Dynamic evolution at pericentromeres

Abstract

Pericentromeres are exceptional genomic regions: in animals they contain extensive segmental duplications implicated in gene creation, and in plants they sustain rearrangements and insertions uncommon in euchromatin. To examine the mechanisms and patterns of plant pericentromere evolution, we compared pericentromere sequence from four Brassicaceae species separated by <15 million years (Myr). This flowering plant family is ideal for studying relationships between genome reorganization and pericentromere evolution-its members have undergone recent polyploidization and hybridization, with close relatives changing in genome size and chromosome number. Through sequence and hybridization analyses, we examined regions from Arabidopsis arenosa, Capsella rubella, and Olimarabidopsis pumila that are homologous to Arabidopsis thaliana pericentromeres (peri-CENs) III and V, and used FISH to demonstrate they have been maintained near centromere satellite arrays in each species. Sequence analysis revealed a set of highly conserved genes, yet we discovered substantial differences in intergenic length and species-specific changes in sequence content and gene density. We discovered that A. thaliana has undergone recent, significant expansions within its pericentromeres, in some cases measuring hundreds of kilobases; these findings are in marked contrast to euchromatic segments in these species that exhibit only minor length changes. While plant pericentromeres do contain some duplications, we did not find evidence of extensive segmental duplications, as has been documented in primates. Our data support a model in which plant pericentromeres may experience selective pressures distinct from euchromatin, tolerating rapid, dynamic changes in structure and sequence content, including large insertions of mobile elements, 5S rDNA arrays and pseudogenes.[Supplemental material is available online at www.genome.org. The sequence data from this study have been submitted to GenBank under accession nos. DQ103593, DQ103594, and DQ103595.]Centromere functions are conserved throughout higher eukaryotes and mediated by common proteins, yet centromere satellite DNA sequences diverge rapidly, even in organisms separated by a few million years (Hall et al. 2003. Pericentromere DNA flanking these satellites also changes rapidly (She et al. 2004;Horvath et al. 2005), but the rate and magnitude of these changes make it challenging to infer pericentromere evolution in small taxonomic families. Here, we perform the first comparative analysis of plant pericentromeres, selecting a family of 3350 members. We show that homologous pericentromeres from four Brassicaceae species are remarkably dynamic, undergoing rapid changes in structure and sequence content.In most multicellular organisms, centromere DNA sequences are highly repetitive, methylated, and heterochromatic; they inhibit reciprocal homologous recombination, mediate meiotic sister-chromatid cohesion, and assemble kinetochore proteins (Amor et al. 2004). Centromere cores contain tandem satellite a...

Evolutionary History and Positional Shift of a Rice Centromere

“…This observation parallels the previous finding that LTR retrotransposons make up an exceptionally small portion of O. brachyantha centromeres (Lee et al 2005). Differential expansion of orthologous pericentromeric regions of related Brassicaceae species has been previously described (Hall et al 2006). Differences in the activity of mechanisms for LTR-retrotransposon regulation (Bennetzen et al 2005) and DNA rearrangements, e.g., segmental duplication as found in the Cen8 and Cen4 regions (Ma and Bennetzen 2006;Ma and Jackson 2006;Ma et al 2007), could partially explain the rapid and dramatic size variation between these regions.…”

High DNA Sequence Diversity in Pericentromeric Genes of the Plant Arabidopsis lyrata

“…Despite other karyotypic differences between these species, including some reciprocal translocations, most chromosome arms are syntenic, and the positions of the five centromeres in A. thaliana are probably unchanged from their ancestral positions Kawabe et al 2006b;Lysak et al 2006). For regions corresponding to the pericentromeres of A. lyrata AL5 (homologous to A. thaliana CEN3) and AL7 (A. thaliana CEN5), the gene content is the same as in three other related species investigated: Capsella rubella, Olimarabidopsis pumila, and A. arenosa, and the A. arenosa BAC clone homologous to A. thaliana CEN3 also includes some centromeric repeat sequences, definitively identifying this as a pericentromere region (Hall et al 2006). Finally, mapping of loci located near the centromeres of A. thaliana shows low crossingover frequencies in A. lyrata.…”

“…The difference is, however, partly due to the large regions containing the 5S rDNA loci inserted in the A. thaliana chromosomes 3 and 5 pericentromere regions . The mean pericentromeric region gene densities in C. rubella and A. arenosa (0.17 and 0.12 genes per kb, respectively), are nevertheless considerably lower than in the A. thaliana chromosome arm regions (.0.25 genes/kb, see Hall et al 2006). Gene densities are therefore probably lower than for chromosome arm regions in A. lyrata also.…”

“…Our comparison between chromosome arm regions and pericentromeric regions does not require detailed knowledge of gene densities in A. lyrata in the regions we compared. However, some information from related species is pertinent, since the pericentromeric regions of A. thaliana appear to be expanded relative to those of C. rubella, O. pumila and A. arenosa (Hall et al 2006), so that pericentromeric regions of related species might not have low gene densities. The difference is, however, partly due to the large regions containing the 5S rDNA loci inserted in the A. thaliana chromosomes 3 and 5 pericentromere regions .…”

Dynamic Rearrangements Determine Genome Organization and Useful Traits in Soybean

“…phytozome.com/soybean). Pericentromeric chromosomal regions were reported to be greatly expanded by transposable elements and repetitive DNA in Arabidopsis (Arabidopsis thaliana; Hall et al, 2006). Also, tandem repeats with interspersed retroelements were concentrated in pericentromere of soybean (Lin et al, 2005).…”