Transcriptome Profiling Revealed Potentially Critical Roles for Digestion and Defense-Related Genes in Insects’ Use of Resistant Host Plants: A Case Study with Sitobion Avenae

Abstract

Using host plant resistance (HPR) in management of insect pests is often environmentally friendly and suitable for sustainable development of agricultural industries. However, this strategy can be limited by rapid evolution of insect populations that overcome HPR, for which the underlying molecular factors and mechanisms are not well understood. To address this issue, we analyzed transcriptomes of two distinct biotypes of the grain aphid, Sitobion avenae (Fabricius), on wheat and barley. This analysis revealed a large number of differentially expressed genes (DEGs) between biotypes 1 and 3 on wheat and barley. The majority of them were common DEGs occurring on both wheat and barley. GO and KEGG enrichment analyses for these common DEGs demonstrated significant expression divergence between both biotypes in genes associated with digestion and defense. Top defense-related common DEGs with the most significant expression changes included three peroxidases, two UGTs (UDP-glycosyltransferase), two cuticle proteins, one glutathione S-transferases (GST), one superoxide dismutase, and one esterase, suggesting their potentially critical roles in the divergence of S. avenae biotypes. A relatively high number of specific DEGs on wheat were identified for peroxidases (9) and P450s (8), indicating that phenolic compounds and hydroxamic acids may play key roles in resistance of wheat against S. avenae. Enrichment of specific DEGs on barley for P450s and ABC transporters suggested their key roles in this aphid’s detoxification against secondary metabolites (e.g., alkaloids) in barley. Our results can provide insights into the molecular factors and functions that explain biotype adaptation in insects and their use of resistant plants. This study also has significant implications for developing new resistant cultivars, developing strategies that limit rapid development of insect biotypes, and extending resistant crop cultivars’ durability and sustainability in integrated management programs.