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The barley powdery mildew disease caused by the biotrophic fungus Blumeria hordei (Bh) poses enormous risks to crop production due to yield and quality losses. Plants and fungi can produce and release volatile organic compounds (VOCs) that serve as signals in plant communication and defense response to protect themselves. The present study aims to identify VOCs released by barley (Hordeum vulgare) during Bh‐infection and to decipher VOC‐induced disease resistance in receiver plants. VOC profiles of susceptible MLO wild type (MLO WT) and a resistant near‐isogenic backcross line (mlo5) were characterized over time (one day or three days after Bh inoculation) using TD‐GC/MS. Comparative analysis revealed genotype‐dependent VOC profiles and significant differences in emission rates for β‐caryophyllene, linalool, (Z)‐3‐hexenol, and methyl salicylate. Furthermore, susceptible barley plants were exposed to the complex VOC bouquet of MLO WT or mlo5 sender plants in plant‐to‐plant communication. We found that VOC‐induced resistance in receiver plants depended on the sender genotype in a Bh susceptibility assay. Additionally, untargeted metabolomics and gene expression studies provide evidence toward an SA‐dependent pathway mediating VOC‐induced resistance against powdery mildew. The exogenous application of methyl salicylate resulted in the enhanced expression of the BARLEY CHEMICALLY INDUCED‐4 marker gene and induced resistance in receiver plants. The findings suggest genotype‐dependent alterations in barley VOC profiles during biotrophic plant‐fungus interactions and show a VOC‐mediated resistance that shares components with salicylic acid‐related pathways. The VOC signals identified here could serve as non‐invasive markers for disease progression in barley‐powdery mildew interactions and as signals for resistance induction in recipient plants. [ABSTRACT FROM AUTHOR]

Infected barley plants send airborne cues that are recognized as defence signals in conspecific neighbours. β-Ionone and nonanal from the volatile blend of infected barley contribute to defence priming. Plants activate biochemical responses to combat stress. (Hemi-)biotrophic pathogens are fended off by systemic acquired resistance (SAR), a primed state allowing plants to respond faster and more strongly upon subsequent infection. Here, we show that SAR-like defences in barley (Hordeum vulgare) are propagated between neighbouring plants, which respond with enhanced resistance to the volatile cues from infected senders. The emissions of the sender plants contained 15 volatile organic compounds (VOCs) associated with infection. Two of these, β-ionone and nonanal, elicited resistance upon plant exposure. Whole-genome transcriptomics analysis confirmed that interplant propagation of defence in barley is established as a form of priming. Although gene expression changes were more pronounced after challenge infection of the receiver plants with Blumeria graminis f. sp. hordei, differential gene expression in response to the volatile cues of the sender plants included an induction of HISTONE DEACETYLASE 2 (HvHDA2) and priming of TETRATRICOPEPTIDE REPEAT-LIKE superfamily protein (HvTPL). Because HvHDA2 and HvTPL transcript accumulation was also enhanced by exposure of barley to β-ionone and nonanal, our data identify both genes as possible defence/priming markers in barley. Our results suggest that VOCs and plant–plant interactions are relevant for possible crop protection strategies priming defence responses in barley. [ABSTRACT FROM AUTHOR]