Advertisement

Chromosome Research

, Volume 22, Issue 1, pp 71–83 | Cite as

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

  • Marla C. McPherson
  • Charmaine M. Robinson
  • Lida P. Gehlen
  • Mary E. Delany
Research Article

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.

Keywords

Japanese Quail Chicken Turkey Telomere Telomerase Ribosomal DNA Major Histocompatibility Complex 

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

Notes

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.

References

  1. Ainsworth SJ, Stanley RL, Evans DJR (2010) Developmental stages of the Japanese quail. J Anat 216:3–15PubMedCentralPubMedCrossRefGoogle Scholar
  2. 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):6–9PubMedCrossRefGoogle Scholar
  3. 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):070–073CrossRefGoogle Scholar
  4. 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):335–343CrossRefGoogle Scholar
  5. Biederman BM, Florence D, Lin CC (1980) Cytogenetic analysis of great horned owls (Bubo virginianus). Cytogenet Cell Genet 28(1–2):79–86PubMedCrossRefGoogle Scholar
  6. 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):146–154PubMedGoogle Scholar
  7. Burt DW, Bruley C, Dunn IC et al (1999) The dynamics of chromosome evolution in birds and mammals. Nature 402:411–413PubMedCrossRefGoogle Scholar
  8. Chaves LD, Kreuth SB, Reed KM (2007) Characterization of the turkey MHC chromosome through genetic and physical mapping. Cytogenet Genome Res 117:213–220PubMedCrossRefGoogle Scholar
  9. Chaves LD, Krueth SB, Reed KM (2009) Defining the turkey MHC: sequence and genes of the B locus. J Immunol 183:6530–6537PubMedCrossRefGoogle Scholar
  10. Christidis L (1990) Chordata, no. 3: aves. animal cytogenetics 4. Gebrüder Borntraeger, BerlinGoogle Scholar
  11. Delany ME, Daniels LM (2003a) Molecular and cytogenetic organization of the 5S ribosomal DNA array in chicken (Gallus gallus). Chromosom Res 11:305–317CrossRefGoogle Scholar
  12. 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 102:309–317PubMedCrossRefGoogle Scholar
  13. Delany ME, Daniels LM (2004) The chicken telomerase reverse transcriptase (chTERT): molecular and cytogenetic characterization with a comparative analysis. Gene 339:61–69PubMedCrossRefGoogle Scholar
  14. Delany ME, Krupkin AB (1999) Molecular characterization of ribosomal gene variation within and among NORs segregating in specialized populations of chicken. Genome 42:60–71PubMedCrossRefGoogle Scholar
  15. 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 90:139–145PubMedCrossRefGoogle Scholar
  16. 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 117:54–63PubMedCrossRefGoogle Scholar
  17. 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):507–514PubMedCrossRefGoogle Scholar
  18. 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):715–723CrossRefGoogle Scholar
  19. 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 75:7–9CrossRefGoogle Scholar
  20. 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):307–313CrossRefGoogle Scholar
  21. Griffin DK, Robertson LBW, Tempest HG, Skinner BM (2007) The evolution of the avian genome as revealed by comparative molecular cytogenetics. Cytogenet Genome Res 117:64–77PubMedCrossRefGoogle Scholar
  22. 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 9:168PubMedCentralPubMedCrossRefGoogle Scholar
  23. Huss D, Poynter G, Lansford R (2008) Japanese quail (Coturnix japonica) as a laboratory animal model. Lab Anim 37(11):513–519CrossRefGoogle Scholar
  24. International Chicken Genome Sequencing Consortium (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432(7018):695–716CrossRefGoogle Scholar
  25. 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 7:101PubMedCentralPubMedCrossRefGoogle Scholar
  26. Knibiehler B, Navarro A, Mirre C, Stahl A (1977) Localization of ribosomal cistrons in the quail oocyte during meiotic prophase I. Exp Cell Res 110:153–157PubMedCrossRefGoogle Scholar
  27. Le Douarin NM (2008) Developmental patterning deciphered in avian chimeras. Dev Growth Differ 50(suppl 1):S11–S28PubMedCrossRefGoogle Scholar
  28. Lee MK, Ren CW, Yan B et al (2003) Construction and characterization of three BAC libraries for analysis of the chicken genome. Anim Genet 34:151–152PubMedCrossRefGoogle Scholar
  29. Lithgrow, et al. 2014 (current issue) Chromosome Research.Google Scholar
  30. Miller M, Bacon LD, Hala K et al (2004) Nomenclature for the chicken major histocompatibility (B and Y) complex. Immunogenetics 56(4):261–279PubMedCrossRefGoogle Scholar
  31. 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):215–227PubMedCrossRefGoogle Scholar
  32. 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 17:947–964CrossRefGoogle Scholar
  33. 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):1–102Google Scholar
  34. Reed KM, Chaves LD, Hall MK, Knutson TP, Harry DE (2005) A comparative genetic map of the turkey genome. Cytogenet Genome Res 111(2):118–127PubMedCrossRefGoogle Scholar
  35. 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):753–771PubMedCrossRefGoogle Scholar
  36. 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):581–591CrossRefGoogle Scholar
  37. Sasaki M, Nishida C (1981) Nucleolar chromosomes of the domestic chicken and the Japanese quail. Chr Inf Serv 30:25–27Google Scholar
  38. Schmid M, Nanda I, Guttenbach M et al (2000) First report on chicken genes and chromosomes. Cytogenet Cell Genet 90:169–218PubMedCrossRefGoogle Scholar
  39. Shetty S, Griffin DK, Marshall-Graves JA (1999) Comparative chromosome painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosom Res 7:289–295CrossRefGoogle Scholar
  40. 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):103–109Google Scholar
  41. 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):111–119PubMedCrossRefGoogle Scholar
  42. 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 10:357PubMedCentralPubMedCrossRefGoogle Scholar
  43. Skinner et al. 2014 (current issue). Chromosome Research.Google Scholar
  44. 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):305–315PubMedCrossRefGoogle Scholar
  45. Takagi N, Sasaki M (1974) A phylogenetic study of bird karyotypes. Chromosoma 46:91–120PubMedCrossRefGoogle Scholar
  46. Van Tuinen M, Dyke GJ (2004) Calibration of galliform molecular clocks using multiple fossils and genetic partitions. Mol Phylogenet Evol 30(1):74–86PubMedCrossRefGoogle Scholar
  47. Van Tuinen M, Hedges SB (2001) Calibration of avian molecular clocks. Mol Biol Evol 18:206–213PubMedCrossRefGoogle Scholar
  48. 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 20:503–511PubMedCentralPubMedCrossRefGoogle Scholar
  49. 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 12:447PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Marla C. McPherson
    • 1
  • Charmaine M. Robinson
    • 1
  • Lida P. Gehlen
    • 1
  • Mary E. Delany
    • 1
  1. 1.Department of Animal ScienceUniversity of CaliforniaDavisUSA

Personalised recommendations