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Jos van Damme was een bevlogen en eigenzinnig populatiebioloog, afdelingshoofd en hoogleraar, die ging werken als verpleegkundige om ook 'iets voor mensen te betekenen'.

Insect herbivory can affect interactions between plants and arbuscular mycorrhizal (AM) fungi through herbivore-modified root carbon pools, while the specific metabolic changes underlying fungal responses to herbivory are poorly understood. Here we explored the impacts of foliar herbivory and mechanical wounding on AM colonisation and AM community composition of common ragweed (Ambrosia artemisiifolia) and the role of root metabolites in mediating these effects. Foliar insect herbivory enhanced AM colonisation, whereas mechanical wounding only enhanced AM colonisation in combination with application of caterpillar oral secretions. Meanwhile, the relative abundance of Glomus species was increased in root endosphere, rhizoplane and rhizosphere soils after foliar herbivory. Foliar herbivory also increased the concentrations of fatty acids in roots but decreased phenolics, and their concentrations were significantly correlated with AM colonisation. Addition of exudates from plants exposed to herbivory resulted in increases in AM colonisation of plants without herbivory. Moreover, widely targeted metabolomic analyses revealed that foliar herbivory enhanced the relative abundance of lipids and decreased phenols in root exudates. Synthesis. We show that plants can enhance their associations with arbuscular mycorrhizal (AM) fungi when subject to above-ground herbivory, possibly mediated by herbivore-induced increases in the levels of root lipids. Our findings highlight the role of root lipids in above-below-ground biological interactions, providing novel insights into plant-AM fungi integrative responses to biotic stresses.

Beneficial soil microbes can enhance plant growth and defense, but the extent to which this occurs depends on the availability of resources, such as water and nutrients. However, relatively little is known about the role of light quality, which is altered during shading, resulting in a low red: far-red ratio (R:FR) of light. We examined how low R:FR light influences arbuscular mycorrhizal fungus (AMF)-mediated changes in plant growth and defense using Solanum lycopersicum (tomato) and the insect herbivore Chrysodeixis chalcites. We also examined effects on third trophic level interactions with the parasitoid Cotesia marginiventris. Under low R:FR light, non-mycorrhizal plants activated the shade avoidance syndrome (SAS), resulting in enhanced biomass production. However, mycorrhizal inoculation decreased stem elongation in shaded plants, thus counteracting the plant’s SAS response to shading. Unexpectedly, activation of SAS under low R:FR light did not increase plant susceptibility to the herbivore in either non-mycorrhizal or mycorrhizal plants. AMF did not significantly affect survival or growth of caterpillars and parasitoids but suppressed herbivore-induced expression of jasmonic acid-signaled defenses genes under low R:FR light. These results highlight the context-dependency of AMF effects on plant growth and defense and the potentially adverse effects of AMF under shading., Beneficial soil microbes can enhance plant growth and defense, but the extent to which this occurs depends on the availability of resources, such as water and nutrients. However, relatively little is known about the role of light quality, which is altered during shading, resulting in a low red: far-red ratio (R:FR) of light. We examined how low R:FR light influences arbuscular mycorrhizal fungus (AMF)-mediated changes in plant growth and defense using Solanum lycopersicum (tomato) and the insect herbivore Chrysodeixis chalcites. We also examined effects on third trophic level interactions with the parasitoid Cotesia marginiventris. Under low R:FR light, non-mycorrhizal plants activated the shade avoidance syndrome (SAS), resulting in enhanced biomass production. However, mycorrhizal inoculation decreased stem elongation in shaded plants, thus counteracting the plant’s SAS response to shading. Unexpectedly, activation of SAS under low R:FR light did not increase plant susceptibility to the herbivore in either non-mycorrhizal or mycorrhizal plants. AMF did not significantly affect survival or growth of caterpillars and parasitoids but suppressed herbivore-induced expression of jasmonic acid-signaled defenses genes under low R:FR light. These results highlight the context-dependency of AMF effects on plant growth and defense and the potentially adverse effects of AMF under shading.

Entomopathogenic fungi have been well exploited as biocontrol agents that can kill insects through direct contact. However, recent research has shown that they can also play an important role as plant endophytes, stimulating plant growth, and indirectly suppressing pest populations. In this study, we examined the indirect, plant-mediated, effects of a strain of entomopathogenic fungus, Metarhizium brunneum on plant growth and population growth of two-spotted spider mites (Tetranychus urticae) in tomato, using different inoculation methods (seed treatment, soil drenching and a combination of both). Furthermore, we investigated changes in tomato leaf metabolites (sugars and phenolics), and rhizosphere microbial communities in response to M. brunneum inoculation and spider mite feeding. A significant reduction in spider mite population growth was observed in response to M. brunneum inoculation. The reduction was strongest when the inoculum was supplied both as seed treatment and soil drench. This combination treatment also yielded the highest shoot and root biomass in both spider mite-infested and non-infested plants, while spider mite infestation increased shoot but reduced root biomass. Fungal treatments did not consistently affect leaf chlorogenic acid and rutin concentrations, but M. brunneum inoculation via a combination of seed treatment and soil drenching reinforced chlorogenic acid (CGA) induction in response to spider mites and under these conditions the strongest spider mite resistance was observed. However, it is unclear whether the M. brunneum-induced increase in CGA contributed to the observed spider mite resistance, as no general association between CGA levels and spider mite resistance was observed. Spider mite infestation resulted in up to two-fold increase in leaf sucrose concentrations and a three to five-fold increase in glucose and fructose concentrations, but these concentrations were not affected by fungal inoculation. Metarhizium, especially w

The physiological performance of organisms depends on their environmental context, resulting in performance-response curves along environmental gradients. Parasite performance-response curves are generally expected to be broader than those of their hosts due to shorter generation times and hence faster adaptation. However, certain environmental conditions may limit parasite performance more than that of the host, thereby providing an environmental refuge from disease. Thermal disease refuges have been extensively studied in response to climate warming, but other environmental factors may also provide environmental disease refuges which, in turn, respond to global change. Here, we 1) showcase laboratory and natural examples of refuges from parasites along various environmental gradients, and 2) provide hypotheses on how global environmental change may affect these refuges. We strive to synthesise knowledge on potential environmental disease refuges along different environmental gradients including salinity and nutrients, in both natural and food-production systems. Although scaling up from single host-parasite relationships along one environmental gradient to their interaction outcome in the full complexity of natural environments remains difficult, integrating host and parasite performance-response can serve to formulate testable hypotheses about the variability in parasitism outcomes and the occurrence of environmental disease refuges under current and future environmental conditions.

The physiological performance of organisms depends on their environmental context, resulting in performance–response curves along environmental gradients. Parasite performance–response curves are generally expected to be broader than those of their hosts due to shorter generation times and hence faster adaptation. However, certain environmental conditions may limit parasite performance more than that of the host, thereby providing an environmental refuge from disease. Thermal disease refuges have been extensively studied in response to climate warming, but other environmental factors may also provide environmental disease refuges which, in turn, respond to global change. Here, we (1) showcase laboratory and natural examples of refuges from parasites along various environmental gradients, and (2) provide hypotheses on how global environmental change may affect these refuges. We strive to synthesize knowledge on potential environmental disease refuges along different environmental gradients including salinity and nutrients, in both natural and food-production systems. Although scaling up from single host–parasite relationships along one environmental gradient to their interaction outcome in the full complexity of natural environments remains difficult, integrating host and parasite performance–response can serve to formulate testable hypotheses about the variability in parasitism outcomes and the occurrence of environmental disease refuges under current and future environmental conditions.

Introduction: Fitness of plants is affected by their symbiotic interactions with arbuscular mycorrhizal fungi (AMF), and such effects are highly dependent on the environmental context. Methods: In the current study, we inoculated the nursery shrub species Artemisia ordosica with AMF species Funneliformis mosseae under contrasting levels of soil water and nutrients (diammonium phosphate fertilization), to assess their effects on plant growth, physiology and natural infestation by herbivores. Results: Overall, plant biomass was synergistically enhanced by increasing soil water and soil nutrient levels. However, plant height was surprisingly repressed by AMF inoculation, but only under low water conditions. Similarly, plant biomass was also reduced by AMF but only under low water and nutrient conditions. Furthermore, AMF significantly reduced leaf phosphorus levels, that were strongly enhanced under high nutrient conditions, but had only minor effects on leaf chlorophyll and proline levels. Under low water and nutrient conditions, specific root length was enhanced, but average root diameter was decreased by AMF inoculation. The negative effects of AMF on plant growth at low water and nutrient levels may indicate that under these conditions AMF inoculation does not strongly contribute to nutrient and water acquisition. On the contrary, the AMF might have suppressed the direct pathway of water and nutrient absorption by the plant roots themselves despite low levels of mycorrhizal colonization. AMF inoculation reduced the abundance of the foliar herbivore Chrysolina aeruginosa on plants that had been grown on the low nutrient soil, but not on high nutrient soil. Fertilization enhanced the abundance of this herbivore but only in plants that had received the high water treatment. The lower abundance of the herbivore on AMF plants could be related to their decreased leaf P content. In conclusion, our results indicate that AMF negatively affect the growth of Artemisia ordo

Release from enemies can lead to rapid evolution in invasive plants, including reduced metabolic investment in defence. Conversely, reassociation with enemies leads to renewed evolution of defence, but the potential costs of this evolution are poorly documented. We report increased resistance of the invader Ambrosia artemisiifolia after reassociation with a coevolved specialist herbivore, and that this increase corresponds with reduced abiotic stress tolerance. Herbivore resistance was higher, but drought tolerance was lower in plants from populations with a longer reassociation history, and this corresponded with changes in phenylpropanoids involved in insect resistance and abiotic stress tolerance. These changes were corroborated by shifts in the expression of underlying biosynthetic genes and plant anti-oxidants. Together, our findings suggest rapid evolution of plant traits after reassociation with coevolved enemies, resulting in genetically based shifts in investment between abiotic and biotic stress responses, providing insights into co-evolution, plant invasion and biological control.

Beneficial soil microbes can enhance plant growth and defense, but the extent to which this occurs depends on the availability of resources, such as water and nutrients. However, relatively little is known about the role of light quality, which is altered during shading, resulting a low red: far-red ratio (R:FR) of light. We examined how low R:FR light influences arbuscular mycorrhizal fungus (AMF)-mediated changes in plant growth and defense using Solanum lycopersicum (tomato) and the insect herbivore Chrysodeixis chalcites. We also examined effects on third trophic level interactions with the parasitoid Cotesia marginiventris. Under low R:FR light, non-mycorrhizal plants activated the shade avoidance syndrome (SAS), resulting in enhanced biomass production. However, mycorrhizal inoculation decreased stem elongation in shaded plants, thus counteracting the plant’s SAS response to shading. Unexpectedly, activation of SAS under low R:FR light did not increase plant susceptibility to the herbivore in either non-mycorrhizal or mycorrhizal plants. AMF did not significantly affect survival or growth of caterpillars and parasitoids but suppressed herbivore-induced expression of jasmonic acid-signaled defenses genes under low R:FR light. These results highlight the context-dependency of AMF effects on plant growth and defense and the potentially adverse effects of AMF under shading.

Many specialist herbivores have evolved strategies to cope with plant defences, with gut microbiota potentially participating to such adaptations. In this study, we assessed whether the history of plant use (population origin) and microbiota may interact with plant defence adaptation. We tested whether microbiota enhance the performance of Melitaea cinxia larvae on their host plant, Plantago lanceolata and increase their ability to cope the defensive compounds, iridoid glycosides (IGs). The gut microbiota were significantly affected by both larval population origin and host plant IG level. Contrary to our prediction, impoverishing the microbiota with antibiotic treatment did not reduce larval performance. As expected for this specialized insect herbivore, sequestration of one of IGs was higher in larvae fed with plants producing higher concentration of IGs. These larvae also showed metabolic signature of intoxication (i.e. decrease in Lysine levels). However, intoxication on highly defended plants was only observed when larvae with a history of poorly defended plants were simultaneously treated with antibiotics. Our results suggest that both adaptation and microbiota contribute to the metabolic response of herbivores to plant defence though complex interactions. Read the free Plain Language Summary for this article on the Journal blog.

Plant protection with beneficial microbes is considered to be a promising alternative to chemical control of pests and pathogens. Beneficial microbes can boost plant defences via induced systemic resistance (ISR), enhancing plant resistance against future biotic stresses. Although the use of ISR-inducing microbes in agriculture seems promising, the activation of ISR is context-dependent: it often occurs only under particular biotic and abiotic conditions, thus making its use unpredictable and hindering its application. Although major breakthroughs in research on mechanistic aspects of ISR have been reported, ISR research is mainly conducted under highly controlled conditions, differing from those in agricultural systems. This forms one of the bottlenecks for the development of applications based on ISR-inducing microbes in commercial agriculture. We propose an approach that explicitly incorporates context-dependent factors in ISR research to improve the predictability of ISR induction under environmentally variable conditions. Here, we highlight how abiotic and biotic factors influence plant–microbe interactions in the context of ISR. We also discuss the need to raise awareness in harnessing interdisciplinary efforts between researchers and stakeholders partaking in the development of applications involving ISR-inducing microbes for sustainable agriculture.

Recent research shows that earthworms can alter defense traits of plants against herbivores and pathogens by affecting soil biochemistry. Yet, the effects of invasive earthworms on defense traits of native plants from previously earthworm-free ecosystems as well as the consequences for multitrophic interactions are virtually unknown. Here we use a combination of an observational study and a complementary experimental study to investigate the effects of invasive earthworms on leaf defense traits, herbivore damage and pathogen infection in two poplar tree species (Populus balsamifera and Populus tremuloides) native to North American boreal forests. Our observational study showed that earthworm invasion was associated with enhanced leaf herbivory (by leaf-chewing insects) in saplings of both tree species. However, we only detected significant shifts in the concentration of chemical defense compounds in response to earthworm invasion for P. balsamifera. Specifically, leaf phenolic concentrations, including salicinoids and catechin, were lower in P. balsamifera from earthworm-invaded sites. Our experimental study confirmed an earthworm-induced reduction in leaf defense levels in P. balsamifera for one of the defense compounds, tremulacin. The experimental study additionally showed that invasive earthworms reduced leaf dry matter content, potentially increasing leaf palatability, and enhanced susceptibility of trees to infection by a fungal pathogen, but not to aphid infestation, in the same tree species. Synthesis. Our results show that invasive earthworms can decrease the concentrations of some chemical defense compounds in P. balsamifera, which could make them susceptible to leaf-chewing insects. Such potential impacts of invasive earthworms are likely to have implications for tree survival and competition, native tree biodiversity and ecosystem functioning.

Plant–microbe–arthropod (PMA) three-way interactions have important implications for plant health. However, our poor understanding of the underlying regulatory mechanisms hampers their biotechnological applications. To this end, we searched for potential common patterns in plant responses regarding taxonomic groups or lifestyles. We found that most signaling modules regulating two-way interactions also operate in three-way interactions. Furthermore, the relative contribution of signaling modules to the final plant response cannot be directly inferred from two-way interactions. Moreover, our analyses show that three-way interactions often result in the activation of additional pathways, as well as in changes in the speed or intensity of defense activation. Thus, detailed, basic knowledge of plant–microbe–arthropod regulation will be essential for the design of environmentally friendly crop management strategies.

Plant–soil feedbacks of plants that are exposed to herbivory have been shown to differ from those of plants that are not exposed to herbivores. Likely, this process is mediated by jasmonic acid (JA) and salicylic acid (SA) defense pathways, which are induced by aboveground herbivory. Furthermore, exogenous application of these phytohormones to plants alters belowground communities, but whether this changes plant–soil feedbacks in natural systems is unknown. We applied exogenous sprays of JA and SA individually and in combination to field plots in a restored grassland. Control plots were sprayed with demineralized water. After three repeated application rounds, we transplanted seedlings of the plant–soil feedback model plant Jacobaea vulgaris as phytometer plants to test the effects of potential phytohormone-mediated changes in the soil, on plant performance during the response phase. We further measured how exogenous application of phytohormones altered plant-related ecosystem characteristics (plot-level); soil chemistry, plot productivity, insect communities and predation. Biomass of the phytometer plants only co-varied with plot productivity, but was not influenced by phytohormone applications. However, we did observe compound-specific effects of SA application on insect communities, most notably on parasitoid attraction, and of JA application on soil nitrogen levels. Although we did not find effects on plant–soil feedbacks, the effects of exogenous application of phytohormones did alter other ecosystem-level processes related to soil nutrient cycling, which may lead to legacy effects in the longer term. Furthermore, exogenous application of phytohormones led to altered attraction of specific insect groups.

Rapid human population growth and associated urbanization lead to increased artificial illumination of the environment. By changing the natural light–dark cycle, artificial lighting can affect the functioning of natural ecosystems. Many plants rely on insects in order to reproduce but these insects are known to be disturbed by artificial light. Therefore, plant–insect interactions may be affected when exposed to artificial illumination. These effects can potentially be reduced by using different light spectra than white light. We studied the effect of artificial lighting on plant–insect interactions in the Silene latifolia–Hadena bicruris system using a field set-up with four different light treatments: red, green, white and a dark control. We compared the proportion of fertilized flowers and fertilized ovules as well as the infestation of fruits by Hadena bicruris, a pollinating seed predator. We found no difference in the proportion of fertilized flowers among the treatments. The proportion of fruits infested by H. bicruris was however significantly higher under green and white light and a significantly lower proportion of fertilized ovules was found under green light. We show that artificial light with different colours impacts plant–insect interactions differently, with direct consequences for plant fitness.

Plant–soil feedbacks of plants that are exposed to herbivory have been shown to differ from those of plants that are not exposed to herbivores. Likely, this process is mediated by jasmonic acid (JA) and salicylic acid (SA) defense pathways, which are induced by aboveground herbivory. Furthermore, exogenous application of these phytohormones to plants alters belowground communities, but whether this changes plant–soil feedbacks in natural systems is unknown. We applied exogenous sprays of JA and SA individually and in combination to field plots in a restored grassland. Control plots were sprayed with demineralized water. After three repeated application rounds, we transplanted seedlings of the plant–soil feedback model plant Jacobaea vulgaris as phytometer plants to test the effects of potential phytohormone-mediated changes in the soil, on plant performance during the response phase. We further measured how exogenous application of phytohormones altered plant-related ecosystem characteristics (plot-level); soil chemistry, plot productivity, insect communities and predation. Biomass of the phytometer plants only co-varied with plot productivity, but was not influenced by phytohormone applications. However, we did observe compound-specific effects of SA application on insect communities, most notably on parasitoid attraction, and of JA application on soil nitrogen levels. Although we did not find effects on plant–soil feedbacks, the effects of exogenous application of phytohormones did alter other ecosystem-level processes related to soil nutrient cycling, which may lead to legacy effects in the longer term. Furthermore, exogenous application of phytohormones led to altered attraction of specific insect groups.

Plant–microbe–arthropod (PMA) three-way interactions have important implications for plant health. However, our poor understanding of the underlying regulatory mechanisms hampers their biotechnological applications. To this end, we searched for potential common patterns in plant responses regarding taxonomic groups or lifestyles. We found that most signaling modules regulating two-way interactions also operate in three-way interactions. Furthermore, the relative contribution of signaling modules to the final plant response cannot be directly inferred from two-way interactions. Moreover, our analyses show that three-way interactions often result in the activation of additional pathways, as well as in changes in the speed or intensity of defense activation. Thus, detailed, basic knowledge of plant–microbe–arthropod regulation will be essential for the design of environmentally friendly crop management strategies.

Plants form mutualistic relationship with a variety of belowground fungal species. Such a mutualistic relationship can enhance plant growth and resistance to pathogens. Yet, we know little about how interactions between functionally diverse groups of fungal mutualists affect plant performance and competition. We experimentally determined the effects of interaction between two functional groups of belowground fungi that form mutualistic relationship with plants, arbuscular mycorrhizal (AM) fungi and Trichoderma, on interspecific competition between pairs of closely related plant species from four different genera. We hypothesized that the combination of two functionally diverse belowground fungal species would allow plants and fungi to partition their symbiotic relationships and relax plant?plant competition. Our results show that: 1) the AM fungal species consistently outcompeted the Trichoderma species independent of plant combinations; 2) the fungal species generally had limited effects on competitive interactions between plants; 3) however, the combination of fungal species relaxed interspecific competition in one of the four instances of plant?plant competition, despite the general competitive superiority of AM fungi over Trichoderma. We highlight that the competitive outcome between functionally diverse fungal species may show high consistency across a broad range of host plants and their combinations. However, despite this consistent competitive hierarchy, the consequences of their interaction for plant performance and competition can strongly vary among plant communities.

Anthropogenic global warming and attendant effects like heatwaves affect the biology and ecology of both individuals and species within and across different trophic levels. Here, we examined the effects of a simulated heatwave on development of and competition between two hyperparasitoid wasps, Lysibia nana and Acrolyta nens when attacking the same host, cocoons of the primary parasitoid, Cotesia glomerata. Parasitized hosts were exposed to three different day and night temperature regimes (low, medium and high) that reflect cool, normal and heatwave conditions in the Netherlands. We found that higher temperatures decreased survival to eclosion more strongly in the hyperparasitoids than in their host. Heatwave conditions also shortened development time and led to the production of smaller adult wasps of both hyperparasitoid species in singly parasitized hosts. In multiparasitized hosts, L. nana won most of the contests when it oviposited first, irrespective of the time interval between the first and second parasitism, whereas A. nens only dominated when it had a 24 h head start or longer. Most importantly, our results show that L. nana in particular benefited in competition at higher temperatures, perhaps due to an increase in the metabolic rate and more rapid egg and/or larval development. This may potentially reduce opportunities for coexistence following heat waves. Our results suggest that heatwaves associated with global warming will enhance the rate of development, but negatively affect survival and other fitness-related traits in (hyper)parasitoids. Moreover, the outcome of larval competition may be determined via physiological responses that are species-specific and thus influence phenology. This article is protected by copyright. All rights reserved.