The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis.
The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis.
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DOI：
10.1371/journal.pbio.1001792
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发表时间：
2014-02
期刊：
影响因子：
9.8
通讯作者：
Solano R
中科院分区：
文献类型：
--
作者：
Gimenez-Ibanez S;Boter M;Fernández-Barbero G;Chini A;Rathjen JP;Solano R
细菌效应蛋白HopX 1靶向宿主植物JAZ转录阻遏物进行降解以激活茉莉酸途径，从而通过抑制宿主防御反应促进细菌致病。假单胞菌的致病性依赖于III型分泌系统，其分泌一套毒力效应蛋白到宿主细胞质中，以及许多毒素的产生，例如冠菌素（COR），其是植物激素茉莉酸酯-异白素（JA-Ile）的模拟物。在植物细胞内，效应子靶向宿主分子以破坏宿主细胞生理学并破坏防御。然而，尽管阐明效应子作用对于理解细菌发病机理至关重要，但绝大多数效应子的分子功能和宿主靶点在很大程度上仍然未知。在这里，我们发现，从假单胞菌pv. tabaci（Pta）11528是一种不产生COR的菌株，它与JAZ蛋白相互作用并促进JAZ蛋白的降解，JAZ蛋白是JAZ阻遏物的一个关键家族。我们发现，hopX 1编码的半胱氨酸蛋白酶，活性所需的降解JAZ的HopX 1。HopX 1通过其中心ZIM结构域与JAZ蛋白结合，并且以COI 1非依赖性方式发生降解。此外，异位表达的HopX 1在拟南芥诱导的JA依赖性基因的表达，抑制水杨酸（SA）诱导的标记，并补充了生长的COR-缺陷的P.番茄（Pto）DC 3000菌株在自然菌侵染过程中的生长情况。此外，HopX 1促进易感性时，提供的自然III型分泌系统，以类似的程度作为添加COR，这种效果是依赖于其催化活性。总之，我们的研究结果表明，JAZ蛋白是细菌效应子的直接靶标，以促进激活JA诱导的拟南芥防御和易感性。HopX 1说明了COR的替代进化解决方案的一个范例，具有类似的生理结果。细菌性植物病原体分泌毒素并将效应蛋白注入宿主细胞以促进感染，并且鉴定这些分子的个体功能对于理解感染过程至关重要。值得注意的是，一些假单胞菌菌株已经进化出一种复杂的策略，通过产生毒素冠菌素（COR）来操纵激素平衡，这种毒素模仿植物激素茉莉酸-异亮氨酸（JA-Ile）。JA-Ile途径通过激活对真菌病原体的防御在植物免疫中起关键作用，同时通过抑制假单胞菌抗性所需的水杨酸（SA）依赖性防御来促进细菌生长。在这里，我们报告说，从假单胞菌菌株，不产生COR的效应HopX 1利用一种替代的进化策略来激活JA-Ile途径。我们发现，HopX 1编码的半胱氨酸蛋白酶，相互作用，并促进降解的关键JA通路抑制剂，JAZ蛋白。相应地，在模式植物拟南芥中异位表达HopX 1诱导JA依赖性基因的表达，并且产生HopX 1的假单胞菌的自然感染以与COR类似的方式促进细菌生长。我们的研究结果突出了一个新的例子，细菌效应器直接操纵激素信号的核心调节因子，以促进感染。
A bacterial effector protein, HopX1, targets host plant JAZ transcriptional repressors for degradation to activate the jasmonate pathway, thereby promoting bacterial pathogenesis by suppressing host defense responses. Pathogenicity of Pseudomonas syringae is dependent on a type III secretion system, which secretes a suite of virulence effector proteins into the host cytoplasm, and the production of a number of toxins such as coronatine (COR), which is a mimic of the plant hormone jasmonate-isoleuce (JA-Ile). Inside the plant cell, effectors target host molecules to subvert the host cell physiology and disrupt defenses. However, despite the fact that elucidating effector action is essential to understanding bacterial pathogenesis, the molecular function and host targets of the vast majority of effectors remain largely unknown. Here, we found that effector HopX1 from Pseudomonas syringae pv. tabaci (Pta) 11528, a strain that does not produce COR, interacts with and promotes the degradation of JAZ proteins, a key family of JA-repressors. We show that hopX1 encodes a cysteine protease, activity that is required for degradation of JAZs by HopX1. HopX1 associates with JAZ proteins through its central ZIM domain and degradation occurs in a COI1-independent manner. Moreover, ectopic expression of HopX1 in Arabidopsis induces the expression of JA-dependent genes, represses salicylic acid (SA)-induced markers, and complements the growth of a COR-deficient P. syringae pv. tomato (Pto) DC3000 strain during natural bacterial infections. Furthermore, HopX1 promoted susceptibility when delivered by the natural type III secretion system, to a similar extent as the addition of COR, and this effect was dependent on its catalytic activity. Altogether, our results indicate that JAZ proteins are direct targets of bacterial effectors to promote activation of JA-induced defenses and susceptibility in Arabidopsis. HopX1 illustrates a paradigm of an alternative evolutionary solution to COR with similar physiological outcome. Bacterial plant pathogens secrete toxins and inject effector proteins into the host cells to promote infection, and the identification of the individual functions of these molecules is essential to understand the infective process. Remarkably, some Pseudomonas strains have evolved a sophisticated strategy for manipulating hormonal balance by producing the toxin coronatine (COR), which mimics the plant hormone jasmonate-isoleucine (JA-Ile). The JA-Ile pathway plays a key role in plant immunity by activating defenses against fungal pathogens, while promoting bacterial growth by inhibiting the salicylic acid (SA)-dependent defenses required for Pseudomonas resistance. Here, we report that the effector HopX1 from a Pseudomonas syringae strain that does not produce COR exploits an alternative evolutionary strategy to activate the JA-Ile pathway. We show that HopX1 encodes a cysteine protease that interacts with and promotes the degradation of key JA pathway repressors, the JAZ proteins. Correspondingly, ectopically expressing HopX1 in the model plant Arabidopsis induces the expression of JA-dependent genes, and natural infection with Pseudomonas producing HopX1 promotes bacterial growth in a similar fashion to COR. Our results highlight a novel example by which a bacterial effector directly manipulates core regulators of hormone signaling to facilitate infection.
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影响因子：
2.8
作者：
Kakimoto, T
通讯作者：
Kakimoto, T
影响因子：
11.6
作者：
Chung, Hoo Sun;Howe, Gregg A.
通讯作者：
Howe, Gregg A.
DOI：
10.1073/pnas.0409468102
发表时间：
2005-02-08
影响因子：
11.1
作者：
Chisholm, ST;Dahlbeck, D;Staskawicz, BJ
通讯作者：
Staskawicz, BJ
DOI：
10.1074/jbc.m900519200
发表时间：
2009-06-05
期刊：
The Journal of biological chemistry
影响因子：
--
作者：
Dowen RH;Engel JL;Shao F;Ecker JR;Dixon JE
通讯作者：
Dixon JE
影响因子：
7.2
作者：
Clough, SJ;Bent, AF
通讯作者：
Bent, AF