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Subcellular analyses of planarian meiosis implicates a novel, double-membraned vesiculation process in nuclear envelope breakdown

Longhua Guo, View ORCID ProfileFengli Guo, Shasha Zhang, Kexi Yi, Melainia McClain, Claus-D. Kuhn, Tari Parmely, View ORCID ProfileAlejandro Sánchez Alvarado
doi: https://doi.org/10.1101/620609
Longhua Guo
1Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
4University of California Los Angeles (UCLA), Los Angeles, California 90095, USA
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  • For correspondence: longhuaguo@mednet.ucla.edu asa@stowers.org
Fengli Guo
1Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
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  • ORCID record for Fengli Guo
Shasha Zhang
1Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
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Kexi Yi
1Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
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Melainia McClain
1Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
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Claus-D. Kuhn
3Gene regulation by Non-coding RNA, Elite Network of Bavaria and University of Bayreuth, Universitätsstrasse 30, Bayreuth 95447, Germany
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Tari Parmely
1Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
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Alejandro Sánchez Alvarado
1Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
2Howard Hughes Medical Institute, Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
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  • ORCID record for Alejandro Sánchez Alvarado
  • For correspondence: longhuaguo@mednet.ucla.edu asa@stowers.org
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Abstract

The cell nuclei of Ophisthokonts, the eukaryotic supergroup defined by fungi and metazoans, is remarkable in the constancy of both their double-membraned structure and protein composition. Such remarkable structural conservation underscores common and ancient evolutionary origins. Yet, the dynamics of disassembly and reassembly displayed by Ophisthokont nuclei vary extensively. Besides closed mitosis in fungi and open mitosis in some animals, little is known about the evolution of nuclear envelope break down (NEBD) during cell division. Here, we uncovered a novel form of NEBD in primary oocytes of the flatworm Schmidtea mediterranea. From zygotene to metaphase II, both nuclear envelope (NE) and peripheral endoplasmic reticulum (ER) expand notably in size, likely involving de novo membrane synthesis. 3-D electron microscopy reconstructions demonstrated that the NE transforms itself into numerous double-membraned vesicles similar in membrane architecture to NE doublets in mammalian oocytes after germinal vesicle breakdown. The vesicles are devoid of nuclear pore complexes and DNA, yet are loaded with nuclear proteins, including a planarian homologue of PIWI, a protein essential for the maintenance of stem cells in this and other organisms. Our data contribute a new model to the canonical view of NE dynamics and support that NEBD is an evolutionarily adaptable trait in multicellular organisms.

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Posted May 05, 2019.
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Subcellular analyses of planarian meiosis implicates a novel, double-membraned vesiculation process in nuclear envelope breakdown
Longhua Guo, Fengli Guo, Shasha Zhang, Kexi Yi, Melainia McClain, Claus-D. Kuhn, Tari Parmely, Alejandro Sánchez Alvarado
bioRxiv 620609; doi: https://doi.org/10.1101/620609
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Subcellular analyses of planarian meiosis implicates a novel, double-membraned vesiculation process in nuclear envelope breakdown
Longhua Guo, Fengli Guo, Shasha Zhang, Kexi Yi, Melainia McClain, Claus-D. Kuhn, Tari Parmely, Alejandro Sánchez Alvarado
bioRxiv 620609; doi: https://doi.org/10.1101/620609

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