Massive LINE‐1 retrotransposon enrichment in tamarins of the Cebidae family (Platyrrhini, Primates) and its significance for genome evolution

Abstract

To study heterochromatin distribution differences among tamarins, we applied LINE-1 probes using fluorescence in situ hybridization onto chromosomes of Saguinus mystax, Leontocebus fuscicollis, and Leontopithecus rosalia with the aim to investigate possible evolutionary implications. LINE-1 repeats were shown to be involved in genome architecture and in the occurrence of chromosomal rearrangements in many vertebrates. We found bright LINE-1 probe signals at centromeric or pericentromeric areas, GC rich, on almost all chromosomes in three tamarin species. We also found noncentromeric signals along chromosome arms. In a phylogenetic perspective, we analyzed the pattern of LINE-1 distribution considering human chromosomal homologies and C banding patterns. Our data indicate that LINE-1 centromeric expansions and accumulation presumably arose in a common tamarin ancestor and that the presence of LINE-1 at the junction of human chromosome associations is presumably linked to interchromosomal rearrangements. For example, we found bright centromeric signals as well as non-centromeric signals on chromosomes 1 and 2, in all species analyzed, in correspondence to human chromosome associations 13/9/22 and 20/17/13, which are synapomorphic for all tamarins. Furthermore, we found other faint signals that could be apomorphisms linked both to intrachromosomal rearrangements as well as to retro-transposition events. Our results confirm that the three species have similar karyotypes but small differences in LINE-1 and heterochromatin amplification and distribution; in particular on chromosome pairs 19-22, where we show the occurrence of small inversions, in agreement with previous classic cytogenetic hypotheses.

Centromeric enrichment of LINE-1 retrotransposon in two species of South American monkeys Alouatta belzebul and Ateles nancymaae (Platyrrhini, Primates)

“…In our work, we found LINE-1 elements by FISH in the two species analyzed of both the Cebidae and Atelidae families, at centromeric position in agreement with previous cytogenetic molecular data (Serfaty et al 2017, Ceraulo et al, 2021b and supporting also previous molecular data (Sookdeo et al 2018). LINE-1 probes displayed a non-random distribution by accumulating primarily in CMA3 positive bands at centromeres or pericentromeric regions, co-localizing with C-positive heterochromatin bands (Fig 1, 2); the co-localization of LINE-1 with C-positive bands was previously identified not only in primates but also in other taxa (Kapitonov et al 1998;Serfaty et al 2017).…”

“…However, the pattern of LINE-1 distribution at the centromere is not a common phenomenon among the mammalian genome (Waters et al 2004;Dobigny et al 2004Dobigny et al , 2006Acosta et al 2008;Vieira-da-Silva et al 2016;de Sotero-Caio et al 2017); indeed, these elements are not often incorporated at major core centromeres, with the exception of the X chromosome euchromatic regions where they are usually abundant along the chromosomal length (Waters et al 2004;Acosta et al 2008). On the other hand, massive accumulations of repetitive elements at the centromeres was previously shown in many other mammals, such as bats and rodents (Sotero-Caio et al 2017;Paco et al 2015;Paço et al 2019), and in some primates (Carbone et al 2012;Serfaty et al 2017, Ceraulo et al, 2021b. In particular, among primates species, LINE-1 have been previously identified through FISH into platyrrhine genomes, in Saguinus midas and Saguinus bicolor (Serfaty et al 2017), in Saguinus mystax, Leontocebus fuscicollis, Leontopithecus rosalia (Ceraulo et al, 2021b)…”

“…On the other hand, massive accumulations of repetitive elements at the centromeres was previously shown in many other mammals, such as bats and rodents (Sotero-Caio et al 2017;Paco et al 2015;Paço et al 2019), and in some primates (Carbone et al 2012;Serfaty et al 2017, Ceraulo et al, 2021b. In particular, among primates species, LINE-1 have been previously identified through FISH into platyrrhine genomes, in Saguinus midas and Saguinus bicolor (Serfaty et al 2017), in Saguinus mystax, Leontocebus fuscicollis, Leontopithecus rosalia (Ceraulo et al, 2021b)…”

“…The possible link between transposable elements and alphasatellite DNA, could be show in the LINE signal amplification at the centromere position of subtelocentric/ acrocentric chromosome p arms, localizing with heterochromatin C-positive bands in Ateles chromosomes; these regions are the same where often it is found telomeric signal probes and rDNA probes amplification in many primates, as previous works have demonstrated (Mazzoleni et al 2017, Ceraulo et al, 2021a; thus, this observation presumably indicates that these LINE-1, alpha-satellite and other repetitive sequences could be involved to this DNA remodeling mechanism. However, considering that LINE have also been linked with chromosomal rearrangements (Böhne et al 2008;de Sotero-Caio et al 2017, Klein andO'Neill 2018), we should take into consideration that these sequences could have had a role in the process leading to the increased rates of chromosomal evolution responsible for the highly rearranged karyotypes of many taxa; for example, the link between evolutionary reshufflings and LI accumulation have been hypothesized in other platyhirrine species Saguinus mystax, Leontocebus fuscicollis, Leontopithecus rosalia (Ceraulo et al, 2021b) and from data obtained in rodent genera, where the most derived species display a higher level of LINE-1 accumulation on both autosomal and sex chromosomes then the more conserved ones (with accumulation usually only in the sex chromosomes) (Dobigny et al 2004;Rebuzzini et al 2009;Vieira-Dasilva et al 2016).…”

“…In humans and anthropoids, LINE-1 sequence comparisons have been made (Ovchinnikov et al 2001, Mathews et al 2003 showing that LINE-1 amplification may change rapidly during primate evolution giving different families with variable forms Among New World monkeys, high LINE activity has also been shown in the Saimiri and Saguinus lineages (Callitrichini), and reduced activity has been found in the Ateles lineage (Boissinot et al 2004, Sookdeo et al 2018. So far, however, the distribution of these repetitive sequences through FISH with LINE-1 probes has been studied in few platyrrhine species, belonging to the Callithricini subfamily of the Cebidae family (Serfaty et al 2017, Ceraulo et al 2021b.…”