Chromosome spreading of associated transposable elements and ribosomal DNA in the fish Erythrinus erythrinus. Implications for genome change and karyoevolution in fish

Abstract

BackgroundThe fish, Erythrinus erythrinus, shows an interpopulation diversity, with four karyomorphs differing by chromosomal number, chromosomal morphology and heteromorphic sex chromosomes. Karyomorph A has a diploid number of 2n = 54 and does not have differentiated sex chromosomes. Karyomorph D has 2n = 52 chromosomes in females and 2n = 51 in males, and it is most likely derived from karyomorph A by the differentiation of a multiple X1X2Y sex chromosome system. In this study, we analyzed karyomorphs A and D by means of cytogenetic approaches to evaluate their evolutionary relationship.ResultsConspicuous differences in the distribution of the 5S rDNA and Rex3 non-LTR retrotransposon were found between the two karyomorphs, while no changes in the heterochromatin and 18S rDNA patterns were found between them. Rex3 was interstitially dispersed in most chromosomes. It had a compartmentalized distribution in the centromeric regions of only two acrocentric chromosomes in karyomorph A. In comparison, in karyomorph D, Rex3 was found in 22 acrocentric chromosomes in females and 21 in males. All 5S rDNA sites co-localized with Rex3, suggesting that these are associated in the genome. In addition, the origin of the large metacentric Y chromosome in karyomorph D by centric fusion was highlighted by the presence of internal telomeric sites and 5S rDNA/Rex3 sites on this chromosome.ConclusionWe demonstrated that some repetitive DNAs (5S rDNA, Rex3 retroelement and (TTAGGG)n telomeric repeats) were crucial for the evolutionary divergence inside E. erythrinus. These elements were strongly associated with the karyomorphic evolution of this species. Our results indicate that chromosomal rearrangements and genomic modifications were significant events during the course of evolution of this fish. We detected centric fusions that were associated with the differentiation of the multiple sex chromosomes in karyomorph D, as well as a surprising increase of associated 5S rDNA/Rex3 loci, in contrast to karyomorph A. In this sense, E. erythrinus emerges as an excellent model system for better understanding the evolutionary mechanisms underlying the huge genome diversity in fish. This organism can also contribute to understanding vertebrate genome evolution as a whole.

Comparative cytogenetic mapping of rRNA genes among naked catfishes: implications for genomic evolution in the Bagridae family

“…By contrast, 5S rDNA signals were revealed in 2, 3, and 5 pairs of chromosomes in H. nemurus, H. wyckii, and H. filamentus, respectively. Multiple loci of minor ribosomal genes have been found in some fishes (Martins and Galetti, 2001;Hatanaka and Galetti, 2004;Rocco et al, 2005); variation in the number of 5S rDNA loci has also been observed among other species, such as the red wolf fish Erythrinus erythrinus, which has more than 20 sites (Cioffi et al, 2010), the cichlid Astatotilapia latifasciata, which has 15 clusters (Poleto et al, 2010) and the cichlid Laetacara dorsigera, which has 14 sites (Nakajima et al, 2012), In general, 5S rDNA loci can be found in the interstitial regions of fish chromosomes, and their pattern may represent an ancestral condition or even some advantage for the genome organization of these sequences (Martins and Galetti, 2001). H. wyckioides, M. atrifasciatus, and M. multiradiatus appear to maintain the ancestral location of the 5S rDNA loci, while the other genera studied had 5S rDNA loci at the terminal positions of the chromosomes.…”

Transposable elements as a potential source for understanding the fish genome

“…On the other hand, Cioffi et al 47 describes a more complex structuring of TEs in Erythrinus erythrinus. This species, pertaining to the order Characiformes, presents an expressive intrapopulational chromosome diversity, with four cytotypes differentiated by the number, chromosome morphology and presence of heteromorphic systems of sex chromosomes.…”

“…The authors point out that the origin of metacentric chromosome Y in cytotype D has possibly occurred by centric fusion, which is evidenced by the presence of one telomeric site in interstitial position and by the association of DNAr with Rex3 in this chromosome. 47 Besides being part of heterochromatin regions of chromosomes of some species and spread throughout the genome in others, TEs can also be associated with supranumerary or B chromosomes in teleosts. B chromosomes, additional genomic elements found in organisms, are usually heterochromatic, and do not generally present homology to the elements of the A complement.…”

Differentiation and evolutionary relationships in Erythrinus erythrinus (Characiformes, Erythrinidae): occurrence and distribution of B chromosomes

“…Indeed, its biodiversity is evidenced by the distinct chromosomal rearrangements that are a characteristic of each karyomorph Cioffi et al, 2010), including the origin of a multiple sex chromosome system and the supernumerary chromosomes presently found in some populations.…”