Cite this paper:
LU Xia, LUAN Sheng, KONG Jie, HU Longyang, MAO Yong, ZHONG Shengping. Genome-wide mining, characterization, and development of microsatellite markers in Marsupenaeus japonicus by genome survey sequencing[J]. Journal of Oceanology and Limnology, 2017, 35(1): 203-214

Genome-wide mining, characterization, and development of microsatellite markers in Marsupenaeus japonicus by genome survey sequencing

LU Xia1, LUAN Sheng1, KONG Jie1, HU Longyang1, MAO Yong2, ZHONG Shengping2
1 Key Laboratory for Sustainable Utilization of Marine Fisheries Resources, Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China;
2 College of Ocean and Earth Sciences, Xiamen University, Xiamen 361005, China
Abstract:
The kuruma prawn, Marsupenaeus japonicus, is one of the most cultivated and consumed species of shrimp. However, very few molecular genetic/genomic resources are publically available for it. Thus, the characterization and distribution of simple sequence repeats (SSRs) remains ambiguous and the use of SSR markers in genomic studies and marker-assisted selection is limited. The goal of this study is to characterize and develop genome-wide SSR markers in M. japonicus by genome survey sequencing for application in comparative genomics and breeding. A total of 326 945 perfect SSRs were identified, among which dinucleotide repeats were the most frequent class (44.08%), followed by mononucleotides (29.67%), trinucleotides (18.96%), tetranucleotides (5.66%), hexanucleotides (1.07%), and pentanucleotides (0.56%). In total, 151 541 SSR loci primers were successfully designed. A subset of 30 SSR primer pairs were synthesized and tested in 42 individuals from a wild population, of which 27 loci (90.0%) were successfully amplified with specific products and 24 (80.0%) were polymorphic. For the amplified polymorphic loci, the alleles ranged from 5 to 17 (with an average of 9.63), and the average PIC value was 0.796. A total of 58 256 SSR-containing sequences had significant Gene Ontology annotation; these are good functional molecular marker candidates for association studies and comparative genomic analysis. The newly identified SSRs significantly contribute to the M. japonicus genomic resources and will facilitate a number of genetic and genomic studies, including high density linkage mapping, genome-wide association analysis, marker-aided selection, comparative genomics analysis, population genetics, and evolution.
Key words:    Marsupenaeus japonicus|genome-wide SSR markers|genome survey sequencing|functional annotation   
Received: 2015-10-08   Revised: 2015-11-04
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References:
Ansari M J, Al-Ghamdi A, Kumar R, Usmani S, Al-Attal Y, Nuru A, Mohamed A A, Singh K, Dhaliwal H S. 2013.Characterization and gene mapping of a chlorophylldeficient mutant clm1 of Triticum monococcum L.Biologia Plantarum, 57(3): 442-448.
Barchi L, Lanteri S, Portis E, Acquadro A, Valè G, Toppino L, Rotino G L. 2011. Identification of SNP and SSR markers in eggplant using RAD tag sequencing. BMC Genomics, 12: 304.
Barzegar R, Peyvast G, Ahadi A M, Rabiei B, Ebadi A A, Babagolzadeh A. 2013. Biochemical systematic, population structure and genetic variability studies among Iranian Cucurbita (Cucurbita pepo L.) accessions, using genomic SSRs and implications for their breeding potential. Biochemical System atics and Ecology, 50: 187-198.
Bhargava A, Fuentes F F. 2010. Mutational dynamics of microsatellites. Molecular Biotechnology, 44(3): 250-266, http://dx.doi.org/10.1007/s12033-009-9230-4.
Biswas M K, Xu Q, Mayer C, Deng X X, Niedz R P. 2014.Genome wide characterization of short tandem repeat markers in sweet orange (Citrus sinensis). PLoS One, 9(8): e104182, http://dx.doi.org/10.1371/journal.pone.0104182.
Bohra A, Dubey A, Saxena R K, Penmetsa R V, Poornima K N, Kumar N, Farmer A D, Srivani G, Upadhyaya H D, Gothalwal R, Ramesh S, Singh D, Saxena K, Kishor P B K, Singh N K, Town C D, May G D, Cook D R, Varshney R K. 2011. Analysis of BAC-end sequences (BESs) and development of BES-SSR markers for genetic mapping and hybrid purity assessment in pigeonpea (Cajanus spp.). BMC Plant Biology, 11: 56.
Bohra A, Jha U C, Kavi Kishor P B, Pandey S, Singh N P. 2014. Genomics and molecular breeding in lesser explored pulse crops: current trends and future opportunities.Biotechnology Advances, 32(8): 1 410-1 428.
Bruford M W, Wayne R K. 1993. Microsatellites and their application to population genetic studies. Current Opinion in Genetics & Development, 3(6): 939-943.
Cardle L, Ransay L, Milbourne D, Macaulay M, Marshall D, Waugh R. 2000. Computational and experimental characterization of physically clustered simple sequence repeats in plants. Genetics, 156(2): 847-854.
Castoe T A, Polle A W, Gu W J, de Koning A P J, Daza L M, Smith E N, Pollock D D. 2010. Rapid identification of thousands of copperhead snake (Agkistrodon contortrix)microsatellite loci from modest amounts of 454 shotgun genome sequence. Molecular Ecology Resource, 10(2):341-347.
Castoe T A, Poole A W, de Koning A P J, Jones K L, Tomback D F, Oyler-McCance S J, Fike J A, Lance S L, Streicher J W, Smith E N, Pollock D D, Hansson B. 2012. Rapid microsatellite identification from illumina paired-end genomic sequencing in two birds and a snake. PLoS One, 7(2): e30953, http://dx.doi.org/10.1371/journal.pone.0030953.
Cavagnaro P F, Senalik D A, Yang L M, Simon P W, Harkins T T, Kodira C D, Huang S W, Weng Y Q. 2010. Genomewide characterization of simple sequence repeats in cucumber (Cucumis sativus L.). BMC Genomics, 11: 569.
Cheng L, Liao X, Yu X, Tong J. 2007. Development of ESTSSRs by an efficient FIASCO-based strategy: a case study in rare minnow (Gobiocyrpis Rarus). Animal Biotechnology, 18(3): 143-152.
Cruz F, Pérez M, Prese P. 2005. Distribution and abundance of microsatellites in the genome of bivalves. Gene, 346: 241-247.
Doulati-Baneh H, Mohammadi S A, Labra M. 2013. Genetic structure and diversity analysis in Vitis vinifera L.cultivars from Iran using SSR markers. Scientia Horticulturae, 160: 29-36.
Guichoux E, Lagache L, Wagner S, Chaumeil P, Léger P, Lepais O, Lepoittevin C, Malausa T, Revardel E, Salin F, Petit R J. 2011. Current trends in microsatellite genotyping.Molecular Ecology Resource, 11(4): 591-611.
Guo E M, Cui Z X, Wu D H, Hui M, Liu Y, Wang H X. 2013.Genetic structure and diversity of Portunus trituberculatus in Chinese population revealed by microsatellite markers.Biochemical System atics and Ecology, 50: 313-321.
Hancock J M. 1995. The contribution of slippage-like processes to genome evolution. Journal of Molecular Evolution, 41(6): 1 038-1 047.
Hewitt D R, Duncan P F. 2001. Effect of high water temperature on the survival, moulting and food consumption of Penaeus (Marsupenaeus) japonicus (Bate, 1888).Aquaculture Research, 32(4): 305-313.
Hoffman J I, Nichols H J. 2011. A novel approach for mining polymorphic microsatellite markers in silico. PLoS One, 6: e23283, http://dx.doi.org/10.1371/journal.pone.0023283.
Holthuis L B. 1980. FAO Species Catalogue. Vol. 1. Shrimps and Prawns of the World. An Annotated Catalogue of Species of Interest to Fisheries. FAO Fisheries Synopsis, No. 125, 1. Food and Agricultural Organization of the United Nations, Rome. 271p.
Hosseini A, Ranade S H, Ghosh I, Khandekar P. 2008. Simple sequence repeats in different genome sequences of Shigella and comparison with high GC and AT-rich genomes. DNA Sequence, 19(3): 167-176, http://dx.doi.org/10.1080/10425170701461730.
Iranawati F, Jung H, Chand V, Hurwood D A, Mather P B. 2012. Analysis of genome survey sequences and SSR marker development for Siamese mud carp, H enicorhynchus siamensis, using 454 pyrosequencing.International Journal of Molecular Sciences, 13(12):10 807-10 827.
Jarne P, Lagodav P J L. 1996. Microsatellites, from molecules to populations and back. Trends in Ecology & Evolution, 11(10): 424-429.
Jennings T N, Knaus B J, Mullins T D, Haiq S M, Cronn R C. 2011. Multiplexed microsatellite recovery using massively parallel sequencing. Molecular Ecology Resource, 11(6):1 060-1 067.
Ji P F, Liu G M, Xu J, Wang X M, Li J T, Zhao Z X, Zhang X F, Zhang Y, Xu P, Sun X W, Liu Z J. 2012. Characterization of common carp transcriptome: sequencing, de novo assembly, annotation and comparative genomics. PLoS One, 7(4): e35152.
Jiao W Q, Fu X T, Dou J Z, Li H D, Su H L, Mao J X, Yu Q, Zhang L L, Hu X L, Huang X T, Wang Y F, Wang S, Bao Z M. 2014. High-resolution linkage and quantitative trait locus mapping aided by genome survey sequencing:building up an integrative genomic framework for a bivalve mollusc. DNA Research, 21(1): 85-101.
Jurka J, Pethiyagod C. 1995. Simple repetitive DNA sequences from primates: compilation and analysis. Journal of Molecular Evolution, 40(2): 120-126.
Kashi Y, King D, Soller M. 1997. Simple sequence repeats as a source of quantitative genetic variation. Trends in Genetics, 13(2): 74-78.
Kofler R, Schlotterer C, Lelley T. 2007. SciRoKo: a new tool for whole genome microsatellite search and investigation.Bioinformatics, 23(13): 1 683-1 685.
Kohany O, Gentles A J, Hankus L, Jurka J. 2006. Annotation, submission and screening of repetitive elements in repbase: repbase submitter and censor. BMC Bioinformatics, 7: 474.
Králová-Hromadová I, Minárik G, Bazsalovicsová E, Mikulíček P, Oravcová A, Pálková L, Hanzelová V. 2015.Development of microsatellite markers in Caryophyllaeus laticeps (Cestoda: Caryophyllidea), monozoic fish tapeworm, using next-generation sequencing approach.Parasitology Research, 114(2): 721-726.
Kumpatla S P, Mukhopadhyay S. 2005. Mining and survey of simple sequence repeats in expressed sequence tags of dicotyledonous species. Genome, 48(6): 985-998.
Lee G A, Sung J S, Lee S Y, Chung J W, Yi J Y, Kim Y G, Lee M C. 2014. Genetic assessment of safflower (Carthamus tinctorius L.) collection with microsatellite markers acquired via pyrosequencing method. Molecular Ecology Resource, 14(1): 69-78, http://dx.doi.org/10.1111/1755-0998.12146.
Li R Q, Fan W, Tian G et al. 2010. The sequence and de novo assembly of the giant panda genome. Nature, 463(7279):311-317.
Liu H F, Li S Q, Hu P, Zhang Y Y, Zhang J B. 2013. Isolation and characterization of EST-based microsatellite markers for Scatophagus argus based on transcriptome analysis.Conservation Genetic s Research, 5(2): 483-485, http://dx.doi.org/10.1007/s12686-012-9833-0.
Martins W S, Lucas D C S, Neves K F S, Bertioli D J. 2009.WebSat-A web software for microsatellite marker development. Bioinformation, 3(6): 282-283.
Miller M R, Dunhamv J P, Amores A, Cresko W A, Johnson E A. 2007. Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. Genome Research, 17(2): 240-248.
Nagy I, Stágel A, Sasvári Z, Röder M, Ganal M. 2007.Development, characterization, and transferability to other Solanaceae of microsatellite markers in pepper(Capsicum annuum L.). Genom e, 50(7): 668-688.
Nybom H, Weising K, Rotter B. 2014. DNA fingerprinting in botany: past, present, future. Invest igative Genetic, 5: 1, http://dx.doi.org/10.1186/2041-2223-5-1.
Parobek C M, Jiang L Y, Patel J C, Alvarez-Martínez M J, Miro J M, Worodria W, Andama A, Fong S, Huang L, Meshnick S R, Taylor S M, Juliano J J. 2014. Multilocus microsatellite genotyping array for investigation of genetic epidemiology of Pneumocystis jirovecii. Journal of Clinical Microbiology, 52(5): 1 391-1 399.
Rowe H C, Renaut S, Guggisberg A. 2011. RAD in the realm of next-generation sequencing technologies. Molecular Ecology, 20(17): 3 499-3 502.
Schlötterer C, Tautz D. 1992. Slippage synthesis of simple sequence DNA. Nucleic Acids Research, 20(2): 211-215.
Shikano T, Ramadevi J, Shimada Y, Merilä J. 2010. Utility of sequenced genomes for microsatellite marker development in non-model organisms: a case study of functionally important genes in nine-spined sticklebacks (Pungitius pungitius). BMC Genomics, 11: 334, http://dx.doi.org/10.1186/1471-2164-11-334.
Shirasawa K, Asamizu E, Fukuoka H, Ohyama A, Sato S, Nakamura Y, Tabata S, Sasamoto S, Wada T, Kishida Y, Tsuruoka H, Fujishiro T, Yamada M, Isobe S. 2010. An interspecific linkage map of SSR and intronic polymorphism markers in tomato. Theoretical and Applied Genetics, 121(4): 731-739.
Sinden R R. 1999. Biological implications of the DNA structures associated with disease-causing triplet repeats.American Journal of Human Genetic, 64(2): 346-353.
Smee M R, Pauchet Y, Wilkinson P, Wee B, Singer M C, ffrench-Constant R H, Hodgson D J, Mikheyev A S. 2013.Microsatellites for the marsh fritillary butterfly: de novo transcriptome sequencing, and a comparison with amplified fragment length polymorphism (AFLP)markers. PLoS One, 8(1): e54721.
Somridhivej B, Wang S L, Sha Z X, Liu H, Quilang J, Xu P, Li P, Hu Z L, Liu Z J. 2008. Characterization, polymorphism assessment, and database construction for microsatellites from BAC end sequences of channel catfish (Ictalurus punctatus): a resource for integration of linkage and physical maps. Aquaculture, 275(1-4): 76-80.
Stàgel A, Portis E, Toppino L, Rotino G L, Lanteri S. 2008.Gene-based microsatellite development for mapping and phylogeny studies in eggplant. BMC Genomics, 9: 357.
Strong W B, Nelson R G. 2000. Preliminary profile of the Cryptosporidium parvum genome: An expressed sequence tag and genome survey sequence analysis. Molecular and Biochemical Parasitology, 107(1): 1-32.
Subramanian S, Mishra R K, Singh L. 2003. Genome-wide analysis of microsatellite repeats in humans: their abundance and density in specific genomic regions.Genome Biology, 4: R13, http://dx.doi.org/10.1186/gb-2003-4-2-r13.
Tadano R, Nunome M, Mizutani M, Kawahara-Miki R, Fujiwara A, Takahashi S, Kawashima T, Nirasawa K, Ono T, Kono T, Matsuda Y. 2014. Cost-effective development of highly polymorphic microsatellite in Japanese quail facilitated by next-generation sequencing. Animal Genetics, 45(6): 881-884.
Tanguy A, Bierne N, Saavedra C et al. 2008. Increasing genomic information in bivalves through new EST collections in four species: development of new genetic markers for environmental studies and genome evolution.Gene, 408(1-2): 27-36.
Tautz D, Renz M. 1984. Simple sequences are ubiquitous repetitive components of eukaryotic genomes. Nucleic Acids Research, 12(10): 4 127-4 138.
Tautz D, Trick M, Dover G A. 1986. Cryptic simplicity in DNA is a major source of genetic variation. Nature, 322(6080): 652-656.
Thanh N M, Jung H, Lyons R E, Chand V, Tuan N V, Thu V T M, Mather P. 2014. A transcriptomic analysis of striped catfish (Pangasianodon hypophthalmus) in response to salinity adaptation: De novo assembly, gene annotation and marker discovery. Comparative Biochemistry and Physiology P art D: Genomics and Proteomics, 10: 52-63.
Tóth G, Gáspári Z, Jurka J. 2000. Microsatellites in different eukaryotic genomes: survey and analysis. Genome Research, 10(7): 967-981.
Touriol C, Bornes S, Bonnal S, Audigier S, Prats H, Prats A C, Vagner S. 2003. Generation of protein isoform diversity by alternative initiation of translation at non-AUG codons.Biology of the Cell, 95(4): 169-178, http://dx.doi.org/10.1016/S0248-4900(03)00033-9.
Triwitayakorn K, Chatkulkawin P, Kanjanawattanawong S, Sraphet S, Yoocha T, Sangsrakru D, Chanprasert J, Ngamphiw C, Jomchai N, Therawattanasuk K, Tangphatsornruang S. 2011. Transcriptome sequencing of Hevea brasiliensis for development of microsatellite markers and construction of a genetic linkage map. DNA Research, 18(6): 471-482.
Turanov A A, Lobanov A V, Fomenko D E, Morrison H G, Sogin M L, Klobutcher L A, Hatfield D L, Gladyshev V N. 2009. Genetic code supports targeted insertion of two amino acids by one codon. Science, 323(5911): 259-261, http://dx.doi.org/10.1126/science.1164748.
Varshney R K, Graner A, Sorrells M E. 2005. Genic microsatellite markers in plants: features and applications.Trends in Biotechnology, 23(1): 48-55.
Vukosavljev M, Di Guardo M, van de Weg W E, Arens P, Smulders M J M. 2012. Quantification of Allele Dosage in tetraploid Roses. Science MED (Bologna), 3: 277-282.
Vukosavljev M, Zhang J, Esselink G D, van’t Westende W P C, Cox P, Visser R G F, Arens P, Smulders M J M. 2013.Genetic diversity and differentiation in roses: a garden rose perspective. Science Horticulturae, 162: 320-332, http://dx.doi.org/10.1016/j.scienta.2013.08.015.
Wahba A J, Gardner R S, Basilio C, Miller R S, Speyer J F, Lengyel P. 1963. Synthetic polynucleotides and the amino acid code. VⅢ. Proceedings of the National Academy of Sciences of the United States of America, 49: 116-122.
Wang H X, Huan P, Lu X, Liu B Z. 2011. Mining of EST-SSR markers in clam Meretrix meretrix larvae from 454 shotgun transcriptome. Genes & Genetic System, 86(3):197-205.
Wang J Y, Song X M, Li Y, Hou X L. 2013. In-silico detection of EST-SSR markers in three Brassica species and transferability in B. rapa. The Journal of Horticultural Science & Biotechnology, 88(2): 135-140.
Wang W J, Kong J, Dong S R, Luan S, Wang Q Y. 2006.Genetic mapping of the Chinese shrimp Fenneropenaeus chinensis using AFLP markers. Acta Zoologica Sinica, 52(3): 575-584. (in Chinese with English abstract)
Weber J L, Wong C. 1993. Mutation of human short tandem repeats. Human Molecular Genetics, 2(8): 1 123-1 128.
Xu P X, Wu X H, Luo J, Wang B G, Liu Y H, Ehlers J D, Wang S, Lu Z F, Li G J. 2011. Partial sequencing of the bottle gourd genome reveals markers useful for phylogenetic analysis and breeding. BMC Genomics, 12: 467.
Xu P X, Xu S Z, Wu X H, Tao Y, Wang B G, Wang S, Qin D H, Lu Z F, Li G J. 2014. Population genomic analyses from low-coverage RAD-Seq data: a case study on the nonmodel cucurbit bottle gourd. The Plant Journal, 77(3):430-442, http://dx.doi.org/10.1111/tpj.12370.
Yuan S X, Ge L, Liu C, Ming J. 2013. The development of EST-SSR markers in Lilium regale and their crossamplification in related species. Euphytica, 189(3): 393-419.
Zane L, Bargelloni L, Patarnello T. 2002. Strategies for microsatellite isolation: a review. Molecular Ecology, 11(1): 1-16.
Zeng S H, Xiao G, Guo J, Fei Z J, Xu Y Q, Roe B A, Wang Y. 2010. Development of a EST dataset and characterization of EST-SSRs in a traditional Chinese medicinal plant, Epimedium sagittatum (Sieb. Et Zucc.) Maxim. BMC Genomics, 11: 94.
Zhou W, Hu Y Y, Sui Z H, Fu F, Wang J G, Chang L P, Guo W H, Li B B, Sun H. 2013. Genome survey sequencing and genetic background characterization of Gracilariopsis lemaneiformis (Rhodophyta) based on next-generation sequencing. PLoS One, 8(7): e69909, http://dx.doi.org/10.1371/journal.pone.0069909.
Zitouna N, Marghali S, Gharbi M, Chennaoui-Kourda H, Haddioui A, Trifi-Farah N. 2013. Mediterranean Hedysarum phylogeny by transferable microsatellites from Medicago. Biochemical System atics and Ecology, 50: 129-135.
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