Abstract
Common carp (Cyprinus carpio) is one of the most widely studied fish species due to its great economic value and strong environmental adaptability. Scattered scale, a typical phenotype of the mirror carp that is derived from Europe, has never been observed in the Yellow River carp previously. We recently identified approximately one fourth of the F1 progenies displaying scattered scale in a full-sib Yellow River carp family in our breeding program, despite both parents that showed wild type with normal scale patterns. This family provides us unique materials to investigate the genetic basis underlying the abnormal scale mutant in Yellow River carp population. Genome-wide association study (GWAS) and association mapping were performed based on genome-wide single nucleotide polymorphisms (SNP) genotyped with common carp 250 K SNP genotyping array in 82 samples of the Yellow River carp family. We identified a 1.4 Mb genome region that was significantly associated with abnormal scattered scale patterns. We further identified a deletion mutation in fibroblast growth factor receptor 1 a1 (fgfr1a1) gene within this genome region. Amplification and sequencing analysis of this gene revealed a 311-bp deletion in intron 10 and exon 11, which proved that fgfr1a1 could be the causal gene responsible for abnormal scattered scale in the Yellow River carp family. Since similar fragment mutation with 306-bp and 310-bp deletions had been previously reported as causal mutation of scattered scale patterns in the mirror carp, we speculate that either the deletion mutation was introduced from Europe-derived mirror carp or the deletion independently occurred in the mutation hotspot in fgfr1a1 gene. The results provided insights into the genetic basis of scale pattern mutant in Yellow River carp population, which would help us to eliminate the recessive allele of the abnormal scale patterns in Yellow River carp population by molecular marker-assisted breeding.
Similar content being viewed by others
References
Arendt ML, Melin M, Tonomura N, Koltookian M, Courtaycahen C, Flindall N, Bass J, Boerkamp K, Megquir K, Youell L (2015) Genome-wide association study of golden retrievers identifies germ-line risk factors predisposing to mast cell tumours. PLoS Genet 11:e1005647
Balon EK (1995) Origin and domestication of the wild carp, Cyprinus-Carpio—from Roman Gourmets to the Swimming Flowers. Aquaculture 129:3–48
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635
Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G, Dickson M, Grimwood J, Schmutz J, Myers RM, Schluter D, Kingsley DM (2005) Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307:1928–1933
Correa K, Lhorente JP, Bassini L, López ME, Genova AD, Maass A, Davidson WS, Yáñez JM (2016) Genome wide association study for resistance to Caligus rogercresseyi in Atlantic salmon ( Salmo salar L.) using a 50K SNP genotyping array. Aquaculture 472(Suppl1):61–65
Goddard ME, Hayes BJ (2009) Mapping genes for complex traits in domestic animals and their use in breeding programmes. Nat Rev Genet 10:381–391
Gutierrez AP, Yáñez JM, Fukui S, Swift B, Davidson WS (2015) Genome-wide association study (GWAS) for growth rate and age at sexual maturation in Atlantic Salmon (Salmo salar). PLoS One 10:e0119730
Jin Y, Zhou T, Geng X, Liu S, Chen A, Yao J, Jiang C, Tan S, Su B, Liu Z (2016) A genome-wide association study of heat stress-associated SNPs in catfish. Anim Genet 48(2):233–236
Johnson RC, Nelson GW, Troyer JL, Lautenberger JA, Kessing BD, Winkler CA, O'brien SJ (2010) Accounting for multiple comparisons in a genome-wide association study (GWAS). BMC Genomics 11:724
Kirpitchnikov VS, Billard R (1999) Genetics and breeding of common carp. Editions Quae, Versailles, France.
Li Y, Xu P, Zhao Z, Wang J, Zhang Y, Sun XW (2011) Construction and characterization of the BAC library for common carp Cyprinus carpio L. and establishment of microsynteny with zebrafish Danio rerio. Mar Biotechnol (NY) 13:706–712
Li HL, Gu XH, Li BJ, Chen CH, Lin HR, Xia JH (2017a) Genome-wide QTL analysis identified significant associations between hypoxia tolerance and mutations in the GPR132 and ABCG4 genes in Nile Tilapia. Mar Biotechnol 19:441–453
Li Y, Geng X, Bao L, Elaswad A, Huggins KW, Dunham R, Liu Z (2017b) A deletion in the Hermansky-Pudlak syndrome 4 (Hps4) gene appears to be responsible for albinism in channel catfish. Mol Genet Genomics 292:663–670
Liu JH, Zhang Y, Chang YM, Liang LQ, Cui-Yun LU, Mei-Jia XU, Sun XW (2009a) Mapping QTLs related to body weight and full size of common carp (Cyprinus carpio). J Guangdong Ocean Univ 29(4):19–24
Liu JH, Zhang Y, Chang YM, Liang LQ, Lu CY, Zhang XF, Xu MJ, Sun XW (2009b) Mapping QTLs related to head length, eye diameter and eye cross of common carp (Cyprinus carpio L.). Hereditas 31:508–514
Liu S, Vallejo RL, Gao G, Palti Y, Weber GM, Hernandez A, Rd RC (2015) Identification of single-nucleotide polymorphism markers associated with cortisol response to crowding in rainbow trout. Mar Biotechnol 17:328–337
Liu Z, Liu S, Yao J, Bao L, Zhang J, Li Y, Jiang C, Sun L, Wang R, Zhang Y (2016) The channel catfish genome sequence provides insights into the evolution of scale formation in teleosts. Nat Commun 7:11757
Miyabe K, Tokunaga H, Endo H, Inoue H, Suzuki M, Tsutsui N, Yokoo N, Kogure T, Nagasawa H (2013) GSP-37, a novel goldfish scale matrix protein: identification, localization and functional analysis. Faraday Discuss 159:463–481
Moffitt CM, Cajas-Cano L (2014) Blue growth: the 2014 FAO state of world fisheries and aquaculture. Fisheries 39:552–553
Monnot MJ, Babin PJ, Poleo G, Andre M, Laforest L, Ballagny C, Akimenko MA (1999) Epidermal expression of apolipoprotein E gene during fin and scale development and fin regeneration in zebrafish. Dev Dyn Off Publ Am Assoc Anat 214:207–215
Ooijen V (2011) Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet Res 93:343–349
Peng W, Xu J, Zhang Y, Feng J, Dong C, Jiang L, Feng J, Chen B, Gong Y, Chen L, Xu P (2016) An ultra-high density linkage map and QTL mapping for sex and growth-related traits of common carp (Cyprinus carpio). Sci Rep 6:26693
Rohner N, Bercsényi M, Orbán L, Kolanczyk ME, Linke D, Brand M, Nüssleinvolhard C, Harris MP (2009) Duplication of fgfr1 permits Fgf signaling to serve as a target for selection during domestication. Curr Biol 19:1642–1647
Shu K, Kuwahara Y, Kondo M, Naruse K, Mitani H, Wakamatsu Y, Ozato K, Asakawa S, Shimizu N, Shima A (2001) The medaka rs-3 locus required for scale development encodes ectodysplasin—a receptor. Curr Biol 11:1202
Tsai HY, Hamilton A, Tinch AE, Guy DR, Gharbi K, Stear MJ, Matika O, Bishop SC, Houston RD (2015) Genome wide association and genomic prediction for growth traits in juvenile farmed Atlantic salmon using a high density SNP array. BMC Genomics 16:969
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J hered 93:77–78
Wang L, Liu P, Huang S, Ye B, Chua E, Wan ZY, Yue GH (2017) Genome-wide association study identifies loci associated with resistance to viral nervous necrosis disease in Asian seabass. Mar Biotechnol 19:255–265
Xiao T, Lu C, Xu Y, Chao L, Zheng X, Cao D, Lei C, Mahboob S, Sun X (2015) Screening of SSR markers associated with scale cover pattern and mapped to a genetic linkage map of common carp (Cyprinus carpio L.). J Appl Genet 56:1–9
Xin G, Jin S, Liu S, Bao L, Zhang J, Wang R, Yao J, Chao L, Feng J, Sun F (2015) A genome-wide association study in catfish reveals the presence of functional hubs of related genes within QTLs for columnaris disease resistance. BMC Genomics 16:196
Xin G, Liu S, Yao J, Bao L, Zhang J, Chao L, Wang R, Jin S, Peng Z, Zhi D (2016) A genome-wide association study identifies multiple regions associated with head size in catfish. G3 Genesgenetics 6:3389–3398
Xu P, Li J, Li Y, Cui R, Wang J, Wang J, Zhang Y, Zhao Z, Sun X (2011a) Genomic insight into the common carp (Cyprinus carpio) genome by sequencing analysis of BAC-end sequences. BMC Genomics 12:188
Xu P, Wang J, Wang J, Cui R, Li Y, Zhao Z, Ji P, Zhang Y, Li J, Sun X (2011b) Generation of the first BAC-based physical map of the common carp genome. BMC Genomics 12:537
Xu J, Zhao Z, Zhang X, Zheng X, Li J, Jiang Y, Kuang Y, Zhang Y, Feng J, Li C, Yu J, Li Q, Zhu Y, Liu Y, Xu P, Sun X (2014a) Development and evaluation of the first high-throughput SNP array for common carp (Cyprinus carpio). BMC Genomics 15:307
Xu P, Zhang X, Wang X, Li J, Liu G, Kuang Y, Xu J, Zheng X, Ren L, Wang G (2014b) Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nat Genet 46:1212–1219
Xu P, Zhang X, Wang X, Li J, Liu G, Kuang Y, Xu J, Zheng X, Ren L, Wang G, Zhang Y, Huo L, Zhao Z, Cao D, Lu C, Li C, Zhou Y, Liu Z, Fan Z, Shan G, Li X, Wu S, Song L, Hou G, Jiang Y, Jeney Z, Yu D, Wang L, Shao C, Song L, Sun J, Ji P, Wang J, Li Q, Xu L, Sun F, Feng J, Wang C, Wang S, Wang B, Li Y, Zhu Y, Xue W, Zhao L, Wang J, Gu Y, Lv W, Wu K, Xiao J, Wu J, Zhang Z, Yu J, Sun X (2014c) Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nat Genet 46:1212–1219
Zhang Y, Xu P, Lu C, Kuang Y, Zhang X, Cao D, Li C, Chang Y, Hou N, Li H (2011) Genetic linkage mapping and analysis of muscle fiber-related QTLs in common carp (Cyprinus carpio L.). Mar Biotechnol 13:376–392
Zhang X, Zhang Y, Zheng X, Kuang Y, Zhao Z, Zhao L, Li C, Jiang L, Cao D, Lu C, Xu P, Sun X (2013) A consensus linkage map provides insights on genome character and evolution in common carp (Cyprinus carpio L.). Mar Biotechnol (NY) 15:275–312
Zhao L, Zhang Y, Ji P, Zhang X, Zhao Z, Hou G, Huo L, Liu G, Li C, Xu P, Sun X (2013) A dense genetic linkage map for common carp and its integration with a BAC-based physical map. PLoS One 8:e63928
Zheng X, Kuang Y, Lv W, Cao D, Sun Z, Sun X (2016) Genome-wide association study for muscle fat content and abdominal fat traits in common carp (Cyprinus carpio). PLoS One 11:e0169127
Zhong X, Wang X, Zhou T, Jin Y, Tan S, Jiang C, Geng X, Li N, Shi H, Zeng Q, Yang Y, Yuan Z, Bao L, Liu S, Tian C, Peatman E, Li Q, Liu Z (2017) Genome-wide association study reveals multiple novel QTL associated with low oxygen tolerance in hybrid catfish. Mar Biotechnol (NY) 19:379–390
Zhou X, Stephens M (2012) Genome-wide efficient mixed-model analysis for association studies. Nat Genet 44:821–824
Zhou T, Liu S, Geng X, Jin Y, Jiang C, Bao L, Yao J, Zhang Y, Zhang J, Sun L (2016) GWAS analysis of QTL for enteric septicemia of catfish and their involved genes suggest evolutionary conservation of a molecular mechanism of disease resistance. Mol Gen Genomics 292(1):231–242
Acknowledgements
We acknowledge grant support from the National Natural Science Foundation of China (No. 31422057), the National High-Technology Research and Development Program of China (863 program; 2011AA100401), the Open Project of State Key Laboratory of Large Yellow Croaker Breeding (No. LYC2017RS05), Fundamental Research Funds for the Central Universities, Xiamen University (20720160110), and the Local Science and Technology Development Project Guide by The Central Government (2017L3019).
Author information
Authors and Affiliations
Contributions
PX and JS conceived and supervised the study. ZZ analyzed the data and drafted the manuscript. CD, WP, SK, and BC helped on data analysis. FP helped on manuscript preparation. JF helped with carp family construction and sample collection. PX and LC revised the manuscript. All authors have read and approved the manuscript.
Corresponding author
Ethics declarations
This study was approved by the Animal Care and Use committee at College of Ocean and Earth Sciences, Xiamen University. All the methods used in this study were carried out in accordance with approved guidelines.
Conflict of Interest
The authors declare that there is no conflict of interest.
Rights and permissions
About this article
Cite this article
Zhou, Z., Chen, L., Dong, C. et al. Genome-Scale Association Study of Abnormal Scale Pattern in Yellow River Carp Identified Previously Known Causative Gene in European Mirror Carp. Mar Biotechnol 20, 573–583 (2018). https://doi.org/10.1007/s10126-018-9827-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-018-9827-3