Aluminum (Al) is a primary constraint for crop production on acid soils, which make up more than 30% of the arable land in the world. Al resistance in Arabidopsis (Arabidopsis thaliana) is achieved by malate secretion mediated by the Al-ACTIVATED MALATE TRANSPORTER1 (AtALMT1) transporter. The C2H2-type transcription factor SENSITIVE TO PROTON RHIZOTOXICITY1 (STOP1) is essential and required for Al resistance, where it acts by inducing the expression of Al-resistance genes, including AtALMT1. In this study, we report that STOP1 protein function is modified by SUMOylation. The SMALL UBIQUITIN-LIKE MODIFIER (SUMO) protease ESD4, but not other SUMO proteases, specifically interacts with and deSUMOylates STOP1. Mutation of ESD4 increases the level of STOP1 SUMOylation and the expression of the STOP1-regulated gene AtALMT1, which contributes to the increased Al resistance in esd4. The esd4 mutation does not influence STOP1 protein abundance but increases the association of STOP1 with the AtALMT1 promoter, which might explain the elevated expression of AtALMT1 in esd4. We demonstrate that STOP1 is mono-SUMOylated at K40, K212, or K395 sites, and blocking STOP1 SUMOylation reduces STOP1 stability and the expression of STOP1-regulated genes, leading to the reduced Al resistance. Our results thus reveal the involvement of SUMOylation in the regulation of STOP1 and Al resistance in Arabidopsis.

铝 (Al) 是酸性土壤上作物生产的主要限制因素，酸性土壤占世界可耕地的 30% 以上。拟南芥 ( Arabidopsis thaliana ) 中的铝抗性是通过铝激活苹果酸转运蛋白 1 (AtALMT1) 转运蛋白介导的苹果酸分泌实现的。C2H2 型转录因子 SENSITIVE TO PROTON RHIZOTOXICITY1 (STOP1) 是 Al 抗性所必需的，它通过诱导 Al 抗性基因（包括AtALMT1）的表达起作用。在这项研究中，我们报告 STOP1 蛋白功能被 SUMOylation 修饰。小型泛素样修饰剂 (SUMO) 蛋白酶 ESD4，但不是其他 SUMO 蛋白酶，特别与 STOP1 相互作用并使其脱去SUMOylate。ESD4突变增加 STOP1 SUMOylation的水平和 STOP1 调节基因AtALMT1的表达，这有助于增加esd4 中的铝电阻。该ESD4突变不影响停止1蛋白质丰度，但会增加STOP1与关联AtALMT1启动，这或许可以解释的表达升高AtALMT1在ESD4。我们证明 STOP1 在 K40、K212 或 K395 位点被单 SUMO 化，阻断 STOP1 SUMO 化会降低 STOP1 的稳定性和 STOP1 调节基因的表达，从而导致铝抗性降低。因此，我们的结果揭示了 SUMOylation 参与了拟南芥中 STOP1 和 Al 抗性的调节。