Abstract
BackgroundChromosomes reorganize in early meiotic prophase to form the so-called telomere bouquet. In fission yeast, telomeres localize to the nuclear periphery via interaction of the telomeric protein Rap1 with the membrane protein Bqt4. During meiotic prophase, the meiotic proteins Bqt1-2 bind Rap1 and tether to the spindle pole body to form the bouquet. Although it is known that this polarized chromosomal arrangement plays a crucial role in meiotic progression, the molecular mechanisms of telomere bouquet regulation are poorly understood.ResultsHere, we detected high levels of Rap1 phospho-modification throughout meiotic prophase, and identified a maximum of 35 phosphorylation sites. Concomitant phosphomimetic mutation of the modification sites suggests that Rap1 hyper-phosphorylation does not directly regulate telomere bouquet formation or dissociation. Despite the negative charge conferred by its highly phosphorylated state, Rap1 maintains interactions with its binding partners. Interestingly, mutations that change the charge of negatively charged residues within the Bqt1-2 binding site of Rap1 abolished the affinity to the Bqt1-2 complex, suggesting that the intrinsic negative charge of Rap1 is crucial for telomere bouquet formation.ConclusionsWhereas Rap1 hyper-phosphorylation observed in meiotic prophase does not have an apparent role in bouquet formation, the intrinsic negative charge of Rap1 is important for forming interactions with its binding partners. Thus, Rap1 is able to retain bouquet formation under heavily phosphorylated status.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0149-x) contains supplementary material, which is available to authorized users.
Highlights
Chromosomes reorganize in early meiotic prophase to form the so-called telomere bouquet
Bouquet formation is achieved by expression of a pair of meiosisspecific proteins, Bqt1 and Bqt2, which bridge the telomeric proteins Taz1 and Rap1 to the Spindle pole body (SPB) component Sad1 [7]
Our data indicates that Rap1 phosphorylation accumulates as meiotic prophase progresses, and Rap1 becomes hyper-phosphorylated at the onset of meiosis I, when the bouquet stage ends [5]
Summary
Chromosomes reorganize in early meiotic prophase to form the so-called telomere bouquet. The position of chromosomes within the nucleus is dramatically reorganized and telomeres cluster within a limited area of the nuclear envelope to form the so-called telomere bouquet [2, 3]. This conserved reorganization of chromosomes during meiotic prophase has been observed in most eukaryotic organisms and is shown to promote homolog pairing and meiotic recombination [4]. In fission yeast Schizosaccharomyces pombe, the telomere bouquet is observed throughout meiotic prophase This period is known as the ‘horsetail nucleus’ stage, during which the nucleus elongates and oscillates back and forth between the cell poles, following the spindle pole body or SPB (the yeast equivalent of the centrosome) driven by cytoplasmic microtubules [6]. The telomere bouquet does function in alignment of chromosomes but is crucial for the recruitment of a chromosome to the SPB to create a functional meiotic spindle
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