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The wheat stem sawfly (WSS), Cephus cinctus Norton (Hymenoptera: Cephidae), is an important pest of wheat and other cereals, threatening the quality and quantity of grain production. WSS larvae feed and develop inside the stem where they are protected from the external environment; therefore, pest management strategies primarily rely on host plant resistance. A major locus on the long arm of wheat chromosome 3B underlies most of the variation in stem solidness; however, the impact of stem solidness on WSS feeding has not been completely characterized. Here, we used a multiomics approach to examine the response to WSS in both solid- and semi-solid-stemmed wheat varieties. The combined transcriptomic, proteomic, and metabolomic data revealed that two important molecular pathways, phenylpropanoid and phosphate pentose, are involved in plant defense against WSS. We also detected a general downregulation of several key defense transcripts, including those encoding secondary metabolites such as DIMBOA, tricetin, and lignin, which suggested that the WSS larva might interfere with plant defense. We comparatively analyzed the stem solidness genomic region known to be associated with WSS tolerance in wild emmer, durum, and bread wheats, and described syntenic regions in the close relatives barley, Brachypodium, and rice. Additionally, microRNAs identified from the same genomic region revealed potential regulatory pathways associated with the WSS response. We propose a model outlining the molecular responses of the WSS-wheat interactions. These findings provide insight into the link between stem solidness and WSS feeding at the molecular level. [ABSTRACT FROM AUTHOR]

Several species of wheat stem sawflies ( WSS) are pests of wheat, including Cephus cinctus Norton in North America. Larvae feed inside the stems and cut the stem near plant maturity. The primary means of control is resistance due to solid stems, largely controlled by a locus on chromosome 3B ( Qss.msub-3 BL). Cultivars that differed for WSS resistance, but with similar stem solidness, were crossed to determine the genetic basis for the differences. The cultivar 'Scholar' is susceptible, while 'Conan' shows resistance. Scholar and Conan possessed different alleles at Qss.msub-3 BL. Both alleles conferred solidness, yet the Conan allele conferred higher WSS resistance. An allele from Conan on chromosome 4A also decreased infestation and stem cutting. The 3B and 4A alleles from Conan acted in an additive fashion to provide increased WSS resistance without increasing stem solidness. Stem solidness has long been used by breeders as a proxy for WSS resistance because of its simplicity. Our results suggest that other resistance mechanisms may complement solid stems. [ABSTRACT FROM AUTHOR]