Using ‘mute’ plants to translate volatile signals

When attacked by herbivores, plants release volatile organic compounds (VOCs) that attract natural enemies of the herbivores and function as indirect defenses. Whether or not neighboring plants 'eavesdrop' on these VOCs remains controversial because most studies use unrealistic experimental conditions and VOC exposures. In order to manipulate exposures of wild-type (WT) Nicotiana attenuata'receiver' plants, we elicited transformed 'emitter' plants, whose production of herbivore-induced C6 green leaf volatiles (GLVs) or terpenoid volatiles was genetically silenced, and placed them up-wind of WT 'receiver' plants in open-flow experimental chambers. We compared the transcriptional and secondary metabolite defense responses of WT receiver plants exposed to VOCs from these transgenic emitter plants with those of plants exposed to VOCs from WT emitter plants. No differences in the constitutive accumulation of defense metabolites and the signal molecule jasmonic acid (JA) were found. Additional elicitation of receiver plants revealed that exposure to WT, GLV-deficient and terpenoid-deficient volatile blends did not prime induced defenses, JA accumulation, or the expression of lipoxygenase 3 (NaLOX3), a gene involved in JA biosynthesis. However, exposure to wound- and herbivore-induced VOCs significantly altered the transcriptional patterns in receiver plants. We identified GLV-dependent genes by complementing the GLV-deficient volatile blend with a mixture of synthetic GLVs. Blends deficient in GLVs or cis-alpha-bergamotene regulated numerous genes in receiver plants that did not respond to the complete VOC blends of WT emitters, indicating a suppressive effect of GLVs and terpenoids. Whether these transcriptional responses translate into changes in plant fitness in nature remains to be determined.