The Role of Ascorbate–Glutathione System and Volatiles Emitted by Insect-Damaged Lettuce Roots as Navigation Signals for Insect and Slug Parasitic Nematodes

SIMPLE SUMMARY: In a glasshouse experiment, the effects of wireworm-damaged lettuce roots on the antioxidative defense system and movement of insect/slug parasitic nematodes were studied. Lettuce seedlings were grown with or without wireworms, and antioxidants and photosynthetic pigments were analyzed. Volatile organic compounds emitted from lettuce roots were investigated, and certain compounds were selected for a chemotaxis assay with nematodes. Results showed that wireworm-damaged roots negatively affected photosynthetic pigment contents and induced reactive oxygen species even before visible symptoms appeared. The ascorbate–glutathione system was identified as a redox hub in defense response against wireworms. Entomopathogenic nematodes were found to be more mobile than slug parasitic nematodes towards chemotaxis compounds, and 2,4-nonadienal repelled all tested nematodes. The study highlights the importance of understanding belowground tritrophic interactions for pest management in agricultural systems. ABSTRACT: The effect of wireworm-damaged lettuce roots on the antioxidative defense system (ascorbate–glutathione cycle, photosynthetic pigments) and movement of insect/slug parasitic nematodes towards determined root exudates was studied in a glasshouse experiment. Lettuce seedlings were grown in a substrate soil in the absence/presence of wireworms (Elateridae). The ascorbate–glutathione system and photosynthetic pigments were analyzed by HPLC, while volatile organic compounds (VOC) emitted by lettuce roots were investigated by GC-MS. Herbivore-induced root compounds, namely 2,4-nonadienal, glutathione, and ascorbic acid, were selected for a chemotaxis assay with nematodes Steinernema feltiae, S. carpocapsae, Heterorhabditis bacteriophora, Phasmarhabditis papillosa, and Oscheius myriophilus. Root pests had a negative effect on the content of photosynthetic pigments in the leaves of infested plants, indicating that they reacted to the presence of reactive oxygen species (ROS). Using lettuce as a model plant, we recognized the ascorbate–glutathione system as a redox hub in defense response against wireworms and analyzed its role in root-exudate-mediated chemotaxis of nematodes. Infected plants also demonstrated increased levels of volatile 2,4-nonadienal. Entomopathogenic nematodes (EPNs, S. feltiae, S. carpocapsae, and H. bacteriophora) proved to be more mobile than parasitic nematodes O. myriophilus and P. papillosa towards chemotaxis compounds. Among them, 2,4-nonadienal repelled all tested nematodes. Most exudates that are involved in belowground tritrophic interactions remain unknown, but an increasing effort is being made in this field of research. Understanding more of these complex interactions would not only allow a better understanding of the rhizosphere but could also offer ecologically sound alternatives in the pest management of agricultural systems.