AUTHOR=Sporer Theresa , Körnig Johannes , Wielsch Natalie , Gebauer-Jung Steffi , Reichelt Michael , Hupfer Yvonne , Beran Franziska 

TITLE=Hijacking the Mustard-Oil Bomb: How a Glucosinolate-Sequestering Flea Beetle Copes With Plant Myrosinases

JOURNAL=Frontiers in Plant Science

VOLUME=12

YEAR=2021

URL=https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2021.645030

DOI=10.3389/fpls.2021.645030

ISSN=1664-462X

ABSTRACT=<p>Myrosinase enzymes play a key role in the chemical defense of plants of the order Brassicales. Upon herbivory, myrosinases hydrolyze the β-S-linked glucose moiety of glucosinolates, the characteristic secondary metabolites of brassicaceous plants, which leads to the formation of different toxic hydrolysis products. The specialist flea beetle, <italic>Phyllotreta armoraciae</italic>, is capable of accumulating high levels of glucosinolates in the body and can thus at least partially avoid plant myrosinase activity. In feeding experiments with the myrosinase-deficient <italic>Arabidopsis thaliana tgg1</italic> × <italic>tgg2</italic> (<italic>tgg</italic>) mutant and the corresponding <italic>Arabidopsis</italic> Col-0 wild type, we investigated the influence of plant myrosinase activity on the metabolic fate of ingested glucosinolates in adult <italic>P. armoraciae</italic> beetles. <italic>Arabidopsis</italic> myrosinases hydrolyzed a fraction of ingested glucosinolates and thereby reduced the glucosinolate sequestration rate by up to 50% in adult beetles. These results show that <italic>P. armoraciae</italic> cannot fully prevent glucosinolate hydrolysis; however, the exposure of adult beetles to glucosinolate hydrolysis products had no impact on the beetle’s energy budget under our experimental conditions. To understand how <italic>P. armoraciae</italic> can partially prevent glucosinolate hydrolysis, we analyzed the short-term fate of ingested glucosinolates and found them to be rapidly absorbed from the gut. In addition, we determined the fate of ingested <italic>Arabidopsis</italic> myrosinase enzymes in <italic>P. armoraciae</italic>. Although we detected <italic>Arabidopsis</italic> myrosinase protein in the feces, we found only traces of myrosinase activity, suggesting that <italic>P. armoraciae</italic> can inactivate plant myrosinases in the gut. Based on our findings, we propose that the ability to tolerate plant myrosinase activity and a fast glucosinolate uptake mechanism represent key adaptations of <italic>P. armoraciae</italic> to their brassicaceous host plants.</p>