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The Fission Yeast RNA-Binding Protein Meu5 Is Involved in Outer Forespore Membrane Breakdown during Spore Formation
In Schizosaccharomyces pombe, the spore wall confers strong resistance against external stress. During meiosis II, the double-layered intracellular forespore membrane (FSM) forms de novo and encapsulates the nucleus. Eventually, the inner FSM layer becomes the plasma membrane of the spore, while the...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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MDPI
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7712723/ https://www.ncbi.nlm.nih.gov/pubmed/33202882 http://dx.doi.org/10.3390/jof6040284 |
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author | Zhang, Bowen Teraguchi, Erika Imada, Kazuki Tahara, Yuhei O. Nakamura, Shuko Miyata, Makoto Kagiwada, Satoshi Nakamura, Taro |
author_facet | Zhang, Bowen Teraguchi, Erika Imada, Kazuki Tahara, Yuhei O. Nakamura, Shuko Miyata, Makoto Kagiwada, Satoshi Nakamura, Taro |
author_sort | Zhang, Bowen |
collection | PubMed |
description | In Schizosaccharomyces pombe, the spore wall confers strong resistance against external stress. During meiosis II, the double-layered intracellular forespore membrane (FSM) forms de novo and encapsulates the nucleus. Eventually, the inner FSM layer becomes the plasma membrane of the spore, while the outer layer breaks down. However, the molecular mechanism and biological significance of this membrane breakdown remain unknown. Here, by genetic investigation of an S. pombe mutant (E22) with normal prespore formation but abnormal spores, we showed that Meu5, an RNA-binding protein known to bind to and stabilize more than 80 transcripts, is involved in this process. We confirmed that the E22 mutant does not produce Meu5 protein, while overexpression of meu5(+) in E22 restores the sporulation defect. Furthermore, electron microscopy revealed that the outer membrane of the FSM persisted in meu5∆ spores. Investigation of the target genes of meu5(+) showed that a mutant of cyc1(+) encoding cytochrome c also showed a severe defect in outer FSM breakdown. Lastly, we determined that outer FSM breakdown occurs coincident with or after formation of the outermost Isp3 layer of the spore wall. Collectively, our data provide novel insights into the molecular mechanism of spore formation. |
format | Online Article Text |
id | pubmed-7712723 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | MDPI |
record_format | MEDLINE/PubMed |
spelling | pubmed-77127232020-12-04 The Fission Yeast RNA-Binding Protein Meu5 Is Involved in Outer Forespore Membrane Breakdown during Spore Formation Zhang, Bowen Teraguchi, Erika Imada, Kazuki Tahara, Yuhei O. Nakamura, Shuko Miyata, Makoto Kagiwada, Satoshi Nakamura, Taro J Fungi (Basel) Article In Schizosaccharomyces pombe, the spore wall confers strong resistance against external stress. During meiosis II, the double-layered intracellular forespore membrane (FSM) forms de novo and encapsulates the nucleus. Eventually, the inner FSM layer becomes the plasma membrane of the spore, while the outer layer breaks down. However, the molecular mechanism and biological significance of this membrane breakdown remain unknown. Here, by genetic investigation of an S. pombe mutant (E22) with normal prespore formation but abnormal spores, we showed that Meu5, an RNA-binding protein known to bind to and stabilize more than 80 transcripts, is involved in this process. We confirmed that the E22 mutant does not produce Meu5 protein, while overexpression of meu5(+) in E22 restores the sporulation defect. Furthermore, electron microscopy revealed that the outer membrane of the FSM persisted in meu5∆ spores. Investigation of the target genes of meu5(+) showed that a mutant of cyc1(+) encoding cytochrome c also showed a severe defect in outer FSM breakdown. Lastly, we determined that outer FSM breakdown occurs coincident with or after formation of the outermost Isp3 layer of the spore wall. Collectively, our data provide novel insights into the molecular mechanism of spore formation. MDPI 2020-11-13 /pmc/articles/PMC7712723/ /pubmed/33202882 http://dx.doi.org/10.3390/jof6040284 Text en © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/). |
spellingShingle | Article Zhang, Bowen Teraguchi, Erika Imada, Kazuki Tahara, Yuhei O. Nakamura, Shuko Miyata, Makoto Kagiwada, Satoshi Nakamura, Taro The Fission Yeast RNA-Binding Protein Meu5 Is Involved in Outer Forespore Membrane Breakdown during Spore Formation |
title | The Fission Yeast RNA-Binding Protein Meu5 Is Involved in Outer Forespore Membrane Breakdown during Spore Formation |
title_full | The Fission Yeast RNA-Binding Protein Meu5 Is Involved in Outer Forespore Membrane Breakdown during Spore Formation |
title_fullStr | The Fission Yeast RNA-Binding Protein Meu5 Is Involved in Outer Forespore Membrane Breakdown during Spore Formation |
title_full_unstemmed | The Fission Yeast RNA-Binding Protein Meu5 Is Involved in Outer Forespore Membrane Breakdown during Spore Formation |
title_short | The Fission Yeast RNA-Binding Protein Meu5 Is Involved in Outer Forespore Membrane Breakdown during Spore Formation |
title_sort | fission yeast rna-binding protein meu5 is involved in outer forespore membrane breakdown during spore formation |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7712723/ https://www.ncbi.nlm.nih.gov/pubmed/33202882 http://dx.doi.org/10.3390/jof6040284 |
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