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Molecular Plant Virus—Insect Vector Interactions

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A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Insect Viruses".

Deadline for manuscript submissions: closed (30 June 2016) | Viewed by 67313

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Special Issue Editor

Dr. Ralf Georg Dietzgen

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Guest Editor

Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St. Lucia, QLD 4072, Australia
Interests: virus evolution and epidemiology; negative-sense RNA viruses; plant virus control; virus taxonomy
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Many plant viruses are transmitted by insects, including aphids, planthoppers, leafhoppers, thrips, whiteflies, mealybugs and mites. The mode of transmission can be non-persistent or persistent with or without virus replication in the insect. Over the last few years, molecular data on these interactions have increasingly become available and have revealed intimate associations between viral and host proteins that underpin uptake and transmission of plant viruses. This may include specific receptors in various insect tissues and close molecular interactions between propagative plant viruses and their insect hosts. Symbiotic bacteria have also been shown to play a role.

Insects mount immune and RNA silencing responses to propagative plant virus infections as the viruses move through insect organs and tissues. Plant virus infections of insect vectors may also effect their behaviour and may be linked to plant virus emergence. With the recent application of RNA interference technologies in vector insects and high throughput sequencing technologies, new insights can be expected on how they respond to plant virus acquisition, replication, movement and transmission. This may lead to identification of host proteins involved and to novel potential targets to control plant virus acquisition and transmission. This special issue contains both reviews and updates on research relating to plant virus – vector interactions at the molecular level.

Dr. Ralf G. Dietzgen
Guest Editor

Manuscript Submission Information

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Keywords

Plant virus acquisition and transmission
Persistent insect transmission
Non-persistent insect transmission
Molecular plant virus-insect interactions
Insect transcriptome and proteome
Immune responses to plant virus infection
Plant virus receptors
Salivary gland and virus transmission
RNA silencing defence

Published Papers (7 papers)

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Research

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1827 KiB

Open AccessArticle

Comparative Analysis of RNAi-Based Methods to Down-Regulate Expression of Two Genes Expressed at Different Levels in Myzus persicae

by Michaël Mulot, Sylvaine Boissinot, Baptiste Monsion, Maryam Rastegar, Gabriel Clavijo, David Halter, Nicole Bochet, Monique Erdinger and Véronique Brault

Viruses 2016, 8(11), 316; https://0-doi-org.brum.beds.ac.uk/10.3390/v8110316 - 19 Nov 2016

Cited by 20 | Viewed by 6345

Abstract

With the increasing availability of aphid genomic data, it is necessary to develop robust functional validation methods to evaluate the role of specific aphid genes. This work represents the first study in which five different techniques, all based on RNA interference and on oral acquisition of double-stranded RNA (dsRNA), were developed to silence two genes, ALY and Eph, potentially involved in polerovirus transmission by aphids. Efficient silencing of only Eph transcripts, which are less abundant than those of ALY, could be achieved by feeding aphids on transgenic Arabidopsis thaliana expressing an RNA hairpin targeting Eph, on Nicotiana benthamiana infected with a Tobacco rattle virus (TRV)-Eph recombinant virus, or on in vitro-synthesized Eph-targeting dsRNA. These experiments showed that the silencing efficiency may differ greatly between genes and that aphid gut cells seem to be preferentially affected by the silencing mechanism after oral acquisition of dsRNA. In addition, the use of plants infected with recombinant TRV proved to be a promising technique to silence aphid genes as it does not require plant transformation. This work highlights the need to pursue development of innovative strategies to reproducibly achieve reduction of expression of aphid genes. Full article

(This article belongs to the Special Issue Molecular Plant Virus—Insect Vector Interactions)

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6110 KiB

Open AccessArticle

Role of Pea Enation Mosaic Virus Coat Protein in the Host Plant and Aphid Vector

by Juliette Doumayrou, Melissa Sheber, Bryony C. Bonning and W. Allen Miller

Viruses 2016, 8(11), 312; https://0-doi-org.brum.beds.ac.uk/10.3390/v8110312 - 18 Nov 2016

Cited by 8 | Viewed by 8669

Abstract

Understanding the molecular mechanisms involved in plant virus–vector interactions is essential for the development of effective control measures for aphid-vectored epidemic plant diseases. The coat proteins (CP) are the main component of the viral capsids, and they are implicated in practically every stage of the viral infection cycle. Pea enation mosaic virus 1 (PEMV1, Enamovirus, Luteoviridae) and Pea enation mosaic virus 2 (PEMV2, Umbravirus, Tombusviridae) are two RNA viruses in an obligate symbiosis causing the pea enation mosaic disease. Sixteen mutant viruses were generated with mutations in different domains of the CP to evaluate the role of specific amino acids in viral replication, virion assembly, long-distance movement in Pisum sativum, and aphid transmission. Twelve mutant viruses were unable to assemble but were able to replicate in inoculated leaves, move long-distance, and express the CP in newly infected leaves. Four mutant viruses produced virions, but three were not transmissible by the pea aphid, Acyrthosiphon pisum. Three-dimensional modeling of the PEMV CP, combined with biological assays for virion assembly and aphid transmission, allowed for a model of the assembly of PEMV coat protein subunits. Full article

(This article belongs to the Special Issue Molecular Plant Virus—Insect Vector Interactions)

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732 KiB

Open AccessArticle

Tomato Infection by Whitefly-Transmitted Circulative and Non-Circulative Viruses Induce Contrasting Changes in Plant Volatiles and Vector Behaviour

by Alberto Fereres, Maria Fernanda G. V. Peñaflor, Carla F. Favaro, Kamila E. X. Azevedo, Carolina H. Landi, Nathalie K. P. Maluta, José Mauricio S. Bento and Joao R.S. Lopes

Viruses 2016, 8(8), 225; https://0-doi-org.brum.beds.ac.uk/10.3390/v8080225 - 11 Aug 2016

Cited by 87 | Viewed by 8027

Abstract

Virus infection frequently modifies plant phenotypes, leading to changes in behaviour and performance of their insect vectors in a way that transmission is enhanced, although this may not always be the case. Here, we investigated Bemisia tabaci response to tomato plants infected by Tomato chlorosis virus (ToCV), a non-circulative-transmitted crinivirus, and Tomato severe rugose virus (ToSRV), a circulative-transmitted begomovirus. Moreover, we examined the role of visual and olfactory cues in host plant selection by both viruliferous and non-viruliferous B. tabaci. Visual cues alone were assessed as targets for whitefly landing by placing leaves underneath a Plexiglas plate. A dual-choice arena was used to assess whitefly response to virus-infected and mock-inoculated tomato leaves under light and dark conditions. Thereafter, we tested the whitefly response to volatiles using an active air-flow Y-tube olfactometer, and chemically characterized the blends using gas chromatography coupled to mass spectrometry. Visual stimuli tests showed that whiteflies, irrespective of their infectious status, always preferred to land on virus-infected rather than on mock-inoculated leaves. Furthermore, whiteflies had no preference for either virus-infected or mock-inoculated leaves under dark conditions, but preferred virus-infected leaves in the presence of light. ToSRV-infection promoted a sharp decline in the concentration of some tomato volatiles, while an increase in the emission of some terpenes after ToCV infection was found. ToSRV-viruliferous whiteflies preferred volatiles emitted from mock-inoculated plants, a conducive behaviour to enhance virus spread, while volatiles from ToCV-infected plants were avoided by non-viruliferous whiteflies, a behaviour that is likely detrimental to the secondary spread of the virus. In conclusion, the circulative persistent begomovirus, ToSRV, seems to have evolved together with its vector B. tabaci to optimise its own spread. However, this type of virus-induced manipulation of vector behaviour was not observed for the semi persistent crinivirus, ToCV, which is not specifically transmitted by B. tabaci and has a much less intimate virus-vector relationship. Full article

(This article belongs to the Special Issue Molecular Plant Virus—Insect Vector Interactions)

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Open AccessArticle

The Whitefly Bemisia tabaci Knottin-1 Gene Is Implicated in Regulating the Quantity of Tomato Yellow Leaf Curl Virus Ingested and Transmitted by the Insect

by Aliza Hariton Shalev, Iris Sobol, Murad Ghanim, Shu-Sheng Liu and Henryk Czosnek

Viruses 2016, 8(7), 205; https://0-doi-org.brum.beds.ac.uk/10.3390/v8070205 - 22 Jul 2016

Cited by 36 | Viewed by 6287

Abstract

The whitefly Bemisia tabaci is a major pest to agricultural crops. It transmits begomoviruses, such as Tomato yellow leaf curl virus (TYLCV), in a circular, persistent fashion. Transcriptome analyses revealed that B. tabaci knottin genes were responsive to various stresses. Upon ingestion of tomato begomoviruses, two of the four knottin genes were upregulated, knot-1 (with the highest expression) and knot-3. In this study, we examined the involvement of B. tabaci knottin genes in relation to TYLCV circulative transmission. Knottins were silenced by feeding whiteflies with knottin dsRNA via detached tomato leaves. Large amounts of knot-1 transcripts were present in the abdomen of whiteflies, an obligatory transit site of begomoviruses in their circulative transmission pathway; knot-1 silencing significantly depleted the abdomen from knot-1 transcripts. Knot-1 silencing led to an increase in the amounts of TYLCV ingested by the insects and transmitted to tomato test plants by several orders of magnitude. This effect was not observed following knot-3 silencing. Hence, knot-1 plays a role in restricting the quantity of virions an insect may acquire and transmit. We suggest that knot-1 protects B. tabaci against deleterious effects caused by TYLCV by limiting the amount of virus associated with the whitefly vector. Full article

(This article belongs to the Special Issue Molecular Plant Virus—Insect Vector Interactions)

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Review

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753 KiB

Open AccessReview

RNA Interference in Insect Vectors for Plant Viruses

by Surapathrudu Kanakala and Murad Ghanim

Viruses 2016, 8(12), 329; https://0-doi-org.brum.beds.ac.uk/10.3390/v8120329 - 12 Dec 2016

Cited by 38 | Viewed by 9243

Abstract

Insects and other arthropods are the most important vectors of plant pathogens. The majority of plant pathogens are disseminated by arthropod vectors such as aphids, beetles, leafhoppers, planthoppers, thrips and whiteflies. Transmission of plant pathogens and the challenges in managing insect vectors due to insecticide resistance are factors that contribute to major food losses in agriculture. RNA interference (RNAi) was recently suggested as a promising strategy for controlling insect pests, including those that serve as important vectors for plant pathogens. The last decade has witnessed a dramatic increase in the functional analysis of insect genes, especially those whose silencing results in mortality or interference with pathogen transmission. The identification of such candidates poses a major challenge for increasing the role of RNAi in pest control. Another challenge is to understand the RNAi machinery in insect cells and whether components that were identified in other organisms are also present in insect. This review will focus on summarizing success cases in which RNAi was used for silencing genes in insect vector for plant pathogens, and will be particularly helpful for vector biologists. Full article

(This article belongs to the Special Issue Molecular Plant Virus—Insect Vector Interactions)

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Open AccessReview

Plant Virus–Insect Vector Interactions: Current and Potential Future Research Directions

by Ralf G. Dietzgen, Krin S. Mann and Karyn N. Johnson

Viruses 2016, 8(11), 303; https://0-doi-org.brum.beds.ac.uk/10.3390/v8110303 - 09 Nov 2016

Cited by 149 | Viewed by 18102

Abstract

Acquisition and transmission by an insect vector is central to the infection cycle of the majority of plant pathogenic viruses. Plant viruses can interact with their insect host in a variety of ways including both non-persistent and circulative transmission; in some cases, the latter involves virus replication in cells of the insect host. Replicating viruses can also elicit both innate and specific defense responses in the insect host. A consistent feature is that the interaction of the virus with its insect host/vector requires specific molecular interactions between virus and host, commonly via proteins. Understanding the interactions between plant viruses and their insect host can underpin approaches to protect plants from infection by interfering with virus uptake and transmission. Here, we provide a perspective focused on identifying novel approaches and research directions to facilitate control of plant viruses by better understanding and targeting virus–insect molecular interactions. We also draw parallels with molecular interactions in insect vectors of animal viruses, and consider technical advances for their control that may be more broadly applicable to plant virus vectors. Full article

(This article belongs to the Special Issue Molecular Plant Virus—Insect Vector Interactions)

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Open AccessReview

Viral RNA Silencing Suppression: The Enigma of Bunyavirus NSs Proteins

by Marcio Hedil and Richard Kormelink

Viruses 2016, 8(7), 208; https://0-doi-org.brum.beds.ac.uk/10.3390/v8070208 - 23 Jul 2016

Cited by 33 | Viewed by 9206

Abstract

The Bunyaviridae is a family of arboviruses including both plant- and vertebrate-infecting representatives. The Tospovirus genus accommodates plant-infecting bunyaviruses, which not only replicate in their plant host, but also in their insect thrips vector during persistent propagative transmission. For this reason, they are generally assumed to encounter antiviral RNA silencing in plants and insects. Here we present an overview on how tospovirus nonstructural NSs protein counteracts antiviral RNA silencing in plants and what is known so far in insects. Like tospoviruses, members of the related vertebrate-infecting bunyaviruses classified in the genera Orthobunyavirus, Hantavirus and Phlebovirus also code for a NSs protein. However, for none of them RNA silencing suppressor activity has been unambiguously demonstrated in neither vertebrate host nor arthropod vector. The second part of this review will briefly describe the role of these NSs proteins in modulation of innate immune responses in mammals and elaborate on a hypothetical scenario to explain if and how NSs proteins from vertebrate-infecting bunyaviruses affect RNA silencing. If so, why this discovery has been hampered so far. Full article

(This article belongs to the Special Issue Molecular Plant Virus—Insect Vector Interactions)

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