Institute of Molecular Plant Science, School of Biological Sciences, University of Edinburgh, Daniel Rutherford Building, Max Born Crescent, Edinburgh, United Kingdom.
Smurfit Institute of Genetics, Trinity College Dublin, Ireland.
PLoS Genet. 2020 May 28;16(5):e1008681. doi: 10.1371/journal.pgen.1008681. eCollection 2020 May.
A large fraction of plant genomes is composed of transposable elements (TE), which provide a potential source of novel genes through "domestication"-the process whereby the proteins encoded by TE diverge in sequence, lose their ability to catalyse transposition and instead acquire novel functions for their hosts. In Arabidopsis, ANTAGONIST OF LIKE HETEROCHROMATIN PROTEIN 1 (ALP1) arose by domestication of the nuclease component of Harbinger class TE and acquired a new function as a component of POLYCOMB REPRESSIVE COMPLEX 2 (PRC2), a histone H3K27me3 methyltransferase involved in regulation of host genes and in some cases TE. It was not clear how ALP1 associated with PRC2, nor what the functional consequence was. Here, we identify ALP2 genetically as a suppressor of Polycomb-group (PcG) mutant phenotypes and show that it arose from the second, DNA binding component of Harbinger transposases. Molecular analysis of PcG compromised backgrounds reveals that ALP genes oppose silencing and H3K27me3 deposition at key PcG target genes. Proteomic analysis reveals that ALP1 and ALP2 are components of a variant PRC2 complex that contains the four core components but lacks plant-specific accessory components such as the H3K27me3 reader LIKE HETEROCHROMATION PROTEIN 1 (LHP1). We show that the N-terminus of ALP2 interacts directly with ALP1, whereas the C-terminus of ALP2 interacts with MULTICOPY SUPPRESSOR OF IRA1 (MSI1), a core component of PRC2. Proteomic analysis reveals that in alp2 mutant backgrounds ALP1 protein no longer associates with PRC2, consistent with a role for ALP2 in recruitment of ALP1. We suggest that the propensity of Harbinger TE to insert in gene-rich regions of the genome, together with the modular two component nature of their transposases, has predisposed them for domestication and incorporation into chromatin modifying complexes.
植物基因组的很大一部分由转座元件 (TE) 组成，这些元件通过“驯化”——即 TE 编码的蛋白质在序列上发生分歧、失去催化转座的能力、转而获得宿主新功能的过程——为新基因提供了潜在来源。在拟南芥中，拮抗同源异型蛋白 1 (ALP1) 是通过驯化类 Harbinger TE 的核酸酶组件产生的，并获得了作为多梳抑制复合物 2 (PRC2) 的组成部分的新功能，PRC2 是一种组蛋白 H3K27me3 甲基转移酶，参与宿主基因的调控，在某些情况下还参与 TE 的调控。目前尚不清楚 ALP1 如何与 PRC2 相关联，也不清楚其功能后果是什么。在这里，我们通过遗传鉴定将 ALP2 鉴定为 Polycomb-group (PcG) 突变体表型的抑制剂，并表明它是由 Harbinger 转座酶的第二个 DNA 结合组件产生的。在 PcG 受损背景下的分子分析表明，ALP 基因在关键 PcG 靶基因上对抗沉默和 H3K27me3 沉积。蛋白质组学分析表明，ALP1 和 ALP2 是一种变体 PRC2 复合物的组成部分，该复合物包含四个核心组件，但缺乏植物特异性辅助组件，如组蛋白 H3K27me3 读码器 LIKE HETEROCHROMATION PROTEIN 1 (LHP1)。我们表明，ALP2 的 N 端与 ALP1 直接相互作用，而 ALP2 的 C 端与 MULTICOPY SUPPRESSOR OF IRA1 (MSI1) 相互作用，后者是 PRC2 的核心组件。蛋白质组学分析表明，在 alp2 突变体背景下，ALP1 蛋白不再与 PRC2 相关联，这与 ALP2 在 ALP1 募集中的作用一致。我们认为，Harbinger TE 倾向于插入基因组中基因丰富的区域，以及它们转座酶的模块化两组件性质，使它们易于驯化并整合到染色质修饰复合物中。
