SDG2-Mediated H3K4 Methylation Is Required for Proper Arabidopsis Root Growth and Development

Trithorax group (TrxG) proteins are evolutionarily conserved in eukaryotes and play critical roles in transcriptional activation via deposition of histone H3 lysine 4 trimethylation (H3K4me3) in chromatin. Several Arabidopsis TrxG members have been characterized, and among them SET DOMAIN GROUP 2 (SDG2) has been shown to be necessary for global genome-wide H3K4me3 deposition. Although pleiotropic phenotypes have been uncovered in the sdg2 mutants, SDG2 function in the regulation of stem cell activity has remained largely unclear. Here, we investigate the sdg2 mutant root phenotype and demonstrate that SDG2 is required for primary root stem cell niche (SCN) maintenance as well as for lateral root SCN establishment. Loss of SDG2 results in drastically reduced H3K4me3 levels in root SCN and differentiated cells and causes the loss of auxin gradient maximum in the root quiescent centre. Elevated DNA damage is detected in the sdg2 mutant, suggesting that impaired genome integrity may also have challenged the stem cell activity. Genetic interaction analysis reveals that SDG2 and CHROMATIN ASSEMBLY FACTOR-1 act synergistically in root SCN and genome integrity maintenance but not in telomere length maintenance. We conclude that SDG2-mediated H3K4me3 plays a distinctive role in the regulation of chromatin structure and genome integrity, which are key features in pluripotency of stem cells and crucial for root growth and development.Trithorax组（Trithorax group, TrxG）蛋白在真核生物中进化保守，并通过在染色质中沉积组蛋白H3赖氨酸4三甲基化（H3K4me3）在转录激活过程中发挥关键作用。目前已有多个拟南芥TrxG家族成员被鉴定，其中SET结构域家族2（SET DOMAIN GROUP 2, SDG2）被证实是全基因组H3K4me3沉积所必需的因子。尽管sdg2突变体已被报道存在多效性表型，但SDG2在干细胞活性调控中的功能仍不甚明确。本研究对sdg2突变体的根表型开展了分析，证实SDG2对于维持主根干细胞巢（stem cell niche, SCN）以及建立侧根干细胞巢均不可或缺。SDG2功能缺失会导致根干细胞巢及分化细胞内的H3K4me3水平显著降低，并引发根静止中心的生长素梯度峰值消失。研究还在sdg2突变体中检测到DNA损伤水平升高，提示基因组完整性受损可能也会对干细胞活性造成负面影响。遗传互作分析表明，SDG2与染色质组装因子1（chromatin assembly factor-1, CAF-1）在维持根干细胞巢及基因组完整性的过程中存在协同作用，但二者并不参与端粒长度的维持。综上，SDG2介导的H3K4me3在调控染色质结构与基因组完整性中发挥独特作用，而这二者是干细胞多能性的关键特征，同时对根的生长发育至关重要。