A conserved disruption of nucleocytoplasmic compartmentalization in meiosis is controlled by a kinase-phosphatase pair in Saccharomyces cerevisiae
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a-conserved-disruption-of-nucleocytoplasmic-compartmentalization-in-meiosis-is-controlled-by-a-kinase-phosphatase-pair.pdf
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Published version
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9.99 MB
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Checksum (MD5)
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Author(s)
Walsh, Madison E
Chetlapalli, Keerthana
Styler, Benjamin S
Upadhyayula, Srigokul
King, Grant A
Ünal, Elçin
Date Issued
December 1, 2025
Journal
Molecular Biology of the Cell
Publisher
American Society for Cell Biology (ASCB)
Citation
Walsh, Madison E, Chetlapalli, Keerthana, Styler, Benjamin S, Upadhyayula, Srigokul, King, Grant A et al. 2025. "A conserved disruption of nucleocytoplasmic compartmentalization in meiosis is controlled by a kinase-phosphatase pair in Saccharomyces cerevisiae." Molecular Biology of the Cell, 36 (12).
Version
Final published version
Abstract
In eukaryotic organisms, the nucleus is remodeled to accommodate the space required for chromosome segregation. Remodeling strategies range from closed division, where the nuclear envelope remains intact, to open division, where the nuclear envelope is temporarily disassembled. While the budding yeast Saccharomyces cerevisiae (S. cerevisiae) undergoes closed mitosis, its meiotic nuclear division strategy is less understood. Here, we investigate nucleocytoplasmic compartmentalization during budding yeast meiosis and discover that meiosis II represents a semi-closed division marked by bidirectional mixing between the nucleus and cytoplasm. This includes nuclear entry of the Ran GTPase activating protein (RanGAP), typically cytoplasmic, although RanGAP relocalization appears to be a consequence, rather than a cause of permeability changes. This intercompartmental mixing occurs without nuclear envelope breakdown or dispersal of nucleoporins and is independent of known nuclear pore complex remodeling events. This phenomenon, termed virtual nuclear envelope breakdown (vNEBD), represents a unique mechanism distinct from other semi-closed divisions. We demonstrate that vNEBD is integrated into the meiotic program and regulated by the conserved meiotic kinase Ime2, and the meiosis-specific protein phosphatase 1 regulatory subunit, Gip1. Remarkably, the vNEBD event is conserved between S. cerevisiae and the distantly related Schizosaccharomyces pombe (S. pombe), indicating a fundamental role in meiosis.
MIT Department
Massachusetts Institute of Technology. Department of Biology
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DOI of Published Version
https://doi.org/10.1091/mbc.E25-05-0229
