Skip to main content
SpringerLink
Log in

Construction of a Genomic Bacterial Artificial Chromosome (BAC) Library for the Prawn Macrobrachium rosenbergii and Initial Analysis of ZW Chromosome-Derived BAC Inserts

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Knowledge on sex determination has proven valuable for commercial production of the prawn Macrobrachium rosenbergii due to sex dimorphism of the male and female individuals. Previous studies indicated that prawn sex is determined by a ZW–ZZ chromosomal system, but no genomic information is available for the sex chromosome. Herein, we constructed a genomic bacterial artificial chromosome (BAC) library and identified the ZW-derived BAC clones for initial analysis of the sex chromosomal DNA sequence. The arrayed BAC library contains 200,448 clones with average insert size of 115.4 kb, corresponding to ∼ 4× coverage of the estimated 5.38 Gb genome. Based on a short female-specific marker, a Z- and a W-fragment were retrieved with the genomic walking method. Screening the BAC library using a ZW-specific marker as probe resulted in 12 positive clones. From these, a Z-derived (P331M17) and a W-derived (P122G2) BAC clones were randomly selected and sequenced by PacBio method. We report the construction of a large insert, deep-coverage, and high-quality BAC library for M. rosenbergii that provides a useful resource for positional cloning of target genes, genomic organization, and comparative genomics analysis. Our study not only confirmed the ZW/ZZ system but also discovered sex-linked genes on ZW chromosomes for the first time, contributing to a comprehensive understanding of the genomic structure of sex chromosomes in M. rosenbergii.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aflalo ED, Hoang TTT, Nguyen VH, Lam Q, Nguyen DM, Trinh QS, Raviv S, Sagi A (2006) A novel two-step procedure for mass production of all-male populations of the giant freshwater prawn Macrobrachium rosenbergii. Aquaculture 256:468–478

    Article  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Becking T, Giraud I, Raimond M, Moumen B, Chandler C, Cordaux R, Gilbert C (2017) Diversity and evolution of sex determination systems in terrestrial isopods. Sci Rep 7:1084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonami JR, Widada JS (2011) Viral diseases of the giant fresh water prawn Macrobrachium rosenbergii: a review. J Invertebr Pathol 106:131–142

    Article  PubMed  Google Scholar 

  • Botstein D, Risch N (2003) Discovering genotypes underlying human phenotypes: past successes for mendelian disease, future approaches for complex disease. Nat Genet 33:228–237

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118–128

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Zhang G, Shao C, Huang Q, Liu G, Zhang P, Song W, An N, Chalopin D, Volff JN, Hong Y, Li Q, Sha Z, Zhou H, Xie M, Yu Q, Liu Y, Xiang H, Wang N, Wu K, Yang C, Zhou Q, Liao X, Yang L, Hu Q, Zhang J, Meng L, Jin L, Tian Y, Lian J, Yang J, Miao G, Liu S, Liang Z, Yan F, Li Y, Sun B, Zhang H, Zhang J, Zhu Y, Du M, Zhao Y, Schartl M, Tang Q, Wang J (2014) Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat Genet 46:253–260

    Article  CAS  PubMed  Google Scholar 

  • Chin CS, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, Clum A, Copeland A, Huddleston J, Eichler EE, Turner SW, Korlach J (2013) Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10:563–569

    Article  CAS  PubMed  Google Scholar 

  • Cui Z, Hui M, Liu Y, Song C, Li X, Li Y, Liu L, Shi G, Wang S, Li F, Zhang X, Liu C, Xiang J, Chu KH (2015) High-density linkage mapping aided by transcriptomics documents ZW sex determination system in the Chinese mitten crab Eriocheir sinensis. Heredity 115:206–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dalton JE, Fear JM, Knott S, Baker BS, McIntyre LM, Arbeitman MN (2013) Male-specific fruitless isoforms have different regulatory roles conferred by distinct zinc finger DNA binding domains. BMC Genomics 14:659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dan C, Mei J, Wang D, Gui JF (2013) Genetic differentiation and efficient sex-specific marker development of a pair of Y- and X-linked markers in yellow catfish. Int J Biol Sci 9:1043–1049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5:e11147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dolezel J, Bartos J, Voglmayr H, Greilhuber J (2003) Nuclear DNA content and genome size of trout and human. Cytometry 51A:127–128

    Article  Google Scholar 

  • Faber-Hammond JJ, Phillips RB, Brown KH (2015) Comparative analysis of the shared sex-determination region (SDR) among salmonid fishes. Genome Biol Evol 7:1972–1987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ford AT (2008) Can you feminise a crustacean? Aquat Toxicol 88:316–321

    Article  CAS  PubMed  Google Scholar 

  • Gatto KP, Mattos JV, Seger KR, Lourenco LB (2018) Sex chromosome differentiation in the frog genus Pseudis involves satellite DNA and chromosome rearrangements. Front Genet 9:301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Genet C, Dehais P, Palti Y, Gao G, Gavory F, Wincker P, Quillet E, Boussaha M (2011) Analysis of BAC-end sequences in rainbow trout: content characterization and assessment of synteny between trout and other fish genomes. BMC Genomics 12:314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gong SC, Yang XW, Li CJ, Heintz N (2002) Highly efficient modification of bacterial artificial chromosomes (BACs) using novel shuttle vectors containing the R6K gamma origin of replication. Genome Res 12:1992–1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gregory TR (2018) Animal genome size database. http://www.genomesize.com. Accessed 15 Sept 2018

  • Jiang XH, Qiu GF (2013) Female-only sex-linked amplified fragment length polymorphism markers support ZW/ZZ sex determination in the giant freshwater prawn Macrobrachium rosenbergii. Anim Genet 44:782–785

    Article  CAS  PubMed  Google Scholar 

  • Jiang L, You W, Zhang X, Xu J, Jiang Y, Wang K, Zhao Z, Chen B, Zhao Y, Mahboob S, Al-Ghanim KA, Ke C, Xu P (2016) Construction of the BAC library of small abalone (Haliotis diversicolor) for gene screening and genome characterization. Mar Biotechnol 18:49–56

    Article  CAS  Google Scholar 

  • Katagiri T, Asakawa S, Hirono I, Aoki T, Shimizu N (2000) Genomic bacterial artificial chromosome library of the Japanese flounder Paralichthys olivaceus. Mar Biotechnol 2:571–576

    Article  CAS  Google Scholar 

  • Koerich LB, Dupim EG, Faria LL, Dias FA, Dias AF, Trindade GS, Mesquita RD, Carvalho AB (2016) First report of Y-linked genes in the kissing bug Rhodnius prolixus. BMC Genomics 17:100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koyama T, Asakawa S, Katagiri T, Shimizu A, Fagutao FF, Mavichak R, Santos MD, Fuji K, Sakamoto T, Kitakado T, Kondo H, Shimizu N, Aoki T, Hirono I (2010) Hyper-expansion of large DNA segments in the genome of kuruma shrimp, Marsupenaeus japonicus. BMC Genomics 11:141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lecher P, Defaye D, Noel P (1995) Chromosomes and nuclear DNA of Crustacea. Invertebr Reprod Dev 27:85–114

    Article  Google Scholar 

  • Lee TH, Naitoh N, Yamazaki F (2004) Chromosome studies on the mitten crabs Eriocheir japonica and E. sinensis. Fish Sci 70:211–214

    Article  CAS  Google Scholar 

  • Li Y, Liu S, Qin Z, Waldbieser G, Wang R, Sun L, Bao L, Danzmann RG, Dunham R, Liu Z (2015) Construction of a high-density, high-resolution genetic map and its integration with BAC-based physical map in channel catfish. DNA Res 22:39–52

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Jiang Y, Wang S, Ninwichian P, Somridhivej B, Xu P, Abernathy J, Kucuktas H, Liu Z (2009) Comparative analysis of catfish BAC end sequences with the zebrafish genome. BMC Genomics 10:592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu L, Cui Z, Xia SCW, Liu Y, Hui M, Wang CL (2016a) Flow cytometric analysis of DNA content for four commercially important crabs in China. Acta Oceanol Sin 35:7–11

    Article  CAS  Google Scholar 

  • Liu ZJ, Liu SK, Yao J, Bao LS, Zhang JR, Li Y, Jiang C, Sun LY, Wang RJ, Zhang Y, Zhou T, Zeng QF, Fu Q, Gao S, Li N, Koren S, Jiang Y, Zimin A, Xu P, Phillippy AM, Geng X, Song L, Sun FY, Li C, Wang XZ, Chen A, Jin YL, Yuan ZH, Yang Y, Tan S, Peatman E, Lu J, Qin Z, Dunham R, Li Z, Sonstegard T, Feng J, Danzmann RG, Schroeder S, Scheffler B, Duke MV, Ballard L, Kucuktas H, Kaltenboeck L, Liu H, Armbruster J, Xie Y, Kirby ML, Tian Y, Flanagan ME, Mu W, Waldbieser GC (2016b) The channel catfish genome sequence provides insights into the evolution of scale formation in teleosts. Nat Commun 7:11757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lubieniecki KP, Lin S, Cabana EI, Li J, Lai YYY, Davidson WS (2015) Genomic instability of the sex-determining locus in Atlantic salmon (Salmo salar). G3: Genes Genomes Genet 5:2513–2522

    Article  CAS  Google Scholar 

  • Luo MZ, Wing RA (2003) An improved method for plant BAC library construction. Methods Mol Biol 236:3–20

    CAS  PubMed  Google Scholar 

  • Luo MZ, Wang YH, Frisch D, Joobeur T, Wing RA, Dean RA (2001) Melon bacterial artificial chromosome (BAC) library construction using improved methods and identification of clones linked to the locus conferring resistance to melon Fusarium wilt (Fom-2). Genome 44:154–162

    Article  CAS  PubMed  Google Scholar 

  • Luo MZ, Kim HR, Kudrna D, Sisneros NB, Lee SJ, Mueller C, Collura K, Zuccolo A, Buckingham EB, Grim SM, Yanagiya K, Inoko H, Shiina T, Flajnik MF, Wing RA, Ohta Y (2006) Construction of a nurse shark (Ginglymostoma cirratum) bacterial artificial chromosome (BAC) library and a preliminary genome survey. BMC Genomics 7:106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma KY, Qiu GF, Feng JB, Li JL (2012) Transcriptome analysis of the oriental river prawn, Macrobrachium nipponense using 454 pyrosequencing for discovery of genes and markers. PLoS One 7:e39727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma KY, Liu ZQ, Lin JY, Li JL, Qiu GF (2016) Molecular characterization of a novel ovary-specific gene fem-1 homolog from the oriental river prawn, Macrobrachium nipponense. Gene 575:244–252

    Article  CAS  PubMed  Google Scholar 

  • Malecha SR, Nevin PA, Ha P, Barck LE, Lamadrid-Rose Y, Masuno S, Hedgecock D (1992) Sex-ratios and sex-determination in progeny from crosses of surgically sex-reversed freshwater prawns, Macrobrachium rosenbergii. Aquaculture 105:201–218

    Article  Google Scholar 

  • Mawaribuchi S, Takahashi S, Wada M, Uno Y, Matsuda Y, Kondo M, Fukui A, Takamatsu N, Taira M, Ito M (2017) Sex chromosome differentiation and the W- and Z-specific loci in Xenopus laevis. Dev Biol 426:393–400

    Article  CAS  PubMed  Google Scholar 

  • Pan ZJ, Li XY, Zhou FJ, Qiang XG, Gui JF (2015) Identification of sex-specific markers reveals male heterogametic sex determination in Pseudobagrus ussuriensis. Mar Biotechnol 17:441–451

    Article  CAS  Google Scholar 

  • Rees DJ, Dufresne F, Glemet H, Belzile C (2007) Amphipod genome sizes: first estimates for Arctic species reveal genomic giants. Genome 50:151–158

    Article  CAS  PubMed  Google Scholar 

  • Rheinsmith EL, Hinegardner R, Bachmann K (1974) Nuclear DNA amounts in Crustacea. Comp Biochem Physiol B Biochem Mol Biol 15:343–348

    Article  Google Scholar 

  • Shao CW, Chen SL, Scheuring CF, Xu JY, Sha ZX, Dong XL, Zhang HB (2010) Construction of two BAC libraries from half-smooth tongue sole Cynoglossus semilaevis and identification of clones containing candidate sex-determination genes. Mar Biotechnol 12:558–568

    Article  CAS  Google Scholar 

  • Shi X, Zeng HY, Xue YD, Luo MZ (2011) A pair of new BAC and BIBAC vectors that facilitate BAC/BIBAC library construction and intact large genomic DNA insert exchange. Plant Methods 7:33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soler L, Conte MA, Katagiri T, Howe AE, Lee BY, Amemiya C, Stuart A, Dossat C, Poulain J, Johnson J, Di Palma F, Lindblad-Toh K, Baroiller JF, D'Cotta H, Ozouf-Costaz C, Kocher TD (2010) Comparative physical maps derived from BAC end sequences of tilapia (Oreochromis niloticus). BMC Genomics 11:636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Staelens J, Rombaut D, Vercauteren I, Argue B, Benzie J, Vuylsteke M (2008) High-density linkage maps and sex-linked markers for the black tiger shrimp (Penaeus monodon). Genetics 179:917–925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stanke M, Morgenstern B (2005) AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res 33:W465–W467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Traut W, Vogel H, Gloeckner G, Hartmann E, Heckel DG (2013) High-throughput sequencing of a single chromosome: a moth W chromosome. Chromosom Res 21:491–505

    Article  CAS  Google Scholar 

  • Tremblay JJ, Viger RS (2003) A mutated form of steroidogenic factor 1 (SF-1 G35E) that causes sex reversal in humans fails to synergize with transcription factor GATA-4. J Biol Chem 278:42637–42642

    Article  CAS  PubMed  Google Scholar 

  • Vale L, Dieguez R, Sanchez L, Martinez P, Vinas A (2014) A sex-associated sequence identified by RAPD screening in gynogenetic individuals of turbot (Scophthalmus maximus). Mol Biol Rep 41:1501–1509

    Article  CAS  PubMed  Google Scholar 

  • Ventura T, Manor R, Aflalo ED, Weil S, Raviv S, Glazer L, Sagi A (2009) Temporal silencing of an androgenic gland-specific insulin-like gene affecting phenotypical gender differences and spermatogenesis. Endocrinology 150:1278–1286

    Article  CAS  PubMed  Google Scholar 

  • Ventura T, Aflalo ED, Weil S, Kashkush K, Sagi A (2011) Isolation and characterization of a female-specific DNA marker in the giant freshwater prawn Macrobrachium rosenbergii. Heredity 107:456–461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Lu Y, Zhang Y, Ning Z, Li Y, Zhao Q, Lu H, Huang R, Xia X, Feng Q, Liang X, Liu K, Zhang L, Lu T, Huang T, Fan D, Weng Q, Zhu C, Lu Y, Li W, Wen Z, Zhou C, Tian Q, Kang X, Shi M, Zhang W, Jang S, Du F, He S, Liao L, Li Y, Gui B, He H, Ning Z, Yang C, He L, Luo L, Yang R, Luo Q, Liu X, Li S, Huang W, Xiao L, Lin H, Han B, Zhu Z (2015) The draft genome of the grass carp (Ctenopharyngodon idellus) provides insights into its evolution and vegetarian adaptation. Nat Genet 47:625–631

    Article  CAS  PubMed  Google Scholar 

  • Xu P, Wang S, Liu L, Peatman E, Somridhivej B, Thimmapuram J, Gong G, Liu Z (2006) Channel catfish BAC-end sequences for marker development and assessment of syntenic conservation with other fish species. Anim Genet 37:321–326

    Article  CAS  PubMed  Google Scholar 

  • Xu P, Wang J, Wang J, Cui R, Li Y, Zhao Z, Ji P, Zhang Y, Li J, Sun X (2011a) Generation of the first BAC-based physical map of the common carp genome. BMC Genomics 12:537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu P, Li J, Li Y, Cui R, Wang J, Wang J, Zhang Y, Zhao Z, Sun X (2011b) Genomic insight into the common carp (Cyprinus carpio) genome by sequencing analysis of BAC-end sequences. BMC Genomics 12:188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zarkower D, Hodgkin J (1992) Molecular analysis of the C. elegans sex-determining gene tra-1: a gene encoding two zinc finger proteins. Cell 70:237–249

    Article  CAS  PubMed  Google Scholar 

  • Zhang LS, Yang CJ, Zhang Y, Li L, Zhang XM, Zhang QL, Xiang JH (2007) A genetic linkage map of Pacific white shrimp (Litopenaeus vannamei): sex-linked microsatellite markers and high recombination rates. Genetica 131:37–49

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Zhang X, Scheuring CF, Zhang HB, Huan P, Li F, Xiang J (2008) Construction and characterization of two bacterial artificial chromosome libraries of Zhikong scallop, Chlamys farreri Jones et Preston, and identification of BAC clones containing the genes involved in its innate immune system. Mar Biotechnol 10:358–365

    Article  CAS  Google Scholar 

  • Zhang XJ, Zhang Y, Scheuring C, Zhang HB, Huan P, Wang B, Liu CZ, Li FH, Liu B, Xiang JH (2010) Construction and characterization of a bacterial artificial chromosome (BAC) library of Pacific white shrimp, Litopenaeus vannamei. Mar Biotechnol 12:141–149

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key R&D Program of China (project number 2018YFD0900201), the Natural Science Foundation of China (project number 31772841), the Shanghai Sailing Program (project number 17YF1408000), and the Special Fund for the Development of Science and Technology of Shanghai Ocean University (project number A2-0203-17-100201).

Author information

Author notes

  1. Ke-Yi Ma and Shu-Hui Yu contributed equally.

Authors and Affiliations

  1. Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture, National Demonstration Center for Experimental Fisheries Science Education, Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, 201306, Shanghai, People’s Republic of China

    Ke-Yi Ma, Shu-Hui Yu, Yu-Xin Du, Shi-Qing Feng, Dai-Yi Ke & Gao-Feng Qiu

  2. College of Life Science and Technology, Huazhong Agricultural University, 430070, Wuhan, People’s Republic of China

    Liang-Jie Qiu & Mei-Zhong Luo

  3. College of Fisheries and Life Science, Shanghai Ocean University, 999 Hucheng Huan Road, Pudong New Area, 201306, Shanghai, People’s Republic of China

    Gao-Feng Qiu

Authors
  1. Ke-Yi Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shu-Hui Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yu-Xin Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shi-Qing Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Liang-Jie Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dai-Yi Ke
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mei-Zhong Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Gao-Feng Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gao-Feng Qiu.

Ethics declarations

Competing Interests

The authors have declared that no competing interest exists.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Table S1

Sequence comparison of the W- and Z-derived chromosome regions. (XLSX 15 kb)

Table S2

Deletions with length larger than 100 bp on the BAC inserts revealed by MAUVE. (XLSX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, KY., Yu, SH., Du, YX. et al. Construction of a Genomic Bacterial Artificial Chromosome (BAC) Library for the Prawn Macrobrachium rosenbergii and Initial Analysis of ZW Chromosome-Derived BAC Inserts. Mar Biotechnol 21, 206–216 (2019). https://doi.org/10.1007/s10126-018-09873-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-018-09873-8

Keywords

Search

Navigation