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Comparative cytogenomics of poultry: mapping of single gene and repeat loci in the Japanese quail (Coturnix japonica)

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Abstract

Well-characterized molecular and cytogenetic maps are yet to be established in Japanese quail (Coturnix japonica). The aim of the current study was to cytogenetically map and determine linkage of specific genes and gene complexes in Japanese quail through the use of chicken (Gallus gallus) and turkey (Meleagris gallopavo) genomic DNA probes and conduct a comparative study among the three genomes. Chicken and turkey clones were used as probes on mitotic metaphase and meiotic pachytene stage chromosomes of the three species for the purpose of high-resolution fluorescence in situ hybridization (FISH). The genes and complexes studied included telomerase RNA (TR), telomerase reverse transcriptase (TERT), 5S rDNA, 18S-5.8S-28S rDNA (i.e., nucleolus organizer region (NOR)), and the major histocompatibility complex (MHC). The telomeric profile of Japanese quail was investigated through the use of FISH with a TTAGGG-PNA probe. A range of telomeric array sizes were confirmed as found for the other poultry species. Three NOR loci were identified in Japanese quail, and single loci each for TR, TERT, 5S rDNA and the MHC-B. The MHC-B and one NOR locus were linked on a microchromosome in Japanese quail. We confirmed physical linkage of 5S rDNA and the TR gene on an intermediate-sized chromosome in quail, similar to both chicken and turkey. TERT localized to CJA 2 in quail and the orthologous chromosome region in chicken (GGA 2) and in turkey (MGA 3). The cytogenetic profile of Japanese quail was further developed by this study and synteny was identified among the three poultry species.

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Abbreviations

BAC:

Bacterial artificial chromosome

CE:

Chicken embryo

CEF:

Chicken embryo fibroblast

CJA:

Coturnix japonica

DAPI:

4′,6-Diamidino-2-phenylindole

E:

Embryonic day or days of embryogenesis

ETS:

External transcribed spacer

FISH:

Fluorescence in situ hybridization

GGA:

Gallus gallus

MGA:

Meleagris gallopavo

MHC:

Major histocompatibility complex

MY:

Million years

NOR:

Nucleolus organizer region

PNA:

Peptide nucleic acid

rDNA:

Ribosomal DNA

TEF:

Turkey embryo fibroblast

TERT:

Telomerase reverse transcriptase

TR:

Telomerase RNA

UCD:

University of California, Davis

References

  • Ainsworth SJ, Stanley RL, Evans DJR (2010) Developmental stages of the Japanese quail. J Anat 216:3–15

    Article  PubMed Central  PubMed  Google Scholar 

  • Ansari HA, Takagi N, Sasaki M (1986) Interordinal conservatism of chromosome banding patterns in Gallus domesticus (Galliformes) and Melopsittacus undulates (Psittaciformes). Cytogenet Cell Genet 43(1–2):6–9

    Article  PubMed  CAS  Google Scholar 

  • Barbosa MO, Silva RR, Correia VCS, Santos LP, Garner AV, Gunski RJ (2013) Nucleolar organizer regions in Sittasomus griseicapillus and Lepidocolaptes angustirostris (Aves, Dendrocolaptidae): evidence of a chromosome inversion. Genet Mol Biol 36(1):070–073

    Article  CAS  Google Scholar 

  • Bed’Hom B, Coullin P, Guillier-Gencik Z, Moulin S, Bernheim A, Volobouev V (2003) Characterization of the atypical karyotype of the black-winged kite Elanus caeruleus (Falconiformes: Accipitridae) by means of classical and molecular cytogenetic techniques. Chromosom Res 11(4):335–343

    Article  Google Scholar 

  • Biederman BM, Florence D, Lin CC (1980) Cytogenetic analysis of great horned owls (Bubo virginianus). Cytogenet Cell Genet 28(1–2):79–86

    Article  PubMed  CAS  Google Scholar 

  • Bloom SE, Bacon LD (1985) Linkage of the major histocompatibility (B) complex and the nucleolar organizer in the chicken: assignment to a microchromosome. J Hered 76(3):146–154

    PubMed  CAS  Google Scholar 

  • Burt DW, Bruley C, Dunn IC et al (1999) The dynamics of chromosome evolution in birds and mammals. Nature 402:411–413

    Article  PubMed  CAS  Google Scholar 

  • Chaves LD, Kreuth SB, Reed KM (2007) Characterization of the turkey MHC chromosome through genetic and physical mapping. Cytogenet Genome Res 117:213–220

    Article  PubMed  CAS  Google Scholar 

  • Chaves LD, Krueth SB, Reed KM (2009) Defining the turkey MHC: sequence and genes of the B locus. J Immunol 183:6530–6537

    Article  PubMed  CAS  Google Scholar 

  • Christidis L (1990) Chordata, no. 3: aves. animal cytogenetics 4. Gebrüder Borntraeger, Berlin

    Google Scholar 

  • Delany ME, Daniels LM (2003a) Molecular and cytogenetic organization of the 5S ribosomal DNA array in chicken (Gallus gallus). Chromosom Res 11:305–317

    Article  Google Scholar 

  • Delany ME, Daniels LM (2003b) The chicken telomerase RNA gene: conservation of sequence, regulatory elements and synteny among viral, avian and mammalian genomes. Cytogenet Genome Res 102:309–317

    Article  PubMed  CAS  Google Scholar 

  • Delany ME, Daniels LM (2004) The chicken telomerase reverse transcriptase (chTERT): molecular and cytogenetic characterization with a comparative analysis. Gene 339:61–69

    Article  PubMed  CAS  Google Scholar 

  • Delany ME, Krupkin AB (1999) Molecular characterization of ribosomal gene variation within and among NORs segregating in specialized populations of chicken. Genome 42:60–71

    Article  PubMed  CAS  Google Scholar 

  • Delany ME, Krupkin AB, Miller MM (2000) Organization of telomere sequences in birds: evidence for arrays of extreme length and for in vivo shortening. Cytogenet Cell Genet 90:139–145

    Article  PubMed  CAS  Google Scholar 

  • Delany ME, Gessaro TM, Rodrigue KL, Daniels LM (2007) Chromosomal mapping of chicken mega-telomere arrays to GGA9, 16, 28 and W using a cytogenomic approach. Cytogenet Genome Res 117:54–63

    Article  PubMed  CAS  Google Scholar 

  • Delany ME, Robinson CR, Goto RM, Miller MM (2009) Architecture and organization of chicken microchromosome 16: order of the NOR, MHC-Y, and MHC-B subregions. J Hered 100(5):507–514

    Article  PubMed  CAS  Google Scholar 

  • Derjusheva S, Kurganova A, Habermann F, Gaginskaya E (2004) High chromosome conservation detected by comparative chromosome painting in chicken, pigeon and passerine birds. Chromosom Res 12(7):715–723

    Article  CAS  Google Scholar 

  • Fillon V, Zoorob R, Yerle M, Auffray C, Vignal A (1996) Mapping of the genetically independent chicken major histocompatibility complexes B and RFP-Y to the same microchromosome by two-color fluorescent in situ hybridization. Cytogenet Genome Res 75:7–9

    Article  CAS  Google Scholar 

  • Fillon V, Morisson M, Zoorob R et al (1998) Identification of 16 chicken microchromosomes by molecular markers using two-colour fluorescence in situ hybridization (FISH). Chromosom Res 6(4):307–313

    Article  CAS  Google Scholar 

  • Griffin DK, Robertson LBW, Tempest HG, Skinner BM (2007) The evolution of the avian genome as revealed by comparative molecular cytogenetics. Cytogenet Genome Res 117:64–77

    Article  PubMed  CAS  Google Scholar 

  • Griffin DK, Robertson LB, Tempest HG et al (2008) Whole genome comparative studies between chicken and turkey and their implications for avian genome evolution. BMC Genomics 9:168

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Huss D, Poynter G, Lansford R (2008) Japanese quail (Coturnix japonica) as a laboratory animal model. Lab Anim 37(11):513–519

    Article  Google Scholar 

  • International Chicken Genome Sequencing Consortium (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432(7018):695–716

    Article  CAS  Google Scholar 

  • Kayang BB, Fillon V, Inoue-Murayama M et al (2006) Integrated maps in quail (Coturnix japonica) confirm the high degree of synteny conservation with chicken (Gallus gallus) despite 35 million years of divergence. BMC Genomics 7:101

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Knibiehler B, Navarro A, Mirre C, Stahl A (1977) Localization of ribosomal cistrons in the quail oocyte during meiotic prophase I. Exp Cell Res 110:153–157

    Article  PubMed  CAS  Google Scholar 

  • Le Douarin NM (2008) Developmental patterning deciphered in avian chimeras. Dev Growth Differ 50(suppl 1):S11–S28

    Article  PubMed  Google Scholar 

  • Lee MK, Ren CW, Yan B et al (2003) Construction and characterization of three BAC libraries for analysis of the chicken genome. Anim Genet 34:151–152

    Article  PubMed  CAS  Google Scholar 

  • Lithgrow, et al. 2014 (current issue) Chromosome Research.

  • Miller M, Bacon LD, Hala K et al (2004) Nomenclature for the chicken major histocompatibility (B and Y) complex. Immunogenetics 56(4):261–279

    Article  PubMed  CAS  Google Scholar 

  • Nanda I, Schrama D, Feichtinger W, Haaf T, Schartl M, Schmid M (2002) Distribution of telomeric (TTAGGG) (n) sequences in avian chromosomes. Chromosoma 111(4):215–227

    Article  PubMed  CAS  Google Scholar 

  • O’Hare TH, Delany ME (2009) Genetic variation exists for telomeric array organization within and among the genomes of normal, immortalized, and transformed chicken systems. Chromosom Res 17:947–964

    Article  CAS  Google Scholar 

  • Pisenti JM, Delany ME, Taylor RL Jr, Abbott UK, Abplanalp H, Arthur JA, Bakst MR, CBaxter-Jones C, Bitgood JJ, Bradley F, Cheng KM, Dietert RR, Dodgson JB, Donoghue A, Emsley AE, Etches R, Frahm RR, Gerrits RJ, Goetinck PF, Grunder AA, Harry DE, Lamont SJ, Martin GR, McGuire PE, Moberg GP, Pierro LJ, Qualset CO, Qureshi M, Schultz F, Wilson BW (2001) Avian genetic resources at risk: an assessment and proposal for conservation of genetic stocks in the USA and Canada. Avian Poult Biol Rev 12(1&2):1–102

    Google Scholar 

  • Reed KM, Chaves LD, Hall MK, Knutson TP, Harry DE (2005) A comparative genetic map of the turkey genome. Cytogenet Genome Res 111(2):118–127

    Article  PubMed  CAS  Google Scholar 

  • Reed KM, Bauer MM, Monson MS, Benoit B, Chaves LD, O’Hare TH, Delany ME (2011) Defining the turkey MHC: identification of expressed class I- and class IIB-like genes independent of the MHC-B. Immunogenetics 63(11):753–771

    Article  PubMed  CAS  Google Scholar 

  • Rodrigue KL, May BP, Famula TR, Delany ME (2005) Meiotic instability of chicken ultra-long telomeres and mapping of a 2.8 megabase array to the W-sex chromosome. Chromosom Res 13(6):581–591

    Article  CAS  Google Scholar 

  • Sasaki M, Nishida C (1981) Nucleolar chromosomes of the domestic chicken and the Japanese quail. Chr Inf Serv 30:25–27

    Google Scholar 

  • Schmid M, Nanda I, Guttenbach M et al (2000) First report on chicken genes and chromosomes. Cytogenet Cell Genet 90:169–218

    Article  PubMed  CAS  Google Scholar 

  • Shetty S, Griffin DK, Marshall-Graves JA (1999) Comparative chromosome painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosom Res 7:289–295

    Article  CAS  Google Scholar 

  • Shibusawa M, Minai S, Nishida-Umehara C et al (2001) A comparative cytogenetic study of chromosome homology between chicken and Japanese quail. Cytogenet Cell Genet 95(1–2):103–109

    Google Scholar 

  • Shibusawa M, Nishibori M, Nishida-Umehara C, Tsudzuki M, Masabanda J, Griffin DK, Matsuda Y (2004) Karyotypic evolution in the Galliformes: an examination of the process of karyotypic evolution by comparison of the molecular cytogenetic findings with the molecular phylogeny. Cytogenet Genome Res 106(1):111–119

    Article  PubMed  CAS  Google Scholar 

  • Skinner BM, Robertson LBW, Tempest HG, Langley EJ, Ioannou D, Fowler KE, Crooijmans RPMA, Hall AD, Griffin DK, VÖlker M (2009) Comparative genomics in chicken and Pekin duck using FISH mapping and microarray analysis. BMC Genomics 10:357

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Skinner et al. 2014 (current issue). Chromosome Research.

  • Stanyon R, Bigoni F, Slaby T et al (2004) Multi-directional chromosome painting maps homologies between species belonging to three genera of New World monkeys and humans. Chromosoma 113(6):305–315

    Article  PubMed  CAS  Google Scholar 

  • Takagi N, Sasaki M (1974) A phylogenetic study of bird karyotypes. Chromosoma 46:91–120

    Article  PubMed  CAS  Google Scholar 

  • Van Tuinen M, Dyke GJ (2004) Calibration of galliform molecular clocks using multiple fossils and genetic partitions. Mol Phylogenet Evol 30(1):74–86

    Article  PubMed  CAS  Google Scholar 

  • Van Tuinen M, Hedges SB (2001) Calibration of avian molecular clocks. Mol Biol Evol 18:206–213

    Article  PubMed  Google Scholar 

  • VÖlker M, BackstrÖm N, Skinner B, Langley EJ, Bunzey SK, Ellegren H, Griffin DK (2010) Copy number variation, chromosome rearrangement, and their association with recombination during avian evolution. Genome Res 20:503–511

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhang Y, Zhang X, O’Hare TH et al (2011) A comparative physical map reveals the pattern of chromosomal evolution between the turkey (Meleagris gallopavo) and chicken (Gallus gallus) genomes. BMC Genomics 12:447

    Article  PubMed Central  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors greatly appreciate the research contributions of Andrew Jiang, Thomas H. O’Hare, and Elizabeth A. Robb. Research was funded by United States Department of Agriculture-National Institute of Food and Agriculture multistate and nation projects: National Research Support Program-8 (CA-D*-ASC-7233-RR), NC-1170 (CA-D*-ASC-6414-RR), and NE-1034 (CA-D*-ASC-7281-RR). We appreciate the support of the California Agricultural Experiment Station and the Department of Animal Science and College of Agricultural and Environmental Sciences at the University of California, Davis.

Ethical standards

The authors declare that all experiments performed in this study comply with the current laws of the USA. All institutional and national guidelines for the care and use of laboratory animals were followed.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Animal Science, University of California, One Shields Ave, Davis, CA, 95616, USA

    Marla C. McPherson, Charmaine M. Robinson, Lida P. Gehlen & Mary E. Delany

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  1. Marla C. McPherson
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  2. Charmaine M. Robinson
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  3. Lida P. Gehlen
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  4. Mary E. Delany
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Correspondence to Mary E. Delany.

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Responsible Editors: Darren K. Griffin and Beth A. Sullivan.

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McPherson, M.C., Robinson, C.M., Gehlen, L.P. et al. Comparative cytogenomics of poultry: mapping of single gene and repeat loci in the Japanese quail (Coturnix japonica). Chromosome Res 22, 71–83 (2014). https://doi.org/10.1007/s10577-014-9411-2

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