Abstract
A candidate gene approach using type I single nucleotide polymorphism (SNP) markers can provide an effective method for detecting genes and gene regions that underlie phenotypic variation in adaptively significant traits. In the absence of available genomic data resources, transcriptomes were recently generated in Macrobrachium rosenbergii to identify candidate genes and markers potentially associated with growth. The characterisation of 47 candidate loci by ABI re-sequencing of four cultured and eight wild samples revealed 342 putative SNPs. Among these, 28 SNPs were selected in 23 growth-related candidate genes to genotype in 200 animals selected for improved growth performance in an experimental GFP culture line in Vietnam. The associations between SNP markers and individual growth performance were then examined. For additive and dominant effects, a total of three exonic SNPs in glycogen phosphorylase (additive), heat shock protein 90 (additive and dominant) and peroxidasin (additive), and a total of six intronic SNPs in ankyrin repeats-like protein (additive and dominant), rolling pebbles (dominant), transforming growth factor-β induced precursor (dominant), and UTP-glucose-1-phosphate uridylyltransferase 2 (dominant) genes showed significant associations with the estimated breeding values in the experimental animals (P = 0.001 − 0.031). Individually, they explained 2.6 − 4.8 % of the genetic variance (R 2 = 0.026 − 0.048). This is the first large set of SNP markers reported for M. rosenbergii and will be useful for confirmation of associations in other samples or culture lines as well as having applications in marker-assisted selection in future breeding programs.
Similar content being viewed by others
References
Aflalo ED, Raju DVSN, Bommi NA, Verghese JT, Samraj TYC, Hulata G et al (2012) Toward a sustainable production of genetically improved all-male prawn (Macrobrachium rosenbergii): evaluation of production traits and obtaining neo-females in three Indian strains. Aquaculture 338–341:197–207
Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Quart Rev Biol 72:149–177
Audzijonyte A, Vrijenhoek RC (2010) Three nuclear genes for phylogenetic, SNP and population genetic studies of molluscs and other invertebrates. Mol Ecol Resour 10:200–204
Avirneni-Vadlamudi U, Galindo KA, Endicott TR, Paulson V, Cameron S, Galindo RL (2012) Drosophila and mammalian models uncover a role for the myoblast fusion gene TANC1 in rhabdomyosarcoma. J Clin Invest 122:403–407
Babu KN, Pallavi PN, Reedy DC, Kalarani V (2012) Effect of 5-hydroxytryptamine and dopamine on the carbohydrate metabolism in the shrimp, Penaeus monodon (Fabricius). World J Fish Marine Sci 4:586–593
Bacca H, Huvet A, Fabioux C, Daniel JY, Delaporte M, Pouvreau S et al (2005) Molecular cloning and seasonal expression of oyster glycogen phosphorylase and glycogen synthase genes. Comp Biochem Physiol B 140:635–646
Barrick D, Ferreiro DU, Komives EA (2008) Folding landscapes of ankyrin repeat proteins: experiments meet theory. Curr Opin Struct Biol 18:27–34
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc B 57:289–300
Bennett AK, Hester PY, Spurlock DM (2007) Relationships of a transforming growth factor-β2 single nucleotide polymorphism and messenger ribonucleic acid abundance with bone and production traits in chickens. Poult Sci 86:829–834
Bouck A, Vision T (2007) The molecular ecologist’s guide to expressed sequence tags. Mol Ecol 16:907–924
Boulding EG, Culling M, Glebe B, Berg PR, Lien S, Moen T (2008) Conservation genomics of Atlantic salmon: SNPs associated with QTLs for adaptive traits in parr from four trans-Atlantic backcrosses. Heredity 101:381–391
Cesar JRO, Yang J (2007) Expression patterns of ubiquitin, heat shock protein70, α-actin and β-actin over the molt cycle in the abdominal muscle of marine shrimp Litopenaeus vannamei. Mol Reprod Dev 74:554–559
Chen K, Hawken R, Flickinger GH, Rodriguez-Zas SL, Rund LA, Wheeler MB et al (2012a) Association of the porcine transforming growth factor beta type I receptor (TGFBR1) gene with growth and carcass traits. Anim Biotechnol 23:43–63
Chen R, Irwin DM, Zhang YP (2012b) Differences in selection drive olfactory receptor genes in different direction in dogs and wolf. Mol Biol Evol 29:3475–3348
Chithra C, Devaraj H (2012) Purification and characterisation of a 48 kDa protein involved in the moulting cycle of Penaeus monodon. Food Chem 134:15–20
Ciobanu DC, Bastiaansen JWM, Magrin J, Jiang DH, Yu N, Geiger B et al (2010) A major SNP resource for dissection of phenotypic and genetic variation in Pacific white shrimp (Litopenaeus vannamei). Anim Genet 41:39–47
Cutter AD, Baird SE, Charlesworth D (2006) High nucleotide polymorphism and rapid decay of linkage disequilibrium in wild populations of Caenorhabditis remanei. Genetics 174:901–913
Denholm B, Skaer H (2009) Bringing together components of the fly renal system. Curr Opin Genet Dev 19:526–532
De-Santis C, Jerry DR (2007) Candidate growth genes in finfish: where should we be looking? Aquaculture 272:22–38
Dinh H, Coman G, Hurwood DA, Mather PB (2012) Experimental assessment of the utility of visible implant elastomer tags in a stock improvement programme for giant freshwater prawn (Macrobrachium rosenbergii) in Vietnam. Aqua Res 43:1471–1479
Dinh H, Vu NT, Nguyen NH, Ponzoni RW, Hurwood DA, Mather PM (2013) Quantitative genetic parameter estimates for body and carcass traits in a cultured stock of giant freshwater prawn (Macrobrachium rosenbergii) selected for fast growth. Aquaculture (in press)
Dong B, Liu F, Gao H, Wang B, Xiang J (2009) cDNA cloning and gene expression pattern following bacterial challenge of peroxinectin in Chinese shrimp Fenneropenaeus chinensis. Mol Biol Rep 36:2333–2339
Du ZQ, Ciobanu DC, Onteru SK, Gorbach D, Mileham AJ, Jaramillo G et al (2010) A gene-based SNP linkage map for pacific white shrimp, Litopenaeus vannamei. Anim Genet 41:286–294
Ekblom R, Galindo J (2010) Application of next generation sequencing in molecular ecology of non-model organisms. Heredity 107:1–15
Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Prentice-Hall, San Francisco
FAO (2010) Fisheries Statistical Database, Global Aquaculture Production (Fisheries Global Information System, online query)
Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rew Physiol 61:243–282
Genissel A, Pastinen T, Dowell A, Mackay TFC, Long AD (2004) No evidence for an association between common nonsynonymous polymorphisms in Delta and bristle number variation in natural and laboratory populations of Drosophila melanogaster. Genetics 166:291–306
Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2009) ASReml user guide release 3.0. VSN International Ltd., Hemel Hampstead, HP11ES UK
Gitterle T, Salte R, Gjerde B, Cock J, Johansen H, Salazar M et al (2005) Genetic (co)variation in resistance to White Spot Syndrome Virus (WSSV) and harvest weight in Penaeus (Litopenaeus) vannamei. Aquaculture 246:139–149
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
Gorbach DM, Hu ZL, Du ZQ, Rothschild MF (2009) SNP discovery in Litopenaeus vannamei with a new computational pipeline. Anim Genet 40:106–109
Gotenstein JR, Swale RE, Fukuda T, Wu Z, Giurumescu CA, Goncharov A et al (2010) The C. elegans peroxidasin PXN-2 is essential for embryonic morphogenesis and inhibits adult axon regeneration. Development 137:3603–3613
Greenberg CC, Jurczak MJ, Danos AM, Brady MJ (2006) Glycogen branches out: new perspectives on the role of glycogen metabolism in the integration of metabolic pathways. Am J Physiol Endocrinol Metab 291:E1–E8
Gruber JD, Vogel K, Kalay G, Wittkopp PJ (2012) Contrasting properties of gene-specific regulatory, coding, and copy number mutations in Saccharomyces cerevisiae: frequency, effects, and dominance. PLoS Genet 8:e1002497
Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858
Hastings ML, Resta N, Traum D, Stella A, Guanti G, Krainer AR (2005) An LKB1 ATAC intron mutation causes Peutz–Jeghers syndrome via splicing at noncanonical cryptic splice sites. Nat Struct Mol Biol 12:54–59
Hayter AJ (1984) A proof of the conjecture that the Tukey–Kramer multiple comparisons procedure is conservative. Ann Stat 12:61–75
Hsu PI, Liu CH, Tseng DY, Lee PP, Cheng W (2006) Molecular cloning and characterisation of peroxinectin, a cell adhesion molecule, from the giant freshwater prawn Macrobrachium rosenbergii. Fish Shellfish Immunol 21:1–10
Hu X, Gao Y, Feng C, Liu Q, Wang X, Du Z et al (2009) Advanced technologies for genomic analysis in farm animals and its application for QTL mapping. Genetica 136:371–386
Hull J, Campino S, Rowlands K, Chan MS, Copley RR, Taylor MS et al (2007) Identification of common genetic variation that modulates alternative splicing. PLoS Genet 3:1009–1018
Hurwood DA, Singh S, Dammannagoda ST, Nandlal S, Mather PB (2013) Experimental evaluation of the culture performance of three exotic and a ‘local’ giant freshwater prawn (Macrobrachium rosenbergii, De Man 1879) culture strain in Fiji. Aqua Res (in press)
Irimia JM, Rovira J, Nielsen JN, Guerrero M, Wojtaszewski JFP, Cussó R (2012) Hexokinase 2, glycogen synthase and phosphorylase play a key role in muscle glycogen supercompensation. PLoS One 7:e42453
Jung H, Lyons RE, Dinh H, Hurwood DA, McWilliam S, Mather PB (2011) Transriptomics of giant freshwater prawn (Macrobrachium rosenbergii): de novo assembly, annotation and marker discovery. PLoS One 6:e27938
Jung H, Lyons RE, Hurwood DA, Mather PM (2013) Genes and growth performance in crustacean species: a review of relevant genomic studies in crustaceans and other taxa. Rev Aquaculture 5:77–110
Kim WJ, Jung HT, Gaffney PM (2011) Development of type I genetic markers from expressed sequence tags in highly polymorphic species. Mar Biotechnol 13:127–132
Kimchi-Sarfaty C, Oh JM, Kim IW, Sauna ZE, Calcagno AM, Ambudkar SV et al (2007) A “silent” polymorphism in the MDR1 gene changes substrate specificity. Science 315:525–528
Kitcharoen N, Rungsin W, Koonawootrittriron S, Na-Nakorn U (2012) Heritability for growth traits in giant freshwater prawn, Macrobrachium rosenbergii (de Mann 1879) based on best linear unbiased prediction methodology. Aqua Res 43:19–25
Kruglyak L, Nickerson DA (2001) Variation is the spice of life. Nat Genet 27:234–236
Li P, Zha J, Huang H, Zhang Z, Sun H, Song D et al (2009) Identification, mRNA expression and characterization of a novel ANK-like gene from Chinese mitten crab Eriocheir japonica sinensis. Comp Biochem Physiol B 153:332–339
Liberek K, Lewandowska A, Ziętkiewicz S (2008) Chaperones in control of protein disaggregation. EMBO J 27:328–335
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Liu Z (2007) Single nucleotide polymorphism (SNP). In: Liu Z (ed) Aquaculture genome technologies. Blackwell, New York, pp 59–72
Liu XD, Zhao GT, Cai MY, Wang ZY (2013) Estimated genetic parameters for growth-related traits in large yellow croaker Larimichthys crocea using microsatellites to assign parentage. J Fish Biol (in press)
Loukovitis D, Sarropoulou E, Tsigenopoulos CS, Batargias C, Magoulas A, Apostolidis AP et al (2011) Quantitative trait loci involved sex determination and body growth in the gilthead sea bream (Sparus aurata L.) through targeted genome scan. PLoS One 6:e16599
Luan S, Yang G, Wang J, Luo K, Zhang Y, Gao Q et al (2012) Genetic parameters and response to selection for harvest body weight of the giant freshwater prawn Macrobrachium rosenbergii. Aquaculture 362–363:88–96
Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Assoc Inc., Sunderland
Lyons RE, Dierens LM, Tan SH, Preston NP, Li Y (2007) Characterization of AFLP markers associated with growth in the Kuruma prawn, Marsupenaeus japonicas, and identification of a candidate gene. Mar Biotechnol 9:712–721
Mackay TFC, Stone EA, Ayroles JF (2009) The genetics of quantitative traits: challenges and prospects. Nat Rev Genet 10:565–577
Mangel M, Stamps J (2001) Trade-offs between growth and mortality and the maintenance of individual variation in growth. Evol Ecol Res 3:583–593
Mao Y, Freeman M (2008) Fasciclin 2, the Drosophila orthologue of neural cell adhesion molecule, inhibits EGF receptor signalling. Development 136:473–481
McClelland EK, Naish KA (2010) Quantitative trait locus analysis of hatch timing, weight, length and growth rate in coho salmon, Oncorhynchus kisutch. Heredity 105:562–573
Menon SD, Osman Z, Chenchill K, Chia W (2005) A positive feedback loop between dumbfounded and rolling pebbles leads to myotube enlargement in Drosophila. J Cell Biol 169:909–920
Metzker M (2010) Sequencing technologies: the next generation. Nat Rev Genet 11:31–46
Miller SA, Dykes DD, Polesky HF (1998) A simple salting out procedure for extracting DNA from human nucleated cells. Nuc Acids Res 16:1215
Morin PA, Luikart G, Wayne RK, Grp SW (2004) SNPs in ecology, evolution and conservation. Trends Ecol Evol 19:208–216
Mosavi LK, Cammett TJ, Desrosiers DC, Peng ZY (2004) The ankyrin repeat as molecular architecture for protein recognition. Proc Natl Acad Sci U S A 13:1435–1448
Nagai C, Nagata S, Nagasawa H (2011) Effects of crustacean hyperglycaemic hormone (CHH) on the transcript expression of carbohydrate metabolism-related enzyme genes in the kuruma prawn, Marsupenaeus japonicas. Gen Comp Endocrinol 172:293–304
Oliveira GT, Rossi IC, Kucharski LC, Da Silva RS (2004) Hepatopancreas gluconeogenesis and glycogen content during fasting in crabs previously maintained on a high-protein or carbohydrate-rich diet. Comp Biochem Physiol A 137:383–390
Pagani F, Baralle FE (2004) Genomic variants in exons and introns: indentifying the splicing spoilers. Nat Rev Genet 5:389–396
Panphut W, Senapin S, Sriurairatana S, Withyachumanarnkul B, Flegel TW (2011) A novel integrase-containing element may interact with Laem–Singh virus (LSNV) to cause slow growth in giant tiger shrimp. BMC Vet Res 7:18
Pillai BR, Mahapatra KD, Ponzoni RW, Sahoo L, Lalrinsanga PL, Nguyen NH et al (2011) Genetic evaluation of a complete diallel cross involving three populations of freshwater prawn (Macrobrachium rosenbergii) from different geographical regions of India. Aquaculture 319:347–354
Rafter JA, Abell ML, Braselton JP (2002) Multiple comparison methods for means. Soc Ind Appl Math 44:259–279
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Reddy PS, Reddy PR, Pushpalatha T (2007) Differential mode of action of hyperglycaemic hormones obtained from crab (Crustacea) and millipede (Myriapoda) in the crab, Oziotelphusa senex senex. J Biol Sci 7:141–152
Rezvani Gilkolaei S, Safari R, Laloei F, Taqavi J, Matinfar A (2011) Using RAPD markers potential to identify heritability for growth in Fenneropenaeus indicus. Iran J Fish Sci 10:123–134
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Rousset F (2008) Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106
Rubtsov AM, Lopina OD (2000) Ankyrins. FEBS Lett 482:1–5
SAS Institute (2002). SAS OnlineDoc, Version 8.2. SAS Institute Inc.: Cary, NC, USA
Sauvage C, Bierne N, Lapègue S, Boudry P (2007) Single nucleotide polymorphisms and their relationship to codon usage bias in the Pacific oyster Crassostrea gigas. Gene 406:13–22
Schneider KJ, Tidwell JH, Gomelsky B, Pomper KW, Waldbieser GC, Saillant E et al. (2013) Genetic diversity of cultured and wild populations of the giant freshwater prawn Macrobrachium rosenbergii (de Man, 1879) based on microsatellite analysis. Aqua Res (in press)
Schwantes VS, Diana JS, Yi Y (2009) Social, economic, and production characteristics of giant freshwater prawn Macrobrachium rosenbergii culture in Thailand. Aquaculture 287:120–127
Seeb JE, Carvalho G, Hauser L, Naish K, Roberts S, Seeb LW (2011) Single-nucleotide polymorphism (SNP) discovery and applications of SNP genotyping in nonmodel organisms. Mol Ecol Resour 11S1:1–8
Small KS, Brudno M, Hill MM, Sidow A (2007) Extreme genomic variation in a natural population. PNAS 104:5698–5703
Soudi M, Zamocky M, Jakopitsch C, Furtmüller PG, Obinger C (2012) Molecular evolution, structure, and function of peroxidasins. Chem Biodivers 9:1776–1793
Spees JL, Chang SA, Mykles DL, Snyder MJ, Chang ES (2003) Molt cycle-dependent molecular chaperone and polyubiquitin gene expression in lobster. Cell Stress Chaperones 3:258–264
Sritunyalucksana K, Wongsuebsantati K, Johansson MW, Söderhäll (2001) Peroxinectin, a cell adhesive protein associated with the proPO system from the black tiger shrimp, Penaeus monodon. Dev Comp Immunol 25:353–363
Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction. Am J Hum Genet 73:1162–1169
Sun L, Dong X, Fan B, Liu B (2011) The association of ANKRD2 with loin depth and muscle firmness in pigs. J Anim Vet Adv 10:1462–1468
Sundstrom LF, Lohmus M, Devlin RH (2005) Selection on increased intrinsic growth rates in coho salmon, Oncorhynchus kisutch. Evolution 59:1560–1569
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 28:2731–2739
Tangprasittipap A, Tiensuwan M, Withyachumnarnkul B (2010) Characterization of candidate genes involved in growth of black tiger shrimp Penaeus monodon. Aquaculture 307:150–156
Tao W, Boulding EG (2003) Associations between single nucleotide polymorphisms in candidate genes and growth rate in Arctic charr (Salvelinus alpines L.). Heredity 91:60–69
Thanh NM, Ponzoni R, Nguyen NH, Vu NT, Barnes A, Mather PB (2009) Evaluation of growth performance in a diallel cross of three strains of giant freshwater prawn (Macrobrachium rosenbergii) in Vietnam. Aquaculture 287:75–83
Thanh NM, Nguyen NH, Ponzoni RW, Vu NT, Barnes AC, Mather PB (2010a) Estimates of strain additive and non-additive genetic effects for growth traits in a diallel cross of three strains of giant freshwater prawn (Macrobrachium rosenbergii) in Vietnam. Aquaculture 299:30–36
Thanh NM, Barnes AC, Mather PB, Yutao L, Lyons RE (2010b) 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 301:7–15
Thoden JB, Holden HM (2006) The molecular architecture of glucose-1-phosphate uridylyltransferase. Proc Natl Acad Sci U S A 16:432–440
Tindall AJ, Elizabeth M, Pownall E, Morris ID, Issacs HV (2005) Xenopus tropicalis peroxidasin gene is expressed within the developing neural tube and pronephric kidney. Dev Dyn 232:377–384
Verhoeven KJ, Simonsen KL, McIntyre LM (2005) Implementing false discovery rate control: increasing your power. Oikos 108:643–647
Wang S, Peatman E, Abernathy J, Waldbieser G, Lindquist E, Richardson P et al (2010) Assembly of 500,000 inter-specific catfish expressed sequence tags and large scale gene-associated marker development for whole genome association studies. Genome Biol 11:R8
Zhang L, Guo X (2010) Development and validation of single nucleotide polymorphism markers in the eastern oyster Crassostrea virginica Gmelin by mining ESTs and resequencing. Aquacutlrue 302:124–129
Acknowledgements
Authors wish to thank to Dr. Woo-Jin Kim, Dr. Peter Prentis and two anonymous reviewers for useful comments. This research forms a part of Hyungtaek Jung’s PhD project, and is supported by an International Postgraduate Research Scholarship (Australia) and a Queensland University of Technology Postgraduate Award (N7333978). Additional funding for this work was provided by Queensland University of Technology awarded to Peter B. Mather (VC NPSG award).
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
ESM 1
(FAS 2 kb)
ESM 2
(FAS 2 kb)
ESM 3
(FAS 3 kb)
ESM 4
(FAS 4 kb)
ESM 5
(FAS 9 kb)
ESM 6
(FAS 5 kb)
ESM 7
(FAS 3 kb)
ESM 8
(FAS 5 kb)
ESM 9
(FAS 7 kb)
ESM 10
(FAS 3 kb)
ESM 11
(FAS 0 kb)
ESM 12
(FAS 3 kb)
ESM 13
(FAS 3 kb)
ESM 14
(FAS 6 kb)
ESM 15
(FAS 4 kb)
ESM 16
(FAS 5 kb)
ESM 17
(FAS 4 kb)
ESM 18
(FAS 3 kb)
ESM 19
(FAS 2 kb)
ESM 20
(FAS 10 kb)
ESM 21
(FAS 3 kb)
ESM 22
(FAS 3 kb)
ESM 23
(FAS 7 kb)
ESM 24
(FAS 3 kb)
ESM 25
(FAS 3 kb)
ESM 26
(FAS 6 kb)
ESM 27
(FAS 3 kb)
ESM 28
(FAS 3 kb)
ESM 29
(FAS 5 kb)
ESM 30
(FAS 4 kb)
ESM 31
(FAS 2 kb)
ESM 32
(FAS 2 kb)
ESM 33
(FAS 5 kb)
ESM 34
(FAS 2 kb)
ESM 35
(FAS 4 kb)
ESM 36
(FAS 2 kb)
ESM 37
(FAS 8 kb)
ESM 38
(FAS 3 kb)
ESM 39
(FAS 2 kb)
ESM 40
(FAS 6 kb)
ESM 41
(FAS 2 kb)
ESM 42
(FAS 2 kb)
ESM 43
(FAS 2 kb)
ESM 44
(FAS 4 kb)
ESM 45
(FAS 5 kb)
ESM 46
(FAS 2 kb)
ESM 47
(FAS 2 kb)
ESM 48
(XLSX 117 kb)
Rights and permissions
About this article
Cite this article
Jung, H., Lyons, R.E., Li, Y. et al. A Candidate Gene Association Study for Growth Performance in an Improved Giant Freshwater Prawn (Macrobrachium rosenbergii) Culture Line. Mar Biotechnol 16, 161–180 (2014). https://doi.org/10.1007/s10126-013-9555-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-013-9555-7