The antagonistic role of an E3 ligase pair in regulating plant NLR-mediated autoimmunity and fungal pathogen resistance

IF 20.6 1区医学 Q1 MICROBIOLOGY

Cell host & microbe Pub Date : 2024-07-01 DOI:10.1016/j.chom.2024.06.004

Jun Liu, Yong Yang, Fausto Andres Ortiz-Morea, Yulu Zhou, Derui Liu, Yanyan Huang, Jiarui Zheng, Yan Chen, Liang Kong, Zunyong Liu, Dongdong Ge, Mingli Yong, Wenwei Lin, Eugenia Russinova, Libo Shan, Ping He

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引用次数: 0

Abstract

Plant immune homeostasis is achieved through a balanced immune activation and suppression, enabling effective defense while averting autoimmunity. In Arabidopsis, disrupting a mitogen-activated protein (MAP) kinase cascade triggers nucleotide-binding leucine-rich-repeat (NLR) SUPPRESSOR OF mkk1/2 2 (SUMM2)-mediated autoimmunity. Through an RNAi screen, we identify PUB5, a putative plant U-box E3 ligase, as a critical regulator of SUMM2-mediated autoimmunity. In contrast to typical E3 ligases, PUB5 stabilizes CRCK3, a calmodulin-binding receptor-like cytoplasmic kinase involved in SUMM2 activation. A closely related E3 ligase, PUB44, functions oppositely with PUB5 to degrade CRCK3 through monoubiquitylation and internalization. Furthermore, CRCK3, highly expressed in roots and conserved across plant species, confers resistance to Fusarium oxysporum, a devastating soil-borne fungal pathogen, in both Arabidopsis and cotton. These findings demonstrate the antagonistic role of an E3 ligase pair in fine-tuning kinase proteostasis for the regulation of NLR-mediated autoimmunity and highlight the function of autoimmune activators in governing plant root immunity against fungal pathogens.

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一对 E3 连接酶在调节植物 NLR 介导的自身免疫和真菌病原体抗性中的拮抗作用

植物免疫平衡是通过平衡免疫激活和抑制来实现的，这样既能有效防御，又能避免自身免疫。在拟南芥中，破坏丝裂原活化蛋白（MAP）激酶级联会引发核苷酸结合亮氨酸-富复性（NLR）mkk1/2 2抑制因子（SUMM2）介导的自身免疫。通过 RNAi 筛选，我们发现 PUB5（一种推定的植物 U-box E3 连接酶）是 SUMM2 介导的自身免疫的关键调控因子。与典型的 E3 连接酶不同，PUB5 能稳定 CRCK3，CRCK3 是一种钙调蛋白结合受体样细胞质激酶，参与 SUMM2 的活化。一种密切相关的 E3 连接酶 PUB44 与 PUB5 的功能相反，通过单泛素化和内化降解 CRCK3。此外，在拟南芥和棉花中，CRCK3 在根部高表达且在不同植物物种中保守，它能赋予拟南芥和棉花对镰刀菌（一种毁灭性土传真菌病原体）的抗性。这些发现证明了一对 E3 连接酶在微调激酶蛋白稳态以调节 NLR 介导的自身免疫中的拮抗作用，并强调了自身免疫激活剂在管理植物根系免疫以抵抗真菌病原体中的功能。

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来源期刊

Cell host & microbe 生物-微生物学

CiteScore

45.10

自引率

1.70%

发文量

201

审稿时长

4-8 weeks

期刊介绍： Cell Host & Microbe is a scientific journal that was launched in March 2007. The journal aims to provide a platform for scientists to exchange ideas and concepts related to the study of microbes and their interaction with host organisms at a molecular, cellular, and immune level. It publishes novel findings on a wide range of microorganisms including bacteria, fungi, parasites, and viruses. The journal focuses on the interface between the microbe and its host, whether the host is a vertebrate, invertebrate, or plant, and whether the microbe is pathogenic, non-pathogenic, or commensal. The integrated study of microbes and their interactions with each other, their host, and the cellular environment they inhabit is a unifying theme of the journal. The published work in Cell Host & Microbe is expected to be of exceptional significance within its field and also of interest to researchers in other areas. In addition to primary research articles, the journal features expert analysis, commentary, and reviews on current topics of interest in the field.