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

Anne-Sophie Fiorucci,Soon Kap Kim,Gérald Zabulon,Bérangère Lombard,Martin Rougée,Clara Bourbousse,David Latrasse,Lorenzo Concia,Corinne Blugeon,David Stroebel,Sophie Lemoine,Christophe Bailly,Ammara Mohammad,Elodie Layat,Damarys Loew,Chris Bowler,Nicole Chaumont,Anne-Flore Deton-Cabanillas,Moussa Benhamed,Frédy Barneche

doi:10.1186/s13059-019-1705-4

Abstract

BackgroundThe 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.ResultsWe 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.ConclusionsCollectively, 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.

Highlights

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
Fiorucci et al Genome Biology (2019) 20:100 cerevisiae, H3K4me3 deposition is catalyzed by the SET1 histone methyltransferase (HMT) embedded in a socalled COMPlex of Proteins Associated with Set1 (COMPASS), which contains the WD40 repeatscontaining proteins Swd1, Swd2, and Swd3 as well as Bre2, Spp1, and Sdc1 subunits
We report that SWD2-like b (S2Lb) is a euchromatic protein that functionally associates with an AtCOMPASS-like complex and with the plant-specific SET DOMAIN GROUP 2 (SDG2) HMT to broaden H3K4me3 enrichment over most transcribing genes, especially those abundantly occupied by RNA polymerase II (RNPII)

Summary

Introduction

The functional determinants of H3K4me, 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 H3K4me as part of COMPlex of proteins ASsociated with Set (COMPASS), in Arabidopsis thaliana, this activity involves multiple histone methyltransferases. Genome-wide profiling of histone PTMs in the Arabidopsis thaliana plant species has established that transcriptionally active genes are typically marked by acetylated histones H3 and H4, One of the best-described cases of functional trans-histone crosstalk is that of H2Bub promotion of histone H3K4me deposition on actively transcribed genes in yeast [10] and metazoans [11]. Fiorucci et al Genome Biology (2019) 20:100 cerevisiae, H3K4me deposition is catalyzed by the SET1 histone methyltransferase (HMT) embedded in a socalled COMPlex of Proteins Associated with Set (COMPASS), which contains the WD40 repeatscontaining proteins Swd, Swd, and Swd as well as Bre, Spp, and Sdc subunits (reviewed in [12, 13]). H3K4me is usually found on a limited number of nucleosomes surrounding the transcription start site (TSS) and is functionally linked to RNPII transcriptional activation and the switch to elongation in many eukaryotes including plants [5, 23,24,25,26,27,28]

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