Telomeres in plant meiosis, their structure, dynamics and function

Although the primary role of the telomeres is to protect the chromosome ends from being recognized and processed as DNA double-strand breaks, evidence is emerging that they have a pivotal role in early events in the movement and synapsis of homologous chromosomes in the meiotic pathway. Attention has been paid to the bouquet, a nearly universal event, during which the telomeres cluster on the nuclear envelope (NE) in early prophase I. It has been suggested that their close proximity promotes homologous pairing. We have previously shown in wild-type Arabidopsis thaliana that the telomeres are organized around the nucleolus in somatic cells and during the early stages of meiosis. While still associated with the nucleolus, homologous telomeres undergo pairing at the transition from G2 to leptotene at around the same time as assembly of the axial elements. We do not observe a classical bouquet, but as the homologues synapse during zygotene, the paired telomeres occasionally reveal a loose clustering on the NE, which may represent a transient bouquet. As Arabidopsis homologous telomere pairing precedes transient bouquet formation, we have suggested that close juxtaposition of the homologues by virtue of the tethering of the paired telomeres to the NE may facilitate subsequent chromosome alignment and synapsis. Identifying proteins that link the telomeres and the NE has been stimulated by observations in Schizosaccharomyces pombe, where meiotic telomere clustering at the spindle polar body (SPB) involves Sad1, a SPB protein that is indirectly connected to a telomere binding protein, Rap1. Sad1 and the related protein UNC-84 from Caenorhabditis elegans contain a so-called SUN domain consisting of conserved C-terminal protein regions a few hundred amino acids long. SUN domains are usually found following a transmembrane domain and a less conserved region of amino acids. Similar proteins have subsequently been identified in other yeasts and mammalian species. In the mouse and C. elegans, they appear to be required for telomere attachment to the NE and for moving the chromosomes via the telomeres in meiosis. Several components of the NE of plants have only recently been identified. This review focuses on the structure of the telomeres in Arabidopsis and their behaviour in the meiotic pathway. We also discuss recent observations linking a role for the meiotic telomeres and their association with the NE in meiotic prophase I.