Jasmonic acid and heat stress induce high volatile organic compound emissions in Picea abies from needles, but not from roots

Abstract Plants emit diverse volatile organic compounds from their leaves and roots for protection against biotic and abiotic stress. An important signaling cascade activated by aboveground herbivory is the jasmonic acid pathway that stimulates the production of volatile organic compounds. So far it remains unclear if the activation of this pathway also leads to enhanced volatile organic compound emissions from conifer roots, and how the interplay of above- and below-ground defenses in plants are affected by multiple stressors. Therefore, we simultaneously analyzed needle and root volatile organic compound emissions of Picea abies saplings, as well as CO2 and H2O fluxes in response to aboveground jasmonic acid treatment, heat stress and their interaction in a controlled climate chamber experiment. Continuous online volatile organic compound measurements by proton-transfer time-of-flight mass-spectrometry showed an inverse pattern of total needle and root volatile organic compound emissions, when plants were treated with jasmonic acid and heat. While needle sesquiterpene emissions increased ninefold 1 day after jasmonic acid application, total root volatile organic compound emissions decreased. This was mainly due to reduced emissions of acetone and monoterpenes by roots. In response to aboveground jasmonic acid treatment, root total carbon emitted as volatile organic compounds decreased from 31% to only 4%. While volatile organic compound emissions aboveground increased, net CO2 assimilation strongly declined due to jasmonic acid treatment, resulting in net respiration during the day. Interestingly, root respiration was not affected by aboveground jasmonic acid application. Under heat the effect of jasmonic acid on volatile organic compound emissions of needles and roots was less pronounced. The buffering effect of heat on volatile organic compound emissions following jasmonic acid treatment points towards an impaired defense reaction of the plants under multiple stress. Our results indicate efficient resource allocation within the plant to protect threatened tissues by a rather local volatile organic compound release. Roots may only be affected indirectly by reduced belowground carbon allocation, but are not involved directly in the jasmonic acid-induced stress response.