Mechanisms of arthropod transmission of plant and animal viruses.

A majority of the plant-infecting viruses and many of the animal-infecting viruses are dependent upon arthropod vectors for transmission between hosts and/or as alternative hosts. The viruses have evolved specific associations with their vectors, and we are beginning to understand the underlying mechanisms that regulate the virus transmission process. A majority of plant viruses are carried on the cuticle lining of a vector's mouthparts or foregut. This initially appeared to be simple mechanical contamination, but it is now known to be a biologically complex interaction between specific virus proteins and as yet unidentified vector cuticle-associated compounds. Numerous other plant viruses and the majority of animal viruses are carried within the body of the vector. These viruses have evolved specific mechanisms to enable them to be transported through multiple tissues and to evade vector defenses. In response, vector species have evolved so that not all individuals within a species are susceptible to virus infection or can serve as a competent vector. Not only are the virus components of the transmission process being identified, but also the genetic and physiological components of the vectors which determine their ability to be used successfully by the virus are being elucidated. The mechanisms of arthropod-virus associations are many and complex, but common themes are beginning to emerge which may allow the development of novel strategies to ultimately control epidemics caused by arthropod-borne viruses.     

Characteristics of pathogenic and mutualistic relationships of ascoviruses in field populations of parasitoid wasps

Ascoviruses are disseminated among larvae in lepidopteran populations by parasitic wasps during oviposition. Ascovirus relationships with these wasps vary from pathogenic to mutualistic, and experimentally can be shown possibly to be commensal non-pathogenic virus having little or no effect. Most ascoviruses are pathogens that female wasps vector mechanically. Other ascoviruses have a more intimate relationship with their wasp vectors in that their genome is stably maintained in all wasp nuclei through several generations by vertical transmission. In this relationship, these viruses are mutualistic, enhancing the successful development of the wasp larvae by suppressing lepidopteran defence mechanisms. The DpAV4 ascovirus is a mutualist in certain Diadromus wasps but is pathogenic or not when vectored by other species of this genus. These various biologies suggest that ascovirus/wasp relationships depend on wasp regulatory factors that control virus replication. Thus, certain ascoviruses can potentially have either a pathogenic, mutualistic, or non-pathogenic relationship with a specific wasp vector, the type of relationship being dependent upon the species system in which the relationship evolved. Finally, because ascoviruses appear to be related to ichnoviruses (Polydnaviridae), the DpAV4/Diadromus system constitutes a possible interesting intermediate between the pathogenic ascoviruses and symbiotic viruses that evolved to be ichnoviruses.     

Plant infection by two different viruses induce contrasting changes of vectors fitness and behavior

Insect-vectored plant viruses can induce changes in plant phenotypes,thus influencing plant-vector interactions in a way that may promote their dispersal according to their mode of transmission (i.e.,circulative vs.noncirculative).This indirect vector manipulation requires host-virus-vector coevolution and would thus be effective solely in very specific plant-virus-vector species associations.Some studies suggest this manipulation may depend on multiple factors relative to various intrinsic characteristics of vectors such as transmission efficiency.In anintegrative study,we tested the effects of infection of the Brassicaceae Camelina sativa with the noncirculative Cauliflower mosaic virus (CaMV)or the circulative Turnip yellows virus (TuYV)on the host-plant colonization of two aphid species differing in their virus transmission efficiency:the polyphagous Myzus persicae,efficient vector of both viruses,and the Brassicaceae specialist Brevicoryne brassicae,poor vector of TuYV and efficient vector of CaMV.Results confirmed the important role of virus mode of transmission as plant-mediated effects of CaMV on the two aphid species induced negative alterations of feeding behavior (i.e.,decreased phloem sap ingestion)and performance that were both conducive for virus fitness by promoting dispersion after a rapid acquisition.In addition,virus transmission efficiency may also play a role in vector manipulation by viruses as only the responses of the efficient vector to plant-mediated effects of TuYV,that is,enhanced feeding behavior and performances,were favorable to their acquisition and further dispersal.Altogether,this work demonstrated that vector transmission efficiency also has to be considered when studying the mechanisms underlying vector manipulation by viruses.Our results also re- inforce the idea that vector manipulation requires coevolution between plant,virus and vector.     

植物病原-媒介昆虫互作:研究进展与展望

大多数植物病毒及一些植物病原细菌由介体昆虫传播。植物病原与介体昆虫关系的研究有助于找到防控介体传播病原的关键环节,因此植物病原与介体昆虫的互作关系是植物病原传播机理研究中的核心问题。本文概述了国内外在植物病原与介体昆虫互作研究的最新进展,推介了本专辑论文的主要内容,并在此基础上,从生态和进化的角度提出了在植物病原-媒介昆虫互作研究中以下3个值得关注的研究方向:(1)植物病原与介体昆虫互作对生态系统的影响;(2)昆虫介体传播植物病毒的不同方式之间的关联性以及病毒、介体和植物之间的协同进化关系;(3)自然条件下植物病原-媒介昆虫互作的机理。植物病原与媒介昆虫互作的研究,既是生态和进化的理论问题,也和植物病原及其介体昆虫的绿色防控密切相关。     

Biological and molecular events associated with simultaneous transmission of plant viruses by invertebrate and fungal vectors

Viruses are likely to be the most dangerous parasites of living organisms because of their widespread occurrence, possible deleterious effects on their hosts and high rates of evolution. Virus host‐to‐host transmission is a critical step in the virus life cycle, because it enables survival in a given environment and efficient dissemination. As hosts of plant viruses are not mobile, these pathogens have adopted diverse transmission strategies involving various vector organisms, mainly arthropods, nematodes, fungi and protists. In nature, plants are often infected with more than one virus at a time, thereby creating potential sources for vectors to acquire and transmit simultaneously two or more viruses. Simultaneous transmission can result in multiple infections of new host plants, which become subsequent potential sources of the viruses, thus enhancing the spread of the diseases caused by these pathogens. Moreover, it can contribute to the maintenance of viral genetic diversity in the host communities. However, despite its possible significance, the problem of the simultaneous transmission of plant viruses by vectors has not been investigated in detail. In this review, the current knowledge on multiple viral transmissions by aphids, whiteflies, leafhoppers, planthoppers, nematodes and fungi is outlined.     

Insects as alternative hosts for phytopathogenic bacteria

Phytopathogens have evolved specialized pathogenicity determinants that enable them to colonize their specific plant hosts and cause disease, but their intimate associations with plants also predispose them to frequent encounters with herbivorous insects, providing these phytopathogens with ample opportunity to colonize and eventually evolve alternative associations with insects. Decades of research have revealed that these associations have resulted in the formation of bacterial-vector relationships, in which the insect mediates dissemination of the plant pathogen. Emerging research, however, has highlighted the ability of plant pathogenic bacteria to use insects as alternative hosts, exploiting them as they would their primary plant host. The identification of specific bacterial genetic determinants that mediate the interaction between bacterium and insect suggests that these interactions are not incidental, but have likely arisen following the repeated association of microorganisms with particular insects over evolutionary time. This review will address the biology and ecology of phytopathogenic bacteria that interact with insects, including the traditional role of insects as vectors, as well as the newly emerging paradigm of insects serving as alternative primary hosts. Also discussed is one case where an insect serves as both host and vector, which may represent a transitionary stage in the evolution of insect-phytopathogen associations.     

The pollen virome: A review of pollen-associated viruses and consequences for plants and their interactions with pollinators

The movement of pollen grains from anthers to stigmas, often by insect pollinator vectors, is essential for plant reproduction. However, pollen is also a unique vehicle for viral spread. Pollen-associated plant viruses reside on the outside or inside of pollen grains, infect susceptible individuals through vertical or horizontal infection pathways, and can decrease plant fitness. These viruses are transferred with pollen between plants by pollinator vectors as they forage for floral resources; thus, pollen-associated viral spread is mediated by floral and pollen grain phenotypes and pollinator traits, much like pollination. Most of what is currently known about pollen-associated viruses was discovered through infection and transmission experiments in controlled settings, usually involving one virus and one plant species of agricultural or horticultural interest. In this review, we first provide an updated, comprehensive list of the recognized pollen-associated viruses. Then, we summarize virus, plant, pollinator vector, and landscape traits that can affect pollen-associated virus transmission, infection, and distribution. Next, we highlight the consequences of plant–pollinator–virus interactions that emerge in complex communities of co-flowering plants and pollinator vectors, such as pollen-associated virus spread between plant species and viral jumps from plant to pollinator hosts. We conclude by emphasizing the need for collaborative research that bridges pollen biology, virology, and pollination biology.     

The polerovirus minor capsid protein determines vector specificity and intestinal tropism in the aphid

Aphid transmission of poleroviruses is highly specific, but the viral determinants governing this specificity are unknown. We used a gene exchange strategy between two poleroviruses with different vectors, Beet western yellows virus (BWYV) and Cucurbit aphid-borne yellows virus (CABYV), to analyze the role of the major and minor capsid proteins in vector specificity. Virus recombinants obtained by exchanging the sequence of the readthrough domain (RTD) between the two viruses replicated in plant protoplasts and in whole plants. The hybrid readthrough protein of chimeric viruses was incorporated into virions. Aphid transmission experiments using infected plants or purified virions revealed that vector specificity is driven by the nature of the RTD. BWYV and CABYV have specific intestinal sites in the vectors for endocytosis: the midgut for BWYV and both midgut and hindgut for CABYV. Localization of hybrid virions in aphids by transmission electron microscopy revealed that gut tropism is also determined by the viral origin of the RTD.     

The tortoise or the hare? Impacts of within-host dynamics on transmission success of arthropod-borne viruses

Arthropod-borne viruses (arboviruses) are maintained in a cycle of alternating transmission between vertebrate hosts and arthropod vectors. Arboviruses possess RNA genomes capable of rapid diversification and adaptation, and the between-host trade-offs inherent to host alternation impose well-documented constraints on arbovirus evolution. Here, we investigate the less well-studied within-host trade-offs that shape arbovirus replication dynamics and transmission. Arboviruses generally establish lifelong infection in vectors but transient infection of variable magnitude (i.e. peak virus concentration) and duration in vertebrate hosts. In the majority of experimental infections of vertebrate hosts, both the magnitude and duration of arbovirus replication depended upon the dose of virus administered, with increasing dose resulting in greater magnitude but shorter duration of viraemia. This pattern suggests that the vertebrate immune response imposes a trade-off between the height and breadth of the virus replication curve. To investigate the impact of this trade-off on transmission, we used a simple modelling approach to contrast the effect of ‘tortoise’ (low magnitude, long duration viraemia) and ‘hare’ (high magnitude, short duration viraemia) arbovirus replication strategies on transmission. This model revealed that, counter to previous theory, arboviruses that adopt a tortoise strategy have higher rates of persistence in both host and vector populations.     

昆虫介体行为与植物病毒的传播

大多数植物病毒都是依赖昆虫介体进行传播,其中超过80%的传毒介体昆虫都是属于半翅目同翅亚目。昆虫介体识别寄主植物和取食的过程与病毒的传播密切相关,本文主要综述了同翅亚目昆虫、蓟马等介体昆虫取食行为与植物病毒的相互作用方面的研究进展,着重于介绍昆虫不同取食阶段的行为对植物病毒传播的影响,病毒侵染对介体取食和识别寄主行为的影响。     

Improvement of the movement and host range properties of a plant virus vector through DNA shuffling

Virus expression vectors based on the tobacco mosaic virus (TMV) genome are powerful tools for foreign gene expression in plants. However, the inclusion of increased genetic load in the form of foreign genes limits the speed of systemic plant invasion and host range of these vectors due to reduced replication and movement efficiencies. To improve these properties of TMV vectors, the gene encoding the 30-kDa movement protein was subjected to mutagenesis and DNA shuffling. A vector that expresses the green fluorescent protein was used to allow simple visual discrimination of mutants with enhanced movement phenotypes. An initial round of mutagenesis produced 53 clones with a faster local movement phenotype. Two subsequent rounds of DNA shuffling produced additional clones that showed further increased rates of cell-to-cell movement and degrees of systemic invasion in restrictive hosts. Surprisingly, sequence analysis of the best performing shuffled genes revealed alterations resulting in coding and silent changes in the movement protein gene. Separation of these coding and silent alterations into distinct gene backgrounds revealed that each contributes to improved movement protein function to differing degrees. The resulting vectors demonstrate that the complex activities of the movement protein genes of viruses can be evolved to have improved movement phenotypes, as evidenced by cell-to-cell and systemic invasion. The experiments produced improved vectors that will be of use both for in planta functional screening and for therapeutic protein production and demonstrated the power of shuffling for plant virus vector improvement.     

Aphids as transport devices for plant viruses

Plant viruses have evolved a wide array of strategies to ensure efficient transfer from one host to the next. Any organism feeding on infected plants and traveling between plants can potentially act as a virus transport device. Such organisms, designated vectors, are found among parasitic fungi, root nematodes and plant-feeding arthropods, particularly insects. Due to their extremely specialized feeding behavior – exploring and sampling all plant tissues, from the epidermis to the phloem and xylem – aphids are by far the most important vectors, transmitting nearly 30% of all plant virus species described to date. Several different interaction patterns have evolved between viruses and aphid vectors and, over the past century, a tremendous number of studies have provided details of the underlying mechanisms. This article presents an overview of the different types of virus-aphid relationships, state-of-the-art knowledge of the molecular processes underlying these interactions, and the remaining black boxes waiting to be opened in the near future.     

Virulence not only costs but also benefits the transmission of a fungal virus

Current theory suggests that cost-benefit relationships govern the evolution of parasite virulence. The cost of virulence is expected to be high for fungal viruses, which are obligate parasites and completely dependent on their hosts. The majority of fungal viruses infect their hosts without any apparent symptoms. Cryphonectria hypovirus 1 (CHV-1), in contrast, is virulent and debilitates its host, Cryphonectria parasitica. However, the virulence of CHV-1 is associated with high costs for virus transmission, such as an attenuated fungal growth and reduced production of the fungal spores spreading the virus. In this study, we tested the hypothesis that virulence may not only have costs but also benefits for transmitting CHV-1 across vegetative incompatibility barriers between fungi. We investigated viruses with low, medium, and high virulence, and determined their transmission rate per host-to-host contact (transmissibility). The average transmission rate across all combinations tested was 53% for the most virulent virus, 37% for the virus with intermediate virulence, and 20% for the virus with lowest virulence. These results showed that increased virulence was strongly correlated with increased transmissibility, potentially counterbalancing virulence costs. This association of virulence and transmissibility may explain why CHV-1 spread widely and evolved higher virulence than most other fungal viruses.     

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.     

A single amino acid position in the helper component of cauliflower mosaic virus can change the spectrum of transmitting vector species

Viruses frequently use insect vectors to effect rapid spread through host populations. In plant viruses, vector transmission is the major mode of transmission, used by nearly 80% of species described to date. Despite the importance of this phenomenon in epidemiology, the specificity of the virus-vector relationship is poorly understood at both the molecular and the evolutionary level, and very limited data are available on the precise viral protein motifs that control specificity. Here, using the aphid-transmitted Cauliflower mosaic virus (CaMV) as a biological model, we confirm that the "noncirculative" mode of transmission dominant in plant viruses (designated "mechanical vector transmission" in animal viruses) involves extremely specific virus-vector recognition, and we identify an amino acid position in the "helper component" (HC) protein of CaMV involved in such recognition. Site-directed mutagenesis revealed that changing the residue at this position can differentially affect transmission rates obtained with various aphid species, thus modifying the spectrum of vector species for CaMV. Most interestingly, in a virus line transmitted by a single vector species, we observed the rapid appearance of a spontaneous mutant specifically losing its transmissibility by another aphid species. Hence, in addition to the first identification of an HC motif directly involved in specific vector recognition, we demonstrate that change of a virus to a different vector species requires only a single mutation and can occur rapidly and spontaneously.     

Evidence that binding of cucumber necrosis virus to vector zoospores involves recognition of oligosaccharides

Despite the importance of vectors in natural dissemination of plant viruses, relatively little is known about the molecular features of viruses and vectors that permit their interaction in nature. Cucumber necrosis virus (CNV) is a small spherical virus whose transmission in nature is facilitated by zoospores of the fungus Olpidium bornovanus. Previous studies have shown that specific regions of the CNV capsid are involved in transmission and that transmission defects in several CNV transmission mutants are due to inefficient attachment of virions to the zoospore surface. In this study, we have undertaken to determine if zoospores contain specific receptors for CNV. We show that in vitro binding of CNV to zoospores is saturable and that vector zoospores bind CNV more efficiently than nonvector zoospores. Further studies show that treatment of zoospores with periodate and trypsin reduces CNV binding, suggesting the involvement of glycoproteins in zoospore attachment. In virus overlay assays, CNV binds to several proteins, whereas CNV transmission mutants either fail to bind or bind at significantly reduced levels. The possible involvement of specific sugars in attachment was investigated by incubating CNV with zoospores in the presence of various sugars. Two mannose derivatives (methyl alpha-D-mannopyranoside and D-mannosamine), as well as three mannose-containing oligosaccharides (mannotriose, alpha3,alpha6-mannopentaose, and yeast mannan) and L-(-)-fucose, all inhibited CNV binding at relatively low concentrations. Taken together, our studies suggest that binding of CNV to zoospores is mediated by specific mannose and/or fucose-containing oligosaccharides. This is the first time sugars have been implicated in transmission of a plant virus.     

Herbivore arthropods benefit from vectoring plant viruses

Plants infected with pathogens often attract the pathogens’ vectors, but it is not clear if this is advantageous to the vectors. We therefore quantified the direct and indirect (through the host plant) effects of a pathogen on its vector. A positive direct effect of the plant‐pathogenic Tomato spotted wilt virus on its thrips vector (Frankliniella occidentalis) was found, but the main effect was indirect; juvenile survival and developmental rate of thrips was lower on pepper plants that were damaged by virus‐free thrips than on unattacked plants, but such negative effects were absent on plants that were damaged and inoculated by infected thrips or were mechanically inoculated with the virus. Hence, potential vectors benefit from attacking plants with virus because virus‐infected plants are of higher quality for the vector's offspring. We propose that plant pathogens in general have evolved mechanisms to overcome plant defences against their vectors, thus promoting pathogen spread.     

Molecular variation in vector-borne plant viruses: epidemiological significance

Patterns of variation are examined in four groups of plant viruses, with special reference to their particle proteins and to changes in vector transmissibility and specificity. In the nepoviruses and potyviruses, non-circulative transmission, by nematodes and aphids respectively, seems dependent on structural features on the surface of the virus particles. The N-terminal part of the particle protein may play the key role in potyviruses. Similarly in the luteoviruses, and possibly in the geminiviruses, specificity of circulative transmission by aphids, whiteflies and leafhoppers is linked to the antigenic specificity of the virus particles. Among naturally occurring isolates of the same virus, variation seems often to be discontinuous, and is predominantly of two sorts. Minor variations, characterized by loss of an epitope or substitutions of a few amino acids, can be associated with loss of transmissibility in luteoviruses and potyviruses, or have no effect. Major variations are associated with differences in vector specificity and seem likely to involve radical genetic changes that have evolved over long periods. The adaptation of virus particle proteins for transmission by vectors probably results in conservation of the genes that encode them, and in greater conservation of some parts of these genes than of others.