DOI QR코드

DOI QR Code

Identification of Sex-specific Expression Markers in the Giant Tiger Shrimp (Penaeus monodon)

  • Khamnamtong, Bavornlak (Center of Excellence for Marine Biotechnology, Faculty of Science, Chulalongkorn University) ;
  • Thumrungtanakit, Supaporn (Center of Excellence for Marine Biotechnology, Faculty of Science, Chulalongkorn University) ;
  • Klinbunga, Sirawut (Center of Excellence for Marine Biotechnology, Faculty of Science, Chulalongkorn University) ;
  • Aoki, Takashi (Laboratory of Genome Science, Graduate School of Marine Science and Technology, Tokyo University of Marine Science and Technology) ;
  • Hirono, Ikuo (Laboratory of Genome Science, Graduate School of Marine Science and Technology, Tokyo University of Marine Science and Technology) ;
  • Menasveta, Piamsak (Center of Excellence for Marine Biotechnology, Faculty of Science, Chulalongkorn University)
  • Received : 2005.08.31
  • Accepted : 2005.09.28
  • Published : 2006.01.31

Abstract

Bulked segregant analysis (BSA) and AFLP were used for isolation of genomic sex determination markers in Penaeus monodon. A total of 256 primer combinations were tested against 6-10 bulked genomic DNA of P. monodon. Five and one candidate female- and male-specific AFLP fragments were identified. Female-specific fragments were cloned and further characterized. SCAR markers derived from FE10M9520, FE10M10725.1, FE10M10725.2 and FE14M16340 provided the positive amplification product in both male and female P. monodon. Further analysis of these markers using SSCP and genome walk analysis indicated that they were not sex-linked. In addition, sex-specific (or differential) expression markers in ovaries and testes of P. monodon were analyzed by RAP-PCR (150 primer combinations). Twenty-one and fourteen RAP-PCR fragments specifically/differentially expressed in ovaries and testes of P. monodon were successfully cloned and sequenced. Expression patterns of 25 transcripts were tested against the first stranded cDNA of ovaries and testes of 3-month-old and broodstock-sized P. monodon (N = 5 and N = 7 - 10 for females and N = 4 and N = 5 - 7 for males, respectively). Five (FI-4, FI-44, FIII-4, FIII-39 and FIII-58) and two (M457-A01 and MII-51) derived RAP-PCR markers revealed female- and male-specific expression patterns in P. monodon. Surprisingly, MII-5 originally found in testes showed a higher expression level in ovaries than did testes of juvenile shrimps but a temporal female-specific pattern in P. monodon adults.

Keywords

References

  1. Benzie, J. A. H. (1998) Penaeid genetics and biotechnology. Aquaculture 164, 23-47 https://doi.org/10.1016/S0044-8486(98)00175-6
  2. Boag, P. R., Newton, S. E., Hansen, N-P., Christensen, C. M., Nansen, P. and Gasser, R. B. (2000) Isolation and characterisation of sex-specific transcripts from Oesophagostomum dentatum by RNA arbitrarily-primed PCR. Mol. Biochem. Parasitol. 108, 217-224 https://doi.org/10.1016/S0166-6851(00)00217-6
  3. Browdy, C. L. (1998) Recent development in penaeid broodstock and seed production technologies: improving the outlook for superior stock. Aquaculture 164, 3-21 https://doi.org/10.1016/S0044-8486(98)00174-4
  4. Griffiths, R. and Orr, K. (1999) The use of amplified fragment length polymorphism (AFLP) in the isolation of sex-specific markers. Mol. Ecol. 8, 671-674 https://doi.org/10.1046/j.1365-294x.1999.00578.x
  5. Hoelzel, A. R. and Green, A. (1992) Analysis of population-level variation by sequencing PCR-amplified DNA; in: Molecular Genetic Analysis of Populations, Hoelzel, A. R. (ed.), pp. 159-187, Oxford University Press, Oxford, UK
  6. Klinbunga, S., Sodsuk, S., Penman, D. J. and McAndrew, B. J. (1996) An improved protocol for total DNA isolation and visualisation of mtDNA RFLP (s) in tiger prawn, Penaeus monodon. Thai J. Aquat. Sci. 3, 36-41
  7. 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
  8. 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
  9. 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. Reproduct. 64, 1090-1099 https://doi.org/10.1095/biolreprod64.4.1090
  10. 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, 506-510
  11. 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, 143-149 https://doi.org/10.1016/S0044-8486(02)00355-1
  12. Li, Y., Hill, J. A., Yue, G. H., Chen, F. and Orban, L. (2002) Extensive search does not identify genomic sex markers in Tetradon nigroviridis. J. Fish. Biol. 61, 1314-1317 https://doi.org/10.1111/j.1095-8649.2002.tb02475.x
  13. 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, 528-35 https://doi.org/10.1007/s10126-002-0103-0
  14. Michalski, M. L. and Weil, G. J. (1999) Gender-specific gene expression in Brugia malayi. Mol. Biochem. Parasitol. 104, 247-257 https://doi.org/10.1016/S0166-6851(99)00149-8
  15. Michelmore, R. W., Paran, I. and Kesseli, R. V. (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc. Natl. Acad. Sci. USA 88, 9828-9832 https://doi.org/10.1073/pnas.88.21.9828
  16. Ohbayashi, F., Suzuki, M. G., Mita, K., Okano, K. and Shimada, T. (2001) A homologue of the Drosophila doublesex gene is transcribed into sex-specific mRNA isoforms in the silkworm, Bombyx mori. Comp. Biochem. Physiol. B 128, 145-158 https://doi.org/10.1016/S1096-4959(00)00304-3
  17. Poonlaphdecha, S. (2004) Identification of sex-specific markers from black tiger shrimp Penaeus monodon using subtraction analysis. MSc Thesis. 180 pp. Chulalongkorn University, Bangkok, Thailand
  18. Preechaphol, R. (2004) Sex determination markers and gene expression in androgenic gland of different male morphotypes of the giant freshwater prawn Macrobrachium rosenbergii. MSc Thesis. 195 pp. Chulalongkorn University, Bangkok, Thailand
  19. Rosenberry, B. (2001) World shrimp farming 2001. San Diego: Shrimp News International
  20. Sambrook, J. and Russell, D. W. (2001) Molecular Cloning: A Laboratory Manual, 3rd ed., Cold Spring Harbor Laboratory Press, New York, USA
  21. Siebert, P. D., Chenchik, A., Kellog, D. E., Lukyanov, K. A. and Lukyanov, S. A. (1995) An improved method for walking in uncloned genomic DNA. Nucleic Acids Res. 23, 1087-1088 https://doi.org/10.1093/nar/23.6.1087
  22. Srisuparbh, D., Klinbunga, S., Wongsiri, S. and Sittipraneed, S. (2003) Isolation and partial characterization of royal jelly cDNA 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
  23. Supungul, P., Sootanan, P., Klinbunga, S., Kamonrat, W., Jarayabhand, P. and Tassanakajon, A. (2000) Microsatellite polymorphism and the population structure of the black tiger shrimp (Penaeus monodon) in Thailand. Mar. Biotechnol. 2, 339-347
  24. Vos, P., Hogers, R., Bleeker, M., Reijans, M., van de Lee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J. and Kuiper, M. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 23, 4407-4414 https://doi.org/10.1093/nar/23.21.4407
  25. Welsh, J., Chada, K., Dalal, S. S., Cheng, R., Ralph, D. and McClelland, M. (1992) Arbitrarily primed PCR fingerprinting of RNA. Nucleic Acids Res. 20, 4965-4970 https://doi.org/10.1093/nar/20.19.4965
  26. Withyachumnarnkul, B., Boonsaeng, W., 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. Chiangmai, Thailand
  27. Yamano, K., Qiu, G. F. and Unuma, T. (2004) Molecular cloning and ovarian expression profiles of thrombospondin, a major components of cortical rods in mature oocytes in penaeid shrimp, Marsupenaeus japonicus. Biol. Reproduct. 70, 1670-1678 https://doi.org/10.1095/biolreprod.103.025379

Cited by

  1. No AFLP sex-specific markers detected in Pangasianodon gigas and P. hypophthalmus vol.273, pp.4, 2007, https://doi.org/10.1016/j.aquaculture.2007.09.018
  2. Detection of a single nucleotide polymorphism (SNP) DNA marker linked to cocoon traits in the mulberry silkworm, Bombyx mori (Lepidoptera: Bombycidae) vol.108, pp.3, 2011, https://doi.org/10.14411/eje.2011.043
  3. 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
  4. 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
  5. Isolation and Characterization of Male-Specific DNA Markers in the Rock Bream Oplegnathus fasciatus vol.15, pp.2, 2013, https://doi.org/10.1007/s10126-012-9480-1
  6. Sequence characterized amplified regions (SCAR) reveal candidate markers linked to growth traits in the Chinese shrimp Fenneropenaeus chinensis vol.75, pp.5, 2009, https://doi.org/10.1007/s12562-009-0137-6
  7. Development of a Species-diagnostic SCAR Marker of the Blue Swimming Crab (Portunus pelagicus) vol.45, pp.11-12, 2007, https://doi.org/10.1007/s10528-007-9108-8
  8. 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
  9. Genetic diversity of wild and domesticated stocks of Thai abalone, Haliotis asinina (Haliotidae), analyzed by single-strand conformational polymorphism of AFLP-derived markers vol.9, pp.2, 2010, https://doi.org/10.4238/vol9-2gmr808
  10. Species identification of the blue swimming crab Portunus pelagicus in Thai waters using mtDNA and RAPD-derived SCAR markers vol.308, 2010, https://doi.org/10.1016/j.aquaculture.2010.06.033
  11. 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
  12. Aquacultural biotechnology in Thailand: the case of the shrimp industry vol.10, pp.6, 2008, https://doi.org/10.1504/IJBT.2008.022494
  13. 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
  14. Screening of Genes Specifically Expressed in Males ofFenneropenaeus chinensisand Their Potential as Sex Markers vol.2013, 2013, https://doi.org/10.1155/2013/921067
  15. A novel male-specific DNA sequence in the common carp, Cyprinus carpio vol.23, pp.5, 2009, https://doi.org/10.1016/j.mcp.2009.04.004