Root and shoot glucosinolate allocation patterns follow optimal defence allocation theory

Abstract

Summary Optimal defence allocation theory (ODT) is one of the most prominent theoretical frameworks to explain the allocation of defence compounds within plants. It predicts that the most valuable and vulnerable plant organs have the highest levels of chemical defence. The ODT has been well worked out and experimentally tested for shoot defences, but not for root defences. To assess if ODT principles apply similarly to roots and shoots, we examined glucosinolates in above‐ground and below‐ground organs of nine plant species belonging to two families. In order to evaluate whether ODT equally applies to shoot and root organs, we designed a conceptual model in which above‐ground and below‐ground organs were assigned to orders of importance to plant performance. We hypothesized that organs constituting the plant's core structure are better protected than more distal organs. The nine plant species were cultivated, and their roots and shoots were harvested and divided into three orders for glucosinolate analysis. Using a specialist (Delia radicum) and a generalist (Amphimallon solstitiale) root herbivore, we also experimentally tested the hypothesis that the generalist herbivore prefers to feed on fine roots (FRs) with a low glucosinolate concentration, while the specialist prefers taproots (TRs) with a high glucosinolate concentration. We found that both in roots and shoots, the higher ordered core structural organs (TRs and stems) had the highest levels of glucosinolates. Below‐ground, TRs and lateral roots were better protected than the more distal, and less costly, FRs in seven out of nine species tested. The specialist root herbivore preferred feeding on the highly defended TRs, which is in line with what has been found for above‐ground specialist herbivores. Moreover, the glucosinolate concentration in roots overall was significantly higher than that in shoots. Synthesis. These results support the hypothesis that Optimal defence allocation theory (ODT) generally applies to glucosinolate allocation in above‐ground and below‐ground organs and may mainly serve to maintain the integrity of the main plant structure. Moreover, it suggests that above‐ground and below‐ground insect herbivores independently exert similar selection pressures on defence allocation patterns in roots and shoots.