Cargando…
Integrating analog and digital modes of gene expression at Arabidopsis FLC
Quantitative gene regulation at the cell population level can be achieved by two fundamentally different modes of regulation at individual gene copies. A ‘digital’ mode involves binary ON/OFF expression states, with population-level variation arising from the proportion of gene copies in each state,...
Autores principales: | , , , , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2023
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10356135/ https://www.ncbi.nlm.nih.gov/pubmed/37466633 http://dx.doi.org/10.7554/eLife.79743 |
_version_ | 1785075204267966464 |
---|---|
author | Antoniou-Kourounioti, Rea L Meschichi, Anis Reeck, Svenja Berry, Scott Menon, Govind Zhao, Yusheng Fozard, John Holmes, Terri Zhao, Lihua Wang, Huamei Hartley, Matthew Dean, Caroline Rosa, Stefanie Howard, Martin |
author_facet | Antoniou-Kourounioti, Rea L Meschichi, Anis Reeck, Svenja Berry, Scott Menon, Govind Zhao, Yusheng Fozard, John Holmes, Terri Zhao, Lihua Wang, Huamei Hartley, Matthew Dean, Caroline Rosa, Stefanie Howard, Martin |
author_sort | Antoniou-Kourounioti, Rea L |
collection | PubMed |
description | Quantitative gene regulation at the cell population level can be achieved by two fundamentally different modes of regulation at individual gene copies. A ‘digital’ mode involves binary ON/OFF expression states, with population-level variation arising from the proportion of gene copies in each state, while an ‘analog’ mode involves graded expression levels at each gene copy. At the Arabidopsis floral repressor FLOWERING LOCUS C (FLC), ‘digital’ Polycomb silencing is known to facilitate quantitative epigenetic memory in response to cold. However, whether FLC regulation before cold involves analog or digital modes is unknown. Using quantitative fluorescent imaging of FLC mRNA and protein, together with mathematical modeling, we find that FLC expression before cold is regulated by both analog and digital modes. We observe a temporal separation between the two modes, with analog preceding digital. The analog mode can maintain intermediate expression levels at individual FLC gene copies, before subsequent digital silencing, consistent with the copies switching OFF stochastically and heritably without cold. This switch leads to a slow reduction in FLC expression at the cell population level. These data present a new paradigm for gradual repression, elucidating how analog transcriptional and digital epigenetic memory pathways can be integrated. |
format | Online Article Text |
id | pubmed-10356135 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
spelling | pubmed-103561352023-07-20 Integrating analog and digital modes of gene expression at Arabidopsis FLC Antoniou-Kourounioti, Rea L Meschichi, Anis Reeck, Svenja Berry, Scott Menon, Govind Zhao, Yusheng Fozard, John Holmes, Terri Zhao, Lihua Wang, Huamei Hartley, Matthew Dean, Caroline Rosa, Stefanie Howard, Martin eLife Chromosomes and Gene Expression Quantitative gene regulation at the cell population level can be achieved by two fundamentally different modes of regulation at individual gene copies. A ‘digital’ mode involves binary ON/OFF expression states, with population-level variation arising from the proportion of gene copies in each state, while an ‘analog’ mode involves graded expression levels at each gene copy. At the Arabidopsis floral repressor FLOWERING LOCUS C (FLC), ‘digital’ Polycomb silencing is known to facilitate quantitative epigenetic memory in response to cold. However, whether FLC regulation before cold involves analog or digital modes is unknown. Using quantitative fluorescent imaging of FLC mRNA and protein, together with mathematical modeling, we find that FLC expression before cold is regulated by both analog and digital modes. We observe a temporal separation between the two modes, with analog preceding digital. The analog mode can maintain intermediate expression levels at individual FLC gene copies, before subsequent digital silencing, consistent with the copies switching OFF stochastically and heritably without cold. This switch leads to a slow reduction in FLC expression at the cell population level. These data present a new paradigm for gradual repression, elucidating how analog transcriptional and digital epigenetic memory pathways can be integrated. eLife Sciences Publications, Ltd 2023-07-19 /pmc/articles/PMC10356135/ /pubmed/37466633 http://dx.doi.org/10.7554/eLife.79743 Text en © 2023, Antoniou-Kourounioti, Meschichi, Reeck et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited. |
spellingShingle | Chromosomes and Gene Expression Antoniou-Kourounioti, Rea L Meschichi, Anis Reeck, Svenja Berry, Scott Menon, Govind Zhao, Yusheng Fozard, John Holmes, Terri Zhao, Lihua Wang, Huamei Hartley, Matthew Dean, Caroline Rosa, Stefanie Howard, Martin Integrating analog and digital modes of gene expression at Arabidopsis FLC |
title | Integrating analog and digital modes of gene expression at Arabidopsis FLC |
title_full | Integrating analog and digital modes of gene expression at Arabidopsis FLC |
title_fullStr | Integrating analog and digital modes of gene expression at Arabidopsis FLC |
title_full_unstemmed | Integrating analog and digital modes of gene expression at Arabidopsis FLC |
title_short | Integrating analog and digital modes of gene expression at Arabidopsis FLC |
title_sort | integrating analog and digital modes of gene expression at arabidopsis flc |
topic | Chromosomes and Gene Expression |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10356135/ https://www.ncbi.nlm.nih.gov/pubmed/37466633 http://dx.doi.org/10.7554/eLife.79743 |
work_keys_str_mv | AT antonioukourouniotireal integratinganaloganddigitalmodesofgeneexpressionatarabidopsisflc AT meschichianis integratinganaloganddigitalmodesofgeneexpressionatarabidopsisflc AT reecksvenja integratinganaloganddigitalmodesofgeneexpressionatarabidopsisflc AT berryscott integratinganaloganddigitalmodesofgeneexpressionatarabidopsisflc AT menongovind integratinganaloganddigitalmodesofgeneexpressionatarabidopsisflc AT zhaoyusheng integratinganaloganddigitalmodesofgeneexpressionatarabidopsisflc AT fozardjohn integratinganaloganddigitalmodesofgeneexpressionatarabidopsisflc AT holmesterri integratinganaloganddigitalmodesofgeneexpressionatarabidopsisflc AT zhaolihua integratinganaloganddigitalmodesofgeneexpressionatarabidopsisflc AT wanghuamei integratinganaloganddigitalmodesofgeneexpressionatarabidopsisflc AT hartleymatthew integratinganaloganddigitalmodesofgeneexpressionatarabidopsisflc AT deancaroline integratinganaloganddigitalmodesofgeneexpressionatarabidopsisflc AT rosastefanie integratinganaloganddigitalmodesofgeneexpressionatarabidopsisflc AT howardmartin integratinganaloganddigitalmodesofgeneexpressionatarabidopsisflc |