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Sumoylation is Largely Dispensable for Normal Growth but Facilitates Heat Tolerance in Yeast

Numerous proteins are sumoylated in normally growing yeast and SUMO conjugation levels rise upon exposure to several stress conditions. We observe high levels of sumoylation also during early exponential growth and when nutrient-rich medium is used. However, we find that reduced sumoylation (∼75% le...

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Autores principales: Moallem, Marjan, Akhter, Akhi, Burke, Giovanni L., Babu, John, Bergey, Benjamin G., McNeil, J. Bryan, Baig, Mohammad S., Rosonina, Emanuel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Taylor & Francis 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9936996/
https://www.ncbi.nlm.nih.gov/pubmed/36720466
http://dx.doi.org/10.1080/10985549.2023.2166320
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author Moallem, Marjan
Akhter, Akhi
Burke, Giovanni L.
Babu, John
Bergey, Benjamin G.
McNeil, J. Bryan
Baig, Mohammad S.
Rosonina, Emanuel
author_facet Moallem, Marjan
Akhter, Akhi
Burke, Giovanni L.
Babu, John
Bergey, Benjamin G.
McNeil, J. Bryan
Baig, Mohammad S.
Rosonina, Emanuel
author_sort Moallem, Marjan
collection PubMed
description Numerous proteins are sumoylated in normally growing yeast and SUMO conjugation levels rise upon exposure to several stress conditions. We observe high levels of sumoylation also during early exponential growth and when nutrient-rich medium is used. However, we find that reduced sumoylation (∼75% less than normal) is remarkably well-tolerated, with no apparent growth defects under nonstress conditions or under osmotic, oxidative, or ethanol stresses. In contrast, strains with reduced activity of Ubc9, the sole SUMO conjugase, are temperature-sensitive, implicating sumoylation in the heat stress response, specifically. Aligned with this, a mild heat shock triggers increased sumoylation which requires functional levels of Ubc9, but likely also depends on decreased desumoylation, since heat shock reduces protein levels of Ulp1, the major SUMO protease. Furthermore, we find that a ubc9 mutant strain with only ∼5% of normal sumoylation levels shows a modest growth defect, has abnormal genomic distribution of RNA polymerase II (RNAPII), and displays a greatly expanded redistribution of RNAPII after heat shock. Together, our data implies that SUMO conjugations are largely dispensable under normal conditions, but a threshold level of Ubc9 activity is needed to maintain transcriptional control and to modulate the redistribution of RNAPII and promote survival when temperatures rise.
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spelling pubmed-99369962023-02-22 Sumoylation is Largely Dispensable for Normal Growth but Facilitates Heat Tolerance in Yeast Moallem, Marjan Akhter, Akhi Burke, Giovanni L. Babu, John Bergey, Benjamin G. McNeil, J. Bryan Baig, Mohammad S. Rosonina, Emanuel Mol Cell Biol Molecular and Cellular Biology Numerous proteins are sumoylated in normally growing yeast and SUMO conjugation levels rise upon exposure to several stress conditions. We observe high levels of sumoylation also during early exponential growth and when nutrient-rich medium is used. However, we find that reduced sumoylation (∼75% less than normal) is remarkably well-tolerated, with no apparent growth defects under nonstress conditions or under osmotic, oxidative, or ethanol stresses. In contrast, strains with reduced activity of Ubc9, the sole SUMO conjugase, are temperature-sensitive, implicating sumoylation in the heat stress response, specifically. Aligned with this, a mild heat shock triggers increased sumoylation which requires functional levels of Ubc9, but likely also depends on decreased desumoylation, since heat shock reduces protein levels of Ulp1, the major SUMO protease. Furthermore, we find that a ubc9 mutant strain with only ∼5% of normal sumoylation levels shows a modest growth defect, has abnormal genomic distribution of RNA polymerase II (RNAPII), and displays a greatly expanded redistribution of RNAPII after heat shock. Together, our data implies that SUMO conjugations are largely dispensable under normal conditions, but a threshold level of Ubc9 activity is needed to maintain transcriptional control and to modulate the redistribution of RNAPII and promote survival when temperatures rise. Taylor & Francis 2023-01-31 /pmc/articles/PMC9936996/ /pubmed/36720466 http://dx.doi.org/10.1080/10985549.2023.2166320 Text en © 2023 The Author(s). Published with license by Taylor & Francis Group, LLC. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License (http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) ), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way.
spellingShingle Molecular and Cellular Biology
Moallem, Marjan
Akhter, Akhi
Burke, Giovanni L.
Babu, John
Bergey, Benjamin G.
McNeil, J. Bryan
Baig, Mohammad S.
Rosonina, Emanuel
Sumoylation is Largely Dispensable for Normal Growth but Facilitates Heat Tolerance in Yeast
title Sumoylation is Largely Dispensable for Normal Growth but Facilitates Heat Tolerance in Yeast
title_full Sumoylation is Largely Dispensable for Normal Growth but Facilitates Heat Tolerance in Yeast
title_fullStr Sumoylation is Largely Dispensable for Normal Growth but Facilitates Heat Tolerance in Yeast
title_full_unstemmed Sumoylation is Largely Dispensable for Normal Growth but Facilitates Heat Tolerance in Yeast
title_short Sumoylation is Largely Dispensable for Normal Growth but Facilitates Heat Tolerance in Yeast
title_sort sumoylation is largely dispensable for normal growth but facilitates heat tolerance in yeast
topic Molecular and Cellular Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9936996/
https://www.ncbi.nlm.nih.gov/pubmed/36720466
http://dx.doi.org/10.1080/10985549.2023.2166320
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