Journal Mobile Options
Table of Contents
Vol. 122, No. 2, 2008
Issue release date: December 2008
Cytogenet Genome Res 122:150–156 (2008)
(DOI:10.1159/000163092)

Synteny conservation of the Z chromosome in 14 avian species (11 families) supports a role for Z dosage in avian sex determination

Nanda I. · Schlegelmilch K. · Haaf T. · Schartl M. · Schmid M.
Institutes of aHuman Genetics and bPhysiological Chemistry I, University of Würzburg, Würzburg; cInstitute of Human Genetics, University of Mainz, Mainz (Germany)

Individual Users: Register with Karger Login Information

Please create your User ID & Password





Contact Information











I have read the Karger Terms and Conditions and agree.

To view the fulltext, please log in

To view the pdf, please log in

Abstract

In order to determine synteny conservation of the avian Z chromosome, a chicken (Gallus gallus, GGA) Z chromosome painting probe was hybridized to the chromosomes of 14 bird species belonging to 11 different families. The GGAZ painted the Z chromosomes in all species analyzed, suggesting strong conservation of its gene content among the different avian lineages. This was confirmed by the mapping of five GGAZ-orthologous genes (DMRT1, GHR, CHRNB3, ALDOB, B4GALT1) to the Z chromosomes of eight other species. The shuffled order of these genes on different Z chromosomes can be explained by the prevalence of intrachromosomal rearrangements during avian evolution. Synteny conservation of the mammalian X is generally thought to be the result of X chromosome inactivation. The absence of Z chromosome inactivation implies sex-specific dosage differences of a highly conserved array of Z-linked genes in birds. The evolutionary conservation of the entire Z chromosome among avian lineages supports the idea that avian sex determination and/or sex-specific functions are largely based on sex chromosome dosage. We propose that the accumulation of male-specific genes on the Z chromosome confers selective pressure on the Z to conserve its synteny.



Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. Backström N, Brandström M, Gustafsson L, Qvarnström A, Cheng H, Ellegren H: Genetic mapping in a natural population of collared flycatchers (Ficedula albicollis): conserved synteny but gene order rearrangements on the avian Z chromosome. Genetics 174:377–386 (2006).
  2. Baverstock PR, Adams M, Polkinghorne RW, Gelder M: A sex-linked enzyme in birds – Z-chromosome conservation but no dosage compensation. Nature 296:763–766 (1982).
  3. Bloom SE, Delaney ME, Muscarella DE: Constant and variable features of avian chromosomes, in Etches RJ, Gibbons AMV (eds): Manipulation of the Avian Genome, pp 39–60 (CRC Press, Guelph 1993).
  4. Burt DW, Bruley C, Dunn IC, Jones CT, Ramage A, et al: The dynamics of chromosome evolution in birds and mammals. Nature 402:411–413 (1999).
  5. Carter NP, Ferguson-Smith MA, Perryman MT, Telenius H, Pelmear AH, et al: Reverse chromosome painting: a method for the rapid analysis of aberrant chromosomes in clinical cytogenetics. J Med Genet 29:299–307 (1992).
  6. Chen X, Agate RJ, Itoh Y, Arnold AP: Sexually dimorphic expression of trkB, a Z-linked gene, in early posthatch zebra finch brain. Proc Natl Acad Sci USA 102:7730–7735 (2005).
  7. Christidis L: Aves, in John B (ed): Animal Cytogenetics, Vol 4, Chordata 3 (Gebrüder Bornträger, Berlin 1990).
  8. de Oliveira EH, Habermann FA, Lacerda O, Sbalqueiro IJ, Wienberg J, Müller S: Chromosome reshuffling in birds of prey: the karyotype of the world’s largest eagle (Harpy eagle, Harpia harpyja) compared to that of the chicken (Gallus gallus). Chromosoma 114:338–343 (2005).
  9. Derjusheva S, Kurganova A, Habermann F, Gaginskaya E: High chromosome conservation detected by comparative chromosome painting in chicken, pigeon and passerine birds. Chromosome Res 12:715–723 (2004).
  10. Ellegren H: Evolution of the avian sex chromosomes and their role in sex determination. Trends Ecol Evol 15:188–192 (2000).
  11. Ellegren H, Hultin-Rosenberg L, Brunström B, Dencker L, Kultima K, Scholz B: Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes. BMC Biol 5:40 (2007).
  12. Fridolfsson AK, Cheng H, Copeland NG, Jenkins NA, Liu HC, et al: Evolution of the avian sex chromosomes from an ancestral pair of autosomes. Proc Natl Acad Sci USA 95:8147–8152 (1998).
  13. González J, Ranz JM, Ruiz A: Chromosomal elements evolve at different rates in the Drosophila genome. Genetics 161:1137–1154 (2002).
  14. Graves JA: Sex chromosome specialization and degeneration in mammals. Cell 124:901–914 (2006).
  15. Guttenbach M, Nanda I, Feichtinger W, Masabanda JS, Griffin DK, Schmid M: Comparative chromosome painting of chicken autosomal paints 1–9 in nine different bird species. Cytogenet Genome Res 103:173–184 (2003).
  16. Hillier LW, Miller RD, Baird SE, Chinwalla A, Fulton LA, et al: Comparison of C. elegans and C. briggsae genome sequences reveals extensive conservation of chromosome organization and synteny. PLoS Biol 5:e167 (2007).
  17. International Chicken Genome Sequencing Consortium: Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695–716 (2004).
  18. Itoh Y, Arnold AP: Chromosomal polymorphism and comparative painting analysis in the zebra finch. Chromosome Res 13:47–56 (2005).
  19. Itoh Y, Kampf K, Arnold AP: Comparison of the chicken and zebra finch Z chromosomes shows evolutionary rearrangements. Chromosome Res 14:805–815 (2006).
  20. Itoh Y, Melamed E, Yang X, Kampf K, Wang S, et al: Dosage compensation is less effective in birds than in mammals. J Biol 6:2 (2007).
  21. Kaiser VB, Ellegren H: Nonrandom distribution of genes with sex-biased expression in the chicken genome. Evolution 60:1945–1951 (2006).
  22. Khil PP, Smirnova NA, Romanienko PJ, Camerini-Otero RD: The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat Genet 36:642–646 (2004).
  23. Kuroda Y, Arai N, Arita M, Teranishi M, Hori T, et al: Absence of Z-chromosome inactivation for five genes in male chickens. Chromosome Res 9:457–468 (2001).
  24. Lahn BT, Page DC: Four evolutionary strata on the human X chromosome. Science 286:964–967 (1999).
  25. Lercher MJ, Urrutia AO, Hurst LD: Evidence that the human X chromosome is enriched for male-specific but not female-specific genes. Mol Biol Evol 20:1113–1116 (2003).
  26. Matsubara K, Tarui H, Toriba M, Yamada K, Nishida-Umehara C, et al: Evidence for different origin of sex chromosomes in snakes, birds, and mammals and step-wise differentiation of snake sex chromosomes. Proc Natl Acad Sci USA 103:18190–18195 (2006).
  27. Murphy WJ, Sun S, Chen ZQ, Pecon-Slattery J, O’Brien SJ: Extensive conservation of sex chromosome organization between cat and human revealed by parallel radiation hybrid mapping. Genome Res 9:1223–1230 (1999).
  28. Nanda I, Shan Z, Schartl M, Burt DW, Koehler M, et al: 300 million years of conserved synteny between chicken Z and human chromosome 9. Nat Genet 21:258–259 (1999).
  29. Nanda I, Haaf T, Schartl M, Schmid M, Burt DW: Comparative mapping of Z-orthologous genes in vertebrates: implications for the evolution of avian sex chromosomes. Cytogenet Genome Res 99:178–184 (2002).
  30. Nanda I, Karl E, Volobouev V, Griffin DK, Schartl M, Schmid M: Extensive gross genomic rearrangements between chicken and Old World vultures (Falconiformes: Accipitridae). Cytogenet Genome Res 112:286–295 (2006).
  31. Nanda I, Karl E, Griffin DK, Schartl M, Schmid M: Chromosome repatterning in three representative parrots (Psittaciformes) inferred from comparative chromosome painting. Cytogenet Genome Res 117:43–53 (2007).
  32. Nishida-Umehara C, Tsuda Y, Ishijima J, Ando J, Fujiwara A, et al: The molecular basis of chromosome orthologies and sex chromosomal differentiation in palaeognathous birds. Chromosome Res 15:721–734 (2007).
  33. Ohno S: Sex Chromosomes and Sex Linked Genes (Springer Verlag, Berlin 1967).
  34. Rahn MI, Solari AJ: Recombination nodules in the oocytes of the chicken, Gallus domesticus. Cytogenet Cell Genet 43:187–193 (1986).
  35. Raudsepp T, Houck ML, O’Brien PC, Ferguson-Smith MA, Ryder OA, Chowdhary BP: Cytogenetic analysis of California condor (Gymnogyps californianus) chromosomes: comparison with chicken (Gallus gallus) macrochromosomes. Cytogenet Genome Res 98:54–60 (2002).
  36. Raudsepp T, Lee EJ, Kata SR, Brinkmeyer C, Mickelson JR, et al: Exceptional conservation of horse-human gene order on X chromosome revealed by high-resolution radiation hybrid mapping. Proc Natl Acad Sci USA 101:2386–2391 (2004).
  37. Reinke V, Smith HE, Nance J, Wang J, Van Doren C, et al: A global profile of germline gene expression in C. elegans. Mol Cell 6:605–616 (2000).
  38. Ross MT, Grafham DV, Coffey AJ, Scherer S, McLay K, et al: The DNA sequence of the human X chromosome. Nature 434:325–337 (2005).
  39. Saether SA, Saetre GP, Borge T, Wiley C, Svedin N, et al: Sex chromosome-linked species recognition and evolution of reproductive isolation in flycatchers. Science 318:95–97 (2007).
  40. Schmid M: Chromosome banding in Amphibia. IV. Differentiation of GC- and AT-rich chromosome regions in Anura. Chromosoma 77:83–103 (1980).
  41. Schmid M, Enderle E, Schindler D, Schempp W: Chromosome banding and DNA replication patterns in bird karyotypes. Cytogenet Cell Genet 52:139–146 (1989).
  42. Schmid M, Nanda I, Guttenbach M, Steinlein C, Hoehn M, et al: First report on chicken genes and chromosomes 2000. Cytogenet Cell Genet 90:169–218 (2000).
  43. Shan Z, Nanda I, Wang Y, Schmid M, Vortkamp A, Haaf T: Sex-specific expression of an evolutionarily conserved male regulatory gene, DMRT1, in birds. Cytogenet Cell Genet 89:252–257 (2000).
  44. Shetty S, Griffin DK, Graves JA: Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosome Res 7:289–295 (1999).
  45. Shibusawa M, Nishibori M, Nishida-Umehara C, Tsudzuki M, Masabanda J, et al: 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 106:111–119 (2004a).
  46. Shibusawa M, Nishida-Umehara C, Tsudzuki M, Masabanda J, Griffin DK, Matsuda Y: A comparative karyological study of the blue-breasted quail (Coturnix chinensis, Phasianidae) and California quail (Callipepla californica, Odontophoridae). Cytogenet Genome Res 106:82–90 (2004b).
  47. Smith CA, Roeszler KN, Hudson QJ, Sinclair AH: Avian sex determination: what, when and where? Cytogenet Genome Res 117:165–173 (2007).
  48. Stein LD, Bao Z, Blasiar D, Blumenthal T, Brent MR, et al: The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol 1:E45 (2003).
  49. Storchová R, Divina P: Nonrandom representation of sex-biased genes on chicken Z chromosome. J Mol Evol 63:676–681 (2006).
  50. Sturgill D, Zhang Y, Parisi M, Oliver B: Demasculinization of X chromosomes in the Drosophila genus. Nature 450:238–241 (2007).
  51. Sumner AT: A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306 (1972).
  52. Suzuki T, Kansaku N, Kurosaki T, Shimada K, Zadworny D, et al: Comparative FISH mapping on Z chromosomes of chicken and Japanese quail. Cytogenet Cell Genet 87:22–26 (1999).
  53. Tsuda Y, Nishida-Umehara C, Ishijima J, Yamada K, Matsuda Y: Comparison of the Z and W sex chromosomal architectures in elegant crested tinamou (Eudromia elegans) and ostrich (Struthio camelus) and the process of sex chromosome differentiation in palaeognathous birds. Chromosoma 116:159–173 (2007).
  54. van Tuinen M, Hedges SB: Calibration of avian molecular clocks. Mol Biol Evol 18:206–213 (2001).
  55. Wang PJ, McCarrey JR, Yang F, Page DC: An abundance of X-linked genes expressed in spermatogonia. Nat Genet 27:422–426 (2001).
  56. Yang F, Müller S, Just R, Ferguson-Smith MA, Wienberg J: Comparative chromosome painting in mammals: human and the Indian muntjac (Muntiacus muntjak vaginalis). Genomics 39:396–401 (1997).


Pay-per-View Options
Direct payment This item at the regular price: USD 38.00
Payment from account With a Karger Pay-per-View account (down payment USD 150) you profit from a special rate for this and other single items.
This item at the discounted price: USD 26.50