Mechanisms and ecological implications of plant-mediated interactions between belowground and aboveground insect herbivores

Plant-mediated interactions between belowground (BG) and aboveground (AG) herbivores have received increasing interest recently. However, the molecular mechanisms underlying ecological consequences of BG–AG interactions are not fully clear yet. Herbivore-induced plant defenses are complex and comprise phytohormonal signaling, gene expression and production of defensive compounds (defined here as response levels), each with their own temporal dynamics. Jointly they shape the response that will be expressed. However, because different induction methods are used in different plant-herbivore systems, and only one or two response levels are measured in each study, our ability to construct a general framework for BG–AG interactions remains limited. Here we aim to link the mechanisms to the ecological consequences of plant-mediated interactions between BG and AG insect herbivores. We first outline the molecular mechanisms of herbivore-induced responses involved in BG–AG interactions. Then we synthesize the literature on BG–AG interactions in two well-studied plant-herbivore systems, Brassica spp. and Zea mays, to identify general patterns and specific differences. Based on this comprehensive review, we conclude that phytohormones can only partially mimic induction by real herbivores. BG herbivory induces resistance to AG herbivores in both systems, but only in maize this involves drought stress responses. This may be due to morphological and physiological differences between monocotyledonous (maize) and dicotyledonous (Brassica) species, and differences in the feeding strategies of the herbivores used. Therefore, we strongly recommend that future studies explicitly account for these basic differences in plant morphology and include additional herbivores while investigating all response levels involved in BG–AG interactions.