Reinterpreting pericentromeric heterochromatin

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In fission yeast, pericentromeric heterochromatin is directly responsible for the sister chromatid cohesion that assures accurate chromosome segregation. In plants, however, heterochromatin and chromosome segregation appear to be largely unrelated: chromosome transmission is impaired by mutations in cohesion but not by mutations that affect heterochromatin formation. We argue that the formation of pericentromeric heterochromatin is primarily a response to constraints on chromosome mechanics that disfavor the transmission of recombination events in pericentromeric regions. This effect allows pericentromeres to expand to enormous sizes by the accumulation of transposons and through large-scale insertions and inversions. Although sister chromatid cohesion is spatially limited to pericentromeric regions at mitosis and meiosis II, the cohesive domains appear to be defined independently of heterochromatin. The available data from plants suggest that sister chromatid cohesion is marked by histone phosphorylation and mediated by Aurora kinases.

Introduction

The chromatin domains that flank centromeres are known as pericentromeric heterochromatin, pericentric heterochromatin, or simply as pericentromeres. Pericentromeres are the primary sites of sister chromatid cohesion, which is necessary for proper orientation of paired kinetochores during cell division. There is a long history of proposing functional relationships between heterochromatin and cohesion (e.g. [1, 2]) but the strongest data come from recent years, Schizosaccharomyces pombe. In this fission yeast, an interplay of weak repeat transcription, double-stranded DNA (dsDNA) formation and processing, and short interfering RNA (siRNA)-directed histone modification creates a biochemically defined pericentric heterochromatin domain [3, 4]. Virtually any disturbance of the heterochromatic state in S. pombe results in severe cell division defects due to loss of cohesion [3, 4]. In plants, however, recent data suggest there is very little functional relationship between heterochromatin and cohesion. Here, we review these data and present our perspectives on the origin of heterochromatin and the cell biology of chromosome segregation.

Section snippets

The role of the functional pericentromere in cell division

Accurate chromosome segregation requires a series of timely molecular events. Chief among these are the deposition and removal of cohesin complexes that mediate the association of sister chromatids during mitosis and meiosis. Cohesins consist of four subunits that are thought to form ring structures that link DNA and align replicated chromosomes along their lengths [5, 6]. Cohesin facilitates chromosome inheritance in two important ways: first, it ensures that sister kinetochores attach to the

The evolutionary biology of pericentromeres

Unlike their compact and genetically stable yeast counterparts, plant pericentromeres are ill-defined and genetically labile [15]. These traits have given pericentromeres a reputation as genomic ‘junkyards’: silent repositories of repetitive DNA and other useless DNA elements. To some extent this view is probably correct, but the large reservoirs of DNA within pericentromeres might also contribute to the evolution of new genes and new forms of gene regulation.

The portion of pericentromeres that

The origin of heterochromatin

What factors contribute to the expansion of pericentromeres and their associated rapid evolutionary change? This question can be recast in terms of recombination suppression because recombination is thought to be a primary force in the removal of unnecessary sequences: when recombination is reduced by any mechanism, repeats are expected to accumulate ([24]; Figure 1). It is possible that cohesin suppresses recombination, but we know of no data from multicellular eukaryotes that would support

The heterochromatin-cohesion connection

It is increasingly apparent that the boundaries of eukaryotic centromeres and pericentromeres are defined by epigenetic mechanisms. Ironically, the key to pericentric silencing is a low level of transcription. Pericentric transcripts are processed into siRNAs by RNA interference (RNAi) machinery and fed into a loop that maintains a heterochromatic state, which in S. pombe and animals is defined by methylation at histone H3 lysine 9 (H3K9) and the presence of HP-1/Swi6 (Heterochromatin

Histone phosphorylation as an epigenetic mark for cohesin deposition

During cell division in many organisms, pericentromeric chromatin is phosphorylated at conserved histone H3 residues serine10 and 28 (H3S10ph and H3S28ph) by Aurora kinases, which are key regulators of the transition from metaphase to anaphase and the release of chromatids [44, 45, 46]. These phosphorylation events are thought to be important for chromosome condensation [47], and in plants are strongly correlated with cohesion [43, 48, 49••]. Maize plants that carry mutations in the meiotic

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

Work in the corresponding author's laboratory is supported by a grant from the National Science Foundation (0421671).

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