Telomere organization and the interstitial telomeric sites involvement in insects and vertebrates chromosome evolution

Abstract

Telomere has a central role in chromosomal stability events. Chromosome ends organized in telomere-loop prevent activation of DNA damage response (DDR) mechanisms, thus keeping the chromosome structure organized. On the other hand, free chromosome ends, dysfunctional telomeres, and interstitial telomeric sequences (ITS) can trigger chromosome rearrangements. Here, the telomere organization, function, and maintenance mechanisms, in addition to ITS types and their involvement in chromosome changes, were revisited. Despite a general (TTAGGG) n sequence being present in vertebrate telomeres, insects show more diversification of their telomere motif. The relation between ITS and chromosome rearrangements was observed in insects and vertebrates, demonstrating different types of genome organization and distribution. Some ITS cannot be considered relicts of chromosome rearrangements because probable they were inserted during a double-strand break repair mechanism. On the other hand, the involvement of telomere sequences participating or triggering chromosome rearrangements or organizing satellite DNA components in several species groups is evident. The genomic assembling advances and applying other methodologies over ITS, and their flanking regions, can help to understand the telomere participation in the chromosomal evolution in species groups with highly diversified karyotypes.

Conserved satellite DNA motif and lack of interstitial telomeric sites in highly rearranged AfricanNothobranchiuskillifish karyotypes

“…This absence of interstitial telomeric sites (ITSs) is striking especially in species with highly reduced 2n compared to modal chromosome counts (2n = 36–38; [Krysanov and Demidova, 2018]), such as N. rachovii (2n = 16) or N. krysanovi (2n = 18), where multiple chromosome fusions apparently took place during the evolution. ITSs which may represent remnants of previous rearrangements [Meyne et al, 1990; Ocalewicz, 2013; Vicari et al, 2022] were lacking also on neo-Y chromosomes of F. thierryi and four Nothobranchius species with X 1 X 2 Y sex chromosome system. As discused above, these Y chromosomes highly likely emerged after fusion of ancestral Y with an autosome.…”

“…Most widely used repeats have been so far ribosomal DNA (rDNA) clusters and telomeric sequences, due to their deep sequence conservation and mostly easy visualization by fluorescence in situ hybridization (FISH) [Cioffi and Bertollo, 2012;Ocalewicz, 2013;Sochorová et al, 2018;Vicari et al, 2022]. Developments in genomics and in bioinformatic pipelines during the last decade greatly boosted the analysis of highly variable and formerly hardly tractable repeats, such as mobile elements and satDNA (e.g., [Ruiz-Ruano et al, 2016;Garrido-Ramos, 2017;Lower et al, 2018;Novák et al, 2020;Vondrak et al, 2020;Šatović-Vukšić and Plohl, 2023]).…”

“…For instance, specific telomeric tandem repeats being in vertebrates composed of TTAGGG monomeres [Meyne et al, 1990] act in concert with associated protein complexes to protect chromosome ends from being recognized as aberrant double-stranded breaks, and from digestion by nucleases. They also counteract the possibly deleterious effect of genetic material loss during the replication of linear chromosomes [O’Sullivan and Karlseder, 2010; Lazzerini-Denchi and Sfeir, 2016; Vicari et al, 2022].…”

“…In teleost fishes, similarly to other organisms, repetitive DNA classes serve as chromosomal landmarks for tracking lineage-specific genome, karyotype and sex chromosome dynamics, and for cytotaxonomic purposes (e.g., [Bellafronte et al, 2005; Schemberger et al, 2011; Cioffi and Bertollo, 2012; Glugoski et al, 2020; Goes et al, 2020; Yano et al, 2021]). Most widely used repeats have been so far ribosomal DNA (rDNA) clusters and telomeric sequences, due to their deep sequence conservation and mostly easy visualization by fluorescence in situ hybridization (FISH) [Cioffi and Bertollo, 2012; Ocalewicz, 2013; Sochorová et al, 2018; Vicari et al, 2022]. Developments in genomics and in bioinformatic pipelines during the last decade greatly boosted the analysis of highly variable and formerly hardly tractable repeats, such as mobile elements and satDNA (e.g., [Ruiz-Ruano et al, 2016; Garrido-Ramos, 2017; Lower et al, 2018; Novák et al, 2020; Vondrak et al, 2020; Šatović-Vukšić and Plohl, 2023]).…”

Haplotype-resolved assembly of the African catfish (Clarias gariepinus) provides insights for semi-terrestrial adaptation of airbreathing catfishes

“…This suggests that the terminal scaffold is probably misoriented. Though, these ITS may also indicate relics of ancient chromosomal rearrangements in C. gariepinus , including centric and tandem chromosome fusion 110,111 .…”