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Distinct requirements for the COMPASS core subunits Set1, Swd1, and Swd3 during meiosis in the budding yeast Saccharomyces cerevisiae

Meiosis-specific chromatin structures, guided by histone modifications, are critical mediators of a meiotic transient transcription program and progression through prophase I. Histone H3K4 can be methylated up to three times by the Set1-containing COMPASS complex and each methylation mark correspond...

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Autores principales: Trainor, Brandon M, Ciccaglione, Kerri, Czymek, Miranda, Law, Michael J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8527496/
https://www.ncbi.nlm.nih.gov/pubmed/34849786
http://dx.doi.org/10.1093/g3journal/jkab283
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author Trainor, Brandon M
Ciccaglione, Kerri
Czymek, Miranda
Law, Michael J
author_facet Trainor, Brandon M
Ciccaglione, Kerri
Czymek, Miranda
Law, Michael J
author_sort Trainor, Brandon M
collection PubMed
description Meiosis-specific chromatin structures, guided by histone modifications, are critical mediators of a meiotic transient transcription program and progression through prophase I. Histone H3K4 can be methylated up to three times by the Set1-containing COMPASS complex and each methylation mark corresponds to a different chromatin conformation. The level of H3K4 modification is directed by the activity of additional COMPASS components. In this study, we characterized the role of the COMPASS subunits during meiosis in Saccharomyces cerevisiae. In vegetative cells, previous studies revealed a role for subunits Swd2, Sdc1, and Bre2 for H3K4me2 while Spp1 supported trimethylation. However, we found that Bre2 and Sdc1 are required for H3K4me3 as yeast prepare to enter meiosis while Spp1 is not. Interestingly, we identified distinct meiotic functions for the core COMPASS complex members that required for all H3K4me, Set1, Swd1, and Swd3. While Set1 and Swd1 are required for progression through early meiosis, Swd3 is critical for late meiosis and spore morphogenesis. Furthermore, the meiotic requirement for Set1 is independent of H3K4 methylation, suggesting the presence of nonhistone substrates. Finally, checkpoint suppression analyses indicate that Set1 and Swd1 are required for both homologous recombination and chromosome segregation. These data suggest that COMPASS has important new roles for meiosis that are independent of its well-characterized functions during mitotic divisions.
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spelling pubmed-85274962021-10-20 Distinct requirements for the COMPASS core subunits Set1, Swd1, and Swd3 during meiosis in the budding yeast Saccharomyces cerevisiae Trainor, Brandon M Ciccaglione, Kerri Czymek, Miranda Law, Michael J G3 (Bethesda) Investigation Meiosis-specific chromatin structures, guided by histone modifications, are critical mediators of a meiotic transient transcription program and progression through prophase I. Histone H3K4 can be methylated up to three times by the Set1-containing COMPASS complex and each methylation mark corresponds to a different chromatin conformation. The level of H3K4 modification is directed by the activity of additional COMPASS components. In this study, we characterized the role of the COMPASS subunits during meiosis in Saccharomyces cerevisiae. In vegetative cells, previous studies revealed a role for subunits Swd2, Sdc1, and Bre2 for H3K4me2 while Spp1 supported trimethylation. However, we found that Bre2 and Sdc1 are required for H3K4me3 as yeast prepare to enter meiosis while Spp1 is not. Interestingly, we identified distinct meiotic functions for the core COMPASS complex members that required for all H3K4me, Set1, Swd1, and Swd3. While Set1 and Swd1 are required for progression through early meiosis, Swd3 is critical for late meiosis and spore morphogenesis. Furthermore, the meiotic requirement for Set1 is independent of H3K4 methylation, suggesting the presence of nonhistone substrates. Finally, checkpoint suppression analyses indicate that Set1 and Swd1 are required for both homologous recombination and chromosome segregation. These data suggest that COMPASS has important new roles for meiosis that are independent of its well-characterized functions during mitotic divisions. Oxford University Press 2021-08-05 /pmc/articles/PMC8527496/ /pubmed/34849786 http://dx.doi.org/10.1093/g3journal/jkab283 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of Genetics Society of America. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Investigation
Trainor, Brandon M
Ciccaglione, Kerri
Czymek, Miranda
Law, Michael J
Distinct requirements for the COMPASS core subunits Set1, Swd1, and Swd3 during meiosis in the budding yeast Saccharomyces cerevisiae
title Distinct requirements for the COMPASS core subunits Set1, Swd1, and Swd3 during meiosis in the budding yeast Saccharomyces cerevisiae
title_full Distinct requirements for the COMPASS core subunits Set1, Swd1, and Swd3 during meiosis in the budding yeast Saccharomyces cerevisiae
title_fullStr Distinct requirements for the COMPASS core subunits Set1, Swd1, and Swd3 during meiosis in the budding yeast Saccharomyces cerevisiae
title_full_unstemmed Distinct requirements for the COMPASS core subunits Set1, Swd1, and Swd3 during meiosis in the budding yeast Saccharomyces cerevisiae
title_short Distinct requirements for the COMPASS core subunits Set1, Swd1, and Swd3 during meiosis in the budding yeast Saccharomyces cerevisiae
title_sort distinct requirements for the compass core subunits set1, swd1, and swd3 during meiosis in the budding yeast saccharomyces cerevisiae
topic Investigation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8527496/
https://www.ncbi.nlm.nih.gov/pubmed/34849786
http://dx.doi.org/10.1093/g3journal/jkab283
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