Skip to main content
Log in

Expression of chicken zygote arrest 1 (Zar1) and Zar1-like genes during sexual maturation and embryogenesis

  • Original Article
  • Published:
Veterinary Research Communications Aims and scope Submit manuscript

Abstract

Maternal mRNAs, which are expressed in oocytes, play an important role in the success of early embryo development, as they allow the first cleavages to occur. Zygote arrest 1 (Zar1) is an oocyte-specific maternal-effect gene that functions at the oocyte-to-embryo transition in many vertebrate species including human, pig, cattle, sheep, mouse, rat, frog and zebrafish. Recently, through in silico studies, a gene structurally related to Zar1, called Zar1-like has been identified in many vertebrates, including the chicken. The objectives of this study were to investigate the expression of the chicken Zar1 and Zar1-like genes in chicken tissues and embryos and to determine whether sexual maturation affects their mRNA abundance. RNA was extracted from various organs of chickens aged from one month up to two years old and from chicken embryos until day ten of embryonic development. Expression analysis of the genes was performed using RT-PCR and real-time PCR. RT-PCR analysis revealed that both genes were preferentially expressed in chicken oocytes, ovary and testes and in embryos during embryonic development. Quantitative real-time PCR analysis revealed a significant up regulation of Zar1 in the mature ovary, and also a significant up regulation of Zar1 and Zar1-like genes in the testes of sexually mature roosters, suggesting a key role of these genes in the chicken fertility. In contrast, expression of Zar1-like was not affected by age in the chicken ovary. Our results indicate that the chicken Zar1 and Zar1-like transcripts are co-expressed in high levels in the chicken gonads. In addition their expression beyond the stage of embryonic genome activation suggests an embryonic and not only a maternal origin of these transcripts.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aapola U, Liiv I, Peterson P (2002) Imprinting regulator DNMT3L is a transcriptional repressor associated with histone deacetylase activity. Nucleic Acids Res 30:3602–3608

    Article  CAS  PubMed  Google Scholar 

  • Aasland R, Gibson TJ, Stewart AF (1995) The PHD finger: implications for chromatin-mediated transcriptional regulation. Trends Bioch Sci 20:56–59

    Article  CAS  Google Scholar 

  • Bebbere D, Bogliolo L, Ariu F, Fois S, Leoni GG, Tore S, Succu S, Berlinguer F, Naitana S, Ledda S (2008) Expression pattern of zygote arrest 1 (ZAR1), maternal antigen that embryo requires (MATER), growth differentiation factor 9 (GDF9) and bone morphogenetic protein 15 (BMP15) genes in ovine oocytes and in vitro-produced preimplantation embryos. Reprod Fertil Dev 20:908–915

    Article  CAS  PubMed  Google Scholar 

  • Bienz M (2006) The PHD finger, a nuclear protein-interaction domain. Trends Bioch Sci 31:35–40

    Article  CAS  Google Scholar 

  • Brevini TA, Cillo F, Colleoni S, Lazzari G, Galli C, Gandolfi F (2004) Expression pattern of the maternal factor zygote arrest 1 (Zar1) in bovine tissues, oocytes, and embryos. Mol Reprod Dev 69:375–380

    Article  CAS  PubMed  Google Scholar 

  • Bultman SJ, Gebuhr TC, Pan H, Svoboda P, Schultz RM, Magnuson T (2006) Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev 20:1744–1754

    Article  CAS  PubMed  Google Scholar 

  • Burns KH, Viveiros MM, Ren Y, Wang P, DeMayo FJ, Frail DE, Eppig JJ, Matzuk MM (2003) Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos. Science 300:633–636

    Article  CAS  PubMed  Google Scholar 

  • Christians E, Davis AA, Thomas SD, Benjamin IJ (2000) Embryonic development: Maternal effect of Hsf1 on reproductive success. Nature 407:693–694

    Article  CAS  PubMed  Google Scholar 

  • Dalbiès-Tran R, Papillier P, Pennetier S, Uzbekova S, Monget P (2005) Bovine mater-like NALP9 is an oocyte marker gene. Mol Reprod Dev 71:414–421

    Article  PubMed  Google Scholar 

  • Dean J (2002) Oocyte-specific genes regulate follicle formation, fertility and early mouse development. J Reprod Immunol 53:171–180

    Article  CAS  PubMed  Google Scholar 

  • Elis S, Batellier F, Couty I, Balzergue S, Martin-Magniette ML, Monget P, Blesbois E, Govoroun MS (2008) Search for the genes involved in oocyte maturation and early embryo development in the hen. BMC Genomics 9:110

    Article  PubMed  Google Scholar 

  • Hamatani T, Carter MG, Sharov AA, Ko MSH (2004) Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell 6:117–131

    Article  CAS  PubMed  Google Scholar 

  • Howell CY, Bestor TH, Ding F, Latham KE, Mertineit C, Trasler JM, Chaillet JR (2001) Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell 104:829–838

    Article  CAS  PubMed  Google Scholar 

  • Jacobson S, Pillus L (1999) Modifying chromatin and concepts of cancer. Curr Opin Genet Dev 9:175–184

    Article  CAS  PubMed  Google Scholar 

  • Ko MS, Kitchen JR, Wang X, Threat TA, Wang X, Hasegawa A, Sun T, Grahovac MJ, Kargul GJ, Lim MK, Cui Y, Sano Y, Tanaka T, Liang Y, Mason S, Paonessa PD, Sauls AD, DePalma GE, Sharara R, Rowe LB, Eppig J, Morrell C, Doi H (2000) Large-scale cDNA analysis reveals phased gene expression patterns during preimplantation mouse development. Development 127:1737–1749

    Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2-ΔΔC T Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Meade KG, Higgs R, Lloyd AT, Giles S, O’Farrelly C (2009) Differential antimicrobial peptide gene expression patterns during early chicken embryological development. Dev Comp Immunol 33:516–524

    Article  CAS  PubMed  Google Scholar 

  • Minami N, Tsukamoto S (2006) Role of oocyte-specific genes in the development of mammalian embryos. Reprod Med Biol 5:175–182

    Article  CAS  Google Scholar 

  • Minami N, Suzuki T, Tsukamoto S (2007) Zygotic gene activation and maternal factors in mammals. J Reprod Dev 53:4707–4715

    Article  Google Scholar 

  • Onagbesan O, Bruggeman V, Decuypere E (2009) Intra-ovarian growth factors regulating ovarian function in avian species: A review. Anim Reprod Sci 11:121–140

    Article  Google Scholar 

  • Payer B, Saitou M, Barton SC, Thresher R, Dixon JP, Zahn D, Colledge WH, Carlton MB, Nakano T, Surani MA (2003) Stella is a maternal effect gene required for normal early development in mice. Curr Biol 13:2110–2117

    Article  CAS  PubMed  Google Scholar 

  • Pennetier S, Uzbekova S, Perreau C, Papillier P, Mermillod P, Dalbiès-Tran R (2004) Spatio-temporal expression of the germ cell marker genes MATER, ZAR1, GDF9, BMP15, and VASA in adult bovine tissues, oocytes, and preimplantation embryos. Biol Reprod 71:1359–1366

    Article  CAS  PubMed  Google Scholar 

  • Rajkovic A, Matzuk MM (2002) Functional analysis of oocyte-expressed genes using transgenic models. Mol Cell Endocrinol 187:5–9

    Article  CAS  PubMed  Google Scholar 

  • Rosenstrauch A, Degen AA, Friedlander M (1994) Spermatozoa retention by Sertoli cells during the decline in fertility in aging roosters. Biol Reprod 50:129–136

    Article  CAS  PubMed  Google Scholar 

  • Rosenstrauch A, Weil S, Degen AA, Friedlander M (1998) Leydig cell functional structure and plasma androgen level during the decline in fertility in aging roosters. Gen Comp Endocrinol 109:251–258

    Article  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    CAS  PubMed  Google Scholar 

  • Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, van den Hoff MJB, Moorman AFM (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37:e45

    Article  CAS  PubMed  Google Scholar 

  • Sangiorgio L, Strumbo B, Brevini TAL, Ronchi S, Simonic T (2008) A putative protein structurally related to zygote arrest 1 (Zar1), Zar1-like, is encoded by a novel gene conserved in the vertebrate lineage. Comp Biochem Physiol B Biochem Mol Biol 150:233–239

    Article  PubMed  Google Scholar 

  • Schier AF (2006) The maternal-zygotic transition: Death and birth of RNAs. Science 316:406–407

    Article  Google Scholar 

  • Schultz RM (1993) Regulation of zygotic gene activation in the mouse. BioEssays 15:531–538

    Article  CAS  PubMed  Google Scholar 

  • Schultz RM (2002) The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum Reprod Update 8:323–331

    Article  CAS  PubMed  Google Scholar 

  • Telford NA, Watson AJ, Schultz GA (1990) Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev 26:90–100

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acid Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  • Tong ZB, Gold L, Pfeifer KE, Dorward H, Lee E, Bondy CA, Dean J, Nelson LM (2000) Mater, a maternal effect gene required for early embryonic development in mice. Nat Genet 26:267–268

    Article  CAS  PubMed  Google Scholar 

  • Tsunekawa N, Naito M, Sakai Y, Nishida T, Noce T (2000) Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells. Development 127:2741–2750

    CAS  PubMed  Google Scholar 

  • Uzbekova S, Sabau-Roy M, Dalbiès-Tran R, Perreau C, Papillier P, Mompart F, Thelie A, Pennetier S, Cognie J, Cadoret V, Royere D, Monget P, Mermillod P (2006) Zygote arrest 1 gene in pig, cattle and human: evidence of different transcript variants in male and female germ cells. Reprod Biol Endocrinol 4:12

    Article  PubMed  Google Scholar 

  • Weil S, Rozenboim I, Degen AA, Dawson A, Friedlander M, Rosenstrauch A (1999) Fertility decline in aging roosters is related to increased testicular and plasma levels of estradiol. Gen Comp Endocrinol 115:23–28

    Article  CAS  PubMed  Google Scholar 

  • Wu X, Viveiros MM, Eppig JJ, Bai Y, Fitzpatrick SL, Matzuk MM (2003a) Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat Genet 33:187–191

    Article  CAS  PubMed  Google Scholar 

  • Wu X, Wang P, Brown CA, Zilinski CA, Matzuk MM (2003b) Zygote arrest 1 (Zar1) is an evolutionarily conserved gene expressed in vertebrate ovaries. Biol Reprod 69:861–867

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Hecht NB, Schultz RM (2001) Expression of MSY2 in mouse oocytes and preimplantation embryos. Biol Reprod 65:1260–1270

    Article  CAS  PubMed  Google Scholar 

  • Zagris N, Kalantzis K, Guialis A (1998) Activation of embryonic genome in chick. Zygote 6:227–231

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Georgios Michailidis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Michailidis, G., Argiriou, A. & Avdi, M. Expression of chicken zygote arrest 1 (Zar1) and Zar1-like genes during sexual maturation and embryogenesis. Vet Res Commun 34, 173–184 (2010). https://doi.org/10.1007/s11259-010-9343-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11259-010-9343-z

Keywords

Navigation