FISH mapping in Xenopus pygmaeus refines understanding of genomic rearrangements and reveals jumping NORs in African clawed frogs

. 2025 Mar 01 ; () : . [epub] 20250301

Status Publisher Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid40025138

Grantová podpora
186024 Grantová Agentura, Univerzita Karlova (Charles University Grant Agency)
186024 Grantová Agentura, Univerzita Karlova (Charles University Grant Agency)
54123 Grantová Agentura, Univerzita Karlova (Charles University Grant Agency)
DKRVO 2024-2028/6.I.a, National Museum of the Czech Republic 00023272 Ministerstvo Kultury (Ministry of Culture, Czech Republic)

Odkazy

PubMed 40025138
DOI 10.1038/s41437-025-00749-x
PII: 10.1038/s41437-025-00749-x
Knihovny.cz E-zdroje

Chromosomal rearrangements are fundamental evolutionary drivers leading to genomic diversification. African clawed frogs (genus Xenopus, subgenera Silurana and Xenopus) represent an allopolyploid model system with conserved chromosome numbers in species with the same ploidy within each subgenus. Two significant interchromosomal rearrangements have been identified: a translocation between chromosomes 9 and 2, found in subgenus Silurana, and a fusion between chromosomes 9 and 10, probably widespread in subgenus Xenopus. Here, we study the allotetraploid Xenopus pygmaeus (subgenus Xenopus) based on in-depth karyotype analysis using chromosome measurements and fluorescent in situ hybridization (FISH). We designed FISH probes for genes associated with translocation and fusion to test for the presence of the two main types of rearrangements. We also examined the locations of 5S and 28S ribosomal tandem repeats, with the former often associated with telomeric regions and the latter with nucleolus organizer regions (NORs). The translocation-associated gene mapping did not detect the translocation in X. pygmaeus, supporting the hypothesis that the translocation is restricted to Silurana, but instead identified a pericentromeric inversion on chromosome 2S. The fusion-associated gene mapping confirmed the fusion of chromosomes 9 and 10, supporting this fusion as an ancestral state in subgenus Xenopus. As expected, the 5S repeats were found predominantly in telomere regions on almost all chromosomes. The nucleolar 28S repeats were localized on chromosome 6S, a position previously found only in the closely related species X. parafraseri, whereas other, phylogenetically more distant species have NORs located on different chromosomes. We therefore hypothesize that a jumping mechanism could explain the relatively frequent changes in the location of NORs during Xenopus evolution.

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Badjedjea G, Masudi FM, Akaibe BD, Gvoždík V (2022) Amphibians of Kokolopori: an introduction to the amphibian fauna of the Central Congolian Lowland Forests, Democratic Republic of the Congo. Amphib Reptil Conserv 16:35–70

Bredeson JV, Mudd AB, Medina-Ruiz S, Mitros T, Smith OK, Miller KE et al. (2024) Conserved chromatin and repetitive patterns reveal slow genome evolution in frogs. Nat Commun 15:579 PubMed DOI PMC

Cannatella DC, de Sá RO (1993) Xenopus laevis as a model organism. Syst Biol 42:476–507 DOI

Castro J, Rodríguez S, Pardo BG, Sánchez L, Martínez P (2001) Population analysis of an unusual NOR-site polymorphism in brown trout (Salmo trutta L.). Heredity (Edinb) 86:291–302 PubMed DOI

Cauret CMS, Gansauge MT, Tupper AS, Furman BLS, Knytl M, Song XY et al. (2020) Developmental systems drift and the drivers of sex chromosome evolution. Mol Biol Evol 37:799–810 PubMed DOI

Chain FJJ, Ilieva D, Evans BJ (2008) Duplicate gene evolution and expression in the wake of vertebrate allopolyploidization. BMC Evol Biol 8:43 PubMed DOI PMC

Chan TM, Man KF, Kwong S, Tang KS (2008) A jumping gene paradigm for evolutionary multiobjective optimization. IEEE Trans Evol Comput 12:143–159 DOI

Courtet M, Flajnik M, Du Pasquier L (2001) Major histocompatibility complex and immunoglobulin loci visualized by in situ hybridization on Xenopus chromosomes. Dev Comp Immunol 25:149–157 PubMed DOI

Dedukh D, Riumin S, Chmielewska M, Rozenblut-Kościsty B, Kolenda K, Kazmierczak M et al. (2020) Micronuclei in germ cells of hybrid frogs from Pelophylax esculentus complex contain gradually eliminated chromosomes. Sci Rep. 10:8720 PubMed DOI PMC

Dedukh D, Altmanova M, Klima J, Kratochvil L (2022) Premeiotic endoreplication is essential for obligate parthenogenesis in geckos. Dev 149:dev200345 DOI

Dias S, Souza RC, Vasconcelos EV, Vasconcelos S, da Silva Oliveira AR, do Vale Martins L et al. (2024) Cytomolecular diversity among Vigna Savi (Leguminosae) subgenera. Protoplasma 261:859–875 PubMed DOI

Dittrich C, Hoelzl F, Smith S, Fouilloux CA, Parker DJ, O'Connell LA et al. (2024) Genome assembly of the dyeing poison frog provides insights into the dynamics of transposable element and genome-size evolution. Genome Biol Evol 16:evae109 PubMed DOI PMC

Dobigny G, Ozouf-Costaz C, Bonillo C, Volobouev V (2002) “Ag-NORs” are not always true NORs: new evidence in mammals. Cytogenet Genome Res 98:75–77 PubMed DOI

Evans BJ, Kelley DB, Tinsley RC, Melnick DJ, Cannatella DC (2004) A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution. Mol Phylogenet Evol 33:197–213 PubMed DOI

Evans BJ, Kelley DB, Melnick DJ, Cannatella DC (2005) Evolution of RAG-1 in polyploid clawed frogs. Mol Biol Evol 22:1193–1207 PubMed DOI

Evans BJ, Carter TF, Greenbaum E, Gvoždík V, Kelley DB, McLaughlin PJ et al. (2015) Genetics, morphology, advertisement calls, and historical records distinguish six new polyploid species of African clawed frog (Xenopus, Pipidae) from West and Central Africa. PLoS One 10:e0142823 PubMed DOI PMC

Evans BJ, Mudd AB, Bredeson JV, Furman BLS, Wasonga DV, Lyons JB et al. (2022) New insights into Xenopus sex chromosome genomics from the Marsabit clawed frog X. borealis. J Evol Biol 35:1777–1790 PubMed DOI PMC

Evans BJ, Gvoždík V, Knytl M, Cauret CMS, Herrel A, Greenbaum E et al. (2024) Rapid sex chromosome turnover in African Clawed Frogs (Xenopus) and the origins of new sex chromosomes. Mol Biol Evol 41::msae234 PubMed DOI

Feng YJ, Blackburn DC, Liang D, Hillis DM, Wake DB, Cannatella DC et al. (2017) Phylogenomics reveals rapid, simultaneous diversification of three major clades of Gondwanan frogs at the Cretaceous-Paleogene boundary. Proc Natl Acad Sci USA 114:E5864–E5870 PubMed DOI PMC

Fornaini NR, Bergelová B, Gvoždík V, Černohorská H, Krylov V, Kubíčková S et al. (2023) Consequences of polyploidy and divergence as revealed by cytogenetic mapping of tandem repeats in African clawed frogs (Xenopus, Pipidae). Eur J Wildl Res 69:81 PubMed DOI PMC

Fornaini NR, Černohorská H, do Vale Martins L, Knytl M (2024) Cytogenetic analysis of the fish genus Carassius indicates divergence, fission, and segmental duplication as drivers of tandem repeat and microchromosome evolution. Genome Biol Evol 16:evae028 PubMed DOI PMC

Furman BLS, Cauret CMS, Knytl M, Song XY, Premachandra T, Ofori-Boateng C et al. (2020) A frog with three sex chromosomes that co-mingle together in nature: Xenopus tropicalis has a degenerate W and a Y that evolved from a Z chromosome. PLoS Genet 16:e1009121 PubMed DOI PMC

Gvoždík V, Knytl M, Zassi-Boulou A-G, Fornaini NR, Bergelová B (2024) Tetraploidy in the Boettger’s dwarf clawed frog (Pipidae: Hymenochirus boettgeri) from the Congo indicates non-conspecificity with the captive population. Zool J Linn Soc 200:1034–1047 DOI

Hellsten U, Harland RM, Gilchrist MJ, Hendrix D, Jurka J, Kapitonov V et al. (2010) The genome of the Western clawed frog Xenopus tropicalis. Sci 328:633–636 DOI

Holtz MA, Racicot R, Preininger D, Stuckert AMM, Mangiamele LA (2023) Genome assembly of the foot-flagging frog, Staurois parvus: a resource for understanding mechanisms of behavior. G3 (Bethesda) 13:jkad193 PubMed DOI

Khokha MK, Krylov V, Reilly MJ, Gall JG, Bhattacharya D, Cheung CYJ et al. (2009) Rapid gynogenetic mapping of Xenopus tropicalis mutations to chromosomes. Dev Dyn 238:1398–1346 PubMed DOI PMC

Knytl M, Fornaini NR (2021) Measurement of chromosomal arms and FISH reveal complex genome architecture and standardized karyotype of model fish, genus Carassius. Cells 10:2343 PubMed DOI PMC

Knytl M, Smolík O, Kubíčková S, Tlapáková T, Evans BJ, Krylov V (2017) Chromosome divergence during evolution of the tetraploid clawed frogs, Xenopus mellotropicalis and Xenopus epitropicalis as revealed by Zoo-FISH. PLoS One 12:e0177087 PubMed DOI PMC

Knytl M, Tlapakova T, Vankova T, Krylov V (2018) Silurana chromosomal evolution: A new piece to the puzzle. Cytogenet Genome Res 156:223–228 PubMed DOI

Knytl M, Forsythe A, Kalous L (2022) A fish of multiple faces, which show us enigmatic and incredible phenomena in nature: biology and cytogenetics of the genus Carassius. Int J Mol Sci 23:8095 PubMed DOI PMC

Knytl M, Fornaini NR, Bergelová B, Gvoždík V, Černohorská H, Kubíčková S et al. (2023) Divergent subgenome evolution in the allotetraploid frog Xenopus calcaratus. Gene 851:146974 PubMed DOI

Knytl M, Bergelová B, Fornaini NR, Černohorská H, Kubíčková S, Tlapáková T et al. (2024) Cytogenomics uncovers novel rearrangements in frogs of the genus Xenopus. In TAGC24, March 6–10, 619–620 (Metro Washington, DC, 2024).

Kobel HR, Du Pasquier L, Tinsley RC (1981) Natural hybridization and gene introgression between Xenopus gilli and Xenopus laevis laevis (Anura: Pipidae). J Zool 194:317–322 DOI

Krylov V, Tlapakova T, Macha J (2007) Localization of the single copy gene Mdh2 on Xenopus tropicalis chromosomes by FISH-TSA. Cytogenet Genome Res 116:110–112 PubMed DOI

Krylov V, Kubickova S, Rubes J, Macha J, Tlapakova T, Seifertova E et al. (2010) Preparation of Xenopus tropicalis whole chromosome painting probes using laser microdissection and reconstruction of X. laevis tetraploid karyotype by Zoo-FISH. Chromosom Res 18:431–439 DOI

Kuhl H, Tan WH, Klopp C, Kleiner W, Koyun B, Ciorpac M et al. (2024) A candidate sex determination locus in amphibians which evolved by structural variation between X- and Y-chromosomes. Nat Commun 15:4781 PubMed DOI PMC

Lau Q, Igawa T, Ogino H, Katsura Y, Ikemura T, Satta Y (2020) Heterogeneity of synonymous substitution rates in the Xenopus frog genome. PLoS One 15:e0236515 PubMed DOI PMC

Levan A, Fredga K, Sandberg AA (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52:201–220 DOI

Matsuda Y, Uno Y, Kondo M, Gilchrist MJ, Zorn AM, Rokhsar DS et al. (2015) A new nomenclature of Xenopus laevis chromosomes based on the phylogenetic relationship to Silurana/Xenopus tropicalis. Cytogenet Genome Res 145:187–191 PubMed DOI

McClintock B (1950) The origin and behavior of mutable loci in maize. Proc Natl Acad Sci USA 36:344–355 PubMed DOI PMC

Mezzasalma M, Glaw F, Odierna G, Petraccioli A, Guarino FM (2015) Karyological analyses of Pseudhymenochirus merlini and Hymenochirus boettgeri provide new insights into the chromosome evolution in the anuran family Pipidae. Zool Anz - A J Comp Zool 258:47–53 DOI

Mezzasalma M, Brunelli E, Odierna G, Guarino FM (2023) Evolutionary and genomic diversity of true polyploidy in tetrapods. Animals 13:1033 PubMed DOI PMC

Mitros T, Lyons JB, Session AM, Jenkins J, Shu S, Kwon T et al. (2019) A chromosome-scale genome assembly and dense genetic map for Xenopus tropicalis. Dev Biol 452:8–20 PubMed DOI

Morescalchi A (1973) Amphibia. In Chiarelli AB & Capanna E (eds.) Cytotaxonomy Vertebr. Evol., Academic Press, London, pp 233–348

Naito E, Dewa K, Ymanouchi H, Kominami R (1992) Ribosomal ribonucleic acid (rRNA) gene typing for species identification. J Forensic Sci 37:396–403 PubMed DOI

Pardue ML (1974) Localization of repeated DNA sequences in Xenopus chromosomes. Cold Spring Harb Symp Quant Biol 38:475–482 PubMed DOI

Pardue ML, Brown DD, Birnstiel ML (1973) Location of the genes for 5S ribosomal RNA in Xenopus laevis. Chromosoma 42:191–203 PubMed DOI

R Core Team (2020) R: A language and environment for statistical computing, Vienna, Austria

Rebollo R, Horard B, Hubert B, Vieira C (2010) Jumping genes and epigenetics: Towards new species. Gene 454:1–7 PubMed DOI

Roco ÁS, Liehr T, Ruiz-García A, Guzmán K, Bullejos M (2021) Comparative distribution of repetitive sequences in the karyotypes of Xenopus tropicalis and Xenopus laevis (Anura, Pipidae). Genes (Basel) 12:617 PubMed DOI

Sánchez A, Jiménez R, Burgos M, Stitou S, Zurita F, Díaz de La Guardia R (1995) Cytogenetic peculiarities in the Algerian hedgehog: silver stains not only NORs but also heterochromatic blocks. Heredity (Edinb) 75:10–16 PubMed DOI

Schmid M, Steinlein C (2015) Chromosome banding in Amphibia. XXXII. The genus Xenopus (Anura, Pipidae). Cytogenet Genome Res 145:201–217 PubMed DOI

Schmid M, Evans BJ, Bogart JP (2015) Polyploidy in Amphibia. Cytogenet Genome Res 145:315–330 PubMed DOI

Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675 PubMed DOI PMC

Sember A, Pelikánová Š, de Bello Cioffi M, Šlechtová V, Hatanaka T, Do Doan H et al. (2020) Taxonomic diversity not associated with gross karyotype differentiation: the case of bighead carps, genus Hypophthalmichthys (Teleostei, Cypriniformes, Xenocyprididae). Genes (Basel) 11:479 PubMed DOI

Session AM, Uno Y, Kwon T, Chapman JA, Toyoda A, Takahashi S et al. (2016) Genome evolution in the allotetraploid frog Xenopus laevis. Nature 538:336–343 PubMed DOI PMC

da Silva DS, da Silva Filho HF, Cioffi MB, de Oliveira EHC, Gomes AJB (2021) Comparative cytogenetics in four Leptodactylus species (Amphibia, Anura, Leptodactylidae): Evidence of inner chromosomal diversification in highly conserved karyotypes. Cytogenet Genome Res 161:52–62 PubMed DOI

da Silva DS, de Sousa RPC, Vallinoto M, da Costa Lima MR, da Costa RA, de Oliveira Furo I et al. (2024) Comparative molecular and conventional cytogenetic analyses of three species of Rhinella (Anura; Bufonidae). PLoS One 19:e0308785 PubMed DOI PMC

Sinzelle L, Thuret R, Hwang HY, Herszberg B, Paillard E, Bronchain OJ et al. (2012) Characterization of a novel Xenopus tropicalis cell line as a model for in vitro studies. Genesis 50:316–324 PubMed DOI

Smith OK, Limouse C, Fryer KA, Teran NA, Sundararajan K, Heald R et al. (2021) Identification and characterization of centromeric sequences in Xenopus laevis. Genome Res 31:958–967 PubMed DOI PMC

Song XY, Furman BLS, Premachandra T, Knytl M, Cauret CMS, Wasonga DV et al. (2021) Sex chromosome degeneration, turnover, and sex-biased expression of sex-linked transcripts in African clawed frogs (Xenopus). Philos Trans R Soc Lond B Biol Sci 376:20200095 PubMed DOI PMC

Stöck M, Steinlein C, Lamatsch DK, Schartl M, Schmid M (2005) Multiple origins of tetraploid taxa in the Eurasian Bufo viridis subgroup. Genetica 124:255–272 PubMed DOI

Symonová R, Howell WM (2018) Vertebrate genome evolution in the light of fish cytogenomics and rDNAomics. Genes (Basel) 9:96 PubMed DOI

Tandon P, Conlon F, Furlow JD, Horb ME (2017) Expanding the genetic toolkit in Xenopus: Approaches and opportunities for human disease modeling. Dev Biol 426:325–335 PubMed DOI

Teixeira LSR, Seger KR, Targueta CP, Orrico VGD, Lourenço LB (2016) Comparative cytogenetics of tree frogs of the Dendropsophus marmoratus (Laurenti, 1768) group: Conserved karyotypes and interstitial telomeric sequences. Comp Cytogenet 10:753–767 PubMed DOI PMC

Tennessen JA, Wei N, Straub SCK, Govindarajulu R, Liston A, Ashman TL (2018) Repeated translocation of a gene cassette drives sex-chromosome turnover in strawberries. PLoS Biol 16:e2006062 PubMed DOI PMC

Tymowska J (1991) Polyploidy and cytogenetic variation in frogs of the genus Xenopus. In: Green DM & Sessions SK (eds.) Amphibian cytogenetics and evolution, Academic Press, San Diego, pp 259–297

Tymowska J, Kobel HR (1972) Karyotype analysis of Xenopus muelleri (Peters) and Xenopus laevis (Daudin), Pipidae. Cytogenetics 11:270–278 PubMed DOI

Unal Karakus S, Gaffaroğlu M, Karasu Ayata M, Knytl M (2024) A detailed karyological investigation of three endemic Cobitis Linnaeus, 1758 species (Teleostei, Cobitidae) in Anatolia, Türkiye. Cytogenet Genome Res 164:243–256 PubMed DOI

Uno Y, Nishida C, Takagi C, Ueno N, Matsuda Y (2013) Homoeologous chromosomes of Xenopus laevis are highly conserved after whole-genome duplication. Heredity (Edinb) 111:430–436 PubMed DOI

Wang W, Zhang X, Garcia S, Leitch AR, Kovarik A (2023) Intragenomic rDNA variation - the product of concerted evolution, mutation, or something in between? Heredity (Edinb) 131:179–188 PubMed DOI

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