Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plan Sciences, University of California at Riverside, Riverside, CA, United States of America.
College of Life Sciences, Fujian Agricultural and Forestry University, Fuzhou, Fujian, China.
PLoS Genet. 2020 Sep 14;16(9):e1008993. doi: 10.1371/journal.pgen.1008993. eCollection 2020 Sep.
Plant NLR-type receptors serve as sensitive triggers of host immunity. Their expression has to be well-balanced, due to their interference with various cellular processes and dose-dependency of their defense-inducing activity. A genetic "arms race" with fast-evolving pathogenic microbes requires plants to constantly innovate their NLR repertoires. We previously showed that insertion of the COPIA-R7 retrotransposon into RPP7 co-opted the epigenetic transposon silencing signal H3K9me2 to a new function promoting expression of this Arabidopsis thaliana NLR gene. Recruitment of the histone binding protein EDM2 to COPIA-R7-associated H3K9me2 is required for optimal expression of RPP7. By profiling of genome-wide effects of EDM2, we now uncovered additional examples illustrating effects of transposons on NLR gene expression, strongly suggesting that these mobile elements can play critical roles in the rapid evolution of plant NLR genes by providing the "raw material" for gene expression mechanisms. We further found EDM2 to have a global role in NLR expression control. Besides serving as a positive regulator of RPP7 and a small number of other NLR genes, EDM2 acts as a suppressor of a multitude of additional NLR genes. We speculate that the dual functionality of EDM2 in NLR expression control arose from the need to compensate for fitness penalties caused by high expression of some NLR genes by suppression of others. Moreover, we are providing new insights into functional relationships of EDM2 with its interaction partner, the RNA binding protein EDM3/AIPP1, and its target gene IBM1, encoding an H3K9-demethylase.
植物 NLR 型受体是宿主免疫的敏感触发因子。由于它们会干扰各种细胞过程，并且其防御诱导活性具有剂量依赖性，因此它们的表达必须保持平衡。与快速进化的致病微生物的遗传“军备竞赛”要求植物不断创新其 NLR 库。我们之前曾表明，将 COPIA-R7 逆转录转座子插入 RPP7 中，将表观遗传转座子沉默信号 H3K9me2 共同转导到一个新的功能，促进了拟南芥 NLR 基因的表达。组蛋白结合蛋白 EDM2 募集到 COPIA-R7 相关的 H3K9me2 对于 RPP7 的最佳表达是必需的。通过对 EDM2 全基因组效应的分析，我们现在发现了其他例子，说明了转座子对 NLR 基因表达的影响，这强烈表明这些移动元件可以通过提供基因表达机制的“原材料”，在植物 NLR 基因的快速进化中发挥关键作用。我们进一步发现 EDM2 在 NLR 表达调控中具有全局作用。除了作为 RPP7 和少数其他 NLR 基因的正调控因子外，EDM2 还作为大量其他 NLR 基因的抑制因子发挥作用。我们推测，EDM2 在 NLR 表达调控中的双重功能源于通过抑制其他基因来补偿某些 NLR 基因高表达所带来的适应性代价的需要。此外，我们为 EDM2 与其相互作用伙伴，即 RNA 结合蛋白 EDM3/AIPP1 和其靶基因 IBM1（编码 H3K9 去甲基酶）之间的功能关系提供了新的见解。
