Effector-Triggered Immunity Is a Key Component of Nonhost Resistance in Nicotiana benthamiana against the Rice Blast Pathogen Magnaporthe oryzae.

IF 2.5 3区 农林科学 Q2 PLANT SCIENCES
Jihyun Kim, Subin Lee, Min-Ki Seo, Dongmin Byun, Eunyoung Chae, Eunsook Park, Doil Choi
{"title":"Effector-Triggered Immunity Is a Key Component of Nonhost Resistance in Nicotiana benthamiana against the Rice Blast Pathogen Magnaporthe oryzae.","authors":"Jihyun Kim, Subin Lee, Min-Ki Seo, Dongmin Byun, Eunyoung Chae, Eunsook Park, Doil Choi","doi":"10.5423/PPJ.OA.02.2025.0024","DOIUrl":null,"url":null,"abstract":"<p><p>Magnaporthe oryzae is the causal agent of rice blast disease, a major threat to global food security. Although M. oryzae infects a broad range of monocotyledonous plants, it fails to colonize dicot species such as Nicotiana benthamiana, offering a useful system to investigate nonhost resistance (NHR). In this study, we characterized the immune responses of N. benthamiana to M. oryzae by profiling defense-related gene expression, analyzing fungal invasion, and functionally dissecting key immune components. Time-course expression analyses revealed sustained upregulation of NbBAK1, NbEAS, NbWRKY22, and NbPR1, alongside dynamic regulation of NbCYP71D20 and NbSGT1. Virus-induced gene silencing demonstrated that silencing of NbSGT1, but not NbEAS or NbBAK1, significantly enhanced fungal colonization. Furthermore, salicylic acid (SA)-deficient NahG plants exhibited increased susceptibility, suggesting that SA and SGT1-dependent immunity synergistically contribute to NHR. Visualization of infection using a GFP-expressing fungal strain confirmed that suppression of SGT1 and SA signaling facilitated hyphal expansion into adjacent host cells. High-throughput screening of 179 M. oryzae candidate effectors revealed that 70 induced hypersensitive response-like cell death in N. benthamiana, a response that was abrogated by NbSGT1 silencing. These findings collectively demonstrate that SA signaling and SGT1-dependent effector-triggered immunity are critical barriers against M. oryzae invasion and highlight the potential of nonhost immune components as resources for engineering durable resistance in crops.</p>","PeriodicalId":20173,"journal":{"name":"Plant Pathology Journal","volume":"41 4","pages":"472-483"},"PeriodicalIF":2.5000,"publicationDate":"2025-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12332412/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Plant Pathology Journal","FirstCategoryId":"97","ListUrlMain":"https://doi.org/10.5423/PPJ.OA.02.2025.0024","RegionNum":3,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0

Abstract

Magnaporthe oryzae is the causal agent of rice blast disease, a major threat to global food security. Although M. oryzae infects a broad range of monocotyledonous plants, it fails to colonize dicot species such as Nicotiana benthamiana, offering a useful system to investigate nonhost resistance (NHR). In this study, we characterized the immune responses of N. benthamiana to M. oryzae by profiling defense-related gene expression, analyzing fungal invasion, and functionally dissecting key immune components. Time-course expression analyses revealed sustained upregulation of NbBAK1, NbEAS, NbWRKY22, and NbPR1, alongside dynamic regulation of NbCYP71D20 and NbSGT1. Virus-induced gene silencing demonstrated that silencing of NbSGT1, but not NbEAS or NbBAK1, significantly enhanced fungal colonization. Furthermore, salicylic acid (SA)-deficient NahG plants exhibited increased susceptibility, suggesting that SA and SGT1-dependent immunity synergistically contribute to NHR. Visualization of infection using a GFP-expressing fungal strain confirmed that suppression of SGT1 and SA signaling facilitated hyphal expansion into adjacent host cells. High-throughput screening of 179 M. oryzae candidate effectors revealed that 70 induced hypersensitive response-like cell death in N. benthamiana, a response that was abrogated by NbSGT1 silencing. These findings collectively demonstrate that SA signaling and SGT1-dependent effector-triggered immunity are critical barriers against M. oryzae invasion and highlight the potential of nonhost immune components as resources for engineering durable resistance in crops.

效应触发免疫是本烟对稻瘟病菌非寄主抗性的关键组成部分。
稻瘟病是全球粮食安全的一大威胁,稻瘟病是稻瘟病的致病因子。虽然M. oryzae侵染广泛的单子叶植物,但它不能定殖于双子叶植物,如Nicotiana benthamiana,为研究非寄主抗性(NHR)提供了一个有用的系统。在这项研究中,我们通过分析防御相关基因表达,分析真菌入侵,以及功能解剖关键免疫成分来表征benthamiana对m.o ryzae的免疫反应。时间过程表达分析显示NbBAK1、NbEAS、NbWRKY22和NbPR1持续上调,同时NbCYP71D20和NbSGT1动态上调。病毒诱导的基因沉默表明,NbSGT1的沉默,而NbEAS或NbBAK1的沉默,显著增强了真菌的定植。此外,水杨酸(SA)缺乏的NahG植物表现出更高的敏感性,表明SA和sgt1依赖性免疫协同促进了NHR。利用表达gfp的真菌菌株对感染进行可视化观察证实,抑制SGT1和SA信号有助于菌丝向邻近宿主细胞扩展。对179种M. oryzae候选效应物的高通量筛选显示,70种诱导benthamiana的超敏反应样细胞死亡,这种反应被NbSGT1沉默所消除。这些发现共同表明,SA信号和sgt1依赖的效应物触发的免疫是抵抗m.o ryzae入侵的关键屏障,并突出了非宿主免疫成分作为工程作物持久抗性资源的潜力。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Plant Pathology Journal
Plant Pathology Journal 生物-植物科学
CiteScore
4.90
自引率
4.30%
发文量
71
审稿时长
12 months
期刊介绍: Information not localized
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:604180095
Book学术官方微信