Abstract
The Pacific white shrimp Litopenaeus vannamei is one of the major economic aquaculture species. The growth trait is considered as the most important trait in L. vannamei aquaculture. Identification of the genetic components underlying growth-related traits in L. vannamei could be useful for the selective breeding of growth trait. Our previous work identified several growth-related SNPs by genome-wide association study (GWAS). Based on the assembled genome, we identified a new candidate gene (LvMMD2) beside the associated marker. This gene encodes the progestin and AdipoQ receptor 10 (PAQR10) protein. We further investigate the polymorphisms of LvMMD2 and their association with body weight of L. vannamei. By resequencing the coding region of LvMMD2, a total of 8 SNPs were identified, including 6 synonymous mutations and 2 nonsynonymous mutations. Association analyses based on a population of 322 individuals revealed that several SNPs located in the coding region of LvMMD2 were significantly associated with the body weight, especially the nonsynonymous mutation named as MMD_5 contributed the most association to the trait and it could explain 10.5% of phenotypic variance. In addition, several genes involved in growth and development have been identified as LvMMD2-interacting genes. These findings strongly suggested that LvMMD2 might be an important gene regulating the shrimp growth. More importantly, the MMD_5 could be a promising candidate locus for marker-assisted selection (MAS) of the body weight in L. vannamei.
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References
Andriantahina F, Liu X, Huang H, Xiang J (2013) Selection for growth performance of tank-reared Pacific white shrimp, Litopenaeus vannamei. Chin J Oceanol Limnol 31:534–541
Argue BJ, Arce SM, Lotz JM, Moss SM (2002) Selective breeding of Pacific white shrimp (Litopenaeus vannamei) for growth and resistance to Taura syndrome virus. Aquaculture 204:447–460
Bräuer AU, Nitsch R, Savaskan NE (2004) Identification of macrophage/microglia activation factor (MAF) associated with late endosomes/lysosomes in microglial cells. FEBS Lett 563:41–48
Demeure O, Duclos MJ, Bacciu N, Le Mignon G, Filangi O, Pitel F, Boland A, Lagarrigue S, Cogburn LA, Simon J (2013) Genome-wide interval mapping using SNPs identifies new QTL for growth, body composition and several physiological variables in an F2 intercross between fat and lean chicken lines. Genet Sel Evol 45:36
Dong L, Han Z, Fang M, Xiao S, Wang Z (2019) Genome-wide association study identifies loci for body shape in the large yellow croaker (Larimichthys crocea). Aquacult Fish 4:3–8
FAO (2018) The State of the World Fisheries and Aquaculture (SOFIA) 2018. Fisheries and Aquaculture Department, Rome, Italy 250 pp
Fjalestad K, Gjedrem T, Carr W, Sweeney J (1997) Final report: the shrimp breeding program, selective breeding of Penaeus vannamei. The Oceanic Institute, Waimanalo
Gaut BS, Long AD (2003) The lowdown on linkage disequilibrium. Plant Cell 15:1502–1506
Hicks D, Sarkozy A, Muelas N, Köehler K, Huebner A, Hudson G, Chinnery PF, Barresi R, Eagle M, Polvikoski T (2010) A founder mutation in Anoctamin 5 is a major cause of limb girdle muscular dystrophy. Brain 134:171–182
Hill WG (1974) Estimation of linkage disequilibrium in randomly mating populations. Heredity 33:229–239
Hirschhorn JN, Daly MJ (2005) Genome-wide association studies for common diseases and complex traits. Nat Rev Genet 6:95–108
Huang X, Han B (2014) Natural variations and genome-wide association studies in crop plants. Annu Rev Plant Biol 65:531–551
Huang H, Jin T, He J, Ding Q, Xu D, Wang L, Zhang Y, Pan Y, Wang Z, Chen Y (2012) Progesterone and adipoQ receptor 11 links ras signaling to cardiac development in zebrafish. Arterioscler Thromb Vasc Biol 32:2158–2170
Huang W, Cheng C, Liu J, Zhang X, Ren C, Jiang X, Chen T, Cheng K, Li H, Hu C (2020) Fine mapping of the high-pH tolerance and growth trait-related quantitative trait loci (QTLs) and identification of the candidate genes in Pacific white shrimp (Litopenaeus vannamei). Mar Biotechnol 22:1–18
Jin Y, Ha N, Forés M, Xiang J, Gläßer C, Maldera J, Jiménez G, Edgar BA (2015) EGFR/Ras signaling controls Drosophila intestinal stem cell proliferation via Capicua-regulated genes. PLoS Genet 11:e1005634
Jung H, Lyons RE, Hurwood DA, Mather PB (2013) Genes and growth performance in crustacean species: a review of relevant genomic studies in crustaceans and other taxa. Rev Aquac 5:77–110
Korte A, Farlow A (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9:29
Lee KT, Park EW, Moon S, Park HS, Kim HY, Jang GW, Choi BH, Chung H, Lee JW, Cheong IC (2006) Genomic sequence analysis of a potential QTL region for fat trait on pig chromosome 6. Genomics 87:218–224
Liu J, Aoki M, Illa I, Wu C, Fardeau M, Angelini C, Serrano C, Urtizberea JA, Hentati F, Hamida MB (1998) Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limb girdle muscular dystrophy. Nat Genet 20:31–36
Lu X, Luan S, Hu LY, Mao Y, Tao Y, Zhong SP, Kong J (2016) High-resolution genetic linkage mapping, high-temperature tolerance and growth-related quantitative trait locus (QTL) identification in Marsupenaeus japonicus. Mol Gen Genomics 291:1391–1405
Lu X, Kong J, Meng X, Cao B, Luo K, Dai P, Luan S (2018) Identification of SNP markers associated with tolerance to ammonia toxicity by selective genotyping from de novo assembled transcriptome in Litopenaeus vannamei. Fish Shellfish Immunol 73:158–166
Mueller JC (2004) Linkage disequilibrium for different scales and applications. Brief Bioinform 5:355–364
Neira R (2010) Breeding in aquaculture species: genetic improvement programs in developing countries. In: Proceedings of the 9th World Congress on Genetics Applied to Livestock Production
Peleman JD, Van der Voort JR (2003) Breeding by design. Trends Plant Sci 8:330–334
R Core Team (2018) R: a language and environment for statistical computing (Version 3.5.2). Available: https://www.R-project.org/
Rye M, Gjerde B, Gjedrem T (2010) Genetic improvement programs for aquaculture species in developed countries. In: Proceedings of the 9th world congress on genetics applied to livestock production
Shin JH, Blay S, Mcneney B, Graham J (2006) LDheatmap: an R function for graphical display of pairwise linkage disequilibria between single. J Stat Softw 16:3
Sun Z, Li S, Li F, Xiang J (2014) Bioinformatic prediction of WSSV-host protein-protein interaction. Biomed Res Int 2014:416543
Svensk E, Ståhlman M, Andersson CH, Johansson M, Borén J, Pilon M (2013) PAQR-2 regulates fatty acid desaturation during cold adaptation in C. elegans. PLoS Genet 9:e1003801
Tang Y, Hu T, Arterburn M, Boyle B, Bright JM, Emtage PC, Funk WD (2005) PAQR proteins: a novel membrane receptor family defined by an ancient 7-transmembrane pass motif. J Mol Evol 61:372–380
Tangprasittipap A, Tiensuwan M, Withyachumnarnkul B (2010) Characterization of candidate genes involved in growth of black tiger shrimp Penaeus monodon. Aquaculture 307:150–156
Taniguchi M, Basarab JA, Dodson MV, Moore SS (2008) Comparative analysis on gene expression profiles in cattle subcutaneous fat tissues. Comp Biochem Physiol Part D Genomics Proteomics 3:251–256
Thomas P, Pang Y, Dong J, Groenen P, Kelder JD, De Vlieg J, Zhu Y, Tubbs C (2007) Steroid and G protein binding characteristics of the seatrout and human progestin membrane receptor α subtypes and their evolutionary origins. Endocrinology 148:705–718
Wang X, Wang H, Liu S, Ferjani A, Li J, Yan J, Yang X, Qin F (2016) Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings. Nat Genet 48:1233–1241
Wang Q, Yu Y, Zhang Q, Zhang X, Yuan J, Huang H, Xiang J, Li F (2019) A novel candidate gene associated with body weight in the Pacific white shrimp Litopenaeus vannamei. Front Genet 10:520
Xue Y (2013) Next-generation biotechnological breeding techniques for the future—designer breading by molecular modules. Bull Chin Acad Sci 28:308–314
Yamauchi T, Kamon J, Ito Y, Tsuchida A, Yokomizo T, Kita S, Sugiyama T, Miyagishi M, Hara K, Tsunoda M (2003) Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 423:762–769
Yang Y, Wu L, Wu X, Li B, Huang W, Weng Z, Lin Z, Song L, Guo Y, Meng Z, Liu X, Xia J (2020) Identification of candidate growth-related SNPs and genes using GWAS in brown-marbled grouper (Epinephelus fuscoguttatus). Mar Biotechnol 22:153–166
Yu Y, Zhang X, Yuan J, Li F, Chen X, Zhao Y, Huang L, Zheng H, Xiang J (2015) Genome survey and high-density genetic map construction provide genomic and genetic resources for the Pacific white shrimp Litopenaeus vannamei. Sci Rep 5:15612
Yu Y, Zhang X, Yuan J, Wang Q, Li S, Huang H, Li F, Xiang J (2017) Identification of sex-determining loci in Pacific white shrimp Litopeneaus vannamei using linkage and association analysis. Mar Biotechnol 19:277–286
Yu Y, Wang Q, Zhang Q, Luo Z, Wang Y, Zhang X, Huang H, Xiang J, Li F (2019) Genome scan for genomic regions and genes associated with growth trait in Pacific white shrimp Litopeneaus vannamei. Mar Biotechnol 21:374–383
Yue GH (2014) Recent advances of genome mapping and marker-assisted selection in aquaculture. Fish Fish 15:376–396
Zhang H, Wang Z, Wang S, Li H (2012) Progress of genome wide association study in domestic animals. J Anim Sci Biotechnol 3:26
Zhang X, Yuan J, Sun Y, Li S, Gao Y, Yu Y, Liu C, Wang Q, Lv X, Zhang X (2019) Penaeid shrimp genome provides insights into benthic adaptation and frequent molting. Nat Commun 10:356
Zhong X, Wang X, Zhou T, Jin Y, Tan S, Jiang C, Geng X, Li N, Shi H, Zeng Q (2017) Genome-wide association study reveals multiple novel QTL associated with low oxygen tolerance in hybrid catfish. Mar Biotechnol 19:379–390
Zhou Z, Han K, Wu Y, Bai H, Ke Q, Pu F, Wang Y, Xu P (2019) Genome-wide association study of growth and body-shape-related traits in large yellow croaker (Larimichthys crocea) using ddRAD sequencing. Mar Biotechnol 21:655–670
Funding
This work was supported by National Key R&D Program of China (2018 YFD0901301, 2018YFD0900303), Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No. XDA24030105), Agricultural Variety Improvement Project of Shandong Province (2019LZGC014), and China Agriculture Research System-48.
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Wang, Q., Yu, Y., Zhang, Q. et al. The Polymorphism of LvMMD2 and Its Association with Growth Traits in Litopenaeus vannamei. Mar Biotechnol 22, 564–571 (2020). https://doi.org/10.1007/s10126-020-09977-0
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DOI: https://doi.org/10.1007/s10126-020-09977-0