Herbivore feeding preference corroborates optimal defense theory for specialized metabolites within plants

Abstract

Numerous plants protect themselves from attackers by using specialized metabolites. The biosynthesis of these deterrent, often toxic metabolites is costly, as their synthesis diverts energy and resources on account of growth and development. How plants diversify investments into growth and defense is explained by the optimal defense theory. The central prediction of the optimal defense theory is that plants maximize growth and defense by concentrating specialized metabolites in tissues that are decisive for fitness. To date, supporting physiological evidence relies on the correlation between plant metabolite presence and animal feeding preference. Here, we use glucosinolates as a model to examine the effect of changes in chemical defense distribution on feeding preference. Taking advantage of the uniform glucosinolate distribution in transporter mutants, we show that high glucosinolate accumulation in tissues important to fitness protects them by guiding larvae of a generalist herbivore to feed on other tissues. Moreover, we show that the mature leaves of Arabidopsis thaliana supply young leaves with glucosinolates to optimize defense against herbivores. Our study provides physiological evidence for the central hypothesis of the optimal defense theory and sheds light on the importance of integrating glucosinolate biosynthesis and transport for optimizing plant defense.

Plants protect themselves from herbivores by optimizing the distribution of chemical defenses

“…These patterns have been rationalized by various theories, chief among them the optimal defense theory, but this theory has proved very difficult to test until a recent report from Hunziker et al. ( 1 ).…”

“…Hunziker et al. ( 1 ) exploit membrane transporters to test the influence of glucosinolate distribution on caterpillar herbivory in the model plant Arabidopsis thaliana . Glucosinolates are the characteristic mustard oil glucoside defenses of A. thaliana and other Brassicaceae species, such as cabbages, broccoli, and rapeseed ( 12 ).…”

“…To test whether this pattern confers fitness benefits, Hunziker et al. ( 1 ) employ a double glucosinolate transporter mutant in which the concentration of glucosinolates is the same in all leaf age classes ( B ). On wild-type plants, caterpillars fed only on older leaves, with little effect on plant survival to reproduction.…”

“…Such dramatic differences in glucosinolate distribution provide an ideal chance to test the predictions of the optimal defense hypothesis. When newly hatched Egyptian cotton leafworm ( Spodoptera littoralis ) caterpillars, a supergeneralist feeder, were allowed to feed on wild-type A. thaliana , they fed exclusively on old leaves because of their significantly reduced glucosinolate concentrations, as low as one-tenth of the concentrations found in young leaves ( 1 ). However, on the double glucosinolate transporter mutant gtr1grtr2 , caterpillars switched completely to feeding on young leaves.…”

“…An important control was the use of a quadruple mutant in glucosinolate biosynthetic genes that produces no residual glucosinolates ( 1 , 14 ). With this A. thaliana line, caterpillars also fed predominantly on young leaves, suggesting that the distribution of glucosinolates was the key factor mediating leaf preference in the transporter mutants, not differential distributions of other metabolites.…”