Glucosinolate Abundance and Composition in Brassicaceae Influence Sequestration in a Specialist Flea Beetle

Abstract

The horseradish flea beetle Phyllotreta armoraciae exclusively feeds on Brassicaceae, which contain glucosinolates as characteristic defense compounds. Although glucosinolates are usually degraded by plant enzymes (myrosinases) to toxic isothiocyanates after ingestion, P. armoraciae beetles sequester glucosinolates. Between and within brassicaceous plants, the glucosinolate content and composition can differ drastically. But how do these factors influence sequestration in P. armoraciae? To address this question, we performed a five-day feeding experiment with three Arabidopsis thaliana lines that differ four-fold in glucosinolate content and the composition of aliphatic and indolic glucosinolates. We quantified the amounts of ingested, sequestered, and excreted glucosinolates, and analyzed the changes in glucosinolate levels and composition in beetles before and after feeding on Arabidopsis. P. armoraciae accumulated almost all ingested glucosinolate types. However, some glucosinolates were accumulated more efficiently than others, and selected glucosinolates were modified by the beetles. The uptake of new glucosinolates correlated with a decrease in the level of stored glucosinolates so that the total glucosinolate content remained stable at around 35 nmol/mg beetle fresh weight. Beetles excreted previously stored as well as ingested glucosinolates from Arabidopsis, which suggests that P. armoraciae regulate their endogenous glucosinolate level by excretion. The metabolic fate of ingested glucosinolates, i.e. the proportions of sequestered and excreted glucosinolates, depended on glucosinolate type, content, and composition in the food plant. Overall, P. armoraciae sequestered and excreted up to 41% and 31% of the total ingested aliphatic and indolic glucosinolates from Arabidopsis, respectively. In summary, we show that glucosinolate variability in Brassicaceae influences the composition but not the level of sequestered glucosinolates in P. armoraciae beetles.

Ontogenetic differences in the chemical defence of flea beetles influence their predation risk

“…Since larvae were still able to sequester GLS from the myrosinase-deficient tgg mutant, the ingested GLS from A. thaliana wild type plants were likely hydrolysed by plant myrosinases. Although P. armoraciae adults were principally able to sequester other GLS types after they were shifted from B. juncea to A. thaliana, adults preferred to excrete the ingested GLS from A. thaliana and not the previously sequestered allyl GLS (Yang et al, 2020). Together, these results indicate that larvae and adults use different mechanisms to selectively sequester allyl GLS (Yang et al, 2020).…”

“…Although P. armoraciae adults were principally able to sequester other GLS types after they were shifted from B. juncea to A. thaliana, adults preferred to excrete the ingested GLS from A. thaliana and not the previously sequestered allyl GLS (Yang et al, 2020). Together, these results indicate that larvae and adults use different mechanisms to selectively sequester allyl GLS (Yang et al, 2020). This sequestration strategy might have played an important role in the evolution of the close association between P. armoraciae and horseradish.…”

“…Previous studies with P. armoraciae revealed the presence of high GLS levels in newly emerged adults, which indicates that sequestered GLS are transferred from the larval to the adult stage (Yang, Kunert, Sporer, Körnig, & Beran, 2020). Compared to P. armoraciae adults, we know much less about the chemical defence of the less mobile immature life stages, which have a different life style than adults (Vig, 1999).…”

“…Larvae were not able to accumulate ingested GLS from A. thaliana wild type plants, but sequestered GLS from the myrosinase-deficient tgg mutant and from B. juncea. This result was unexpected, because P. armoraciae adults accumulated all GLS types from A. thaliana wild type plants(Yang et al, 2020). To find out why larvae can sequester GLS from B. juncea, but not from A. thaliana, we compared the…”

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

“…Here, we investigated the influence of plant myrosinase activity on glucosinolate sequestration in the adult life stage of P. armoraciae . In a previous feeding study, we recovered about 35% of the total ingested glucosinolates from wild type leaves in the beetle body and feces, whereas the metabolic fate of more than 60% of the total ingested glucosinolates remained unknown (Yang et al, 2020). One possible explanation is that the unrecovered glucosinolates were hydrolyzed by plant myrosinases.…”