DOI QR코드

DOI QR Code

Expressed Sequence Tag Analysis for Identification and Characterization of Sex-Related Genes in the Giant Tiger Shrimp Penaeus monodon

  • Preechaphol, Rachanimuk (Program in Biotechnology, Faculty of Science, Chulalongkorn University) ;
  • Leelatanawit, Rungnapa (Program in Biotechnology, Faculty of Science, Chulalongkorn University) ;
  • Sittikankeaw, Kanchana (Program in Biotechnology, Faculty of Science, Chulalongkorn University) ;
  • Klinbunga, Sirawut (Center of Excellence for Marine Biotechnology, Faculty of Science, Chulalongkorn University) ;
  • Khamnamtong, Bavornlak (Center of Excellence for Marine Biotechnology, Faculty of Science, Chulalongkorn University) ;
  • Puanglarp, Narongsak (Center of Excellence for Marine Biotechnology, Faculty of Science, Chulalongkorn University) ;
  • Menasveta, Piamsak (Center of Excellence for Marine Biotechnology, Faculty of Science, Chulalongkorn University)
  • Published : 2007.07.31

Abstract

Sex-related genes expressed in vitellogenic ovaries of the giant tiger shrimp, Penaeus monodon, were identified by an EST approach. A total of 1051 clones were unidirectionally sequenced from the 5 terminus. Nucleotide sequences of 743 EST (70.7%) significantly matched known genes previously deposited in the GenBank (E-value <$10^{-4}$) whereas 308 ESTs (29.3%) were regarded as newly unidentified transcripts (E-value >$10^{-4}$). A total of 559 transcripts (87 contigs and 472 singletons) were obtained. Thrombospondin (TSP) and peritrophin (79 and 87 clones accounting for 7.5 and 8.3% of clones sequenced, respectively) predominated among characterized transcripts. everal full length transcripts (e.g. cyclophilin, profillin and thioredoxin peroxidase) were also isolated. A gene homologue encoding chromobox protein (PMCBX, ORF of 567 nucleotides encoding a protein of 188 amino acids) which is recognized as a new member of the HP1 family was identified. Expression patterns of 14 of 25 sex-related gene homologues in ovaries and testes of P. monodon broodstock were examined by RT-PCR. Female sterile and ovarian lipoprotein receptor homologues were only expressed in ovaries whereas the remaining transcripts except disulfide isomerase related P5 precursor and adenine nucleotide translocator 2 were higher expressed in ovaries than testes of P. monodon broodstock. A homologue of ubiquitin specific proteinase 9, X chromosome (Usp9X) revealed a preferential expression level in ovaries than testes of broodstock-sized P. monodon (N = 13 and 11, P<0.05) but was only expressed in ovaries of 4-month-old shrimp (N = 5 for each sex).

Keywords

References

  1. Alekseev, O. M., Widgren, E. E., Richardson, R. T. and O'Rand, M. G. (2005) Association of NASP with HSP90 in mouse spermatogenic cells stimulation of ATPase activity and transport of linker histones into nuclei. J. Biol. Chem. 280, 2904-2911. https://doi.org/10.1074/jbc.M410397200
  2. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410. https://doi.org/10.1016/S0022-2836(05)80360-2
  3. Asian Shrimp Culture Council (1996) Asian Shrimp News 1st quarter.
  4. Avarre, J. -C., Khayat, M., Michelis, R., Nagasawa, H., Tietz, A. and Lubzens, E. (2001) Inhibition of de novo synthesis of a jelly layer precursor protein by crustacean hyperglycemic hormone family peptides and posttranscriptional regulation by sinus gland extracts in Penaeus semisulcatus ovaries. Gen. Comp. Endocrinol. 124, 257-268. https://doi.org/10.1006/gcen.2001.7710
  5. Benzie, J. A. H. (1998) Penaeid genetics and biotechnology. Aquaculture 164, 23-47. https://doi.org/10.1016/S0044-8486(98)00175-6
  6. Browdy, C. L. (1998) Recent developments in penaeid broodstock and seed production technologies: improving the outlook for superior captive stocks. Aquaculture 164, 3-21. https://doi.org/10.1016/S0044-8486(98)00174-4
  7. Clifford, H. C. and Preston, N. P. (2006) Genetic improvement; in Operating Procedures for Shrimp Farming: Global Shrimp OP Survey Results and Recommendations, pp. 73-77. Global Aquaculture Alliance, St. Louis, USA.
  8. Coman, G. J., Arnold, S. J., Peixoto, S., Crocos, P. J., Coman, F. E. and Preston, N. P. (2006) Reproductive performance of reciprocally crossed wild-caught and tank reared Penaeus monodon broodstock. Aquaculture 252, 372-384. https://doi.org/10.1016/j.aquaculture.2005.07.028
  9. Du, X.-J., Wang, J.-X., Liu, N., Zhao, X.-F., Li, F.-H. and Xiang, J.-H. (2006) Identification and molecular characterization of a peritrophin-like protein from fleshy prawn (Fenneropenaeus chinensis). Mol. Immunol. 43, 1633-1644. https://doi.org/10.1016/j.molimm.2005.09.018
  10. Fassnacht, W., Mempel, A., Strowitzki, T. and Vogt, P. H. (2006) Premature ovarian failure (POF) syndrome: towards the molecular clinical analysis of its genetic complexity. Curr. Med. Chem. 13, 1397-1410. https://doi.org/10.2174/092986706776872943
  11. Felsenstein, J. (1993) PHYLIP (Phylogenetic Inference Package) version 3.5c. Department of Genetics, University of Washington, Seattle.
  12. Gross, P. S., Bartlett, T. C., Browdy, C. L., Chapman, R. W. and Warr, G. W. (2001) Immune gene discovery by expressed sequence tag analysis of hemocytes and hepatopancreas in the Pacific white shrimp, Litopenaeus vannamei, and the Atlantic white shrimp, L. setiferus. Dev. Comp. Immunol. 25, 565-577. https://doi.org/10.1016/S0145-305X(01)00018-0
  13. Harrison, K. E. (1990) The role of nutrition in maturation, reproduction and embryonic development of decapod crustaceans: A review. J. Shellfish Res. 9, 1-28.
  14. Huang, X. and Madan, A. (1999) CAP3: A DNA sequence assembly program. Genome Res. 9, 868-877. https://doi.org/10.1101/gr.9.9.868
  15. Jones, D. O., Mattei, M. G., Horsley, D., Cowell, I. G. and Singh, P. B. (2001) The gene and pseudogenes of Cbx3/mHP1 gamma. DNA Seq. 12, 147-160. https://doi.org/10.3109/10425170109080769
  16. Jones, M. H., Furlong, R. A., Burkin, H., Chalmers, I. J., Brown, G. M., Khwaja, O. and Affara, N. A. (1996) The Drosophila developmental gene fat facets has a human homologue in Xp11.4 which escapes X-inactivation and has related sequences on Yq11.2. Hum. Mol. Genet. 5, 1695-1701. https://doi.org/10.1093/hmg/5.11.1695
  17. Khayat, M., Babin, P. J., Funkenstein, B., Sammar, M., Nagasawa, H., Tietz, A. and Lubzens, E. (2001) Molecular characterization and high expression during oocyte development of a shrimp ovarian cortical rod protein homologous to insect intestinal peritrophins. Biol. Reprod. 64, 1090-1099. https://doi.org/10.1095/biolreprod64.4.1090
  18. Klinbunga, S., Penman, D. J., McAndrew, B. J. and Tassanakajon, A. (1999) Mitochondrial DNA diversity in three populations of the giant tiger shrimp, Penaeus monodon. Mar. Biotechnol. 1, 113-121. https://doi.org/10.1007/PL00011758
  19. Klinbunga, S., Siludjai, D., Wuthijinda, W., Tassanakajon, A., Jarayabhand, A. and Menasveta, P. (2001) Genetic heterogeneity of the giant tiger shrimp (Penaeus monodon) in Thailand revealed by RAPD and mtDNA-RFLP analyses. Mar. Biotechnol. 3, 428-438. https://doi.org/10.1007/s10126-001-0055-9
  20. Khamnamtong, B., Klinbunga, S. and Menasveta, P. (2005) Species identification of five penaeid shrimps using PCR-RFLP and SSCP analyses of 16S ribosomal DNA. J. Biochem. Mol. Biol. 38, 491-499. https://doi.org/10.5483/BMBRep.2005.38.4.491
  21. Leelatanawit, R., Klinbunga, S., Puanglarp, N., Tassanakajon, A., Jarayabhand, P., Hirono, I., Aoki, T. and Menasveta, P. (2004) Isolation and characterization of differentially expressed genes in ovaries and testes of the giant tiger shrimp (Penaeus monodon). Mar. Biotechnol. 6, S506-S510.
  22. Lee, Y.-H., Harada, S., Smith, R. M., Friedman, R. and Jarett, L. (1996). The expression of an insulin binding to cellular thyroid hormone binding protein, but not insulin degrading enzyme, is increased during 3T3-L1 adipocytes differentiation. Biochem. Biophy. Res. Com. 222, 839-843. https://doi.org/10.1006/bbrc.1996.0831
  23. Li, F., Xiang, J., Zhang, X., Zhou, L., Zhang, C. and Wu, C. (2003) Gonad development characteristics and sex ratio in triploid Chinese shrimp (Fenneropenaeus chinensis). Mar. Biotechnol. 5, 528-535. https://doi.org/10.1007/s10126-002-0103-0
  24. Li, Y., Byrne, K., Miggiano, E., Whan, V., Moore, S., Keys, S., Crocos, P., Preston, N. and Lehnert, S. (2003) Genetic mapping of the kuruma prawn Penaeus japonicus using AFLP markers. Aquaculture 219, 143-156. https://doi.org/10.1016/S0044-8486(02)00355-1
  25. Limsuwan, C. (2004) Diseases of Pacific white shrimp (Litopenaeus vannamei) cultured in Thailand. Proceeding of the JSPS-NRCT International Symposium Joint Seminar 2004: Management of Food Safety in Aquaculture and HACCP. pp. 36-41, Kasetsart University, Thailand.
  26. Lyons, R. E. and Li, Y. (2002) Crustacean genomics: implications for the future in aquaculture. AgBiotechNet 4, 1-6.
  27. Makinouchi, S. and Hirata, H. (1995) Studies on maturation and reproduction of pond-reared Penaeus monodon for developing a closed life-cycle culture system. Israeli J. Aqua.-Bamidgeh 47, 68-77.
  28. Meusy, J. -J. and Payen, G. G. (1988) Female reproduction in Malacostracan Crustacea. Zool. Sci. 5, 217-265.
  29. Noma, T., Kanai, Y., Kanai-Azuma, M., Ishii, M., Fujisawa, M., Kurohmaru, M., Kawakami, H., Wood, S. A. and Hayashi, Y. (2002) Stage- and sex-dependent expressions of Usp9x, an Xlinked mouse ortholog of Drosophila Fat facets, during gonadal development and oogenesis in mice. Mech. Dev. 119S, S91-S95.
  30. Okumura, T. (2004) Perspectives on hormonal manipulation of shrimp reproduction. JARQ 38, 49-54. https://doi.org/10.6090/jarq.38.49
  31. Okumura, T., Kim, Y. K., Kawazoe, I., Yamano, K., Tsutsui, N. and Aida, K. (2006) Expression of vitellogenin and cortical rod proteins during induced ovarian development by eyestalk ablation in the kuruma prawn, Marsupenaeus japonicus. Comp. Biochem. Physiol. A 143, 246-253. https://doi.org/10.1016/j.cbpa.2005.12.002
  32. Perrimon, N., Mohler, D., Engstrom, L. and Mahowald, A. P. (1986) X-linked female-sterile loci in Drosophila melanogaster. Genetics 113, 695-712.
  33. Pertea, G., Huang, X., Liang, F., Antonescu, V., Sultana, R., Karamycheva, S., Lee, Y., White, J., Cheung, F., Parvizi, B., Tsai, J. and Quackenbush, J. (2003) TIGR gene indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19, 651-652. https://doi.org/10.1093/bioinformatics/btg034
  34. Preston, N. P., Sellars, M. J. and Coman, F. E. (2004) Ploidy manipulation induces sterility in Kuruma Prawns. Global Aquaculture Advocate 7, 70-71.
  35. Primm, T. P. and Gilbert, H. F. (2001) Hormone binding by protein disulfide isomerase, a high capacity hormone reservoir of the endoplasmic reticulum. J. Biol. Chem. 276, 281-286. https://doi.org/10.1074/jbc.M007670200
  36. Qiu, G. -F. and Yamano, K. (2005) Three forms of cyclin B transcripts in the ovary of the kuruma prawn Marsupenaeus japonicus: Their molecular characterizations and expression profiles during oogenesis. Comp. Biochem. Physiol. B 141, 186-195. https://doi.org/10.1016/j.cbpc.2005.03.003
  37. Qiu, G. -F., Yamano, K. and Unuma, T. (2005) Cathepsin C transcripts are differentially expressed in the final stages of oocyte maturation in kuruma prawn Marsupenaeus japonicus. Comp. Biochem. Physiol. B 140, 171-181. https://doi.org/10.1016/j.cbpc.2004.09.027
  38. Quackenbush, L. S. (2001) Yolk synthesis in the marine shrimp, Penaeus vannamei. Am. Zool. 41, 458-464. https://doi.org/10.1668/0003-1569(2001)041[0458:YSITMS]2.0.CO;2
  39. Richardson, R. T., Batova, I. N., Widgren, E. E., Zheng, L.-X., Whitfield, M., Marzluff, W. F. and O'Rand, M. G. (2000) Characterization of the histone H1-binding protein, NASP, as a cell cycle-regulated somatic protein. J. Biol. Chem. 275, 30378-30386. https://doi.org/10.1074/jbc.M003781200
  40. Rojtinnakorn, J., Hirono, I., Itami, T., Takahashi, Y. and Aoki, T. (2002) Gene expression in haemocytes of kuruma prawn, Penaeus japonicus, in response to infection with WSSV by EST approach. Fish Shellfish Immunol. 13, 69-83. https://doi.org/10.1006/fsim.2001.0382
  41. Rosenberry, B. (2003) World shrimp farming 2003. Shrimp News International, San Diego, USA.
  42. Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
  43. Sambrook, J. and Russell, D. W. (2001) Molecular Cloning: A Laboratory Manual, 3th ed., Cold Spring Harbor Laboratory Press, New York, USA.
  44. Shen, Y. Q., Xiang, J. H., Wang, B., Li, F. H. and Tong, W. (2004) Discovery of immune related factors in Fenneropenaeus chinensis by annotation of ESTs. Prog. Nat. Sci. 14, 47-54. https://doi.org/10.1080/10020070412331343131
  45. Srisuparbh, D., Klinbunga, S., Wongsiri, S. and Sittipraneed, S. (2003) Isolation and characterization of major royal jelly cDNAs and proteins of the honey bee (Apis cerana). J. Biochem. Mol. Biol. 36, 572-579. https://doi.org/10.5483/BMBRep.2003.36.6.572
  46. Supungul, P., Klinbunga, S., Pichyangkura, R., Hirono, I., Aoki, T. and Tassanakajon, A. (2004) Antimicrobial peptides discovered in the black tiger shrimp Penaeus monodon by using the EST approach. Dis. Aquat. Org. 61, 123-135. https://doi.org/10.3354/dao061123
  47. Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight metrix choice. Nucleic Acids Res. 22, 4673-4680. https://doi.org/10.1093/nar/22.22.4673
  48. Welch, J. E. and O'Rand, M. G. (1990) Characterization of a sperm-specific nuclear autoantigenic protein. II. Expression and localization in the testis. Biol. Reprod. 43, 569-578. https://doi.org/10.1095/biolreprod43.4.569
  49. Withyachumnarnkul, B., Boonsaeng, V., Flegel, T. W., Panyim, S. and Wongteerasupaya C. (1998) Domestication and selective breeding of Penaeus monodon in Thailand, in: Proceedings to the Special Session on Advances in Shrimp Biotechnology, Felgel, T. (ed.), pp. 73-77, The Fifth Asian Fisheries Forum: International Conference on Fisheries and Food Security Beyond the Year 2000. 11-14 November 1998. Chiengmai, Thailand.
  50. Yamano, K., Qiu, G.-F. and Unuma, T. (2004) Molecular cloning and ovarian expression profiles of thrombospondin, a major component of cortical rods in mature oocytes of penaeid shrimp, Marsupenaeus japonicus. Biol. Reprod. 70, 1670-1678. https://doi.org/10.1095/biolreprod.103.025379
  51. Yamaguchi, K., Hidema, S. and Mizuno, S. (1998) Chicken chromobox proteins: cDNA cloning of CHCB1, -2, -3 and their relation to W-heterochromatin. Exp. Cell Res. 242, 303-314. https://doi.org/10.1006/excr.1997.4082

Cited by

  1. Differential expression of X-box binding protein 1 during ovarian development and association between its SNP and growth-related parameters of the giant tiger shrimp Penaeus monodon vol.448, 2015, https://doi.org/10.1016/j.aquaculture.2015.05.050
  2. Identification, characterization and expression of sex-related genes in testes of the giant tiger shrimp Penaeus monodon vol.152, pp.1, 2009, https://doi.org/10.1016/j.cbpa.2008.09.004
  3. ReproArrayGTS: A cDNA microarray for identification of reproduction-related genes in the giant tiger shrimp Penaeus monodon and characterization of a novel nuclear autoantigenic sperm protein (NASP) gene vol.4, pp.2, 2009, https://doi.org/10.1016/j.cbd.2008.11.003
  4. Isolation of cDNA, genomic organization and expression of small androgen receptor-interacting protein 1 (PmSARIP1) in the giant tiger shrimp Penaeus monodon vol.412-413, 2013, https://doi.org/10.1016/j.aquaculture.2013.07.011
  5. Molecular characterization and expression profiles of cyclin A and cyclin B during ovarian development of the giant tiger shrimp Penaeus monodon vol.152, pp.4, 2009, https://doi.org/10.1016/j.cbpa.2008.12.011
  6. Identification, characterization and expression of adipose differentiation-related protein (ADRP) gene and protein in ovaries of the giant tiger shrimp Penaeus monodon vol.308, 2010, https://doi.org/10.1016/j.aquaculture.2010.06.039
  7. Molecular characterization and expression of the Prostaglandin reductase 1 gene and protein during ovarian development of the giant tiger shrimp Penaeus monodon vol.322-323, 2011, https://doi.org/10.1016/j.aquaculture.2011.09.037
  8. Identification and expression analysis of the Broad-Complex core protein isoform 6 (BR-C Z6) gene in the giant tiger shrimp Penaeus monodon (Penaeidae: Decapoda) vol.10, pp.4, 2011, https://doi.org/10.4238/2011.October.3.6
  9. Gonadal transcriptomic analysis and differentially expressed genes in the testis and ovary of the Pacific white shrimp (Litopenaeus vannamei) vol.16, pp.1, 2015, https://doi.org/10.1186/s12864-015-2219-4
  10. Expression levels of RuvBL2 during ovarian development and association between its single nucleotide polymorphism (SNP) and growth of the giant tiger shrimp Penaeus monodon vol.308, 2010, https://doi.org/10.1016/j.aquaculture.2010.06.038
  11. Transcriptome analysis of the copepod Eurytemora affinis upon exposure to endocrine disruptor pesticides: Focus on reproduction and development vol.176, 2016, https://doi.org/10.1016/j.aquatox.2016.04.010
  12. Up-regulation of Ribophorin I after yellow head virus (YHV) challenge in black tiger shrimp Penaeus monodon vol.25, pp.1-2, 2008, https://doi.org/10.1016/j.fsi.2007.12.003
  13. EST analysis and identification of gonad-related genes from the normalized cDNA library of large yellow croaker, Larimichthys crocea vol.5, pp.2, 2010, https://doi.org/10.1016/j.cbd.2010.01.002
  14. A Review of the Major Penaeid Shrimp EST Studies and the Construction of a Shrimp Transcriptome Database Based on the ESTs from Four Penaeid Shrimp vol.13, pp.4, 2011, https://doi.org/10.1007/s10126-010-9286-y
  15. A gene-based SNP linkage map for pacific white shrimp, Litopenaeus vannamei vol.41, pp.3, 2010, https://doi.org/10.1111/j.1365-2052.2009.02002.x
  16. Analysis of expressed sequence tags from the liver and ovary of the euryhaline hermaphroditic fish, Kryptolebias marmoratus vol.6, pp.3, 2011, https://doi.org/10.1016/j.cbd.2011.05.001
  17. Expression and polymorphism of farnesoic acid O-methyltransferase (FAMeT) and association between its SNPs and reproduction-related parameters of the giant tiger shrimp Penaeus monodon vol.441, 2015, https://doi.org/10.1016/j.aquaculture.2015.02.021
  18. Molecular cloning and expression pattern analysis of two novel disulfide isomerases in shrimp vol.153, pp.3, 2011, https://doi.org/10.1016/j.cbpc.2010.11.007
  19. Characterization, expression and localization of valosin-containing protein in ovaries of the giant tiger shrimp Penaeus monodon vol.533, pp.1, 2014, https://doi.org/10.1016/j.gene.2013.09.089
  20. Constructing and random sequencing analysis of normalized cDNA library of testis tissue from oriental river prawn (Macrobrachium nipponense) vol.7, pp.3, 2012, https://doi.org/10.1016/j.cbd.2012.04.003
  21. Expression of Sex and Reproduction-Related Genes in Marsupenaeus japonicus vol.12, pp.6, 2010, https://doi.org/10.1007/s10126-009-9254-6
  22. Molecular cloning and expression analysis of the Mitogen-activating protein kinase 1 (MAPK1) gene and protein during ovarian development of the giant tiger shrimp Penaeus monodon vol.78, pp.5, 2011, https://doi.org/10.1002/mrd.21310
  23. Immune gene discovery by expressed sequence tag (EST) analysis of hemocytes in the ridgetail white prawn Exopalaemon carinicauda vol.34, pp.1, 2013, https://doi.org/10.1016/j.fsi.2012.10.026
  24. Molecular cloning and expression of progestin membrane receptor component 1 (Pgmrc1) of the giant tiger shrimp Penaeus monodon vol.168, pp.3, 2010, https://doi.org/10.1016/j.ygcen.2010.06.002
  25. Screening of genes related to ovary development in Chinese shrimp Fenneropenaeus chinensis by suppression subtractive hybridization vol.5, pp.2, 2010, https://doi.org/10.1016/j.cbd.2010.02.001
  26. Suppression subtractive hybridization (SSH) for isolation and characterization of genes related to testicular development in the giant tiger shrimp Penaeus monodon vol.41, pp.11, 2008, https://doi.org/10.5483/BMBRep.2008.41.11.796
  27. Stimulation of ovarian development in white shrimp, Fenneropenaeus merguiensis De Man, with a recombinant ribosomal protein L10a vol.432, 2014, https://doi.org/10.1016/j.aquaculture.2014.04.025
  28. Characterization and expression analysis of Cyclin-dependent kinase 7 gene and protein in ovaries of the giant tiger shrimp Penaeus monodon vol.432, 2014, https://doi.org/10.1016/j.aquaculture.2014.05.022
  29. Gene discovery from an ovary cDNA library of oriental river prawn Macrobrachium nipponense by ESTs annotation vol.4, pp.2, 2009, https://doi.org/10.1016/j.cbd.2008.12.004
  30. Proteomic analysis of ovarian proteins and characterization of thymosin-β and RAC-GTPase activating protein 1 of the giant tiger shrimp Penaeus monodon vol.11, 2014, https://doi.org/10.1016/j.cbd.2014.05.002
  31. Isolation and characterization of progesterone receptor-related protein p23 (Pm-p23) differentially expressed during ovarian development of the giant tiger shrimp Penaeus monodon vol.308, 2010, https://doi.org/10.1016/j.aquaculture.2010.06.037
  32. Expression profiles and localization of vitellogenin mRNA and protein during ovarian development of the giant tiger shrimp Penaeus monodon vol.412-413, 2013, https://doi.org/10.1016/j.aquaculture.2013.07.026
  33. Applying the Power of Transcriptomics: Understanding Male Sexual Development in Decapod Crustacea vol.56, pp.6, 2016, https://doi.org/10.1093/icb/icw007
  34. Microarray Analyses of Shrimp Immune Responses vol.13, pp.4, 2011, https://doi.org/10.1007/s10126-010-9291-1
  35. Molecular characterization of Calreticulin: A biomarker for temperature stress responses of the giant tiger shrimp Penaeus monodon vol.308, 2010, https://doi.org/10.1016/j.aquaculture.2010.06.040
  36. Construction of reproduction-specific cDNA microarrays for the black tiger shrimp (Penaeus monodon) vol.136, 2008, https://doi.org/10.1016/j.jbiotec.2008.07.1283
  37. Contributions of functional genomics and proteomics to the study of immune responses in the Pacific white leg shrimp Litopenaeus vannamei vol.128, pp.1-3, 2009, https://doi.org/10.1016/j.vetimm.2008.10.329
  38. Analysis and comparison of a set of expressed sequence tags of the parthenogenetic water flea Daphnia carinata vol.282, pp.2, 2009, https://doi.org/10.1007/s00438-009-0459-1
  39. EST analysis on the gonad development related organs and microarray screen for differentially expressed genes in mature ovary and testis of Scylla paramamosain vol.6, pp.2, 2011, https://doi.org/10.1016/j.cbd.2010.12.003
  40. Identification of reproduction-related proteins and characterization of the protein disulfide isomerase A6 cDNA in ovaries of the giant tiger shrimp Penaeus monodon vol.7, pp.2, 2012, https://doi.org/10.1016/j.cbd.2012.02.003
  41. Characterization and expression analysis of the Broad-complex (Br-c) gene of the giant tiger shrimp Penaeus monodon vol.164, pp.4, 2013, https://doi.org/10.1016/j.cbpb.2013.02.004
  42. Screening of Genes Specifically Expressed in Males ofFenneropenaeus chinensisand Their Potential as Sex Markers vol.2013, 2013, https://doi.org/10.1155/2013/921067
  43. Expression levels of vitellogenin receptor (Vtgr) during ovarian development and association between its single nucleotide polymorphisms (SNPs) and reproduction-related parameters of the giant tiger shrimp Penaeus monodon vol.435, 2015, https://doi.org/10.1016/j.aquaculture.2014.09.013
  44. The State of “Omics” Research for Farmed Penaeids: Advances in Research and Impediments to Industry Utilization vol.9, pp.1664-8021, 2018, https://doi.org/10.3389/fgene.2018.00282