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Initial egg load (i.e. number of eggs counted in both ovaries) of twenty-five newly emerged Aphidius colemani females developing in Myzus persicae reared on control or infected plants at 20 ± 1 °C, 60 ± 5% relative humidity (RH), and 16L:8D photoperiod. Asterisks indicate significant differences between treatments (p < 0.001). Mean ± SE
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Plant viruses strongly influence the physiology of their host plants and phytophagous insect vectors, thereby affecting ecological interactions between them. Despite the important role of natural enemies on insect vector control and thus on virus dissemination, the influence of plant viruses on the third trophic level received little attention. We...
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BACKGROUND
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BACKGROUND
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Citations
... The binding of the Ras-related protein Rab-1A (RAB1) of L. striatellus to the nucleocapsid protein (NP) of RSV can lead to its transmission [18]. Discovering the receptors in vectors can help us understand the transmission mechanisms of plant viruses and provide an effective strategy for controlling the spread of the virus by intervening with these receptors [19][20][21][22]. Therefore, the study of identified and functionally validated receptors in vectors is particularly important. ...
Many plant viruses are transmitted by insect vectors, and the transmission process is regulated by key genes within the vector. However, few of these genes have been reported. Previous studies in our laboratory have shown that the expression of the signal transducer and activator of transcription 5B (STAT5B) in viruliferous vector aphids carrying barley yellow dwarf virus (BYDV) was upregulated, and the complement component 1 Q subcomponent binding protein (C1QBP) within the aphid interacted with the coat protein (CP) and aphid transmission protein (ATP) of BYDV. In this study, we examined the expression levels of STAT5B and C1QBP in the vector aphid Sitobion avenae (Fabricius) (Hemiptera: Aphididae) using the qPCR method. We conducted this analysis during the acquisition accession periods (AAPs) and inoculation accession periods (IAPs) of the BYDV species GAV (BYDV-GAV). Furthermore, the effects of STAT5B and C1QBP on the acquisition, retention, and transmission of BYDV-GAV in S. avenae were verified using the RNA interference (RNAi) method. The results show the following: (1) the expression levels of STAT5B and C1QBP were significantly upregulated during the AAPs and IAPs of BYDV-GAV; (2) the silencing of STAT5B led to a significant increase in BYDV-GAV retention during IAPs; and (3) the silencing of C1QBP resulted in a notable decrease in BYDV-GAV acquisition during the AAPs, as well as a significant increase in BYDV-GAV retention during the IAPs. These results suggest that STAT5B and C1QBP in S. avenae play a role in BYDV-GAV transmission. These findings highlight the functions of the STAT5B and C1QBP genes and identify C1QBP as a potential target gene for further RNAi-based studies to control the transmission of BYDV-GAV.
... 56 Due to plant virus-specific factors, several previous studies indicated that plant viruses have indirect positive, neutral, or negative effects on vector susceptibility to parasitoids mediated through changes in the host plant's physiological and biochemical characteristics. [57][58][59][60][61][62] Our results indicate that parasitism, mummification and emergence of A. gifuensis decreased significantly in viruliferous aphids compared with non-viruliferous aphids. These results suggest that BYDV-PAV can directly and positively affect the resistance of S. avenae to this parasitoid. ...
BACKGROUND
The complex interaction between plant viruses and their insect vectors is the basis for the epidemiology of plant viruses. The ‘Vector Manipulation Hypothesis’ (VMH) was proposed to demonstrate the evolution of strategies in plant viruses to enhance their transmission to new hosts through direct effects on insect vector behavior and/or physiology. However, the aphid vectors used in previous studies were mostly obtained by feeding on virus‐infected plants and as a result, it was difficult to eliminate the confounding effects of infected host plants. Furthermore, the mechanisms of the direct effects of plant viruses on insect vectors have rarely been examined comprehensively.
RESULTS
We fed Sitobion avenae on an artificial diet infused with a purified suspension of Barley yellow dwarf virus (BYDV) PAV strain to obtain viruliferous aphids. We then examined their growth and reproduction performance, resistance to the parasitoid Aphidius gifuensis Ashmead, and feeding behavior. The results indicate that (1) viruliferous aphids had a shorter life span and a lower relative growth rate at the nymphal stage; (2) A. gifuensis had a lower parasitism rate, mummification rate, and emergence rate in viruliferous aphids; (3) Viruliferous aphids spent more time on non‐probing and salivation behavior and had a shorter total duration of penetration and ingestion compared with healthy conspecifics.
CONCLUSION
These results suggest that plant virus infection may directly alter vector fitness and behavior that improves plant virus transmission, but not vector growth. These findings highlight the mechanisms of VMH and the ecological significance of vector manipulation by plant viruses, and have implications for plant virus disease and vector management. © 2024 Society of Chemical Industry.
... Similarly, in the presence of the persistently transmitted turnip yellows virus (TuYV, Polerovirus) infecting bastard saffron plants, A. colemani exhibited a similar response to infected and uninfected plants. However, parasitoids emerged smaller when developing from viruliferous aphids compared to those from non-viruliferous aphids [25]. ...
Natural enemies are an additional component that may interact directly with the plant–virus–vector association, affecting viral dispersion. In our study, we conducted olfactometry assays to explore how single and mixed infections with CMV or/and CABYV modify the attractiveness of A. colemani to aphid-free and aphid-infested melon plants using two melon genotypes. Subsequently, we investigated the influence of CABYV-infected plants infested by A. gossypii on the parasitism rate and emergence of A. colemani in a dual-choice assay under greenhouse conditions. Our study demonstrates that males showed no preference for either infected or non-infected plants. Female parasitoids exhibit a preference for volatiles emitted by CMV and mixed-infected melon plants over clean air but not over mock-inoculated plants, suggesting a response influenced by plant genotype. Female parasitoid responses to CABYV and its interactions with aphids revealed a preference for mock-inoculated plants over CABYV-infected plants and a parasitism rate slightly higher (7.12%) on non-infected plants. Our study revealed that (1) parasitoids may reject olfactory cues from CABYV-infected plants, potentially interfering with the plant’s “cry for help” response; (2) in the case of CMV, whether in single or mixed infections, non-infected plants are as attractive as infected ones to parasitoids. Our findings suggest that persistent viruses manipulate aphid parasitoid be-havior to their advantage, promoting virus disease in melon crops.
... Therefore, the effect of these strategies on virus dynamics is not easy to predict . It is even more complicated because virus infection might affect higher trophic levels through vector and natural enemy fitness and behaviour (Moiroux et al. 2018). ...
Plant viruses transmitted by vector pests are one of the most important worldwide threats to global food production and security. Biological control strategies to enhance natural enemies (parasitoids and predators) have mainly focused on their ability to reduce pest density. In contrast, few studies have examined how natural enemies affect the spread and the incidence of viruses in a crop, although those results could be used as levers for a more sustainable management of viral diseases. Vector-borne plant viruses can be classified in three categories based on their transmission mode: non-persistently transmitted viruses, semi-persistently transmitted viruses and persistently transmitted viruses, whereas vector density, fitness and movement were identified as main drivers of virus spread in a crop, their relative contributions to virus epidemiology may also depend on both the transmission mode and the presence of natural enemies. The first part of the review focuses on virus transmission dynamics in relation to vector activity and density. Because we identify different patterns for each type of plant viruses, control strategies that lead to changes in vector traits, should be adapted to the targeted virus. However, biological control of insect vectors has been rarely adapted to the mode of transmission of the target virus. Thus, the last part of the review explores the conditions required for natural enemies (parasitoids and predators) to prevent epidemics outbreaks of each type of plant viruses. Briefly, if combined with other practices, biological control of vectors to keep virus incidence below the economic threshold is a promising approach for persistently transmitted viruses but might be more difficult to achieve with non-persistently transmitted viruses and semi-persistently transmitted viruses.
... ( (Table 3). (Joffrey et al., 2018). ...
... These results are in agreement with the study which showed that virus infection affects plant suitability for aphids through modulating plant physiology and chemistry (Joffrey et al., 2018). ...
Luteoviruses are plant‐infecting RNA viruses that are transmitted by aphids in a persistent circulative mode. Luteoviruses have been shown to positively influence their aphid vectors fitness. To find out the physiological responses of aphid vectors to luteoviruses, fatty acid (FA) composition and energy components (EC) of aphid vectors including pea aphid (Acyrthosiphon pisum Harris), black bean aphid (Aphis fabae Scopoli) and bird cherry‐oat aphid (Rhopalosiphum padi L.) were evaluated in response to Pea enation mosaic virus 1 (PEMV1), Bean leafroll virus (BLRV) and Barley yellow dwarf virus‐PAV (BYDV‐PAV), respectively. Our results showed that the number and the proportion of FA of total lipid are altered in aphid vectors in response to the luteoviruses. Compared to non‐viruliferous (NV) aphids, BLRV and PEMV1 elevated the amount of myristic acid (1.13 and 1.03‐fold increase) in A. fabae and A. pisum, respectively. V R. padi individuals exhibited a 1.11‐fold increase in palmitic acid content compared to the NV individuals. In contrast, other V aphids showed a reduced proportion of FA in response to the viruses. These changes in FA profile enhanced the ratio of saturated to unsaturated FA in V aphids (4.09‐fold increase). BLRV decreased protein and lipid contents in its aphid vector, A. fabae, while carbohydrate content was found to increase in V R. padi and A. pisum. Thus, our results demonstrate that luteoviruses change the content of some FA and EC in their aphid vectors highlighting a specific interaction among virus species, plant host and aphid vector.
... By contrast, several studies show that viruses do not alter natural enemy visitations or their ability to attack prey. For example, Joffrey et al. (2018) showed that the infection of Camelina sativa plants by turnip yellows virus does not render the plants more attractive or repellent to an aphid parasitoid Aphidius colemani. Similarly, CMV infection of squash has no significant impact on the ability of predatory insects to locate aphid prey (Mauck et al., 2015). ...
Attacks on plants by both viruses and their vectors is common in nature. Yet the dynamics of the plant–virus–vector tripartite system, in particular the effects of viral infection on plant–insect interactions, have only begun to emerge in the last decade. Viruses can modulate the interactions between insect vectors and plants via the jasmonate, salicylic acid and ethylene phytohormone pathways, resulting in changes in fitness and viral transmission capacity of their insect vectors. Virus infection of plants may also modulate other phytohormones, such as auxin, gibberellins, cytokinins, brassinosteroids and abscisic acid, with yet undefined consequences on plant–insect interactions. Moreover, virus infection in plants may incur changes to other plant traits, such as nutrition and secondary metabolites, that potentially contribute to virus‐associated, phytohormone‐mediated manipulation of plant–insect interactions. In this article, we review the research progress, discuss issues related to the complexity and variability of the viral modulation of plant interactions with insect vectors, and suggest future directions of research in this field.
... Plant viruses can affect their aphid vector performance directly but mainly through their host plant. The performance of aphids' natural enemies can be likewise modified by the pathogen (Hodge and Powell 2008) and the effects of virus infection on bottom-up regulation of plant-aphid-parasitoid systems have 123 Combined effects of elevated CO 2 and temperature on multitrophic interactions involving a… been recently investigated, with negative (Moiroux et al., 2004) or no effects (Albittar et al. 2019) of virus infection on biological control of aphids by parasitoids. On the other hand, top-down processes could also be affected, as predators and parasitoids can influence the distribution of virus vectors, in turn affecting the epidemiology of vector-transmitted diseases (Christiansen-Weniger et al. 1998;Smyrnioudis et al. 2001). ...
Atmospheric concentration of carbon dioxide (CO2) is predicted to double by late twenty-first century, likely increasing global temperature by 2.2 °C. Elevated CO2 (eCO2) and temperature (eT) affect agricultural crops as well as pests and their natural enemies. Changes in any part of multitrophic systems due to environmental factors can affect pest infestation and disease dynamics, as well as the effectiveness of biological control programs. Our study evaluated the effects of eCO2 and eT combined on the performance of the parasitoid Aphidius colemani Vierick (Hymenoptera: Braconidae) when its aphid host Rhopalosiphum padi L. (Hemiptera: Aphididae) was exposed to non-infected or Barley yellow dwarf virus (BYDV–PAV) infected wheat (Triticum aestivum L., Poaceae). Using controlled environment chambers, plant physiology and parasitoid performance were examined under ambient (aCO2&aT; aCO2 = 400 ppm, aT = 20 °C) and elevated (eCO2&eT; eCO2 = 800 ppm, eT = 22 °C) conditions. Virus infection reduced plant biomass and chlorophyll content more pronouncedly under eCO2&eT. Developmental time from oviposition to adult emergence of A. colemani significantly decreased under eCO2&eT, on virus-infected and non-infected plants. However, parasitism rate, sex ratio and pupal survivorship remained unchanged under eCO2&eT, regardless of virus infection. Therefore, we incline to suggest that the biocontrol of R. padi by A. colemani will continue being effective in a future climate with similar conditions as studied here. This study provides empirical data on a particular tritrophic system (plant-pest-parasitoid) affected by plant virus and eCO2&eT, essential to complement scientific knowledge about the impact of climate change on complex interactions of agro-ecosystems.
... The preference-performance hypothesis contends that insect herbivore performance matches their host plant preferences [15], a suggestion which has received support [16,17], albeit not always [18,19]. Few studies have considered similar effects at higher trophic levels, where there is again some support for this idea [7,20], but this is not always so [21][22][23][24]. ...
Indirect effects are ubiquitous in nature, and have received much attention in terrestrial
plant–insect herbivore–enemy systems. In such tritrophic systems, changes in plant quality can have consequential effects on the behavior and abundance of insect predators and parasitoids. Plant quality as perceived by insect herbivores may vary for a range of reasons, including because of infection by plant pathogens. However, plant diseases vary in their origin (viral, bacterial or fungal) and as a result may have differing effects on plant physiology. To investigate if the main groups of plant pathogens differ in their indirect effects on higher trophic levels, we performed a meta-analysis using 216 measured responses from 29 primary studies. There was no overall effect of plant pathogens on natural enemy traits as differences between pathogen types masked their effects. Infection by fungal plant pathogens showed indirect negative effects on the performance and preference of natural enemies via both chewing and piercing-sucking insect herbivore feeding guilds. Infection by bacterial plant pathogens had a positive effect on the natural enemies (parasitoids) of chewing herbivores. Infection by viral plant pathogens showed no clear effect, although parasitoid preference may be positively affected by their presence. It is important to note that given the limited volume of studies to date on such systems, this work should be considered exploratory. Plant pathogens are very common in nature, and tritrophic systems provide an elegant means to examine the consequences of indirect interactions in ecology. We suggest that further studies examining how plant pathogens affect higher trophic levels would be of considerable value.
... Parasitoids may thus suffer costs when developing on pathogen-infected hosts, through increased mortality (Hajek and van Nouhuys 2016) and development time, as well as reduced size, and an increase in time required to successfully attack infected hosts (Flick et al. 2016). The effect of plant pathogens, particularly viruses, on higher trophic levels has received much less attention (Finke 2012;Moiroux et al. 2018). Virus infection can indeed drastically affect the physiology and photosynthetic functioning of the host plant (Balachandran et al. 1997), the accumulation of nitrogen compounds, or expanded oxidase activities (Culver and Padmanabhan 2007). ...
... Plant viruses may further modulate bottom-up regulation, because virus infection affects plant development and sap composition (Jensen 1972;Fereres et al. 1990), as well as aphid development, growth rates, body size, reproduction, and longevity (Donaldson and Gratton 2007;Srinivasan et al. 2008;Jimenez-Martinez and Bosque-Perez 2009). As a consequence, virus infection of plants may affect parasitoid behaviour and fitness (Moiroux et al. 2018). The suitability of aphids as hosts for parasitoids is thus expected to depend on the infection status of the plant used for feeding. ...
... Cascading effects of the plant virus on the plant-aphid interaction may depend on the mode of transmission: persistent viruses tend to improve host plant quality for aphid vectors and promote long-term feeding, whereas non-persistent viruses tend to reduce plant quality and promote rapid aphid dispersal (Mauck et al. 2012). Accordingly, pronounced effects of infected plants mediated by the aphids on some life history traits of parasitoids were highlighted by several authors, particularly the cascading effects on tritrophic interactions (plant-aphid interaction) of non-persistent cucumber mosaic virus (Bromoviridae) and persistent turnip yellows virus (Luteoviridae) (de Oliveira et al. 2014;Mauck et al. 2015;Moiroux et al. 2018). However, to our knowledge, no study has assessed the impact of semi-persistent viruses on the foraging behaviour of parasitoids. ...
Effects of plants on herbivores can cascade up the food web and modulate the abundance of higher trophic levels. In agro-ecosystems, plant viruses can affect the interactions between crops, crop pests, and natural enemies. Little is known, however, about the effects of viruses on higher trophic levels, including parasitoids and their ability for pest regulation. We tested the hypothesis that a plant virus affects parasitoid foraging behaviour through cascading effects on higher trophic levels. We predicted that the semi-persistent Beet yellows virus (BYV) would influence plant (Beta vulgaris) quality, as well as aphid host (Aphis fabae) quality for a parasitoid Lysiphlebus fabarum. We determined amino acid and sugar content in healthy and infected plants (first trophic level), lipid content and body size of aphids (second trophic level) fed on both plants, as well as foraging behaviour and body size of parasitoids (third trophic level) that developed on aphids fed on both plants. Our results showed that virus infection increased sugars and decreased total amino acid content in B. vulgaris. We further observed an increase in aphid size without modification in host aphid quality (i.e., lipid content), and a slight effect on parasitoid behaviour through an increased number of antennal contacts with host aphids. Although the BYV virus clearly affected the first two trophic levels, it did not affect development or emergence of parasitoids. As the parasitoid L. fabarum does not seem to be affected by the virus, we discuss the possibility of using it for the development of targeted biological control against aphids.
