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Characterizing nuclear remodeling during budding yeast meiosis


The nucleus, the defining organelle of the eukaryotic cell, must be remodeled during every cell division in order to accommodate the division of genetic material. While this remodeling has been extensively studied during mitosis, it remains poorly understood how the nucleus is remodeled during meiosis. In this study, we provide a comprehensive analysis of nuclear behavior during meiosis in the model organism budding yeast. First, we find that the nuclear envelope undergoes a five-way division, forming a nuclear-envelope bound compartment that is excluded from gametes. This compartment, termed the Gametogenesis Uninherited Nuclear Compartment or GUNC, contains nuclear pore complexes (NPCs) in all cells and age-induced damage in old cells. The material sequestered to the GUNC is subsequently eliminated by release of vacuolar proteases, establishing this remodeling event as a novel nuclear quality control mechanism that contributes to meiotic cellular rejuvenation. Second, we find that the NPC undergoes two mechanistically-distinct meiotic remodeling events: partial nuclear basket detachment during meiosis I and full nuclear basket detachment during meiosis II. Meiosis I detachment, which involves Nup60 and its binding partner Nup2, is driven by Polo kinase-dependent phosphorylation of Nup60 at its binding interface with the NPC core. Notably, this remodeling event also occurs in the distantly related Schizosaccharomyces pombe, suggesting basket detachment involves conserved nuclear basket organizational principles and fulfills an important function. Finally, we find that the nuclear permeability barrier is transiently disrupted during meiosis II, driving intermixing of the cytoplasm and nucleoplasm. Since the nuclear envelope stays intact throughout meiosis, regulation of nuclear transport machinery is likely involved in this event. Several meiotic regulators disrupt barrier loss or return, although their precise mechanistic contributions remain unclear. In all, this work establishes the nuclear periphery as a highly dynamic and regulated entity during budding yeast meiosis. Studying the budding yeast meiotic nucleus will continue to improve our understanding of nuclear organization and its contributions to cellular health for years to come.

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