Plants constantly release fragrances into the air, and these so-called volatile compounds carry important information about the status and physiology of the plant which can be used by both friends and foes in its vicinity. Previous studies had shown that when tobacco hornworm caterpillars feed on tobacco plants the fragrances the plant releases become more attractive to one of caterpillar's natural enemies: Geocoris spp., commonly known as big-eyed bugs. This phenomenon naturally benefits the plant by attracting predators that help control the caterpillar population. Contrary to expectations, however, the study revealed that the modification of the plant's fragrance is not a cry-for-help signal emitted by the plant itself, but rather the result of an enzyme introduced into the plant wounds by the caterpillar itself during feeding.
We were initially perplexed by the observation that the caterpillars essentially betray themselves by making the plant's volatile bouquet more alluring to a natural enemy. This led us to investigate potential beneficial roles that this caterpillar enzyme may have for the insect itself.Yu-Hsien Lin, first author of the new study
In their new publication, the researchers provide a comprehensive explanation for this puzzling phenomenon. They have identified an enzyme - called hexenal isomerase - in the caterpillar's saliva and confirmed its ability to modify the volatile profile of plants. To further validate their findings, the researchers created mutant caterpillars that were unable to produce the enzyme. Remarkably, these mutants exhibited severe developmental impairments: they took longer to develop into adults and had lower pupal weights (the measure of their mass during the transformation from caterpillar to moth). The hexenal isomerase-deficient adults also displayed more physiological deformities, such as wings that didn't fully open. These discoveries indicate that the hexenal isomerase enzyme plays a crucial role in the healthy development of tobacco hornworms.
‘Our study sheds lighton why these caterpillars produce an enzyme that attracts their own predators, and why evolution has not eliminated this seemingly counterproductive trait. We have discovered that the enzyme, besides modifying plant fragrances, likely serves a vital or beneficial function in the caterpillar's development, outweighing any costs associated with its interaction with the plant,’ says team leader Silke Allmann.
Yu-Hsien Lin, Juliette Silven, Nicky Wybouw, Richard A. Fandino, Henk L. Dekker, Heiko Vogel, Yueh-Lung Wu, Chris de Koster, Ewald Grosse-Wilde, Michel A. Haring, Robert C. Schuurink & Silke Allmann: ‘A salivary GMC oxidoreductase of Manduca sexta re-arranges the green leaf volatile profile of its host plant’, in: Nature Communication (28 June 2023). DOI: 10.1038/s41467-023-39353-0.