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

Many 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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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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In VitroEvidence Supports Membrane Alanyl Aminopeptidase N as a Receptor for a Plant Virus in the Pea Aphid Vector

Journal of Virology ◽

10.1128/jvi.01479-15 ◽

2015 ◽

Vol 89 (22) ◽

pp. 11203-11212 ◽

Cited By ~ 38

Author(s):

Lucas B. Linz ◽

Sijun Liu ◽

Nanasaheb P. Chougule ◽

Bryony C. Bonning

Keyword(s):

Plant Virus ◽

Food Production ◽

Virus Transmission ◽

Plant Viruses ◽

Aminopeptidase N ◽

Pea Aphid ◽

Aphid Vector ◽

Alanyl Aminopeptidase

ABSTRACTInsect-borne plant viruses cause significant agricultural losses and jeopardize sustainable global food production. Although blocking plant virus transmission would allow for crop protection, virus receptors in insect vectors are unknown. Here we identify membrane alanyl aminopeptidase N (APN) as a receptor for pea enation mosaic virus (PEMV) coat protein (CP) in the gut of the pea aphid,Acyrthosiphon pisum, using a far-Western blot method. Pulldown and immunofluorescence binding assays and surface plasmon resonance were used to confirm and characterize CP-APN interaction. PEMV virions and a peptide comprised of PEMV CP fused to a proline-rich hinge (-P-) and green fluorescent protein (CP-P-GFP) specifically bound to APN. Recombinant APN expressed in Sf9 cells resulted in internalization of CP-P-GFP, which was visualized by confocal microscopy; such internalization is an expected hallmark of a functional gut receptor. Finally, in assays with aphid gut-derived brush border membrane vesicles, binding of CP-P-GFP competed with binding of GBP3.1, a peptide previously demonstrated to bind to APN in the aphid gut and to impede PEMV uptake into the hemocoel; this finding supports the hypothesis that GBP3.1 and PEMV bind to and compete for the same APN receptor. Thesein vitrodata combined with previously publishedin vivoexperiments (S. Liu, S. Sivakumar, W. O. Sparks, W. A. Miller, and B. C. Bonning, Virology 401:107–116, 2010,http://dx.doi.org/10.1016/j.virol.2010.02.009) support the identification of APN as the first receptor in a plant virus vector. Knowledge of this receptor will provide for technologies based on PEMV-APN interaction designed to block plant virus transmission and to suppress aphid populations.IMPORTANCEA significant proportion of global food production is lost to insect pests. Aphids, in addition to weakening plants by feeding on their sap, are responsible for transmitting about half of the plant viruses vectored by insects. Growers rely heavily on the application of chemical insecticides to manage both aphids and aphid-vectored plant viral disease. To increase our understanding of plant virus-aphid vector interaction, we providein vitroevidence supporting earlierin vivowork for identification of a receptor protein in the aphid gut called aminopeptidase N, which is responsible for entry of the plant virus pea enation mosaic virus into the pea aphid vector. Enrichment of proteins found on the surface of the aphid gut epithelium resulted in identification of this first aphid gut receptor for a plant virus. This discovery is particularly important since the disruption of plant virus binding to such a receptor may enable the development of a nonchemical strategy for controlling aphid-vectored plant viruses to maximize food production.

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A Theoretical Assessment of the Effects of Vector-Virus Transmission Mechanism on Plant Virus Disease Epidemics

Phytopathology ◽

10.1094/phyto.2000.90.6.576 ◽

2000 ◽

Vol 90 (6) ◽

pp. 576-594 ◽

Cited By ~ 95

Author(s):

L. V. Madden ◽

M. J. Jeger ◽

F. van den Bosch

Keyword(s):

Population Dynamics ◽

Plant Virus ◽

Virus Disease ◽

Disease Incidence ◽

Virus Transmission ◽

Rate Of Change ◽

Transmission Mechanism ◽

Model Parameters ◽

Disease Epidemics ◽

Plant Virus Disease

A continuous-time and deterministic model was used to characterize plant virus disease epidemics in relation to virus transmission mechanism and population dynamics of the insect vectors. The model can be written as a set of linked differential equations for healthy (virus-free), latently infected, infectious, and removed (postinfectious) plant categories, and virus-free, latent, and infective insects, with parameters based on the transmission classes, vector population dynamics, immigration/emigration rates, and virus-plant interactions. The rate of change in diseased plants is a function of the density of infective insects, the number of plants visited per time, and the probability of transmitting the virus per plant visit. The rate of change in infective insects is a function of the density of infectious plants, the number of plants visited per time by an insect, and the probability of acquiring the virus per plant visit. Numerical solutions of the differential equations were used to determine transitional and steady-state levels of disease incidence (d*); d* was also determined directly from the model parameters. Clear differences were found in disease development among the four transmission classes: nonpersistently transmitted (stylet-borne [NP]); semipersistently transmitted (foregut-borne [SP]); circulative, persistently transmitted (CP); and propagative, persistently transmitted (PP), with the highest disease incidence (d) for the SP and CP classes relative to the others, especially at low insect density when there was no insect migration or when the vector status of emigrating insects was the same as that of immigrating ones. The PP and CP viruses were most affected by changes in vector longevity, rates of acquisition, and inoculation of the virus by vectors, whereas the PP viruses were least affected by changes in insect mobility. When vector migration was explicitly considered, results depended on the fraction of infective insects in the immigration pool and the fraction of dying and emigrating vectors replaced by immigrants. The PP and CP viruses were most sensitive to changes in these factors. Based on model parameters, the basic reproductive number (R0)—number of new infected plants resulting, from an infected plant introduced into a susceptible plant population—was derived for some circumstances and used to determine the steady-state level of disease incidence and an approximate exponential rate of disease increase early in the epidemic. Results can be used to evaluate disease management strategies.

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Simulation of leaf curl disease dynamics in chili for strategic management options

Scientific Reports ◽

10.1038/s41598-020-79937-0 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Buddhadeb Roy ◽

Shailja Dubey ◽

Amalendu Ghosh ◽

Shalu Misra Shukla ◽

Bikash Mandal ◽

...

Keyword(s):

Disease Risk ◽

Virus Transmission ◽

Host Population ◽

High Rate ◽

Disease Dynamics ◽

Model Framework ◽

Management Options ◽

Transmission Parameters ◽

Vector Population ◽

Leaf Curl

AbstractLeaf curl, a whitefly-borne begomovirus disease, is the cause of frequent epidemic in chili. In the present study, transmission parameters involved in tripartite interaction are estimated to simulate disease dynamics in a population dynamics model framework. Epidemic is characterized by a rapid conversion rate of healthy host population into infectious type. Infection rate as basic reproduction number, R0 = 13.54, has indicated a high rate of virus transmission. Equilibrium population of infectious host and viruliferous vector are observed to be sensitive to the immigration parameter. A small increase in immigration rate of viruliferous vector increased the population of both infectious host and viruliferous vector. Migrant viruliferous vectors, acquisition, and transmission rates as major parameters in the model indicate leaf curl epidemic is predominantly a vector -mediated process. Based on underlying principles of temperature influence on vector population abundance and transmission parameters, spatio-temporal pattern of disease risk predicted is noted to correspond with leaf curl distribution pattern in India. Temperature in the range of 15–35 °C plays an important role in epidemic as both vector population and virus transmission are influenced by temperature. Assessment of leaf curl dynamics would be a useful guide to crop planning and evolution of efficient management strategies.

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Aphid–Plant–Phytovirus Pathosystems: Influencing Factors from Vector Behaviour to Virus Spread

Agriculture ◽

10.3390/agriculture11060502 ◽

2021 ◽

Vol 11 (6) ◽

pp. 502

Author(s):

Junior Corneille Fingu-Mabola ◽

Frédéric Francis

Keyword(s):

Influencing Factors ◽

Virus Transmission ◽

Physical Factors ◽

Factors Affecting ◽

Vector Borne Diseases ◽

Vector Behaviour ◽

Crop Fields ◽

Host Seeking ◽

The Impact ◽

Vector Efficiency

Aphids are responsible for the spread of more than half of the known phytovirus species. Virus transmission within the plant–aphid–phytovirus pathosystem depends on vector mobility which allows the aphid to reach its host plant and on vector efficiency in terms of ability to transmit phytoviruses. However, several other factors can influence the phytoviruses transmission process and have significant epidemiological consequences. In this review, we aimed to analyse the aphid behaviours and influencing factors affecting phytovirus spread. We discussed the impact of vector host-seeking and dispersal behaviours mostly involved in aphid-born phytovirus spread but also the effect of feeding behaviours and life history traits involved in plant–aphid–phytovirus relationships on vector performances. We also noted that these behaviours are influenced by factors inherent to the interactions between pathosystem components (mode of transmission of phytoviruses, vector efficiency, plant resistance, …) and several biological, biochemical, chemical or physical factors related to the environment of these pathosystem components, most of them being manipulated as means to control vector-borne diseases in the crop fields.

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Softening of Processed Plant Virus Infected Cucumis sativus Fruits

Agronomy ◽

10.3390/agronomy11081451 ◽

2021 ◽

Vol 11 (8) ◽

pp. 1451

Author(s):

Anne-Katrin Kersten ◽

Sabrina Scharf ◽

Martina Bandte ◽

Peer Martin ◽

Peter Meurer ◽

...

Keyword(s):

Cucumis Sativus ◽

Plant Virus ◽

Plant Viruses ◽

Economic Losses ◽

Symptom Expression ◽

Considerable Influence ◽

Mechanical Inoculation ◽

Morphological Alterations ◽

Texture Properties ◽

Textural Changes

Texture softening of pickled cucumbers does not meet consumers’ quality expectations and leads to economic losses. The factor(s) triggering this phenomenon is still unknown. We investigated the importance of plant viruses such as Cucumber green mottle mosaic tobamovirus (CGMMV) and Zucchini yellow mosaic potyvirus (ZYMV) in the context of softening of pickles. Cucumber plants (Cucumis sativus) were infected by mechanical inoculation, grown under greenhouse conditions and tested positive for the viral infection by ELISA. The severity of virus infection was reflected in yield and symptom expression. Histological and morphological alterations were observed. All fruits were pasteurized, separately stored in jars and subjected to texture measurements after four, six and 12 months. CGMMV-infections were asymptomatic or caused mild symptoms on leaves and fruit, and texture quality was comparable to control. At the same time, fruits of ZYMV-infected plants showed severe symptoms like deformations and discoloration, as well as a reduction in firmness and crunchiness after pasteurization. In addition, histological alterations were detected in such fruits, possibly causing textural changes. We conclude that plant viruses could have a considerable influence on the firmness and crunchiness of pickled cucumbers after pasteurization. It is possible that the severity of symptom expression has an influence on texture properties.

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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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Novel Functional Genomics Approaches: A Promising Future in the Combat Against Plant Viruses

Phytopathology ◽

10.1094/phyto-03-16-0145-fi ◽

2016 ◽

Vol 106 (10) ◽

pp. 1231-1239 ◽

Cited By ~ 10

Author(s):

Vincent N. Fondong ◽

Ugrappa Nagalakshmi ◽

Savithramma P. Dinesh-Kumar

Keyword(s):

Functional Genomics ◽

Plant Virus ◽

Reverse Genetics ◽

Plant Viruses ◽

Micro Rna ◽

Viral Genomes ◽

Virus Control ◽

Local Lesions ◽

Short Palindromic Repeat ◽

Interfering Rna

Advances in functional genomics and genome editing approaches have provided new opportunities and potential to accelerate plant virus control efforts through modification of host and viral genomes in a precise and predictable manner. Here, we discuss application of RNA-based technologies, including artificial micro RNA, transacting small interfering RNA, and Cas9 (clustered regularly interspaced short palindromic repeat–associated protein 9), which are currently being successfully deployed in generating virus-resistant plants. We further discuss the reverse genetics approach, targeting induced local lesions in genomes (TILLING) and its variant, known as EcoTILLING, that are used in the identification of plant virus recessive resistance gene alleles. In addition to describing specific applications of these technologies in plant virus control, this review discusses their advantages and limitations.

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