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Entomopathogenic nematodes as an effective and sustainable alternative to control the fall armyworm in Africa

2024-04-16, Fallet, Patrick, Didace Bazagwira, Livio Ruzzante, Geraldine Ingabire, Sacha Levivier, Bustos Segura, Carlos, Joelle Kajuga, Stefan Toepfer, Turlings, Ted, Joann Whalen

The recent invasion of the fall armyworm (FAW), a voracious pest, into Africa and Asia has resulted in unprecedented increases in insecticide applications, especially in maize cultivation. The health and environmental hazards posed by these chemicals have prompted a call for alternative control practices. Entomopathogenic nematodes are highly lethal to the FAWs, but their application aboveground has been challenging. In this study, we report on season-long field trials with an innocuous biodegradable gel made from carboxymethyl cellulose containing local nematodes that we specifically developed to target the FAW. In several Rwandan maize fields with distinct climatic conditions and natural infestation rates, we compared armyworm presence and damage in control plots and plots that were treated with either our nematode gel formulation, a commercial liquid nematode formulation, or the commonly used contact insecticide cypermethrin. The treatments were applied to the whorl of each plant, which was repeated three to four times, at 2-week intervals, starting when the plants were still seedlings. Although all three treatments reduced leaf damage, only the gel formulation decreased caterpillar infestation by about 50% and yielded an additional ton of maize per hectare compared with untreated plots. Importantly, we believe that the use of nematodes can be cost-effective, since we used nematode doses across the whole season that were at least 3-fold lower than their normal application against belowground pests. The overall results imply that precisely formulated and easy-to-apply nematodes can be a highly effective, affordable, and sustainable alternative to insecticides for FAW control.

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Soil salinization disrupts plant–plant signaling effects on extra-floral nectar induction in wild cotton

2023, Yeyson Briones-May, Teresa Quijano-Medina, Biiniza Pérez-Niño, Benrey, Betty, Turlings, Ted, Bustos Segura, Carlos, Luis Abdala-Roberts

Plant–plant interactions via volatile organic compounds (VOCs) have received much attention, but how abiotic stresses affect these interactions is poorly understood. We tested the effect of VOCs exposure from damaged conspecifics on the production of extra-floral nectar (EFN) in wild cotton plants (Gossypium hirsutum), a coastal species in northern Yucatan (Mexico), and whether soil salinization affected these responses. We placed plants in mesh cages, and within each cage assigned plants as emitters or receivers. We exposed emitters to either ambient or augmented soil salinity to simulate a salinity shock, and within each group subjected half of the emitters to no damage or artificial leaf damage with caterpillar regurgitant. Damage increased the emission of sesquiterpenes and aromatic compounds under ambient but not under augmented salinity. Cor- respondingly, exposure to VOCs from damaged emitters had effect on receiver EFN induction, but this effect was contingent on salinization. Receivers produced more EFN in response to damage after being exposed to VOCs from damaged emitters when the latter were grown under ambient salinity, but not when they were subjected to salinization. These results suggest complex effects of abiotic factors on VOC-mediated plant interactions.

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Laboratory and field trials reveal the potential of a gel formulation of entomopathogenic nematodes for the biological control of fall armyworm caterpillars (Spodoptera frugiperda)

2022-12-1, Fallet, Patrick, Bazagwira, Didace, Guenat, Julie Morgane, Bustos Segura, Carlos, Karangwa, Patrick, Mukundwa, Ishimwe Primitive, Kajuga, Joellee, Degen, Thomas, Toepfer, Stefan, Turlings, Ted

The fall armyworm (FAW), Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) can cause tremendous yield losses in maize. Its invasion into Africa and Asia has dramatically increased the use of insecticides in maize agro-ecosystems. Safe, effective and readily available alternatives are urgently needed. Entomopathogenic nematodes (EPN) represent a promising and sustainable option to control fall armyworm caterpillars on maize. Commonly used against soil insect pests, EPN can also be applied to control above-ground pests if formulated appropriately. We explored the possibility to control FAW by incorporating the EPN species Steinernema carpocapsae into protective formulations that can be easily applied into the whorl of maize plants, where the caterpillars mostly feed. We tested this approach in laboratory cage experiments as well as in field trials. In the laboratory, treating maize plants with a low dose of S. carpocapsae (3000 infective juveniles per plant) formulated in a carboxymethyl cellulose (CMC) gel caused 100% mortality of FAW caterpillars and substantially reduced plant damage, whereas EPN applied in water or a surfactant-polymer-formulation (SPF) caused 72% and 94% mortality, respectively. Under field conditions, one-time treatments with S. carpocapsae applied in water, SPF or CMC decreased plant damage, but only the EPN-gel formulation significantly reduced FAW infestation. As compared to control, about 40% fewer caterpillars were found on plants treated with EPN formulated in the gel. Notably, the EPN-gel formulation was as effective as a standard dose of cypermethrin, a pyrethroid insecticide commonly used against FAW, in reducing FAW infestation. Repeated applications may be needed to reduce re-infestations by FAW across a whole cropping season depending on the local maize phenology and pest dynamics. These findings demonstrate that EPN, when properly formulated, are excellent candidates for the biological control of FAW, and can be a safe and sustainable alternative to synthetic insecticides.

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Field evidence for the role of plant volatiles induced by caterpillar-derived elicitors in the prey location behavior of predatory social wasps

2024, Grof-Tisza, Patrick, Turlings, Ted, Bustos Segura, Carlos, Benrey, Betty

1. One assumed function of herbivore-induced plant volatiles (HIPVs) is to attract natural enemies of the inducing herbivores. Field evidence for this is scarce and often indirect. Also, the assumption that elicitors in insect oral secretions that trigger the volatile emissions are essential for attraction of natural enemies has not yet been demonstrated under field conditions. 2. After observing social wasps removing caterpillars from maize plants in an agricultural field, we hypothesized that these wasps use HIPVs to locate their prey. To test this, we conducted an experiment that simultaneously explored the importance of caterpillar oral secretions in the interaction. 3. We found that Spodoptera caterpillars placed on mechanically damaged plants treated with oral secretion were more likely to be attacked by wasps compared to caterpillars on plants that were only mechanically wounded. Both of the the latter treatments were considerably more attractive than plants that were only treated with oral secretion or left untreated. Subsequent analyses of headspace volatiles confirmed differences in emitted volatiles that likely account for the differential predation events across the treatments. 4. These findings highlight the importance of HIPVs in prey location by social wasps and provide evidence for the role that elicitors play in inducing attractive odor blends.

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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, Clancy, Mary, 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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Belowground and aboveground herbivory differentially affect the transcriptome in roots and shoots of maize

2022-7-22, Ye, Wenfeng, Bustos Segura, Carlos, Degen, Thomas, Erb, Matthias, Turlings, Ted

Plants recognize and respond to feeding by herbivorous insects by upregulating their local and systemic defenses. While defense induction by aboveground herbivores has been well studied, far less is known about local and systemic defense responses against attacks by belowground herbivores. Here, we investigated and compared the responses of the maize transcriptome to belowground and aboveground mechanical damage and infestation by two well-adapted herbivores: the soil-dwelling western corn rootworm Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) and the leaf- chewing fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). In responses to both herbivores, maize plants were found to alter local transcription of genes involved in phytohormone signaling, primary and secondary metabolism. Induction by real herbivore damage was considerably stronger and modified the expression of more genes than mechanical damage. Feeding by the corn rootworm had a strong impact on the shoot transcriptome, including the activation of genes involved in defense and development. By contrast, feeding by the fall armyworm induced only few transcriptional changes in the roots. In conclusion, feeding by a leaf chewer and a root feeder differentially affects the local and systemic defense of maize plants. Besides revealing clear differences in how maize plants respond to feeding by these specialized herbivores, this study reveals several novel genes that may play key roles in plant–insect interactions and thus sets the stage for in depth research into the mechanism that can be exploited for improved crop protection.

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Soil salinization effects on volatile signals that mediate the induction of chemical defenses in wild cotton

2024, Teresa Quijano-Medina, Yeyson Briones-May, Uriel Solís-Rodríguez, Mamin, Marine, Clancy, Mary, Ye, Wenfeng, Bustos Segura, Carlos, Turlings, Ted, Xoaquín Moreira, Luis Abdala-Roberts

Plants respond to complex blends of above- and below-ground volatile organic compounds (VOCs) emitted by neighboring plants. These responses often involve priming (i.e., preparation) or induction (i.e., increase) of defenses by “receiver” plants upon exposure to VOCs released by herbivore-damaged neighboring “emitters.” However, recent work has shown that induc- tion of VOC emissions by herbivory is modulated by abiotic factors, potentially affecting plant–plant signaling. We tested the effect of soil salinization on the induction of VOC emissions in wild cotton (Gossypium hirsutum) due to leaf damage and its consequences for the induction of defenses in neighboring plants. To this end, we performed a greenhouse factorial experiment where emitter plants were subjected to augmented soil salinity (vs. ambient salinity) and within each group emitter plants were subsequently exposed to simulated caterpillar damage (mechanical leaf damage treated with Spodoptera frugiperda oral secretion) or no damage (control). After 48 h of exposure, we collected VOCs released by emitter plants and then damaged the receivers and collected their leaves to measure levels of chemical defenses (terpenoid aldehydes of known insecticidal effects). We found an interaction between leaf damage and salinization for two groups of VOCs released by emitters (sesquiterpenes and other aromatic compounds), whereby damaged receivers had higher emissions than control plants under ambient but not salinized soil conditions. We also found that, upon being damaged, receiver plants exposed to damaged emitters exhibited a significantly higher concentration of heliocides (but not gossypol) than control plants. However, salinization did not alter this VOC exposure effect on receiver induced responses to damage. Overall, we show that exposure to induced VOC emissions from damaged plants magnifies the induction of chemical defenses due to leaf damage in neigh- boring individuals and that this is not contingent on the level of soil salinity despite the latter's effect on VOC induction.

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Aphid and caterpillar feeding drive similar patterns of induced defences and resistance to subsequent herbivory in wild cotton

2023, Teresa Quijano-Medina, Jonathan Interian-Aguiñaga, Uriel Solís-Rodríguez, Mamin, Marine, Clancy, Mary, Ye, Wenfeng, Bustos Segura, Carlos, Marta Francisco, José A. Ramos-Zapata, Turlings, Ted, Xoaquín Moreira, Luis Abdala-Roberts

Plant-induced responses to attack often mediate interactions between different species of insect herbivores. These effects are predicted to be contingent on the herbivore’s feeding guild, whereby prior feeding by insects should negatively impact subsequent feeding by insects of the same guild (induced resistance) but may positively influence insects of a differ- ent guild (induced susceptibility) due to interfering crosstalk between plant biochemical pathways specific to each feeding guild. We compared the effects of prior feeding by leaf-chewing caterpillars (Spodoptera frugiperda) vs. sap-sucking aphids (Aphis gossypii) on induced defences in wild cotton (Gossypium hirsutum) and the consequences of these attacks on subse- quently feeding caterpillars (S. frugiperda). To this end, we conducted a greenhouse experiment where cotton plants were either left undamaged or first exposed to caterpillar or aphid feeding, and we subsequently placed caterpillars on the plants to assess their performance. We also collected leaves to assess the induction of chemical defences in response to herbivory. We found that prior feeding by both aphids and caterpillars resulted in reductions in consumed leaf area, caterpillar mass gain, and caterpillar survival compared with control plants. Concomitantly, prior aphid and caterpillar herbivory caused similar increases in phenolic compounds (flavonoids and hydroxycinnamic acids) and defensive terpenoids (hemigossypolone) compared with control plants. Overall, these findings indicate that these insects confer a similar mode and level of induced resistance in wild cotton plants, calling for further work addressing the biochemical mechanisms underpinning these effects.

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Evolutionary changes in an invasive plant support the defensive role of plant volatiles

2021-10-29, Lin, Tiantian, Vrieling, Klaas, Laplanche, Diane, Klinkhamer, Peter G. L., Lou, Yonggen, Bekooy, Leon, Degen, Thomas, Bustos Segura, Carlos, Turlings, Ted, Desurmont, Gaylord A.

It is increasingly evident that plants interact with their outside world through the production of volatile organic compounds, but whether the volatiles have evolved to serve in plant defense is still a topic of considerable debate.Unharmed leaves constitutively release small amounts of volatiles, but when the leaves are damaged by herbivorous arthropods, they emit substantially more volatiles. These herbivore-induced plant volatiles (HIPVs) attract parasitoids and predators that kill insect herbivores, and this can benefit the plants.As yet, however, there is no tangible evolutionary evidence that this tritrophic interplay contrib- utes to the selection forces that have shaped the volatile emissions of plants.With this in mind, we investigated the evolutionary changes in volatile emissions in invasive common ragwort and the respective defensive roles of its constitutive and inducible volatiles. This Eurasian plant has invaded other continents, where it evolved for many generations in the absence of specialized herbivores and their natural enemies. We found that, compared to native ragworts, invasive plants release higher levels of constitutive volatiles but considerably lower levels of herbivore-induced volatiles. As a consequence, invasive ragwort is more attractive to a specialist moth but avoided by an unadapted generalist moth. Importantly, conforming to the indirect defense hypothesis, a specialist parasitoid was much more attracted to caterpillar-damaged native ragwort, which was reflected in higher parasitism rates in a field trial. The evolution of foliar volatile emissions appears to be indeed driven by their direct and indirect roles in defenses against insects.