Academic journal article Genetics

Differential Rates of Local and Global Homogenization in Centromere Satellites from Arabidopsis Relatives

Academic journal article Genetics

Differential Rates of Local and Global Homogenization in Centromere Satellites from Arabidopsis Relatives

Article excerpt

ABSTRACT

Higher eukaryotic centromeres contain thousands of satellite repeats organized into tandem arrays. As species diverge, new satellite variants are homogenized within and between chromosomes, yet the processes by which particular sequences are dispersed are poorly understood. Here, we isolated and analyzed centromere satellites in plants separated from Arabidopsis thaliana by 5-20 million years, uncovering more rapid satellite divergence compared to primate α-satellite repeats. We also found that satellites derived from the same genomic locus were more similar to each other than satellites derived from disparate genomic regions, indicating that new sequence alterations were homogenized more efficiently at a local, rather than global, level. Nonetheless, the presence of higher-order satellite arrays, similar to those identified in human centromeres, indicated limits to local homogenization and suggested that sequence polymorphisms may play important functional roles. In two species, we defined more extensive polymorphisms, identifying physically separated and highly distinct satellite types. Taken together, these data show that there is a balance between plant satellite homogenization and the persistence of satellite variants. This balance could ultimately generate sufficient sequence divergence to cause mating incompatibilities between plant species, while maintaining adequate conservation within a species for centromere activity.

L^RGE tandem arrays of satellite repeats, comprising up to hundreds of kilobases on a single chromosome, are prominent features of eukaryotic centromeres (HENIKOFF et al. 2001). As species diverge, some satellite variants disappear while novel repeats are generated to form a distinct set, or library, of satellite sequences (MESTROVIC et al 1998; NIJMAN and LENSTRA 2001; PONS et al. 2004). The predominant mechanisms by which individual satellites are amplified and homogenized are not understood. Particular sets of satellite variants could be dispersed through the genome in a homogenization process known as molecular drive (DOVER 1982), or alternatively the maintenance of specific repeats could reflect natural selection that ensures proper centromere function.

Higher eukaryotic centromeres mediate kinetochore formation, promote sister chromatid cohesion, and suppress reciprocal crossing over during meiosis. Centromere satellites were once viewed as "junk" or "parasitic" DNA (UNO 1972; ORGEL and CRICK 1980), and their absence from human neocentromeres called their importance into question (BARRY et al. 1999). More recent studies, however, have compiled strong evidence that satellites contribute to centromere functions (WILLARD 1998, 2001; YANG et al 2000; SCHUELER et al 2001; GRIMES et al 2002; NAGAKI et al 2003). For example, when tandem arrays of the 171-bp human á-satellite repeat are placed on a linear or circular artificial chromosome vector, they promote efficient inheritance (WiLLARD 1998, 2001; YANG et al 2000; SCHUELER et al 2001; GRIMES et al. 2002); similar results have been obtained using satellites and cell lines from mice (TELENIUS et al. 1999; Co et al. 2000). In addition, chromatin immunoprecipitation experiments in Arabidopsis thaliana have shown that an essential centromere-binding protein, HTRl 2, associates primarily with the 178-bp satellite repeat that occurs exclusively in the genetically defined centromere region (COPENHAVER et al 1999; ARABIDOPSIS GENOME INITIATIVE 2000; NAGAKI et al 2003). HTR12 is homologous to centromere protein A (CENP-A) or Cid, an essential histone H3-like protein that marks the site of centromere function in species ranging from yeast to human (HENIKOFF et al 2001).

The requirement for partitioning a complete chromosome complement during each mitotic and meiotic cell division places a strong selective pressure on the interactions between satellites and centromere-binding proteins (CLARKE 1998). As satellites evolve, centromere proteins must maintain the ability to bind to satellite sequences, thus creating the need for rapid protein evolution to maintain DNA-protein binding specificity (HENIKOFF et al. …

Search by... Author
Show... All Results Primary Sources Peer-reviewed

Oops!

An unknown error has occurred. Please click the button below to reload the page. If the problem persists, please try again in a little while.