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Identical sequences but different expression patterns of Hira gene in gynogenetic and gonochoristic crucian carps

Fish Physiology and Biochemistry volume 34, pages 175–184 (2008)Cite this article

Abstract

Hir/Hira (histone regulation) genes were first identified in yeast as negative regulators of histone gene expression. It has been confirmed that HIRA is a conserved family of proteins present in various animals and plants. In this paper, the cDNAs of the Hira homolog named CagHira and CaHira were isolated from gynogenetic gibel carp (gyno-carp) and gonochoristic color crucian carp (gono-carp) respectively. The full-length CagHira is 3,860 bp in length with an open reading frame (ORF) of 3,033 bp that encodes 1,011 amino acids, while the full-length CaHira is 3,748 bp in length and also has an ORF of 3,033 bp. The deduced amino acid sequences of both Hira homologs contain seven WD domains and show high identity with other HIRA family members. RT-PCR analyses revealed strong expression of Hira in the ovaries, whereas no expression was detected in the testes of either of the fishes. Hira transcription was not detected in the liver of gyno-carp, but a high level of Hira mRNA was observed in gono-carp. The temporal expression pattern showed that the Hira mRNA is consistently expressed during all embryonic development stages in gyno-carp. However, the abundance of CaHira mRNA significantly decreased (P < 0.05) shortly after fertilization and then increased again and remained stable from gastrula till hatching. The varying spatiotemporal expression patterns of Hira genes in gyno-carp and gono-carp may be associated with the differing reproductive modes used by these two closely related fishes. Our results suggest that Hira may play a role not only in the decondensation of sperm nucleus and the formation of pronucleus during fertilization, but also in gastrulation and the subsequent development of embryos.

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References

  • Ahmad A, Kikuchi H, Takami Y, Nakayama T (2005) Different roles of N-terminal and C-terminal halves of HIRA in transcription regulation of cell cycle-related genes that contribute to control of vertebrate cell growth. J Biol Chem 280:32090–32100

    Article  PubMed  CAS  Google Scholar 

  • Carlson C, Papolos D, Pandita RK, Faedda GL, Veit S, Goldberg R, Shprintzen R, Kucherlapati R, Morrow B (1997) Molecular definition of 22q11 deletions in 151 velo-cardio-facial syndrome patients. Am J Hum Genet 61:620–629

    Article  PubMed  CAS  Google Scholar 

  • Du XZ, Wang YF, Gui JF (2007) Sequence cloning and tissue expression analysis of Hira gene in colored crucian carp Carassius auratus. Acta Hydrobiol Sin 31:220–225

    Google Scholar 

  • Fan LC, Yang ST, Gui JF (2001) Differential screening and characterization analysis of the egg envelope glycoprotein ZP3 cDNAs between gynogenetic and gonochoristic crucian carp. Cell Res 11:17–27

    Article  PubMed  CAS  Google Scholar 

  • Ge W, Shan SX, Jiang YG (1992) Fertilization biology of gynogenetic crucian carp (Carassius auratus gibellio), with a discussion on the reproductive modes of the naturally gynogenetic crucian carp. Acta Hydrobiol Sin 16:97–100

    Google Scholar 

  • Gui JF (1996) A unique study system: gynogenetic fish Carassius auratus gibelio. Sci Found China 4:44–46

    Google Scholar 

  • Kaufman PD, Cohen JL, Osley MA (1998) Hir proteins are required for position-dependent gene silencing in Saccharomyces cerevisiae in the absence of chromatin assembly factor 1. Mol Cell Biol 18:4793–4806

    PubMed  CAS  Google Scholar 

  • Kirov N, Shtilbans A, Rushlow C (1998) Isolation and characterization of a new gene encoding a member of the HIRA family of proteins from Drosophila melanogaster. Gene 212:323–332

    Article  PubMed  CAS  Google Scholar 

  • Komachi K, Redd MJ, Johnson AD (1994) The WD repeats of Tup1 interact with the homeo domain protein α2. Genes Dev 8:2857–2867

    Article  PubMed  CAS  Google Scholar 

  • Lamour V, Lecluse Y, Desmaze C, Spector M, Bodescot M, Aurias A, Osley MA, Lipinski M (1995) A human homolog of the S. cerevisiae HIR1 and HIR2 transcriptional repressors cloned from the DiGeorge syndrome critical region. Hum Mol Genet 4:791–799

    Article  PubMed  CAS  Google Scholar 

  • Li CJ, Gui JF (2003) Comparative studies on in vitro sperm decondensation and pronucleus formation in egg extracts between gynogenetic and bisexual fish. Cell Res 13:159–169

    Article  PubMed  Google Scholar 

  • Llevadot R, Estivill X, Scambler P, Pritchard M (1998) Isolation and genomic characterization of the TUPLE1/HIRA gene of the pufferfish Fugu rubripes. Gene 208:279–283

    Article  PubMed  CAS  Google Scholar 

  • Loppin B, Docquier M, Bonneton F, Couble P (2000) The maternal effect mutation sesame affects the formation of the male pronucleus in Drosophila melanogaster. Dev Biol 222:392–404

    Article  PubMed  CAS  Google Scholar 

  • Loppin B, Berger F, Couble P (2001) The Drosophila maternal gene sesame is required for sperm chromatin remodeling at fertilization. Chromosoma 110:430–440

    Article  PubMed  CAS  Google Scholar 

  • Loppin B, Bonnefoy E, Anselme C, Laurencon A, Karr TL, Couble P (2005) The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437:1386–1390

    Article  PubMed  CAS  Google Scholar 

  • Lorain S, Quivy JP, Monier-Gavelle F (1998) Core histones and HIRIP3, a novel histone-binding protein, directly interact with WD repeat protein HIRA. Mol Cell Biol 18:5546–5556

    PubMed  CAS  Google Scholar 

  • Loyola A, Almouzni G (2004) Bromodomains in living cells participate in deciphering the histone code. Trends Cell Biol 14:279–281

    Article  PubMed  CAS  Google Scholar 

  • Magnaghi P, Roberts C, Lorain S, Lipinski M, Scambler PJ (1998) HIRA, a mammalian homologue of Saccharomyces cerevisiae transcriptional co-repressors, interacts with Pax3. Nat Genet 20:74–77

    Article  PubMed  CAS  Google Scholar 

  • Phelps-Durr TL, Thomas J, Vahab P, Timmermans MCP (2005) Maize rough sheath2 and its Arabidopsis orthologue ASYMMETRIC LEAVES1 interact with HIRA, a predicted histone chaperone, to maintain knox gene silencing and determinacy during organogenesis. Plant Cell 17:2886–2898

    Article  PubMed  CAS  Google Scholar 

  • Pizzuti A, Novelli G, Ratti A, Amati F, Bordoni R, Mandich P, Bellone E, Conti E, Bengala M, Mari A, Silani V, Dallapiccola B (1999) Isolation and characterization of a novel transcript embedded within HIRA, a gene deleted in DiGeorge syndrome. Mol Genet Metab 67:227–235

    Google Scholar 

  • Qian Z, Huang H, Hong JY, Burck CL, Johnston SD, Berman J, Carol A, Liebman SW (1998) Yeast Ty1 retrotransposition is stimulated by a synergistic interaction between mutations in chromatin assembly factor 1 and histone regulatory (Hir) proteins. Mol Cell Biol 18:4783–4792

    PubMed  CAS  Google Scholar 

  • Ray-Gallet D, Quivy JP, Scamps C, Martini EM, Lipinski M, Almouzni G (2002) HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol Cell 9:1091–1100

    Article  PubMed  CAS  Google Scholar 

  • Roberts C, Daw SC, Halford S, Scambler PJ (1997) Cloning and developmental expression analysis of chick Hira (Chira), a candidate gene for DiGeorge syndrome. Hum Mol Genet 6:237–245

    Article  PubMed  CAS  Google Scholar 

  • Roberts C, Sutherland HF, Farmer H, Kimber W, Halford S, Carey A, Brickman JM, Wynshaw-Boris A, Scambler PJ (2002) Targeted mutagenesis of the Hira gene results in gastrulation defects and patterning abnormalities of mesoendodermal derivatives prior to early embryonic lethality. Mol Cell Biol 22:2318–2328

    Article  PubMed  CAS  Google Scholar 

  • Scamps C, Lorain S, Lamour V, Lipinski M (1996) The HIR protein family: isolation and characterization of a complete murine cDNA. Biochim Biophys Acta 1306:5–8

    PubMed  Google Scholar 

  • Sharp JA, Fouts ET, Krawitz DC, Kaufman PD (2001) Yeast histone deposition protein ASF1p requires Hir proteins and PCNA for hetrochromatic silencing. Curr Biol 11:463–473

    Article  PubMed  CAS  Google Scholar 

  • Sharp JA, Franco AA, Osley MA, Kaufman PD (2002) Chromatin assembly factor I and Hir proteins contribute to building functional kinetochores in S. cerevisiae. Genes Dev 16:85–100

    Article  PubMed  CAS  Google Scholar 

  • Sherwood PW, Osley MA (1991) Histone regulatory (hir) mutations suppress delta insertion alleles in Saccharomyces cerevisiae. Genetics 128:729–738

    PubMed  CAS  Google Scholar 

  • Shi YH, Liu J, Xia JH, Gui JF (2002) Screen for stage specific expression genes between tail bud stage and heartbeat beginning stage in embryogenesis of gynogenetic silver crucian carp. Cell Res 12:133–142

    Article  PubMed  Google Scholar 

  • Smith TF, Gaitatzes C, Saxena K, Neer EJ (1999) The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24:181–185

    Article  PubMed  CAS  Google Scholar 

  • Wang YF, Yang ZA, Gui JF (2000) Comparative studies on the changes of MPF kinase activity and cyclin synthesis during oocyte maturation in vitro in gynogenetic crucian carp and amphimictic crucian carp. Acta Zool Sin 46:71–80

    CAS  Google Scholar 

  • Wilming LG, Snoeren CA, van Rijswijk A, Grosveld F, Meijers C (1997) The murine homologue of HIRA, a DiGeorge syndrome candidate gene, is expressed in embryonic structures affected in human CATCH22 patients. Hum Mol Genet 6:247–258

    Article  PubMed  CAS  Google Scholar 

  • Xie J, Wen JJ, Chen B, Gui JF (2001) Differential gene expression in fully-grown oocytes between gynogenetic and gonochoristic crucian carps. Gene 271:109–116

    Article  PubMed  CAS  Google Scholar 

  • Xie J, Wen JJ, Yang ZA, Wang HY, Gui JF (2003) Cyclin A2 is differentially expressed during oocyte maturation between gynogenetic silver crucian carp and gonochoristic color crucian carp. J Exp Zoolog A Comp Exp Biol 295:1–16

    Article  PubMed  Google Scholar 

  • Yamashita M, Onozato H, Nakanishi T, Nagahama Y (1990). Breakdown of the sperm nuclear envelope is a prerequisite for male pronucleus formation: direct evidence from the gynogenetic crucian carp Carassius auratus langsdorfii. Dev Biol 137:155–160

    Article  PubMed  CAS  Google Scholar 

  • Yang ZA, Li QH, Wang YF, Gui JF (1999) Comparative investigation on spindle behavior and MPF activity during oocyte maturation between gynogenetic and amphimictic crucian carp. Cell Res 9:145–154

    Article  PubMed  CAS  Google Scholar 

  • Zhou L, Wang Y, Gui JF (2000a) Analysis of genetic heterogeneity among five gynogenetic clones of silver crucian carp, Carassius auratus gibelio Bloch based on detection of RAPD molecular markers. Cytogenet Cell Genet 88:133–139

    Article  PubMed  CAS  Google Scholar 

  • Zhou L, Wang Y, Gui JF (2000b) Genetic evidence for gonochoristic reproduction in gynogenetic silver crucian carp (Carassius auratus gibelio Bloch) as revealed by RAPD assays. J Mol Evol 51:498–506

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Nature Science Foundation of China (30671609) and grants from the foundation of State Key Laboratory of Freshwater Ecology and Biotechnology (2005FB20). We thank Conor McMeniman of the School of Integrative Biology, University of Queensland, Australia, for reading the manuscript and giving helpful comments.

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Authors and Affiliations

  1. College of Life Sciences, Central China Normal University, Wuhan, 430079, China

    X. Z. Du, L. Zhou, H. B. Zhao & Y. F. Wang

  2. State Key Laboratory of Freshwater Ecology and Biotechnology, Wuhan Center for Developmental Biology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China

    J. F. Gui

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  1. X. Z. Du
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  2. L. Zhou
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  3. H. B. Zhao
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  4. Y. F. Wang
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  5. J. F. Gui
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Correspondence to Y. F. Wang.

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Du, X.Z., Zhou, L., Zhao, H.B. et al. Identical sequences but different expression patterns of Hira gene in gynogenetic and gonochoristic crucian carps. Fish Physiol Biochem 34, 175–184 (2008). https://doi.org/10.1007/s10695-007-9158-1

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  • DOI: https://doi.org/10.1007/s10695-007-9158-1

Keywords

  • Hira gene
  • cDNA cloning
  • Gene expression
  • Gynogenesis
  • Gibel carp

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