Constitutive and Induced Defenses to Herbivory in Above- And Belowground Plant Tissues

Abstract

A recent surge in attention devoted to the ecology of soil biota has prompted interest in quantifying similarities and differences between interactions occurring in above- and belowground communities. Furthermore, linkages that interconnect the dynamics of these two spatially distinct ecosystems are increasingly documented. We use a similar approach in the context of understanding plant defenses to herbivory, including how they are allocated between leaves and roots (constitutive defenses), and potential cross-system linkages (induced defenses). To explore these issues we utilized three different empirical approaches. First, we manipulated foliar and root herbivory on tobacco (Nicotiana tabacum) and measured changes in the secondary chemistry of above- and belowground tissues. Second, we reviewed published studies that compared levels of secondary chemistry between leaves and roots to determine how plants distribute putative defense chemicals across the above- and belowground systems. Last, we used meta-analysis to quantify the impact of induced responses across plant tissue types. In the tobacco system, leaf-chewing insects strongly induced higher levels of secondary metabolites in leaves but had no impact on root chemistry. Nematode root herbivores, however, elicited changes in both leaves and roots. Virtually all secondary chemicals measured were elevated in nematode-induced galls, whereas the impact of root herbivory on foliar chemistry was highly variable and depended on where chemicals were produced within the plant. Importantly, nematodes interfered with aboveground metabolites that have biosynthetic sites located in roots (e.g., nicotine) but had the opposite effect (i.e., nematodes elevated foliar expression) on chemicals produced in shoots (e.g., phenolics and terpenoids). Results from our literature review suggest that, overall, constitutive defense levels are extremely similar when comparing leaves with roots, although certain chemical classes (e.g., alkaloids, glucosinolates) are differentially allocated between above- and belowground parts. Based on a meta-analysis of induced defense studies we conclude that: (1) foliar induction generates strong responses in leaves, but much weaker responses in roots, and (2) root induction elicits responses of equal magnitude in both leaves and roots. We discuss the importance of this asymmetry and the paradox of cross-system induction in relation to optimal defense theory and interactions between above- and belowground herbivory.

Facilitation and inhibition: changes in plant nitrogen and secondary metabolites mediate interactions between above-ground and below-ground herbivores

“…Taken together, changes in tannins in roots and leaves may contribute to the variable performance of Bikasha above-ground adults and below-ground larvae, and their interactions. A growing body of evidence indicates that induced defence to above-ground herbivory may be substantially different from that to below-ground herbivory [14,[31][32][33]. The different tannin responses in above-ground and belowground tissues may also reflect an asymmetric induction and associated transportation in the plant.…”

Reciprocal feeding facilitation between above- and below-ground herbivores

“…Although facilitative, there remained a degree of asymmetry in the interaction, with weevils exerting a much greater effect on aphid abundance than vice versa. While feeding facilitation has been found above-ground [17], positive non-reciprocal effects of above-ground herbivores on belowground herbivores are generally scarce (reviewed in [18]), and only one other study [5] has, to our knowledge, demonstrated reciprocal facilitation between above-and below-ground herbivores. In that case, the abundance of wireworms (Agriotes spp.)…”

Non-systemic fungal endophytes in Carex brevicollis may influence the toxicity of the sedge to livestock

“…Light has been shown to mediate the synthesis and activation of β-carbolines, a set of phytochemicals derived from tryptophan, which includes brevicolline (Downum, 1992). Regarding herbivory, the induction of toxic compounds has been much more studied in plant-insect systems (Kessler & Baldwin, 2002;Castells et al, 2005;Chen, 2008;Kaplan et al, 2008) than in plantmammal systems (Huntzinger et al, 2004;Zinn et al, 2007), although the occurrence of mechanisms of cross-resistance (defences induced by a particular herbivore being effective against other herbivores that consume the same plant) are assumed (Kessler & Baldwin, 2004). In plant-mammal systems, research has particularly addressed the loss of plant digestibility caused by the synthesis of defences against grazing/ browsing (such as phenolic or silica-based compounds, Massey et al, 2007), or it has focused on animals rather than plants, analysing the mechanisms developed by mammals to avoid or tolerate toxicity (Torregrossa & Dearing, 2010).…”