Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways

Glucosinolate accumulation and expression of glucosinolate biosynthetic genes were studied in response to four herbivores in Arabidopsis thaliana (L.) wild-type (Columbia) and mutant lines affected in defense signaling. Herbivory on wild-type plants led to increased aliphatic glucosinolate content for three of four herbivores tested, the aphid generalist Myzus persicae (Sulzer), the aphid specialist Brevicoryne brassicae (L.), and the lepidopteran generalist Spodoptera exigua Hübner. The lepidopteran specialist Pieris rapae L. did not alter aliphatic glucosinolate content in the wild-type, but indole glucosinolates increased slightly. Gene expression associated with aliphatic glucosinolate biosynthesis increased after feeding by all species, indicating that glucosinolate accumulation is not always regulated at the level of these gene transcripts. A. thaliana lines with mutations in jasmonate (coi1), salicylate (npr1), and ethylene signaling (etr1) diverged in gene expression, glucosinolate content, and insect performance compared to wild-type suggesting the involvement of all three modes of signaling in responses to herbivores. The coi1 mutant had much lower constitutive levels of aliphatic glucosinolates than wild-type but content increased in response to herbivory. In contrast, npr1 had higher constitutive levels of aliphatic glucosinolates and levels did not increase after feeding. Glucosinolate content of the etr1 mutant was comparable to wild-type and did not change with herbivory, except for P. rapae feeding which elicited elevated indolyl glucosinolate levels. Unlike the wild-type response, gene transcripts of aliphatic glucosinolate biosynthesis did not generally increase in the mutants. Both glucosinolate content and gene expression data indicate that salicylate and ethylene signaling repress some jasmonate-mediated responses to herbivory.