The smell of danger: The odor of a gall-inducing herbivore primes expression of defense genes in its host plant

Herbivore-associated chemical cues can prime plant defenses against herbivory. After perceiving certain volatile cues, plants can respond more efficiently and strongly when insects attack. Priming likely entails transcriptome-wide rearrangement–the ‘stockpiling of defenses’ in preparation for a future attack–although little has been uncovered about how gene expression changes in the ‘primed state’. We studied phytohormone dynamics and transcriptomic responses of tall goldenrod (Solidago altissima L.) following exposure to the putative sex pheromone of males of the goldenrod gall fly (Eurosta solidaginis Fitch), which has been shown to prime plant defenses.

Our study focused on two questions: 1) what molecular pathways are activated after S. altissima perceives the emission of male E. solidaginis? 2) How does priming influence chemical defenses following subsequent insect damage? To answer these questions, we exposed S. altissima plants to the emission of male E. solidaginis then subjected them to herbivory from a generalist caterpillar and collected tissue at five time points. We extracted phytohormones and RNA from damaged plant tissue for analyses by gas chromatography-coupled mass spectrometry and Illumina RNAseq, respectively. Hormone dynamics of S. altissima appeared to be accelerated by exposure to the volatile emission of E. solidaginis. Our transcriptome analysis showed that priming significantly up-regulated defense-related gene expression. Primed plants showed significant enrichment in many defensive gene ontology terms, including jasmonic acid metabolism, response to other organisms, and biotic stress signaling. We leveraged a model ecology system to show that the S. altissima primed state is one of intensified defense responses to herbivory.