Functional divergence of three glutathione transferases in two biotypes of the English grain aphid, Sitobion avenae

The English grain aphid, Sitobion avenae (Fabricius) (Hemiptera: Aphididae), is a significant pest of cereal crops, but molecular factors and mechanisms that underpin its ability to develop differential biotypes on variable host plants are still not well understood. In this study, we investigated the interactions between two plant secondary metabolites (i.e., gramine and gallic acid) and three glutathione S-transferases (GSTs) of S. avenae. Using artificial diets complemented or not with one of these two plant compounds, we found that gramine had relatively stronger negative effects on fitness of S. avenae biotype 3 (adapted to barley), and gallic acid on that of biotype 4 (adapted to wheat). Gramine significantly induced overexpression of SaveGST1 and SaveGST2 in biotype 4, but not in biotype 3. Gramine also reduced SaveGST3 expression in biotype 4, but not in biotype 3, suggesting biotype-specific effect of GSTs' regulation. In the treatments with gallic acid, the overexpression of SaveGST1, but not SaveGST2 or SaveGST3, was significantly induced in both biotypes, suggesting a critical role of SaveGST1 in detoxification of phenolic compounds such as gallic acid. The total constitutive GST activity was much higher in biotype 4 than in biotype 3. Significant increase in GST activity was obtained by the addition of both secondary metabolites in biotype 4, but not in biotype 3, showing significantly higher expression plasticity of GSTs in biotype 4. Thus, both constitutive and induced expression of GSTs could affect the adaptability of S. avenae on plants with variable secondary compounds, and thus contribute to the divergence of biotypes in this aphid species.