Exosomes mediate horizontal transmission of viral pathogens from insect vectors to plant phloem.
Ontology highlight
ABSTRACT:
SUBMITTER: Chen Q
PROVIDER: S-EPMC8253596 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Bacteria in the genus Rickettsia, best known as vertebrate pathogens vectored by blood-feeding arthropods, can also be found in phytophagous insects. The presence of closely related bacterial symbionts in evolutionarily distant arthropod hosts presupposes a means of horizontal transmission, but no mechanism for this transmission has been described. Using a combination of experiments with live insects, molecular analyses and microscopy, we found that Rickettsia were transferred from an insect host (the whitefly Bemisia tabaci) to a plant, moved inside the phloem, and could be acquired by other whiteflies. In one experiment, Rickettsia was transferred from the whitefly host to leaves of cotton, basil and black nightshade, where the bacteria were restricted to the phloem cells of the plant. In another experiment, Rickettsia-free adult whiteflies, physically segregated but sharing a cotton leaf with Rickettsia-plus individuals, acquired the Rickettsia at a high rate. Plants can serve as a reservoir for horizontal transmission of Rickettsia, a mechanism which may explain the occurrence of phylogenetically similar symbionts among unrelated phytophagous insect species. This plant-mediated transmission route may also exist in other insect-symbiont systems and, since symbionts may play a critical role in the ecology and evolution of their hosts, serve as an immediate and powerful tool for accelerated evolution.
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Project description:Arthropod-borne viruses (arboviruses) can be maternally transmitted by female insects to their offspring, however, it is unknown whether male sperm can directly interact with the arbovirus and mediate its paternal transmission. Here we report that an important rice arbovirus is paternally transmitted by the male leafhoppers by hitchhiking with the sperm. The virus-sperm binding is mediated by the interaction of viral capsid protein and heparan sulfate proteoglycan on the sperm head surfaces. Mating experiments reveal that paternal virus transmission is more efficient than maternal transmission. Such paternal virus transmission scarcely affects the fitness of adult males or their offspring, and plays a pivotal role in maintenance of viral population during seasons unfavorable for rice hosts in the field. Our findings reveal that a preferred mode of vertical arbovirus transmission has been evolved by hitchhiking with insect sperm without disturbing sperm functioning, facilitating the long-term viral epidemic and persistence in nature.
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Project description:Rice gall dwarf virus (RGDV) and its leafhopper vector Recilia dorsalis are plant phloem-inhabiting pests. Currently, how the delivery of plant viruses into plant phloem via piercing-sucking insects modulates callose deposition to promote viral transmission remains poorly understood. Here, we initially demonstrated that nonviruliferous R. dorsalis preferred feeding on RGDV-infected rice plants than viruliferous counterpart. Electrical penetration graph assay showed that viruliferous R. dorsalis encountered stronger physical barriers than nonviruliferous insects during feeding, finally prolonging salivary secretion and ingestion probing. Viruliferous R. dorsalis feeding induced more defense-associated callose deposition on sieve plates of rice phloem. Furthermore, RGDV infection significantly increased the cytosolic Ca2+ level in rice plants, triggering substantial callose deposition. Such a virus-mediated insect feeding behavior change potentially impedes insects from continuously ingesting phloem sap and promotes the secretion of more infectious virions from the salivary glands into rice phloem. This is the first study demonstrating that the delivery of a phloem-limited virus by piercing-sucking insects into the plant phloem activates the defense-associated callose deposition to enhance viral transmission.
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Project description:Drought is a major threat to crop production worldwide and is accentuated by global warming. Plant responses to this abiotic stress involve physiological changes overlapping, at least partially, the defense pathways elicited both by viruses and their herbivore vectors. Recently, a number of theoretical and empirical studies anticipated the influence of climate changes on vector-borne viruses of plants and animals, mainly addressing the effects on the virus itself or on the vector population dynamics, and inferring possible consequences on virus transmission. Here, we directly assess the effect of a severe water deficit on the efficiency of aphid-transmission of the Cauliflower mosaic virus (CaMV) or the Turnip mosaic virus (TuMV). For both viruses, our results demonstrate that the rate of vector-transmission is significantly increased from water-deprived source plants: CaMV transmission reproducibly increased by 34% and that of TuMV by 100%. In both cases, the enhanced transmission rate could not be explained by a higher virus accumulation, suggesting a more complex drought-induced process that remains to be elucidated. The evidence that infected plants subjected to drought are much better virus sources for insect vectors may have extensive consequences for viral epidemiology, and should be investigated in a wide range of plant-virus-vector systems.
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Project description:Small, mobile insects are notoriously challenging to track across landscapes and manage in agricultural fields. However, genetic differentiation among insect populations and host plants acquired through host-associated differentiation could be exploited to infer movement within crop systems and damage potential. Although many insects exhibit host-associated differentiation, management strategies for insect vectors of plant pathogens assume a homogenous population. Nevertheless, phenotypic changes derived from host-associated differentiation could manifest in altered behavior or physiology affecting the likelihood of vector-pathogen-plant interactions, or the subsequent efficiency of pathogen transmission. We used SNPs to assess genotypic structure and host-associated differentiation in the cowpea aphid, Aphis craccivora Koch (Hemiptera: Aphididae). To do so, we sampled A. craccivora across the Midwestern United States. from two host plants, alfalfa (Medicago sativa) and black locust (Robinia pseudoacacia)-putative source populations for winged migrants. Simultaneously, we sampled winged A. craccivora landing in pumpkin fields where they transmit viruses. Structure analyses supported host-associated differentiation by identifying two major genotypic groups: an alfalfa group containing a single multilocus genotype and a locust group containing all others. Winged locust-group aphids landed at a much greater magnitude within focal fields during year 2 than year 1, while those in the alfalfa group remained fairly consistent. Spatial autocorrelation analyses indicated locust-group aphid movement was characterized by small-scale dispersal during year 2, likely originating from populations within 10 km. We also detected strong temporal differences in colonization from the two host plants. Early in the summer, most winged aphids (79.4%) derived from the locust group, whereas late in the summer more (58.3%) were from the alfalfa group. Because early crop growth stages are more susceptible to damage from aphid-vectored viruses, these data implicate locust as the more important source and illustrate how host-associated differentiation can be used to track dispersal and inform management of heterogeneous pest populations.
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Project description:Phytoplasmas (Mollicutes, Acholeplasmataceae), vector-borne obligate bacterial plant parasites, infect nearly 1,000 plant species and unknown numbers of insects, mainly leafhoppers (Hemiptera, Deltocephalinae), which play a key role in transmission and epidemiology. Although the plant-phytoplasma-insect association has been evolving for >300 million years, nearly all known phytoplasmas have been discovered as a result of the damage inflicted by phytoplasma diseases on crops. Few efforts have been made to study phytoplasmas occurring in noneconomically important plants in natural habitats. In this study, a subsample of leafhopper specimens preserved in a large museum biorepository was analyzed to unveil potential new associations. PCR screening for phytoplasmas performed on 227 phloem-feeding leafhoppers collected worldwide from natural habitats revealed the presence of 6 different previously unknown phytoplasma strains. This indicates that museum collections of herbivorous insects represent a rich and largely untapped resource for discovery of new plant pathogens, that natural areas worldwide harbor a diverse but largely undiscovered diversity of phytoplasmas and potential insect vectors, and that independent epidemiological cycles occur in such habitats, posing a potential threat of disease spillover into agricultural systems. Larger-scale future investigations will contribute to a better understanding of phytoplasma genetic diversity, insect host range, and insect-borne phytoplasma transmission and provide an early warning for the emergence of new phytoplasma diseases across global agroecosystems.
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Project description:Horizontal transfer (HT) of DNA is an important factor shaping eukaryote evolution. Although several hundreds of eukaryote-to-eukaryote HTs of transposable elements (TEs) have been reported, the vectors underlying these transfers remain elusive. Here, we show that multiple copies of two TEs from the cabbage looper (Trichoplusia ni) transposed in vivo into genomes of the baculovirus Autographa californica multiple nucleopolyhedrovirus (AcMNPV) during caterpillar infection. We further demonstrate that both TEs underwent recent HT between several sympatric moth species (T. ni, Manduca sexta, Helicoverpa spp.) showing different degrees of susceptibility to AcMNPV. Based on two independent population genomics data sets (reaching a total coverage >330,000X), we report a frequency of one moth TE in ~8,500 AcMNPV genomes. Together, our results provide strong support for the role of viruses as vectors of TE HT between animals, and they call for a systematic evaluation of the frequency and impact of virus-mediated HT on the evolution of host genomes.
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Project description:Most plant viruses are vectored by insects and the interactions of virus-plant-vector have important ecological and evolutionary implications. Insect vectors often perform better on virus-infected plants. This indirect mutualism between plant viruses and insect vectors promotes the spread of virus and has significant agronomical effects. However, few studies have investigated how plant viruses manipulate plant defenses and promote vector performance. Begomoviruses are a prominent group of plant viruses in tropical and sub-tropical agro-ecosystems and are transmitted by whiteflies. Working with the whitefly Bemisia tabaci, begomoviruses and tobacco, we revealed that C2 protein of begomoviruses lacking DNA satellites was responsible for the suppression of plant defenses against whitefly vectors. We found that infection of plants by tomato yellow leaf curl virus (TYLCV), one of the most devastating begomoviruses worldwide, promoted the survival and reproduction of whitefly vectors. TYLCV C2 protein suppressed plant defenses by interacting with plant ubiquitin. This interaction compromised the degradation of JAZ1 protein, thus inhibiting jasmonic acid defense and the expression of MYC2-regulated terpene synthase genes. We further demonstrated that function of C2 protein among begomoviruses not associated with satellites is well conserved and ubiquitination is an evolutionarily conserved target of begomoviruses for the suppression of plant resistance to whitefly vectors. Taken together, these results demonstrate that ubiquitination inhibition by begomovirus C2 protein might be a general mechanism in begomovirus, whitefly and plant interactions.
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Project description:Many viral pathogens are persistently transmitted by insect vectors and cause agricultural or health problems. Generally, an insect vector can use autophagy as an intrinsic antiviral defense mechanism against viral infection. Whether viruses can evolve to exploit autophagy to promote their transmission by insect vectors is still unknown. Here, we show that the autophagic process is triggered by the persistent replication of a plant reovirus, rice gall dwarf virus (RGDV) in cultured leafhopper vector cells and in intact insects, as demonstrated by the appearance of obvious virus-containing double-membrane autophagosomes, conversion of ATG8-I to ATG8-II and increased level of autophagic flux. Such virus-containing autophagosomes seem able to mediate nonlytic viral release from cultured cells or facilitate viral spread in the leafhopper intestine. Applying the autophagy inhibitor 3-methyladenine or silencing the expression of Atg5 significantly decrease viral spread in vitro and in vivo, whereas applying the autophagy inducer rapamycin or silencing the expression of Torc1 facilitate such viral spread. Furthermore, we find that activation of autophagy facilitates efficient viral transmission, whereas inhibiting autophagy blocks viral transmission by its insect vector. Together, these results indicate a plant virus can induce the formation of autophagosomes for carrying virions, thus facilitating viral spread and transmission by its insect vector. We believe that such a role for virus-induced autophagy is common for vector-borne persistent viruses during their transmission by insect vectors.
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Project description:Abstract Recent studies suggest that endosymbionts of herbivore insects can be horizontally transferred to other herbivores feeding on the same host plants, whereby the plant acts as an intermediate stage in the chain of transmission. If this mechanism operates, it is also expected that insect communities sharing the same host plant will have higher chances to share their endosymbionts. In this study, we use a high-throughput 16S rRNA metabarcoding approach to investigate the presence, diversity, and potential sharing of endosymbionts in several species of leaf beetles (Coleoptera: Chrysomelidae) of a local community specialized on an alder diet in North America. Rickettsia and Wolbachia were predominant in the sample, with strong evidence for each species having their own dominant infection, of either or both types of bacteria. However, all species shared a much lower proportion of a particular Wolbachia type, compatible with the same strain dominant in one of the species of leaf beetles. Crucially, the same 16S rRNA haplotype of Wolbachia was found on alder leaf extracts. The combined evidence and the absence of this strain in a syntopic species of leaf beetle feeding on a different host plant support the hypothesis that at least the initial stages of the mechanism that would allow horizontal transmission of endosymbionts across species feeding on the same plant is possible. The accessibility and characteristics of endosymbiont associations of this system make it suitable for deeper analyses of their diversity and transmission in natural conditions.
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