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

Felix Getzke, Lei Wang, Guillaume Chesneau, Nils Böhringer, Fantin Mesny, Nienke Denissen, Hidde Wesseler, Priscilla Tijesuni Adisa, Michael Marner, Paul Schulze-Lefert, Till F. Schäberle () and Stéphane Hacquard ()
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Felix Getzke: Max Planck Institute for Plant Breeding Research
Lei Wang: Justus-Liebig-University Giessen
Guillaume Chesneau: Max Planck Institute for Plant Breeding Research
Nils Böhringer: Justus-Liebig-University Giessen
Fantin Mesny: Max Planck Institute for Plant Breeding Research
Nienke Denissen: Max Planck Institute for Plant Breeding Research
Hidde Wesseler: Max Planck Institute for Plant Breeding Research
Priscilla Tijesuni Adisa: Max Planck Institute for Plant Breeding Research
Michael Marner: Branch for Bioresources
Paul Schulze-Lefert: Max Planck Institute for Plant Breeding Research
Till F. Schäberle: Justus-Liebig-University Giessen
Stéphane Hacquard: Max Planck Institute for Plant Breeding Research

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract 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.

Date: 2024
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DOI: 10.1038/s41467-024-48517-5

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