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Experimental Growth Conditions affect Direct and Indirect Defences in two Cotton Species

2023, Laura Chappuis, Alicia Egger, Röder, Gregory, Glauser, Gaëtan, Geoffrey Jaffuel, Betty Benrey, Luis Abdala-Roberts, Mary V. Clancy, Turlings, Ted, Bustos Segura, Carlos

Cotton has been used as a model plant to study direct and indirect plant defence against herbivorous insects. However, the plant growing conditions could have an important effect on the outcome of such plant defence studies. We examined how common experimental growth conditions influence constitutive and inducible defences in two species of cotton, Gossypium hirsutum and G. herbaceum. We induced plants by applying caterpillar regurgitant to mechanical wounds to compare the induction levels between plants of both species grown in greenhouse or phytotron conditions. For this we measured defence metabolites (gossypol and heliocides) and performance of Spodoptera frugiperda caterpillars on different leaves, the emission of plant volatiles, and their attractiveness to parasitic wasps. Induction increased the levels of defence metabolites, which in turn decreased the performance of S. frugiperda larvae. Constitutive and induced defence levels were the highest in plants grown in the phytotron (compared to greenhouse plants), G. hirsutum and young leaves. Defence induction was more pronounced in plants grown in the phytotron and in young leaves. Also, the differences between growing conditions were more evident for metabolites in the youngest leaves, indicating an interaction with plant ontogeny. The composition of emitted volatiles was different between plants from the two growth conditions, with greenhouse-grown plants showing more variation than phytotron-grown plants. Also, G. hirsutum released higher amounts of volatiles and attracted more parasitic wasps than G. herbaceum. Overall, these results highlight the importance of experimental abiotic factors in plant defence induction and ontogeny of defences. We therefore suggest careful consideration in selecting the appropriate experimental growing conditions for studies on plant defences.

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Elevational gradients in constitutive and induced oak defences based on individual traits and their correlated expression patterns

2020-12-2, Galmán, Andrea, Abdala-Roberts, Luis, Wartalska, Pola, Covelo, Felisa, Röder, Gregory, Szenteczki, Mark, Moreira, Xoaquín, Rasmann, Sergio

Elevational gradients are useful ecological settings for revealing the biotic and abi-otic drivers of plant trait variation and plant–insect interactions. However, most work focusing on plant defences has looked at individual traits and few studies have assessed multiple traits simultaneously, their correlated expression patterns, and abiotic fac-tors associated with such patterns across elevations. To address this knowledge gap, we studied elevational variation in direct (phenolic compounds) and indirect (volatile organic compounds) constitutive defences and their inducibility after feeding by a spe-cialist beetle Altica quercetorum in saplings of 18 wild populations of Quercus pyrenaica. We tested for: 1) clines in each defensive trait individually, 2) their patterns of corre-lated expression and 3) associations between any such clines and climatic factors. We found that constitutive direct defences (lignins and hydrolysable tannins) decreased with increasing elevation. We observed no elevational gradient for constitutive indi-rect defences (volatile organic compounds) or the inducibility of direct or indirect defensive traits when looking at groups of compounds. However, at individual tree-level, increased induction of two monoterpenes (α-fenchene and camphene) at higher elevation was shown. Furthermore, we show a significant pattern of co-expression of constitutive and induced phenolics across populations, which weakened with increas-ing elevation. Finally, we found no evidence that climatic factors were associated with either individual or correlated trait expression patterns across elevations. Overall, these findings call for moving beyond elevational clines in individual plant defences, and argue that assessing elevational shifts in trait correlated expression patterns and their underlying mechanisms can increase our understanding of plant defence evolution and plant–herbivore interactions along environmental gradients.

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Environmental gradients and the evolution of tri‐trophic interactions

2018-11-28, Kergunteuil, Alan, Röder, Gregory, Rasmann, Sergio

Long‐standing theory predicts herbivores and predators should drive selection for increased plant defences, such as the specific production of volatile organic compounds for attracting predators near the site of damage. Along elevation gradients, a general pattern is that herbivores and predators are abundant at low elevation and progressively diminish at higher elevations. To determine whether plant adaptation along such a gradient influences top‐down control of herbivores, we manipulated soil predatory nematodes, root herbivore pressure and plant ecotypes in a reciprocal transplant experiment. Plant survival was significantly higher for low‐elevation plants, but only when in the presence of predatory nematodes. Using olfactometer bioassays, we showed correlated differential nematode attraction and plant ecotype‐specific variation in volatile production. This study not only provides an assessment of how elevation gradients modulate the strength of trophic cascades, but also demonstrates how habitat specialisation drives variation in the expression of indirect plant defences.

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Diffusion of the maize root signal (E)-β-caryophyllene in soils of different textures and the effects on the migration of the entomopathogenic nematode Heterorhabditis megidis

2017-6-10, Chiriboga, Xavier, Campos Herrera, Raquel, Jaffuel, Geoffrey, Röder, Gregory, Turlings, Ted

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Effect of herbivore load on VOC-mediated plant communication in potato

2023, Carla Vázquez-González, Violeta Quiroga, Lucía Martín-Cacheda, Rasmann, Sergio, Röder, Gregory, Luis Abdala-Roberts, Xoaquín Moreira

Herbivore-damaged plants emit volatile organic compounds (VOCs) that can alert neighbours and boost their resistance. While VOC-mediated plant communication has been shown to be herbivore-specific, we know little about its contingency on variation in herbivore load. To address this knowledge gap, we tested herbivore load effects on VOC-mediated communication between potato plants (Solanum tuberosum) using the generalist herbivore Spodoptera exigua. First, we tested whether herbivore load (three levels: undamaged control, low, and high load) affected total VOC emissions and composition. Second, we matched emitter and receiver plants and subjected emitters to the same herbivore load treatments. Finally, we performed a bioassay with S. exigua on receivers to test for induced resistance due to VOC-mediated communication. We found that herbivory significantly increased total VOC emissions relative to control plants, and that such increase was greater under high herbivore load. In contrast, we found no detectable effect of herbivory, regardless of the load, on VOC composition. The communication experiment showed that VOCs released by herbivore-induced emitters boosted resistance in receivers (i.e., lower leaf damage than receivers exposed to VOCs released by control emitters), but the magnitude of such effect was similar for both levels of emitter herbivore load. These findings suggest that changes in VOCs due to variation in herbivore load do not modify the outcomes of plant communication.

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The smell of hunger: Norway rats provision social partners based on odour cues of need

2020-3-24, Schneeberger, Karin, Röder, Gregory, Taborsky, Michael

When individuals exchange helpful acts reciprocally, increasing the benefit of the receiver can enhance its propensity to return a favour, as pay-offs are typically correlated in iterated interactions. Therefore, reciprocally cooperating animals should consider the relative benefit for the receiver when deciding to help a conspecific. Norway rats (Rattus norvegicus) exchange food reciprocally and thereby take into account both the cost of helping and the potential benefit to the receiver. By using a variant of the sequential iterated prisoner’s dilemma paradigm, we show that rats may determine the need of another individual by olfactory cues alone. In an experimental food-exchange task, test subjects were provided with odour cues from hungry or satiated conspecifics located in a different room. Our results show that wild-type Norway rats provide help to a stooge quicker when they receive odour cues from a hungry rather than from a satiated conspecific. Using chemical analysis by gas chromatography-mass spectrometry (GC-MS), we identify seven volatile organic compounds that differ in their abundance between hungry and satiated rats. Combined, this “smell of hunger” can apparently serve as a reliable cue of need in reciprocal cooperation, which supports the hypothesis of honest signalling.

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Root-colonizing bacteria enhance the levels of (E)-β-caryophyllene produced by maize roots in response to rootworm feeding

2018-2-9, Chiriboga, Xavier, Huijuan, Guo, Campos Herrera, Raquel, Röder, Gregory, Imperiali, Nicolas, Keel, Christoph, Maurhofer, Monika, Turlings, Ted

When larvae of rootworms feed on maize roots they induce the emission of the sesquiterpene (E)-β-caryophyllene (EβC). EβC is attractive to entomopathogenic nematodes, which parasitize and rapidly kill the larvae, thereby protecting the roots from further damage. Certain root-colonizing bacteria of the genus Pseudomonas also benefit plants by promoting growth, suppressing pathogens or inducing systemic resistance (ISR), and some strains also have insecticidal activity. It remains unknown how these bacteria influence the emissions of root volatiles. In this study, we evaluated how colonization by the growth-promoting and insecticidal bacteria Pseudomonas protegens CHA0 and Pseudomonas chlororaphis PCL1391 affects the production of EβC upon feeding by larvae of the banded cucumber beetle, Diabrotica balteata Le Conte (Coleoptera: Chrysomelidae). Using chemical analysis and gene expression measurements, we found that EβC production and the expression of the EβC synthase gene (tps23) were enhanced in Pseudomonas protegens CHA0-colonized roots after 72 h of D. balteata feeding. Undamaged roots colonized by Pseudomonas spp. showed no measurable increase in EβC production, but a slight increase in tps23 expression. Pseudomonas colonization did not affect root biomass, but larvae that fed on roots colonized by P. protegens CHA0 tended to gain more weight than larvae that fed on roots colonized by P. chlororaphis PCL1391. Larvae mortality on Pseudomonas spp. colonized roots was slightly, but not significantly higher than on non-colonized control roots. The observed enhanced production of EβC upon Pseudomonas protegens CHA0 colonization may enhance the roots' attractiveness to entomopathogenic nematodes, but this remains to be tested.

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Bioturbation by endogeic earthworms facilitates entomopathogenic nematode movement toward herbivore‑damaged maize roots

2020-12-4, Fattore, Sandrine, Xiao, Zhenggao, Godschalx, Adrienne, Röder, Gregory, Turlings, Ted, Le Bayon, Renée-Claire, Rasmann, Sergio

Entomopathogenic nematodes (EPNs) have been extensively studied as potential biological control agents against root-feeding crop pests. Maize roots under rootworm attack have been shown to release volatile organic compounds, such as (E)-β-caryophyllene (Eβc) that guide EPNs toward the damaging larvae. As yet, it is unknown how belowground ecosystems engineers, such as earthworms, affect the biological control capacity of EPNs by altering the root Eβc-mediated tritrophic interactions. We here asked whether and how, the presence of endogeic earthworms affects the ability of EPNs to find root-feeding larvae of the beetle Diabrotica balteata. First, we performed a field mesocosm experiment with two diverse cropping systems, and revealed that the presence of earthworms increased the EPN infection potential of larvae near maize roots. Subsequently, using climatecontrolled, olfactometer-based bioassays, we confirmed that EPNs response to Eβc alone (released from dispensers) was two-fold higher in earthworm-worked soil than in earthworm-free soil. Together our results indicate that endogeic earthworms, through burrowing and casting activities, not only change soil properties in a way that improves soil fertility but may also enhance the biocontrol potential of EPNs against root feeding pests. For an ecologically-sound pest reduction in crop fields, we advocate agricultural practices that favour earthworm community structure and diversity.

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The combined use of an attractive and repellent sex pheromonal component by a gregarious parasitoid

2019-3-28, Xu, Hao, Dötterl, Stefan, Zhou, Guoxin, Schäffler, Irmgard, von Arx, Martin, Röder, Gregory, Degen, Thomas, Chen, Li, Turlings, Ted

Gregarious parasitoids usually clump their cocoons together and the adults emerge in a synchronized fashion. This makes it easy for them to find mating partners and most copulations indeed take place at the natal patch. Yet, males should leave such sites when females are no longer receptive. As yet, this decision-making process and the possible involvement of pheromones were poorly understood. Here we report on a remarkable use of attractive and repellent pheromones of the well-studied gregarious parasitoid species Cotesia glomerata (L.) (Hymenoptera: Braconidae). Virgin C. glomerata females were found to release an attractive as well as a repellent compound, which in combination arrest males on the natal patch, but after mating the females stop the production of the attractant and the males are repelled. The repellent compound was identified as heptanal, which was also released by males, probably reducing male-male competition on the natal patch. We also confirmed that the sex ratio of the emerging wasps can vary considerably among patches, depending on the relative quality of hosts and the number of females that parasitize a host. The newly revealed use of attractive and repellent pheromone compounds by C. glomerata possibly helps maximize mating success under these variable conditions.

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Formal comment to Soler et al.: Great spotted cuckoo nestlings have no antipredatory effect on magpie or carrion crow host nests in southern Spain

2017-9-18, Canestrari, Daniela, Bolopo, Diana, Turlings, Ted, Röder, Gregory, Marcos, José, Baglione, Vittorio

Replicating research is crucial to assess the generality of findings. Yet, in ecology, the complexity of data collection and experimentation often precludes the possibility of going beyond single–population studies. The study by Soler et al. is therefore most welcome, as it provides new insights on the possible role of great spotted cuckoo in protecting the nest of its corvid hosts. In a previous article, we suggested a mechanism based on the malodorous secretion of great spotted cuckoo chicks to explain why the presence of the parasite in the nests of carrion crows in northern Spain increased the probability of nest success (i.e. fledging at least one host chick) as compared to non-parasitized nests. Soler et al. found no evidence supporting an anti-depredatory function of cuckoo chicks in their studied populations and proposed an alternative mechanism that may explain our experimental results. Here we would like to address a) the differences between the results of the two studies and b) the proposed interpretation of our translocation experiment. We will also respond to the concerns raised by Soler et al. on some of the analyses presented in our paper.