Time-lapse single-cell transcriptomics reveals modulation of histone H3 for dormancy breaking

Hayato Tsuyuzaki; Masahito Hosokawa; Koji Arikawa; Takuya Yoda; Naoyuki Okada; Haruko Takeyama; Masamitsu Sato

doi:10.1101/720680

Time-lapse single-cell transcriptomics reveals modulation of histone H3 for dormancy breaking

Hayato Tsuyuzaki, Masahito Hosokawa, Koji Arikawa, Takuya Yoda, Naoyuki Okada, Haruko Takeyama, Masamitsu Sato

School of Advanced Science and Engineering

Research output: Contribution to journal › Article › peer-review

Abstract

How quiescent cells break dormancy is a key issue in eukaryotic cells including cancer. Fungal spores, for example, remain quiescent for long periods until nourished, although the mechanisms by which dormancy is broken remain enigmatic. Transcriptome analysis could provide a clue, but methods to synchronously germinate large numbers of spores are lacking, and thus it remains a challenge to analyse gene expression upon germination. Hence, we developed methods to assemble transcriptomes from individual, asynchronous spore cells of fission yeast undergoing germination to assess transcriptomic changes over time. The virtual time-lapse analyses highlighted one of three copies of histone H3 genes for which transcription fluctuates during the initial stage of germination. Disruption of this temporal fluctuation caused defects in spore germination despite no visible defects in other stages of the life cycle. We conclude that modulation of histone H3 expression is a crucial ‘wake-up’ trigger at dormancy breaking.

Original language	English
Journal	Unknown Journal
DOIs	https://doi.org/10.1101/720680
Publication status	Published - 2019 Aug 5

ASJC Scopus subject areas

Biochemistry, Genetics and Molecular Biology(all)
Agricultural and Biological Sciences(all)
Immunology and Microbiology(all)
Neuroscience(all)
Pharmacology, Toxicology and Pharmaceutics(all)

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title = "Time-lapse single-cell transcriptomics reveals modulation of histone H3 for dormancy breaking",

abstract = "How quiescent cells break dormancy is a key issue in eukaryotic cells including cancer. Fungal spores, for example, remain quiescent for long periods until nourished, although the mechanisms by which dormancy is broken remain enigmatic. Transcriptome analysis could provide a clue, but methods to synchronously germinate large numbers of spores are lacking, and thus it remains a challenge to analyse gene expression upon germination. Hence, we developed methods to assemble transcriptomes from individual, asynchronous spore cells of fission yeast undergoing germination to assess transcriptomic changes over time. The virtual time-lapse analyses highlighted one of three copies of histone H3 genes for which transcription fluctuates during the initial stage of germination. Disruption of this temporal fluctuation caused defects in spore germination despite no visible defects in other stages of the life cycle. We conclude that modulation of histone H3 expression is a crucial {\textquoteleft}wake-up{\textquoteright} trigger at dormancy breaking.",

author = "Hayato Tsuyuzaki and Masahito Hosokawa and Koji Arikawa and Takuya Yoda and Naoyuki Okada and Haruko Takeyama and Masamitsu Sato",

note = "Publisher Copyright: The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. Copyright: Copyright 2020 Elsevier B.V., All rights reserved.",

year = "2019",

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journal = "Nuclear Physics A",

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AU - Tsuyuzaki, Hayato

AU - Hosokawa, Masahito

AU - Arikawa, Koji

AU - Yoda, Takuya

AU - Okada, Naoyuki

AU - Takeyama, Haruko

AU - Sato, Masamitsu

N1 - Publisher Copyright: The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. Copyright: Copyright 2020 Elsevier B.V., All rights reserved.

PY - 2019/8/5

Y1 - 2019/8/5

N2 - How quiescent cells break dormancy is a key issue in eukaryotic cells including cancer. Fungal spores, for example, remain quiescent for long periods until nourished, although the mechanisms by which dormancy is broken remain enigmatic. Transcriptome analysis could provide a clue, but methods to synchronously germinate large numbers of spores are lacking, and thus it remains a challenge to analyse gene expression upon germination. Hence, we developed methods to assemble transcriptomes from individual, asynchronous spore cells of fission yeast undergoing germination to assess transcriptomic changes over time. The virtual time-lapse analyses highlighted one of three copies of histone H3 genes for which transcription fluctuates during the initial stage of germination. Disruption of this temporal fluctuation caused defects in spore germination despite no visible defects in other stages of the life cycle. We conclude that modulation of histone H3 expression is a crucial ‘wake-up’ trigger at dormancy breaking.

AB - How quiescent cells break dormancy is a key issue in eukaryotic cells including cancer. Fungal spores, for example, remain quiescent for long periods until nourished, although the mechanisms by which dormancy is broken remain enigmatic. Transcriptome analysis could provide a clue, but methods to synchronously germinate large numbers of spores are lacking, and thus it remains a challenge to analyse gene expression upon germination. Hence, we developed methods to assemble transcriptomes from individual, asynchronous spore cells of fission yeast undergoing germination to assess transcriptomic changes over time. The virtual time-lapse analyses highlighted one of three copies of histone H3 genes for which transcription fluctuates during the initial stage of germination. Disruption of this temporal fluctuation caused defects in spore germination despite no visible defects in other stages of the life cycle. We conclude that modulation of histone H3 expression is a crucial ‘wake-up’ trigger at dormancy breaking.

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