Different Plant Viruses Induce Changes in Feeding Behavior of Specialist and Generalist Aphids on Common Bean That Are Likely to Enhance Virus Transmission

Background: Evidence accumulates 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, the genetic basis of these indirect, plant-mediated effects on vectors and their dependence on the plant host and the mode of virus transmission is hardly known. Results: 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 the 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 stronger than did infection with TuYV. Conclusions: Overall, infection with CaMV — relying on the non-circulative 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 aphid probing and feeding behavior on both infected host plants, with potentially distinct effects on virus transmission. Keywords: Caulimovirus, polerovirus, aphid vector, transmission, feeding behavior, insect-plant interactions, transcriptome profiling, RNA-seq.

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Feeding Behavior and Virus-transmission Ability of Insect Vectors Exposed to Systemic Insecticides

Plants ◽

10.3390/plants9070895 ◽

2020 ◽

Vol 9 (7) ◽

pp. 895 ◽

Cited By ~ 3

Author(s):

Elisa Garzo ◽

Aránzazu Moreno ◽

María Plaza ◽

Alberto Fereres

Keyword(s):

Feeding Behavior ◽

Virus Transmission ◽

Plant Viruses ◽

Crop Damage ◽

Insect Vectors ◽

Vector Borne Diseases ◽

Systemic Insecticides ◽

Turnip Yellows Virus ◽

Vector Borne ◽

Leaf Curl Virus

The majority of plant viruses depend on Hemipteran vectors for their survival and spread. Effective management of these insect vectors is crucial to minimize the spread of vector-borne diseases, and to reduce crop damage. The aim of the present study was to evaluate the effect of various systemic insecticides on the feeding behavior of Bemisia tabaci and Myzus persicae, as well as their ability to interfere with the transmission of circulative viruses. The obtained results indicated that some systemic insecticides have antifeeding properties that disrupt virus transmission by their insect vectors. We found that some of the tested insecticides significantly reduced phloem contact and sap ingestion by aphids and whiteflies, activities that are closely linked to the transmission of phloem-limited viruses. These systemic insecticides may play an important role in reducing the primary and secondary spread of tomato yellow leaf curl virus (TYLCV) and turnip yellows virus (TuYV), transmitted by B. tabaci and M. persicae, respectively.

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Unresolved advantages of multipartitism in spatially structured environments

Virus Evolution ◽

10.1093/ve/veab004 ◽

2021 ◽

Vol 7 (1) ◽

Author(s):

Mark P Zwart ◽

Stéphane Blanc ◽

Marcelle Johnson ◽

Susanna Manrubia ◽

Yannis Michalakis ◽

...

Keyword(s):

Genome Organization ◽

Latent Infection ◽

Virus Transmission ◽

Plant Viruses ◽

Epidemic Spread ◽

Virus Particles ◽

Distinct Virus ◽

Network Epidemiology ◽

Short Commentary ◽

Animal Hosts

Abstract Multipartite viruses have segmented genomes and package each of their genome segments individually into distinct virus particles. Multipartitism is common among plant viruses, but why this apparently costly genome organization and packaging has evolved remains unclear. Recently Zhang and colleagues developed network epidemiology models to study the epidemic spread of multipartite viruses and their distribution over plant and animal hosts (Phys. Rev. Lett. 2019, 123, 138101). In this short commentary, we call into question the relevance of these results because of key model assumptions. First, the model of plant hosts assumes virus transmission only occurs between adjacent plants. This assumption overlooks the basic but imperative fact that most multipartite viruses are transmitted over variable distances by mobile animal vectors, rendering the model results irrelevant to differences between plant and animal hosts. Second, when not all genome segments of a multipartite virus are transmitted to a host, the model assumes an incessant latent infection occurs. This is a bold assumption for which there is no evidence to date, making the relevance of these results to understanding multipartitism questionable.

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Aphid endosymbiont facilitates virus transmission by modulating the volatile profile of host plants

BMC Plant Biology ◽

10.1186/s12870-021-02838-5 ◽

2021 ◽

Vol 21 (1) ◽

Author(s):

Xiao-Bin Shi ◽

Shuo Yan ◽

Chi Zhang ◽

Li-Min Zheng ◽

Zhan-Hong Zhang ◽

...

Keyword(s):

Host Plants ◽

Green Peach Aphid ◽

Virus Transmission ◽

Feeding Preference ◽

Plant Viruses ◽

Volatile Profile ◽

Cmv Infection ◽

Buchnera Aphidicola ◽

Plant Volatile ◽

Volatile Profiles

Abstract Background Most plant viruses rely on vectors for their transmission and spread. One of the outstanding biological questions concerning the vector-pathogen-symbiont multi-trophic interactions is the potential involvement of vector symbionts in the virus transmission process. Here, we used a multi-factorial system containing a non-persistent plant virus, cucumber mosaic virus (CMV), its primary vector, green peach aphid, Myzus persicae, and the obligate endosymbiont, Buchnera aphidicola to explore this uncharted territory. Results Based on our preliminary research, we hypothesized that aphid endosymbiont B. aphidicola can facilitate CMV transmission by modulating plant volatile profiles. Gene expression analyses demonstrated that CMV infection reduced B. aphidicola abundance in M. persicae, in which lower abundance of B. aphidicola was associated with a preference shift in aphids from infected to healthy plants. Volatile profile analyses confirmed that feeding by aphids with lower B. aphidicola titers reduced the production of attractants, while increased the emission of deterrents. As a result, M. persicae changed their feeding preference from infected to healthy plants. Conclusions We conclude that CMV infection reduces the B. aphidicola abundance in M. persicae. When viruliferous aphids feed on host plants, dynamic changes in obligate symbionts lead to a shift in plant volatiles from attraction to avoidance, thereby switching insect vector’s feeding preference from infected to healthy plants.

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CHAPTER 4: Whitefly Feeding Behavior and Transmission of Noncirculative Plant Viruses

Vector-Mediated Transmission of Plant Pathogens ◽

10.1094/9780890545355.004 ◽

2016 ◽

pp. 47-58 ◽

Cited By ~ 3

Keyword(s):

Feeding Behavior ◽

Plant Viruses

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Investigations of the mechanism of the transmission of plant viruses by insect vectors III. The insect’s saliva

Proceedings of the Royal Society of London Series B Biological Sciences ◽

10.1098/rspb.1939.0038 ◽

1939 ◽

Vol 127 (849) ◽

pp. 526-543 ◽

Cited By ~ 18

Keyword(s):

Direct Evidence ◽

Virus Transmission ◽

Plant Viruses ◽

Convincing Evidence ◽

Transmission Characteristic ◽

Insect Vectors ◽

Leaf Hopper

For the type of virus transmission characteristic of leaf hopper vectors, there is convincing evidence that the virus passes through the insect's body. The manner in which it emerges from the insect and comes to be inoculated into a plant is much less certainly known. It has generally been assumed that the saliva is the vehicle of the inoculation. For this assumption there is even now little direct evidence. I now describe observations on the excretion of saliva by a leafhopper and attempts to demonstrate experimentally in this saliva the virus of which this insect is a specific vector.

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Citrus tristeza virus P33 Protein Is Required for Efficient Transmission by the Aphid Aphis (Toxoptera) citricidus (Kirkaldy)

Viruses ◽

10.3390/v12101131 ◽

2020 ◽

Vol 12 (10) ◽

pp. 1131

Author(s):

Turksen Shilts ◽

Choaa El-Mohtar ◽

William O. Dawson ◽

Nabil Killiny

Keyword(s):

Citrus Tristeza Virus ◽

Transmission Rate ◽

Control Strategies ◽

Virus Transmission ◽

Plant Viruses ◽

Transmission Mechanisms ◽

Infectious Clones ◽

Underlying Mechanisms ◽

Tristeza Virus ◽

Citrus Tristeza

Plant viruses are threatening many valuable crops, and Citrus tristeza virus (CTV) is considered one of the most economically important plant viruses. CTV has destroyed millions of citrus trees in many regions of the world. Consequently, understanding of the transmission mechanism of CTV by its main vector, the brown citrus aphid, Aphis (Toxoptera) citricidus (Kirkaldy), may lead to better control strategies for CTV. The objective of this study was to understand the CTV–vector relationship by exploring the influence of viral genetic diversity on virus transmission. We built several infectious clones with different 5′-proximal ends from different CTV strains and assessed their transmission by the brown citrus aphid. Replacement of the 5′- end of the T36 isolate with that of the T30 strain (poorly transmitted) did not increase the transmission rate of T36, whereas replacement with that of the T68-1 isolate (highly transmitted) increased the transmission rate of T36 from 1.5 to 23%. Finally, substitution of p33 gene of the T36 strain with that of T68 increased the transmission rate from 1.5% to 17.8%. Although the underlying mechanisms that regulate the CTV transmission process by aphids have been explored in many ways, the roles of specific viral proteins are still not explicit. Our findings will improve our understanding of the transmission mechanisms of CTV by its aphid vector and may lead to the development of control strategies that interfere with its transmission by vector.

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Tenuivirususes a molecular bridge strategy to overcome insect midgut barriers for virus persistent transmission

10.1101/404657 ◽

2018 ◽

Author(s):

Gang Lu ◽

Shuo Li ◽

Changwei Zhou ◽

Xin Qian ◽

Qing Xiang ◽

...

Keyword(s):

Brown Planthopper ◽

Specific Interaction ◽

Virus Transmission ◽

Plant Viruses ◽

Insect Vector ◽

Terminal Protein ◽

Insect Midgut ◽

Helper Component ◽

Vector Interaction ◽

Molecular Bridge

AbstractMany persistent transmitted plant viruses, includingRice stripe tenuivirus(RSV), cause serious damages to crop productions in China and worldwide. Although many reports have indicated that successful insect-mediated virus transmission depends on proper virus–insect vector interactions, the mechanism(s) controlling interactions between viruses and insect vectors for virus persistent transmission remained poorly understood. In this study, we used RSV and its small brown planthopper (SBPH) vector as a working model to elucidate the molecular mechanism controlling RSV virion entrance into SBPH midgut for persistent transmission. We have now demonstrated that this non-envelopedTenuivirususes its non-structural glycoprotein NSvc2 as a helper component to bridge the specific interaction between virion and SBPH midgut cells, leading to overcome SBPH midgut barriers for virus persistent transmission. In the absence of this glycoprotein, purified RSV virion is not capable of entering SBPH midgut cells. In RSV-infected cells, glycoprotein NSvc2 is processed into two mature proteins: an amino-terminal protein NSvc2-N and a carboxyl-terminal protein NSvc2-C. We determined that NSvc2-N interacted with RSV virion and bound directly to midgut lumen surface via its N-glycosylation sites. Upon recognition by midgut cells, the midgut cells underwent endocytosis followed by compartmentalizing RSV virion and NSvc2 into early and then late endosomes. The acidic condition inside the late endosome triggered conformation change of NSvc2-C and caused cell membrane fusion via its highly conserved fusion loop motifs, leading to the release of RSV virion from endosome into cytosol. In summary, our results showed for the first time that a riceTenuivirususes a molecular bridge strategy to ensure proper interactions between virus and insect midgut for successful persistent transmission.Author summaryOver 75% of the known plant viruses are insect transmitted. Understanding how plant viruses interacted with their insect vectors during virus transmission is one of the key steps to manage virus diseases worldwide. Both the direct and indirect virus–insect vector interaction models have been proposed for virus non-persistent and semi-persistent transmission. However, the indirect virus–vector interaction mechanism during virus persistent transmission has not been reported previously. In this study, we developed a new reverse genetics technology and demonstrated that the circulative and propagative transmittedRice stripe tenuivirusutilizes a glycoprotein NSvc2 as a helper component to ensure a specific interaction betweenTenuivirusvirion and midgut cells of small brown planthopper (SBPH), leading to conquering the midgut barrier of SBPH. This is the first report of a helper component mediated-molecular bridge mechanism for virus persistent transmission. These new findings and our new model on persistent transmission expand our understanding of molecular mechanism(s) controlling virus–insect vector interactions during virus transmission in nature.

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Epidemiological and ecological consequences of virus manipulation of host and vector in plant virus transmission

10.1101/2021.09.08.459452 ◽

2021 ◽

Author(s):

Nik J. Cunniffe ◽

Nick P. Taylor ◽

Frédéric M. Hamelin ◽

Michael J. Jeger

Keyword(s):

Population Dynamics ◽

Plant Virus ◽

Complex Dynamics ◽

Virus Transmission ◽

Plant Viruses ◽

Infection Status ◽

Vector Behaviour ◽

Interactive Interface ◽

Vector Population ◽

Plant Infection

ABSTRACTMany plant viruses are transmitted by insect vectors. Transmission can be described as persistent or non-persistent depending on rates of acquisition, retention, and inoculation of virus. Much experimental evidence has accumulated indicating vectors can prefer to settle and/or feed on infected versus noninfected host plants. For persistent transmission, vector preference can also be conditional, depending on the vector’s own infection status. Since viruses can alter host plant quality as a resource for feeding, infection potentially also affects vector population dynamics. Here we use mathematical modelling to develop a theoretical framework addressing the effects of vector preferences for landing, settling and feeding – as well as potential effects of infection on vector population density – on plant virus epidemics. We explore the consequences of preferences that depend on the host (infected or healthy) and vector (viruliferous or nonviruliferous) phenotypes, and how this is affected by the form of transmission, persistent or non-persistent. We show how different components of vector preference have characteristic effects on both the basic reproduction number and the final incidence of disease. We also show how vector preference can induce bistability, in which the virus is able to persist even when it cannot invade from very low densities. Feedbacks between plant infection status, vector population dynamics and virus transmission potentially lead to very complex dynamics, including sustained oscillations. Our work is supported by an interactive interface https://plantdiseasevectorpreference.herokuapp.com/. Our model reiterates the importance of coupling virus infection to vector behaviour, life history and population dynamics to fully understand plant virus epidemics.

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Neem extracts on Aphis nerii behavior and papaya ringspot virus transmission

The Journal of Agriculture of the University of Puerto Rico ◽

10.46429/jaupr.v89i1-2.1071 ◽

1969 ◽

Vol 89 (1-2) ◽

pp. 75-84

Author(s):

Elías Hernández-Castro ◽

Víctor Utrera-Landa ◽

Juan A. Villanueva-Jiménez ◽

Daniel A. Rodríguez-Lagunes ◽

Mario M. Ojeda-Ramírez

Keyword(s):

Feeding Behavior ◽

Virus Transmission ◽

Viral Transmission ◽

Ringspot Virus ◽

Papaya Ringspot Virus ◽

Neem Seed ◽

Water Control ◽

Aphis Nerii ◽

Aphid Feeding ◽

Time Periods

The effect of neem extracts on feeding behavior of Aphis nerii, as well as Papaya Ringspot Virus (PRSV-p) transmission, was determined. We evaluated papaya seedlings sprayed under laboratory conditions with a 10% aqueous extract of unpeeled neem seed and with a water control. Two time periods, exploratory (0 to 3 min) and feeding (>3 to 20 min), were used to evaluate aphid feeding behavior. Aphid mortality was determined 24 h after spraying. Viral transmission was measured by ELISA tests. No significant differences (p > 0.05) were obtained in the exploratory feeding behavior. However, significantly more aphids (p < 0.05) stopped feeding on neemsprayed plants from the >3 to 20 min period. Also, higher (p < 0.05) aphid mortality (37% vs. 10%) was found in neem-sprayed plants. However, no significant differences (p > 0.05) were found in PRSV-p transmission, thus indicating that neem seed aqueous extracts did not prevent viral transmission.

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