Highly differentiated ZW sex microchromosomes in the australian varanus species evolved through rapid amplification of repetitive sequences

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Matsubara, Kazumi ^a   Sarre, Stephen D ^a   Georges, Arthur ^a   Matsuda, Yoichi ^b   Marshall Graves, Jennifer A ^a   Ezaz, Tariq ^a  

^a UNIVERSITY OF CANBERRA   (Australia)

^b NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MICROSATELLITE DNA;

ANIMAL CELL; ARTICLE; C BANDING; CENTROMERE; CLADISTICS; COMPARATIVE GENOMIC HYBRIDIZATION; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE AMPLIFICATION; GENE MAPPING; GENE SEQUENCE; GENETIC VARIABILITY; KARYOTYPE; LIZARD; MALE; MICROCHROMOSOME; NONHUMAN; PHYLOGENY; PROTEIN MOTIF; REPETITIVE SEQUENCE; SEX CHROMOSOME; SPECIES COMPARISON; VARANUS; VARANUS ACANTHURUS; VARANUS GOULDII; VARANUS ROSENBERGI; ANIMAL; AUSTRALIA; GENETICS; IMMUNOLOGY; MOLECULAR EVOLUTION; NUCLEOTIDE REPEAT;

ANIMALS; AUSTRALIA; EVOLUTION, MOLECULAR; FEMALE; GENE AMPLIFICATION; LIZARDS; MALE; REPETITIVE SEQUENCES, NUCLEIC ACID; SEX CHROMOSOMES;

EID: 84899682487     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095226     Document Type: Article

References (35)

1. Janzen FJ, Krenz JG (2004) Phylogenetics: Which was first, TSD or GSD? In: Valenzuela N, Lance VA, editors. Temperature dependent sex determination in vertebrates. Washington: Smithsonian Institution Scholarly Press. 121-130.
2. Organ CL, Janes DE (2008) Evolution of sex chromosomes in Sauropsida. Integr Comp Biol 48: 512-519.
3. Pokorna M, Kratochvil L (2009) Phylogeny of sex-determining mechanisms in squamate reptiles: Are sex chromosomes an evolutionary trap? Zool J Linn Soc 156: 168-183.
4. Sarre SD, Ezaz T, Georges A (2011) Transitions between sex-determining systems in reptiles and amphibians. Annu Rev Genomics Hum Genet 12: 391- 406.
5. Sarre SD, Georges A, Quinn A (2004) The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. Bioessays 26: 639-645. (Pubitemid 38758341)
6. Ezaz T, Sarre SD, O'Meally D, Graves JAM, Georges A (2009) Sex chromosome evolution in lizards: independent origins and rapid transitions. Cytogenet Genome Res 127: 249-260.
7. Ezaz T, Stiglec R, Veyrunes F, Graves JAM (2006) Relationships between vertebrate ZW and XY sex chromosome systems. Curr Biol 16: 736-743.
8. Moritz C (1984) The evolution of a highly variable sex chromosome in Gehyra purpurascens (Gekkonidae). Chromosoma 90: 111-119. (Pubitemid 14034540)
9. Matsubara K, Knopp T, Sarre SD, Georges A, Ezaz T (2013) Karyotypic analysis and FISH mapping of microsatellite motifs reveal highly differentiated XX/XY sex chromosomes in the pink-tailed worm-lizard (Aprasia parapulchella, Pygopodidae, Squamata). Mol Cytogenet 6: 60.
10. Matsubara K, Tarui H, Toriba M, Yamada K, Nishida-Umehara C, et al. (2006) 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. (Pubitemid 44871634)
11. Vicoso B, Emerson JJ, Zektser Y, Mahajan S, Bachtrog D (2013) Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol 11: e1001643.
12. Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95: 118-128. (Pubitemid 41133194)
13. Uetz P, Hosek J (2013) The Reptile Database. Available: http://www.reptiledatabase.org.
14. Fuller S, Baverstock P, King D (1998) Biogeographic origins of goannas (Varanidae): A molecular perspective. Mol Phylogenet Evol 9: 294-307. (Pubitemid 128349939)
15. Ast JC (2001) Mitochondrial DNA evidence and evolution in Varanoidea (Squamata). Cladistics 17: 211-226. (Pubitemid 34175738)
16. Fitch AJ, Goodman AE, Donnellan SC (2006) A molecular phylogeny of the Australian monitor lizards (Squamata:Varanidae) inferred from mitochondrial DNA sequences. Australian Journal of Zoology 54: 253-269. (Pubitemid 44221775)
17. Amer SA, Kumazawa Y (2008) Timing of a mtDNA gene rearrangement and intercontinental dispersal of varanid lizards. Genes Genet Syst 83: 275-280.
18. Vidal N, Marin J, Sassi J, Battistuzzi FU, Donnellan S, et al. (2012) Molecular evidence for an Asian origin of monitor lizards followed by Tertiary dispersals to Africa and Australasia. Biol Lett 8: 853-855.
19. King M, King D (1975) Chromosomal evolution in the lizard genus Varanus (Reptilia). Aust J BioI Sci 28: 89-108.
20. King M, Mengden GA, King D (1982) A pericentric-inversion polymorphism and a ZZ/ZW sex-chromosome system in Varanus acanthurus Boulenger analyzed by G- And C-banding and Ag staining. Gertetica 58: 39-45.
21. Olmo E, Signorino GG (2005) Chromorep: A reptile chromosomes database. Available: http://chromorep.univpm.it/.
22. Cogger HG (1992) Reptiles and Amphibians of Australia. 5th ed. Chatswood: Reed International Books.
23. Ezaz T, O'Meally D, Quinn AE, Sarre SD, Georges A, et al. (2008) A simple non-invasive protocol to establish primary cell lines from tail and toe explants for cytogenetic studies in Australian dragon lizards (Squamata: Agamidae). Cytotechnology 58: 135-139.
24. Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75: 304-306.
25. Ezaz T, Quinn AE, Miura I, Sarre SD, Georges A, et al. (2005) The dragon lizard Pogona vitticeps has ZZ/ZW micro-sex chromosomes. Chromosome Res 13: 763-776. (Pubitemid 41768767)
26. Srikulnath K, Uno Y, Nishida C, Matsuda Y (2013) Karyotype evolution in monitor lizards: cross-species chromosome mapping of cDNA reveals highly conserved synteny and gene order in the Toxicofera clade. Chromosome Res 21: 805-819.
27. Viets BE, Ewert MA, Talent LG, Nelson CE (1994) Sex-determining mechanisms in squamate reptiles. J Exp Zool 270: 45-56.
28. Nanda I, Feichtinger W, Schmid M, Schröder JH, Zischler H, et al. (1990) Simple repetitive sequences are associated with differentiation of the sex chromosomes in the guppy fish. J Mol Evo 30: 456-462. (Pubitemid 20167651)
29. Kraemer C, Schmidt ER (1993) The sex determining region of Chironomus thummi is associated with highly repetitive DNA and transposable elements. Chromosoma 102: 553-562. (Pubitemid 23290834)
30. Liu Z, Moore PH, Ma H, Ackerman CM, Ragiba M, et al. (2004) A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427: 348-352. (Pubitemid 38133661)
31. Hobza R, Lengerova M, Svoboda J, Kubekova H, Kejnovsky E, et al. (2006) An accumulation of tandem DNA repeats on the Y chromosome in Silene latifolia during early stages of sex chromosome evolution. Chromosoma 115: 376-382. (Pubitemid 44288796)
32. Kawai A, Nishida-Umehara C, Ishijima J, Tsuda Y, Ota H, et al. (2007) Different origins of bird and reptile sex chromosomes inferred from comparative mapping of chicken Z-linked genes. Cytogenet Genome Res 117: 92-102. (Pubitemid 47202669)
33. O'Meally D, Patel HR, Stiglec R, Sarre SD, Georges A, et al. (2010) Nonhomologous sex chromosomes of birds and snakes share repetitive sequences. Chromosome Res 18: 787-800.
34. Cioffi MB, Camacho JPM, Bertollo LAC (2011) Repetitive DNAs and differentiation of sex chromosomes in neotropical fishes. Cytogenet Genome Res 132: 188-194.
35. Ezaz T, Azad B, O'Meally D, Young MJ, Matsubara K, et al. (2013) Sequence and gene content of a large fragment of a lizard sex chromosome and evaluation of candidate sex differentiating gene R-spondin 1. BMC Genomics 14: 899.