Abstract
Plants actively interact with antagonists and beneficial organisms occurring in the above- and belowground domains of terrestrial ecosystems. In the past decade, studies have focused on the role of plant–soil feedbacks (PSF) in a broad range of ecological processes. However, PSF and its legacy effects on plant defense traits, such as induction of defense-related genes and production of defensive secondary metabolites, have not received much attention. Here, we study soil legacy effects created by twelve common grassland plant species on the induction of four defense-related genes, involved in jasmonic acid signaling, related to chewing herbivore defense (LOX2, PPO7), and in salicylic acid signaling, related to pathogen defense (PR1 and PR2) in Plantago lanceolata in response to aboveground herbivory by Mamestra brassicae. We also assessed soil legacy and herbivory effects on the production of terpenoid defense compounds (the iridoid glycosides aucubin and catalpol) in P. lanceolata. Our results show that both soil legacy and herbivory influence phenotypes of P. lanceolata in terms of induction of Pl PPO7 and Pl LOX2, whereas the expression of Pl PR1 and Pl PR2-1 is not affected by soil legacies, nor by herbivory. We also find species-specific soil legacy effects on the production of aucubin. Moreover, P. lanceolata accumulates more catalpol when they are grown in soils conditioned by grass species. Our study highlights that PSF can influence aboveground plant–insect interactions through the impacts on plant defense traits and suggests that aboveground plant defense responses can be determined, at least partly, by plant-specific legacy effects induced by belowground organisms.
Highlights
As plants are members of complex communities, they simultaneously interact with both antagonists and beneficial organisms occurring both above and below the ground (Pieterse et al 2013; Biere and Goverse 2016)
We found an interaction between herbivory and the plant species that conditioned the soil on the overall transcript levels of Pl LOX2-2, a gene that is involved in the biosynthesis of jasmonic acid (JA)
Pl LOX2-2 was up-regulated by herbivory in some of the conditioned soils, most notably in soils conditioned by P. lanceolata, T. officinale, H. lanatus and F. ovina
Summary
As plants are members of complex communities, they simultaneously interact with both antagonists and beneficial organisms occurring both above and below the ground (Pieterse et al 2013; Biere and Goverse 2016). To cope with challenges by harmful pathogens and insect herbivores, plants have evolved a complex immune system that modulates plant defensive responses, from recognition of alien molecules or signals from damaged plant cells to activation of effective immune responses against the attackers (Jones and Dangl 2006; Howe and Jander 2008). Benefits of the associations with microbes to the plants are often based on the growth-promoting effects of beneficial microbes, as well as on the activation of induced systemic resistance (ISR) resulting in sensitization of the plant immune system (priming) for a more efficient activation of plant defenses upon a future attack (Zamioudis and Pieterse 2012). Beneficial rhizosphere microbes can prime the plant for enhanced defense against a broad range of insect herbivores (Van Oosten et al 2008; Van Wees et al 2008; Jung et al 2012; van de Mortel et al 2012; Pangesti et al 2013)
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