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. 2019 Feb 6;20(3):701.
doi: 10.3390/ijms20030701.

Insertion Hot Spots of DIRS1 Retrotransposon and Chromosomal Diversifications among the Antarctic Teleosts Nototheniidae

Juliette Auvinet  1 , Paula Graça  2 , Laura Ghigliotti  3 , Eva Pisano  4 , Agnès Dettaï  5 , Catherine Ozouf-Costaz  6 , Dominique Higuet  7   8
Affiliations

Insertion Hot Spots of DIRS1 Retrotransposon and Chromosomal Diversifications among the Antarctic Teleosts Nototheniidae

Juliette Auvinet et al. Int J Mol Sci. .

Abstract

By their faculty to transpose, transposable elements are known to play a key role in eukaryote genomes, impacting both their structuration and remodeling. Their integration in targeted sites may lead to recombination mechanisms involved in chromosomal rearrangements. The Antarctic fish family Nototheniidae went through several waves of species radiations. It is a suitable model to study transposable element (TE)-mediated mechanisms associated to genome and chromosomal diversifications. After the characterization of Gypsy (GyNoto), Copia (CoNoto), and DIRS1 (YNoto) retrotransposons in the genomes of Nototheniidae (diversity, distribution, conservation), we focused on their chromosome location with an emphasis on the three identified nototheniid radiations (the Trematomus, the plunderfishes, and the icefishes). The strong intrafamily TE conservation and wide distribution across species of the whole family suggest an ancestral acquisition with potential secondary losses in some lineages. GyNoto and CoNoto (including Hydra and GalEa clades) mostly produced interspersed signals along chromosomal arms. On the contrary, insertion hot spots accumulating in localized regions (mainly next to centromeric and pericentromeric regions) highlighted the potential role of YNoto in chromosomal diversifications as facilitator of the fusions which occurred in many nototheniid lineages, but not of the fissions.

Keywords: DIRS1; FISH; Nototheniidae; chromosomal rearrangements; insertion hot spots; retrotransposons; species radiation.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Phylogenetic relationships (cladogram) of the nototheniid sub-families presented in this study (as defined in [63]). Total number of genera for each nototheniid sub-families are indicated in parenthesis. Genera used in this study: Pleuragramma (Pleuragramminae), Dissostichus (Dissostichinae), Trematomus, Lepidonotothen, Patagonotothen (Trematominae), Gobionotothen (Gobionototheniinae), Notothenia, Paranotothenia (Nototheniinae), Histiodraco, Pogonophryne (Artedidraconinae), Champsocephalus, Chionodraco, Cryodraco (Channichthyinae), Cygnodraco (Cygnodraconinae), Gymnodraco (Gymnodraconinae).
Figure 2
Figure 2
Neighbor joining (NJ) unrooted trees for (A) YNoto, (B) CoNoto, (C) GyNoto (RT/RH) and (D) GyNoto (Int) nucleotide sequences for the whole nototheniid transposable element (TE) datasets. Alignements used to construct these trees are presented in Figure S1. Analyses were run using the Jukes–Cantor model and no outgroup. Support for individual clusters was evaluated using non-parametric bootstrapping with 1000 replicates. Arrows show the additional DIRS1 and Gypsy sequences originating from the N. coriiceps genome sequencing [67].
Figure 3
Figure 3
Fluorescent in-situ hybridization (FISH)-mapping of TEs on the chromosomes of six nototheniid species. (A) YNoto, GyNoto and CoNoto positioning in three non Trematomus Nototheniidae, (B) YNoto positioning in three Trematomus species. The chromosomal numbers of C. hamatus and T. nicolai are sex dependent. The number for the sex represented in the figure (male for C. hamatus, female for T. nicolai) is underlined. Each probe was labeled with biotin and bound probes were detected with incubation with Avidin-FITC (fluorescein, greenish spots). Probe characteristics are indicated in Table S3. Chromosomal DNA was counterstained with 4′,6-diamidino-2-phenylindole (DAPI). One family from each retrotransposon superfamily is represented in this figure for YNoto (YNotoJ) and GyNoto elements (GyNotoA), and two families for CoNoto elements (CoNotoA (GalEa clade) and CoNotoB (Hydra clade)). Examples of TE distributions for pattern 1: a, e, i; pattern 2: j, h; and pattern 1 + 2: d, l. White arrows point examples of TE accumulations. Red arrows point the heteromorphic Y sex chromosome in C. hamatus and purple arrows indicate the largest sub-metacentric pair in H. velifer. Scale bars: 10 μm.
Figure 4
Figure 4
FISH patterns of YNoto on fused chromosomes of T. eulepidotus, N. coriiceps, C. hamatus, and H. velifer. The chromosomal number of C. hamatus is sex dependent. The number for the sex represented in the figure (male) is underlined. Diploid sets for DAPI captures and haploid sets for scheme representations are presented. The main YNoto insertion hot spots observed by FISH are represented by the green rectangles. Scale bars: 7 µm.
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