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

Summary

Scientists discovered that fungi and plants exchange genetic instructions called small RNAs to control each other during infection. A fungal pathogen called Botrytis cinerea uses special proteins called Argonautes to deliver these instructions into plant cells, which helps the fungus cause disease. Plants also send back their own genetic instructions to defend themselves. Understanding these molecular communications could lead to new ways to protect crops from fungal diseases.

Background

Cross-kingdom RNA interference (RNAi) is an emerging mechanism in plant-microbe interactions where pathogens and hosts exchange small RNAs to modulate gene expression. Argonaute (AGO) proteins are key factors in RNAi pathways that bind small RNAs to induce gene silencing. Previously, fungal small RNAs from Botrytis cinerea were shown to target plant immunity genes, but the role of pathogen AGOs in this process remained unclear.

Objective

To characterize the functional roles of Botrytis cinerea AGO (BcAGO) proteins in bidirectional cross-kingdom RNAi during plant infection. The study aimed to determine how different BcAGO family members contribute to fungal virulence and cross-kingdom RNAi mechanisms.

Results

BcAGO1 was required for fungal small RNA (BcsRNA) accumulation and mediates bidirectional cross-kingdom RNAi, acting on both fungal and plant small RNAs during infection. BcAGO2 was essential for effective delivery of BcsRNAs into plant cells and is a pathogenicity factor. The study identified at least 21 tomato-derived small RNAs that bind to BcAGOs and suppress fungal virulence genes during infection.

Conclusion

Different BcAGO family members have diversified functions in bidirectional cross-kingdom RNAi during plant infection. The findings provide mechanistic insights into how pathogen AGOs regulate both fungal virulence and host immunity suppression, which could inform the development of novel RNA-based strategies for crop protection.
  • Published in:Proceedings of the National Academy of Sciences USA,
  • Study Type:Experimental Research,
  • Source: PMID: 40267130, DOI: 10.1073/pnas.2422756122
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