The evolutionary life cycle of the resilient centromere

Abstract

The centromere is a chromosomal structure that is essential for the accurate segregation of replicated eukaryotic chromosomes to daughter cells. In most centromeres, the underlying DNA is principally made up of repetitive DNA elements, such as tandemly repeated satellite DNA and retrotransposable elements. Paradoxically, for such an essential genomic region, the DNA is rapidly evolving both within and between species. In this review, we show that the centromere locus is a resilient structure that can undergo evolutionary cycles of birth, growth, maturity, death and resurrection. The birth phase is highlighted by examples in humans and other organisms where centromere DNA deletions or chromosome rearrangements can trigger the epigenetic assembly of neocentromeres onto genomic sites without typical features of centromere DNA. In addition, functional centromeres can be generated in the laboratory using various methodologies. Recent mapping of the foundation centromere mark, the histone H3 variant CENP-A, onto near-complete genomes has uncovered examples of new centromeres which have not accumulated centromere repeat DNA. During the growth period of the centromere, repeat DNA begins to appear at some, but not all, loci. The maturity stage is characterised by centromere repeat accumulation, expansions and contractions and the rapid evolution of the centromere DNA between chromosomes of the same species and between species. This stage provides inherent centromere stability, facilitated by repression of gene activity and meiotic recombination at and around the centromeres. Death to a centromere can result from genomic instability precipitating rearrangements, deletions, accumulation of mutations and the loss of essential centromere binding proteins. Surprisingly, ancestral centromeres can undergo resurrection either in the field or in the laboratory, via as yet poorly understood mechanisms. The underlying principle for the preservation of a centromeric evolutionary life cycle is to provide resilience and perpetuity for the all-important structure and function of the centromere.

High-resolution mapping and transcriptional activity analysis of chicken centromere sequences on giant lampbrush chromosomes

“…If this is true, non-tandemly repetitive centromere regions could accumulate centromeric repeats and thus blocks of heterochromatin during the centromere growth period according to postulated centromere life cycle (Kalitsis and Choo 2012). On the other hand, centromeres of GGAZ and GGA5 cannot be surrounded by arrays of tandem repeats in pericentric regions because in the chicken genome assembly CenZ and Cen5 sequences interacting with CENP-A map to long contigs that are not interrupted by gaps.…”

“…Among vertebrates, the domestic chicken (Gallus gallus domesticus) represents an adequate model for studying the difference between recently evolved centromeres and mature centromeres (Hori and Fukagawa 2012;Kalitsis and Choo 2012). Genome-wide characterisation of DNA fragments associated with CENP-A has demonstrated unique features of centromere organisation in chicken karyotype: there are both mature centromeres, comprising chromosome-specific tandem repeats, and recently evolved primitive centromeres, consisting of non-repetitive DNA sequences (Shang et al 2010).…”

Paternal chromosome loss and metabolic crisis contribute to hybrid inviability in Xenopus

“…Chromosome loss and partial deletion has been observed in nonviable hybrids in fish 13,14 and Drosophila 15 , but the underlying mechanisms were unclear. Our results suggest that t e × l s hybrid incompatibility may be due to divergence of centromeric sequences, which are poorly characterized in Xenopus but known to evolve rapidly 16 , or to other unidentified repetitive DNA elements that lead to chromosome instability and ultimately prevent kinetochore assembly on chromosomes 3L and 4L.…”

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

“…Despite this apparent preference for repetitive DNA, a fully functional centromere, called a neocentromere, can occasionally form by assembling cenH3 nucleosomes on a single-copy DNA sequence that was not previously part of a centromere, indicating that centromere specification is epigenetic in plants and animals (for reviews, see refs. [1][2][3][4].…”