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PLoS One
2017 Jan 01;125:e0177087. doi: 10.1371/journal.pone.0177087.
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Chromosome divergence during evolution of the tetraploid clawed frogs, Xenopus mellotropicalis and Xenopus epitropicalis as revealed by Zoo-FISH.
Knytl M
,
Smolík O
,
Kubíčková S
,
Tlapáková T
,
Evans BJ
,
Krylov V
.
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Whole genome duplication (WGD) generates new species and genomic redundancy. In African clawed frogs of the genus Xenopus, this phenomenon has been especially important in that (i) all but one extant species are polyploid and (ii) whole genome sequences of some species provide an evidence for genomic rearrangements prior to or after WGD. Within Xenopus in the subgenus Silurana, at least one allotetraploidization event gave rise to three extant tetraploid (2n = 4x = 40) species-Xenopus mellotropicalis, X. epitropicalis, and X. calcaratus-but it is not yet clear the degree to which these tetraploid genomes experienced rearrangements prior to or after allotetraploidization. To explore genome evolution during diversification of these species, we performed cytogenetic analyses of X. mellotropicalis, including assessment of the localization of nucleolar organizer region, chromosome banding, and determination of the p/q arm ratios for each chromosome pair. We compared these data to a previously characterized karyotype of X. epitropicalis. Morphometric, C-banding and Zoo-FISH data support a previously hypothesized common allotetraploid predecessor of these species. Zoo-FISH with whole chromosome painting (WCP) probes derived from the closely related diploid species X. tropicalis confirmed the existence of ten chromosomal quartets in X. mellotropicalis somatic cells, as expected by its ploidy level and tetraploid ancestry. The p/q arm ratio of chromosome 2a was found to be substantially different between X. mellotropicalis (0.81) and X. epitropicalis (0.67), but no substantial difference between these two species was detected in this ratio for the homoeologous chromosome pair 2b, or for other chromosome pairs. Additionally, we identified variation between these two species in the locations of a heterochromatic block on chromosome pair 2a. These results are consistent with a dynamic history of genomic rearrangements before and/or after genome duplication, a surprising finding given the otherwise relatively conserved genomic structure of most frogs.
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28545147
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Fig 2. Double colour 5S and 28S rDNA FISH on X. tropicalis and X. mellotropicalis chromosomes.
DAPI counter-stained metaphase spreads showed all (A) 20 chromosomes (B&W) in X. tropicalis and/or (D) 40 chromosomes in X. mellotropicalis. 28S rDNA amplicon labelled by Digoxigenin-11-dUTP (green) stained (B) XTR 7 secondary constriction and telomeres of XTR 6, 7 and 9 and/or (E) XME 7a secondary constriction and telomeres of XME 4a and 5b. 5S rDNA amplicon labelled by Biotin-16-dUTP (red) revealed positive signals on telomeric segments of (C) XTR 2, 3, 4, 5, 6, 7, 8 and 9 and/or (F) XME 4a, 5b and 8b. Arrows show NORs situated on secondary constrictions of (B) XTR 7 and (E) XME 7a. Scale bar represents 10 μm.
https://doi.org/10.1371/journal.pone.0177087.g002
Fig 3. Painting FISH with X. tropicalis WCP probes.
White arrows indicate staining of whole chromosome pairs using WCP probes derived from (A) XTR 1, (B) XTR 2, (C) XTR 3, (D) XTR 4, (E) XTR 5, (F) XTR 6, (G) XTR 7, (H) XTR 8, (I) XTR 9, and (J) XTR 10. In addition to red-stained homologous chromosome pairs, some WCP probes also had additional signal on telomeres and centromeres, which presumably is caused by high abundance of repetitive sequences. Scale bar represents 10 μm.
https://doi.org/10.1371/journal.pone.0177087.g003
Fig 4. Zoo-FISH on X. mellotropicalis chromosomes using X. tropicalis WCP probes.
XTR WCP probes stained the appropriate chromosomal quartets. (A) XTR 1 –XME 1a and 1b, (B) XTR 2 –XME 2a and 2b, (C) XTR 3 –XME 3a and 3b, (D) XTR 4 –XME 4a and 4b, (E) XTR 5 –XME 5a and 5b, (F) XTR 6 –XME 6a and 6b, (G) XTR 7 –XME 7a and 7b, (H) XTR 8 –XME 8a and 8b, (I) XTR 9 –XME 9a and 9b and (J) XTR 10 –XME 10a and 10b. White arrows show labelled chromosomal quartets. In (I) yellow arrows highlight the additional signals on XME 2a chromosome pair after hybridization with XTR 9 WCP. Gray arrows indicate the residue of constitutive heterochromatin in XME 9b. Scale bar represents 10 μm.
https://doi.org/10.1371/journal.pone.0177087.g004
Fig 5. Potential evolutionary scenarios forming X. mellotropicalis and X. epitropicalis karyotypes based on a common allotetraploid ancestor.
At least two evolutionary scenarios could form the allotetraploid species with the observed differences in the chromosomal locations of constitutive heterochromatic blocks. Scenario A indicates the translocation of a complete constitutive heterochromatic block from chromosome 9 to 2, and scenario B indicates the translocation of an incomplete constitutive heterochromatic block from chromosome 9 to 2. In (A), an ancestor of both allotetraploid species carried heterochromatic blocks on chromosomes 2a and 9b. In (B), genomic rearrangement produced a karyotype with the complete heterochromatic block on chromosomes 2a and 9b and a partial one on chromosome 9a. Sequence similarity of heterochromatic blocks from different chromosomes then facilitated a second incomplete (A) or complete (B) insertion of a heterochromatic block from chromosome 9b to 2a, which gave rise to the X. mellotropicalis karyotype. A residual hetrochromatic block on X. mellotropicalis chromosomes 9 was revealed by Zoo-FISH and is thus located either on chromosome 9b (A) or chromosome 9a (B). The formation of the X. epitropicalis karyotype from an allotetraploid ancestral species could have occurred via complete non-reciprocal recombination of a heterochromatic block between chromosomes 9a (or 9b) and 2a followed by an asymmetric pericentric inversion on chromosome 2a. Chromosome labelling “a”and “b”reflects the ancestral karyotypes (i.e. from which diploid ancestor a homoeologous pair is derived) and does not necessarily correspond with the chromosome names in the text which are based on the relative size of each homoeologous pair [23]. Chromosomal rearrangements between hypothetical or observed karyotypes of ancestral and extant species depicted out of the rectangular boxes are represented on haploid chromosomes.
https://doi.org/10.1371/journal.pone.0177087.g005
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