Physiochemical interaction between osmotic stress and a bacterial exometabolite promotes plant disease

Various microbes isolated from healthy plants are detrimental under laboratory conditions, indicating the existence of molecular mechanisms preventing disease in nature. Here, we demonstrated that application of sodium chloride (NaCl) in natural and gnotobiotic soil systems is sufficient to induce p...

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Published in:	Nature communications Vol. 15; no. 1; p. 4438
Main Authors:	Getzke, Felix, Wang, Lei, Chesneau, Guillaume, Böhringer, Nils, Mesny, Fantin, Denissen, Nienke, Wesseler, Hidde, Adisa, Priscilla Tijesuni, Marner, Michael, Schulze-Lefert, Paul, Schäberle, Till F., Hacquard, Stéphane
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 28-05-2024 Nature Publishing Group Nature Portfolio
Subjects:	38/109 38/91 45 45/22 45/41 45/70 45/77 45/90 631/326/41/2531 631/449/2169 631/449/2661/1797 64 Arabidopsis - drug effects Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis - microbiology Combinatorial analysis Gnotobiotic Homeostasis Host plants Humanities and Social Sciences Lipopeptides - metabolism Lipopeptides - pharmacology Microbiomes Molecular modelling multidisciplinary Opportunist infection Osmotic Pressure Osmotic stress Physiochemistry Plant diseases Plant Diseases - microbiology Plant Roots - metabolism Plant Roots - microbiology Pseudomonas - genetics Pseudomonas - metabolism Salts Science Science (multidisciplinary) Sodium chloride Sodium Chloride - metabolism Sodium Chloride - pharmacology Soil Microbiology
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Summary:	Various microbes isolated from healthy plants are detrimental under laboratory conditions, indicating the existence of molecular mechanisms preventing disease in nature. Here, we demonstrated that application of sodium chloride (NaCl) in natural and gnotobiotic soil systems is sufficient to induce plant disease caused by an otherwise non-pathogenic root-derived Pseudomonas brassicacearum isolate (R401). Disease caused by combinatorial treatment of NaCl and R401 triggered extensive, root-specific transcriptional reprogramming that did not involve down-regulation of host innate immune genes, nor dampening of ROS-mediated immunity. Instead, we identified and structurally characterized the R401 lipopeptide brassicapeptin A as necessary and sufficient to promote disease on salt-treated plants. Brassicapeptin A production is salt-inducible, promotes root colonization and transitions R401 from being beneficial to being detrimental on salt-treated plants by disturbing host ion homeostasis, thereby bolstering susceptibility to osmolytes. We conclude that the interaction between a global change stressor and a single exometabolite from a member of the root microbiome promotes plant disease in complex soil systems. A single exometabolite produced by an opportunistic bacterial pathogen of the root microbiome enhances host susceptibility to salt stress and promotes plant disease in complex soil systems.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
ISSN:	2041-1723 2041-1723
DOI:	10.1038/s41467-024-48517-5