Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana

Abstract

The intranuclear arrangements of centromeres and telomeres during meiotic interphase and early prophase I of meiosis in Arabidopsis thaliana were analysed by fluorescent in situ hybridisation to spread pollen mother cells and embryo-sac mother cells. Meiocyte identification, staging and progression were established by spreading and sectioning techniques, including various staining procedures and bromodeoxyuridine labeling of replicating DNA. Centromere regions of Arabidopsis are unpaired, widely dispersed and peripherally located in nuclei during meiotic interphase, and they remain unpaired and unassociated throughout leptotene. Eventually they associate pairwise during zygotene, as part of the nucleus-wide synapsis of homologous chromosomes. Telomeres, by contrast, show a persistent association with the nucleolus throughout meiotic interphase. Variation in telomere signal number indicates that telomeres undergo pairing during this interval, preceding the onset of general chromosome synapsis. During leptotene the paired telomeres lose their association with the nucleolus and become widely dispersed. As the chromosomes synapse during zygotene, the telomeres reveal a loose clustering within one hemisphere, which may represent a degenerate or relic bouquet configuration. We propose that in Arabidopsis the classical leptotene/zygotene bouquet is absent and is replaced functionally by nucleolus-associated telomere clustering.