Vector-plant Interactions Research Articles

Research on arthropod vectors of plant pathogens in a post-Subsection Cc world: current status and future prospects

Abstract The study of herbivorous arthropod vectors of plant pathogens has been a subdiscipline within entomology for more than a century. It was recognized as a unique field with the establishment of a Subsection (Cc) in the Entomological Society of America (ESA) from 1953 through 2007. During that period, work in the field expanded from an initial emphasis on management of vector-borne plant pathogens to include biology of the pathosystems. Since 2007, when ESA reorganized the subsections within the society, work on herbivorous vectors of plant pathogens has continued to grow. This article briefly summarizes the work in this field prior to, during, and after the ESA Subsection Cc era. We identify and describe 4 research areas that have characterized the field since 2007: Molecular mechanisms of vector–plant interactions, managing vectors and pathogen transmission in agriculture, illuminating the ecology of vectors and pathogens outside of crops, and pathogen manipulation of host phenotypes and vector behavior. We then identify 10 frontiers and prospects for the field in the coming years that build on these 4 research areas, ranging from molecular and cellular aspects to ramifications for managed and natural ecosystems. We also examine trends in funding and professional opportunities for scientists working on herbivorous vectors and pathogens. Finally, we renew the call for greater integration of work addressing vector-borne plant, animal, and human pathogens due to fundamental similarities in their biology and importance for human well-being within an expanded understanding of the “One Health” paradigm, which currently emphasizes human and animal health.

Turnip Mosaic Virus Infection Differentially Modifies Cabbage Aphid Probing Behavior in Spring and Winter Oilseed Rape (Brassica napus).

Simple SummaryWinter oilseed rape accounts for about 90% of total oilseed rape planting area in China, with the majority of it concentrated in the Yangtze River basin. The remaining 10% is mostly found in the provinces of China’s northwest plateau. Winter oilseed rape areas in China have gradually expanded to the north in the last decade, resulting in cabbage aphids and turnip mosaic virus (TuMV). The aphid is a vector for TuMV and is gradually increasing on winter and spring oilseed rape. Quantifying the probing behaviors of the aphids on spring oilseed rape and winter oilseed rape helps us to understand TuMV regulation of the aphids. We found that compared to mock-inoculated plants, cabbage aphids on infected plants increased brief probing frequency, cell penetration frequency, intracellular probing time, decreased time to first probe and pathway duration, potentially promoting viral acquisition and minimizing viral loss and plant damage. Viruliferous aphids had reduced pathway duration, increased cell penetration frequency, increased intracellular probing time, increased salivation frequency, and ingested less sap compared with non-viruliferous aphids, primed for viral infection. TuMV infection also differentially modified aphid feeding behavior on winter and spring oilseed rape cultivars, primarily on uninfected plants.Direct and indirect effects of plant virus infection on vector behavior have been discovered to improve virus transmission efficiency, but the impact of plant cultivars in virus–vector–plant interactions has received little attention. Electropenetrography (EPG) allows real-time tracking and quantification of stylet penetration behaviors, pathogen transmission, and plant resistance mechanisms. Quantitative probing behaviors on a spring oilseed rape cultivar, ‘Xinyou17’, and a winter oilseed rape cultivar, ‘Zheping4’, were investigated using EPG to compare turnip mosaic virus (TuMV) regulation of cabbage aphid probing behavior. Results for indirect effects showed that compared to mock-inoculated plants, cabbage aphids on infected plants increased brief probing frequency, cell penetration frequency, intracellular probing time, and decreased time to first probe and pathway time, potentially promoting viral acquisition. TuMV also directly influences aphid probing behavior. Viruliferous aphids had reduced pathway time, increased cell penetration frequency, increased intracellular probing time, increased salivation frequency, and ingested less sap than non-viruliferous aphids, primed for viral infection. Although oilseed rape cultivars can also influence aphid behavior, the main effect of cultivars was not significant on TuMV-infected plants.

Roles of Bacterial Symbionts in Transmission of Plant Virus by Hemipteran Vectors

The majority of plant viruses are transmitted by hemipteran insects. Bacterial symbionts in hemipteran hosts have a significant impact on the host life, physiology and ecology. Recently, the involvement of bacterial symbionts in hemipteran vector-virus and vector-plant interactions has been documented. Thus, the exploitation and manipulation of bacterial symbionts have great potential for plant viral disease control. Herein, we review the studies performed on the impact of symbiotic bacteria on plant virus transmission, including insect-bacterial symbiont associations, the role of these bacterial symbionts in viral acquisition, stability and release during viral circulation in insect bodies, and in viral vertical transmission. Besides, we prospect further studies aimed to understand tripartite interactions of the virus-symbiotic microorganisms-insect vector.

The molecular mechanism of efficient transmission of plant viruses in variable virus–vector–plant interactions

Plant viruses are mainly transmitted by insect vectors in the non-persistent, semi-persistent, or persistent modes. In the non-persistent mode, plant viruses are retained in the stylets of their insect vectors. In the semi-persistent mode, plant viruses are carried to vector foreguts or salivary glands, but they cannot spread to salivary glands. In the persistent mode, plant viruses are retained in vector guts and can spread to salivary glands. In the non-persistent and semi-persistent modes, plant viruses are retained for a short time and cannot enter the hemolymph of insect vectors, whereas in the persistent mode, plant viruses are retained for a relatively long time and can be found in the hemolymph. Here, we reviewed recent studies that uncovered molecular mechanisms of how plant viruses manipulate host traits for efficient transmission by insect vectors. Normally, plants that are infected with viruses, regardless of the transmission mode, tend to release more attractive volatiles to vectors. However, plant defensive systems are regulated differently by viruses in these three modes. In the non-persistent mode, virus infections significantly induce plant defense responses, which probably trigger vectors (e.g., winged aphids) to disperse and transmit viruses in a short time. In the semi-persistent mode, virus infections frequently suppress plant defense responses, resulting in an increase of vector population and facilitating viral transmissions during vector outbreaks. In the persistent mode, virus infections reduce plant defense responses and manipulate plant traits to become suitable feeding sites in a relatively long period of time. Understanding the underlying mechanisms of virus–vector–plant interactions will lay a foundation for preventing virus transmission.

Coinfection by Two Begomoviruses Aggravates Plant Symptoms But Does Not Influence the Performance and Preference of Insect Vector Bemisia tabaci (Hemiptera: Aleyrodidae).

In nature, a plant can be infected by multiple viruses simultaneously. However, the effects of coinfection on plant-vector interactions are less well studied. Two begomoviruses of the family Geminiviridae, Tomato yellow leaf curl virus (TYLCV) and Tomato yellow leaf curl China virus (TYLCCNV), occur sympatrically in China. Each of them is reported to increase the performance of whitefly vector via manipulation of plant traits. In this study, we examined the effects of coinfection by the two viruses TYLCV and TYLCCNV on plant-whitefly interactions, compared to that infected by a single virus. We found that plants infected by two viruses showed aggravated symptoms but the performance and preference of whiteflies were not altered significantly compared to singly-infected plants. Coinfection suppressed the transcription of genes involved in jasmonic acid (JA) signaling pathway in plants, but showed no significant difference to single-virus infected plants. These findings suggest that although TYLCV and TYLCCNV may synergistically induce plant symptoms, they did not manipulate synergistically plant-mediated responses to the insect vector.

The Epidemiology of Plant Virus Disease: Towards a New Synthesis.

Epidemiology is the science of how disease develops in populations, with applications in human, animal and plant diseases. For plant diseases, epidemiology has developed as a quantitative science with the aims of describing, understanding and predicting epidemics, and intervening to mitigate their consequences in plant populations. Although the central focus of epidemiology is at the population level, it is often necessary to recognise the system hierarchies present by scaling down to the individual plant/cellular level and scaling up to the community/landscape level. This is particularly important for diseases caused by plant viruses, which in most cases are transmitted by arthropod vectors. This leads to range of virus-plant, virus-vector and vector-plant interactions giving a distinctive character to plant virus epidemiology (whilst recognising that some fungal, oomycete and bacterial pathogens are also vector-borne). These interactions have epidemiological, ecological and evolutionary consequences with implications for agronomic practices, pest and disease management, host resistance deployment, and the health of wild plant communities. Over the last two decades, there have been attempts to bring together these differing standpoints into a new synthesis, although this is more apparent for evolutionary and ecological approaches, perhaps reflecting the greater emphasis on shorter often annual time scales in epidemiological studies. It is argued here that incorporating an epidemiological perspective, specifically quantitative, into this developing synthesis will lead to new directions in plant virus research and disease management. This synthesis can serve to further consolidate and transform epidemiology as a key element in plant virus research.

Virus Accumulation and Whitefly Performance Modulate the Role of Alternate Host Species as Inoculum Sources of Tomato Yellow Leaf Curl Virus.

Evaluating alternate hosts that facilitate the persistence of a virus in the landscape is key to understanding virus epidemics. In this study, we explored the role of several plant species (eggplant, pepper, and Palmer amaranth) as inoculum sources of tomato yellow leaf curl virus (TYLCV) and as reservoirs for its insect vector, Bemisia tabaci (Gennadius). All inoculated species were infected with TYLCV, but whiteflies acquired fewer viral copies via feeding from pepper and eggplant than from tomato and Palmer amaranth. Further, back-transmission assays to recipient tomato resulted in TYLCV infection only when TYLCV was acquired from Palmer amaranth or tomato. Analysis suggested that the role of plant species as TYLCV inoculum sources may be determined by the accumulation of viral copies in the plant, and consequently in the insect vector. In addition, results showed that all three alternate species could sustain populations of B. tabaci, while differentially influencing fitness of whiteflies. Eggplant was a superior host for whiteflies, whereas whitefly survival was compromised on pepper. Together, we demonstrate that both plant-virus and plant-vector interactions could influence the role of an alternate host in TYLCV epidemics, and in our region of study we highlight the potential risk of hosts such as Palmer amaranth in the spread of TYLCV.

Specific and Spillover Effects on Vectors Following Infection of Two RNA Viruses in Pepper Plants.

Simple SummaryMixed infection of plant viruses is pervasive in agricultural systems. Mixed infection-induced host effects on vector/s fitness are often not well characterized. This study examined how infection of cucumber mosaic virus (CMV) and/or tomato spotted wilt orthotospovirus (TSWV) in pepper plants influenced the preference and fitness of their vectors Myzus persicae and Frankliniella fusca, respectively. Mixed infection resulted in more severe symptoms when compared with single infection. An antagonistic interaction between CMV and TSWV was also observed, wherein CMV titer was suppressed in mixed-infected compared with singly-infected plants. At instances, mixed-infected plants negatively impacted vector/s fitness more evidently than singly-infected plants. In others, the effects of mixed infection on vector preference or fitness did not vary from single infection. Overall, mixed infection in pepper plants did not enhance vector/s fitness and was not conductive to facilitate CMV and/or TSWV transmission and epidemics. The effects of CMV/TSWV infection extended to specific and non-specific vectors. CMV infection enhanced thrips fitness and TSWV infection enhanced aphid fitness. These spillover effects could result in crosstalk between vectors and viruses in the pathosystem, which in turn could lead to mixed infection. The driving forces of these interactions and the outcomes of these interactions remain to be characterized.Mixed infection of plant viruses is ubiquitous in nature and can affect virus–plant–vector interactions differently than single virus infection. While several studies have examined virus–virus interactions involving mixed virus infection, relatively few have examined effects of mixed virus infection on vector preference and fitness, especially when multiple vectors are involved. This study explored how single and mixed viral infection of a non-persistently transmitted cucumber mosaic virus (CMV) and propagative and persistently-transmitted tomato spotted wilt orthotospovirus (TSWV) in pepper, Capsicum annum L., influenced the preference and fitness of their vectors, the green peach aphid, Myzus persicae (Sulzer), and the tobacco thrips, Frankliniella fusca (Hinds), respectively. In general, mixed infected plants exhibited severe symptoms compared with individually infected plants. An antagonistic interaction between the two viruses was observed when CMV titer was reduced following mixed infection with TSWV in comparison with the single infection. TSWV titer did not differ between single and mixed infection. Myzus persicae settling preference and median developmental were not significantly different between CMV and/or TSWV-infected and non-infected plants. Moreover, M. persicae fecundity did not differ between CMV-infected and non-infected pepper plants. However, M. persicae fecundity was substantially greater on TSWV-infected plants than non-infected plants. Myzus persicae fecundity on mixed-infected plants was significantly lower than on singly-infected and non-infected plants. Frankliniella fusca fecundity was higher on CMV and/or TSWV-infected pepper plants than non-infected pepper plants. Furthermore, F. fusca-induced feeding damage was higher on TSWV-infected than on CMV-infected, mixed-infected, or non-infected pepper plants. Overall, our results indicate that the effects of mixed virus infection on vectors were not different from those observed following single virus infection. Virus-induced host phenotype-modulated effects were realized on both specific and non-specific vectors, suggesting crosstalk involving all vectors and viruses in this pathosystem. The driving forces of these interactions need to be further examined. The effects of interactions between two viruses and two vectors towards epidemics of one or both viruses also need to be examined.

The Oxylipin Signaling Pathway Is Required for Increased Aphid Attraction and Retention on Virus-Infected Plants.

Many studies have shown that virus infection alters phytohormone signaling and insect vector contact with hosts. Increased vector contact and movement among plants should increase virus survival and host range. In this study we examine the role of virus-induced changes in phytohormone signaling in plant-aphid interactions, using Pea enation mosaic virus (PEMV), pea aphids (Acyrthosiphon pisum), and pea (Pisum sativum) as a model. We observed that feeding by aphids carrying PEMV increases salicylic acid and jasmonic acid accumulation in pea plants compared to feeding by virus-free aphids. To determine if induction of the oxylipin jasmonic acid is critical for aphid settling, attraction, and retention on PEMV-infected plants, we conducted insect bioassays using virus-induced gene silencing (VIGS), an oxylipin signaling inducer, methyl jasmonate (MeJA), and a chemical inhibitor of oxylipin signaling, phenidone. Surprisingly, there was no impact of phenidone treatment on jasmonic acid or salicylic acid levels in virus-infected plants, thoughaphid attraction and retention werealtered. These results suggest that the observed impacts of phenidone on aphid attraction to and retention on PEMV-infected plants are independent of the jasmonic acid and salicylic acid pathway but may be mediated by another component of the oxylipin signaling pathway. These results shed light on the complexity of viral manipulation of phytohormone signaling and vector-plant interactions.

A polerovirus, Potato leafroll virus, alters plant-vector interactions using three viral proteins.

Potato leafroll virus (PLRV), genus Polerovirus, family Luteoviridae, is a major pathogen of potato worldwide. PLRV is transmitted among host plants by aphids in a circulative-nonpropagative manner. Previous studies have demonstrated that PLRV infection increases aphid fecundity on, and attraction to, infected plants as compared to controls. However, the molecular mechanisms mediating this relationship are still poorly understood. In this study, we measured the impact of PLRV infection on plant-aphid interactions and plant chemistry in two hosts: Solanum tuberosum and Nicotiana benthamiana. Our study demonstrates that PLRV infection attenuates the induction of aphid-induced jasmonic acid and ethylene in S. tuberosum and N. benthamiana. Using transient expression experiments, insect bioassays and chemical analysis, we show that expression of three PLRV proteins (P0, P1, and P7) mediate changes in plant-aphid interactions and inhibition of aphid-induced jasmonic acid and ethylene in N. benthamiana. This study enhances our understanding of the plant-vector-pathogen interface by elucidating new mechanisms by which plant viruses transmitted in a circulative manner can manipulate plant hosts.

The Power of Electropenetrography in Enhancing Our Understanding of Host Plant-Vector Interactions.

The invasive Asian citrus psyllid, Diaphorina citri (Hemiptera: Liviidae), is the primary vector of the phloem-infecting bacterium, Candidatus Liberibacter asiaticus. Candidatus L. asiaticus is the putative causal agent of Huanglongbing (HLB) disease, a destructive disease of Citrus. While many Citrus species are susceptible to D. citri probing and HLB disease, there are marked behavioral differences in D. citri probing responses and Ca. Liberibacter asiaticus infection severity among Citrus species. Using four mandarin hybrid selections and pummelo plants variably resistant to D. citri probing, oviposition, and survival, we explored probing differences using electropenetrography (EPG), conducted an oviposition and survival study, and determined host plant metabolites using gas-chromatography mass-spectroscopy (GC-MS). We found thirty-seven D. citri probing variables to be significantly different among tested mandarin selections and pummelo, in addition to differential oviposition and survivorship abilities on tested plants. We found sixty-three leaf metabolites with eight being significantly different among tested mandarin selections and pummelo. Detailed analysis of probing behavior, oviposition, survivorship, and host plant metabolite concentrations reveals the complex, layered resistance mechanisms utilized by resistant Citrus against D. citri probing. EPG is a powerful technology for screening Asian citrus psyllid resistant Citrus to elucidate host plant-vector interactions, with an aim to minimize vector probing and eliminate the spread of the bacterial pathogen, Ca. L. asiaticus.

Pathogenic modification of plants enhances long-distance dispersal of nonpersistently transmitted viruses to new hosts.

Aphids spread the majority of plant viruses through nonpersistent transmission (NPT), whereby virus particles attach transiently to these insects’ probing mouthparts. Virus acquisition from infected plants and inoculation to healthy host plants is favored when aphids briefly probe plant epidermal cells. It is well established that NPT virus infection can alter plant–vector interactions, and, moreover, such pathogen modifications are found in a range of plant and animal systems. In particular, viruses can make plants more attractive to aphids but inhibit aphid settling on infected plants. It is hypothesized that this viral “reprogramming” of plants promotes virus acquisition and encourages dispersal of virus‐bearing aphids to fresh hosts. In contrast, it is hypothesized that virus‐induced biochemical changes encouraging prolonged feeding on infected hosts inhibit NPT. To understand how these virus‐induced modifications affect epidemics, we developed a modeling framework accounting for important but often neglected factors, including feeding behaviors (probing or prolonged feeding) and distinct spatial scales of transmission (as conditioned by wingless or winged aphids). Analysis of our models confirmed that when viruses inhibit aphid settling on infected plants this initially promotes virus transmission. However, initially enhanced transmission is self‐limiting because it decreases vector density. Another important finding is that virus‐induced changes encouraging settling will stimulate birth of winged aphids, which promotes epidemics of NPT viruses over greater distances. Thus our results illustrate how plant virus modifications influence epidemics by altering vector distribution, density, and even vector form. Our insights are important for understanding how pathogens in general propagate through natural plant communities and crops.

Transmission Efficiency of Xylella fastidiosa subsp. pauca Sequence Types by Sharpshooter Vectors after In Vitro Acquisition.

Xylella fastidiosa subsp. pauca is genetically diverse and has many vector species. However, there is limited information on vector specificity and efficiency for different sequence types (STs) within the pathogen subspecies. Both STs of X. fastidiosa and vectors differ in their associations with plants; therefore, assessment of vector competence should include the standardized vector acquisition ability of bacteria from artificial diets. This work aimed to adapt and validate an in vitro acquisition system for strains of X. fastidiosa that cause citrus variegated chlorosis, and to compare the transmission efficiency of STs of subsp. pauca by different species of sharpshooter vector. First, acquisition and transmission of ST13 by Bucephalogonia xanthophis and Macugonalia leucomelas was tested using an artificial diet with bacteria grown on minimum defined medium (X. fastidiosa medium) with or without 1% galacturonic acid (GA). Subsequently, four sharpshooter species (B. xanthophis, M. leucomelas, M. cavifrons, and Sibovia sagata) were compared as vectors of ST13 acquired from artificial diets, and four STs of subsp. pauca (11, 13, 65, and 70) were tested for acquisition and transmission by M. leucomelas. The artificial system allowed efficient acquisition and transmission of ST13 to plants, with no differences between the media tested. ST13 was transmitted more efficiently by B. xanthophis and M. leucomelas when compared with M. cavifrons and S. sagata. Different STs influenced acquisition and transmission rates by M. leucomelas. The differences in vector competence, despite the standardized acquisition system, suggest that ST-vector foregut or vector-plant interactions may influence bacterial acquisition, retention and inoculation by the insect.

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 reinforce the idea that vector manipulation requires coevolution between plant, virus and vector.

Effects of single and mixed infections of Bean pod mottle virus and Soybean mosaic virus on host‐plant chemistry and host–vector interactions

Summary Co‐infection by vector‐borne plant viruses is common, yet few studies have explored the effects of mixed infections on host‐plant phenotypes or plant–vector interactions. We documented the effects of single and mixed infection by Bean pod mottle virus (BPMV) and Soybean mosaic virus (SMV) on key biochemical plant traits and the behaviour and performance of virus vectors (BPMV: Epilachna varivestis, SMV: Aphis glycines) in order to understand how virus‐induced changes in plant phenotypes might influence (i) the acquisition and transmission of each virus by its respective vector in single infections, (ii) the likelihood of secondary infection for plants singly infected with either virus and (iii) the implications of co‐infection for virus transmission by vectors. Single infection by either BPMV or SMV increased host‐plant palatability for E. varivestis, potentially enhancing vector acquisition of BPMV from BPMV‐infected plants as well as the risk of secondary BPMV infection in plants infected with SMV. However, co‐infected plants were no more palatable to beetle vectors than mock‐inoculated plants. BPMV infection had minimal impacts on A. glycines. SMV infection reduced A. glycines population growth, but increased aphid feeding preferences for infected plants, a pattern likely not conducive to the (non‐persistent) transmission of SMV. Co‐infection eliminated the negative effects of single SMV infection on aphid population growth, and aphids exhibited a feeding preference for co‐infected (relative to mock‐inoculated) plants. Our results demonstrate that virus effects on host phenotype and vector behaviour can be modified by the presence of a co‐infecting virus, with potentially important implications for disease transmission.

The effects of Gibberella zeae, Barley Yellow Dwarf Virus, and co-infection on Rhopalosiphum padi olfactory preference and performance

Insect-borne viruses promote several changes in plant phenotype, which can modify plant-vector interactions in favor of virus survival and dissemination. Although co-infections commonly occur in the field, little is known about their effects on interactions with the vector. The ecological interactions between Barley Yellow Dwarf Virus (BYDV) and its aphid vector, Rhopalosiphum padi, have been investigated extensively, but the vector’s behavior in more complex scenarios has yet to be examined. We assessed olfactory response and performance of R. padi to wheat singly and doubly infected by the pathogenic fungus Giberella zeae and BYDV. Non-viruliferous aphids preferred odors of BYDV-infected wheat over healthy wheat, as previously reported in the literature, and they were still preferentially attracted to BYDV-infected plant during co-infection. However, around 35% more non-viruliferous aphids chose healthy wheat over G. zeae-infected wheat. Viruliferous aphids did not show any preference to the treatments. BYDV-infected wheat was a superior host than healthy wheat for the aphids whose population increased in 25%. We observed a synergistic effect of the co-infected wheat, which was the best host for aphids, and promoted an elevation of 42% on population growth. Our results indicate that co-infection might be beneficial for virus spread as does not interfere with aphid olfactory preference and provides greater colony growth than in singly infected plants.

Disruption of Ethylene Responses by Turnip mosaic virus Mediates Suppression of Plant Defense against the Green Peach Aphid Vector

Plants employ diverse responses mediated by phytohormones to defend themselves against pathogens and herbivores. Adapted pathogens and herbivores often manipulate these responses to their benefit. Previously, we demonstrated that Turnip mosaic virus (TuMV) infection suppresses callose deposition, an important plant defense induced in response to feeding by its aphid vector, the green peach aphid (Myzus persicae), and increases aphid fecundity compared with uninfected control plants. Further, we determined that production of a single TuMV protein, Nuclear Inclusion a-Protease (NIa-Pro) domain, was responsible for changes in host plant physiology and increased green peach aphid reproduction. To characterize the underlying molecular mechanisms of this phenomenon, we examined the role of three phytohormone signaling pathways, jasmonic acid, salicylic acid, and ethylene (ET), in TuMV-infected Arabidopsis (Arabidopsis thaliana), with or without aphid herbivory. Experiments with Arabidopsis mutants ethylene insensitive2 and ethylene response1, and chemical inhibitors of ET synthesis and perception (aminoethoxyvinyl-glycine and 1-methylcyclopropene, respectively), show that the ET signaling pathway is required for TuMV-mediated suppression of Arabidopsis resistance to the green peach aphid. Additionally, transgenic expression of NIa-Pro in Arabidopsis alters ET responses and suppresses aphid-induced callose formation in an ET-dependent manner. Thus, disruption of ET responses in plants is an additional function of NIa-Pro, a highly conserved potyvirus protein. Virus-induced changes in ET responses may mediate vector-plant interactions more broadly and thus represent a conserved mechanism for increasing transmission by insect vectors across generations.

Plant-mediated whitefly–begomovirus interactions: research progress and future prospects

Plant-mediated interactions between begomoviruses and whiteflies exert important influences on the population dynamics of vectors and the epidemiology of plant diseases. In this article, we synthesize the relevant literature to identify patterns to the interactions. We then review studies on the ecological, biochemical and molecular mechanisms underlying the interactions and finally elaborate on the most interesting issues for future research. The interactions between begomoviruses and the insect vector, the whitefly Bemisia tabaci, via their shared host plants can be mutualistic, neutral or negative. However, in contrast to a pattern of improved performance of vectors on virus-infected plants that has been observed with persistently transmitted RNA viruses, the number of cases exhibiting mutualistic, neutral or negative effects in the indirect interactions between begomoviruses and whiteflies appear evenly distributed. With regard to the mechanisms of plant-mediated positive effects on whiteflies, two case studies indicate that suppression of plant defence and/or alteration in plant nutrition as a result of virus infection can be important. Our review shows that we are only just beginning to understand the tripartite interactions between begomoviruses, whiteflies and plants. Future efforts in this area should try to expand the number and diversity of pathosystems for investigation to reveal the patterns of interactions, to investigate the molecular and biochemical mechanisms of the interactions using a multidisciplinary approach, and to examine the virus-plant-vector interactions in the field and in natural plant communities.

Volatile phytochemicals as mosquito semiochemicals

Plant biochemical processes result in the release of an array of volatile chemical substances into the environment, some of which are known to play important plant fitness enhancing functions, such as attracting pollinators, thermal tolerance of photosynthesis, and defense against herbivores. Cunningly, phytophagous insects have evolved mechanisms to utilize these volatiles to their own advantage, either to colonize a suitable host for feeding, reproduction and oviposition or avoid an unsuitable one. The volatile compounds involved in plant–insect chemical interactions have been widely exploited in the management of agricultural pests. On the other hand, use of plant volatiles in the management of medically important insects is limited, mainly due to paucity of information on their role in disease vector–plant interactions. To date, a total of 29 plant volatile compounds from various chemical classes, including phenols, aldehydes, alcohols, ketones and terpenes, have been identified as mosquito semiochemicals. In this review, we present highlights of mosquito–plant interactions, the available evidence of nectar feeding, with particular emphasis on sources of plant attractants, methods of plant volatile collection and the candidate plant volatile compounds that attract mosquitoes to nectar sources. We also highlight the potential application of these phytochemical attractants in integrated mosquito management.

New horizon in the research on plant-virus-vector interaction

Understanding the mechanisms controlling vector-transmission of plant viruses requires integrating information from at least three different viewpoints: virus-vector interactions, plant-vector interactions and virus-plant interactions. While some of these aspects have been covered by past and present investigations, others have been bypassed completely, due either to technical bottlenecks or conceptual lacunas. Here, we highlight recent advances and needs in hitherto poorly documented aspects of vector transmission, such as characterization of the vector molecules responsible for initial viral recognition, and the role of vector saliva in inoculation and initial onset of infection in a new plant. We also propose and discuss some novel conceptual and complementary questions that are opening up fascinating new horizons in this field. We explore the possible existence of viral morphs with specific properties that facilitate acquisition by vectors, and discuss the dynamics/genetics of such viral subpopulations, which could differentiate and specialize in different host compartments.