Tetranychus urticae metabolic responses to Arabidopsis thaliana defensive phenylpropanoids

Tetranychus urticae – the two-spotted spider mite (TSSM) – is an extreme composite plant generalist that employs xenobiotic detoxification alongside short generational life cycles to quickly establish high performance on initially unfavorable plant hosts. I investigated the role that phenylpropanoids, a class of plant metabolites, play in Arabidopsis defense against mite herbivory. Using TSSMs adapted to Arabidopsis (Arabidopsis-adapted) and an ancestral population adapted to bean (bean-adapted) I assessed the toxicity of common (between Arabidopsis and bean) and Arabidopsis specific phenylpropanoids to TSSMs. I show that sinapoyl malate, an Arabidopsis specific phenylpropanoid, is acaricidal and exclusively reduces bean-adapted TSSM fecundity. An untargeted metabolomic analysis of bean- and Arabidopsis-adapted TSSMs treated with sinapoyl malate revealed conserved TSSM responses. I identified sinapoyl malate derivatives, such as sinapoyl glucose, that accumulate in mites following treatment with sinapoyl malate. This allowed me to reconstitute a TSSM detoxification pathway implicating TSSM enzymes, like esterases and UGTs, in sinapoyl malate metabolism.