Locally and systemically induced glucosinolates follow optimal defence allocation theory upon root herbivory

Abstract

Herbivore-induced defences in plants are considered a strategy to manage multiple interactions while saving resources. The optimal defence theory (ODT) is one of the most prominent theoretical frameworks to explain the defence allocation patterns within plants. It was recently shown that the ODT generally applies to constitutive glucosinolate (GSL) allocation in shoot and root organs. Previous studies showed that both root and shoot herbivore feeding may alter defence allocation over plant organs. For shoots, the effect depends on where the herbivores feed. It is as yet unknown whether similar principles apply to root-herbivore-induced GSLs. To analyse the effects of root localized herbivore feeding on GSL allocation, we conducted a pot experiment using Anomala cuprea grubs and four Brassicaceae; Brassica rapa, B. nigra, B. oleracea and Sinapis alba. Individuals of these four plant species were grown in dedicated mesocosms. The grubs were confined either to the bottom soil, the middle section or the topsoil. Plants grown in the same set-ups but without root herbivores served as controls. Glucosinolate levels of the leaf lamina, petiole and stem as well as of the taproot, lateral roots and fine roots were measured after 8 days of herbivory. Plant biomass reduction due to herbivory was the largest when herbivores were confined to the topsoil. In the three Brassica species, taproot GSL levels increased upon herbivory independent of where the root herbivores were feeding. Glucosinolate levels in fine roots and shoots, on the other hand, hardly responded to root herbivory. Indole GSLs, which are more effective to pathogens than to herbivores, were more strongly induced than aliphatic and aromatic GSLs, especially in the taproots. Sinapis alba did not show remarkable increments in any GSL level upon herbivory. These results show that locally and systemically induced defences in roots are consistent with the ODT: The taproot which is the most vulnerable and valuable to plant performance shows the highest increase in defence induction. The induced GSL profiles suggest that the response may not only target herbivores, but may also help to prevent secondary infection by microbial pathogens. A plain language summary is available for this article.