SDE19, a SEC-dependent effector from ‘Candidatus Liberibacter asiaticus’ suppresses plant immunity and targets Citrus sinensis Sec12 to interfere with vesicle trafficking

IF 6.7 1区 医学 Q1 Immunology and Microbiology
Guiyan Huang, Xiaopeng Chang, Yanan Hu, Fuxuan Li, Nian Wang, Ruimin Li
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引用次数: 0

Abstract

Citrus huanglongbing (HLB), which is caused by the phloem-colonizing bacteria Candidatus Liberibacter asiaticus (CLas), poses a significant threat to citrus production worldwide. The pathogenicity mechanism of HLB remains poorly understood. SEC-dependent effectors (SDEs) have been suggested to play critical roles in the interaction between citrus and CLas. Here, we explored the function of CLIBASIA_05320 (SDE19), a core SDE from CLas, and its interaction with its host target. Our data revealed that SDE19 is expressed at higher level during infection of citrus than that during infection of the Asian citrus psyllid. Subcellular localization assays showed that SDE19 is localized in the nucleus and cytoplasm and is capable of moving from cell to cell in Nicotiana benthamiana. To investigate whether SDE19 facilitates pathogen infection, we generated transgenic Arabidopsis thaliana and citrus plants overexpressing SDE19. Transgenic A. thaliana and citrus plants were more susceptible to Pseudomonas syringae pv. tomato (Pst) and Xanthomonas citri subsp. citri (Xcc), respectively. In addition, RNA-seq analysis demonstrated that overexpression of SDE19 resulted in a reprogramming of expression of genes related to biotic stimulus responses. SDE19 interacts with Citrus sinensis Sec12, a guanine nucleotide exchange factor responsible for the assembly of plant COPII (coat protein II)-coated vesicles, which mediate vesicle trafficking from the ER to the Golgi. SDE19 colocalizes with Sec12 in the ER by binding to its N-terminal catalytic region, affecting the stability of Sec12 through the 26S proteasome. This interaction hinders the secretion of apoplastic defense-related proteins such as PR1, P69B, GmGIP1, and RCR3. Furthermore, the secretion of PR1 and callose deposition is decreased in SDE19-transgenic A. thaliana. Taken together, SDE19 is a novel virulent SDE secreted by CLas that interacts with Sec12 to disrupt vesicle trafficking, inhibit defense-related proteins secretion, and promote bacterial infection. This study sheds light on how CLas manipulates the host vesicle trafficking pathway to suppress the secretion of defense-related proteins and interfere with plant immunity.
SDE19是一种来自 "亚洲自由杆菌 "的依赖于SEC的效应子,可抑制植物免疫,并以柑橘Sec12为目标干扰囊泡贩运
柑橘黄龙病(HLB)是由韧皮部定殖细菌 Candidatus Liberibacter asiaticus(CLas)引起的,对全球柑橘生产构成严重威胁。人们对 HLB 的致病机制仍然知之甚少。有研究表明,SEC 依赖性效应器(SDEs)在柑橘与 CLas 的相互作用中发挥着关键作用。在此,我们探讨了 CLas 的核心 SDE CLIBASIA_05320(SDE19)的功能及其与宿主靶标的相互作用。我们的数据显示,SDE19在柑橘感染过程中的表达水平高于在亚洲柑橘虫害感染过程中的表达水平。亚细胞定位分析表明,SDE19定位于细胞核和细胞质中,并能在烟草中的细胞间移动。为了研究 SDE19 是否有助于病原体感染,我们生成了过表达 SDE19 的转基因拟南芥和柑橘植株。转基因拟南芥和柑橘植株分别对西红柿假单胞菌(Pst)和柠檬黄单胞菌亚种(Xcc)更敏感。此外,RNA-seq分析表明,SDE19的过表达导致与生物刺激反应相关的基因表达重编程。SDE19与Citrus sinensis Sec12相互作用,后者是一种鸟嘌呤核苷酸交换因子,负责组装植物COPII(衣壳蛋白II)包裹的囊泡,介导囊泡从ER向高尔基体的迁移。SDE19 通过与其 N 端催化区结合,在 ER 中与 Sec12 共定位,通过 26S 蛋白酶体影响 Sec12 的稳定性。这种相互作用阻碍了 PR1、P69B、GmGIP1 和 RCR3 等细胞凋亡防御相关蛋白的分泌。此外,在 SDE19 转基因的拟南芥中,PR1 的分泌和胼胝质的沉积都有所减少。综上所述,SDE19是一种由CLas分泌的新型毒性SDE,它能与Sec12相互作用,破坏囊泡贩运,抑制防御相关蛋白的分泌,促进细菌感染。这项研究揭示了CLas如何操纵宿主囊泡贩运途径,从而抑制防御相关蛋白的分泌,干扰植物免疫。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
PLoS Pathogens
PLoS Pathogens 生物-病毒学
CiteScore
11.40
自引率
3.00%
发文量
598
审稿时长
2 months
期刊介绍: Bacteria, fungi, parasites, prions and viruses cause a plethora of diseases that have important medical, agricultural, and economic consequences. Moreover, the study of microbes continues to provide novel insights into such fundamental processes as the molecular basis of cellular and organismal function.
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