The evolutionary dynamics of α-satellite

Abstract

␣-Satellite is a family of tandemly repeated sequences found at all normal human centromeres. In addition to its significance for understanding centromere function, ␣-satellite is also a model for concerted evolution, as ␣-satellite repeats are more similar within a species than between species. There are two types of ␣-satellite in the human genome; while both are made up of ∼171-bp monomers, they can be distinguished by whether monomers are arranged in extremely homogeneous higher-order, multimeric repeat units or exist as more divergent monomeric ␣-satellite that lacks any multimeric periodicity. In this study, as a model to examine the genomic and evolutionary relationships between these two types, we have focused on the chromosome 17 centromeric region that has reached both higher-order and monomeric ␣-satellite in the human genome assembly. Monomeric and higher-order ␣-satellites on chromosome 17 are phylogenetically distinct, consistent with a model in which higher-order evolved independently of monomeric ␣-satellite. Comparative analysis between human chromosome 17 and the orthologous chimpanzee chromosome indicates that monomeric ␣-satellite is evolving at approximately the same rate as the adjacent non-␣-satellite DNA. However, higher-order ␣-satellite is less conserved, suggesting different evolutionary rates for the two types of ␣-satellite.[Supplemental material is available online at www.genome.org.]All ␣-satellite DNA is made up of tandem monomers, each ∼171 bp in length (Manuelidis and Wu 1978;Willard and Waye 1987b). As revealed by patterns of monomer organization, there are two major types of ␣-satellite DNA in the human genome, designated higher-order and monomeric (Warburton and Willard 1996;Alexandrov et al. 2001;. Higher-order ␣-satellite DNA is made up of monomers arranged in multimeric repeat units that are highly similar from repeat unit to repeat unit. These higher-order repeat units are positioned tandemly to make up an array of extremely homogeneous higher-order ␣-satellite typically several megabases in size. In contrast, monomeric ␣-satellite lacks detectable higher-order periodicity, and its constituent monomers are far less homogeneous than are higher-order repeat units . All normal human centromeres contain large arrays of higher-order ␣-satellite (Warburton and Willard 1996;Alexandrov et al. 2001), and, where investigated, these arrays have been found to be bordered by more heterogeneous monomeric ␣-satellite (Wevrick et al. 1992;Horvath et al. 2000;Schueler et al. 2001;Guy et al. 2003;. The adjacent organization of higherorder and monomeric ␣-satellite, as well as the fact that lower primates have only monomeric ␣-satellite at their centromeres (Rosenberg et al. 1978;Musich et al. 1980;Maio et al. 1981;Thayer et al. 1981;Alves et al. 1994), has led to the hypothesis that higher-order ␣-satellite evolved from ancestral arrays of monomeric ␣-satellite and subsequently transposed to the centromeric regions of all great ape chromosomes (Warburton and Willard 1996;Alexandrov et al. ...

Clusters of alpha satellite on human chromosome 21 are dispersed far onto the short arm and lack ancient layers

“…This model for AS evolution is supported by studies of the detailed organization of AS clusters on chromosomes X, 8 and 17 (Schueler et al 2001, Schueler et al 2005, Rudd et al 2006, Shepelev et al 2009). In all cases the HOR-containing functional centromere is surrounded by multiple monomeric AS clusters arrayed roughly symmetrically on both chromosome arms.…”

The CentO satellite confers translational and rotational phasing on cenH3 nucleosomes in rice centromeres

“…Satellite sequences are known to undergo rapid expansions or contractions (7,8,36), which has been attributed to their "selfish" competition for preferential transmission in female meiosis, or "centromere drive" (2,46). However, the reasons for the success or failure of any particular satellite in this competition have remained obscure.…”

“…The tandem arrays of highly repeated satellite sequences that compose most plant and animal centromeres can differ dramatically between closely related species (5), and even between different chromosomes (6)(7)(8), suggesting that satellite arrays undergo rapid evolution through expansions, contractions, gene conversions, and transpositions. Monomers of satellite repeats range in length from 5 bp in Drosophila to 1,419 bp in cattle although more than half of described monomers in 282 species have lengths between 100 and 200 bp, often regarded as approximately the length of nucleosomal DNA (6,9).…”

Evolutionary dynamics and sites of illegitimate recombination revealed in the interspersion and sequence junctions of two nonhomologous satellite DNAs in cactophilic Drosophila species

“…Reproductive barriers would subsequently allow homogenization of different mutations in the genome of different populations and species. There is evidence that the homogenization process is more efficient within clusters of neighboring monomers than between more distal monomers located in the same chromosome or in nonhomologous chromosomes (Hall et al, 2005;Rudd et al, 2006).…”

“…Satellite DNAs often exhibit a higher degree of sequence similarity among repeats from the same species compared with lower similarity between orthologous repeats, even in closely related species (Bachmann and Sperlich, 1993;Mantovani et al, 1997;Fernández et al, 2001;Heslop-Harrison et al, 2003;Rudd et al, 2006). Models to explain this phenomenon, known as concerted evolution, assume that once mutations arise in individual repeats, repeated cycles of unequal crossing-over and gene conversion can duplicate and spread them simultaneously throughout a sequence family and a population of reproductive individuals (Dover, 1982;Kuhn et al, 2008).…”