A fungal effector suppresses the nuclear export of AGO1-miRNA complex to promote infection in plants.
A fungal effector suppresses the nuclear export of AGO1-miRNA complex to promote infection in plants.
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DOI：
10.1073/pnas.2114583119
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发表时间：
2022-03-22
影响因子：
11.1
通讯作者：
Duan CG
中科院分区：
文献类型：
--
作者：
Zhu C;Liu JH;Zhao JH;Liu T;Chen YY;Wang CH;Zhang ZH;Guo HS;Duan CG
越来越多的证据表明，小RNA可以作为运输效应子，在相互作用的生物体（包括植物病原真菌系统）中介导双向跨界RNA干扰（RNAi）。先前的研究结果表明，植物可以向真菌病原体大丽黄萎病发送 microRNA (miRNA)，从而触发抗真菌 RNAi。在这里，我们报道大丽花弧菌能够向植物细胞核分泌效应物，干扰 AGO1-miRNA 复合物的核输出，从而抑制抗真菌 RNA 干扰并增加植物的毒力。因此，我们揭示了一种拮抗机制，真菌病原体可以利用该机制通过操纵植物小RNA功能来抵消抗真菌RNAi免疫。相互作用的生物体之间通过生物活性分子进行的通讯在自然界中广泛存在，并在不同的生物过程中发挥着关键作用。小RNA (sRNA) 可以在宿主植物和丝状病原体之间传播，触发受体细胞中的跨界RNA 干扰(RNAi)，并调节植物防御和病原体毒力。然而，真菌病原体如何对抗跨界抗真菌 RNAi 却鲜有报道。在这里，我们发现来自大丽黄萎病的分泌蛋白 VdSSR1（分泌沉默阻遏蛋白 1）是植物中真菌毒力所必需的，大丽黄萎病是一种土传植物病原真菌，可在多种植物宿主中引起枯萎病。 VdSSR1 可以易位至植物细胞核并作为 sRNA 核质穿梭的一般抑制因子。我们进一步揭示，VdSSR1 隔离 ALY 家族蛋白（TREX 复合物的接头），干扰 AGO1-microRNA (AGO1-miRNA) 复合物的核输出，导致细胞质 AGO1 蛋白和 sRNA 水平大幅降低。通过这种机制，大丽弧菌可以抑制真菌细胞中移动植物miRNA的积累，并随后跨界沉默毒力基因，从而增加其在植物中的毒力。我们的研究结果揭示了植物病原真菌拮抗抗真菌 RNAi 依赖性植物免疫的机制，并扩大了对宿主和丝状病原体之间复杂相互作用的理解。
Increasing evidence demonstrates that small RNAs can serve as trafficking effectors to mediate bidirectional transkingdom RNA interference (RNAi) in interacting organisms, including plant–pathogenic fungi systems. Previous findings demonstrated that plants can send microRNAs (miRNAs) to fungal pathogen Verticillium dahliae to trigger antifungal RNAi. Here we report that V. dahliae is able to secret an effector to the plant nucleus to interfere with the nuclear export of AGO1–miRNA complexes, leading to an inhibition in antifungal RNAi and increased virulence in plants. Thus, we reveal an antagonistic mechanism that can be exploited by fungal pathogens to counteract antifungal RNAi immunity via manipulation of plant small RNA function. Communication between interacting organisms via bioactive molecules is widespread in nature and plays key roles in diverse biological processes. Small RNAs (sRNAs) can travel between host plants and filamentous pathogens to trigger transkingdom RNA interference (RNAi) in recipient cells and modulate plant defense and pathogen virulence. However, how fungal pathogens counteract transkingdom antifungal RNAi has rarely been reported. Here we show that a secretory protein VdSSR1 (secretory silencing repressor 1) from Verticillium dahliae, a soil-borne phytopathogenic fungus that causes wilt diseases in a wide range of plant hosts, is required for fungal virulence in plants. VdSSR1 can translocate to plant nucleus and serve as a general suppressor of sRNA nucleocytoplasmic shuttling. We further reveal that VdSSR1 sequesters ALY family proteins, adaptors of the TREX complex, to interfere with nuclear export of the AGO1–microRNA (AGO1–miRNA) complex, leading to a great attenuation in cytoplasmic AGO1 protein and sRNA levels. With this mechanism, V. dahliae can suppress the accumulation of mobile plant miRNAs in fungal cells and succedent transkingdom silencing of virulence genes, thereby increasing its virulence in plants. Our findings reveal a mechanism by which phytopathogenic fungi antagonize antifungal RNAi-dependent plant immunity and expand the understanding on the complex interaction between host and filamentous pathogens.
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影响因子：
6
作者：
Hegedues, Nikoletta;Marx, Florentine
通讯作者：
Marx, Florentine
影响因子：
30.8
作者：
Dunoyer, Patrice;Himber, Christophe;Voinnet, Olivier
通讯作者：
Voinnet, Olivier
DOI：
10.1126/science.aar4142
发表时间：
2018-06-08
期刊：
Science (New York, N.Y.)
影响因子：
--
作者：
Cai Q;Qiao L;Wang M;He B;Lin FM;Palmquist J;Huang SD;Jin H
通讯作者：
Jin H
影响因子：
7.2
作者：
Clough, SJ;Bent, AF
通讯作者：
Bent, AF
影响因子：
27.5
作者：
Cambiagno, Damian A.;Giudicatti, Axel J.;Manavella, Pablo A.
通讯作者：
Manavella, Pablo A.