Evolution of subterminal satellite (StSat) repeats in hominids

Abstract

Subterminal satellite (StSat) repeats, consisting of 32-bp-long AT-rich units (GATATTTCCATGTT(T/C)ATACAGATAGCGGTGTA), were first found in chimpanzee and gorilla (African great apes) as one of the major components of heterochromatic regions located proximal to telomeres of chromosomes. StSat repeats have not been found in orangutan (Asian great ape) or human. This patchy distribution among species suggested that the StSat repeats were present in the common ancestor of African great apes and subsequently lost in the lineage leading to human. An alternative explanation is that the StSat repeats in chimpanzee and gorilla have different origins and the repeats did not occur in human. The purpose of the present study was quantitative evaluation of the above alternative possibilities by analyzing the nucleotide variation contained in the repeats. We collected large numbers of sequences of repeat units from genome sequence databases of chimpanzee and gorilla, and also bonobo (an African great ape phylogenetically closer to chimpanzee). We then compared the base composition of the repeat units among the 3 species, and found statistically significant similarities in the base composition. These results support the view that the StSat repeats had already formed multiple arrays in the common ancestor of African great apes. It is thus suggested that humans lost StSat repeats which had once grown to multiple arrays.

The evolution of African great ape subtelomeric heterochromatin and the fusion of human chromosome 2

“…These subtelomeric caps are heterochromatic in nature and are completely absent from the karyotype of human and orangutan (Haaf and Schmid 1987;IJdo et al 1991;Ventura et al 2011). Subterminal heterochromatin has been thought to be composed primarily of a tandem array of a 32-bp subterminal satellite (StSat) creating large subterminal blocks of constitutive heterochromatic regions (Royle et al 1994;Koga et al 2011) adjacent to the canonical telomeric TTAGGG sequence (Greider and Blackburn 1989). While almost all gorilla chromosomes show the presence of subterminal caps, only half of chimpanzee chromosomes possess such structures (Fan et al 2002).…”

“…Unlike centromeric satellite sequences, which were well-characterized prior to the era of full genome sequencing (Rudd and Willard 2004), there are relatively few detailed molecular studies of the organization or evolution of the subterminal caps (Royle et al 1994). Conservatively, it has been estimated by dot-blot analysis that the subterminal heterochromatin constitutes >3 Mbp (0.1%) of the total genomic DNA of each species (Yunis and Prakash 1982;Koga et al 2011).…”

Repetitive sequences originating from the centromere constitute large-scale heterochromatin in the telomere region in the siamang, a small ape

“…Here, we assume that change from 0 to þþ always passes through þ . We assume, however, that a direct change from þþ to 0 can happen because such a change is likely to have occurred in the human lineage with the StSat repeats (Koga et al, 2011). One possible mechanism we have in mind is truncation of chromosomes and regeneration of the telomere.…”

“…Fluorescent in-situ hybridization (FISH) analysis of an StSat repeat probe to metaphase chromosomes revealed that the repeats are present in the majority of chimpanzee and bonobo chromosomes and in all chromosomes of the gorilla (H Hirai, unpublished results). We have previously estimated the total size of the StSat repeats to be as large as 0.1% of the chimpanzee genome (Koga et al, 2011). The distribution of the StSat repeats among the hominid species (human and African great apes) is somewhat puzzling because humans are phylogenetically closer to chimpanzees and bonobos than to gorillas.…”

“…A question that readily arose from this patchy distribution was whether the StSat repeats were generated independently in the gorilla lineage and the chimpanzee/bonobo lineage, or whether the repeats were already present in the common ancestor of these great apes and were subsequently lost in the human lineage. We have recently settled this question (Koga et al, 2011): the latter explanation is more likely to be correct because the pattern of within-species variation is similar between gorilla and chimpanzee/bonobo, and this similarity is thought to stem from variation already present in the common ancestor. The molecular and cellular mechanisms of the emergence and disappearance of these structures have yet to be elucidated.…”