Deadly scents: Exposure to plant volatiles increases mortality of entomopathogenic nematodes during infection

Authors: Gaffke, Alexander; Shapiro Ilan, David; Alborn, Hans

Submitted to: Frontiers in Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/26/2022
Publication Date: 9/14/2022
Citation: Gaffke, A.M., Shapiro-Ilan, D., Alborn, H.T. 2022. Deadly scents: Exposure to plant volatiles increases mortality of entomopathogenic nematodes during infection. Frontiers in Physiology. 13:978359. https://doi.org/10.3389/fphys.2022.978359.
DOI: https://doi.org/10.3389/fphys.2022.978359

Interpretive Summary: Entomopathogenic nematodes, small soil dwelling round worms that infect and kill pest insects, are known to provide significant pest control in many agricultural systems. These nematodes locate insect pests to attack based on specific odors released from the plants in response to the insect feeding and due to the resulting insect mortality, are considered beneficial. As some plant volatiles have been reported to affect immune responses of insects to microorganisms, scientists at USDA-ARS, Center for Medical, Agricultural and Veterinary Entomology, Gainesville, Florida, examined the impact of insect exposure to various plant-derived odors on success of nematode attack. Negative impacts on nematode infections were observed as some plant-produced odors enhanced insect immune responses ultimately protecting them from nematode attack. This better understanding the below ground interactions of plant volatiles, insects, and entomopathogenic nematodes can provide the basis for refinement in procedures of using nematodes for root feeding pest insects and optimization in insect pest management strategies.

Technical Abstract: Plants attacked by insects commonly mobilize various defense mechanisms, including the biosynthesis and release of so-called herbivore-induced plant volatiles (HIPVs). Entomopathogenic nematodes (EPNs) can be attracted to these belowground HIPVs, which can enhance biocontrol services from EPNs. However, recent research has also demonstrated that HIPVs can induce and prime insect immune responses, decreasing the insect’s susceptibility to pathogens and parasites. Therefore, experiments were conducted to test the impact of HIPVs on insects and EPNs during the initial stage of EPN infection. Compounds that can impact EPN attraction and infectivity such as pregeijerene, ß-caryophyllene, and a-pinene, and compounds that have been determined to increase or decrease susceptibility of insects to pathogens, such as (Z)-3-hexenyl acetate, linalool, and ß-ocimene, were selected. Exposure of Galleria mellonella larvae to pregeijerene, linalool, ß-ocimene and a-pinene during invasion significantly increased mortality of Steinernema diaprepesi and Heterorhabditis bacteriophora after 48 hrs. Larval treatment with ß-caryophyllene only increased mortality for Heterorhabditis bacteriophora. (Z)-3-hexenyl acetate did not cause differential mortality from the controls for either nematode species. In additional experiments, we found that EPNs exposed to a-pinene and linalool were more readily recognized by the insects’ immune cells compared to the control treatment, thus the observed increased mortality was likely due to HIPVs-EPN interactions with the insect’s immune system. These results show that the presence of HIPVs can impact EPN survival in the model host, G. mellonella.