Quantitative imaging of RNA polymerase II activity in plants reveals the single-cell basis of tissue-wide transcriptional dynamics.


Journal

Nature plants
ISSN: 2055-0278
Titre abrégé: Nat Plants
Pays: England
ID NLM: 101651677

Informations de publication

Date de publication:
08 2021
Historique:
received: 15 10 2020
accepted: 22 06 2021
pubmed: 11 8 2021
medline: 24 9 2021
entrez: 10 8 2021
Statut: ppublish

Résumé

The responses of plants to their environment are often dependent on the spatiotemporal dynamics of transcriptional regulation. While live-imaging tools have been used extensively to quantitatively capture rapid transcriptional dynamics in living animal cells, the lack of implementation of these technologies in plants has limited concomitant quantitative studies in this kingdom. Here, we applied the PP7 and MS2 RNA-labelling technologies for the quantitative imaging of RNA polymerase II activity dynamics in single cells of living plants as they respond to experimental treatments. Using this technology, we counted nascent RNA transcripts in real time in Nicotiana benthamiana (tobacco) and Arabidopsis thaliana. Examination of heat shock reporters revealed that plant tissues respond to external signals by modulating the proportion of cells that switch from an undetectable basal state to a high-transcription state, instead of modulating the rate of transcription across all cells in a graded fashion. This switch-like behaviour, combined with cell-to-cell variability in transcription rate, results in mRNA production variability spanning three orders of magnitude. We determined that cellular heterogeneity stems mainly from stochasticity intrinsic to individual alleles instead of variability in cellular composition. Together, our results demonstrate that it is now possible to quantitatively study the dynamics of transcriptional programs in single cells of living plants.

Identifiants

pubmed: 34373604
doi: 10.1038/s41477-021-00976-0
pii: 10.1038/s41477-021-00976-0
pmc: PMC8616715
mid: NIHMS1737891
doi:

Substances chimiques

RNA, Messenger 0
RNA Polymerase II EC 2.7.7.-

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1037-1049

Subventions

Organisme : NICHD NIH HHS
ID : DP2 HD094655
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2021. The Author(s), under exclusive licence to Springer Nature Limited.

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Auteurs

Simon Alamos (S)

Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA, USA.

Armando Reimer (A)

Biophysics Graduate Group, University of California Berkeley, Berkeley, CA, USA.

Krishna K Niyogi (KK)

Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA, USA. niyogi@berkeley.edu.
Howard Hughes Medical Institute, University of California Berkeley, Berkeley, CA, USA. niyogi@berkeley.edu.
Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA. niyogi@berkeley.edu.

Hernan G Garcia (HG)

Biophysics Graduate Group, University of California Berkeley, Berkeley, CA, USA. hggarcia@berkeley.edu.
Department of Molecular and Cell Biology, University of California Berkeley, Berkeley, CA, USA. hggarcia@berkeley.edu.
Department of Physics, University of California Berkeley, Berkeley, CA, USA. hggarcia@berkeley.edu.
Institute for Quantitative Biosciences-QB3, University of California Berkeley, Berkeley, CA, USA. hggarcia@berkeley.edu.

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Classifications MeSH