Volatile signaling in weed plant Ageratina adenophora: Understanding the key emissions influencing Procecidochares utilis attraction to gall formation

Abstract

The stem gall fly (Procecidochares utilis) significantly impacts host–plant biology by inhabiting specific parts of stem tissue, ensuring its own survival. Despite this, comprehensive identification of the primary bioactive compounds within host plants that are involved in gall formation remains elusive. This study aims to elucidate the crucial volatile compounds utilized by gall flies to alter host–plant defenses, either through direct or indirect manipulation via the release of an enticing volatile compound attractive to the fly. Employing Y-tube olfactometer assays, we examined the response of Procecidochares utilis to host plants from three Asteraceae weed species—Ageratina adenophora, Ageratum conyzoides, and Praxelis clematidea. Volatile compounds were extracted using headspace solid-phase microextraction (HS-SPME) and SPME-FIBER. Subsequently, gas chromatography-electroantennography and electroantennography were employed to analyze the antennal responses to individual odorants. The analysis revealed that the primary bioactive compound varied among the three weed species. Out of a total of 805 known volatiles, 65 main active compounds were exclusive to Ageratina adenophora (host plant). Remarkably, only 8 bioactive compounds were identified to elicit an antennal response from Procecidochares utilis. Notably, caryophyllene, β-bisabolene, and 4-thujen-2-α-yl acetate exhibited the remarkable ability to elicit an attraction response from both sexes of Procecidochares utilis. Among these, β-bisabolene emerged as the key compound, eliciting the most significant response from the gall fly antenna. Our findings offer novel insights into the specific attraction of the stem gall fly to Ageratina adenophora, utilizing key odorants as unique cues for initiating gall formation on its host plant. This discovery highlights how these cues enable the gall fly to exert direct or indirect control over its host. Additionally, these findings underscore the potential of this approach in the development of sustainable pest management strategies in the context of field trials.