Hyperosmotic Stress Response Memory is Modulated by Gene Positioning in Yeast

Cellular memory is a critical ability that allows microorganisms to adapt to potentially detrimental environmental fluctuations. In the unicellular eukaryote <i>Saccharomyces cerevisiae</i>, cellular memory can take the form of faster or slower responses within the cell population to rep...

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Published in:Cells
Main Authors: Zacchari Ben Meriem, Yasmine Khalil, Pascal Hersen, Emmanuelle Fabre
Format: Article
Language:English
Published: MDPI AG 2019-06-01
Subjects:
Online Access:https://www.mdpi.com/2073-4409/8/6/582
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author Zacchari Ben Meriem
Yasmine Khalil
Pascal Hersen
Emmanuelle Fabre
author_facet Zacchari Ben Meriem
Yasmine Khalil
Pascal Hersen
Emmanuelle Fabre
author_sort Zacchari Ben Meriem
collection DOAJ
container_title Cells
description Cellular memory is a critical ability that allows microorganisms to adapt to potentially detrimental environmental fluctuations. In the unicellular eukaryote <i>Saccharomyces cerevisiae</i>, cellular memory can take the form of faster or slower responses within the cell population to repeated stresses. Using microfluidics and fluorescence time-lapse microscopy, we studied how yeast responds to short, pulsed hyperosmotic stresses at the single-cell level by analyzing the dynamic behavior of the stress-responsive <i>STL1</i> promoter (pSTL1) fused to a fluorescent reporter. We established that pSTL1 exhibits variable successive activation patterns following two repeated short stresses. Despite this variability, most cells exhibited a memory of the first stress as decreased pSTL1 activity in response to the second stress. Notably, we showed that genomic location is important for the memory effect, since displacement of the promoter to a pericentromeric chromatin domain decreased the transcriptional strength of pSTL1 and led to a loss of memory. This study provides a quantitative description of a cellular memory that includes single-cell variability and highlights the contribution of chromatin structure to stress memory.
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spelling doaj-art-ca015c9b117c4635bc0a5fd86fc0adbd2025-08-19T20:39:19ZengMDPI AGCells2073-44092019-06-018658210.3390/cells8060582cells8060582Hyperosmotic Stress Response Memory is Modulated by Gene Positioning in YeastZacchari Ben Meriem0Yasmine Khalil1Pascal Hersen2Emmanuelle Fabre3Université de Paris, Laboratoire Matière et Systèmes Complexes, CNRS UMR 7057, F-75013 Paris, FranceUniversité de Paris, Laboratoire Génomes, Biologie Cellulaire et Thérapeutiques, CNRS UMR7212, INSERM U944, Centre de Recherche St Louis, F- 75010 Paris, FranceUniversité de Paris, Laboratoire Matière et Systèmes Complexes, CNRS UMR 7057, F-75013 Paris, FranceUniversité de Paris, Laboratoire Génomes, Biologie Cellulaire et Thérapeutiques, CNRS UMR7212, INSERM U944, Centre de Recherche St Louis, F- 75010 Paris, FranceCellular memory is a critical ability that allows microorganisms to adapt to potentially detrimental environmental fluctuations. In the unicellular eukaryote <i>Saccharomyces cerevisiae</i>, cellular memory can take the form of faster or slower responses within the cell population to repeated stresses. Using microfluidics and fluorescence time-lapse microscopy, we studied how yeast responds to short, pulsed hyperosmotic stresses at the single-cell level by analyzing the dynamic behavior of the stress-responsive <i>STL1</i> promoter (pSTL1) fused to a fluorescent reporter. We established that pSTL1 exhibits variable successive activation patterns following two repeated short stresses. Despite this variability, most cells exhibited a memory of the first stress as decreased pSTL1 activity in response to the second stress. Notably, we showed that genomic location is important for the memory effect, since displacement of the promoter to a pericentromeric chromatin domain decreased the transcriptional strength of pSTL1 and led to a loss of memory. This study provides a quantitative description of a cellular memory that includes single-cell variability and highlights the contribution of chromatin structure to stress memory.https://www.mdpi.com/2073-4409/8/6/582chromosome organizationcellular memorysingle cellstress responseyeast
spellingShingle Zacchari Ben Meriem
Yasmine Khalil
Pascal Hersen
Emmanuelle Fabre
Hyperosmotic Stress Response Memory is Modulated by Gene Positioning in Yeast
chromosome organization
cellular memory
single cell
stress response
yeast
title Hyperosmotic Stress Response Memory is Modulated by Gene Positioning in Yeast
title_full Hyperosmotic Stress Response Memory is Modulated by Gene Positioning in Yeast
title_fullStr Hyperosmotic Stress Response Memory is Modulated by Gene Positioning in Yeast
title_full_unstemmed Hyperosmotic Stress Response Memory is Modulated by Gene Positioning in Yeast
title_short Hyperosmotic Stress Response Memory is Modulated by Gene Positioning in Yeast
title_sort hyperosmotic stress response memory is modulated by gene positioning in yeast
topic chromosome organization
cellular memory
single cell
stress response
yeast
url https://www.mdpi.com/2073-4409/8/6/582
work_keys_str_mv AT zaccharibenmeriem hyperosmoticstressresponsememoryismodulatedbygenepositioninginyeast
AT yasminekhalil hyperosmoticstressresponsememoryismodulatedbygenepositioninginyeast
AT pascalhersen hyperosmoticstressresponsememoryismodulatedbygenepositioninginyeast
AT emmanuellefabre hyperosmoticstressresponsememoryismodulatedbygenepositioninginyeast