Secrets of the Forest: Volatiles First Discovered in Pine Trees Propagate Defense Signals within and between Plants[OPEN]

Systemicacquired resistance (SAR)—aplantwide heightened state of defense following localized exposure to a pathogen—is characterized by increased salicylic acid (SA) and reactive oxygen species (ROS) levels and elevated expression of pathogenesisrelated genes. SARdependsonENHANCED DISEASE SUSCEPTIBILITY1 (EDS1), which both generates the SAR signal at the primary infection site and perceives it in distal, uninfected tissues (Breitenbach et al., 2014). Various vascular mobile signals function within SAR, including methyl salicylate (Park et al., 2007), the nonproteogenic amino acid pipecolic acid (Návarová et al., 2012), and the dicarboxylic acid azelaic acid (Jung et al., 2009). In a new study, Riedlmeier et al. (2017) examinedtheroleofvolatileorganiccompounds (VOCs) in SAR. Using gas chromatography/ mass spectrometry, they compared the emissions released by wild-type Arabidopsis thalianaplants andSAR-deficienteds1-2 mutants several hours after induction of SAR.Whereas thewild-typeplants released substantial amounts of the bicyclic monoterpenes a-pinene and b-pinene—volatiles best known for giving pine forests their enchanting scent—the mutants with compromised SAR released almost undetectable levels of these VOCs. Based on these findings, the authors hypothesizedthata-pineneandb-pinene induce SAR. To test this possibility, they exposed wild-type plants to a mixture of a-pinene and b-pinene or to the VOC solvent control for 3 d and then challenged the plants with the pathogenic bacterium Pseudomonas syringae pv tomato strain DC3000 (Pst). They found that bacterial growth was ;10-fold less in the leaves of plants that had been exposed to the monoterpenes and that the effect depended on pinene concentration. Bacterial growth was not limited in the nonexpressor of PR genes1-1 mutant, which has defects in signaling downstream of SA, or in the sa induction deficient2-1 (sid2-1) mutant, which has defects in SA biosynthesis, after 3 d ofmonoterpene exposure. Furthermore, ROS O2 2 accumulated in the leaves of plants treated with pinenes, but not in those of control plants. Microarray analysis showed that pinene treatment directly influenced key regulatory genes in SAbiosynthesis andSAR (e.g., the geneencoding the lipid transfer protein AZELAIC ACID INDUCED1). Therefore, pinenes appear to induce SAR, in a manner that depends on SA signaling. As monoterpenes are highly volatile, the authors directly tested whether these VOCs could function as mobile plant-to-plant defense signals. Wild-type receiver plants enclosed in a vacuum dessicator for 3 d with SAR-induced (i.e., monoterpene-emitting) sender plants were indeed more resistant to Pst infection than were receiver plants enclosed with control plants. Thus, in addition to functioning in SAR signalingwithin theplant,a-pineneandb-pinene act as airborne signals that prime neighboring plants for impending danger (see figure). This exciting finding suggests that the aroma of a pine forest has an important function.