Different plant viruses induce changes in feeding behavior of specialist and generalist aphids on common bean that are likely to enhance virus transmission

Bean common mosaic virus (BCMV), bean common mosaic necrosis virus (BCMNV), and cucumber mosaic virus (CMV) cause serious epidemics in common bean (Phaseolus vulgaris), a vital food security crop in many low-to-medium income countries, particularly in Sub-Saharan Africa. Aphids transmit these viruses “non-persistently,” i.e., virions attach loosely to the insects' stylets. Viruses may manipulate aphid-host interactions to enhance transmission. We used direct observation and electrical penetration graph measurements to see if the three viruses induced similar or distinct changes in feeding behaviors of two aphid species, Aphis fabae and Myzus persicae. Both aphids vector BCMV, BCMNV, and CMV but A. fabae is a legume specialist (the dominant species in bean fields) while M. persicae is a generalist that feeds on and transmits viruses to diverse plant hosts. Aphids of both species commenced probing epidermal cells (behavior optimal for virus acquisition and inoculation) sooner on virus-infected plants than on mock-inoculated plants. Infection with CMV was especially disruptive of phloem feeding by the bean specialist aphid A. fabae. A. fabae also experienced mechanical stylet difficulty when feeding on virus-infected plants, and this was also exacerbated for M. persicae. Overall, feeding on virus-infected host plants by specialist and generalist aphids was affected in different ways but all three viruses induced similar effects on each aphid type. Specifically, non-specialist (M. persicae) aphids encountered increased stylet difficulties on plants infected with BCMV, BCMNV, or CMV, whereas specialist aphids (A. fabae) showed decreased phloem ingestion on infected plants. Probing and stylet pathway activity (which facilitate virus transmission) were not decreased by any of the viruses for either of the aphid species, except in the case of A. fabae on CMV-infected bean, where these activities were increased. Overall, these virus-induced changes in host-aphid interactions are likely to enhance non-persistent virus transmission, and data from this work will be useful in epidemiological modeling of non-persistent vectoring of viruses by aphids

Cucumber mosaic virus and its 2b protein alter emission of host volatile organic compounds but not aphid vector settling in tobacco

BACKGROUND: Aphids, including the generalist herbivore Myzus persicae, transmit cucumber mosaic virus (CMV). CMV (strain Fny) infection affects M. persicae feeding behavior and performance on tobacco (Nicotiana tabacum), Arabidopsis thaliana and cucurbits in varying ways. In Arabidopsis and cucurbits, CMV decreases host quality and inhibits prolonged feeding by aphids, which may enhance virus transmission rates. CMV-infected cucurbits also emit deceptive, aphid-attracting volatiles, which may favor virus acquisition. In contrast, aphids on CMV-infected tobacco (cv. Xanthi) exhibit increased survival and reproduction. This may not increase transmission but might increase virus and vector persistence within plant communities. The CMV 2b counter-defense protein diminishes resistance to aphid infestation in CMV-infected tobacco plants. We hypothesised that in tobacco CMV and its 2b protein might also alter the emission of volatile organic compounds that would influence aphid behavior. RESULTS: Analysis of headspace volatiles emitted from tobacco plants showed that CMV infection both increased the total quantity and altered the blend produced. Furthermore, experiments with a CMV 2b gene deletion mutant (CMV∆2b) showed that the 2b counter-defense protein influences volatile emission. Free choice bioassays were conducted where wingless M. persicae could choose to settle on infected or mock-inoculated plants under a normal day/night regime or in continual darkness. Settling was recorded at 15 min, 1 h and 24 h post-release. Statistical analysis indicated that aphids showed no marked preference to settle on mock-inoculated versus infected plants, except for a marginally greater settlement of aphids on mock-inoculated over CMV-infected plants under normal illumination. CONCLUSIONS: CMV infection of tobacco plants induced quantitative and qualitative changes in host volatile emission and these changes depended in part on the activity of the 2b counter-defense protein. However, CMV-induced alterations in tobacco plant volatile emission did not have marked effects on the settling of aphids on infected versus mock-inoculated plants even though CMV-infected plants are higher quality hosts for M. persicae.This work was supported by grants from the Leverhulme Trust (F/09741/F, RPG-2012-667), UK Biotechnology and Biological Sciences Research Council (BB/D014376/1, BB/J011762/1) and the Cambridge University Isaac Newton Trust (12.07/I)

Three Aphid-Transmitted Viruses Encourage Vector Migration From Infected Common Bean ( Phaseolus vulgaris ) Plants Through a Combination of Volatile and Surface Cues

Bean common mosaic virus (BCMV), bean common mosaic necrosis virus (BCMNV), and cucumber mosaic virus (CMV) are important pathogens of common bean (Phaseolus vulgaris), a crop vital for food security in sub-Saharan Africa. These viruses are vectored by aphids non-persistently, with virions bound loosely to stylet receptors. These viruses also manipulate aphid-mediated transmission by altering host properties. Virus-induced effects on host-aphid interactions were investigated using choice test (migration) assays, olfactometry, and analysis of insect-perceivable volatile organic compounds (VOCs) using gas chromatography (GC)-coupled mass spectrometry, and GC-coupled electroantennography. When allowed to choose freely between infected and uninfected plants, aphids of the legume specialist species Aphis fabae, and of the generalist species Myzus persicae, were repelled by plants infected with BCMV, BCMNV, or CMV. However, in olfactometer experiments with A. fabae, only the VOCs emitted by BCMNV-infected plants repelled aphids. Although BCMV, BCMNV, and CMV each induced distinctive changes in emission of aphid-perceivable volatiles, all three suppressed emission of an attractant sesquiterpene, α-copaene, suggesting these three different viruses promote migration of virus-bearing aphids in a similar fashion

Three Aphid-Transmitted Viruses Encourage Vector Migration From Infected Common Bean ( Phaseolus vulgaris ) Plants Through a Combination of Volatile and Surface Cues

Bean common mosaic virus (BCMV), bean common mosaic necrosis virus (BCMNV), and cucumber mosaic virus (CMV) are important pathogens of common bean (Phaseolus vulgaris), a crop vital for food security in sub-Saharan Africa. These viruses are vectored by aphids non-persistently, with virions bound loosely to stylet receptors. These viruses also manipulate aphid-mediated transmission by altering host properties. Virus-induced effects on host-aphid interactions were investigated using choice test (migration) assays, olfactometry, and analysis of insect-perceivable volatile organic compounds (VOCs) using gas chromatography (GC)-coupled mass spectrometry, and GC-coupled electroantennography. When allowed to choose freely between infected and uninfected plants, aphids of the legume specialist species Aphis fabae, and of the generalist species Myzus persicae, were repelled by plants infected with BCMV, BCMNV, or CMV. However, in olfactometer experiments with A. fabae, only the VOCs emitted by BCMNV-infected plants repelled aphids. Although BCMV, BCMNV, and CMV each induced distinctive changes in emission of aphid-perceivable volatiles, all three suppressed emission of an attractant sesquiterpene, α-copaene, suggesting these three different viruses promote migration of virus-bearing aphids in a similar fashion

Three aphid-transmitted viruses encourage vector migration from infected common bean (Phaseolus vulgaris) plants through a combination of volatile and surface cues

Bean common mosaic virus (BCMV), bean common mosaic necrosis virus (BCMNV), and cucumber mosaic virus (CMV) are important pathogens of common bean (Phaseolus vulgaris), a crop vital for food security in sub-Saharan Africa. These viruses are vectored by aphids non-persistently, with virions bound loosely to stylet receptors. These viruses also manipulate aphid-mediated transmission by altering host properties. Virus-induced effects on host-aphid interactions were investigated using choice test (migration) assays, olfactometry, and analysis of insect-perceivable volatile organic compounds (VOCs) using gas chromatography (GC)-coupled mass spectrometry, and GC-coupled electroantennography. When allowed to choose freely between infected and uninfected plants, aphids of the legume specialist species Aphis fabae, and of the generalist species Myzus persicae, were repelled by plants infected with BCMV, BCMNV, or CMV. However, in olfactometer experiments with A. fabae, only the VOCs emitted by BCMNV-infected plants repelled aphids. Although BCMV, BCMNV, and CMV each induced distinctive changes in emission of aphid-perceivable volatiles, all three suppressed emission of an attractant sesquiterpene, α-copaene, suggesting these three different viruses promote migration of virus-bearing aphids in a similar fashion

Factors influencing oviposition behaviour of the invasive pest, Drosophila suzukii, derived from interactions with other Drosophila species: potential applications for control

Drosophila suzukii (Matsumura) or spotted wing Drosophila is a worldwide invasive pest of soft‐ and stone‐fruit production. Female D. suzukii lay their eggs in ripening fruit and the hatched larvae damage fruit from the inside, rendering it unmarketable and causing significant economic loss. Current methods to reduce D. suzukii population in the field primarily rely on chemical insecticides which are not a sustainable long‐term solution and increase the risk of resistance developing. Several studies demonstrate that when D. suzukii encounter or coexist with other Drosophila on a food source, this is usually a disadvantage to D. suzukii, leading to reduced oviposition and increased larval mortality. These effects have potential to be exploited from a pest management perspective. In this review we summarise recent research articles focusing on the interspecific interactions between D. suzukii and other Drosophila species aimed at understanding how this drives D. suzukii behaviour. Potential semiochemical and microbiome impacts are postulated as determinants of D. suzukii behaviour. Development of control practices focusing on reducing D. suzukii populations and deterring them from laying eggs by utilising factors that drive their behaviour are discussed. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry

Induction of aphid resistance in tobacco by the cucumber mosaic virus CMV∆2b mutant is jasmonate-dependent.

Funder: Cambridge Philosophical SocietyFunder: Cambridge Department of Plant Sciences Frank Smart StudentshipFunder: Gatsby Summer Undergraduate BursaryFunder: National Research Foundation of KoreaFunder: Cambridge Africa StudentshipCucumber mosaic virus (CMV) is vectored by aphids, including Myzus persicae. Tobacco (Nicotiana tabacum 'Xanthi') plants infected with a mutant of the Fny strain of CMV (Fny-CMVΔ2b, which cannot express the CMV 2b protein) exhibit strong resistance against M. persicae, which is manifested by decreased survival and reproduction of aphids confined on the plants. Previously, we found that the Fny-CMV 1a replication protein elicits aphid resistance in plants infected with Fny-CMVΔ2b, whereas in plants infected with wild-type Fny-CMV this is counteracted by the CMV 2b protein, a counterdefence protein that, among other things, inhibits jasmonic acid (JA)-dependent immune signalling. We noted that in nontransformed cv. Petit Havana SR1 tobacco plants aphid resistance was not induced by Fny-CMVΔ2b, suggesting that not all tobacco varieties possess the factor(s) with which the 1a protein interacts. To determine if 1a protein-induced aphid resistance is JA-dependent in Xanthi tobacco, transgenic plants were made that expressed an RNA silencing construct to diminish expression of the JA co-receptor CORONATINE-INSENSITIVE 1. Fny-CMVΔ2b did not induce resistance to M. persicae in these transgenic plants. Thus, aphid resistance induction by the 1a protein requires JA-dependent defensive signalling, which is countered by the CMV 2b protein.Work was funded by grants from the UK Biotechnological and Biological Sciences Research Council (SCPRID grant number BB/J011762/1, GCRF grant number BB/P023223/1, and 21ROMITIGATIONFUND CAMBRIDGE BB/W510609/1 https://www.ukri.org/ (accessed on 31 July 2022)) and BBSRC CONNECTED Network (BB/R005397/1: https://www.connectedvirus.net/ accessed on 31 July 2022), and The Leverhulme Trust (F/09741/F and RPG-2012-667, https://www.leverhulme.ac.uk/ accessed on 31 July 2022). W.A. had a Cambridge Africa studentship with additional support from a Cambridge Department of Plant Sciences Frank Smart Studentship, and the Cambridge Philosophical Society. E.B. was supported by a Korean National Research Foundation Postdoctoral Fellowship. J.J. was in receipt of a Gatsby Summer Undergraduate Bursary

Induction of aphid resistance in tobacco by the cucumber mosaic virus CMV∆2b mutant is jasmonate-dependent.

Cucumber mosaic virus (CMV) is vectored by aphids, including Myzus persicae. Tobacco (Nicotiana tabacum 'Xanthi') plants infected with a mutant of the Fny strain of CMV (Fny-CMVΔ2b, which cannot express the CMV 2b protein) exhibit strong resistance against M. persicae, which is manifested by decreased survival and reproduction of aphids confined on the plants. Previously, we found that the Fny-CMV 1a replication protein elicits aphid resistance in plants infected with Fny-CMVΔ2b, whereas in plants infected with wild-type Fny-CMV this is counteracted by the CMV 2b protein, a counterdefence protein that, among other things, inhibits jasmonic acid (JA)-dependent immune signalling. We noted that in nontransformed cv. Petit Havana SR1 tobacco plants aphid resistance was not induced by Fny-CMVΔ2b, suggesting that not all tobacco varieties possess the factor(s) with which the 1a protein interacts. To determine if 1a protein-induced aphid resistance is JA-dependent in Xanthi tobacco, transgenic plants were made that expressed an RNA silencing construct to diminish expression of the JA co-receptor CORONATINE-INSENSITIVE 1. Fny-CMVΔ2b did not induce resistance to M. persicae in these transgenic plants. Thus, aphid resistance induction by the 1a protein requires JA-dependent defensive signalling, which is countered by the CMV 2b protein.Work was funded by grants from the UK Biotechnological and Biological Sciences Research Council (SCPRID grant number BB/J011762/1, GCRF grant number BB/P023223/1, and 21ROMITIGATIONFUND CAMBRIDGE BB/W510609/1 https://www.ukri.org/ (accessed on 31 July 2022)) and BBSRC CONNECTED Network (BB/R005397/1: https://www.connectedvirus.net/ accessed on 31 July 2022), and The Leverhulme Trust (F/09741/F and RPG-2012-667, https://www.leverhulme.ac.uk/ accessed on 31 July 2022). W.A. had a Cambridge Africa studentship with additional support from a Cambridge Department of Plant Sciences Frank Smart Studentship, and the Cambridge Philosophical Society. E.B. was supported by a Korean National Research Foundation Postdoctoral Fellowship. J.J. was in receipt of a Gatsby Summer Undergraduate Bursary

Induction of aphid resistance in tobacco by the cucumber mosaic virus CMV∆2b mutant is jasmonate‐dependent

Funder: Cambridge Africa StudentshipFunder: Cambridge Department of Plant Sciences Frank Smart StudentshipFunder: Cambridge Philosophical Society; Id: http://dx.doi.org/10.13039/100013858Funder: National Research Foundation of Korea; Id: http://dx.doi.org/10.13039/501100003725Funder: Gatsby Summer Undergraduate BursaryCucumber mosaic virus (CMV) is vectored by aphids, including Myzus persicae. Tobacco (Nicotiana tabacum ‘Xanthi’) plants infected with a mutant of the Fny strain of CMV (Fny‐CMVΔ2b, which cannot express the CMV 2b protein) exhibit strong resistance against M. persicae, which is manifested by decreased survival and reproduction of aphids confined on the plants. Previously, we found that the Fny‐CMV 1a replication protein elicits aphid resistance in plants infected with Fny‐CMVΔ2b, whereas in plants infected with wild‐type Fny‐CMV this is counteracted by the CMV 2b protein, a counterdefence protein that, among other things, inhibits jasmonic acid (JA)‐dependent immune signalling. We noted that in nontransformed cv. Petit Havana SR1 tobacco plants aphid resistance was not induced by Fny‐CMVΔ2b, suggesting that not all tobacco varieties possess the factor(s) with which the 1a protein interacts. To determine if 1a protein‐induced aphid resistance is JA‐dependent in Xanthi tobacco, transgenic plants were made that expressed an RNA silencing construct to diminish expression of the JA co‐receptor CORONATINE‐INSENSITIVE 1. Fny‐CMVΔ2b did not induce resistance to M. persicae in these transgenic plants. Thus, aphid resistance induction by the 1a protein requires JA‐dependent defensive signalling, which is countered by the CMV 2b protein

Cucumber mosaic virus 2b proteins inhibit virus-induced aphid resistance in tobacco.

Cucumber mosaic virus (CMV), which is vectored by aphids, has a tripartite RNA genome encoding five proteins. In tobacco (Nicotiana tabacum), a subgroup IA CMV strain, Fny-CMV, increases plant susceptibility to aphid infestation but a viral mutant unable to express the 2b protein (Fny-CMV∆2b) induces aphid resistance. We hypothesized that in tobacco, one or more of the four other Fny-CMV gene products (the 1a or 2a replication proteins, the movement protein, or the coat protein) are potential aphid resistance elicitors, whilst the 2b protein counteracts induction of aphid resistance. Mutation of the Fny-CMV 2b protein indicated that inhibition of virus-induced resistance to aphids (Myzus persicae) depends on amino acid sequences known to control nucleus-to-cytoplasm shuttling. LS-CMV (subgroup II) also increased susceptibility to aphid infestation but the LS-CMV∆2b mutant did not induce aphid resistance. Using reassortant viruses comprising different combinations of LS and Fny genomic RNAs, we showed that Fny-CMV RNA 1 but not LS-CMV RNA 1 conditions aphid resistance in tobacco, suggesting that the Fny-CMV 1a protein triggers resistance. However, the 2b proteins of both strains suppress aphid resistance, suggesting that the ability of 2b proteins to inhibit aphid resistance is conserved among divergent CMV strains.This work was supported by grants from the UK Biotechnological and Biological Sciences Research Council (SCPRID grant number BB/J011762/1, and GCRF grant number BB/P023223/1) and the Leverhulme Trust (F/09741/F, RPG-2012-667), and QL was funded by the China Scholarship Council