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The green peach aphid ( Myzus persicae ) is a generalist pest damaging crops and transmitting viral pathogens. Using Illumina sequencing of small (s)RNAs and poly(A)-enriched long RNAs, we analyzed aphid virome components, viral gene expression and antiviral RNA interference (RNAi) responses. Myzus persicae densovirus (family Parvoviridae ), a single-stranded (ss)DNA virus persisting in the aphid population, produced 22 nucleotide sRNAs from both strands of the entire genome, including 5'- and 3'-inverted terminal repeats. These sRNAs likely represent Dicer-dependent small interfering (si)RNAs, whose double-stranded RNA precursors are produced by readthrough transcription beyond poly(A) signals of the converging leftward and rightward transcription units, mapped here with Illumina reads. Additionally, the densovirus produced 26-28 nucleotide sRNAs, comprising those enriched in 5'-terminal uridine and mostly derived from readthrough transcripts and those enriched in adenosine at position 10 from their 5'-end and mostly derived from viral mRNAs. These sRNAs likely represent PIWI-interacting RNAs generated by a ping-pong mechanism. A novel ssRNA virus, reconstructed from sRNAs and classified into the family Flaviviridae , co-persisted with the densovirus and produced 22 nucleotide siRNAs from the entire genome. Aphids fed on plants versus artificial diets exhibited distinct RNAi responses affecting densovirus transcription and flavivirus subgenomic RNA production. In aphids vectoring turnip yellows virus (family Solemoviridae ), a complete virus genome was reconstituted from 21, 22 and 24 nucleotide viral siRNAs likely acquired with plant phloem sap. Collectively, deep-sequencing analysis allowed for the identification and de novo reconstruction of M. persicae virome components and uncovered RNAi mechanisms regulating viral gene expression and replication.

Many plant viruses modify the phenotype of their hosts, which may influence the behaviour of their vectors and facilitate transmission. Among them is the turnip yellows virus (TuYV), which can modify the orientation, feeding, and performance of its main aphid vector, Myzus persicae. However, the virus factors driving these mechanisms have not been elucidated. In this study, we compared the feeding behaviour and fecundity of aphids on TuYV-infected and transgenic Arabidopsis thaliana expressing individual TuYV proteins (CP, RT and P0) to define the role of these proteins in aphid-plant interactions. Aphids on TuYV-infected plants had shorter pathway phases and ingested phloem sap for longer times, which is expected to promote the acquisition of the phloem-limited TuYV. No change in aphid fecundity was observed on TuYV-infected plants. The transmission-conducive feeding behaviour changes could be fully reproduced by phloem-specific expression of the capsid protein (CP) in transgenic plants, whereas expression of P0 had minor and RT had no effects on aphid feeding behaviour. We then carried out a metabolomic analysis to determine plant compounds that could be involved in the modification of the aphid behaviour. A few metabolites were specific for TuYV-infected or CP-transgenic A. thaliana, and are good candidates for inducing behavioural changes., (© 2024 The Author(s). Plant, Cell & Environment published by John Wiley & Sons Ltd.)

Multi-infection of plants by viruses is very common and can change drastically infection parameters such as virus accumulation, distribution, and vector transmission. Sugar beet is an important crop that is frequently co-infected by the polerovirus beet chlorosis virus (BChV) and the closterovirus beet yellows virus (BYV), both vectored by the green peach aphid ( Myzus persicae ). These phloem-limited viruses are acquired while aphids ingest phloem sap from infected plants. Here we found that co-infection decreased transmission of BChV by ~50% but had no impact on BYV transmission. The drastic reduction of BChV transmission was due to neither lower accumulation of BChV in co-infected plants nor reduced phloem sap ingestion by aphids from these plants. Using the signal amplification by exchange reaction fluorescent in situ hybridization technique on plants, we observed that 40% of the infected phloem cells were co-infected and that co-infection caused redistribution of BYV in these cells. The BYV accumulation pattern changed from distinct intracellular spherical inclusions in mono-infected cells to a diffuse form in co-infected cells. There, BYV co-localized with BChV throughout the cytoplasm, indicative of virus-virus interactions. We propose that BYV-BChV interactions could restrict BChV access to the sieve tubes and reduce its accessibility for aphids and present a model of how co-infection could alter BChV intracellular movement and/or phloem loading and reduce BChV transmission.IMPORTANCEMixed viral infections in plants are understudied yet can have significant influences on disease dynamics and virus transmission. We investigated how co-infection with two unrelated viruses, BChV and BYV, affects aphid transmission of the viruses in sugar beet plants. We show that co-infection reduced BChV transmission by about 50% without affecting BYV transmission, despite similar virus accumulation rates in co-infected and mono-infected plants. Follow-up experiments examined the localization and intracellular distribution of the viruses, leading to the discovery that co-infection caused a redistribution of BYV in the phloem vessels and altered its repartition pattern within plant cells, suggesting virus-virus interactions. In conclusion, the interplay between BChV and BYV affects the transmission of BChV but not BYV, possibly through direct or indirect virus-virus interactions at the cellular level. Understanding these interactions could be crucial for managing virus propagation in crops and preventing yield losses., Competing Interests: The authors declare no conflict of interest.

There is growing evidence that plant viruses manipulate their hosts and vectors in ways that increase transmission. However, to date only few viral components underlying these phenomena have been identified. Here we show that cauliflower mosaic virus (CaMV) protein P2 modifies the feeding behavior of its aphid vector. P2 is necessary for CaMV transmission because it mediates binding of virus particles to the aphid mouthparts. We compared aphid feeding behavior on plants infected with the wild-type CaMV strain Cabb B-JI or with a deletion mutant strain, Cabb B-JIΔP2, which does not produce P2. Only aphids probing Cabb B-JI infected plants doubled the number of test punctures during the first contact with the plant, indicating a role of P2. Membrane feeding assays with purified P2 and virus particles confirmed that these viral products alone are sufficient to cause the changes in aphid probing. The behavior modifications were not observed on plants infected with a CaMV mutant expressing P2Rev5, unable to bind to the mouthparts. These results are in favor of a virus manipulation, where attachment of P2 to a specific region in the aphid stylets-the acrostyle-exercises a direct effect on vector behavior at a crucial moment, the first vector contact with the infected plant, which is essential for virus acquisition., Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2023 Verdier et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

Evidence is accumulating that plant viruses alter host plant traits in ways that modify their insect vectors' behavior. These alterations often enhance virus transmission, which has led to the hypothesis that these effects are manipulations caused by viral adaptation. However, we lack a mechanistic understanding of the genetic basis of these indirect, plant-mediated effects on vectors, their dependence on the plant host, and their relation to the mode of virus transmission. Transcriptome profiling of Arabidopsis thaliana and Camelina sativa plants infected with turnip yellows virus (TuYV) or cauliflower mosaic virus (CaMV) and infested with the common aphid vector Myzus persicae revealed strong virus- and host-specific differences in gene expression patterns. CaMV infection caused more severe effects on the phenotype of both plant hosts than did TuYV infection, and the severity of symptoms correlated strongly with the proportion of differentially expressed genes, especially photosynthesis genes. Accordingly, CaMV infection modified aphid behavior and fecundity more strongly than did infection with TuYV. Overall, infection with CaMV, relying on the noncirculative transmission mode, tends to have effects on metabolic pathways, with strong potential implications for insect vector-plant host interactions (e.g., photosynthesis, jasmonic acid, ethylene, and glucosinolate biosynthetic processes), while TuYV, using the circulative transmission mode, alters these pathways only weakly. These virus-induced deregulations of genes that are related to plant physiology and defense responses might impact both aphid probing and feeding behavior on infected host plants, with potentially distinct effects on virus transmission. IMPORTANCE Plant viruses change the phenotype of their plant hosts. Some of the changes impact interactions of the plant with insects that feed on the plants and transmit these viruses. These modifications may result in better virus transmission. We examine here the transcriptomes of two plant species infected with two viruses with different transmission modes to work out whether there are plant species-specific and transmission mode-specific transcriptome changes. Our results show that both are the case.

Background: Poleroviruses, such as turnip yellows virus (TuYV), are plant viruses strictly transmitted by aphids in a persistent and circulative manner. Acquisition of either virus particles or plant material altered by virus infection is expected to induce gene expression deregulation in aphids which may ultimately alter their behavior., Results: By conducting an RNA-Seq analysis on viruliferous aphids fed either on TuYV-infected plants or on an artificial medium containing purified virus particles, we identified several hundreds of genes deregulated in Myzus persicae, despite non-replication of the virus in the vector. Only a few genes linked to receptor activities and/or vesicular transport were common between the two modes of acquisition with, however, a low level of deregulation. Behavioral studies on aphids after virus acquisition showed that M. persicae locomotion behavior was affected by feeding on TuYV-infected plants, but not by feeding on the artificial medium containing the purified virus particles. Consistent with this, genes potentially involved in aphid behavior were deregulated in aphids fed on infected plants, but not on the artificial medium., Conclusions: These data show that TuYV particles acquisition alone is associated with a moderate deregulation of a few genes, while higher gene deregulation is associated with aphid ingestion of phloem from TuYV-infected plants. Our data are also in favor of a major role of infected plant components on aphid behavior., (© 2022. The Author(s).)

Emerging evidence suggests that viral infection modifies host plant traits that in turn alter behaviour and performance of vectors colonizing the plants in a way conducive for transmission of both nonpersistent and persistent viruses. Similar evidence for semipersistent viruses like cauliflower mosaic virus (CaMV) is scarce. Here we compared the effects of Arabidopsis infection with mild (CM) and severe (JI) CaMV isolates on the feeding behaviour (recorded by the electrical penetration graph technique) and fecundity of the aphid vector Myzus persicae. Compared to mock-inoculated plants, feeding behaviour was altered similarly on CM- and JI-infected plants, but only aphids on JI-infected plants had reduced fecundity. To evaluate the role of the multifunctional CaMV protein P6-TAV, aphid feeding behaviour and fecundity were tested on transgenic Arabidopsis plants expressing wild-type (wt) and mutant versions of P6-TAV. In contrast to viral infection, aphid fecundity was unchanged on all transgenic lines, suggesting that other viral factors compromise fecundity. Aphid feeding behaviour was modified on wt P6-CM-, but not on wt P6-JI-expressing plants. Analysis of plants expressing P6 mutants identified N-terminal P6 domains contributing to modification of feeding behaviour. Taken together, we show that CaMV infection can modify both aphid fecundity and feeding behaviour and that P6 is only involved in the latter., (© 2021 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd.)

A growing number of studies suggest that plant viruses manipulate host plant phenotypes to increase transmission-conducive behaviors by vectors. Studies on this phenomenon frequently omit examination of interactions that occur after vectors acquire virions, which provides an incomplete understanding of the ecology of plant virus manipulation. Here, by taking a full factorial approach that considered both the infection status of the host (Montia perfoliata) and viruliferous status of the aphid (Myzus persicae), we explored the effects of a circulative, non-propagative virus (Turnip yellows virus [TuYV]) on a suite of behavior and performance metrics that are relevant for virus transmission. Our results demonstrate that viruliferous aphids exhibited an increased velocity of movement and increased activity levels in locomotor and dispersal-retention assays. They also had increased fecundity and showed a capacity to more efficiently exploit resources by taking less time to reach the phloem and ingesting more sap, regardless of plant infection status. In contrast, non-viruliferous aphids only exhibited enhanced fecundity and biomass on TuYV-infected hosts, and had overall reduced dispersal and locomotor activity relative to viruliferous aphids. In this pathosystem, post-acquisition effects were stronger and more conducive to virus transmission than the purely pre-acquisition effects mediated by virus effects on the host plant. Our study provides additional support for the hypothesis that virus manipulation of vector behavior includes both pre- and post-acquisition effects and demonstrates the importance of considering both components when studying putative virus manipulation strategies.

Plant viruses face many challenges in agricultural environments. Although crop fields appear to be abundant resources for these pathogens, it may be difficult for viruses to "escape" from crop environments prior to host senescence or harvesting. One way for viruses to increase the odds of persisting outside of agricultural fields across seasons is by evolving traits that increase transmission opportunities between crops and wild plant communities. There is accumulating evidence that some viruses can achieve this by manipulating crop plant phenotypes in ways that enhance transmission by vectors. Putative manipulations occur through alteration of plant cues (color, size, texture, foliar volatiles, in-leaf metabolites, defenses, and leaf cuticles) that mediate vector orientation, feeding, and dispersal behaviors. Virus effects on host phenotypes are not uniform but appear to exhibit convergence depending on virus traits underlying transmission, particularly the duration of probing and feeding required to acquire and inoculate distinct types of plant viruses. This shared congruence in manipulation strategies and mechanisms across divergent virus lineages suggests that such effects may be adaptive. To discern if this is the case, researchers must consider molecular and environmental constraints on virus evolution, including those imposed by insect vectors from organismal to landscape scales. In this review, we synthesize applied research on vector-borne virus transmission in laboratory and field settings to identify the main factors determining transmission opportunities for plant viruses, and thus, selection pressure to evolve manipulative traits. We then examine these outputs in the context of studies reporting putative instances of plant virus manipulation. Our synthesis reveals important disconnects between virus manipulation studies and actual selection pressures imposed by vectors in real-world contexts., (Copyright © 2020 Elsevier B.V. All rights reserved.)

Cowpea, Vigna unguiculata , is a crop that is essential to semiarid areas of the world like Sub-Sahara Africa. Cowpea is highly susceptible to cowpea aphid, Aphis craccivora , infestation that can lead to major yield losses. Aphids feed on their host plant by inserting their hypodermal needlelike flexible stylets into the plant to reach the phloem sap. During feeding, aphids secrete saliva, containing effector proteins, into the plant to disrupt plant immune responses and alter the physiology of the plant to their own advantage. Liquid chromatography tandem mass spectrometry (LC-MS/MS) was used to identify the salivary proteome of the cowpea aphid. About 150 candidate proteins were identified including diacetyl/L-xylulose reductase (DCXR), a novel enzyme previously unidentified in aphid saliva. DCXR is a member of short-chain dehydrogenases/reductases with dual enzymatic functions in carbohydrate and dicarbonyl metabolism. To assess whether cowpea aphid DCXR (AcDCXR) has similar functions, recombinant AcDCXR was purified and assayed enzymatically. For carbohydrate metabolism, the oxidation of xylitol to xylulose was tested. The dicarbonyl reaction involved the reduction of methylglyoxal, an α-β-dicarbonyl ketoaldehyde, known as an abiotic and biotic stress response molecule causing cytotoxicity at high concentrations. To assess whether cowpea aphids induce methylglyoxal in plants, we measured methylglyoxal levels in both cowpea and pea ( Pisum sativum ) plants and found them elevated transiently after aphid infestation. Agrobacterium-mediated transient overexpression of AcDCXR in pea resulted in an increase of cowpea aphid fecundity. Taken together, our results indicate that AcDCXR is an effector with a putative ability to generate additional sources of energy to the aphid and to alter plant defense responses. In addition, this work identified methylglyoxal as a potential novel aphid defense metabolite adding to the known repertoire of plant defenses against aphid pests., (Copyright © 2020 MacWilliams, Dingwall, Chesnais, Sugio and Kaloshian.)

During the process of virus acquisition by aphids, plants respond to both the virus and the aphids by mobilizing different metabolic pathways. It is conceivable that the plant metabolic responses to both aggressors may be conducive to virus acquisition. To address this question, we analyze the accumulation of the phloem-limited polerovirus Turnip yellows virus (TuYV), which is strictly transmitted by aphids, and aphid's life traits in six Arabidopsis thaliana mutants ( xth33 , ss3-2 , nata1 , myc234 , quad , atr1D, and pad4-1 ). We observed that mutations affecting the carbohydrate metabolism, the synthesis of a non-protein amino acid and the glucosinolate pathway had an effect on TuYV accumulation. However, the virus titer did not correlate with the virus transmission efficiency. Some mutations in A. thaliana affect the aphid feeding behavior but often only in infected plants. The duration of the phloem sap ingestion phase, together with the time preceding the first sap ingestion, affect the virus transmission rate more than the virus titer did. Our results also show that the aphids reared on infected mutant plants had a reduced biomass regardless of the mutation and the duration of the sap ingestion phase., Competing Interests: The authors declare no conflicts of interest. The funders had no role in the design of the study, in the analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Plant virus infection fundamentally alters chemical and behavioral phenotypes of hosts and vectors. These alterations often enhance virus transmission, leading researchers to surmise that such effects are manipulations caused by virus adaptations and not just by-products of pathology. But identification of the virus components behind manipulation is missing from most studies performed to date. Here, we evaluate causative empirical evidence that virus components are the drivers of manipulated host and vector phenotypes. To do so, we link findings and methodologies on virus pathology with observational and functional genomics studies on virus manipulation. Our synthesis provides an overview of progress, areas of synergy, and new approaches that will lead to an improved mechanistic understanding of host and vector manipulation by plant viruses., (Copyright © 2019 Elsevier Inc. All rights reserved.)

Background: Potato (Solanum tuberosum) is the fourth culture in the world and is widely used in the agri-food industries. They generate by-products in which α-chaconine and α-solanine, the two major solanidine-based glycoalkaloids of potato, are present. As secondary metabolites, they play an important role in the protection system of potato and are involved in plant protection against insects. To add value to these by-products, we described here new glycoalkaloids that could have phytosanitary properties., Results: Solanidine, as a renewable source, was modified with an azido linker and coupled by copper-catalyzed alkyne azide cycloaddition to alkynyl derivatives of the monosaccharides found in the natural potato glycoalkakoids: D-glucose, D-galactose and L-rhamnose. The efficacy of our compounds was evaluated on the potato aphid Macrosiphum euphorbiae. The synthetic compounds have stronger aphicidal properties against nymphs than unmodified solanidine. They also showed strong aphicidal activities on adults and a negative impact on fecundity., Conclusion: Our synthetic neoglycoalkaloids affected Macrosiphum euphorbiae survival at the nymphal stage as well as at the adult stage. Furthermore, they induced a decrease in fecundity. Our results show that chemical modifications of by-products may afford new sustainable compounds for crop and plant protection. © 2018 Society of Chemical Industry., (© 2018 Society of Chemical Industry.)

Insect-vectored plant viruses can induce changes in plant phenotypes, thus influencing plant-vector interactions in a way that may promote their dispersal according to their mode of transmission (i.e., circulative vs. noncirculative). This indirect vector manipulation requires host-virus-vector coevolution and would thus be effective solely in very specific plant-virus-vector species associations. Some studies suggest this manipulation may depend on multiple factors relative to various intrinsic characteristics of vectors such as transmission efficiency. In anintegrative study, we tested the effects of infection of the Brassicaceae Camelina sativa with the noncirculative Cauliflower mosaic virus (CaMV) or the circulative Turnip yellows virus (TuYV) on the host-plant colonization of two aphid species differing in their virus transmission efficiency: the polyphagous Myzus persicae, efficient vector of both viruses, and the Brassicaceae specialist Brevicoryne brassicae, poor vector of TuYV and efficient vector of CaMV. Results confirmed the important role of virus mode of transmission as plant-mediated effects of CaMV on the two aphid species induced negative alterations of feeding behavior (i.e., decreased phloem sap ingestion) and performance that were both conducive for virus fitness by promoting dispersion after a rapid acquisition. In addition, virus transmission efficiency may also play a role in vector manipulation by viruses as only the responses of the efficient vector to plant-mediated effects of TuYV, that is, enhanced feeding behavior and performances, were favorable to their acquisition and further dispersal. Altogether, this work demonstrated that vector transmission efficiency also has to be considered when studying the mechanisms underlying vector manipulation by viruses. Our results also reinforce the idea that vector manipulation requires coevolution between plant, virus and vector., (© 2017 Institute of Zoology, Chinese Academy of Sciences.)

We demonstrated previously that expression of Macrosiphum euphorbiae salivary protein Me10 enhanced aphid reproduction on its host tomato (Solanum lycopersicum). However, the mechanism of action of Me10 remained elusive. To confirm the secretion of Me10 by the aphid into plant tissues, we produced Me10 polyclonal antibodies. To identify the plant targets of Me10, we developed a tomato immune induced complementary DNA yeast two-hybrid library and screened it with Me10 as bait. Immunoprecipitation and bimolecular fluorescence complementation (BiFC) assays were performed to validate one of the interactions in planta, and virus-induced gene silencing was used for functional characterization in tomato. We demonstrated that Me10 is secreted into the plant tissues and interacts with tomato 14-3-3 isoform 7 (TFT7) in yeast. Immunoprecipitation assays confirmed that Me10 and its homologue in Aphis gossypii, Ag10k, interact with TFT7 in planta. Further, BiFC revealed that Me10 interaction with TFT7 occurs in the plant cell cytoplasm. While silencing of TFT7 in tomato leaves did not affect tomato susceptibility to M. euphorbiae, it enhanced longevity and fecundity of A. gossypii, the non-host aphid. Our results suggest the model whereby TFT7 plays a role in aphid resistance in tomato and effectors of the Me10/Ag10k family interfere with TFT7 function during aphid infestation., (© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust.)

Aphids are important pests which cause direct damage by feeding or indirect prejudice by transmitting plant viruses. Viruses are known to induce modifications of plant cues in ways that can alter vector behavior and virus transmission. In this work, we addressed whether the modifications induced by the aphid-transmitted Turnip yellows virus (TuYV) in the model plant Arabidopsis thaliana also apply to the cultivated plant Camelina sativa , both belonging to the Brassicaceae family. In most experiments, we observed a significant increase in the relative emission of volatiles from TuYV-infected plants. Moreover, due to plant size, the global amounts of volatiles emitted by C. sativa were higher than those released by A. thaliana . In addition, the volatiles released by TuYV-infected C. sativa attracted the TuYV vector Myzus persicae more efficiently than those emitted by non-infected plants. In contrast, no such preference was observed for A. thaliana . We propose that high amounts of volatiles rather than specific metabolites are responsible for aphid attraction to infected C. sativa . This study points out that the data obtained from the model pathosystem A. thaliana /TuYV cannot be straightforwardly extrapolated to a related plant species infected with the same virus.

Plant viruses possess adaptations for facilitating acquisition, retention, and inoculation by vectors. Until recently, it was hypothesized that these adaptations are limited to virus proteins that enable virions to bind to vector mouthparts or invade their internal tissues. However, increasing evidence suggests that viruses can also manipulate host plant phenotypes and vector behaviors in ways that enhance their own transmission. Manipulation of vector-host interactions occurs through virus effects on host cues that mediate vector orientation, feeding, and dispersal behaviors, and thereby, the probability of virus transmission. Effects on host phenotypes vary by pathosystem but show a remarkable degree of convergence among unrelated viruses whose transmission is favored by the same vector behaviors. Convergence based on transmission mechanism, rather than phylogeny, supports the hypothesis that virus effects are adaptive and not just by-products of infection. Based on this, it has been proposed that viruses manipulate hosts through multifunctional proteins that facilitate exploitation of host resources and elicitation of specific changes in host phenotypes. But this proposition is rarely discussed in the context of the numerous constraints on virus evolution imposed by molecular and environmental factors, which figure prominently in research on virus-host interactions not dealing with host manipulation. To explore the implications of this oversight, we synthesized available literature to identify patterns in virus effects among pathogens with shared transmission mechanisms and discussed the results of this synthesis in the context of molecular and environmental constraints on virus evolution, limitations of existing studies, and prospects for future research., (© 2018 Elsevier Inc. All rights reserved.)

Background: The use of nitrogen fertiliser in agrosystems can alter plant nitrogen and consequently improve nutrient availability for herbivores, potentially leading to better performance for herbivores and higher pest pressure in the field. We compared, in laboratory conditions, the effects of nitrogen fertilisation on a promising biomass crop, Miscanthus × giganteus, and its parents M. sinensis and M. sacchariflorus. The plant-mediated effects were compared on the second trophic level, the green corn leaf aphid Rhopalosiphum maidis., Results: Results showed that the biomass and leaf C:N ratio of M. sinensis plants treated with nitrogen fertiliser were significantly greater than those of non-treated plants. As regards M. × giganteus and M. sacchariflorus, the only reported change was a significantly smaller leaf C:N ratio for treated M. sacchariflorus compared with non-treated plants. Surprisingly, nitrogen fertilisation had opposite effects on plant-herbivore interactions. Following nitrogen treatments, M. sinensis was less suitable in terms of intrinsic rate of increase for R. maidis, the feeding behaviour of which was negatively affected, while M. sacchariflorus and M. × giganteus exhibited greater suitability in terms of aphid weight., Conclusion: Nitrogen fertilisation had contrasting effects on the three species of Miscanthus plants. These effects cascaded up to the second trophic level, R. maidis aphid pests, either through a modification of their weight or demographic parameters. The implications of these results were discussed in the context of agricultural sustainability and intensive production practices. © 2016 Society of Chemical Industry., (© 2016 Society of Chemical Industry.)

Because N is frequently the most limiting mineral macronutrient for plants in terrestrial ecosystems, modulating N input may have ecological consequences through trophic levels. Thus, in agro-ecosystems, the success of natural enemies may depend not only from their herbivorous hosts but also from the host plant whose qualities may be modulated by N input. We manipulated foliar N concentrations by providing to Camelina sativa plants three different nitrogen rates (control, optimal, and excessive). We examined how the altered host-plant nutritional quality influenced the performances of two aphid species, the generalist green peach aphid, Myzus persicae, and the specialist cabbage aphid, Brevicoryne brassicae , and their common parasitoid Diaeretiella rapae . Both N inputs led to increased N concentrations in the plants but induced contrasted concentrations within aphid bodies depending on the species. Compared to the control, plant biomass increased when receiving the optimal N treatment but decreased under the excessive treatment. Performances of M. persicae improved under the optimal treatment compared to the control and excessive treatments whereas B. brassicae parameters declined following the excessive N treatment. In no-choice trials, emergence rates of D. rapae developing in M. persicae were higher on both optimum and excessive N treatments, whereas they remained stable whatever the treatment when developing in B. brassicae . Size of emerging D. rapae females was positively affected by the treatment only when it developed in M. persicae on the excessive N treatment. This work showed that contrary to an optimal N treatment, when N was delivered in excess, plant suitability was reduced and consequently affected negatively aphid parameters. Surprisingly, these negative effects resulted in no or positive consequences on parasitoid parameters, suggesting a buffered effect at the third trophic level. Host N content, host suitability, and dietary specialization appear to be major factors explaining the functioning of our studied system.

Parasitoid host selection behaviour has been extensively studied in experimentally simplified tritrophic systems formed by one single food chain (one plant, one herbivore and one parasitoid species). The "Mother knows best" hypothesis predicts that the preference for a plant-host complex should be positively correlated with plant quality for offspring performance. We studied the host selection behaviour of the generalist endoparasitoid Aphidius matricariae towards the black bean aphid Aphis fabae in the intercrop system including Vicia faba as a focal plant and its companion plant Camelina sativa. Dual-choice laboratory bioassays revealed that parasitoid females preferred to orientate towards (1) the plant-aphid complex over the non-infested plant whatever the complex (2) the C. sativa-A. fabae complex over the V. faba-A. fabae complex. In dual choice attack rate bioassays, parasitoid females showed more interest towards the aphids on C. sativa but paradoxically chose to oviposit more in aphids on V. faba. Ultimately, parasitoids that had developed on the V. faba-A. fabae complex exhibited better fitness parameters. By demonstrating that parasitoid females were able to discriminate the aphid host that offered the highest fitness to their offspring but selected beforehand the least suitable plant-aphid complex, we provide key insight into the disruption in their host selection behaviour potentially triggered by diverse habitats. This suggests that the "Mother knows best" hypothesis could be thwarted by increasing the complexity of the studied systems.