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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...

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Autores principales: Zhang, Bowen, Teraguchi, Erika, Imada, Kazuki, Tahara, Yuhei O., Nakamura, Shuko, Miyata, Makoto, Kagiwada, Satoshi, Nakamura, Taro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
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.
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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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