Interstitial Telomeric Repeats Are Rare in Turtles

. 2020 Jun 16 ; 11 (6) : . [epub] 20200616

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32560114

Telomeres are nucleoprotein complexes protecting chromosome ends in most eukaryotic organisms. In addition to chromosome ends, telomeric-like motifs can be accumulated in centromeric, pericentromeric and intermediate (i.e., between centromeres and telomeres) positions as so-called interstitial telomeric repeats (ITRs). We mapped the distribution of (TTAGGG)n repeats in the karyotypes of 30 species from nine families of turtles using fluorescence in situ hybridization. All examined species showed the expected terminal topology of telomeric motifs at the edges of chromosomes. We detected ITRs in only five species from three families. Combining our and literature data, we inferred seven independent origins of ITRs among turtles. ITRs occurred in turtles in centromeric positions, often in several chromosomal pairs, in a given species. Their distribution does not correspond directly to interchromosomal rearrangements. Our findings support that centromeres and non-recombining parts of sex chromosomes are very dynamic genomic regions, even in turtles, a group generally thought to be slowly evolving. However, in contrast to squamate reptiles (lizards and snakes), where ITRs were found in more than half of the examined species, and birds, the presence of ITRs is generally rare in turtles, which agrees with the expected low rates of chromosomal rearrangements and rather slow karyotype evolution in this group.

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Blackburn E.H. Switching and signaling at the telomere. Cell. 2001;106:661–673. doi: 10.1016/S0092-8674(01)00492-5. PubMed DOI

Moyzis R.K., Buckingham J.M., Crams L.S., Dani M., Larry L., Jones M.D., Meyne J., Ratliff R.L., Wu J.R. A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc. Natl. Acad. Sci. USA. 1988;85:6622–6626. doi: 10.1073/pnas.85.18.6622. PubMed DOI PMC

Meyne J., Baker R.J., Hobart H.H., Hsu T.C., Ryder O.A., Ward O.G., Wiley J.E., Wurster-Hill D.H., Yates T.L., Moyzis R.K. Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma. 1990;99:3–10. doi: 10.1007/BF01737283. PubMed DOI

O’Sullivan R.J., Karlseder J. Telomeres: Protecting chromosomes against genome instability. Nat. Rev. Mol. Cell Biol. 2010;11:171–181. doi: 10.1038/nrm2848. PubMed DOI PMC

Chiodi I., Belgiovine C., Mondello C. Telomerase and telomeric proteins: A life beyond telomeres. In: Gagnon A.N., editor. Telomerase: Composition, Functions and Clinical Implications. Nova Science Publishers, Inc.; Hauppauge, NY, USA: 2010. pp. 35–58.

Zhao Z., Pan X., Liu L., Liu N. Telomere length maintenance, shortening, and lengthening. J. Cell. Physiol. 2014;229:1323–1329. doi: 10.1002/jcp.24537. PubMed DOI

Jafri M.A., Ansari S.A., Alqahtani M.H., Shay J.W. Roles of telomeres and telomerase in cancer, and advances in telomerase-targeted therapies. Genome Med. 2016;8:69. doi: 10.1186/s13073-016-0324-x. PubMed DOI PMC

Cong Y.S., Wright W.E., Shay J.W. Human telomerase and its regulation. Microbiol. Mol. Biol. Rev. 2002;66:407–425. doi: 10.1128/MMBR.66.3.407-425.2002. PubMed DOI PMC

Harley B.C., Futcher B.A., Greider W.C. Telomeres shorten during ageing of human fibroblasts. Nature. 1990;345:458–460. doi: 10.1038/345458a0. PubMed DOI

Hastie N.D., Dempster M., Dunlop M.G., Thompson A.M., Green D.K., Allshire R.C. Telomere reduction in human colorectal carcinoma and with ageing. Nature. 1990;346:866–868. doi: 10.1038/346866a0. PubMed DOI

Lindsey J., McGill N.I., Lindsey L.A., Green D.K., Cooke H.J. In vivo loss of telomeric repeats with age in humans. Mutat. Res. 1991;256:45–48. doi: 10.1016/0921-8734(91)90032-7. PubMed DOI

Hayashi M.T., Cesare A.J., Rivera T., Karlseder J. Cell death during crisis is mediated by mitotic telomere deprotection. Nature. 2015;522:492–496. doi: 10.1038/nature14513. PubMed DOI PMC

Bolzán A.D., Bianchi M.S. Telomeres, interstitial telomeric repeat sequences, and chromosomal aberrations. Mutat. Res. 2006;612:189–214. doi: 10.1016/j.mrrev.2005.12.003. PubMed DOI

Lin K.W., Yan J. Endings in the middle: Current knowledge of interstitial telomeric sequences. Mutat. Res. 2008;658:95–110. doi: 10.1016/j.mrrev.2007.08.006. PubMed 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

Azzalin C.M., Mucciolo E., Bertoni L., Giuliotto E. Fluorescence in situ hybridization with a synthetic (T2AG3)n polynucleotide detects several intrachromosomal telomere-like repeats on human chromosomes. Cytogenet. Genome Res. 1997;78:112–115. doi: 10.1159/000134640. PubMed DOI

Bolzán A.D. Interstitial telomeric sequences in vertebrate chromosomes: Origin, function, instability and evolution. Mutat. Res. 2017;773:51–65. doi: 10.1016/j.mrrev.2017.04.002. PubMed DOI

Santagostino M., Piras F.M., Cappelletti E., Del Giudice S., Semino O., Nergadze S.G., Giulotto E. Insertion of telomeric repeats in the human and horse genomes: An evolutionary perspective. Int. J. Mol. Sci. 2020;21:2838. doi: 10.3390/ijms21082838. PubMed DOI PMC

Azzalin C.M., Nergadze S.G., Giulotto E. Human intrachromosomal telomeric-like repeats: Sequence organization and mechanisms of origin. Chromosoma. 2001;110:75–82. doi: 10.1007/s004120100135. PubMed DOI

Faravelli M., Moralli D., Bertoni L., Attolini C., Chernova O., Raimondi E., Giulotto E. Two extended arrays of a satellite DNA sequence at the centromere and at the short-arm telomere of Chinese hamster chromosome. Cytogenet. Genome Res. 1998;83:281–286. doi: 10.1159/000015171. PubMed DOI

Faravelli M., Azzalin C.M., Bertoni L., Chernova O., Attolini C., Mondello C., Giulotto E. Molecular organization of internal telomeric sequences in Chinese hamster chromosomes. Gene. 2002;283:11–16. doi: 10.1016/S0378-1119(01)00877-0. PubMed DOI

Ruiz-Herrera A., García F., Azzalin C., Giulotto E., Egozcue J., Ponsà M., Garcia M. Distribution of intrachromosomal telomeric sequences (ITS) on Macaca fascicularis (Primates) chromosomes and their implication for chromosome evolution. Hum. Genet. 2002;110:578–586. doi: 10.1007/s00439-002-0730-6. PubMed DOI

Ruiz-Herrera A., García F., Giulotto E., Attolini C., Egozcue J., Ponsà M., Garcia M. Evolutionary breakpoints are co-localized with fragile sites and intrachromosomal telomeric sequences in primates. Cytogenet. Genome Res. 2005;108:234–247. doi: 10.1159/000080822. PubMed DOI

Nergadze S.G., Rocchi M., Azzalin C.M., Mondello C., Giulotto E. Insertion of telomeric repeats at intrachromosomal break sites during primate evolution. Genome Res. 2004;14:1704–1710. doi: 10.1101/gr.2778904. PubMed DOI PMC

Nergadze S.G., Santagostino M.A., Salzano A., Mondello C., Giulotto E. Contribution of telomerase RNA retrotranscription to DNA double-strand break repair during mammalian genome evolution. Genome Biol. 2007;8:R260. doi: 10.1186/gb-2007-8-12-r260. PubMed DOI PMC

Camats N., Ruiz-Herrera A., Parrilla J.J., Acien M., Payá P., Giulotto E., Egozcue J., García F., Garcia M. Genomic instability in rat: Breakpoints induced by ionising radiation and interstitial telomeric-like sequences. Mutat. Res. 2006;595:156–166. doi: 10.1016/j.mrfmmm.2005.11.002. PubMed DOI

Rovatsos M.T., Marchal J.A., Romero-Fernández I., Fernández F.J., Giagia-Athanosopoulou E.B., Sánchez A. Rapid, independent, and extensive amplification of telomeric repeats in pericentromeric regions in karyotypes of arvicoline rodents. Chromosome Res. 2011;19:869–882. doi: 10.1007/s10577-011-9242-3. PubMed DOI

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

Mazzoleni S., Schillaci O., Sineo L., Dumas F. Distribution of interstitial telomeric sequences in primates and the pygmy tree shrew (Scandentia) Cytogenet. Genome Res. 2017;151:141–150. doi: 10.1159/000467634. PubMed DOI

Milioto V., Vlah S., Mazzoleni S., Rovatsos M., Dumas F. Chromosomal localization of 18S-28S rDNA and (TTAGGG)n sequences in two South African dormice of the genus Graphiurus (Rodentia: Gliridae) Cytogenet. Genome Res. 2019;158:145–151. doi: 10.1159/000500985. PubMed DOI

Swier V.J., Anwarali Khan F.A., Baker R.J. Do time, heterochromatin, NORs, or chromosomal rearrangements correlate with distribution of interstitial telomeric repeats in Sigmodon (cotton rats)? J. Hered. 2012;103:493–502. doi: 10.1093/jhered/ess029. PubMed DOI

Nagamachi C.Y., Pieczarka J.C., O’Brien P.C.M., Pinto J.A., Malcher S.M., Pereira A.L., das Dores Rissino J., Mendes-Oliveira A.C., Rossi R.V., Ferguson-Smith M.A. FISH with whole chromosome and telomeric probes demonstrates huge karyotypic reorganization with ITS between two species of Oryzomyini (Sigmodontinae, Rodentia): Hylaeamys megacephalus probes on Cerradomys langguthi karyotype. Chromosome Res. 2013;21:107–119. doi: 10.1007/s10577-013-9341-4. PubMed DOI

Wiley J.E., Meyne J., Little M.L., Stout J.C. Interstitial hybridization sites of the (TTAGGG)n telomeric sequence on the chromosomes of some North American hylid frogs. Cytogenet. Cell Genet. 1992;61:55–57. doi: 10.1159/000133368. PubMed DOI

Park V.M., Gustashaw K.M., Wathen T.M. The presence of interstitial telomeric sequences in constitutional chromosome abnormalities. Am. J. Hum. Genet. 1992;50:914–923. PubMed PMC

Rossi E., Floridia G., Casali M., Danesino C., Chiumello G., Bernardi F., Magnani I., Papi L., Mura M., Zuffardi O. Types, stability, and phenotypic consequences of chromosome rearrangements leading to interstitial telomeric sequences. J. Med. Genet. 1993;30:926–931. doi: 10.1136/jmg.30.11.926. PubMed DOI PMC

Vermeesch J.R., Petit P., Speleman F., Devriendt K., Fryns J.P., Marynen P. Interstitial telomeric sequences at the junction site of a jumping translocation. Hum. Genet. 1997;99:735–737. doi: 10.1007/s004390050440. PubMed DOI

Melek M., Shippen D.E. Chromosome healing: Spontaneous and programmed de novo telomere formation by telomerase. BioEssays. 1996;18:301–308. doi: 10.1002/bies.950180408. PubMed DOI

Shay J.R., Wright W.E. Telomeres and telomerase: Three decades of progress. Nat. Rev. Genet. 2019;20:299–309. doi: 10.1038/s41576-019-0099-1. PubMed DOI

Nanda I., Schrama D., Feichtinger W., Haaf T., Schartl M., Schmid M. Distribution of telomeric (TTAGGG)n sequences in avian chromosomes. Chromosoma. 2002;111:215–227. doi: 10.1007/s00412-002-0206-4. PubMed DOI

Rovatsos M., 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

Ocalewicz K. Telomeres in fishes. Cytogenet. Genome Res. 2013;141:114–125. doi: 10.1159/000354278. PubMed DOI

Bruschi D.P., Rivera M., Lima A.P., Zúñiga A.B., Recco-Pimentel S.M. Interstitial telomeric sequences (ITS) and major rDNA mapping reveal insights into the karyotypical evolution of Neotropical leaf frogs species (Phyllomedusa, Hylidae, Anura) Mol. Cytogenet. 2014;7:22. doi: 10.1186/1755-8166-7-22. PubMed DOI PMC

Schmid M., Steinlein C. Chromosome Banding in Amphibia. XXXIV. Intrachromosomal telomeric DNA sequences in Anura. Cytogenet. Genome Res. 2016;148:211–226. doi: 10.1159/000446298. PubMed DOI

De Oliveira T.D., Kretschmer R., Bertocchi N.A., Degrandi T.M., de Oliveira E.H.C., Cioffi M.B., Garnero A.D.V., Gunski R.J. Genomic organization of repetitive DNA in woodpeckers (Aves, Piciformes): Implications for karyotype and ZW sex chromosome differentiation. PLoS ONE. 2017;12:e0169987. doi: 10.1371/journal.pone.0169987. PubMed DOI PMC

Srikulnath K., Azad B., Singchat W., Ezaz T. Distribution and amplification of interstitial telomeric sequences (ITSs) in Australian dragon lizards support frequent chromosome fusions in Iguania. PLoS ONE. 2019;14:e0212683. doi: 10.1371/journal.pone.0212683. PubMed DOI PMC

Zattera M.L., Lima L., Duarte I., de Sousa D.Y. Cytogenetics chromosome spreading of the (TTAGGG)n repeats in the Pipa carvalhoi Miranda-Ribeiro, 1937 (Pipidae, Anura) karyotype. Comp. Cytogenet. 2019;13:297–309. doi: 10.3897/CompCytogen.v13i3.35524. PubMed DOI PMC

Rovatsos M., Johnson Pokorná M., Altmanová M., Kratochvíl L. Female heterogamety in Madagascar chameleons (Squamata: Chamaeleonidae: Furcifer): Differentiation of sex and neo-sex chromosomes. Sci. Rep. 2015;5:13196. doi: 10.1038/srep13196. PubMed DOI PMC

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

Rovatsos M., Johnson Pokorná M., Altmanová M., Kratochvíl L. Mixed-up sex chromosomes: Identification of sex chromosomes in the X1X1X2X2/X1X2Y system of the legless lizards of the genus Lialis (Squamata: Gekkota: Pygopodidae) Cytogenet. Genome Res. 2016;149:282–289. doi: 10.1159/000450734. PubMed DOI

Rovatsos M., Altmanová M., Johnson Pokorná M., Velenský P., Sánchez Baca A., Kratochvíl L. Evolution of karyotypes in chameleons. Genes. 2017;8:382. doi: 10.3390/genes8120382. PubMed DOI PMC

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

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. Genes. 2019;10:1020. doi: 10.3390/genes10121020. PubMed DOI PMC

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

Srikulnath K., Uno Y., Nishida C., Ota H., Matsuda Y. Karyotype reorganization in the Hokou gecko (Gekko hokouensis, Gekkonidae): The process of microchromosome disappearance in Gekkota. PloS ONE. 2015;10:e0134829. doi: 10.1371/journal.pone.0134829. PubMed DOI PMC

Viana P.F., Ribeiro L.B., Souza G.M., Chalkidis H.D.M., Gross M.C., Feldberg E. Is the karyotype of neotropical boid snakes really conserved? Cytotaxonomy, chromosomal rearrangements and karyotype organization in the Boidae family. PLoS ONE. 2016;11:e0160274. doi: 10.1371/journal.pone.0160274. PubMed DOI PMC

Viana P.F., Ezaz T., Cioffi M.D.B., Almeida B.J., Feldberg E. Evolutionary insights of the ZW sex chromosomes in snakes: A new chapter added by the Amazonian puffing snakes of the genus Spilotes. Genes. 2019;10:288. doi: 10.3390/genes10040288. 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

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. B Mol. Dev. Evol. 2018;330:83–95. doi: 10.1002/jez.b.22790. PubMed DOI

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

Augstenová B., Mazzoleni S., Kostmann A., Altmanová M., Frynta D., Kratochvíl L., Rovatsos M. Cytogenetic analysis did not reveal differentiated sex chromosomes in ten species of boas and pythons (Reptilia: Serpentes) Genes. 2019;10:934. doi: 10.3390/genes10110934. PubMed DOI PMC

Singchat W., O’Connor R.E., Tawichasri P., Suntronpong A., Sillapaprayoon S., Suntrarachun S., Muangmai N., Baicharoen S., Peyachoknagul S., Chanhome L., et al. Chromosome map of the Siamese cobra: Did partial synteny of sex chromosomes in the amniote represent “a hypothetical ancestral super-sex chromosome” or random distribution? BMC Genom. 2018;19:939. doi: 10.1186/s12864-018-5293-6. PubMed DOI PMC

Da Silva M.J., de Araújo Vieira A.P., Galvão Cipriano F.M., dos Santos Cândido M.R., de Oliveira E.H.C., Gimenez Pinheiro T., da Silva E.L. The karyotype of Salvator merianae (Squamata, Teiidae): Analyses by classical and molecular cytogenetic techniques. Cytogenet. Genome Res. 2020;160:94–99. doi: 10.1159/000506140. PubMed DOI

Sidhom M., Said K., Chatti N., Guarino F.M., Odierna G., Petraccioli A., Picariello O., Mezzasalma M. Karyological characterization of the common chameleon (Chamaeleo chamaeleon) provides insights on the evolution and diversification of sex chromosomes in Chamaeleonidae. Zoology. 2020:125738. doi: 10.1016/j.zool.2019.125738. in press. PubMed DOI

Kawagoshi T., Nishida C., Ota H., Kumazawa Y., Endo H., Matsuda Y. Molecular structures of centromeric heterochromatin and karyotypic evolution in the Siamese crocodile (Crocodylus siamensis) (Crocodylidae, Crocodylia) Chromosome Res. 2008;16:1119–1132. doi: 10.1007/s10577-008-1263-1. PubMed DOI

Nishida C., Ishijima J., Kosaka A., Tanabe H., Habermann F.A., Griffin D.K., Matsuda Y. Characterization of chromosome structures of Falconinae (Falconidae, Falconiformes, Aves) by chromosome painting and delineation of chromosome rearrangements during their differentiation. Chromosome Res. 2008;16:171–181. doi: 10.1007/s10577-007-1210-6. PubMed DOI

Seibold-Torres C., Owens E., Chowdhary R., Ferguson-Smith M.A., Tizard I., Raudsepp T. Comparative cytogenetics of the Congo African grey parrot (Psittacus erithacus) Cytogenet. Genome Res. 2015;147:144–153. doi: 10.1159/000444136. PubMed DOI

Liangouzov I.A., Derjusheva S.E., Saifitdinova A.F., Malykh A.G., Gaginskaya E.R. Monomers of a satellite DNA sequence of chaffinch (Fringilla coelebs L., Aves: Passeriformes) contain short clusters of the TTAGGG repeat. Russ. J. Genet. 2002;38:1359–1364. doi: 10.1023/A:1021679520236. PubMed DOI

Derjusheva S., Kurganova A., Habermann F., Gaginskaya E. High chromosome conservation detected by comparative chromosome painting in chicken, pigeon and passerine birds. Chromosome Res. 2004;12:715–723. doi: 10.1023/B:CHRO.0000045779.50641.00. PubMed DOI

Uetz P., Freed P., Hošek J. The Reptile Database. [(accessed on 13 April 2020)]; Available online: http://www.reptile-database.org.

Vargas-Ramírez M., Caballero S., Morales-Betancourt M.A., Lasso C.A., Amaya L., Martínez J.G., das Neves Silvia Viana M., Vogt R.C., Farias I.P., Hrbek T., et al. Genomic analyses reveal two species of the matamata (Testudines: Chelidae: Chelus spp.) and clarify their phylogeography. Mol. Phylogenet. Evol. 2020;148:106823. PubMed

Martinez P.A., Boeris J.M., Sánchez J., Pastori M.C., Bolzán A.D., Ledesma M.A. Karyotypic characterization of Trachemys dorbigni (Testudines: Emydidae) and Chelonoidis (Geochelone) donosobarrosi (Testudines: Testudinidae), two species of cryptodiran turtles from Argentina. Genetica. 2009;137:277–283. doi: 10.1007/s10709-009-9377-8. PubMed DOI

Badenhorst D., Hillier L.D., Literman R., Montiel E.E., Radhakrishnan S., Shen Y., Minx P., Janes D.E., Warren W.C., Edwards S.V., et al. Physical mapping and refinement of the painted turtle genome (Chrysemys picta) inform amniote genome evolution and challenge turtle-bird chromosomal conservation. Genome Biol. Evol. 2013;7:2038–2050. doi: 10.1093/gbe/evv119. PubMed DOI PMC

Ventura K., Moreira C.N., Moretti R., Yonenaga-Yassuda Y., Rodrigues M.T. The lowest diploid number in Testudines: Banding patterns, telomeric and 45s rDNA FISH in Peltocephalus dumerilianus, 2n = 26 and FN = 52 (Pleurodira, Podocnemididae) Genet. Mol. Biol. 2014;37:61–63. doi: 10.1590/S1415-47572014000100011. PubMed DOI PMC

Sánchez J., Alcalde L., Bolzán A.D. First evidence of chromosomal variation within Chelonoidis chilensis (Testudines: Testudinidae) Herpetol. J. 2015;25:83–89.

Montiel E.E., Badenhorst D., Lee L.S., Literman R., Trifonov V., Valenzuela N. Cytogenetic insights into the evolution of chromosomes and sex determination reveal striking homology of turtle sex chromosomes to amphibian autosomes. Cytogenet. Genome Res. 2016;148:292–304. doi: 10.1159/000447478. PubMed DOI

Noronha R.C.R., Barros L.M.R., Araújo R.E.F., Marques D.F., Nagamachi C.Y., Martins C., Pieczarka J.C. New insights of karyoevolution in the Amazonian turtles Podocnemis expansa and Podocnemis unifilis (Testudines, Podocnemidae) Mol. Cytogenet. 2016;9:73. doi: 10.1186/s13039-016-0281-5. PubMed DOI PMC

Cavalcante M.G., Bastos C.E.M.C., Nagamachi C.Y., Pieczarka J.C., Vicari M.R., Noronha R.C.R. Physical mapping of repetitive DNA suggests 2n reduction in Amazon turtles Podocnemis (Testudines: Podocnemididae) PLoS ONE. 2018;13:e0197536. doi: 10.1371/journal.pone.0197536. PubMed DOI PMC

Iannucci A., Svartman M., Bellavita M., Chelazzi G., Stanyon R., Ciofi C. Insights into Emydid turtle cytogenetics: The European pond turtle as a model species. Cytogenet. Genome Res. 2019;157:166–171. doi: 10.1159/000495833. PubMed DOI

Mazzoleni S., Augstenová B., Clemente L., Auer M., Fritz U., Praschag P., Protiva T., Velenský P., Kratochvíl L., Rovatsos M. Turtles of the genera Geoemyda and Pangshura (Testudines: Geoemydidae) lack differentiated sex chromosomes: The end of a 40-year error cascade for Pangshura. PeerJ. 2019;7:e6241. doi: 10.7717/peerj.6241. PubMed DOI PMC

Mazzoleni S., Augstenová B., Clemente L., Auer M., Fritz U., Praschag P., Protiva T., Velenský P., Kratochvíl L., Rovatsos M. Sex is determined by XX/XY sex chromosomes in Australasian side-necked turtles (Testudines: Chelidae) Sci. Rep. 2020;10:4276. doi: 10.1038/s41598-020-61116-w. PubMed DOI PMC

Cavalcante M.G., Souza L.F., Vicari M.R., de Bastos C.E.M., de Sousa J.V., Nagamachi C.Y., Pieczarka J.C., Martins C., Noronha R.C.R. Molecular cytogenetics characterization of Rhinoclemmys punctularia (Testudines, Geoemydidae) and description of a Gypsy-H3 association in its genome. Gene. 2020;738:144477. doi: 10.1016/j.gene.2020.144477. PubMed DOI

Olmo E., Signorino G.G. Chromorep: A reptile chromosomes database. [(accessed on 14 April 2020)]; Available online: http://chromorep.univpm.it.

Bickham J.W. Two hundred million year old chromosomes: Deceleration of the rate of karyotypic evolution in turtles. Science. 1981;212:1291–1293. doi: 10.1126/science.212.4500.1291. PubMed DOI

Olmo E. Trends in the evolution of reptilian chromosomes. Integr. Comp. Biol. 2008;48:486–493. doi: 10.1093/icb/icn049. PubMed DOI

Fritz U., Guicking D., Auer M., Sommer R.S., Wink M., Hundsdörfer A.K. Diversity of the Southeast Asian leaf turtle genus Cyclemys: How many leaves on its tree of life? Zool. Scr. 2008;37:367–390. doi: 10.1111/j.1463-6409.2008.00332.x. DOI

Petzold A., Vargas-Ramírez M., Kehlmaier C., Vamberger M., Branch W.R., Du Preez L., Hofmeyr M.D., Schleicher A., Široký P., Fritz U. A revision of African helmeted terrapins (Testudines: Pelomedusidae: Pelomedusa), with descriptions of six new species. Zootaxa. 2014;3795:523–548. doi: 10.11646/zootaxa.3795.5.2. PubMed DOI

Ihlow F., Vamberger M., Flecks M., Hartmann T., Cota M., Makchai S., Meewattana P., Dawson J.E., Kheng L., Rödder D. Integrative taxonomy of Southeast Asian snail-eating turtles (Geoemydidae: Malayemys) reveals a new species and mitochondrial introgression. PLoS ONE. 2016;11:e0153108. doi: 10.1371/journal.pone.0153108. PubMed DOI PMC

Ijdo J.W., Wells R.A., Baldini A., Reeders S.T. Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res. 1991;19:4780. doi: 10.1093/nar/19.17.4780. PubMed DOI PMC

Pereira A.G., Sterli J., Moreira F.R.R., Schrago C.G. Multilocus phylogeny and statistical biogeography clarify the evolutionary history of major lineages of turtles. Mol. Phylogenet. Evol. 2017;113:59–66. doi: 10.1016/j.ympev.2017.05.008. PubMed DOI

Kehlmaier C., Zhang X., Georges A., Campbell P.D., Thomson S., Fritz U. Mitogenomics of historical type specimens of Australasian turtles: Clarification of taxonomic confusion and old mitochondrial introgression. Sci. Rep. 2019;9:5841. doi: 10.1038/s41598-019-42310-x. PubMed DOI PMC

Maddison W.P., Maddison D.R. Mesquite: A modular system for evolutionary analysis. Version 3.61. [(accessed on 15 March 2020)]; Available online: http://mesquiteproject.org.

Delany M.E., Krupkin A.B., Miller M.M. Organization of telomere sequences in birds: Evidence for arrays of extreme length and for in vivo shortening. Cytogenet. Cell Genet. 2000;90:139–145. doi: 10.1159/000015649. PubMed DOI

Raudsepp T., Houck M.L., O’Brien P.C., Ferguson-Smith M.A., Ryder O.A., Chowdhary B.P. Cytogenetic analysis of California condor (Gymnogyps californianus) chromosomes: Comparison with chicken (Gallus gallus) macrochromosomes. Cytogenet. Genome Res. 2002;98:54–60. doi: 10.1159/000068532. PubMed DOI

Swanberg S.E., Delany M.E. Telomeres in aging: Birds. In: Conn P.M., editor. Handbook of Models for Human Aging. Elsevier Academic Press; Cambridge, MA, USA: 2006. pp. 339–349.

Dos Santos M.S., Kretschmer R., Silva F.A.O., Ledesma M.A., O’Brien P.C.M., Ferguson-Smith M.A., Del Valle Garnero A., de Oliveira E.H.C., Gunski R.J. Intrachromosomal rearrangements in two representatives of the genus Saltator (Thraupidae, Passeriformes) and the occurrence of heteromorphic Z chromosomes. Genetica. 2015;143:535–543. doi: 10.1007/s10709-015-9851-4. PubMed DOI

Kretschmer R., Ferguson-Smith M.A., de Oliveira E.H.C. Karyotype evolution in birds: From conventional staining to chromosome painting. Genes. 2018;9:181. doi: 10.3390/genes9040181. PubMed DOI PMC

Johnson Pokorná M., Rovatsos M., Kratochvíl L. Sex chromosomes and karyotype of the (nearly) mythical creature, the Gila monster, Heloderma suspectum (Squamata: Helodermatidae) PLoS ONE. 2014;9:e104716. PubMed PMC

Stock A.D. Karyological relationships in turtles (Reptilia: Chelonia) Can. J. Genet. Cytol. 1972;14:859–868. doi: 10.1139/g72-105. PubMed DOI

Killebrew F.C. Mitotic chromosomes of turtles. III. The Kinosternidae. Herpetologica. 1975;31:398–403.

Rhodin A.G.J., Iverson J.B., Bour R., Fritz U., Georges A., Shaffer H.B. Turtles of the World: Annotated Checklist and Atlas of Taxonomy. Synon. Distrib. Conserv. Status. 2017;8:9–14.

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

Literman R., Radhakrishnan S., Tamplin J., Burke R., Dresser C., Valenzuela N. Development of sexing primers in Glyptemys insculpta and Apalone spinifera turtles uncovers an XX/XY sex-determining system in the critically-endangered bog turtle Glyptemys muhlenbergii. Conserv. Genet. Res. 2017;9:651–658. doi: 10.1007/s12686-017-0711-7. DOI

Bull J.J., Moon R.G., Legler J.M. Male heterogamety in kinosternid turtles (genus Staurotypus) Cytogenet. Genome Res. 1974;13:419–425. doi: 10.1159/000130295. PubMed DOI

Kawagoshi T., Uno Y., Nishida C., Matsuda Y. The Staurotypus turtles and Aves share the same origin of sex chromosomes but evolved different types of heterogametic sex determination. PLoS ONE. 2014;9:e105315. doi: 10.1371/journal.pone.0105315. PubMed DOI PMC

Kawagoshi T., Nishida C., Matsuda Y. The origin and differentiation process of X and Y chromosomes of the black marsh turtle (Siebenrockiella crassicollis, Geoemydidae, Testudines) Chromosome Res. 2012;20:95–110. doi: 10.1007/s10577-011-9267-7. PubMed DOI

Ohno S. Sex Chromosomes and Sex-Linked Genes. Volume 1 Springer; Berlin, Germany: 1967.

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

Cioffi M.B., Kejnovsky E., Bertollo L.A.C. The chromosomal distribution of microsatellite repeats in the genome of the wolf fish Hoplias malabaricus, focusing on the sex chromosomes. Cytogenet. Genome Res. 2011;132:289–296. doi: 10.1159/000322058. PubMed DOI

Matsubara K., Knopp T., Sarre S.D., Georges A., Ezaz T. 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. 2013;6:60. doi: 10.1186/1755-8166-6-60. PubMed DOI PMC

Scacchetti P.C., Utsunomia R., Pansonato-Alves J.C., da Costa Silva G.J., Vicari M.R., Artoni F.R., Oliveira C., Foresti F. Repetitive DNA sequences and evolution of ZZ/ZW sex chromosomes in Characidium (Teleostei: Characiformes) PLoS ONE. 2015;10:e0137231. doi: 10.1371/journal.pone.0137231. PubMed DOI PMC

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

Meles S., Adega F., Guedes-Pinto H., Chaves R. The karyotype and sex chromosomes of Praomys tullbergi (Muridae, Rodentia): A detailed characterization. Micron. 2008;39:559–568. doi: 10.1016/j.micron.2007.07.002. PubMed DOI

Cioffi M.B., Bertollo L.A.C. Initial steps in XY chromosome differentiation in Hoplias malabaricus and the origin of an X1X2Y sex chromosome system in this fish group. Heredity. 2010;105:554–561. doi: 10.1038/hdy.2010.18. PubMed DOI

Mank J.E. Small but mighty: The evolutionary dynamics of W and Y sex chromosomes. Chromosome Res. 2012;20:21–33. doi: 10.1007/s10577-011-9251-2. 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. Chromosomics: Bridging the gap between genomes and chromosomes. Genes. 2019;10:627. doi: 10.3390/genes10080627. PubMed DOI PMC

Birchler J.A., Presting G.G. Retrotransposon insertion targeting: A mechanism for homogenization of centromere sequences on nonhomologous chromosomes. Genes. Dev. 2012;26:638–640. doi: 10.1101/gad.191049.112. PubMed DOI PMC

Alföldi J., Di Palma F., Grabherr M., Williams C., Kong L., Mauceli E., Russell P., Lowe C.B., Glor R.E., Jaffe J.D. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature. 2011;477:587–591. doi: 10.1038/nature10390. PubMed DOI PMC

Hooper D.M., Price T.D. Chromosomal inversion differences correlate with range overlap in passerine birds. Nat. Ecol. Evol. 2017;1:1526–1534. doi: 10.1038/s41559-017-0284-6. PubMed DOI

Hooper D.M., Griffith S.C., Price T.D. Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone. Mol. Ecol. 2018;28:1246–1262. doi: 10.1111/mec.14874. PubMed DOI

Fuller Z.L., Leonard C.J., Young R.E., Schaeffer W., Phadnis N. Ancestral polymorphisms explain the role of chromosomal inversions in speciation. PLoS Genet. 2018;14:e1007526. doi: 10.1371/journal.pgen.1007526. PubMed DOI PMC

Kirkpatrick M., Barton N. Chromosome inversion, local adaptation and speciation. Genetics. 2006;173:419–434. doi: 10.1534/genetics.105.047985. PubMed DOI PMC

Wellenreuther M., Bernatchez L. Eco-evolutionary genomics of chromosomal inversions. Trends Ecol. Evol. 2018;33:427–440. doi: 10.1016/j.tree.2018.04.002. PubMed DOI

Avise J.C., Bowen B.W., Lamb T., Meylan A.B., Bermingham E. Mitochondrial DNA evolution at a turtle’s place: Evidence for low genetic variability and reduced microevolutionary rate in the Testudines. Mol. Biol. Evol. 1992;9:457–473. PubMed

Lourenço J.M., Glémin S., Chiari Y., Galtier N. The determinants of molecular substitution process in turtles. J. Evol. Biol. 2013;26:38–50. doi: 10.1111/jeb.12031. PubMed DOI

Shaffer B.H., Minx P., Warren D.E., Shedlock A.M., Thomson R.C., Valenzuela N., Abramyan J., Amemiya C.T., Badenhorst D., Biggar K.K. The western painted turtle genome, a model for evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biol. 2013;14:R28. doi: 10.1186/gb-2013-14-3-r28. PubMed DOI PMC

Fritz U. Schildkröten-Hybriden, 2. Halsberger-Schildkröten (Cryptodira) Herpetofauna. 1995;95:19–34.

Karl S.A., Bowen B.W., Avise J.C. Hybridization among the ancient mariners: Characterization of marine turtle hybrids with molecular genetic assays. J. Hered. 1995;86:262–268. doi: 10.1093/oxfordjournals.jhered.a111579. PubMed DOI

Parham J.F., Simison W.B., Kozak K.H., Feldman C.R., Shi H. New Chinese turtles: Endangered or invalid? A reassessment of two species using mitochondrial DNA, allozyme electrophoresis and known-locality specimens. Anim. Conserv. 2001;4:357–367. doi: 10.1017/S1367943001001421. DOI

Fritz U., Mendau D. Ein Gattungsbastard zweier südostasiatischer Schildkröten: Cuora amboinensis kamaroma Rummler & Fritz, 1991 x Mauremys annamensis (Siebenrock, 1903) Salamandra. 2002;38:129–134.

Seminoff J.A., Karl S.A., Schwartz T., Resendiz A. Hybridization of the green turtle (Chelonia mydas) and hawksbill turtle (Eretmochelys imbricata) in the Pacific Ocean: Indication of an absence of gender bias in the directionality of crosses. Bull. Mar. Sci. 2003;73:643–652.

James M.C., Martin K., Dutton P.H. Hybridization between a green turtle, Chelonia mydas, and loggerhead turtle, Caretta caretta, and the first record of a green turtle in Atlantic Canada. Can. Field-Nat. 2004;118:579–582. doi: 10.22621/cfn.v118i4.59. DOI

Lara-Ruiz P., Lopez G.G., Santos F.R., Soares L.S. Extensive hybridization in hawksbill turtles (Eretmochelys imbricata) nesting in Brazil revealed by mtDNA analyses. Conserv. Genet. 2006;7:773–781. doi: 10.1007/s10592-005-9102-9. DOI

Stuart B.L., Parham J.F. Recent hybrid origin of three rare Chinese turtles. Conserv. Genet. 2006;8:169–175. doi: 10.1007/s10592-006-9159-0. DOI

Lee Y., Lin J.W., Tseng S.P., Chen T.S., Lin S.M. Human disturbance as a possible cause of genetic introgression from exotic into native Mauremys turtles. Anim. Conserv. 2019;22:556–567. doi: 10.1111/acv.12494. DOI

Burgtorf C., Bünemann H. A telomere-like satellite (GGGTCAT)n comprises 4% of genomic DNA of Drosophila hydei and is located mainly in centromeric heterochromatin of all large acrocentric autosomes. Gene. 1993;137:287–291. doi: 10.1016/0378-1119(93)90022-U. PubMed DOI

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