Evolutionary Variability of W-Linked Repetitive Content in Lacertid Lizards
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu srovnávací studie, časopisecké články, práce podpořená grantem
PubMed
32403257
PubMed Central
PMC7290949
DOI
10.3390/genes11050531
PII: genes11050531
Knihovny.cz E-zdroje
- Klíčová slova
- C-banding, FISH, GATA, evolution, heterochromatin, karyotype, microsatellites, sex chromosomes, telomeres,
- MeSH
- chromozomy genetika MeSH
- druhová specificita MeSH
- fylogeneze MeSH
- heterochromatin genetika ultrastruktura MeSH
- hybridizace in situ fluorescenční MeSH
- ještěři genetika MeSH
- karyotyp MeSH
- mikrosatelitní repetice genetika MeSH
- molekulární evoluce * MeSH
- nukleotidové motivy MeSH
- pohlavní chromozomy genetika MeSH
- pruhování chromozomů MeSH
- repetitivní sekvence nukleových kyselin MeSH
- telomery genetika MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- srovnávací studie MeSH
- Názvy látek
- heterochromatin MeSH
Lacertid lizards are a widely radiated group of squamate reptiles with long-term stable ZZ/ZW sex chromosomes. Despite their family-wide homology of Z-specific gene content, previous cytogenetic studies revealed significant variability in the size, morphology, and heterochromatin distribution of their W chromosome. However, there is little evidence about the accumulation and distribution of repetitive content on lacertid chromosomes, especially on their W chromosome. In order to expand our knowledge of the evolution of sex chromosome repetitive content, we examined the topology of telomeric and microsatellite motifs that tend to often accumulate on the sex chromosomes of reptiles in the karyotypes of 15 species of lacertids by fluorescence in situ hybridization (FISH). The topology of the above-mentioned motifs was compared to the pattern of heterochromatin distribution, as revealed by C-banding. Our results show that the topologies of the examined motifs on the W chromosome do not seem to follow a strong phylogenetic signal, indicating independent and species-specific accumulations. In addition, the degeneration of the W chromosome can also affect the Z chromosome and potentially also other parts of the genome. Our study provides solid evidence that the repetitive content of the degenerated sex chromosomes is one of the most evolutionary dynamic parts of the genome.
Department of Ecology Faculty of Science Charles University 12844 Prague Czech Republic
Department of Zoology and Marine Biology Faculty of Biology University of Athens 15784 Athens Greece
Zobrazit více v PubMed
Ohno S. Sex Chromosomes and Sex-Linked Genes. Springer; Berlin/Heidelberg, Germany: 1966. Monographs on Endocrinology.
Charlesworth D., Charlesworth B., Marais G. Steps in the evolution of heteromorphic sex chromosomes. Heredity. 2005;95:118–128. doi: 10.1038/sj.hdy.6800697. PubMed DOI
Vicoso B. Molecular and evolutionary dynamics of animal sex-chromosome turnover. Nat. Ecol. Evol. 2019;3:1632–1641. doi: 10.1038/s41559-019-1050-8. PubMed DOI
Kirkpatrick M. How and why chromosome inversions evolve. PLoS Biol. 2010;8:e1000501. doi: 10.1371/journal.pbio.1000501. PubMed DOI PMC
Bachtrog D., Kirkpatrick M., Mank J.E., McDaniel S.F., Pires J.C., Rice W., Valenzuela N. Are all sex chromosomes created equal? Trends Genet. 2011;27:350–357. doi: 10.1016/j.tig.2011.05.005. PubMed DOI
Pokorná M., Kratochvíl L. Phylogeny of sex-determining mechanisms in squamate reptiles: Are sex chromosomes an evolutionary trap? Zool. J. Linn. Soc. 2009;156:168–183. doi: 10.1111/j.1096-3642.2008.00481.x. DOI
Scherthan H., Cremer T., Arnason U., Weier H.-U., Lima-de-Faria A., Frönicke L. Comparative chromosome painting discloses homologous segments in distantly related mammals. Nat. Genet. 1994;6:342–347. doi: 10.1038/ng0494-342. PubMed DOI
Ferguson-Smith M.A., Yang F., O’Brien P.C.M. Comparative mapping using chromosome sorting and painting. ILAR J. 1998;39:68–76. doi: 10.1093/ilar.39.2-3.68. PubMed DOI
Mank J.E., Ellegren H. Parallel divergence and degradation of the avian W sex chromosome. Trends Ecol. Evol. 2007;22:389–391. doi: 10.1016/j.tree.2007.05.003. PubMed DOI
Graphodatsky A.S., Trifonov V.A., Stanyon R. The genome diversity and karyotype evolution of mammals. Mol. Cytogenet. 2011;4:22. doi: 10.1186/1755-8166-4-22. PubMed DOI PMC
Rovatsos M., Pokorná M., Altmanová M., Kratochvíl L. Cretaceous park of sex determination: Sex chromosomes are conserved across iguanas. Biol. Lett. 2014;10:20131093. doi: 10.1098/rsbl.2013.1093. PubMed DOI PMC
Rovatsos M., Vukić J., Lymberakis P., Kratochvíl L. Evolutionary stability of sex chromosomes in snakes. Proc. R. Soc. B. 2015;282:20151992. doi: 10.1098/rspb.2015.1992. PubMed DOI PMC
Rovatsos M., Praschag P., Fritz U., Kratochvíl L. Stable Cretaceous sex chromosomes enable molecular sexing in softshell turtles (Testudines: Trionychidae) Sci. Rep. 2017;7:42150. doi: 10.1038/srep42150. PubMed DOI PMC
Rovatsos M., Farkačová K., Altmanová M., Johnson Pokorná M., Kratochvíl L. The rise and fall of differentiated sex chromosomes in geckos. Mol. Ecol. 2019;28:3042–3052. doi: 10.1111/mec.15126. PubMed DOI
Rovatsos M., Rehák I., Velenský P., Kratochvíl L. Shared ancient sex chromosomes in varanids, beaded lizards, and alligator lizards. Mol. Biol. Evol. 2019;36:1113–1120. doi: 10.1093/molbev/msz024. PubMed DOI
Rovatsos M., Vukić J., Mrugała A., Suwala G., Lymberakis P., Kratochvíl L. Little evidence for switches to environmental sex determination and turnover of sex chromosomes in lacertid lizards. Sci. Rep. 2019;9:7832. doi: 10.1038/s41598-019-44192-5. PubMed DOI PMC
Altmanová M., Rovatsos M., Johnson Pokorná M., Veselý M., Wagner F., Kratochvíl L. All iguana families with the exception of basilisks share sex chromosomes. Zoology. 2018;126:98–102. doi: 10.1016/j.zool.2017.11.007. PubMed DOI
Xu L., Auer G., Peona V., Suh A., Deng Y., Feng S., Zhang G., Blom M.P.K., Christidis L., Prost S., et al. Dynamic evolutionary history and gene content of sex chromosomes across diverse songbirds. Nat. Ecol. Evol. 2019;3:834–844. doi: 10.1038/s41559-019-0850-1. PubMed DOI
Acosta M.J., Marchal J.A., Fernández-Espartero C., Romero-Fernández I., Rovatsos M.T., Giagia-Athanasopoulou E.B., Gornung E., Castiglia R., Sánchez A. Characterization of the satellite DNA Msat-160 from species of Terricola (Microtus) and Arvicola (Rodentia, Arvicolinae) Genetica. 2010;138:1085–1098. doi: 10.1007/s10709-010-9496-2. PubMed DOI
Hughes J.F., Skaletsky H., Pyntikova T., Graves T.A., van Daalen S.K.M., Minx P.J., Fulton R.S., McGrath S.D., Locke D.P., Friedman C., et al. Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature. 2010;463:536–539. doi: 10.1038/nature08700. PubMed DOI PMC
Cortez D., Marin R., Toledo-Flores D., Froidevaux L., Liechti A., Waters P.D., Grützner F., Kaessmann H. Origins and functional evolution of Y chromosomes across mammals. Nature. 2014;508:488–493. doi: 10.1038/nature13151. PubMed DOI
Gamble T., Geneva A.J., Glor R.E., Zarkower D. Anolis sex chromosomes are derived from a single ancestral pair. Evolution. 2014;68:1027–1041. doi: 10.1111/evo.12328. PubMed DOI PMC
Rovatsos M.T., Marchal J.A., Romero-Fernández I., Cano-Linares M., Fernández F.J., Giagia-Athanasopoulou E.B., Sánchez A. Molecular and physical characterization of the complex pericentromeric heterochromatin of the vole species Microtus thomasi. Cytogenet. Genome Res. 2014;144:131–141. doi: 10.1159/000368648. PubMed DOI
Soh Y.Q.S., Alföldi J., Pyntikova T., Brown L.G., Graves T., Minx P.J., Fulton R.S., Kremitzki C., Koutseva N., Mueller J.L., et al. Sequencing the mouse Y chromosome reveals convergent gene acquisition and amplification on both sex chromosomes. Cell. 2014;159:800–813. doi: 10.1016/j.cell.2014.09.052. PubMed DOI PMC
Zhou Q., Zhang J., Bachtrog D., An N., Huang Q., Jarvis E.D., Gilbert M.T.P., Zhang G. Complex evolutionary trajectories of sex chromosomes across bird taxa. Science. 2014;346:1246338. doi: 10.1126/science.1246338. PubMed DOI PMC
Altmanová M., Rovatsos M., Kratochvíl L., Johnson Pokorná M. Minute Y chromosomes and karyotype evolution in Madagascan iguanas (Squamata: Iguania: Opluridae) Biol. J. Linn. Soc. 2016;118:618–633. doi: 10.1111/bij.12751. DOI
Morgan A.P., Pardo-Manuel de Villena F. Sequence and structural diversity of mouse Y chromosomes. Mol. Biol. Evol. 2017;34:3186–3204. doi: 10.1093/molbev/msx250. PubMed DOI PMC
Augstenová B., Mazzoleni S., Kratochvíl L., Rovatsos M. Evolutionary dynamics of the W chromosome in caenophidian snakes. Genes. 2018;9:5. doi: 10.3390/genes9010005. PubMed DOI PMC
Iannucci A., Altmanová M., Ciofi C., Ferguson-Smith M., Milan M., Pereira J.C., Pether J., Rehák I., Rovatsos M., Stanyon R., et al. Conserved sex chromosomes and karyotype evolution in monitor lizards (Varanidae) Heredity. 2019;123:215–227. doi: 10.1038/s41437-018-0179-6. PubMed DOI PMC
Rovatsos M., Altmanová M., Augstenová B., Mazzoleni S., Velenský P., Kratochvíl L. ZZ/ZW sex determination with multiple neo-sex chromosomes is common in Madagascan chameleons of the genus Furcifer (Reptilia: Chamaeleonidae) Genes. 2019;10:1020. doi: 10.3390/genes10121020. PubMed DOI PMC
Deakin J.E., Potter S., O’Neill R., Ruiz-Herrera A., Cioffi M.B., Eldridge M.D.B., Fukui K., Marshall Graves J.A., Griffin D., Grutzner F., et al. Chromosomics: Bridging the gap between genomes and chromosomes. Genes. 2019;10:627. doi: 10.3390/genes10080627. PubMed DOI PMC
Ezaz T., Deakin J.E. Repetitive sequence and sex chromosome evolution in vertebrates. Adv. Evol. Biol. 2014;2014:104683. doi: 10.1155/2014/104683. DOI
Hobza R., Kubat Z., Cegan R., Jesionek W., Vyskot B., Kejnovsky E. Impact of repetitive DNA on sex chromosome evolution in plants. Chromosome Res. 2015;23:561–570. doi: 10.1007/s10577-015-9496-2. PubMed DOI
De Smet W.H. Description of the orcein stained karyotypes of 36 lizard species (Lacertilia, Reptilia) belonging to the families Teiidae, Scincidae, Lacertidae, Cordylidae and Varanidae (Autarchoglossa) Acta Zool. Pathol. Antverp. 1981;76:73–118.
Olmo E., Odierna G., Capriglione T. The karyology of Mediterranean lacertid lizards. In: Valakos E.D., Böhme W., Perez Mellado V., Maragou P., editors. Lacertids of the Mediterranean Region: A Biological Approach. Hellenic Zoological Society; Athens, Greece: 1993. pp. 61–84.
Odierna G., Caprigilone T., Kupriyanova L.A., Olmo E. Further data on sex chromosomes of Lacertidae and a hypothesis on their evolutionary trend. Amphib.-Reptil. 1993;14:1–11. doi: 10.1163/156853893X00147. DOI
Olmo E., Cobror O., Morescalchi A., Odierna G. Homomorphic sex chromosomes in the lacertid lizard Takydromus sexlineatus. Heredity. 1984;53:457–459. doi: 10.1038/hdy.1984.103. DOI
Pokorná M., Kratochvíl L., Kejnovský E. Microsatellite distribution on sex chromosomes at different stages of heteromorphism and heterochromatinization in two lizard species (Squamata: Eublepharidae: Coleonyx elegans and Lacertidae: Eremias velox) BMC Genet. 2011;12:90. doi: 10.1186/1471-2156-12-90. PubMed DOI PMC
Rojo Oróns V. Ph.D. Thesis. Universidade da Coruña; Coruña, Spain: 2015. Cytogenetic and Molecular Characterization of Lacertid Lizard Species from the Iberian Peninsula.
Matsubara K., Uno Y., Srikulnath K., Matsuda Y., Miller E., Olsson M. No interstitial telomeres on autosomes but remarkable amplification of telomeric repeats on the W sex chromosome in the sand lizard (Lacerta agilis) J. Hered. 2015;106:753–757. doi: 10.1093/jhered/esv083. PubMed DOI
Lisachov A.P., Borodin P.M. Microchromosome polymorphism in the sand lizard, Lacerta agilis Linnaeus, 1758 (Reptilia, Squamata) Comp. Cytogenet. 2016;10:387–399. doi: 10.3897/CompCytogen.v10i3.7655. PubMed DOI PMC
Giovannotti M., Nisi Cerioni P., Slimani T., Splendiani A., Paoletti A., Fawzi A., Olmo E., Caputo Barucchi V. Cytogenetic characterization of a population of Acanthodactylus lineomaculatus Duméril and Bibron, 1839 (Reptilia, Lacertidae), from Southwestern Morocco and insights into sex chromosome evolution. Cytogenet. Genome Res. 2017;153:86–95. doi: 10.1159/000484533. PubMed DOI
Giovannotti M., Nisi Cerioni P., Rojo V., Olmo E., Slimani T., Splendiani A., Caputo Barucchi V. Characterization of a satellite DNA in the genera Lacerta and Timon (Reptilia, Lacertidae) and its role in the differentiation of the W chromosome. J. Exp. Zool. 2018;330:83–95. doi: 10.1002/jez.b.22790. PubMed DOI
Lisachov A.P., Giovannotti M., Pereira J.C., Andreyushkova D.A., Romanenko S.A., Ferguson-Smith M.A., Borodin P.M., Trifonov V.A. Chromosome painting does not support a sex chromosome turnover in Lacerta agilis Linnaeus, 1758. Cytogenet. Genome Res. 2020;160:134–140. doi: 10.1159/000506321. PubMed DOI
Olmo E., Signorino G. Chromorep: A Reptile Chromosomes Database. [(accessed on 25 March 2020)];2005 Available online: http://chromorep.univpm.it/
Lisachov A.P., Galkina S.A., Saifitdinova A.F., Romanenko S.A., Andreyushkova D.A., Trifonov V.A., Borodin P.M. Identification of sex chromosomes in Eremias velox (Lacertidae, Reptilia) using lampbrush chromosome analysis. Comp. Cytogenet. 2019;13:121–132. doi: 10.3897/CompCytogen.v13i2.34116. PubMed DOI PMC
Andrade P., Pinho C., Pérez i de Lanuza G., Afonso S., Brejcha J., Rubin C.-J., Wallerman O., Pereira P., Sabatino S.J., Bellati A., et al. Regulatory changes in pterin and carotenoid genes underlie balanced color polymorphisms in the wall lizard. Proc. Natl. Acad. Sci. USA. 2019;116:5633–5642. doi: 10.1073/pnas.1820320116. PubMed DOI PMC
Vertebrate Genome Project Genome of Lacerta agilis. [(accessed on 25 March 2020)];2019 Available online: https://www.ncbi.nlm.nih.gov/genome/?term=txid80427.
Rovatsos M., Vukić J., Altmanová M., Johnson Pokorná M., Moravec J., Kratochvíl L. Conservation of sex chromosomes in lacertid lizards. Mol. Ecol. 2016;25:3120–3126. doi: 10.1111/mec.13635. PubMed DOI
Pokorná M., Rens W., Rovatsos M., Kratochvíl L. A ZZ/ZW sex chromosome system in the thick-tailed gecko (Underwoodisaurus milii; Squamata: Gekkota: Carphodactylidae), a member of the ancient gecko lineage. Cytogenet. Genome Res. 2014;142:190–196. doi: 10.1159/000358847. PubMed DOI
Sumner A.T. A simple technique for demonstrating centromeric heterochromatin. Exp. Cell Res. 1972;75:304–306. doi: 10.1016/0014-4827(72)90558-7. PubMed DOI
Rovatsos M., Johnson Pokorná M., Kratochvíl L. Differentiation of sex chromosomes and karyotype characterisation in the dragonsnake Xenodermus javanicus (Squamata: Xenodermatidae) Cytogenet. Genome Res. 2015;147:48–54. doi: 10.1159/000441646. PubMed DOI
Oguma K. Studies on the sauropsid chromosomes. II. The cytological evidence proving female heterogamety in the lizard (Lacerta vivipara) Arch. Biol. 1934;45:27–46.
Gorman G.C. New chromosome data for 12 species of lacertid lizards. J. Herpet. 1969;3:49–54. doi: 10.2307/1563223. DOI
Ivanov V.G., Fedorova T.A. Sex heteromorphism of chromosomes in Lacerta strigata. Tsitologiia. 1970;12:1582–1585. PubMed
Ivanov V., Bogdanov O., Anisimov E.Y., Fedorova T. Studies into karyotypes of 3 lizard species (Sauria, Scincidae, Lacertidae) Tsitologiia. 1973;15:1291–1296. PubMed
Cano J., Baez M., Lopez-Jurado L.F., Ortega G. Karyotype and chromosome structure in the lizard, Gallotia galloti in the Canary Islands. J. Herpetol. 1984;18:344–346. doi: 10.2307/1564092. DOI
Olmo E., Odierna G., Capriglione T. Evolution of sex-chromosomes in lacertid lizards. Chromosoma. 1987;96:33–38. doi: 10.1007/BF00285880. DOI
Pyron R., Burbrink F.T., Wiens J.J. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol. 2013;13:93. doi: 10.1186/1471-2148-13-93. PubMed DOI PMC
Garcia-Porta J., Irisarri I., Kirchner M., Rodríguez A., Kirchhof S., Brown J.L., MacLeod A., Turner A.P., Ahmadzadeh F., Albaladejo G., et al. Environmental temperatures shape thermal physiology as well as diversification and genome-wide substitution rates in lizards. Nat. Commun. 2019;10:4077. doi: 10.1038/s41467-019-11943-x. PubMed DOI PMC
Rutkowska J., Lagisz M., Nakagawa S. The long and the short of avian W chromosomes: No evidence for gradual W shortening. Biol. Lett. 2012;8:636–638. doi: 10.1098/rsbl.2012.0083. PubMed DOI PMC
Matsubara K., Sarre S.D., Georges A., Matsuda Y., Marshall Graves J.A., Ezaz T. Highly differentiated ZW sex microchromosomes in the Australian Varanus species evolved through rapid amplification of repetitive sequences. PLoS ONE. 2014;9:e95226. doi: 10.1371/journal.pone.0095226. PubMed DOI PMC
Oguiura N., Ferrarezzi H., Batistic R.F. Cytogenetics and molecular data in snakes: A phylogenetic approach. Cytogenet. Genome Res. 2009;127:128–142. doi: 10.1159/000295789. PubMed DOI
Rovatsos M., Vukić J., Kratochvíl L. Mammalian X homolog acts as sex chromosome in lacertid lizards. Heredity. 2016;117:8–13. doi: 10.1038/hdy.2016.18. PubMed DOI PMC
Kejnovsky E., Kubat Z., Hobza R., Lengerova M., Sato S., Tabata S., Fukui K., Matsunaga S., Vyskot B. Accumulation of chloroplast DNA sequences on the Y chromosome of Silene latifolia. Genetica. 2006;128:167–175. doi: 10.1007/s10709-005-5701-0. PubMed DOI
Schartl M., Schmid M., Nanda I. Dynamics of vertebrate sex chromosome evolution: From equal size to giants and dwarfs. Chromosoma. 2016;125:553–571. doi: 10.1007/s00412-015-0569-y. PubMed DOI
Matsubara K., O’Meally D., Azad B., Georges A., Sarre S.D., Graves J.A.M., Matsuda Y., Ezaz T. Amplification of microsatellite repeat motifs is associated with the evolutionary differentiation and heterochromatinization of sex chromosomes in Sauropsida. Chromosoma. 2016;125:111–123. doi: 10.1007/s00412-015-0531-z. PubMed DOI
Singh L., Purdom I.F., Jones K.W. Satellite DNA and evolution of sex chromosomes. Chromosoma. 1976;59:43–62. doi: 10.1007/BF00327708. PubMed DOI
Singh L., Purdom I.F., Jones K.W. Sex chromosome associated satellite DNA: Evolution and conservation. Chromosoma. 1980;79:137–157. doi: 10.1007/BF01175181. PubMed DOI
Rovatsos M., Altmanová M., Johnson Pokorná M., Augstenová B., Kratochvíl L. Cytogenetics of the Javan file snake (Acrochordus javanicus) and the evolution of snake sex chromosomes. J. Zool. Syst. Evol. Res. 2018;56:117–125. doi: 10.1111/jzs.12180. DOI
Johnson Pokorná M., Altmanová M., Rovatsos M., Velenský P., Vodička R., Rehák I., Kratochvíl L. First description of the karyotype and sex chromosomes in the Komodo dragon (Varanus komodoensis) Cytogenet. Genome Res. 2016;148:284–291. doi: 10.1159/000447340. PubMed DOI
Matsubara K., Tarui H., Toriba M., Yamada K., Nishida-Umehara C., Agata K., Matsuda Y. 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. 2006;103:18190–18195. doi: 10.1073/pnas.0605274103. PubMed DOI PMC
Rovatsos M., Kratochvíl L., Altmanová M., Johnson Pokorná M. Interstitial telomeric motifs in squamate reptiles: When the exceptions outnumber the rule. PLoS ONE. 2015;10:e0134985. doi: 10.1371/journal.pone.0134985. PubMed DOI PMC
Rykena S., Nettmann H.K. The karyotype of Lacerta princeps kurdistanica and its meaning in phylogeny. In: Roček Z., editor. Studies in Herpetology. Prague, Czech Republic: 1986. [(accessed on 8 May 2020)]. pp. 193–196. Available online: https://www.lacerta.de/AF/Bibliografie/BIB_4026.pdf.
Odierna G., Olmo E., Capriglione T., Caputo V. Karyological differences between Lacerta lepida and Lacerta pater. J. Herpet. 1990;24:97–99. doi: 10.2307/1564300. DOI
Ruiz-Herrera A., Nergadze S.G., Santagostino M., Giulotto E. Telomeric repeats far from the ends: Mechanisms of origin and role in evolution. Cytogenet. Genome Res. 2008;122:219–228. doi: 10.1159/000167807. PubMed DOI
Schmid M., Steinlein C., Reiter A.M., Rovatsos M., Altmanová M., Mazzoleni S., Johnson Pokorná M., Kratochvíl L. 5-Methylcytosine-rich heterochromatin in reptiles. Cytogenet. Genome Res. 2019;157:53–64. doi: 10.1159/000495893. PubMed DOI
Cytogenetic Analysis of Satellitome of Madagascar Leaf-Tailed Geckos
Sex chromosome evolution among amniotes: is the origin of sex chromosomes non-random?
Cytogenetic Evidence for Sex Chromosomes and Karyotype Evolution in Anguimorphan Lizards