Abstract
The high structural diversity of plant metabolites suggests that interactions among them should be common. We investigated the effects of single metabolites and combinations of plant metabolites on insect herbivores. In particular we studied the interacting effects of pyrrolizidine alkaloid (PAs), and chlorogenic acid (CGA), on a generalist herbivore, Frankliniella occidentalis. We studied both the predominantly occurring PA N-oxides and the less frequent PA free bases. We found antagonistic effects between CGA and PA free bases on thrips mortality. In contrast PA N-oxides showed synergistic interactions with CGA. PA free bases caused a higher thrips mortality than PA N-oxides while the reverse was through for PAs in combination with CGA. Our results provide an explanation for the predominate storage of PA N-oxides in plants. We propose that antagonistic interactions represent a constraint on the accumulation of plant metabolites, as we found here for Jacobaea vulgaris. The results show that the bioactivity of a given metabolite is not merely dependent upon the amount and chemical structure of that metabolite, but also on the co-occurrence metabolites in, e.g., plant cells, tissues and organs. The significance of this study is beyond the concerns of the two specific groups tested here. The current study is one of the few studies so far that experimentally support the general conception that the interactions among plant metabolites are of great importance to plant-environment interactions.
Highlights
In nature plants are challenged by a multitude of herbivores and pathogens and they protect themselves against these attackers (Hartmann, 2008; Gols, 2014) with an array of defensive strategies, among which the chemical defenses are the most important (Johnson, 2011; Mithofer and Boland, 2012)
The combinations of all pyrrolizidine alkaloids (PAs) free bases with chlorogenic acid (CGA) showed a decreased thrips mortality (Figure 3 and Table 1; note that the fraction mortality was plotted in the 3D figures in order to increase the readability of the figure)
For retrorsine and monocrotaline the main effect of CGA concentration on the interaction effect single metabolite X (SX)∗Y is significant indicating that for these two PAs the strength of the antagonistic interaction is dependent on CGA concentration (Table 1)
Summary
In nature plants are challenged by a multitude of herbivores and pathogens and they protect themselves against these attackers (Hartmann, 2008; Gols, 2014) with an array of defensive strategies, among which the chemical defenses are the most important (Johnson, 2011; Mithofer and Boland, 2012). The plant kingdom has evolved an enormous number (>200,000) of chemically diverse metabolites (Dixon and Strack, 2003; Efferth and Koch, 2011). Interacting Effects between Plant Metabolites (Pichersky and Lewinsohn, 2011) were recorded in Arabidopsis thaliana (D’Auria and Gershenzon, 2005). It has become clear that the ability to synthesize SMs evolved in different plant lineages, and these compounds represent adaptations to specific ecological situations, for example, attraction of specific pollinators or defense against specific herbivores. For this reason, we refer to these compounds as “SMs” (Pichersky and Lewinsohn, 2011)
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