Fungal Argonaute proteins act in bidirectional cross-kingdom RNA interference during plant infection

IF 9.1 1区综合性期刊 Q1 MULTIDISCIPLINARY SCIENCES Proceedings of the National Academy of Sciences of the United States of America Pub Date : 2025-04-23 DOI:10.1073/pnas.2422756122

An-Po Cheng, Lihong Huang, Lorenz Oberkofler, Nathan R. Johnson, Adrian-Stefan Glodeanu, Kyra Stillman, Arne Weiberg

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Abstract

Argonaute (AGO) proteins bind to small RNAs to induce RNA interference (RNAi), a conserved gene regulatory mechanism in animal, plant, and fungal kingdoms. Small RNAs of the fungal plant pathogen Botrytis cinerea were previously shown to translocate into plant cells and to bind to the host AGO, which induced cross-kingdom RNAi to promote infection. However, the role of pathogen AGOs during host infection stayed elusive. In this study, we revealed that members of fungal plant pathogen B. cinerea BcAGO family contribute to plant infection. BcAGO1 binds to both fungal and plant small RNAs during infection and acts in bidirectional cross-kingdom RNAi, from fungus to plant and vice versa. BcAGO2 also binds fungal and plant small RNAs but acts independent from BcAGO1 by regulating distinct genes. Nevertheless, BcAGO2 is important for infection, as it is required for effective pathogen small RNA delivery into host cells and fungal induced cross-kingdom RNAi. Providing these mechanistic insights of pathogen AGOs promises to improve RNAi-based crop protection strategies.

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真菌Argonaute蛋白在植物侵染过程中参与双向跨界RNA干扰

Argonaute （AGO）蛋白结合小RNA诱导RNA干扰（RNAi），这是一种在动物、植物和真菌王国中保守的基因调控机制。植物真菌病原体灰霉病菌（Botrytis cinerea）的小rna先前被证明可以转运到植物细胞中并与宿主AGO结合，从而诱导跨界RNAi促进感染。然而，病原体AGOs在宿主感染过程中的作用尚不清楚。在这项研究中，我们揭示了真菌植物病原体B. cinerea BcAGO家族成员参与植物感染。BcAGO1在感染过程中与真菌和植物的小rna结合，并在真菌到植物的双向跨界RNAi中起作用，反之亦然。BcAGO2也结合真菌和植物小rna，但通过调节不同的基因独立于BcAGO2起作用。然而，BcAGO2对感染很重要，因为它是病原体小RNA有效递送到宿主细胞和真菌诱导的跨界RNAi所必需的。提供病原体AGOs的这些机制见解有望改善基于rnai的作物保护策略。

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来源期刊

Proceedings of the National Academy of Sciences of the United States of America 综合性期刊-综合性期刊

CiteScore

19.00

自引率

0.90%

发文量

3575

审稿时长

2.5 months

期刊介绍： The Proceedings of the National Academy of Sciences (PNAS), a peer-reviewed journal of the National Academy of Sciences (NAS), serves as an authoritative source for high-impact, original research across the biological, physical, and social sciences. With a global scope, the journal welcomes submissions from researchers worldwide, making it an inclusive platform for advancing scientific knowledge.