Exogenous dsRNA triggers sequence-specific RNAi and fungal stress responses to control Magnaporthe oryzae in Brachypodium distachyon

Abstract In vertebrates and plants, dsRNA plays crucial roles as PAMP and as a mediator of RNAi. How higher fungi respond to dsRNA is not known. We demonstrate that Magnaporthe oryzae (Mo), a globally significant crop pathogen, internalizes dsRNA across a broad size range of 21 to about 3000 bp. Inc...

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Main Authors: Ying Zheng, Benjamin Moorlach, Desiree Jakobs-Schönwandt, Anant Patel, Chiara Pastacaldi, Stefan Jacob, Ana R. Sede, Manfred Heinlein, Minna M. Poranen, Karl-Heinz Kogel, Maria Ladera Carmona
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-025-07554-6
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author Ying Zheng
Benjamin Moorlach
Desiree Jakobs-Schönwandt
Anant Patel
Chiara Pastacaldi
Stefan Jacob
Ana R. Sede
Manfred Heinlein
Minna M. Poranen
Karl-Heinz Kogel
Maria Ladera Carmona
author_facet Ying Zheng
Benjamin Moorlach
Desiree Jakobs-Schönwandt
Anant Patel
Chiara Pastacaldi
Stefan Jacob
Ana R. Sede
Manfred Heinlein
Minna M. Poranen
Karl-Heinz Kogel
Maria Ladera Carmona
author_sort Ying Zheng
collection DOAJ
description Abstract In vertebrates and plants, dsRNA plays crucial roles as PAMP and as a mediator of RNAi. How higher fungi respond to dsRNA is not known. We demonstrate that Magnaporthe oryzae (Mo), a globally significant crop pathogen, internalizes dsRNA across a broad size range of 21 to about 3000 bp. Incubation of fungal conidia with 10 ng/µL dsRNA, regardless of size or sequence, induced aberrant germ tube elongation, revealing a strong sequence-unspecific effect of dsRNA in this fungus. Accordingly, the synthetic dsRNA analogue poly(I:C) and dsRNA of various sizes and sequences elicited canonical fungal stress pathways, including nuclear accumulation of the stress marker mitogen-activated protein kinase Hog1p and production of ROS. Leaf application of dsRNA to the cereal model species Brachypodium distachyon suppressed the progression of leaf blast disease. Notably, the sequence-unspecific effect of dsRNA depends on higher doses, while pure sequence-specific effects were observed at low concentrations of dsRNA ( < 0.03 ng/µL). The protective effects of dsRNA were further enhanced by maintaining a gap of at least seven days between dsRNA application and inoculation, and by stabilising the dsRNA in alginate-chitosan nanoparticles. Overall, our study opens up additional possibilities for the development and use of dsRNA pesticides in agriculture.
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spelling doaj-art-0f8bb8d80ba44dad83e27014d5c9fd942025-01-26T12:48:01ZengNature PortfolioCommunications Biology2399-36422025-01-018111410.1038/s42003-025-07554-6Exogenous dsRNA triggers sequence-specific RNAi and fungal stress responses to control Magnaporthe oryzae in Brachypodium distachyonYing Zheng0Benjamin Moorlach1Desiree Jakobs-Schönwandt2Anant Patel3Chiara Pastacaldi4Stefan Jacob5Ana R. Sede6Manfred Heinlein7Minna M. Poranen8Karl-Heinz Kogel9Maria Ladera Carmona10Institute of Phytopathology, Research Centre for BioSystems, Land Use and Nutrition, Justus Liebig University Giessen, Heinrich-Buff-Ring 26Fermentation and Formulation of Biologicals and Chemicals, Bielefeld Institute of Applied Materials Research, Bielefeld University of Applied Sciences, Interaktion 1Fermentation and Formulation of Biologicals and Chemicals, Bielefeld Institute of Applied Materials Research, Bielefeld University of Applied Sciences, Interaktion 1Fermentation and Formulation of Biologicals and Chemicals, Bielefeld Institute of Applied Materials Research, Bielefeld University of Applied Sciences, Interaktion 1Institute of Phytopathology, Research Centre for BioSystems, Land Use and Nutrition, Justus Liebig University Giessen, Heinrich-Buff-Ring 26Institute of Biotechnology and Drug Research, Hanns-Dieter-Hüsch-Weg 17Institut de biologie moléculaire des plantes, CNRS, Université de Strasbourg, 12 rue du Général ZimmerInstitut de biologie moléculaire des plantes, CNRS, Université de Strasbourg, 12 rue du Général ZimmerMolecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of HelsinkiInstitut de biologie moléculaire des plantes, CNRS, Université de Strasbourg, 12 rue du Général ZimmerInstitute of Phytopathology, Research Centre for BioSystems, Land Use and Nutrition, Justus Liebig University Giessen, Heinrich-Buff-Ring 26Abstract In vertebrates and plants, dsRNA plays crucial roles as PAMP and as a mediator of RNAi. How higher fungi respond to dsRNA is not known. We demonstrate that Magnaporthe oryzae (Mo), a globally significant crop pathogen, internalizes dsRNA across a broad size range of 21 to about 3000 bp. Incubation of fungal conidia with 10 ng/µL dsRNA, regardless of size or sequence, induced aberrant germ tube elongation, revealing a strong sequence-unspecific effect of dsRNA in this fungus. Accordingly, the synthetic dsRNA analogue poly(I:C) and dsRNA of various sizes and sequences elicited canonical fungal stress pathways, including nuclear accumulation of the stress marker mitogen-activated protein kinase Hog1p and production of ROS. Leaf application of dsRNA to the cereal model species Brachypodium distachyon suppressed the progression of leaf blast disease. Notably, the sequence-unspecific effect of dsRNA depends on higher doses, while pure sequence-specific effects were observed at low concentrations of dsRNA ( < 0.03 ng/µL). The protective effects of dsRNA were further enhanced by maintaining a gap of at least seven days between dsRNA application and inoculation, and by stabilising the dsRNA in alginate-chitosan nanoparticles. Overall, our study opens up additional possibilities for the development and use of dsRNA pesticides in agriculture.https://doi.org/10.1038/s42003-025-07554-6
spellingShingle Ying Zheng
Benjamin Moorlach
Desiree Jakobs-Schönwandt
Anant Patel
Chiara Pastacaldi
Stefan Jacob
Ana R. Sede
Manfred Heinlein
Minna M. Poranen
Karl-Heinz Kogel
Maria Ladera Carmona
Exogenous dsRNA triggers sequence-specific RNAi and fungal stress responses to control Magnaporthe oryzae in Brachypodium distachyon
Communications Biology
title Exogenous dsRNA triggers sequence-specific RNAi and fungal stress responses to control Magnaporthe oryzae in Brachypodium distachyon
title_full Exogenous dsRNA triggers sequence-specific RNAi and fungal stress responses to control Magnaporthe oryzae in Brachypodium distachyon
title_fullStr Exogenous dsRNA triggers sequence-specific RNAi and fungal stress responses to control Magnaporthe oryzae in Brachypodium distachyon
title_full_unstemmed Exogenous dsRNA triggers sequence-specific RNAi and fungal stress responses to control Magnaporthe oryzae in Brachypodium distachyon
title_short Exogenous dsRNA triggers sequence-specific RNAi and fungal stress responses to control Magnaporthe oryzae in Brachypodium distachyon
title_sort exogenous dsrna triggers sequence specific rnai and fungal stress responses to control magnaporthe oryzae in brachypodium distachyon
url https://doi.org/10.1038/s42003-025-07554-6
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