Abstract
Plants have evolved a variety of mechanisms for dealing with insect herbivory among which chemical defense through secondary metabolites plays a prominent role. Physiological, behavioural and sensorical adaptations to these chemicals provide herbivores with selective advantages allowing them to diversify within the newly occupied ecological niche. In turn, this may influence the evolution of plant metabolism giving rise to e.g. new chemical defenses. The association of Pierid butterflies and plants of the Brassicales has been cited as an illustrative example of this adaptive process known as ‘coevolutionary armsrace’. All plants of the Brassicales are defended by the glucosinolate-myrosinase system to which larvae of cabbage white butterflies and related species are biochemically adapted through a gut nitrile-specifier protein. Here, we provide evidence by metabolite profiling and enzyme assays that metabolism of benzylglucosinolate in Pieris rapae results in release of equimolar amounts of cyanide, a potent inhibitor of cellular respiration. We further demonstrate that P. rapae larvae develop on transgenic Arabidopsis plants with ectopic production of the cyanogenic glucoside dhurrin without ill effects. Metabolite analyses and fumigation experiments indicate that cyanide is detoxified by β-cyanoalanine synthase and rhodanese in the larvae. Based on these results as well as on the facts that benzylglucosinolate was one of the predominant glucosinolates in ancient Brassicales and that ancient Brassicales lack nitrilases involved in alternative pathways, we propose that the ability of Pierid species to safely handle cyanide contributed to the primary host shift from Fabales to Brassicales that occured about 75 million years ago and was followed by Pierid species diversification.
Highlights
Insects that feed on plants are confronted with some major challenges
This means that mutations in genes involved in the biosynthesis of cyanogenic glucosides, a group of amino-acid derived b-glucosides of a-hydroxynitriles that are widely distributed in the plant kingdom, led to changed enzyme activities yielding new biosynthetic intermediates that were metabolized into glucosinolates, a trait that is restricted to the Brassicales and the genus Drypetes (Putranjivaceae) [14]
Using metabolite profiling (Fig. S1, Figs. 2, 3) and microsomal enzyme assays (Figs. 4, 5), we provide evidence that benzylglucosinolate metabolism in P. rapae is linked to cyanide production
Summary
Insects that feed on plants are confronted with some major challenges. are many plant organs low in protein and equipped with physical barriers such as trichomes and waxes, but they are protected against herbivory by an array of defensive chemicals derived from secondary metabolism [1,2]. While the diversity of plant secondary metabolites is thought to be shaped, among others, by selection pressures exerted by herbivores [3], evolution of plant chemistry may, in turn, affect the evolution of herbivores in an ‘evolutionary armsrace’ [4,5,6] This means that herbivores develop behavioral and/or biochemical adaptations in response to the chemistry of potential food plants and even become specialized on plants that produce a certain group of secondary metabolites. Glucosinolate biosynthesis has long been thought to have evolved from a ‘cyanogenic predisposition’ about 85–90 million years ago [11,12,13] This means that mutations in genes involved in the biosynthesis of cyanogenic glucosides, a group of amino-acid derived b-glucosides of a-hydroxynitriles that are widely distributed in the plant kingdom, led to changed enzyme activities yielding new biosynthetic intermediates that were metabolized into glucosinolates, a trait that is restricted to the Brassicales and the genus Drypetes (Putranjivaceae) [14]. Recent data suggest independent evolution of glucosinolates and cyanogenic glucosides as metabolites of reactive oximes formed by ancestral cytochrome P450 enzymes [15]
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