Heterochromatin Positioning and Nuclear Architecture

Heitz (1928) first described the two states of chromatin known as euchromatin and heterochromatin. Heterochromatin is often described as the gene-poor part of the genome associated with a silent and condensed state of chromatin inaccessible to transcription factors. However, this simple view has been challenged many times as heterochromatin is indeed transcribed and differences between the two states of chromatin depend on many other criteria. Data collected from the model species Arabidopsis thaliana indicate that heterochromatin relies on the repetitiveness of specific DNA sequences such as satellites, transposable elements and ribosomal DNA (rDNA) but also on epigenetic marks specifically associated with these repeated arrays. Recent studies on smallRNApathways have highlighted the central role of the RNA-directed DNA methylation pathway in heterochromatin specification indicating that heterochromatin is indeed an epigenetic state required for many other genome functions including chromosome segregation, gene regulation or maintenance of genome stability. Heterochromatin is a specific feature of eukaryotes and preferential localization at the nuclear periphery and to the nucleolus is observed in most organisms. This spatial organization of heterochromatin is maintained through the cell cycle although DNA is replicated, chromatin is condensed into chromosomes, and the nuclear envelope is disrupted and reformed. Whether spatial positioning participates in heterochromatin function and how plant cells are able to establish and maintain such a genome organization across the cell cycle is still largely unknown in Arabidopsis. Mechanisms leading to the appropriate positioning of heterochromatin within the nucleus will be discussed in the light of data coming from other species. A better understanding of heterochromatin organization and functions will be an important field of investigation for plants such as maize and wheat with considerably larger genome sizes than Arabidopsis.