Synteny conservation of the Z chromosome in 14 avian species (11 families) supports a role for Z dosage in avian sex determinationNanda I.a · Schlegelmilch K.a · Haaf T.c · Schartl M.b · Schmid M.a
Institutes of aHuman Genetics and bPhysiological Chemistry I, University of Würzburg, Würzburg; cInstitute of Human Genetics, University of Mainz, Mainz (Germany)
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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.
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- 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).
- 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).
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).
- 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).
- 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).
- 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).
Christidis L: Aves, in John B (ed): Animal Cytogenetics, Vol 4, Chordata 3 (Gebrüder Bornträger, Berlin 1990).
- 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).
- 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).
- Ellegren H: Evolution of the avian sex chromosomes and their role in sex determination. Trends Ecol Evol 15:188–192 (2000).
- 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).
- 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).
- González J, Ranz JM, Ruiz A: Chromosomal elements evolve at different rates in the Drosophila genome. Genetics 161:1137–1154 (2002).
- Graves JA: Sex chromosome specialization and degeneration in mammals. Cell 124:901–914 (2006).
- 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).
- 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).
- International Chicken Genome Sequencing Consortium: Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695–716 (2004).
- Itoh Y, Arnold AP: Chromosomal polymorphism and comparative painting analysis in the zebra finch. Chromosome Res 13:47–56 (2005).
- Itoh Y, Kampf K, Arnold AP: Comparison of the chicken and zebra finch Z chromosomes shows evolutionary rearrangements. Chromosome Res 14:805–815 (2006).
- 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).
- Kaiser VB, Ellegren H: Nonrandom distribution of genes with sex-biased expression in the chicken genome. Evolution 60:1945–1951 (2006).
- 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).
- 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).
- Lahn BT, Page DC: Four evolutionary strata on the human X chromosome. Science 286:964–967 (1999).
- 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).
- 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).
- 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).
- 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).
- 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).
- 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).
- 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).
- 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).
Ohno S: Sex Chromosomes and Sex Linked Genes (Springer Verlag, Berlin 1967).
- Rahn MI, Solari AJ: Recombination nodules in the oocytes of the chicken, Gallus domesticus. Cytogenet Cell Genet 43:187–193 (1986).
- 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).
- 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).
- 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).
- 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).
- 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).
- Schmid M: Chromosome banding in Amphibia. IV. Differentiation of GC- and AT-rich chromosome regions in Anura. Chromosoma 77:83–103 (1980).
- Schmid M, Enderle E, Schindler D, Schempp W: Chromosome banding and DNA replication patterns in bird karyotypes. Cytogenet Cell Genet 52:139–146 (1989).
- 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).
- 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).
- 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).
- 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).
- 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).
- Smith CA, Roeszler KN, Hudson QJ, Sinclair AH: Avian sex determination: what, when and where? Cytogenet Genome Res 117:165–173 (2007).
- 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).
- Storchová R, Divina P: Nonrandom representation of sex-biased genes on chicken Z chromosome. J Mol Evol 63:676–681 (2006).
- Sturgill D, Zhang Y, Parisi M, Oliver B: Demasculinization of X chromosomes in the Drosophila genus. Nature 450:238–241 (2007).
- Sumner AT: A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306 (1972).
- 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).
- 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).
- van Tuinen M, Hedges SB: Calibration of avian molecular clocks. Mol Biol Evol 18:206–213 (2001).
- Wang PJ, McCarrey JR, Yang F, Page DC: An abundance of X-linked genes expressed in spermatogonia. Nat Genet 27:422–426 (2001).
- 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).
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