A specialist flea beetle manipulates and tolerates the activated chemical defense in its host plant

Abstract

Glucosinolates, the characteristic secondary metabolites of Brassicales, are hydrolyzed upon herbivory by myrosinases to toxic and deterrent defense metabolites. The specialist flea beetle, Phyllotreta armoraciae, sequesters glucosinolates in the body despite myrosinase activity, but it is unknown whether plant myrosinase activity influences sequestration and how beetles prevent the hydrolysis of ingested glucosinolates. In feeding experiments performed with the myrosinase-deficient Arabidopsis thaliana tgg1×tgg2 (tgg) mutant and the corresponding wild type, we found that plant myrosinases reduced the glucosinolate sequestration rate by up to 50% and hydrolyzed a fraction of ingested glucosinolates in adult beetles. Although these results show that P. armoraciae cannot fully prevent glucosinolate hydrolysis, we observed no negative influence on beetle performance. To understand how P. armoraciae can avoid the hydrolysis of some ingested glucosinolates, we analyzed their fate directly after ingestion. P. armoraciae rapidly absorbed glucosinolates across the gut epithelium, a strategy that has been proposed to prevent hydrolysis in the gut lumen of sequestering insects. Moreover, beetle gut content suppressed in vitro myrosinase activity, and almost no myrosinase activity was detectable in the feces, which indicates that ingested myrosinases are inactivated in the beetle gut. In summary, we show that P. armoraciae uses several strategies to prevent the hydrolysis of ingested glucosinolates but can also tolerate the formation of glucosinolate hydrolysis products.