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 http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13147/suppinfo is available for this article.

Site-dependent induction of jasmonic acid-associated chemical defenses against western flower thrips in Chrysanthemum

“…This variation can be explained by the genetic background, the development plasticity, transmission of long-distance signals, and the vascular architecture of the plant (Van Dam et al 2001;Arnold and Schultz 2002;Arimura et al 2004;Orians 2005;Howe and Jander 2008). For example, glucosinolates, which are important chemical defenses against biotic stresses, are reported to be locally and systemically induced by herbivore feeding in tap and lateral roots of several Brassica species, but not in fine roots (Tsunoda et al 2018). This has been explained by the capacity of plants to increase the protection of tissues that contribute most to plant fitness, such as primary roots.…”

Both Biosynthesis and Transport Are Involved in Glucosinolate Accumulation During Root-Herbivory in Brassica rapa

“…In shoot tissues of Nicotiana sylvestris, accumulation of nicotine is more inducible in younger leaves (Ohnmeiss and Baldwin, 2000). In belowground tissues of Brassica, the taproot responds more strongly to root-herbivory compared to lateral and fine roots, leading to accumulation of high GSL levels in the taproot (Tsunoda et al, 2018). In line with the ODT, herbivore damage on the taproot had a larger impact on plant biomass than herbivore feeding on fine roots (Tsunoda et al, 2018).…”

“…Moreover, GSLs are differentially distributed over different organs. Recent studies showed that the distribution of GSLs over different parts follows optimal defense theory (ODT) (Tsunoda et al, 2018). The ODT predicts that plants allocate defenses preferentially to the plant parts that are highly attractive to potential attackers and are most valuable to the plant at the same time (McKey, 1974;Meldau et al, 2012).…”

“…After hatching, the larvae mine into the taproot, where they cause extensive damage. Because of this feeding behavior, GSL induction is mainly seen in the taproot (Tsunoda et al, 2018). This makes D. radicum an attractive organism to study local and systemic defense induction in belowground tissues.…”

“…This makes D. radicum an attractive organism to study local and systemic defense induction in belowground tissues. In the first experiment, we investigated the effects of root-herbivory on the accumulation of GSLs in both above-and belowground organs after 3 and 7 days, when GSL accumulation is known to occur (Tsunoda et al, 2018). In the second experiment, we focused on the dynamics of the molecular mechanisms underlying this accumulation at earlier time points after the onset of herbivory, and therefore sampled at 12 and 24 h after infestation.…”