Interstitial Telomeric Repeats Are Rare in Turtles

Abstract

Telomeres are nucleoprotein complexes protecting chromosome ends in most eukaryotic organisms. In addition to chromosome ends, telomeric-like motifs can be accumulated in centromeric, pericentromeric and intermediate (i.e., between centromeres and telomeres) positions as so-called interstitial telomeric repeats (ITRs). We mapped the distribution of (TTAGGG)n repeats in the karyotypes of 30 species from nine families of turtles using fluorescence in situ hybridization. All examined species showed the expected terminal topology of telomeric motifs at the edges of chromosomes. We detected ITRs in only five species from three families. Combining our and literature data, we inferred seven independent origins of ITRs among turtles. ITRs occurred in turtles in centromeric positions, often in several chromosomal pairs, in a given species. Their distribution does not correspond directly to interchromosomal rearrangements. Our findings support that centromeres and non-recombining parts of sex chromosomes are very dynamic genomic regions, even in turtles, a group generally thought to be slowly evolving. However, in contrast to squamate reptiles (lizards and snakes), where ITRs were found in more than half of the examined species, and birds, the presence of ITRs is generally rare in turtles, which agrees with the expected low rates of chromosomal rearrangements and rather slow karyotype evolution in this group.

Comparative Cytogenetics of Four Sea Turtle Species (Cheloniidae): G-Banding Pattern and in situ Localization of Repetitive DNA Units

“…Turtles show broad diversity in 2n chromosome number, and ITSs were found in some cytogenetic studies, suggesting that in some turtles, ITSs derive from chromosomal fusion [Montiel et al, 2016;Cavalcante et al, 2018;Srikulnath et al, 2019;Clemente et al, 2020]. Generally, ITSs in chromosomes are associated with (i) unstable chromosomal sites [Bolzán, 2017], (ii) vestigial telomeric sequences at chromosomal fusion points [Meyne et al, 1990;Glugoski et al, 2018], (iii) satellite units at heterochromatic sites [Faravelli et al, 2002], or (iv) sites of telomeric insertion during double-strand break repair with telomerase action [Azzalin et al, 2001;Ruiz-Herrera et al, 2008].…”

The Amazonian Red Side-Necked Turtle Rhinemys rufipes (Spix, 1824) (Testudines, Chelidae) Has a GSD Sex-Determining Mechanism with an Ancient XY Sex Microchromosome System

“…Likewise, interstitial telomeric sequences (ITSs) can be found to be associated with rDNAs, several times attributed to represent hotspots prone to chromosomal rearrangements [ 77 , 78 ]. However, they are relatively rare in some turtle lineages [ 79 ]. Except for the Y-linked accumulation of telomeric motifs in Elseya novaeguinae [ 6 ], hitherto, TTAGGGn repeats on the centromeric position of the sole metacentric chromosome pair of R. rufipes ( Figure 4 ) seem to be the first evidence of ITSs in Chelidae species.…”

“…In many vertebrate groups, ITS repeat has constantly been attributed to relics of ancient chromosomal rearrangements [ 33 , 80 , 81 ]; however, ITSs exhibit a random amplification across lineages [ 80 , 82 ], and, due to their dynamic functioning [ 78 ], sometimes do not represent artifacts or ghosts of past intra/interchromosomal rearrangements. Since the most of closely related species to R. rufipes also exhibits the 2 n = 58, with very similar karyotype structure [ 5 , 7 , 42 , 47 ], the ITS present on the centromeric position of the sole metacentric pair could indeed be the result of past intrachromosomal rearrangements, but combined with the fact that these interstitial telomeric motifs are rarely found in some turtle lineages [ 79 ] and taking into account their dynamic behavior [ 78 ], it is also plausible that such ITSs may have arisen from other mechanisms, such as telomerase activity adding these motifs to nonterminal regions, duplication events, or even association with mobile elements and/or other repetitive sequences [ 83 , 84 , 85 , 86 , 87 , 88 ]. The karyotype of other South American chelids is also required to infer whether this ITS present in R. rufipes is a classical exception to the rule [ 82 ] or ITS sites are frequent and are shaping the karyotype diversity evident in Neotropical chelids.…”

“…Interestingly, as revealed here in our study, even with ancient origin, they can also be found practically intact in recent lineages, where the X and Y of R. rufipes are undistinguished from each other, with the Y sex chromosome being identified solely by comparative genomic hybridization and recruitment of several SSR motifs. The sex chromosomes may remain undifferentiated for many reasons, for example, transitions and turnovers involving XY and ZW, evolutionary advantages promoted by the recombination between XY and/or Z and W, as well as shifts involving autosomes [ 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 , 50 , 51 , 52 , 53 , 54 , 55 , 56 , 57 , 58 , 59 , 60 , 61 , 62 , 63 , 64 , 65 , 66 , 67 , 68 , 69 , 70 , 71 , 72 , 73 , 74 , 75 , 76 , 77 , 78 , 79 , 80 , 81 , 82 , 83 , 84 , 85 , 86 , 87 , …”

Heterochromatin and microsatellites detection in karyotypes of four sea turtle species: Interspecific chromosomal differences

“…The wide variation of 2n (26 -68 chromosomes) observed in turtles implies that their genomes have been deeply reorganized (Noleto et al, 2006;Valenzuela and Adams, 2011;Montiel et al, 2016;Noronha et al, 2016;Cavalcante et al, 2018Cavalcante et al, , 2020aCavalcante et al, , 2020bClemente et al, 2020). In this sense, the characterization of repetitive DNA sequences present in heterochromatin sites allow us to understand chromosomal rearrangements in some species of the group (Cavalcante et al, 2018(Cavalcante et al, , 2020a(Cavalcante et al, , 2020b.…”