Suboptimal pre-anthesis water status mitigates wheat susceptibility to fusarium head blight and triggers specific metabolic responses

Abstract The impact of abiotic challenges on plant physiology reshapes plant-pathogen interactions by modulating the plant immune responses. In wheat, the development of Fusarium Head Blight (FHB) is heavily influenced by environmental conditions, especially during the pre-anthesis stage, just befor...

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Main Authors: Larissa Adamik, Paul Samir Dou, Géraldine Philippe, Richard Blanc, Pedro Vásquez-Ocmín, Guillaume Marti, Thierry Langin, Ludovic Bonhomme
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-025-96159-4
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author Larissa Adamik
Paul Samir Dou
Géraldine Philippe
Richard Blanc
Pedro Vásquez-Ocmín
Guillaume Marti
Thierry Langin
Ludovic Bonhomme
author_facet Larissa Adamik
Paul Samir Dou
Géraldine Philippe
Richard Blanc
Pedro Vásquez-Ocmín
Guillaume Marti
Thierry Langin
Ludovic Bonhomme
author_sort Larissa Adamik
collection DOAJ
description Abstract The impact of abiotic challenges on plant physiology reshapes plant-pathogen interactions by modulating the plant immune responses. In wheat, the development of Fusarium Head Blight (FHB) is heavily influenced by environmental conditions, especially during the pre-anthesis stage, just before fungal infection occurs. The early stages of infection are thus likely conditioned by prior environmental changes with consequences on the disease outcome that require further characterization. In this study, we aimed to assess the impact of pre-anthesis water depletion followed by rapid rehydration at inoculation on the expression of FHB-related molecular determinants with emphasis on susceptibility factors and metabolism-related processes. Water depletion altered plant physiology and its effects remained detectable after three days after rehydration, leading to significantly reduced FHB symptoms. Dual-transcriptomics, combined with untargeted metabolomics, revealed two key findings including (i) extensive metabolic changes specific to prior water stress, and (ii) the strong conservation of previously identified candidate susceptibility genes regulation. Considering the combined stress effects, a unique response signature emerged, highlighting that immune responses are strongly interwoven with physiological adjustments. Our findings provide new insights into the trade-offs that plants make under multiple challenges and identify original wheat metabolic determinants that may improve FHB resistance even in suboptimal physiological conditions.
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spelling doaj-art-b6bc52c96fa04309a4173ec36749d16a2025-08-20T02:12:06ZengNature PortfolioScientific Reports2045-23222025-04-0115111410.1038/s41598-025-96159-4Suboptimal pre-anthesis water status mitigates wheat susceptibility to fusarium head blight and triggers specific metabolic responsesLarissa Adamik0Paul Samir Dou1Géraldine Philippe2Richard Blanc3Pedro Vásquez-Ocmín4Guillaume Marti5Thierry Langin6Ludovic Bonhomme7Université Clermont Auvergne, INRAE, GDECUniversité Clermont Auvergne, INRAE, GDECUniversité Clermont Auvergne, INRAE, GDECUniversité Clermont Auvergne, INRAE, GDECMetaboHUB-MetaToul, National Infrastructure of Metabolomics and FluxomicsMetaboHUB-MetaToul, National Infrastructure of Metabolomics and FluxomicsUniversité Clermont Auvergne, INRAE, GDECUniversité Clermont Auvergne, INRAE, GDECAbstract The impact of abiotic challenges on plant physiology reshapes plant-pathogen interactions by modulating the plant immune responses. In wheat, the development of Fusarium Head Blight (FHB) is heavily influenced by environmental conditions, especially during the pre-anthesis stage, just before fungal infection occurs. The early stages of infection are thus likely conditioned by prior environmental changes with consequences on the disease outcome that require further characterization. In this study, we aimed to assess the impact of pre-anthesis water depletion followed by rapid rehydration at inoculation on the expression of FHB-related molecular determinants with emphasis on susceptibility factors and metabolism-related processes. Water depletion altered plant physiology and its effects remained detectable after three days after rehydration, leading to significantly reduced FHB symptoms. Dual-transcriptomics, combined with untargeted metabolomics, revealed two key findings including (i) extensive metabolic changes specific to prior water stress, and (ii) the strong conservation of previously identified candidate susceptibility genes regulation. Considering the combined stress effects, a unique response signature emerged, highlighting that immune responses are strongly interwoven with physiological adjustments. Our findings provide new insights into the trade-offs that plants make under multiple challenges and identify original wheat metabolic determinants that may improve FHB resistance even in suboptimal physiological conditions.https://doi.org/10.1038/s41598-025-96159-4Bread wheatFHB susceptibilityWater stressSpecialized metabolismMulti-stress genomics
spellingShingle Larissa Adamik
Paul Samir Dou
Géraldine Philippe
Richard Blanc
Pedro Vásquez-Ocmín
Guillaume Marti
Thierry Langin
Ludovic Bonhomme
Suboptimal pre-anthesis water status mitigates wheat susceptibility to fusarium head blight and triggers specific metabolic responses
Scientific Reports
Bread wheat
FHB susceptibility
Water stress
Specialized metabolism
Multi-stress genomics
title Suboptimal pre-anthesis water status mitigates wheat susceptibility to fusarium head blight and triggers specific metabolic responses
title_full Suboptimal pre-anthesis water status mitigates wheat susceptibility to fusarium head blight and triggers specific metabolic responses
title_fullStr Suboptimal pre-anthesis water status mitigates wheat susceptibility to fusarium head blight and triggers specific metabolic responses
title_full_unstemmed Suboptimal pre-anthesis water status mitigates wheat susceptibility to fusarium head blight and triggers specific metabolic responses
title_short Suboptimal pre-anthesis water status mitigates wheat susceptibility to fusarium head blight and triggers specific metabolic responses
title_sort suboptimal pre anthesis water status mitigates wheat susceptibility to fusarium head blight and triggers specific metabolic responses
topic Bread wheat
FHB susceptibility
Water stress
Specialized metabolism
Multi-stress genomics
url https://doi.org/10.1038/s41598-025-96159-4
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