Building the meiotic bouquet: A nuclear polarity pathway in Arabidopsis

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ABSTRACT Meiotic chromosome pairing requires the establishment of a polarized nuclear architecture, but how this polarity emerges from the interplay of telomeres, the nucleolus, and the nuclear envelope remains incompletely understood in plants. Using stage-resolved three-dimensional imaging of intact Arabidopsis thaliana male meiocytes, we reconstruct the early meiotic sequence that links the premeiotic chromosome arrangement to telomere bouquet formation. We show that telomeres enter meiosis positioned around the nucleolus and, at the onset of leptotene, undergo a coordinated and directionally biased departure from the nucleolar surface. This transition establishes asymmetric early contacts with discrete SUN1/2-enriched domains of the nuclear envelope, well before visible clustering occurs, revealing that the envelope is pre-patterned into regions permissive for telomere attachment. As zygotene progresses, these early contacts consolidate into a nucleolus-associated bouquet, whereas the nucleolar organizer regions (NORs) maintain a stable position and remain unsynapsed. Centromeres reorganize in parallel and progressively shift away from the developing telomere domain, giving rise to the classical centromere–telomere opposition. Rare nuclei exhibiting bouquet formation opposite the nucleolus correspond to alternative SUN1/2 microdomain topologies, indicating that nuclear-envelope patterning, rather than telomere behavior, ultimately determines the polarity state. Together, these findings provide a mechanistic framework in which NOR stability, SUN-patterned membrane domains, and telomere migration act sequentially to generate a polarized meiotic nucleus in Arabidopsis.

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