Intraspecific Variation in Plant Defense Alters Effects of Root Herbivores on Leaf Chemistry and Aboveground Herbivore Damage

Abstract

Root herbivores can indirectly affect aboveground herbivores by altering the food quality of the plant. However, it is largely unknown whether plant genotypes differ in their response to root herbivores, leading to variable defensive phenotypes. In this study, we investigated whether rootfeeding insect larvae (Agriotes sp. larvae, wireworms) induce different responses in Plantago lanceolata plants from lines selected for low and high levels of iridoid glycosides (IG). In the absence of wireworms, plants of the "high-IG line" contained approximately twofold higher levels of total IG and threefold higher levels of catalpol (one of the IG) in leaves than plants from the "low-IG line," whereas both lines had similar levels of IG in roots. In response to wireworms, roots of plants from both lines showed increased concentrations of catalpol. Leaves of "low-IG line" plants increased catalpol concentrations in response to wireworms, whereas catalpol concentrations of leaves of "high-IG line" plants decreased. In contrast, glucose concentrations in roots of "low-IG" plants decreased, while they increased in "high-IG" plants after feeding by wireworms. The leaf volatile profile differed between the lines, but was not affected by root herbivores. In the field, leaf damage by herbivores was higher in wireworm-induced compared to noninduced "low-IG" plants and lower in wireworm-induced compared to noninduced "high-IG" plants, despite induction of catalpol in leaves of the "low-IG" plants and reduction in "high-IG" plants. This pattern might arise if damage is caused mainly by specialist herbivores for which catalpol may act as feeding stimulant rather than as deterrent. The present study documents for the first time that intraspecific variation in plant defense affects the outcome of plant-mediated interactions between root and shoot herbivores.

Effects of Soil Organisms on Aboveground Plant-Insect Interactions in the Field: Patterns, Mechanisms and the Role of Methodology

“…Interestingly, on ribwort plantain, Plantago lanceolata that were exposed to belowground herbivory by Agriotes spp., aboveground herbivory levels were three times lower on a high-iridoid glycoside (secondary defense metabolites in Plantago) producing lineage, compared to controls without root herbivores. In contrast, herbivory levels were nine times higher in response to the root herbivore on a low iridoid glycoside lineage (Wurst et al, 2008). This study illustrates that the genetic background of a plant can play an important role in determining plant-mediated effects of root insect herbivores on aboveground chewing insect herbivores.…”

“…In field studies, plant-mediated effects of coleopteran root herbivores on aboveground chewing herbivores can be neutral (Hunt-Joshi et al, 2004;Barber et al, 2015;Borgström et al, 2017), positive (Wurst et al, 2008), or negative (White and Andow, 2006;Wurst et al, 2008;Megías and Müller, 2010, see Figure 2D, Supplementary Table 4). Interestingly, on ribwort plantain, Plantago lanceolata that were exposed to belowground herbivory by Agriotes spp., aboveground herbivory levels were three times lower on a high-iridoid glycoside (secondary defense metabolites in Plantago) producing lineage, compared to controls without root herbivores.…”

“…Moreover, plant secondary defense metabolites, that play a role in the palatability of host plants, can be affected by soil organisms in the field (Wurst et al, 2008;Megías and Müller, 2010). Interactions with soil organisms can also sensitize the immune system of plants so that they can respond faster or more strongly to subsequent attack by antagonists (e.g., Pieterse et al, 2014).…”

Effects of intraspecific variation in white cabbage (Brassica oleracea var. capitata) on soil organisms

“…differences in the production of toxic compounds that affect soil organisms. However, belowground effects of intraspecific plant variation on plant-animal interactions have only been studied to a limited extent and mostly within single organism groups (Andersen et al 2007;Griffiths et al 2005;Wardle 2006;Wurst et al 2008).…”

Arriving at the right time : a temporal perspective on above-belowground herbivore interactions

“…Numerous studies have shown that the concentrations of these compounds in shoots and roots can have strongly negative effects on the performance of generalist above-and belowground insect herbivores, but that they can be used as feeding cues and oviposition stimulants by specialist insect herbivores (e.g. Bowers and Puttick 1989;Nieminen et al 2003;Wurst et al 2008;Reudler Talsma et al 2008, 2011.…”