Spatial and temporal components of induced plant responses in the context of herbivore life history and impact on host

Abstract

Plants defend against herbivores and pathogens through integrated constitutive and induced defences. Induced responses may be expressed locally or tissue/plant-wide, i.e. systemically, and may also be primed for subsequent attack. Although the elicitation and efficacy of induced responses are increasingly well-characterised, we have little understanding of how timing and within-plant spatial patterns of induced defences relate to different herbivore behaviours and selective pressures. We used interactions between pines and their major mortality agents, native bark beetle-fungal complexes, to explore this dimension. We analysed concentrations of multiple terpenoid and phenolic classes, and lesion formation, to provide a comprehensive profile of specialised metabolites and histological responses in red pine (Pinus resinosa) phloem. We examined these profiles in constitutive tissue and following simulated attack, sampling both at the point of challenge and away from the attack site, and following a second simulated attack. Terpenoid concentrations increased by >100-fold at the site of simulated attack. In contrast, systemic induction of terpenoids was absent or weak, with most exhibiting no change and others increasing only 1.5–2 fold. Previous elicitation did not influence terpenoid concentrations, either locally or tissue-wide, when trees were challenged a second time. Phenolics had mixed responses in localised tissues, with some compounds increasing and others decreasing. Like terpenoids, phenolics did not show substantial systemic, tissue-wide changes, and likewise showed no evidence of priming. Collectively, these results indicate that red pine employs a strategy of maximising its response at each point of attack by bark beetles. Pines have been shown to express systemic induced resistance against several canker fungi, so the absence of these responses suggests agent-specific reactions, rather than inherent incapability. Rapid local induction seems to be a better strategy in this instance because if a bark beetle can succeed in entering and producing pheromones from a host, the resulting mass attack usually exceeds defense capacity and kills the tree. These results highlight how plant defence syndromes can modulate the spatial and temporal dynamics of induced responses, in addition to the chemical and morphological traits deployed. A plain language summary is available for this article.