Volatile compounds (VCs) emitted by the fungal phytopathogen Penicillium aurantiogriseum promote root growth and developmental changes in Arabidopsis. Here we characterised the metabolic and molecular responses of roots to fungal volatiles. Proteomic analyses revealed that these compounds reduce the levels of aquaporins, the iron carrier IRT1 and apoplastic peroxidases. Fungal VCs also increased the levels of enzymes involved in the production of mevalonate (MVA)-derived isoprenoids, nitrogen assimilation and conversion of methionine to ethylene and cyanide. Consistently, fungal VC-treated roots accumulated high levels of hydrogen peroxide (H2 O2 ), MVA-derived cytokinins, ethylene, cyanide and long-distance nitrogen transport amino acids. qRT-PCR analyses showed that many proteins differentially expressed by fungal VCs are encoded by VC non-responsive genes. Expression patterns of hormone reporters and developmental characterisation of mutants provided evidence for the involvement of cyanide scavenging and enhanced auxin, ethylene, cytokinin and H2 O2 signalling in the root architecture changes promoted by fungal VCs. Our findings show that VCs from P. aurantiogriseum modify root metabolism and architecture, and improve nutrient and water use efficiencies through transcriptionally and non-transcriptionally regulated proteome resetting mechanisms. Some of these mechanisms are subject to long-distance regulation by photosynthesis and differ from those triggered by VCs emitted by beneficial microorganisms.

Department of Chemical Biology and Genetics Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University Olomouc CZ 78371 Czech Republic

Instituto de Agrobiotecnología Mutilva 31192 Spain

Instituto de Bioquímica Vegetal y Fotosíntesis Consejo Superior de Investigaciones Científicas and Universidad de Sevilla Sevilla 41092 Spain

Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben 06466 Germany

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Glucose-6-P/phosphate translocator2 mediates the phosphoglucose-isomerase1-independent response to microbial volatiles

Enhanced Yield of Pepper Plants Promoted by Soil Application of Volatiles From Cell-Free Fungal Culture Filtrates Is Associated With Activation of the Beneficial Soil Microbiota

Proteostatic Regulation of MEP and Shikimate Pathways by Redox-Activated Photosynthesis Signaling in Plants Exposed to Small Fungal Volatiles