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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

EST;Penaeus monodon;RT-PCR;Sex-specific markers;Shrimp

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

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