A Role for <i>Caenorhabditis elegans</i> COMPASS in Germline Chromatin Organization
Deposition of histone H3 lysine 4 (H3K4) methylation at promoters is catalyzed by the SET1/COMPASS complex and is associated with context-dependent effects on gene expression and local changes in chromatin organization. The role of SET1/COMPASS in shaping chromosome architecture has not been investi...
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MDPI AG
2020-09-01
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| Series: | Cells |
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| Online Access: | https://www.mdpi.com/2073-4409/9/9/2049 |
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| author | Marion Herbette Valérie Robert Aymeric Bailly Loïc Gely Robert Feil David Llères Francesca Palladino |
| author_facet | Marion Herbette Valérie Robert Aymeric Bailly Loïc Gely Robert Feil David Llères Francesca Palladino |
| author_sort | Marion Herbette |
| collection | DOAJ |
| description | Deposition of histone H3 lysine 4 (H3K4) methylation at promoters is catalyzed by the SET1/COMPASS complex and is associated with context-dependent effects on gene expression and local changes in chromatin organization. The role of SET1/COMPASS in shaping chromosome architecture has not been investigated. Here we used <i>Caenorhabditis elegans</i> to address this question through a live imaging approach and genetic analysis. Using quantitative FRET (Förster resonance energy transfer)-based fluorescence lifetime imaging microscopy (FLIM) on germ cells expressing histones eGFP-H2B and mCherry-H2B, we find that SET1/COMPASS influences meiotic chromosome organization, with marked effects on the close proximity between nucleosomes. We further show that inactivation of <i>set-2</i>, encoding the <i>C. elegans</i> SET1 homologue, or CFP-1, encoding the chromatin targeting subunit of COMPASS, enhances germline chromosome organization defects and sterility of condensin-II depleted animals. <i>set-2</i> loss also aggravates germline defects resulting from conditional inactivation of topoisomerase II, another structural component of chromosomes. Expression profiling of <i>set-2</i> mutant germlines revealed only minor transcriptional changes, suggesting that the observed effects are at least partly independent of transcription. Altogether, our results are consistent with a role for SET1/COMPASS in shaping meiotic chromosomes in <i>C. elegans</i>, together with the non-histone proteins condensin-II and topoisomerase. Given the high degree of conservation, our findings expand the range of functions attributed to COMPASS and suggest a broader role in genome organization in different species. |
| first_indexed | 2024-03-10T16:29:22Z |
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| language | English |
| last_indexed | 2024-03-10T16:29:22Z |
| publishDate | 2020-09-01 |
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| series | Cells |
| spelling | doaj.art-1bf55760e4f941a3bb1e2a2928b0cf5b2023-11-20T12:58:54ZengMDPI AGCells2073-44092020-09-0199204910.3390/cells9092049A Role for <i>Caenorhabditis elegans</i> COMPASS in Germline Chromatin OrganizationMarion Herbette0Valérie Robert1Aymeric Bailly2Loïc Gely3Robert Feil4David Llères5Francesca Palladino6Laboratory of Biology and Modeling of the Cell (LBMC), CNRS, Ecole Normale Supérieure de Lyon, Université de Lyon, 69007 Lyon, FranceLaboratory of Biology and Modeling of the Cell (LBMC), CNRS, Ecole Normale Supérieure de Lyon, Université de Lyon, 69007 Lyon, FranceCentre de Recherche en Biologie cellulaire de Montpellier, CRBM, CNRS, University of Montpellier, 34090 Montpellier, FranceLaboratory of Biology and Modeling of the Cell (LBMC), CNRS, Ecole Normale Supérieure de Lyon, Université de Lyon, 69007 Lyon, FranceInstitute of Molecular Genetics of Montpellier (IGMM), CNRS, University of Montpellier, 34090 Montpellier, FranceInstitute of Molecular Genetics of Montpellier (IGMM), CNRS, University of Montpellier, 34090 Montpellier, FranceLaboratory of Biology and Modeling of the Cell (LBMC), CNRS, Ecole Normale Supérieure de Lyon, Université de Lyon, 69007 Lyon, FranceDeposition of histone H3 lysine 4 (H3K4) methylation at promoters is catalyzed by the SET1/COMPASS complex and is associated with context-dependent effects on gene expression and local changes in chromatin organization. The role of SET1/COMPASS in shaping chromosome architecture has not been investigated. Here we used <i>Caenorhabditis elegans</i> to address this question through a live imaging approach and genetic analysis. Using quantitative FRET (Förster resonance energy transfer)-based fluorescence lifetime imaging microscopy (FLIM) on germ cells expressing histones eGFP-H2B and mCherry-H2B, we find that SET1/COMPASS influences meiotic chromosome organization, with marked effects on the close proximity between nucleosomes. We further show that inactivation of <i>set-2</i>, encoding the <i>C. elegans</i> SET1 homologue, or CFP-1, encoding the chromatin targeting subunit of COMPASS, enhances germline chromosome organization defects and sterility of condensin-II depleted animals. <i>set-2</i> loss also aggravates germline defects resulting from conditional inactivation of topoisomerase II, another structural component of chromosomes. Expression profiling of <i>set-2</i> mutant germlines revealed only minor transcriptional changes, suggesting that the observed effects are at least partly independent of transcription. Altogether, our results are consistent with a role for SET1/COMPASS in shaping meiotic chromosomes in <i>C. elegans</i>, together with the non-histone proteins condensin-II and topoisomerase. Given the high degree of conservation, our findings expand the range of functions attributed to COMPASS and suggest a broader role in genome organization in different species.https://www.mdpi.com/2073-4409/9/9/2049COMPASSSET1condensinchromatinFLIM-FRET<i>C. elegans</i> |
| spellingShingle | Marion Herbette Valérie Robert Aymeric Bailly Loïc Gely Robert Feil David Llères Francesca Palladino A Role for <i>Caenorhabditis elegans</i> COMPASS in Germline Chromatin Organization Cells COMPASS SET1 condensin chromatin FLIM-FRET <i>C. elegans</i> |
| title | A Role for <i>Caenorhabditis elegans</i> COMPASS in Germline Chromatin Organization |
| title_full | A Role for <i>Caenorhabditis elegans</i> COMPASS in Germline Chromatin Organization |
| title_fullStr | A Role for <i>Caenorhabditis elegans</i> COMPASS in Germline Chromatin Organization |
| title_full_unstemmed | A Role for <i>Caenorhabditis elegans</i> COMPASS in Germline Chromatin Organization |
| title_short | A Role for <i>Caenorhabditis elegans</i> COMPASS in Germline Chromatin Organization |
| title_sort | role for i caenorhabditis elegans i compass in germline chromatin organization |
| topic | COMPASS SET1 condensin chromatin FLIM-FRET <i>C. elegans</i> |
| url | https://www.mdpi.com/2073-4409/9/9/2049 |
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