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Cited by 47Genomics and Chromatin DynamicsRNA Research and SplicingGene Regulatory Network Analysis

High-resolution analysis of cell-state transitions in yeast suggests widespread transcriptional tuning by alternative starts

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Chia, Minghao, Li, Cai, Marques, Sueli, Pelechano, Vicente, Luscombe, Nicholas M., van Werven, Folkert J.·2021·Genome Biology
DOI 10.1186/s13059-020-02245-3PMC PMC7807719
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Abstract

Background: The start and end sites of messenger RNAs (TSSs and TESs) are highly regulated, often in a cell-type-specific manner. Yet the contribution of transcript diversity in regulating gene expression remains largely elusive. We perform an integrative analysis of multiple highly synchronized cell-fate transitions and quantitative genomic techniques in Saccharomyces cerevisiae to identify regulatory functions associated with transcribing alternative isoforms. Results: Cell-fate transitions feature widespread elevated expression of alternative TSS and, to a lesser degree, TES usage. These dynamically regulated alternative TSSs are located mostly upstream of canonical TSSs, but also within gene bodies possibly encoding for protein isoforms. Increased upstream alternative TSS usage is linked to various effects on canonical TSS levels, which range from co-activation to repression. We identified two key features linked to these outcomes: an interplay between alternative and canonical promoter strengths, and distance between alternative and canonical TSSs. These two regulatory properties give a plausible explanation of how locally transcribed alternative TSSs control gene transcription. Additionally, we find that specific chromatin modifiers Set2, Set3, and FACT play an important role in mediating gene repression via alternative TSSs, further supporting that the act of upstream transcription drives the local changes in gene transcription. Conclusions: The integrative analysis of multiple cell-fate transitions suggests the presence of a regulatory control system of alternative TSSs that is important for dynamic tuning of gene expression. Our work provides a framework for understanding how TSS heterogeneity governs eukaryotic gene expression, particularly during cell-fate changes.

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Authors
Chia, M., Li, C., Marques, S., Pelechano, V., Luscombe, N. M., & van Werven, F. J.
Affiliations
  • The Francis Crick Institute (GB)
  • Science for Life Laboratory (SE)
  • Okinawa Institute of Science and Technology Graduate University (JP)
ORCID
Venue
Genome Biology
Publisher
Springer Science and Business Media LLC
Published
2021-01-14
Volume
22
Issue
1
Pages
34-34
ISSN
  • 1465-6906 (ISSN-L)
  • 1474-760X
DOI
10.1186/s13059-020-02245-3
PMC
PMC7807719
OpenAlex
W3123778796
Cited by
47
References
0
Citations by year
2026: 4 · 2025: 5 · 2024: 7 · 2023: 11 · 2022: 13 · 2021: 7
FWCI
2.98
Type
journal article
Language
en
Update notices
correction (2021-01-25)
Open access
Licence
Locations
  • Genome biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Institutional Repositories DataBase (IRDB) (submittedVersion, cc-by-nc-nd)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • UCL Discovery (University College London) (submittedVersion)
  • Figshare (submittedVersion, cc-by)
  • Okinawa Institute of Science and Technology Graduate University (Okinawa Institute of Science and Technology Graduate University) (submittedVersion, cc-by-nc-nd)
Funders
  • Medical Research Foundation (10203, FC001110)
  • Wellcome Trust (10203, FC001110)
  • Cancer Research UK (10203, FC001110)
  • European Molecular Biology Organization (ALTF 1499–2016)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
Keywords
alternative transcription start sites, cell fate transitions, cell state transitions, Saccharomyces cerevisiae, promoter strength, gene expression regulation, gene repression, chromatin modifiers, Set2, FACT complex, mRNA isoforms
MeSH terms
Chromatin, Promoter Regions, Genetic, RNA, Messenger, Saccharomyces cerevisiae, Transcription Factors, Gene Expression Regulation, Fungal, Protein Isoforms, Transcriptome

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