scholarly journals Comparative plant transcriptome profiling of Arabidopsis and Camelina infested with Myzus persicae aphids acquiring circulative and non-circulative viruses reveals virus- and plant-specific alterations relevant to aphid feeding behavior and transmission

2022 ◽  
Author(s):  
Quentin Chesnais ◽  
Victor Golyaev ◽  
Amadine Velt ◽  
Camille Rustenholz ◽  
Véronique Brault ◽  
...  
Keyword(s):  
Feeding Behavior ◽  
Myzus Persicae ◽  
Virus Transmission ◽  
Transcriptome Profiling ◽  
Defense Responses ◽  
Plant Viruses ◽  
Transmission Mode ◽  
Insect Vector ◽  
Plant Host ◽  
Aphid Vector

Background: Evidence accumulates that plant viruses alter host-plant traits in ways that modify their insect vectors' behavior. These alterations often enhance virus transmission, which has led to the hypothesis that these effects are manipulations caused by viral adaptation. However, the genetic basis of these indirect, plant-mediated effects on vectors and their dependence on the plant host and the mode of virus transmission is hardly known. Results: Transcriptome profiling of Arabidopsis thaliana and Camelina sativa plants infected with turnip yellows virus (TuYV) or cauliflower mosaic virus (CaMV) and infested with the common aphid vector Myzus persicae revealed strong virus- and host-specific differences in the gene expression patterns. CaMV infection caused more severe effects on the phenotype of both plant hosts than did TuYV infection, and the severity of symptoms correlated strongly with the proportion of differentially expressed genes, especially photosynthesis genes. Accordingly, CaMV infection modified aphid behavior and fecundity stronger than did infection with TuYV. Conclusions: Overall, infection with CaMV — relying on the non-circulative transmission mode — tends to have effects on metabolic pathways with strong potential implications for insect-vector / plant-host interactions (e.g. photosynthesis, jasmonic acid, ethylene and glucosinolate biosynthetic processes), while TuYV — using the circulative transmission mode — alters these pathways only weakly. These virus-induced deregulations of genes that are related to plant physiology and defense responses might impact aphid probing and feeding behavior on both infected host plants, with potentially distinct effects on virus transmission. Keywords: Caulimovirus, polerovirus, aphid vector, transmission, feeding behavior, insect-plant interactions, transcriptome profiling, RNA-seq.

scholarly journals Tenuivirususes a molecular bridge strategy to overcome insect midgut barriers for virus persistent transmission

2018 ◽  
Author(s):  
Gang Lu ◽  
Shuo Li ◽  
Changwei Zhou ◽  
Xin Qian ◽  
Qing Xiang ◽  
...  
Keyword(s):  
Brown Planthopper ◽  
Specific Interaction ◽  
Virus Transmission ◽  
Plant Viruses ◽  
Insect Vector ◽  
Terminal Protein ◽  
Insect Midgut ◽  
Helper Component ◽  
Vector Interaction ◽  
Molecular Bridge

AbstractMany persistent transmitted plant viruses, includingRice stripe tenuivirus(RSV), cause serious damages to crop productions in China and worldwide. Although many reports have indicated that successful insect-mediated virus transmission depends on proper virus–insect vector interactions, the mechanism(s) controlling interactions between viruses and insect vectors for virus persistent transmission remained poorly understood. In this study, we used RSV and its small brown planthopper (SBPH) vector as a working model to elucidate the molecular mechanism controlling RSV virion entrance into SBPH midgut for persistent transmission. We have now demonstrated that this non-envelopedTenuivirususes its non-structural glycoprotein NSvc2 as a helper component to bridge the specific interaction between virion and SBPH midgut cells, leading to overcome SBPH midgut barriers for virus persistent transmission. In the absence of this glycoprotein, purified RSV virion is not capable of entering SBPH midgut cells. In RSV-infected cells, glycoprotein NSvc2 is processed into two mature proteins: an amino-terminal protein NSvc2-N and a carboxyl-terminal protein NSvc2-C. We determined that NSvc2-N interacted with RSV virion and bound directly to midgut lumen surface via its N-glycosylation sites. Upon recognition by midgut cells, the midgut cells underwent endocytosis followed by compartmentalizing RSV virion and NSvc2 into early and then late endosomes. The acidic condition inside the late endosome triggered conformation change of NSvc2-C and caused cell membrane fusion via its highly conserved fusion loop motifs, leading to the release of RSV virion from endosome into cytosol. In summary, our results showed for the first time that a riceTenuivirususes a molecular bridge strategy to ensure proper interactions between virus and insect midgut for successful persistent transmission.Author summaryOver 75% of the known plant viruses are insect transmitted. Understanding how plant viruses interacted with their insect vectors during virus transmission is one of the key steps to manage virus diseases worldwide. Both the direct and indirect virus–insect vector interaction models have been proposed for virus non-persistent and semi-persistent transmission. However, the indirect virus–vector interaction mechanism during virus persistent transmission has not been reported previously. In this study, we developed a new reverse genetics technology and demonstrated that the circulative and propagative transmittedRice stripe tenuivirusutilizes a glycoprotein NSvc2 as a helper component to ensure a specific interaction betweenTenuivirusvirion and midgut cells of small brown planthopper (SBPH), leading to conquering the midgut barrier of SBPH. This is the first report of a helper component mediated-molecular bridge mechanism for virus persistent transmission. These new findings and our new model on persistent transmission expand our understanding of molecular mechanism(s) controlling virus–insect vector interactions during virus transmission in nature.

scholarly journals Transcriptome Profiling of ‘Candidatus Liberibacter asiaticus’ in Citrus and Psyllids

2022 ◽  
Author(s):  
Agustina De Francesco ◽  
Amelia H. Lovelace ◽  
Dipan Shaw ◽  
Min Qiu ◽  
Yuanchao Wang ◽  
...  
Keyword(s):  
Stress Responses ◽  
Expression Profiles ◽  
Bacterial Pathogen ◽  
Transcriptome Profiling ◽  
Insect Vector ◽  
Candidatus Liberibacter Asiaticus ◽  
Plant Host ◽  
Cell Wall Modification ◽  
Candidatus Liberibacter ◽  
Liberibacter Asiaticus

‘Candidatus Liberibacter asiaticus’ (Las) is an emergent bacterial pathogen that is associated with the devastating citrus huanglongbing (HLB). Vectored by the Asian citrus psyllid, Las colonizes the phloem tissue of citrus, causing severe damage to infected trees. So far, cultivating pure Las culture in axenic media has not been successful, and dual-transcriptome analyses aiming to profile gene expression in both Las and its hosts have a low coverage of the Las genome because of the low abundance of bacterial RNA in total RNA extracts from infected tissues. Therefore, a lack of understanding of the Las transcriptome remains a significant knowledge gap. Here, we used a bacterial cell enrichment procedure and confidently determined the expression profiles of approximately 84% of the Las genes. Genes that exhibited high expression in citrus include transporters, ferritin, outer membrane porins, specific pilins, and genes involved in phage-related functions, cell wall modification, and stress responses. We also found 106 genes to be differentially expressed in citrus versus Asian citrus psyllids. Genes related to transcription or translation and resilience to host defense response were upregulated in citrus, whereas genes involved in energy generation and the flagella system were expressed to higher levels in psyllids. Finally, we determined the relative expression levels of potential Sec-dependent effectors, which are considered as key virulence factors of Las. This work advances our understanding of HLB biology and offers novel insight into the interactions of Las with its plant host and insect vector.

scholarly journals Application of Genomics for Understanding Plant Virus-Insect Vector Interactions and Insect Vector Control

2016 ◽  
Vol 106 (10) ◽  
pp. 1213-1222 ◽  
Author(s):  
Navneet Kaur ◽  
Daniel K. Hasegawa ◽  
Kai-Shu Ling ◽  
William M. Wintermantel
Keyword(s):  
Gene Expression ◽  
Molecular Mechanisms ◽  
Virus Transmission ◽  
Plant Viruses ◽  
Significant Shift ◽  
Insect Vector ◽  
Insect Vectors ◽  
Genomic Technologies ◽  
Potential Applications ◽  
Generation Sequencing

The relationships between plant viruses and their vectors have evolved over the millennia, and yet, studies on viruses began <150 years ago and investigations into the virus and vector interactions even more recently. The advent of next generation sequencing, including rapid genome and transcriptome analysis, methods for evaluation of small RNAs, and the related disciplines of proteomics and metabolomics offer a significant shift in the ability to elucidate molecular mechanisms involved in virus infection and transmission by insect vectors. Genomic technologies offer an unprecedented opportunity to examine the response of insect vectors to the presence of ingested viruses through gene expression changes and altered biochemical pathways. This review focuses on the interactions between viruses and their whitefly or thrips vectors and on potential applications of genomics-driven control of the insect vectors. Recent studies have evaluated gene expression in vectors during feeding on plants infected with begomoviruses, criniviruses, and tospoviruses, which exhibit very different types of virus-vector interactions. These studies demonstrate the advantages of genomics and the potential complementary studies that rapidly advance our understanding of the biology of virus transmission by insect vectors and offer additional opportunities to design novel genetic strategies to manage insect vectors and the viruses they transmit.

scholarly journals Feeding Behavior and Virus-transmission Ability of Insect Vectors Exposed to Systemic Insecticides

Plants ◽  
2020 ◽  
Vol 9 (7) ◽  
pp. 895 ◽  
Author(s):  
Elisa Garzo ◽  
Aránzazu Moreno ◽  
María Plaza ◽  
Alberto Fereres
Keyword(s):  
Feeding Behavior ◽  
Virus Transmission ◽  
Plant Viruses ◽  
Crop Damage ◽  
Insect Vectors ◽  
Vector Borne Diseases ◽  
Systemic Insecticides ◽  
Turnip Yellows Virus ◽  
Vector Borne ◽  
Leaf Curl Virus

The majority of plant viruses depend on Hemipteran vectors for their survival and spread. Effective management of these insect vectors is crucial to minimize the spread of vector-borne diseases, and to reduce crop damage. The aim of the present study was to evaluate the effect of various systemic insecticides on the feeding behavior of Bemisia tabaci and Myzus persicae, as well as their ability to interfere with the transmission of circulative viruses. The obtained results indicated that some systemic insecticides have antifeeding properties that disrupt virus transmission by their insect vectors. We found that some of the tested insecticides significantly reduced phloem contact and sap ingestion by aphids and whiteflies, activities that are closely linked to the transmission of phloem-limited viruses. These systemic insecticides may play an important role in reducing the primary and secondary spread of tomato yellow leaf curl virus (TYLCV) and turnip yellows virus (TuYV), transmitted by B. tabaci and M. persicae, respectively.

scholarly journals Manipulation of Jasmonate Signaling by Plant Viruses and Their Insect Vectors

Viruses ◽  
2020 ◽  
Vol 12 (2) ◽  
pp. 148 ◽  
Author(s):  
Xiujuan Wu ◽  
Jian Ye
Keyword(s):  
Crop Yield ◽  
Plant Virus ◽  
Plant Viruses ◽  
Insect Vector ◽  
Insect Vectors ◽  
Plant Host ◽  
Effective Strategies ◽  
Secondary Damage ◽  
Molecular And Biochemical Mechanisms ◽  
Ja Signaling

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

scholarly journals Different Plant Viruses Induce Changes in Feeding Behavior of Specialist and Generalist Aphids on Common Bean That Are Likely to Enhance Virus Transmission

2020 ◽  
Vol 10 ◽  
Author(s):  
Francis O. Wamonje ◽  
Ruairí Donnelly ◽  
Trisna D. Tungadi ◽  
Alex M. Murphy ◽  
Adrienne E. Pate ◽  
...  
Keyword(s):  
Feeding Behavior ◽  
Common Bean ◽  
Virus Transmission ◽  
Plant Viruses

scholarly journals Route of a Multipartite Nanovirus across the Body of Its Aphid Vector

2020 ◽  
Vol 94 (9) ◽  
Author(s):  
Jérémy Di Mattia ◽  
Marie-Stéphanie Vernerey ◽  
Michel Yvon ◽  
Elodie Pirolles ◽  
Mathilde Villegas ◽  
...  
Keyword(s):  
Salivary Gland ◽  
Salivary Glands ◽  
Plant Viruses ◽  
The Body ◽  
Insect Vector ◽  
Vector Transmission ◽  
Aphid Vector ◽  
Vector Interaction ◽  
Salivary Gland Cells ◽  
Mode Of Transmission

ABSTRACT Vector transmission plays a primary role in the life cycle of viruses, and insects are the most common vectors. An important mode of vector transmission, reported only for plant viruses, is circulative nonpropagative transmission whereby the virus cycles within the body of its insect vector, from gut to salivary glands and saliva, without replicating. This mode of transmission has been extensively studied in the viral families Luteoviridae and Geminiviridae and is also reported for Nanoviridae. The biology of viruses within these three families is different, and whether the viruses have evolved similar molecular/cellular virus-vector interactions is unclear. In particular, nanoviruses have a multipartite genome organization, and how the distinct genome segments encapsidated individually transit through the insect body is unknown. Here, using a combination of fluorescent in situ hybridization and immunofluorescence, we monitor distinct proteins and genome segments of the nanovirus Faba bean necrotic stunt virus (FBNSV) during transcytosis through the gut and salivary gland cells of its aphid vector Acyrthosiphon pisum. FBNSV specifically transits through cells of the anterior midgut and principal salivary gland cells, a route similar to that of geminiviruses but distinct from that of luteoviruses. Our results further demonstrate that a large number of virus particles enter every single susceptible cell so that distinct genome segments always remain together. Finally, we confirm that the success of nanovirus-vector interaction depends on a nonstructural helper component, the viral protein nuclear shuttle protein (NSP), which is shown to be mandatory for viral accumulation within gut cells. IMPORTANCE An intriguing mode of vector transmission described only for plant viruses is circulative nonpropagative transmission, whereby the virus passes through the gut and salivary glands of the insect vector without replicating. Three plant virus families are transmitted this way, but details of the molecular/cellular mechanisms of the virus-vector interaction are missing. This is striking for nanoviruses that are believed to interact with aphid vectors in ways similar to those of luteoviruses or geminiviruses but for which empirical evidence is scarce. We here confirm that nanoviruses follow a within-vector route similar to that of geminiviruses but distinct from that of luteoviruses. We show that they produce a nonstructural protein mandatory for viral entry into gut cells, a unique phenomenon for this mode of transmission. Finally, noting that nanoviruses are multipartite viruses, we demonstrate that a large number of viral particles penetrate susceptible cells of the vector, allowing distinct genome segments to remain together.

scholarly journals In VitroEvidence Supports Membrane Alanyl Aminopeptidase N as a Receptor for a Plant Virus in the Pea Aphid Vector

2015 ◽  
Vol 89 (22) ◽  
pp. 11203-11212 ◽  
Author(s):  
Lucas B. Linz ◽  
Sijun Liu ◽  
Nanasaheb P. Chougule ◽  
Bryony C. Bonning
Keyword(s):  
Plant Virus ◽  
Food Production ◽  
Virus Transmission ◽  
Plant Viruses ◽  
Aminopeptidase N ◽  
Pea Aphid ◽  
Aphid Vector ◽  
Alanyl Aminopeptidase

ABSTRACTInsect-borne plant viruses cause significant agricultural losses and jeopardize sustainable global food production. Although blocking plant virus transmission would allow for crop protection, virus receptors in insect vectors are unknown. Here we identify membrane alanyl aminopeptidase N (APN) as a receptor for pea enation mosaic virus (PEMV) coat protein (CP) in the gut of the pea aphid,Acyrthosiphon pisum, using a far-Western blot method. Pulldown and immunofluorescence binding assays and surface plasmon resonance were used to confirm and characterize CP-APN interaction. PEMV virions and a peptide comprised of PEMV CP fused to a proline-rich hinge (-P-) and green fluorescent protein (CP-P-GFP) specifically bound to APN. Recombinant APN expressed in Sf9 cells resulted in internalization of CP-P-GFP, which was visualized by confocal microscopy; such internalization is an expected hallmark of a functional gut receptor. Finally, in assays with aphid gut-derived brush border membrane vesicles, binding of CP-P-GFP competed with binding of GBP3.1, a peptide previously demonstrated to bind to APN in the aphid gut and to impede PEMV uptake into the hemocoel; this finding supports the hypothesis that GBP3.1 and PEMV bind to and compete for the same APN receptor. Thesein vitrodata combined with previously publishedin vivoexperiments (S. Liu, S. Sivakumar, W. O. Sparks, W. A. Miller, and B. C. Bonning, Virology 401:107–116, 2010,http://dx.doi.org/10.1016/j.virol.2010.02.009) support the identification of APN as the first receptor in a plant virus vector. Knowledge of this receptor will provide for technologies based on PEMV-APN interaction designed to block plant virus transmission and to suppress aphid populations.IMPORTANCEA significant proportion of global food production is lost to insect pests. Aphids, in addition to weakening plants by feeding on their sap, are responsible for transmitting about half of the plant viruses vectored by insects. Growers rely heavily on the application of chemical insecticides to manage both aphids and aphid-vectored plant viral disease. To increase our understanding of plant virus-aphid vector interaction, we providein vitroevidence supporting earlierin vivowork for identification of a receptor protein in the aphid gut called aminopeptidase N, which is responsible for entry of the plant virus pea enation mosaic virus into the pea aphid vector. Enrichment of proteins found on the surface of the aphid gut epithelium resulted in identification of this first aphid gut receptor for a plant virus. This discovery is particularly important since the disruption of plant virus binding to such a receptor may enable the development of a nonchemical strategy for controlling aphid-vectored plant viruses to maximize food production.

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

Viruses ◽  
2020 ◽  
Vol 12 (3) ◽  
pp. 299 ◽  
Author(s):  
Jérémy Di Mattia ◽  
Faustine Ryckebusch ◽  
Marie-Stéphanie Vernerey ◽  
Elodie Pirolles ◽  
Nicolas Sauvion ◽  
...  
Keyword(s):  
Defense Mechanisms ◽  
Host Plants ◽  
Virus Transmission ◽  
Plant Viruses ◽  
The Body ◽  
Nuclear Shuttle Protein ◽  
Aphid Vector ◽  
Taxonomic Criterion ◽  
Alfalfa Leaf ◽  
Leaf Curl Virus

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

scholarly journals Disruption of Vector Transmission by a Plant-Expressed Viral Glycoprotein

2014 ◽  
Vol 27 (3) ◽  
pp. 296-304 ◽  
Author(s):  
Mauricio Montero-Astúa ◽  
Dorith Rotenberg ◽  
Alexandria Leach-Kieffaber ◽  
Brandi A. Schneweis ◽  
Sunghun Park ◽  
...  
Keyword(s):  
Transgenic Plants ◽  
Frankliniella Occidentalis ◽  
Virus Transmission ◽  
Virus Titer ◽  
Western Flower Thrips ◽  
Plant Viruses ◽  
Insect Vector ◽  
Viral Glycoprotein ◽  
Global Food Security ◽  
Negative Effect

Vector-borne viruses are a threat to human, animal, and plant health worldwide, requiring the development of novel strategies for their control. Tomato spotted wilt virus (TSWV) is one of the 10 most economically significant plant viruses and, together with other tospoviruses, is a threat to global food security. TSWV is transmitted by thrips, including the western flower thrips, Frankliniella occidentalis. Previously, we demonstrated that the TSWV glycoprotein GN binds to thrips vector midguts. We report here the development of transgenic plants that interfere with TSWV acquisition and transmission by the insect vector. Tomato plants expressing GN-S protein supported virus accumulation and symptom expression comparable with nontransgenic plants. However, virus titers in larval insects exposed to the infected transgenic plants were three-log lower than insects exposed to infected nontransgenic control plants. The negative effect of the GN-S transgenics on insect virus titers persisted to adulthood, as shown by four-log lower virus titers in adults and an average reduction of 87% in transmission efficiencies. These results demonstrate that an initial reduction in virus infection of the insect can result in a significant decrease in virus titer and transmission over the lifespan of the vector, supportive of a dose-dependent relationship in the virus–vector interaction. These findings demonstrate that plant expression of a viral protein can be an effective way to block virus transmission by insect vectors.

Sign in / Sign up

Export Citation Format

Share Document