Untargeted metabolomics profiling of oat (Avena sativa L.) and wheat (Triticum aestivum L.) infested with wheat stem sawfly (Cephus cinctus Norton) reveals differences associated with plant defense and insect nutrition

Introduction: Wheat stem sawfly (WSS), Cephus cinctus Norton, is a major pest of common bread wheat (Triticum aestivum L.) and other cultivated cereals in North America. Planting of cultivars with solid stems has been the primary management strategy to prevent yield loss due to WSS infestation, however expression of this phenotype can vary depending on environmental conditions and solid stems hinder biological control of WSS via braconid parasitoids Bracon cephi (Gahan) and Bracon lissogaster Muesebeck. In the hollow stems of oat (Avena sativa L.), WSS larvae experience 100% mortality before they reach late instars, but the mechanisms for this observed resistance have not been characterized. Objective: The objective of this study was to explore additional sources of resistance outside of the historic solid stem phenotype. Methods: Here, we use an untargeted metabolomics approach to examine the response of the metabolome of two cultivars of oat and four cultivars of spring wheat to infestation by WSS. Using liquid chromatography-mass spectrometry (LC-MS), differentially expressed metabolites were identified between oat and wheat which were associated with the phenylpropanoid pathway, phospholipid biosynthesis and signaling, the salicylic acid signaling pathway, indole-3-acetic acid (IAA) degradation, and biosynthesis of 1,4-benzoxazin-3-ones (Bxs). Several phospho- and galacto- lipids were found in higher abundance in oat, and with the exception of early stem solidness cultivar Conan, both species experienced a decrease in abundance once infested. In all wheat cultivars except Conan, an increase in abundance was observed for Bxs HMDBOA-glc and DIBOA-beta-D-glucoside after infestation, indicating that this pathway is involved in wheat response to infestation in both solid and hollow stemmed cultivars. Differences between species in compounds involved in IAA biosynthesis, degradation and inactivation suggest that wheat may respond to infestation by inactivating IAA or altering the IAA pool in stem tissue. Conclusion: We propose that the species differences found here likely affect the survival of WSS larvae and may also be associated with differences in stem architecture at the molecular level. Our findings suggest pathways to focus on for future studies in elucidating plant response to WSS infestation.