Plant pathogen effector utilizes host susceptibility factor NRL1 to degrade the immune regulator SWAP70

First author: Qin He; Affiliations: University of Dundee (邓迪大学): Dundee, United Kingdom

Corresponding author: Paul R. J. Birch

Plant pathogens deliver effectors into plant cells to suppress immunity. Whereas many effectors inactivate positive immune regulators, other effectors associate with negative regulators of immunity: so-called susceptibility (S) factors. Little is known about how pathogens exploit S factors to suppress immunity. Phytophthora infestans (致病疫霉) RXLR effector Pi02860 interacts with host protein NRL1, which is an S factor whose activity suppresses INF1-triggered cell death (ICD) and is required for late blight disease (晚疫病). We show that NRL1 interacts in yeast and in planta with a guanine nucleotide exchange factor called SWAP70. SWAP70 associates with endosomes (核内体) and is a positive regulator of immunity. Virus-induced gene silencing of SWAP70 in Nicotiana benthamiana enhances P. infestans colonization and compromises ICD. In contrast, transient overexpression of SWAP70 reduces P. infestans infection and accelerates ICD. Expression of Pi02860 and NRL1, singly or in combination, results in proteasome-mediated degradation of SWAP70. Degradation of SWAP70 is prevented by silencing NRL1, or by mutation of Pi02860 to abolish its interaction with NRL1. NRL1 is a BTB-domain protein predicted to form the substrate adaptor component of a CULLIN3 ubiquitin E3 ligase. A dimerization-deficient mutant, NRL1NQ, fails to interact with SWAP70 but maintains its interaction with Pi02860. NRL1NQ acts as a dominant-negative mutant, preventing SWAP70 degradation in the presence of effector Pi02860, and reducing P. infestans infection. Critically, Pi02860 enhances the association between NRL1 and SWAP70 to promote proteasome-mediated degradation of the latter and, thus, suppress immunity. Preventing degradation of SWAP70 represents a strategy to combat late blight disease.

植物病原菌会将效应物递送进植物细胞中以抑制植物的免疫。许多效应物能够抑制植物中那些正向免疫调控子，而也有许多效应物与植物免疫负向调控子相关，叫做易感因子（S因子）。而关于病原菌如何利用S因子来抑制植物免疫的还所知甚少。致病疫霉RXLR效应物Pi02860与寄主蛋白NRL1相互作用，而NRL1蛋白植物中的一个S因子，其活性能够抑制INF1诱导的细胞死亡（ICD），并且对于晚疫病的病发是必需的。本文的研究显示NRL1蛋白在酵母和植物体内均能够与鸟嘌呤核苷酸交换因子SWAP70互作。SWAP70与核内体相关，且是植物免疫的正向调控蛋白。在烟草中利用病毒诱导的SWAP70基因沉默能够增强致病疫霉殖民化，并且能够损伤植物中的ICD。相反，过表达SWAP70基因能够降低致病疫霉的侵染，加速ICD。Pi02860和NRL1单个或者一起表达均导致蛋白酶体说介导的SWAP70的降解。而通过沉默NRL1基因，或者是通过突变掉Pi02860以破坏其与NRL1蛋白的互作，均能够防止SWAP70降解。NRL1蛋白是一个含BTB结构域的蛋白，是CULLIN3泛素E3连接酶的底物。NRL1蛋白的二聚缺陷突变NRL1NQ与SWAP70蛋白的互作功能缺失，但与Pi02860互作的功能仍然保留。NRL1NQ作为显性负突变体，在Pi02860存在的情况下可以防止SWAP70蛋白的降解，进而减少致病疫霉的侵染。重要的是，Pi02860增强了NRL1蛋白与SWAP70之间的互作，促进蛋白酶体说介导的SWAP70的降解，从而抑制植物中的免疫。防止SWAP70的降解是一种防治晚疫病的有效策略。

通讯：Paul R. J. Birch (http://www.lifesci.dundee.ac.uk/people/paul-birch)

研究方向：植物病原菌效应物与寄主的互作。

doi: https://doi.org/10.1073/pnas.1808585115

Journal: PNAS

Published date: 26 July, 2018

（P.S. 原文下载：链接:https://pan.baidu.com/s/1qFiSsqwlF_7JjmGMbedfhQ  密码:dmu6）