Identification and characterization of TMV-induced volatile signals in Nicotiana benthamiana: evidence for JA/ET defense pathway priming in congeneric neighbors via airborne (E)-2-octenal

Plants release a mixture of volatile compounds when subjects to environmental stress, allowing them to transmit information to neighboring plants. Here, we find that Nicotiana benthamiana plants infected with tobacco mosaic virus (TMV) induces defense responses in neighboring congeners. Analytical screening of volatiles from N. benthamiana at 7 days post inoculation (dpi) using an optimized SPME–GC–MS method showed that TMV triggers the release of several volatiles, such as (E)-2-octenal, 6-methyl-5-hepten-2-one, and geranylacetone. Exposure to (E)-2-octenal enhances the resistance of N. benthamiana plants to TMV and triggers the immune system with upregulation of pathogenesis-related genes, such as NbPR1a, NbPR1b, NbPR2, and NbNPR1, which are related to TMV resistance. Furthermore, (E)-2-octenal upregulates jasmonic acid (JA) that levels up to 400-fold in recipient N. benthamiana plants and significantly affects the expression pattern of key genes in the JA/ET signaling pathway, such as NbMYC2, NbERF1, and NbPDF1.2, while the salicylic acid (SA) level is not significantly affected. Our results show for the first time that the volatile (E)-2-octenal primes the JA/ET pathway and then activates immune responses, ultimately leading to enhanced TMV resistance in adjacent N. benthamiana plants. These findings provide new insights into the role of airborne compounds in virus-induced interplant interactions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10142-023-01203-z.