Expression Analysis of Genes Putatively Involved in Chicken Gonadal Development

Abstract

In mammals, testis development is initiated by the expression of the sex-determining gene, SRY, whereas the genetic trigger for sex determination in birds remains unknown. In the present study, the expression of seven genes implicated in vertebrate sex determination and differentiation were studied in chicken embryonic gonads from day 4 to day 12 of incubation using reverse transcription and the polymerase chain reaction (RT-PCR). Results showed transcription of cLhx9, cGATA4, cVnn1, cPpt1, cBrd3 were sexually dimorphic during chicken gonadal development, whereas cEki2, cFog2 were expressed at similar levels in both sexes. Results of comparative studies between mammals and chickens show that vertebrate sex-determining pathways comprise both conserved and divergent elements: expression profiles of cGATA4/cFog2 and cVnn1 are similar to those in mammals, while others appear some differences. Possible functions of these genes on chicken gonadal development were analyzed based on their expression profiles.

References

  1. 1.

    Albrecht, K. H., Eicher, E. M. (2001) Evidence that Sry is expressed in pre-Sertoli and granulose cells have a common precursor. Dev. Biol. 240, 92–107.

    CAS  Article  Google Scholar 

  2. 2.

    Birk, O. S., Casiano, D. E., Wassif, C. A., Cogliati, T., Zhao, L. P., Zhao, Y. G., Grinberg, A., Huang, S. P., Kreidberg, J. A., Parker, K. L., Porter, F. D., Westphal, H. (2000) The LIM homeobox gene Lhx9 is essential for mouse gonad formation. Nature 403, 909–913.

    CAS  Article  Google Scholar 

  3. 3.

    Bowles, J., Bullejos, M., Koopman, P. (2000) A subtractive gene expression screen suggests a role for vanin-1 in testis development in mice. Genesis 27, 124–135.

    CAS  Article  Google Scholar 

  4. 4.

    Boyer, A., Lussier, J. G., Sinclair, A. H., McClive, P. J., Silversides, D. W. (2004) Pre-Sertoli specific gene expression profiling reveals differential expression of Ppt1 and Brd3 genes within the mouse genital ridge at the time of sex determination. BOR Papers in Press 71, 820–827.

    CAS  Google Scholar 

  5. 5.

    Feng, Y., Zhang, Sh., Peng, X., Gong, Y. (2003) Identification of the sex of chicken by duplex PCR. The current Development of Poultry science, Proceeding of 11th National Symposium on poultry science, pp. 47-49. (in Chinese)

    Google Scholar 

  6. 6.

    Graves, J. A. M., Shetty, S. (2001) Sex from W to Z: Evolution of vertebrate sex chromosome and sex determining genes. J. Exp. Zool. 290, 449–462.

    Article  Google Scholar 

  7. 7.

    Hamburger, V., Hamilton, H. L. (1951) A series of normal stages in the development of the chicken embryo. J. Morphol. 88, 49–92.

    CAS  Article  Google Scholar 

  8. 8.

    Hurley, T. M., McClive, P. J., Sarraj, M. A., Sinclair, A. H. (2004) Eki2 is upregulated specifically in the testis during mouse sex determination. Gene Exp. Patterns 4, 135–140.

    CAS  Article  Google Scholar 

  9. 9.

    Koopman, P., Gubbay, J., Vivian, N., Goodfellow, P. N., Lovell-Badge, R. (1991) Male development of chromosomally female mice transgenic for Sry. Nature 351, 117–121.

    CAS  Article  Google Scholar 

  10. 10.

    Mizuno, S., Kunita, R., Nakabayashi, O., Kuroda, Y., Arai, N., Harata, M., Ogawa, A., Itoh, Y., Teranishi, M., Hori, T. (2002) Z and W chromosomes of chickens: studies on their gene functions in sex determination and sex differentiation. Cytogenet Genome Res. 99, 236–244.

    CAS  Article  Google Scholar 

  11. 11.

    Mazaud, S., Oreal, E., Guigon, C. J., Carre-Eusebe, D., Magre, S. (2002) Lhx9 expression during gonadal morphogenesis as related to the state of cell differentiation. Gene Exp. Patterns 2, 373–377.

    CAS  Article  Google Scholar 

  12. 12.

    Morrish, B. C., Sinclair, A. H. (2002) Vertebrate sex determination: many means to an end. Reproduction 124, 447–457.

    CAS  Article  Google Scholar 

  13. 13.

    O’Neill, M., Binder, M., Smith, C. A., Andrews, J., Reed, K., Smith, M. J., Millar, C., Lambert, D., Sinclair, A. H. (2000) ASW: a gene with conserved avian W-linkage and female specific expression in chick embryonic gonad. Dev. Gen. Evol. 210, 243–249.

    Article  Google Scholar 

  14. 14.

    Oreal, E., Pieu, C., Matiei, M. G., Josso, N., Picard, J. Y., Eusebe, D. C., Magre, S. (1998) Early expression of AMH in chicken embryonic gonads precedes teaticular SOX9 expression. Dev. Dynam. 212, 522–532.

    CAS  Article  Google Scholar 

  15. 15.

    Parker, K. L., Schinner, B. P. (2002) Genes essential for early events in gonadal development. Ann. Med. 34, 171–178.

    CAS  Article  Google Scholar 

  16. 16.

    Pieau, C. (1996) Temperature variation and sex determination in reptiles. BioEssays 18, 19–26

    CAS  Article  Google Scholar 

  17. 17.

    Pivot-Pajot, C., Caron, C., Govin, J., Vion, A., Rousseaux, S., Khochbin, S. (2003) Acetylation - dependent chromatin reorganization by BRDT, a testis-specific bromodomain-containing protein. Mol. Cell Biol. 23, 5354–5365.

    CAS  Article  Google Scholar 

  18. 18.

    Raymond, C. S., Kettlewell, J. R., Hirsch, B., Bardwell, V. J., Zarkower, D. (1999) Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexually development. Dev. Bio. 215, 208–220.

    CAS  Article  Google Scholar 

  19. 19.

    Reed, K. J., Sinclair, A. H. (2003) FET-1: a novel W-linked, female specific gene upregulated in the embryonic chicken ovary. Gene Exp. Patterns 2, 83–85.

    Article  Google Scholar 

  20. 20.

    Rhee, K., Brunori, M., Besset, V., Trousdale, R., Wolgemuth, D. J. (1998) Expression and potential role of Fsrg1, a murine bromodomain-containing homologue of the Drosophila gene female sterile homeotic. J. Cell Sci. 111, 3541–3550.

    CAS  PubMed  Google Scholar 

  21. 21.

    Shan, Z., Nanda, I., Wang, Y., Schmid, M., Vortkamp, A., Haaf, T. (2000) Sex-specific expression of an evolutionarily conserved male regulatory gene, DMRT1, in birds. Cytogenet. Cell Genet. 89, 252–257.

    CAS  Article  Google Scholar 

  22. 22.

    Shimada, K. (2002) Sex determination and sex differentiation. Avian Poult. Biol. Rev. 13, 1–14.

    Article  Google Scholar 

  23. 23.

    Sinclair, A. H., Berta, P., Hawkins, M. S., Griffiths, B. L., Smith, M. J., Foster, J. W., Frischauf, A. M., Lovell-Badge, R., Goodfellow, P. N. (1990) A gene from the human sex-determining region encodes a protein with homology to a conserved DNA binding motif. Nature 346, 240–244.

    CAS  Article  Google Scholar 

  24. 24.

    Smith, C. A., Clifford, V., Westerm, P. S., Wilcox, S. A., Bell, K. S., Sinclair, A. H. (2000) Cloning and expression of a DAX1 homologue in the chicken embryo. J. Mol. Endocrinol. 24, 23–32.

    CAS  Article  Google Scholar 

  25. 25.

    Smith, C. A., Sinclair, A. H. (2004) Sex determination: insights from the chicken. BioEssays 26, 120–132.

    CAS  Article  Google Scholar 

  26. 26.

    Smith, C. A., Smith, M. J., Sinclair, A. H. (1999) Gene expression during gonadogenesis in the chicken embryo. Gene 234, 395–402.

    CAS  Article  Google Scholar 

  27. 27.

    Tevosian, S. G., Albrecht, K. H., Crispino, J. D., Fujiwara, Y., Eicher, E. M., Orkin, S. H. (2002) Gonadal differentiation, sex determination and normal Sry expression in mice require direct interaction between transcription partners GATA4 and FOG2. Development 129, 4627–4634.

    CAS  PubMed  Google Scholar 

  28. 28.

    Viger, R. S., Mertineit, C., Trasler, J. M., Nemer, M. (1998) Transcription factor GATA-4 is expressed in a sexually dimorphic pattern during mouse gonadal development and is a potent activator of the Müllerian inhibiting substance promoter. Development 125, 2665–2675.

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by Hubei Project grant to the outstanding youth, Project of National Natural Science Foundation (30671494) and the 11th “Five-year Project” to tackling the Key Problems in Hubei province. Special appreciation goes to Professor David Gerrard, Department of Animal Science, Purdue University for his grammatically proofreading. And we thank Dr. Shen Shixue and Dr. Khairy M. Zoheir for critically reading and revising an earlier version of this manuscript.

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Correspondence to Y. Gong.

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Feng, Y., Zhang, S., Peng, X. et al. Expression Analysis of Genes Putatively Involved in Chicken Gonadal Development. BIOLOGIA FUTURA 58, 163–172 (2007). https://doi.org/10.1556/ABiol.58.2007.2.3

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Keywords

  • Gonadal development
  • sex determination
  • sex differentiation
  • RT-PCR
  • chicken