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A Role for Caenorhabditis elegans COMPASS in Germline Chromatin Organization.

Marion Herbette, Valérie Robert, Aymeric Bailly, Loïc Gely, Robert Feil, David Llères, and Francesca Palladino (2020)

Cells, 9(9).

Deposition of histone H3 lysine 4 (H3K4) methylation at promoters is catalyzed bythe SET1/COMPASS complex and is associated with context-dependent effects on geneexpression and local changes in chromatin organization. The role of SET1/COMPASS inshaping chromosome architecture has not been investigated. Here we usedCaenorhabditis elegans to address this question through a live imaging approach andgenetic analysis. Using quantitative FRET (Förster resonance energy transfer)-basedfluorescence lifetime imaging microscopy (FLIM) on germ cells expressing histoneseGFP-H2B and mCherry-H2B, we find that SET1/COMPASS influences meiotic chromosomeorganization, with marked effects on the close proximity between nucleosomes. Wefurther show that inactivation of set-2, encoding the C. elegans SET1 homologue, orCFP-1, encoding the chromatin targeting subunit of COMPASS, enhances germlinechromosome organization defects and sterility of condensin-II depleted animals.set-2 loss also aggravates germline defects resulting from conditional inactivationof topoisomerase II, another structural component of chromosomes. Expressionprofiling of set-2 mutant germlines revealed only minor transcriptional changes,suggesting that the observed effects are at least partly independent oftranscription. Altogether, our results are consistent with a role for SET1/COMPASSin shaping meiotic chromosomes in C. elegans, together with the non-histone proteinscondensin-II and topoisomerase. Given the high degree of conservation, our findingsexpand the range of functions attributed to COMPASS and suggest a broader role ingenome organization in different species.

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