify structural variants and genes under positive selection. Signatures of artificial selection during domestication were identified in HB and YR populations, while phenotype mapping was performed in a segregating population generated by HB×YR crosses. Body color in HB was associated with regions with fixed mutations. The simultaneous mutation and superposition of a pair of homologous genes (mitfa) in chromosomes A06 and B06 conferred the reddish color in domesticated HB. Transcriptome analysis of common carp with different alleles of the mitfa mutation confirmed that gene duplication can buffer the deleterious effects of mutation in allotetraploids. This study provides new insights into genotype-phenotype associations in allotetraploid species and lays a foundation for future breeding of common carp.

[1]  Zhang Zhang.  KaKs_Calculator 3.0: Calculating Selective Pressure on Coding and Non-coding Sequences , 2021, bioRxiv.

[2]  Hongyu Zhang,et al.  Pan-genome analysis of 33 genetically diverse rice accessions reveals hidden genomic variations , 2021, Cell.

[3]  Jianfeng Liu,et al.  Analysis of Structural Variants Reveal Novel Selective Regions in the Genome of Meishan Pigs by Whole Genome Sequencing , 2021, Frontiers in Genetics.

[4]  A. Nagano,et al.  QTL analysis for early growth in an intercross between native Japanese Nagoya and White Plymouth Rock chicken breeds using RAD sequencing-based SNP markers. , 2021, Animal Genetics.

[5]  Thomas M. Keane,et al.  Twelve years of SAMtools and BCFtools , 2020, GigaScience.

[6]  G. Wang,et al.  The evolutionary origin and domestication history of goldfish (Carassius auratus) , 2020, Proceedings of the National Academy of Sciences.

[7]  Shuhong Zhao,et al.  rMVP: A Memory-efficient, Visualization-enhanced, and Parallel-accelerated Tool for Genome-wide Association Study , 2020, bioRxiv.

[8]  P. Fontaine,et al.  How domestication alters fish phenotypes , 2020, Reviews in Aquaculture.

[9]  Michael C. Schatz,et al.  Major Impacts of Widespread Structural Variation on Gene Expression and Crop Improvement in Tomato , 2020, Cell.

[10]  Ryan M. Layer,et al.  The structural variation landscape in 492 Atlantic salmon genomes , 2020, Nature Communications.

[11]  C. Jiggins,et al.  The genomics of coloration provides insights into adaptive evolution , 2020, Nature Reviews Genetics.

[12]  Narmada Thanki,et al.  CDD/SPARCLE: the conserved domain database in 2020 , 2019, Nucleic Acids Res..

[13]  Aaron M Wenger,et al.  Improved assembly and variant detection of a haploid human genome using single‐molecule, high‐fidelity long reads , 2019, Annals of human genetics.

[14]  Juzhong Zhang,et al.  Common carp aquaculture in Neolithic China dates back 8,000 years , 2019, Nature Ecology & Evolution.

[15]  M. Goel,et al.  SyRI: finding genomic rearrangements and local sequence differences from whole-genome assemblies , 2019, bioRxiv.

[16]  Steven L Salzberg,et al.  Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype , 2019, Nature Biotechnology.

[17]  Sergey Koren,et al.  Accurate circular consensus long-read sequencing improves variant detection and assembly of a human genome , 2019, Nature Biotechnology.

[18]  Randle Aaron M. Villanueva,et al.  ggplot2: Elegant Graphics for Data Analysis (2nd ed.) , 2019, Measurement: Interdisciplinary Research and Perspectives.

[19]  Shikai Liu,et al.  Inheritance of shell pigmentation in Pacific oyster Crassostrea gigas , 2019, Aquaculture.

[20]  Heebal Kim,et al.  Whole genome sequencing reveals the impact of recent artificial selection on red sea bream reared in fish farms , 2019, Scientific Reports.

[21]  Hanyuan Zhang,et al.  The allotetraploid origin and asymmetrical genome evolution of common carp Cyprinus carpio , 2018, bioRxiv.

[22]  A. Maass,et al.  Comparing genomic signatures of domestication in two Atlantic salmon (Salmo salar L.) populations with different geographical origins , 2018, Evolutionary applications.

[23]  S. Kelly,et al.  OrthoFinder: phylogenetic orthology inference for comparative genomics , 2019, Genome Biology.

[24]  Shuhong Zhao,et al.  Genomic Analysis To Identify Signatures of Artificial Selection and Loci Associated with Important Economic Traits in Duroc Pigs , 2018, G3: Genes, Genomes, Genetics.

[25]  Q. Gao,et al.  An intercross population study reveals genes associated with body size and plumage color in ducks , 2018, Nature Communications.

[26]  Jia Zhiying,et al.  Developments in Common Carp Culture and Selective Breeding of New Varieties , 2018 .

[27]  Jian Wang,et al.  SOAPnuke: a MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data , 2017, GigaScience.

[28]  Mauricio O. Carneiro,et al.  Scaling accurate genetic variant discovery to tens of thousands of samples , 2017, bioRxiv.

[29]  Jeffrey T Leek,et al.  Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown , 2016, Nature Protocols.

[30]  Yun Ding,et al.  Natural courtship song variation caused by an intronic retroelement in an ion channel gene , 2016, Nature.

[31]  James T. Robinson,et al.  Juicebox Provides a Visualization System for Hi-C Contact Maps with Unlimited Zoom. , 2016, Cell systems.

[32]  Xin Li,et al.  The impact of structural variation on human gene expression , 2016, Nature Genetics.

[33]  Takashi Akagi,et al.  Genome-wide view of genetic diversity reveals paths of selection and cultivar differentiation in peach domestication , 2016, DNA research : an international journal for rapid publication of reports on genes and genomes.

[34]  J. Lenstra,et al.  Yak whole-genome resequencing reveals domestication signatures and prehistoric population expansions , 2015, Nature Communications.

[35]  S. Salzberg,et al.  StringTie enables improved reconstruction of a transcriptome from RNA-seq reads , 2015, Nature Biotechnology.

[36]  M. Czyz,et al.  MITF in melanoma: mechanisms behind its expression and activity , 2014, Cellular and Molecular Life Sciences.

[37]  R. Murphy,et al.  Allopolyploidization is not so simple: evidence from the origin of the tribe Cyprinini (Teleostei: Cypriniformes). , 2014, Current molecular medicine.

[38]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[39]  Qiang Li,et al.  Genome sequence and genetic diversity of the common carp, Cyprinus carpio , 2014, Nature Genetics.

[40]  Eric S. Lander,et al.  Rabbit genome analysis reveals a polygenic basis for phenotypic change during domestication , 2014, Science.

[41]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[42]  M. Stephens,et al.  Genome-wide Efficient Mixed Model Analysis for Association Studies , 2012, Nature Genetics.

[43]  Haiyan Zhang,et al.  ParaAT: a parallel tool for constructing multiple protein-coding DNA alignments. , 2012, Biochemical and biophysical research communications.

[44]  Gonçalo R. Abecasis,et al.  The variant call format and VCFtools , 2011, Bioinform..

[45]  Ramón Doallo,et al.  ProtTest 3: fast selection of best-fit models of protein evolution , 2011, Bioinform..

[46]  Stephen L. Johnson,et al.  mitfa is required at multiple stages of melanocyte differentiation but not to establish the melanocyte stem cell. , 2011, Developmental biology.

[47]  Helga Thorvaldsdóttir,et al.  Integrative Genomics Viewer , 2011, Nature Biotechnology.

[48]  H. Hakonarson,et al.  ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data , 2010, Nucleic acids research.

[49]  Hadley Wickham,et al.  ggplot2 - Elegant Graphics for Data Analysis (2nd Edition) , 2017 .

[50]  Andrew H. Paterson,et al.  Synteny and Collinearity in Plant Genomes , 2008, Science.

[51]  B. Browning,et al.  Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. , 2007, American journal of human genetics.

[52]  Manuel A. R. Ferreira,et al.  PLINK: a tool set for whole-genome association and population-based linkage analyses. , 2007, American journal of human genetics.

[53]  B. Gaut,et al.  Plant domestication, a unique opportunity to identify the genetic basis of adaptation , 2007, Proceedings of the National Academy of Sciences.

[54]  D. Fisher,et al.  MITF: master regulator of melanocyte development and melanoma oncogene. , 2006, Trends in molecular medicine.

[55]  D. Reich,et al.  Principal components analysis corrects for stratification in genome-wide association studies , 2006, Nature Genetics.

[56]  G. Wagner,et al.  Proceedings of the SMBE Tri-National Young Investigators' Workshop 2005. What is the role of genome duplication in the evolution of complexity and diversity? , 2006, Molecular biology and evolution.

[57]  E. Balon.  About the oldest domesticates among fishes. , 2004 .

[58]  J. Zhou,et al.  Genetic Variation Analysis within and among Six Varieties of Common Carp (Cyprinus carpio L.) in China Using Microsatellite Markers , 2004, Russian Journal of Genetics.

[59]  S. Salzberg,et al.  Versatile and open software for comparing large genomes , 2004, Genome Biology.

[60]  M. Feldman,et al.  Recent duplication of the common carp (Cyprinus carpio L.) genome as revealed by analyses of microsatellite loci. , 2003, Molecular biology and evolution.

[61]  L. Rieseberg,et al.  EXPERIMENTAL HYBRIDIZATION AS A TOOL FOR STUDYING SELECTION IN THE WILD , 2003 .

[62]  L. Hurst.  The Ka/Ks ratio: diagnosing the form of sequence evolution. , 2002, Trends in genetics : TIG.

[63]  Wei Qian,et al.  Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. , 2000, Molecular biology and evolution.

[64]  L. Andersson.  The use of a wild pig x domestic pig intercross to map phenotypic trait loci. , 1997, The Journal of heredity.

[65]  S. Wessler,et al.  Alternative splicing induced by insertion of retrotransposons into the maize waxy gene. , 1992, The Plant cell.

[66]  unavoidably withheld.  The Variation of Animals and Plants under Domestication , 1868, The British and foreign medico-chirurgical review.

[67]  Kazutaka Katoh,et al.  Multiple alignment of DNA sequences with MAFFT. , 2009, Methods in molecular biology.

[68]  Lou Yun.  Progress on studies of origin and genetic diversity of three breeds of red carp in Jiangxi Province , 2001 .

[69]  G. Mendel.  EXPERIMENTS IN PLANT HYBRIDIZATION ( 1865 ) , 1998 .

[70]  J. Bakos,et al.  Genetic improvement of common carp strains using intraspecific hybridization , 1995 .