Aquaculture International

, Volume 27, Issue 2, pp 497–508 | Cite as

Single-nucleotide polymorphisms linked to body weight revealed in growth selected Macrobrachium rosenbergii

  • Chandan Haldar
  • S. P. Das
  • Bindu R. Pillai
  • Annam Pavan-Kumar
  • P. Gireesh-Babu
  • P. Das
  • Aparna ChaudhariEmail author


Association of type I single nucleotide polymorphic (SNP) markers with quantitative traits can provide an effective method for detecting genes and functions that are responsible for performance variation in domesticated species. In order to discover novel polymorphisms in candidate genes that could be associated with growth, fragments (175 to 668 bp) from 11 housekeeping, regulatory, and immune response genes of Macrobrachium rosenbergii previously reported to contain 83 SNPs were amplified from genomic DNA of 23 growth selected (cumulative genetic gain of 18%) and 23 unselected individuals and sequenced by Sanger’s method. A total of 45 SNPs were identified from eight genes, of which 20 were novel and 18 were found to be growth associated with allele frequencies > 0.65 in the selected group. Eleven of these were located in exonic regions of which 3 present in crustacean lipocalin (LIPC) and heat shock protein 21 (HSP21) were nonsynonymous. In silico prediction indicates that 2 of the non-synonymous alleles may result in higher stability of the proteins. Of the 5 synonymous growth-associated SNPs, 3 present in phosphoenol pyruvate carboxykinase (PEPCK), cytochrome oxidase 1 (COX1), and HSP70 were a switch to the preferred codon. Seven SNPs were located in the 3′UTRs of lectin 3 and 4 (LEC3, LEC4) and anti-lipopolysaccharide factor 1 (ALF1). Only one altered allele was observed at every locus. No SNPs were found in NaK-ATPase, mitochondrial manganese superoxide dismutase, and tachylectin genes. This is the first such marker association study being reported for M. rosenbergii from India and will be of use in selecting future generations.


Marker association study Candidate gene approach Genotyping Genetic selection Growth-associated SNPs 



The authors thank ICAR for providing post-graduate fellowship to first author. Dr. Gopal Krishna, Director, ICAR-CIFE and Dr. P. Jayasankar, Director, ICAR-CIFA are acknowledged for providing facilities.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical statement

Institutional animal ethics committee guidelines were followed for the care and maintenance of experimental animals.


  1. Agarwal D, Aich N, Pavan-Kumar A, Kumar S, Sabnis S, Joshi CG, Koringa P, Pandya D, Patel N, Karnik T, Bhingarde R, Gireesh-Babu P, Chaudhari A (2016) SNP mining in transcripts and concomitant estimation of genetic variation in Macrobrachium rosenbergii stocks. Conserv Genet Resour 8:159–168CrossRefGoogle Scholar
  2. Bolormaa S, Hayes BJ, Savin K, Hawken R, Barendse W, Arthur PF, Herd RM, Goddard ME (2011) Genome-wide association studies for feedlot and growth traits in cattle. J Anim Sci 89:1684–1697CrossRefGoogle Scholar
  3. Cesar JRO, Yang J (2007) Expression patterns of ubiquitin, heat shock protein 70, α-actin and β-actin over the molt cycle in the abdominal muscle of marine shrimp Litopenaeus vannamei. Mol Reprod Dev 74:554–559CrossRefGoogle Scholar
  4. Chayen NE, Cianci M, Grossmann JG, Habash J, Helliwell JR, Nneji GA, Raftery J, Rizkallah PJ, Zagalsky PF (2003) Unravelling the structural chemistry of the colouration mechanism in lobster shell. Acta Crystallogr D Biol Crystallogr 59:2072–2082CrossRefGoogle Scholar
  5. Ciobanu DC, Bastiaansen JWM, Magrin J, Rocha JL, Jiang DH, Yu N, Geiger B, Deeb N, Rocha D, Gong H, Kinghorn BP (2010) A major SNP resource for dissection of phenotypic and genetic variation in Pacific white shrimp (Litopenaeus vannamei). Anim Genet 41:39–47CrossRefGoogle Scholar
  6. Divu D, Khushiramani R, Malathi S, Karunasagar I, Karunasagar I (2008) Isolation, characterization and evaluation of microsatellite DNA markers in giant freshwater prawn Macrobrachium rosenbergii, from South India. Aquaculture 284:281–284CrossRefGoogle Scholar
  7. Du ZQ, Ciobanu DC, Onteru SK, Gorbach D, Mileham AJ, Jaramillo G, Rothschild MF (2010) A gene-based SNP linkage map for pacific white shrimp, Litopenaeus vannamei. Anim Genet 41:286–294CrossRefGoogle Scholar
  8. FAO (2014) Fisheries statistical database, global aquaculture production (Fisheries Global Information System, online query)Google Scholar
  9. Flower DR (1996) The lipocalin protein family: structure and function. Biochem J 318:1–14CrossRefGoogle Scholar
  10. Gjedrem T, Robinson N, Rye M (2012). The importance of selective breeding in aquaculture to meet future demands for animal protein: a review. Aquaculture 350:117-129Google Scholar
  11. Hartl FU, Hayer-Hartl M (2002). Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852-1858Google Scholar
  12. Henryon M, Jokumsen A, Berg P, Lund I, Pedersen PB, Olesen NJ, Slierendrecht WJ (2002) Genetic variation for growth rate, feed conversion efficiency, and disease resistance exists within a farmed population of rainbow trout. Aquaculture 209:59–76CrossRefGoogle Scholar
  13. Hoggart CJ, Whittaker JC, De Iorio M, Balding DJ (2008) Simultaneous analysis of all SNPs in genome-wide and re-sequencing association studies. PLoS Genet 4:e1000130. CrossRefGoogle Scholar
  14. Jung H, Lyons RE, Dinh H, Hurwood DA, McWilliam S, Mather PB (2011) Transcriptomics of a giant freshwater prawn (Macrobrachium rosenbergii): de novo assembly, annotation and marker discovery. PLoS One 6:e27938CrossRefGoogle Scholar
  15. Jung H, Lyons RE, Li Y, Thanh NM, Dinh H, Hurwood DA, Mather PB (2014) A candidate gene association study for growth performance in an improved giant freshwater prawn (Macrobrachium rosenbergii) culture line. Mar Biotechnol 16:161–180CrossRefGoogle Scholar
  16. Li M, Li C, Ma C, Li H, Zuo H, Weng S, Chen X, Zeng D, He J, Xu X (2014) Identification of a C-type lectin with antiviral and antibacterial activity from pacific white shrimp Litopenaeus vannamei. Dev Comp Immunol 46:231–240CrossRefGoogle Scholar
  17. Li H, Chen Y, Li M, Wang S, Zuo H, Xu X, Weng S, He J, Li C (2015) A C-type lectin (LvCTL4) from Litopenaeus vannamei is a downstream molecule of the NF-κB signaling pathway and participates in antibacterial immune response. Fish Shellfish Immunol 43:257–263CrossRefGoogle Scholar
  18. Liberek K, Lewandowska A, Ziętkiewicz S (2008) Chaperones in control of protein disaggregation. EMBO J 27:328–335CrossRefGoogle Scholar
  19. Liu ZJ, Cordes JF (2004) DNA marker technologies and their applications in aquaculture genetics. Aquaculture 238:1–37CrossRefGoogle Scholar
  20. Ma D, Ma A, Huang Z, Wang G, Wang T, Xia D, Ma B (2016) Transcriptome analysis for identification of genes related to gonad differentiation, growth, immune response and marker discovery in the turbot (Scophthalmus maximus). PLoS One 11:e0149414CrossRefGoogle Scholar
  21. Matukumalli LK, Lawley CT, Schnabel RD, Taylor JF, Allan MF, Heaton MP, O'connell J, Moore SS, Smith TP, Sonstegard TS, Van Tassell CP (2009) Development and characterization of a high density SNP genotyping assay for cattle. PLoS One 4:e5350CrossRefGoogle Scholar
  22. Mohanty P, Sahoo L, Pillai BR, Jayasankar P, Das P (2014) Genetic divergence in Indian populations of M. rosenbergii using microsatellite markers. Aquac Res 47:472–481CrossRefGoogle Scholar
  23. Mykles DL (1997) Crustacean muscle plasticity: molecular mechanisms determining mass and contractile properties. Comp Biochem Physiol B: Biochem Mol Biol 117:367–378CrossRefGoogle Scholar
  24. New MB, Nair CM (2012) Global scale of freshwater prawn farming. Aquaculture 43:960–969CrossRefGoogle Scholar
  25. Ogden R, Gharbi K, Mugue N, Martinsohn J, Senn H, Davey JW, Pourkazemi M, McEwing R, Eland C, Vidotto M, Sergeev A (2013) Sturgeon conservation genomics: SNP discovery and validation using RAD sequencing. Mol Ecol 22:3112–3123CrossRefGoogle Scholar
  26. Pillai BR, Mahapatra KD, Ponzoni RW, Sahoo L, Lalrinsanga PL, Nguyen NH, Mohanty S, Sahu S, Sahu S, Khaw HL, Patra G (2011) Genetic evaluation of a complete diallel cross involving three populations of freshwater prawn (Macrobrachium rosenbergii) from different geographical regions of India. Aquaculture 319:347–354CrossRefGoogle Scholar
  27. Pillai BR, Lalrinsanga PL, Ponzoni RW, Khaw HL, Mahapatra KD, Mohanty S, Patra G, Naik N, Pradhan H, Jayasankar P (2017) Phenotypic and genetic parameters for body traits in the giant freshwater prawn (Macrobrachium rosenbergii) in India. Aquac Res 48:5741–5750CrossRefGoogle Scholar
  28. Salem M, Vallejo RL, Leeds TD, Palti Y, Liu S, Sabbagh A, Rexroad CE III, Yao J (2012) RNA-Seq identifies SNP markers for growth traits in rainbow trout. PLoS One 7:e36264CrossRefGoogle Scholar
  29. See LM, Hassan R, Tan SG, Bhassu S (2008) Genetic characterization of wild stock of Prawn M. rosenbergii using random amplified polymorphic DNA marker. Biotechnology 7:338–342CrossRefGoogle Scholar
  30. Senoo H, Stang E, Nilsson A, Kindberg GM, Berg T, Roos N, Norum KR, Blomhoff R (1990) Internalization of retinol-binding protein in parenchymal and stellate cells of rat liver. J Lipid Res 31:1229–1239Google Scholar
  31. Shojaei M, Mohammad Abadi M, Asadi Fozi M, Dayani O, Khezri A, Akhondi M (2011) Association of growth trait and leptin gene polymorphism in Kermani sheep. J Cell Mol Res 2:67–73Google Scholar
  32. Silverstein JT, Vallejo RL, Palti Y, Leeds TD, Rexroad CE, Welch TJ, Wiens GD, Ducrocq V (2009) Rainbow trout resistance to bacterial cold-water disease is moderately heritable and is not adversely correlated with growth. J Anim Sci 87:860–867CrossRefGoogle Scholar
  33. Sivaprasadarao A, Boudjelal M, Findlay JB (1993) Lipocalin structure and function. Biochem Soc Trans 21:619–622CrossRefGoogle Scholar
  34. Sodsuk PK, Uraiwan S, Sodsuk S (2006) Allozyme marker based comparison on genetic variation among Macrobrachium rosenbergii populations produced from a cross-breeding system of three different stocks in Thailand. SEAFDEC/AQD Institutional repository (Third round table discussion on the development of genetically improved Macrobrachium), 25–29. Aaccessed 20 April 2014
  35. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefGoogle Scholar
  36. Tao WJ, Boulding EG (2003) Associations between single nucleotide polymorphisms in candidate genes and growth rate in Arctic charr (Salvelinus alpinus L.). Heredity 91:60–69CrossRefGoogle Scholar
  37. Thanh NM, Barnes AC, Mather PB, Li Y, Lyons RE (2010) Single nucleotide polymorphisms in the actin and crustacean hyperglycemic hormone genes and their correlation with individual growth performance in giant freshwater prawn Macrobrachium rosenbergii. Aquaculture 301:7–15CrossRefGoogle Scholar
  38. Tharntada S, Ponprateep S, Somboonwiwat K, Liu H, Söderhäll I, Söderhäll K, Tassanakajon A (2009) Role of anti-lipopolysaccharide factor from the black tiger shrimp, Penaeus monodon, in protection from white spot syndrome virus infection. J Gen Virol 90:1491–1498CrossRefGoogle Scholar
  39. 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 16:969CrossRefGoogle Scholar
  40. Venkatesan C, Hameed SA, Sundarraj N, Rajkumar T, Balasubramanian G (2014) Analysis of immune genes and heat shock protein genes under exposure to white spot syndrome virus (WSSV) and herbal immune stimulant in Litopenaeus vannamei. J Bacteriol Parasitol 5:1Google Scholar
  41. Zhan W, He L, Wei X, Wang X, Tang X (2015) An anti-lipopolysaccharide factor in Litopenaeus Vannamei participates in the immune defense against WSSV and Vibrio Anguillarum. J Crustac Biol 35:670–675CrossRefGoogle Scholar
  42. Zhang XW, Xu WT, Wang XW, Mu Y, Zhao XF, Yu XQ, Wang JX (2009) A novel C-type lectin with two CRD domains from Chinese shrimp Fenneropenaeus chinensis functions as a pattern recognition protein. Mol Immunol 46:1626–1637CrossRefGoogle Scholar
  43. Zou L, Liu B (2015) Identification of a serum amyloid a gene and the association of SNPs with vibrio-resistance and growth traits in the clam Meretrix meretrix. Fish Shellfish Immunol 43:301–309CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Chandan Haldar
    • 1
  • S. P. Das
    • 2
  • Bindu R. Pillai
    • 2
  • Annam Pavan-Kumar
    • 1
  • P. Gireesh-Babu
    • 1
  • P. Das
    • 2
  • Aparna Chaudhari
    • 1
    Email author
  1. 1.Fish Genetics and Biotechnology DivisionICAR-Central Institute of Fisheries EducationMumbaiIndia
  2. 2.Fish Genomics Laboratory, Fish Genetics and Biotechnology DivisionICAR-Central Institute of Freshwater AquacultureBhubaneswarIndia

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