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Plant Virus Transmission by Vectors

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A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Viruses of Plants, Fungi and Protozoa".

Deadline for manuscript submissions: closed (15 January 2020) | Viewed by 101006

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Special Issue Editor

Dr. Véronique Brault

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Guest Editor

SVQV, Université de Strasbourg, Institut National de la Recherche Agronomique, Colmar, France
Interests: virus; transmission; Luteoviridae; Polerovirus; aphid

Special Issue Information

Dear Colleagues,

Viruses are transmitted from plant to plant predominantly by vectors, a process relying on the intricate interactions between host plants, viruses, and vectors. With the development of reverse genetics and the advent of high-throughput technologies, our knowledge of the molecular and cellular mechanisms governing the virus transmission process has substantially increased. Interestingly, by connecting these molecular and cellular approaches with research on vector fitness and behavior, virus-induced deregulations in plants, which have an impact on the vector and therefore, potentially, also on virus transmission, have started to be identified. This Special Issue will present an overview of the research focusing on the identification of viral, plant, and vector determinants involved in virus transmission, the decoding of the cross-talk between the three players, and the impact of biotic and abiotic stresses on the transmission process. Combining the different research findings, scales (from molecule to cell, organism, and field), and various experimental approaches (mutagenesis, transcriptomics, metabolomics, behavior), this Special Issue will shed light on this complex but exciting research field.

Dr. Véronique Brault
Guest Editor

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Keywords

Virus
Plant
Vector
Molecular and cellular mechanisms
Virus manipulation
Biotic and abiotic stresses
Epidemiology
Vector behavior

Published Papers (11 papers)

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Research

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14 pages, 5733 KiB

Open AccessArticle

Co-Acquired Nanovirus and Geminivirus Exhibit a Contrasted Localization within Their Common Aphid Vector

by Jérémy Di Mattia, Faustine Ryckebusch, Marie-Stéphanie Vernerey, Elodie Pirolles, Nicolas Sauvion, Michel Peterschmitt, Jean-Louis Zeddam and Stéphane Blanc

Viruses 2020, 12(3), 299; https://doi.org/10.3390/v12030299 - 10 Mar 2020

Cited by 10 | Viewed by 2803

Abstract

Single-stranded DNA (ssDNA) plant viruses belong to the families Geminiviridae and Nanoviridae. They are transmitted by Hemipteran insects in a circulative, mostly non-propagative, manner. While geminiviruses are transmitted by leafhoppers, treehoppers, whiteflies and aphids, nanoviruses are transmitted exclusively by aphids. Circulative transmission involves complex virus–vector interactions in which epithelial cells have to be crossed and defense mechanisms counteracted. Vector taxa are considered a relevant taxonomic criterion for virus classification, indicating that viruses can evolve specific interactions with their vectors. Thus, we predicted that, although nanoviruses and geminiviruses represent related viral families, they have evolved distinct interactions with their vector. This prediction is also supported by the non-structural Nuclear Shuttle Protein (NSP) that is involved in vector transmission in nanoviruses but has no similar function in geminiviruses. Thanks to the recent discovery of aphid-transmitted geminiviruses, this prediction could be tested for the geminivirus alfalfa leaf curl virus (ALCV) and the nanovirus faba bean necrotic stunt virus (FBNSV) in their common vector, Aphis craccivora. Estimations of viral load in midgut and head of aphids, precise localization of viral DNA in cells of insect vectors and host plants, and virus transmission tests revealed that the pathway of the two viruses across the body of their common vector differs both quantitatively and qualitatively. Full article

(This article belongs to the Special Issue Plant Virus Transmission by Vectors)

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18 pages, 2628 KiB

Open AccessArticle

Priming Melon Defenses with Acibenzolar-S-methyl Attenuates Infections by Phylogenetically Distinct Viruses and Diminishes Vector Preferences for Infected Hosts

by Jaimie R. Kenney, Marie-Eve Grandmont and Kerry E. Mauck

Viruses 2020, 12(3), 257; https://doi.org/10.3390/v12030257 - 26 Feb 2020

Cited by 13 | Viewed by 4536

Abstract

Plant virus management is mostly achieved through control of insect vectors using insecticides. However, insecticides are only marginally effective for preventing virus transmission. Furthermore, it is well established that symptoms of virus infections often encourage vector visitation to infected hosts, which exacerbates secondary spread. Plant defense elicitors, phytohormone analogs that prime the plant immune system against attack, may be a viable approach for virus control that complements insecticide use by disrupting pathologies that attract vectors. To explore this, we tested the effect of a commercial plant elicitor, acibenzolar-S-methyl (ASM), on infection rates, virus titers, and symptom development in melon plants inoculated with one of two virus species, Cucumber mosaic virus (CMV) and Cucurbit yellow stunting disorder virus (CYSDV). We also conducted behavioral assays to assess the effect of ASM treatment and virus inoculation on vector behavior. For both pathogens, ASM treatment reduced symptom severity and delayed disease progression. For CYSDV, this resulted in the attenuation of symptoms that encourage vector visitation and virion uptake. We did observe slight trade-offs in growth vs. defense following ASM treatment, but these effects did not translate into reduced yields or plant performance in the field. Our results suggest that immunity priming may be a valuable tool for improving management of insect-transmitted plant viruses. Full article

(This article belongs to the Special Issue Plant Virus Transmission by Vectors)

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16 pages, 1547 KiB

Open AccessArticle

Impact of Mutations in Arabidopsis thaliana Metabolic Pathways on Polerovirus Accumulation, Aphid Performance, and Feeding Behavior

by Florent Bogaert, Aurélie Marmonier, Elodie Pichon, Sylvaine Boissinot, Véronique Ziegler-Graff, Quentin Chesnais, Claire Villeroy, Martin Drucker and Véronique Brault

Viruses 2020, 12(2), 146; https://doi.org/10.3390/v12020146 - 27 Jan 2020

Cited by 8 | Viewed by 3098

Abstract

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. Full article

(This article belongs to the Special Issue Plant Virus Transmission by Vectors)

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15 pages, 2103 KiB

Open AccessArticle

Functional Transcomplementation between Wheat Dwarf Virus Strains in Wheat and Barley

by Isabelle Abt, Marlène Souquet, Gersende Angot, Romain Mabon, Sylvie Dallot, Gaël Thébaud and Emmanuel Jacquot

Viruses 2020, 12(1), 34; https://doi.org/10.3390/v12010034 - 28 Dec 2019

Cited by 9 | Viewed by 3646

Abstract

Wheat dwarf virus, transmitted by the leafhopper Psammotettix alienus in a persistent, non-propagative manner, infects numerous species from the Poaceae family. Data associated with wheat dwarf virus (WDV) suggest that some isolates preferentially infect wheat while other preferentially infect barley. This allowed to define the wheat strain and the barley strain. There are contradictory results in the literature regarding the ability of each of these two strains to infect its non-preferred host. To improve knowledge on the interactions between WDV strains and barley and wheat, transmission experiments were carried out using barcoded P. alienus and an experimental design based on single/sequential acquisitions of WDV strains and on transmissions to wheat and barley. Results showed that (I) WDV strains are transmitted with similar efficiencies by P. alienus males, females and larvae, (II) WDV wheat and barley strains do not infect barley and wheat plants, respectively, and (III) a functional transcomplementation between the wheat and barley strains allows a mixed infection of barley and wheat. The described ability of each WDV strain to infect a non-host plant in the presence of the other viral strain must be considered to analyze data available on WDV host range. Full article

(This article belongs to the Special Issue Plant Virus Transmission by Vectors)

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25 pages, 2716 KiB

Open AccessArticle

Modelling Vector Transmission and Epidemiology of Co-Infecting Plant Viruses

by Linda J. S. Allen, Vrushali A. Bokil, Nik J. Cunniffe, Frédéric M. Hamelin, Frank M. Hilker and Michael J. Jeger

Viruses 2019, 11(12), 1153; https://doi.org/10.3390/v11121153 - 13 Dec 2019

Cited by 19 | Viewed by 4651

Abstract

Co-infection of plant hosts by two or more viruses is common in agricultural crops and natural plant communities. A variety of models have been used to investigate the dynamics of co-infection which track only the disease status of infected and co-infected plants, and which do not explicitly track the density of inoculative vectors. Much less attention has been paid to the role of vector transmission in co-infection, that is, acquisition and inoculation and their synergistic and antagonistic interactions. In this investigation, a general epidemiological model is formulated for one vector species and one plant species with potential co-infection in the host plant by two viruses. The basic reproduction number provides conditions for successful invasion of a single virus. We derive a new invasion threshold which provides conditions for successful invasion of a second virus. These two thresholds highlight some key epidemiological parameters important in vector transmission. To illustrate the flexibility of our model, we examine numerically two special cases of viral invasion. In the first case, one virus species depends on an autonomous virus for its successful transmission and in the second case, both viruses are unable to invade alone but can co-infect the host plant when prevalence is high. Full article

(This article belongs to the Special Issue Plant Virus Transmission by Vectors)

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21 pages, 7486 KiB

Open AccessArticle

From a Movement-Deficient Grapevine Fanleaf Virus to the Identification of a New Viral Determinant of Nematode Transmission

by Lorène Belval, Aurélie Marmonier, Corinne Schmitt-Keichinger, Sophie Gersch, Peggy Andret-Link, Véronique Komar, Emmanuelle Vigne, Olivier Lemaire, Christophe Ritzenthaler and Gérard Demangeat

Viruses 2019, 11(12), 1146; https://doi.org/10.3390/v11121146 - 11 Dec 2019

Cited by 5 | Viewed by 4267

Abstract

Grapevine fanleaf virus (GFLV) and arabis mosaic virus (ArMV) are nepoviruses responsible for grapevine degeneration. They are specifically transmitted from grapevine to grapevine by two distinct ectoparasitic dagger nematodes of the genus Xiphinema. GFLV and ArMV move from cell to cell as virions through tubules formed into plasmodesmata by the self-assembly of the viral movement protein. Five surface-exposed regions in the coat protein called R1 to R5, which differ between the two viruses, were previously defined and exchanged to test their involvement in virus transmission, leading to the identification of region R2 as a transmission determinant. Region R4 (amino acids 258 to 264) could not be tested in transmission due to its requirement for plant systemic infection. Here, we present a fine-tuning mutagenesis of the GFLV coat protein in and around region R4 that restored the virus movement and allowed its evaluation in transmission. We show that residues T258, M260, D261, and R301 play a crucial role in virus transmission, thus representing a new viral determinant of nematode transmission. Full article

(This article belongs to the Special Issue Plant Virus Transmission by Vectors)

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16 pages, 2023 KiB

Open AccessArticle

Detection of Multiple Variants of Grapevine Fanleaf Virus in Single Xiphinema index Nematodes

by Shahinez Garcia, Jean-Michel Hily, Véronique Komar, Claude Gertz, Gérard Demangeat, Olivier Lemaire and Emmanuelle Vigne

Viruses 2019, 11(12), 1139; https://doi.org/10.3390/v11121139 - 10 Dec 2019

Cited by 11 | Viewed by 56426

Abstract

Grapevine fanleaf virus (GFLV) is responsible for a widespread disease in vineyards worldwide. Its genome is composed of two single-stranded positive-sense RNAs, which both show a high genetic diversity. The virus is transmitted from grapevine to grapevine by the ectoparasitic nematode Xiphinema index. Grapevines in diseased vineyards are often infected by multiple genetic variants of GFLV but no information is available on the molecular composition of virus variants retained in X. index following nematodes feeding on roots. In this work, aviruliferous X. index were fed on three naturally GFLV-infected grapevines for which the virome was characterized by RNAseq. Six RNA-1 and four RNA-2 molecules were assembled segregating into four and three distinct phylogenetic clades of RNA-1 and RNA-2, respectively. After 19 months of rearing, single and pools of 30 X. index tested positive for GFLV. Additionally, either pooled or single X. index carried multiple variants of the two GFLV genomic RNAs. However, the full viral genetic diversity found in the leaves of infected grapevines was not detected in viruliferous nematodes, indicating a genetic bottleneck. Our results provide new insights into the complexity of GFLV populations and the putative role of X. index as reservoirs of virus diversity. Full article

(This article belongs to the Special Issue Plant Virus Transmission by Vectors)

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Review

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15 pages, 2481 KiB

Open AccessReview

Molecular Insights into Host and Vector Manipulation by Plant Viruses

by Véronique Ziegler-Graff

Viruses 2020, 12(3), 263; https://doi.org/10.3390/v12030263 - 27 Feb 2020

Cited by 22 | Viewed by 5171

Abstract

Plant viruses rely on both host plant and vectors for a successful infection. Essentially to simplify studies, transmission has been considered for decades as an interaction between two partners, virus and vector. This interaction has gained a third partner, the host plant, to establish a tripartite pathosystem in which the players can react with each other directly or indirectly through changes induced in/by the third partner. For instance, viruses can alter the plant metabolism or plant immune defence pathways to modify vector’s attraction, settling or feeding, in a way that can be conducive for virus propagation. Such changes in the plant physiology can also become favourable to the vector, establishing a mutualistic relationship. This review focuses on the recent molecular data on the interplay between viral and plant factors that provide some important clues to understand how viruses manipulate both the host plants and vectors in order to improve transmission conditions and thus ensuring their survival. Full article

(This article belongs to the Special Issue Plant Virus Transmission by Vectors)

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12 pages, 283 KiB

Open AccessReview

Impact of Abiotic Stresses on Plant Virus Transmission by Aphids

by Manuella van Munster

Viruses 2020, 12(2), 216; https://doi.org/10.3390/v12020216 - 14 Feb 2020

Cited by 23 | Viewed by 4439

Abstract

Plants regularly encounter abiotic constraints, and plant response to stress has been a focus of research for decades. Given increasing global temperatures and elevated atmospheric CO₂ levels and the occurrence of water stress episodes driven by climate change, plant biochemistry, in particular, plant defence responses, may be altered significantly. Environmental factors also have a wider impact, shaping viral transmission processes that rely on a complex set of interactions between, at least, the pathogen, the vector, and the host plant. This review considers how abiotic stresses influence the transmission and spread of plant viruses by aphid vectors, mainly through changes in host physiology status, and summarizes the latest findings in this research field. The direct effects of climate change and severe weather events that impact the feeding behaviour of insect vectors as well as the major traits (e.g., within-host accumulation, disease severity and transmission) of viral plant pathogens are discussed. Finally, the intrinsic capacity of viruses to react to environmental cues in planta and how this may influence viral transmission efficiency is summarized. The clear interaction between biotic (virus) and abiotic stresses is a risk that must be accounted for when modelling virus epidemiology under scenarios of climate change. Full article

(This article belongs to the Special Issue Plant Virus Transmission by Vectors)

16 pages, 1314 KiB

Open AccessReview

Manipulation of Jasmonate Signaling by Plant Viruses and Their Insect Vectors

by Xiujuan Wu and Jian Ye

Viruses 2020, 12(2), 148; https://doi.org/10.3390/v12020148 - 27 Jan 2020

Cited by 34 | Viewed by 5044

Abstract

Plant viruses pose serious threats to stable crop yield. The majority of them are transmitted by insects, which cause secondary damage to the plant host from the herbivore-vector’s infestation. What is worse, a successful plant virus evolves multiple strategies to manipulate host defenses to promote the population of the insect vector and thereby furthers the disease pandemic. Jasmonate (JA) and its derivatives (JAs) are lipid-based phytohormones with similar structures to animal prostaglandins, conferring plant defenses against various biotic and abiotic challenges, especially pathogens and herbivores. For survival, plant viruses and herbivores have evolved strategies to convergently target JA signaling. Here, we review the roles of JA signaling in the tripartite interactions among plant, virus, and insect vectors, with a focus on the molecular and biochemical mechanisms that drive vector-borne plant viral diseases. This knowledge is essential for the further design and development of effective strategies to protect viral damages, thereby increasing crop yield and food security. Full article

(This article belongs to the Special Issue Plant Virus Transmission by Vectors)

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16 pages, 1281 KiB

Open AccessReview

Defenses against Virus and Vector: A Phloem-Biological Perspective on RTM- and SLI1-Mediated Resistance to Potyviruses and Aphids

by Karen J. Kloth and Richard Kormelink

Viruses 2020, 12(2), 129; https://doi.org/10.3390/v12020129 - 22 Jan 2020

Cited by 14 | Viewed by 4620

Abstract

Combining plant resistance against virus and vector presents an attractive approach to reduce virus transmission and virus proliferation in crops. Restricted Tobacco-etch virus Movement (RTM) genes confer resistance to potyviruses by limiting their long-distance transport. Recently, a close homologue of one of the RTM genes, SLI1, has been discovered but this gene instead confers resistance to Myzus persicae aphids, a vector of potyviruses. The functional connection between resistance to potyviruses and aphids, raises the question whether plants have a basic defense system in the phloem against biotic intruders. This paper provides an overview on restricted potyvirus phloem transport and restricted aphid phloem feeding and their possible interplay, followed by a discussion on various ways in which viruses and aphids gain access to the phloem sap. From a phloem-biological perspective, hypotheses are proposed on the underlying mechanisms of RTM- and SLI1-mediated resistance, and their possible efficacy to defend against systemic viruses and phloem-feeding vectors. Full article

(This article belongs to the Special Issue Plant Virus Transmission by Vectors)

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