Altered glucosinolate hydrolysis in genetically engineered Arabidopsis thaliana and its influence on the larval development of Spodoptera littoralis

The antiherbivore potential of the glucosinolate-myrosinase defense system found in plants of the order Capparales is heavily influenced by the types of hydrolysis products (e.g. isothiocyanates, nitriles) formed from the parent glucosinolates upon plant damage. However, comparison of the effects of glucosinolate hydrolysis products on insect herbivores has been hampered by the lack of suitable experimental tools for rigorous bioassays, such as intact plants differing only in the types of hydrolysis products they produce, or artificial diets that can accurately simulate glucosinolate hydrolysis. The wide array of molecular resources for Arabidopsis thaliana has facilitated the identification of several genes that play a role in glucosinolate hydrolysis. One of these encodes the epithio-specifier protein (ESP) that promotes the formation of nitriles at the expense of isothiocyanates in certain ecotypes of A. thaliana. We overexpressed the ESP cDNA from the nitrile-producing ecotype Landsberg erecta in the isothiocyanate-producing ecotype Columbia-0 to generate transgenic lines of A. thaliana that differed from wild-type plants in the type of glucosinolate hydrolysis products formed upon tissue damage, whereas parent glucosinolate profile and myrosinase activity levels, as well as plant morphology and growth habit, remained unchanged. Bioassays with the model generalist herbivore Spodoptera littoralis (Lepidoptera: Noctuidae) demonstrated that larvae reared on the nitrile-producing lines on average gained weight faster in the first larval stages than larvae that fed on isothiocyanate-producing control plants. Furthermore, larvae with medial growth rates showed a tendency to pupate earlier on the ESP-overexpressing plant lines. Together with the results of previous studies, these findings suggest that isothiocyanates are more effective defenses against insect herbivores than nitriles, and raise questions about what conditions select for nitrile formation in plants.