Arabidopsis S2Lb links AtCOMPASS-like and SDG2 activity in histone H3 Lys-4 trimethylation independently from histone H2B monoubiquitination

Abstract

The functional determinants of histone H3 Lys-4 trimethylation (H3K4me3), their potential dependency on histone H2B monoubiquitination (H2Bub) and their contribution to defining transcriptional regimes are poorly defined in plant systems. Unlike in S. cerevisiae, where a single SET1 protein catalyzes H3 Lys-4 trimethylation as part of COMPASS (COMPlex of proteins ASsociated with Set1), in Arabidopsis thaliana this activity involves multiple histone methyltransferases (HMTs). Among these, the plant-specific SDG2 (SET DOMAIN GROUP2) has a prominent role. 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. S2Lb co-purifies with the AtCOMPASS core subunit WDR5 from a highmolecular weight complex, 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. Notwithstanding, s2lb seedlings display little transcriptomic defects as compared to the large repertoire of genes targeted by S2Lb, SDG2 or H3 Lys-4 trimethylation, 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. Collectively, this study unveils that the evolutionarily conserved COMPASS-like complex has been coopted by the plant-specific SDG2 HMT and mediates H3K4me3 deposition through an H2Bub-independent pathway in Arabidopsis.

Elongation factor 1 is a component of the Arabidopsis RNA polymerase II elongation complex and associates with a subset of transcribed genes

“…Various factors that affect the deposition of histone marks over transcribed regions (e.g. PAF1-C, HUB1/2 and SDG proteins) have profound effects on many aspects of plant growth and development (He et al, 2004;Oh et al, 2004;Fleury et al, 2007;Xu et al, 2008;Berr et al, 2010;Fiorucci et al, 2019).…”

A COMPASS histone H3K4 trimethyltransferase pentamer transactivates drought tolerance and growth/biomass production in Populus trichocarpa

“…The first plant COMPASS-like was demonstrated in Arabidopsis, which contains three core subunits, WDR5a, RbBP5 and ASH2, where WDR5a could interact with ATX1 (also named SDG27), forming an ATX1-COMPASS-like methyltransferase complex (Jiang et al, 2011). Subsequently, other plant COMPASS-like HKMT complexes were inferred (Ding et al, 2012;Song et al, 2015;Jiang et al, 2018;Fiorucci et al, 2019;Shang et al, 2021;Oya et al, 2022;Xie et al, 2023) and the COMPASS-like complexes play a crucial role in various plant processes, including the development of floral organs, organogenesis, and responses to abiotic and biotic stresses (Jiang et al, 2011(Jiang et al, , 2018Song et al, 2015;Liu et al, 2016;Yang et al, 2023). Additionally, several H3K4 methyltransferases, such as ATX1, ATX4, and ATX5, have been identified to participate in the plant's response to drought and ABA signaling pathways (Ding et al, 2009(Ding et al, , 2011aLiu et al, 2018).…”

PpyABF3 recruits the COMPASS‐like complex to regulate bud dormancy maintenance via integrating ABA signaling and GA catabolism

“…COMPASS-like (Complex of Proteins Associated with Set1like) is a complex specifically responsible for H3K4me3 histone modification and is highly conserved in animals, yeast, and plants (Miller et al, 2001;Takahashi et al, 2011). The core members of the complex are Ash2, WDR5a, and RbBP5, whereas in Arabidopsis thaliana, homologs of these members are named ASH2R (Arabidopsis Ash2 Relative), WDR5a and RBL (RbBP5-like) (Jiang et al, 2011;Fiorucci et al, 2019). The COMPASS-like complex represses Arabidopsis flowering by enriching H3K4me3 histone modifications at the FLC locus (Jiang et al, 2011).…”