Cytogenomics Unveil Possible Transposable Elements Driving Rearrangements in Chromosomes 2 and 4 of Solea senegalensis

Abstract

Cytogenomics, the integration of cytogenetic and genomic data, has been used here to reconstruct the evolution of chromosomes 2 and 4 of Solea senegalensis. S. senegalensis is a flat fish with a karyotype comprising 2n = 42 chromosomes: 6 metacentric + 4 submetacentric + 8 subtelocentric + 24 telocentric. The Fluorescence in situ Hybridization with Bacterial Artificial Chromosomes (FISH-BAC ) technique was applied to locate BACs in these chromosomes (11 and 10 BACs in chromosomes 2 and 4, respectively) and to generate integrated maps. Synteny analysis, taking eight reference fish species (Cynoglossus semilaevis, Scophthalmus maximus, Sparus aurata, Gasterosteus aculeatus, Xiphophorus maculatus, Oryzias latipes, Danio rerio, and Lepisosteus oculatus) for comparison, showed that the BACs of these two chromosomes of S. senegalensis were mainly distributed in two principal chromosomes in the reference species. Transposable Elements (TE) analysis showed significant differences between the two chromosomes, in terms of number of loci per Mb and coverage, and the class of TE (I or II) present. Analysis of TE divergence in chromosomes 2 and 4 compared to their syntenic regions in four reference fish species (C. semilaevis, S. maximus, O. latipes, and D. rerio) revealed differences in their age of activity compared with those species but less notable differences between the two chromosomes. Differences were also observed in peaks of divergence and coverage of TE families for all reference species even in those close to S. senegalensis, like S. maximus and C. semilaevis. Considered together, chromosomes 2 and 4 have evolved by Robertsonian fusions, pericentric inversions, and other chromosomal rearrangements mediated by TEs.

Genomic Characterization of hox Genes in Senegalese Sole (Solea senegalensis, Kaup 1858): Clues to Evolutionary Path in Pleuronectiformes

“…Among vertebrates, there are qualitative and quantitative differences in TEs: Class I retrotransposons are the most abundant group in mammalian and avian genomes; and Class II DNA transposons are the most abundant transposable element in fish genomes [ 77 ]. Our results have shown that TE content in hox clusters is lower than whole genome coverage values [ 13 , 15 , 17 ] except in the hoxba cluster, where we have reported, as in the lizard species, an increased accumulation of interspersed repeats comprised mainly retrotransposons [ 73 , 74 ].…”

“…The repeat elements analyzed were transposable elements (TEs) (Class I and II), simple repeats, satellite sequences, low-complexity elements and small RNA. The parameters used to measure the abundance of repeated elements of each hox cluster were the number of loci per Mb (NL/Mb) and their coverage, measured as a percentage of length occupied by repeated elements per cluster analyzed (%) [ 13 , 15 ]. To study the distribution of repetitive elements throughout the hoxba cluster, a sliding window of 3 kb was applied using TE annotations from RepeatMasker results.…”

“…Particularly in the Senegalese sole, cytogenomic techniques have contributed to understanding the genome organization, leading to the description of the number and morphology of chromosomes [ 6 , 7 ]. Bioinformatics tools have allowed the characterization of genes and sequences of interest, such as those related to sexual differentiation, metamorphosis, immune response, histones, repetitive sequences, and transposable elements, among others [ 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 ]. In addition, these techniques have allowed evolutionary hypotheses to be inferred as well as the development of a high-density cytogenomic map [ 16 , 17 ].…”

The genomic study of repetitive elements in Solea senegalensis reveals multiple impacts of transposable elements in the evolution and architecture of Pleuronectiformes chromosomes

“…In that sense, we carried out the study of abundance by chromosomes, considering that they could have a seemingly more local behavior, like an ecosystem, and reflect their evolution. In previous studies, partial analyses of the distribution of repetitive elements in S. senegalensis have been carried out by analyzing the content of these elements in BAC clones located in cytogenetic maps (Rodrıǵuez et al, 2019, Rodrıǵuez et al, 2021Ramıŕez et al, 2022). In these studies, clones (between 4 and 8) were analyzed, spaced out in some chromosomes.…”

“…The Senegalese sole (Solea senegalensis) is among the most important flatfish, with a wide distribution along the eastern coast of the Atlantic Ocean and in the Mediterranean Sea and a high economic value (Imsland et al, 2004;Dıáz-Ferguson et al, 2007, Dıáz-Ferguson et al, 2012. This commercial interest has promoted the increase in genomic resources in the last decade (Robledo et al, 2017;Garcıá-Angulo et al, 2018;Cross et al, 2020;Merlo et al, 2021;Rodrıǵuez et al, 2021;de la Herrań et al, 2023), including an initial version of its genome (Guerrero-Coźar et al, 2021) and a recent improved version (de la Herrań et al, 2023). Due to the absence, until 2023, of a quality sequenced genome in this species, repetitive sequence studies on Senegalese sole had been limited to the sequence analysis of some BAC clones mapped on the chromosomes of the species (Garcıá et al, 2019;Rodrıǵuez et al, 2019;Cross et al, 2020;Rodrıǵuez et al, 2021;Ramıŕez et al, 2022) and the study of TEs in the Hox gene clusters of three flatfish species, including S. senegalensis (Mendizabal-Castillero et al, 2022).…”