Arabidopsis S2Lb links AtCOMPASS-like and SDG2 activity in H3K4me3 independently from histone H2B monoubiquitination

Anne-Sophie Fiorucci (1) , Clara Bourbousse (1) , Lorenzo Concia (2) , Martin Rougée (1) , Anne-Flore Deton-Cabanillas (1) , Gérald Zabulon (1) , Elodie Layat (3) , David Latrasse (2) , Soon Kap Kim (2) , Nicole Chaumont (3) , Berangère Lombard , David Stroebel (1) , Sophie Lemoine (1, 4) , Ammara Mohammad (1, 4) , Corinne Blugeon (1, 4) , Damarys Loew (5) , Chris Bowler (1) , Moussa Benhamed (2) , Fredy Barneche (1) , Christophe Bailly

1 IBENS - Institut de biologie de l'ENS Paris
2 IPS2 (UMR_9213 / UMR_1403) - Institut des Sciences des Plantes de Paris-Saclay
3 LBD - Laboratoire de Biologie du Développement [IBPS]
4 Genomique ENS - GenomiqueENS
5 Laboratoire de Spectrométrie de Masse Protéomique

Background: The functional determinants of H3K4me3, their potential dependency on histone H2B monoubiquitination, and their contribution to defining transcriptional regimes are poorly defined in plant systems. Unlike in Saccharomyces cerevisiae, where a single SET1 protein catalyzes H3K4me3 as part of COMPlex of proteins ASsociated with Set1 (COMPASS), in Arabidopsis thaliana, this activity involves multiple histone methyltransferases. Among these, the plant-specific SET DOMAIN GROUP 2 (SDG2) has a prominent role. Results: We report that SDG2 co-regulates hundreds of genes with SWD2-like b (S2Lb), a plant ortholog of the Swd2 axillary subunit of yeast COMPASS. We show that S2Lb co-purifies with the AtCOMPASS core subunit WDR5, and both S2Lb and SDG2 directly influence H3K4me3 enrichment over highly transcribed genes. S2Lb knockout triggers pleiotropic developmental phenotypes at the vegetative and reproductive stages, including reduced fertility and seed dormancy. However, s2lb seedlings display little transcriptomic defects as compared to the large repertoire of genes targeted by S2Lb, SDG2, or H3K4me3, suggesting that H3K4me3 enrichment is important for optimal gene induction during cellular transitions rather than for determining on/off transcriptional status. Moreover, unlike in budding yeast, most of the S2Lb and H3K4me3 genomic distribution does not rely on a trans-histone crosstalk with histone H2B monoubiquitination. Conclusions: Collectively, this study unveils that the evolutionarily conserved COMPASS-like complex has been co-opted by the plant-specific SDG2 histone methyltransferase and mediates H3K4me3 deposition through an H2B monoubiquitination-independent pathway in Arabidopsis.

Domains: Life Sciences [q-bio]; Biochemistry, Molecular Biology; Genomics [q-bio.GN]

Anne-Sophie Fiorucci, Clara Bourbousse, Lorenzo Concia, Martin Rougée, Anne-Flore Deton-Cabanillas, et al.. Arabidopsis S2Lb links AtCOMPASS-like and SDG2 activity in H3K4me3 independently from histone H2B monoubiquitination. Genome Biology, 2019, 20 (100), ⟨10.1186/s13059-019-1705-4⟩. ⟨hal-02156634⟩