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

First author: Anne-Sophie Fiorucci; Affiliations: Université PSL (巴黎文理研究大学): Paris, France

Corresponding author: Fredy Barneche

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. 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. 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.

植物系统中有关H3K4me3的功能性决定因子，是否依赖于组蛋白H2B单泛素化，以及其作用于转录都不是很清楚。酿酒酵母中只有一个SET1蛋白作为COMPASS的一部分催化H3K4me3，与此不同，拟南芥中该过程涉及多个组蛋白甲基转移酶。在这些组蛋白甲基转移酶中，植物特异性的SDG2蛋白具有主要作用。作者报道了SDG2与一个与酵母COMPASS亚基Swd2的同源蛋白S2Lb一起共调控数百个基因。本文的研究显示S2Lb与AtCOMPASS核心亚基WDR5能被一起纯化，另外S2Lb和SDG2都能直接影响高度转录基因上的H3K4me3丰度。S2Lb敲除会诱导营养和生殖阶段多种发育表型，包括降低育性和种子休眠。然而，相比于S2Lb、SDG2或者H3K4me3能够靶向基因数量，s2lb突变体中转录缺陷的基因却很少，说明H3K4me3的丰度对于细胞转变时期最佳基因的诱导要比决定转录状态的开启/闭合更加重要。此外，与芽殖酵母不同的是，大多数S2Lb和H3K4me3在基因组上的分布并不依赖于反式组蛋白与组蛋白H2B单泛素化的相互作用。综上，本研究揭示了在演化上比较保守的类COMPASS复合物在拟南芥中出现分化，由植物特异性SDG2组蛋白甲基转移酶通过一个独立于H2B单泛素化途径调控H3K4me3的沉积。

通讯：Fredy Barneche（https://www.ibens.ens.fr/spip.php?article149&lang=fr）

个人简介：1995年，法国保罗大学，本科研究助理；1997年，法国佩皮尼昂植物基因组与发育实验室，硕士；1998年，美国圣路易斯华盛顿大学，研究生研究助理；2001年，法国佩皮尼昂和图卢兹大学，博士；2002年，瑞士日内瓦大学，博士后。

研究方向：影响植物对于外界环境适应性响应的表观机制。

doi: https://doi.org/10.1186/s13059-019-1705-4

Journal: Genome Biology

Published date: May 21, 2019