Dataset Information

Species-specific plant-soil feedbacks alter herbivore-induced gene expression and defense chemistry in Plantago lanceolata.

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.

SUBMITTER: Zhu F

PROVIDER: S-EPMC6208702 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

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Species-specific plant-soil feedbacks alter herbivore-induced gene expression and defense chemistry in Plantago lanceolata.

Zhu Feng F Heinen Robin R van der Sluijs Martijn M Raaijmakers Ciska C Biere Arjen A Bezemer T Martijn TM

Oecologia 20180814 3

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 b ...[more]

PMID: 30109421

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Project description:Intraspecific negative feedback effects, where performance is reduced on soils conditioned by conspecifics, are widely documented in plant communities. However, interspecific feedbacks are less well studied, and their direction, strength, causes, and consequences are poorly understood. If more closely related species share pathogens, or have similar soil resource requirements, plants may perform better on soils conditioned by more distant phylogenetic relatives. There have been few empirical tests of this prediction across plant life stages, and none of which attempt to account for soil chemistry. Here, we test the utility of phylogeny for predicting soil feedback effects on plant survival and performance (germination, seedling survival, growth rate, biomass). We implement a full factorial experiment growing species representing five families on five plant family-specific soil sources. Our experiments exploit soils that have been cultured for over 30 years in plant family-specific beds at Oxford University Botanic Gardens. Plant responses to soil source were idiosyncratic, and species did not perform better on soils cultured by phylogenetically more distant relatives. The magnitude and sign of feedback effects could, however, be explained by differences in the chemical properties of "home" and "away" soils. Furthermore, the direction of soil chemistry-related plant-soil feedbacks was dependent on plant life stage, with the effects of soil chemistry on germination success and accumulation of biomass inversely related. Our results (1) suggest that the phylogenetic distance between plant families cannot predict plant-soil feedbacks across multiple life stages, and (2) highlight the need to consider changes in soil chemistry as an important driver of population responses. The contrasting responses at plant life stages suggest that studies focusing on brief phases in plant demography (e.g., germination success) may not give a full picture of plant-soil feedback effects.

Project description:Increasing demands to reduce fertilizer and pesticide input in agriculture has triggered interest in arbuscular mycorrhizal fungi (AMF) that can enhance plant growth and confer mycorrhiza-induced resistance (MIR). MIR can be based on a variety of mechanisms, including induction of defense compounds, and sensitization of the plant's immune system (priming) for enhanced defense against later arriving pests or pathogens signaled through jasmonic acid (JA). However, growth and resistance benefits of AMF highly depend on environmental conditions. Low soil P and non-limiting light conditions are expected to enhance MIR, as these conditions favor AMF colonization and because of observed positive cross-talk between the plant's phosphate starvation response (PSR) and JA-dependent immunity. We therefore tested growth and resistance benefits of the AMF Funneliformis mosseae in Plantago lanceolata plants grown under different levels of soil P and light intensity. Resistance benefits were assessed in bioassays with the leaf chewing herbivore Mamestra brassicae. Half of the plants were induced by jasmonic acid prior to the bioassays to specifically test whether AMF primed plants for JA-signaled defense under different abiotic conditions. AMF reduced biomass production but contrary to prediction, this reduction was not strongest under conditions considered least optimal for carbon-for-nutrient trade (low light, high soil P). JA application induced resistance to M. brassicae, but its extent was independent of soil P and light conditions. Strikingly, in younger plants, JA-induced resistance was annulled by AMF under high resource conditions (high soil P, ample light), indicating that AMF did not prime but repressed JA-induced defense responses. In older plants, low soil P and light enhanced susceptibility to M. brassicae due to enhanced leaf nitrogen levels and reduced leaf levels of the defense metabolite catalpol. By contrast, in younger plants, low soil P enhanced resistance. Our results highlight that defense priming by AMF is not ubiquitous and calls for studies revealing the causes of the increasingly observed repression of JA-mediated defense by AMF. Our study further shows that in our system abiotic factors are significant modulators of defense responses, but more strongly so by directly modulating leaf quality than by modulating the effects of beneficial microbes on resistance.

Project description:Backgrounds and aimsNegative plant-soil feedbacks (PSFs) are thought to promote species coexistence, but most evidence is derived from theoretical models and data from plant monoculture experiments.MethodsWe grew Anthoxanthum odoratum and Centaurea jacea in field plots in monocultures and in mixtures with three ratios (3:1, 2:2 and 1:3) for three years. We then tested in a greenhouse experiment the performance of A. odoratum and C. jacea in pots planted with monocultures and 1:1 mixtures and filled with live and sterile soils collected from the field plots.ResultsIn the greenhouse experiment, C. jacea produced less aboveground biomass in soil conditioned by C. jacea monocultures than in soil conditioned by A. odoratum monocultures, while the aboveground biomass of A. odoratum in general did not differ between the two monospecific soils. The negative PSF effect was greater in the 1:1 plant mixture than in plant monocultures for A. odoratum but did not differ for C. jacea. In the greenhouse experiment, the performance of C. jacea relative to A. odoratum in the 1:1 plant mixture was negatively correlated to the abundance of C. jacea in the field plot where the soil was collected from. This relationship was significant both in live and sterile soils. However, there was no relationship between the performance of A. odoratum relative to C. jacea in the 1:1 plant mixture in the greenhouse experiment and the abundance of A. odoratum in the field plots.ConclusionsThe response of a plant to PSF depends on whether the focal species grows in monocultures or in mixtures and on the identity of the species. Interspecific competition can exacerbate the negative plant-soil feedbacks compared to intraspecific competition when a plant competes with a stronger interspecific competitor. Moreover, the abundance of a species in mixed plant communities, via plant-soil feedback, negatively influences the relative competitiveness of that species when it grows later in interspecific competition, but this effect varies between species. This phenomenon may contribute to the coexistence of competing plants under natural conditions through preventing the dominance of a particular plant species.

Dataset Information

Species-specific plant-soil feedbacks alter herbivore-induced gene expression and defense chemistry in Plantago lanceolata.

Publications

Species-specific plant-soil feedbacks alter herbivore-induced gene expression and defense chemistry in Plantago lanceolata.

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