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 ◽  
...  

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.

2015 ◽  
Vol 89 (19) ◽  
pp. 9719-9726 ◽  
Author(s):  
Anne Sicard ◽  
Jean-Louis Zeddam ◽  
Michel Yvon ◽  
Yannis Michalakis ◽  
Serafin Gutiérrez ◽  
...  

ABSTRACTPlant virus species of the familyNanoviridaehave segmented genomes with the highest known number of segments encapsidated individually. They thus likely represent the most extreme case of the so-called multipartite, or multicomponent, viruses. All species of the family are believed to be transmitted in a circulative nonpropagative manner by aphid vectors, meaning that the virus simply crosses cellular barriers within the aphid body, from the gut to the salivary glands, without replicating or even expressing any of its genes. However, this assumption is largely based on analogy with the transmission of other plant viruses, such as geminiviruses or luteoviruses, and the details of the molecular and cellular interactions between aphids and nanoviruses are poorly investigated. When comparing the relative frequencies of the eight genome segments in populations of the speciesFaba bean necrotic stunt virus(FBNSV) (genusNanovirus) within host plants and within aphid vectors fed on these plants, we unexpectedly found evidence of reproducible changes in the frequencies of some specific segments. We further show that these changes occur within the gut during early stages of the virus cycle in the aphid and not later, when the virus is translocated into the salivary glands. This peculiar observation, which was similarly confirmed in three aphid vector species,Acyrthosiphon pisum,Aphis craccivora, andMyzus persicae, calls for revisiting of the mechanisms of nanovirus transmission. It reveals an unexpected intimate interaction that may not fit the canonical circulative nonpropagative transmission.IMPORTANCEA specific mode of interaction between viruses and arthropod vectors has been extensively described in plant viruses in the three familiesLuteoviridae,Geminiviridae, andNanoviridae, but never in arboviruses of animals. This so-called circulative nonpropagative transmission contrasts with the classical biological transmission of animal arboviruses in that the corresponding viruses are thought to cross the vector cellular barriers, from the gut lumen to the hemolymph and to the salivary glands, without expressing any of their genes and without replicating. By monitoring the genetic composition of viral populations during the life cycle ofFaba bean necrotic stunt virus(FBNSV) (genusNanovirus), we demonstrate reproducible genetic changes during the transit of the virus within the body of the aphid vector. These changes do not fit the view that viruses simply traverse the bodies of their arthropod vectors and suggest more intimate interactions, calling into question the current understanding of circulative nonpropagative transmission.


2021 ◽  
Vol In Press (In Press) ◽  
Author(s):  
Nafise Shamloo ◽  
Alireza Ghanadan ◽  
Fahimeh Sadat Hashemian ◽  
Maedeh Ghorbanpour

Background: Salivary gland tumors include a wide variety of benign and malignant tumors in the oral and maxillofacial region. Although these tumors are not common, they are not rare. The prevalence of these tumors varies with regard to age, gender, and their location in the body. Objectives: This study aimed to evaluate the frequency of benign and malignant salivary gland tumors in patients referred to three referral hospitals in Tehran, Iran. Methods: This retrospective cross-sectional study examined the demographic and pathologic records of the patients with salivary gland tumors submitted to the Department of Pathology of Amir Alam, Loghman Hakim, and Shohada Hospitals from 2005 to 2016. In this study, the histological variants of salivary gland tumors and clinical parameters such as age, gender, and the location of the tumor were examined. The clinical data were analyzed using SPSS software version 21. Results: Of 137632 patient records, 1180 cases were salivary gland tumors. Pleomorphic adenoma in 794 cases (67.3%) and adenoid cystic carcinoma in 109 cases (9.2%) were the most common tumors, respectively. Salivary gland tumors were more common in males, and the participants’ mean age was 42.86 ± 16.5 years. The most common site was parotid and minor salivary glands, with 937 (79.4%) and 137 (12%) cases, respectively. Conclusions: In this study, the most common benign tumor was pleomorphic adenoma in the parotid gland, and the most common malignant tumor was adenoid cystic carcinoma in the major salivary glands. Furthermore, benign tumors were more frequent than malignant tumors.


Parasitology ◽  
1941 ◽  
Vol 33 (1) ◽  
pp. 110-116 ◽  
Author(s):  
Kenneth M. Smith

Extracts of caterpillars and other insects are shown to inhibit the infective power of tobacco mosaic and tobacco necrosis viruses. The inhibitor is not sedimented after spinning for 2½ hr. at 30,000 r.p.m. Experiments with non-vector insects such as caterpillars have shown that the virus of sugar-beet curly-top, of tobacco ringspot and other viruses, are destroyed within the body of the insect. On the other hand, tobacco mosaic virus passes through the body of the caterpillar unchanged though greatly reduced in concentration. By the use of the specific insect vector and artificial feeding methods it was possible to recover the virus of curly-top 24 hr. after it had been injected into the blood of the caterpillar but the viruses of tobacco mosaic and tobacco necrosis could not be so recovered. Experimental evidence is given to show that the virus of beet curly-top is present in the saliva of viruliferous insects.


2020 ◽  
Vol 117 (29) ◽  
pp. 16928-16937 ◽  
Author(s):  
Ya-Zhou He ◽  
Yu-Meng Wang ◽  
Tian-Yan Yin ◽  
Elvira Fiallo-Olivé ◽  
Yin-Quan Liu ◽  
...  

Whereas most of the arthropod-borne animal viruses replicate in their vectors, this is less common for plant viruses. So far, only some plant RNA viruses have been demonstrated to replicate in insect vectors and plant hosts. How plant viruses evolved to replicate in the animal kingdom remains largely unknown. Geminiviruses comprise a large family of plant-infecting, single-stranded DNA viruses that cause serious crop losses worldwide. Here, we report evidence and insight into the replication of the geminivirus tomato yellow leaf curl virus (TYLCV) in the whitefly (Bemisia tabaci) vector and that replication is mainly in the salivary glands. We found that TYLCV induces DNA synthesis machinery, proliferating cell nuclear antigen (PCNA) and DNA polymerase δ (Polδ), to establish a replication-competent environment in whiteflies. TYLCV replication-associated protein (Rep) interacts with whitefly PCNA, which recruits DNA Polδ for virus replication. In contrast, another geminivirus, papaya leaf curl China virus (PaLCuCNV), does not replicate in the whitefly vector. PaLCuCNV does not induce DNA-synthesis machinery, and the Rep does not interact with whitefly PCNA. Our findings reveal important mechanisms by which a plant DNA virus replicates across the kingdom barrier in an insect and may help to explain the global spread of this devastating pathogen.


1999 ◽  
Vol 89 (12) ◽  
pp. 1144-1151 ◽  
Author(s):  
Myoung-Ok Kwon ◽  
Astri C. Wayadande ◽  
Jacqueline Fletcher

Spiroplasma citri, a helical, wall-less prokaryote in the class Molli-cutes, is transmitted by the beet leafhopper, Circulifer tenellus. Invasion of leafhopper tissues and cytopathological effects by S. citri were investigated by transmission electron microscopy. All eight cell types of the principle salivary glands, as well as the adjacent muscle cells and the cells of the accessory salivary glands, were colonized by the spiroplas-mas. In both midgut epithelia and salivary gland cells, spiroplasmas usually occurred in membrane-bound cytoplasmic vesicles that often were located near the cell periphery. In several salivary gland cells, spiroplas-mas were also observed within membranous pockets apparently formed by invagination of the plasmalemma beneath intact basal lamina. These observations are consistent with spiroplasma entry into the insect cells by receptor-mediated endocytosis. Cytopathological effects of spiroplasma infection in salivary cells included loss of membrane and basal lamina integrity, presence in some cells of irregular inclusion-like structures containing dense matrices of filamentous material that labeled with anti S. citri antibodies, and apparent disorganization of the endoplasmic reticulum. Compared to the tightly aligned fiber bundles in healthy muscle cells, bundles in spiroplasma-containing muscle cells appeared fragmented and loosely arranged. Such symptoms could contribute to the reduction in longevity and fecundity that has been previously reported for S. citri-infected C. tenellus.


2018 ◽  
Author(s):  
Gang Lu ◽  
Shuo Li ◽  
Changwei Zhou ◽  
Xin Qian ◽  
Qing Xiang ◽  
...  

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.


2018 ◽  
Author(s):  
Thorben Lundsgaard

SummaryThe ultrastructure of cells in the head and thorax from viruliferous Javesella pellucida transmitting Festuca leaf streak virus was studied. Aggregates of nonenveloped nucleocapsid particles were observed at the periphery of viroplasms located in cytoplasm of salivary gland cells, fat cells, and nerve cell bodies. Aggregates of nucleocapsid particles, not associated with viroplasms, were seen within a distance of about 1 μm from the basal lamina of salivary glands. Enveloped virions, singly or aggregated, were observed in nerve cell axons and/or dendrites.


2022 ◽  
Author(s):  
Quentin Chesnais ◽  
Victor Golyaev ◽  
Amadine Velt ◽  
Camille Rustenholz ◽  
Véronique Brault ◽  
...  

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.


2009 ◽  
Vol 8 (4) ◽  
pp. 640-648 ◽  
Author(s):  
Sabine Engelmann ◽  
Olivier Silvie ◽  
Kai Matuschewski

ABSTRACT Accumulation of infectious Plasmodium sporozoites in Anopheles spp. salivary glands marks the final step of the complex development of the malaria parasite in the insect vector. Sporozoites are formed inside midgut-associated oocysts and actively egress into the mosquito hemocoel. Traversal of the salivary gland acinar cells correlates with the sporozoite's capacity to perform continuous gliding motility. Here, we characterized the cellular role of the Plasmodium berghei sporozoite invasion-associated protein 1 (SIAP-1). Intriguingly, SIAP-1 orthologs are found exclusively in apicomplexan hemoprotozoa, parasites that are transmitted by arthropod vectors, e.g., Plasmodium, Babesia, and Theileria species. By fluorescent tagging with mCherry, we show that SIAP-1 is expressed in oocyst-derived and salivary gland-associated sporozoites, where it accumulates at the apical tip. Targeted disruption of SIAP-1 does not affect sporozoite formation but causes a partial defect in sporozoite egress from oocysts and abolishes sporozoite colonization of mosquito salivary glands. Parasites with the siap-1(−) mutation are blocked in their capacity to perform continuous gliding motility. We propose that arthropod-transmitted apicomplexan parasites specifically express secretory factors, such as SIAP-1, that mediate efficient oocyst exit and migration to the salivary glands.


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