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 Aphid endosymbiont facilitates virus transmission by modulating the volatile profile of host plants

2021 ◽  
Vol 21 (1) ◽  
Author(s):  
Xiao-Bin Shi ◽  
Shuo Yan ◽  
Chi Zhang ◽  
Li-Min Zheng ◽  
Zhan-Hong Zhang ◽  
...  
Keyword(s):  
Host Plants ◽  
Green Peach Aphid ◽  
Virus Transmission ◽  
Feeding Preference ◽  
Plant Viruses ◽  
Volatile Profile ◽  
Cmv Infection ◽  
Buchnera Aphidicola ◽  
Plant Volatile ◽  
Volatile Profiles

Abstract Background Most plant viruses rely on vectors for their transmission and spread. One of the outstanding biological questions concerning the vector-pathogen-symbiont multi-trophic interactions is the potential involvement of vector symbionts in the virus transmission process. Here, we used a multi-factorial system containing a non-persistent plant virus, cucumber mosaic virus (CMV), its primary vector, green peach aphid, Myzus persicae, and the obligate endosymbiont, Buchnera aphidicola to explore this uncharted territory. Results Based on our preliminary research, we hypothesized that aphid endosymbiont B. aphidicola can facilitate CMV transmission by modulating plant volatile profiles. Gene expression analyses demonstrated that CMV infection reduced B. aphidicola abundance in M. persicae, in which lower abundance of B. aphidicola was associated with a preference shift in aphids from infected to healthy plants. Volatile profile analyses confirmed that feeding by aphids with lower B. aphidicola titers reduced the production of attractants, while increased the emission of deterrents. As a result, M. persicae changed their feeding preference from infected to healthy plants. Conclusions We conclude that CMV infection reduces the B. aphidicola abundance in M. persicae. When viruliferous aphids feed on host plants, dynamic changes in obligate symbionts lead to a shift in plant volatiles from attraction to avoidance, thereby switching insect vector’s feeding preference from infected to healthy plants.

scholarly journals Alfalfa leaf curl virus is efficiently acquired by its aphid vector Aphis craccivora but inefficiently transmitted

2020 ◽  
Author(s):  
Faustine Ryckebusch ◽  
Michel Peterschmitt ◽  
Martine Granier ◽  
Nicolas Sauvion
Keyword(s):  
Transmission Rate ◽  
Infected Plant ◽  
Aphid Transmission ◽  
Transmission Efficiency ◽  
Aphis Craccivora ◽  
Viral Dna ◽  
Aphid Vector ◽  
Alfalfa Leaf ◽  
Leaf Curl Virus ◽  
Leaf Curl

Alfalfa leaf curl virus (ALCV) is the first geminivirus for which aphid transmission was reported. Transmission by Aphis craccivora was determined previously to be highly specific and circulative. Using various complementary techniques, the transmission journey of ALCV was monitored from its uptake from infected plant tissues up to the head of its vector. ALCV was shown to be restricted to phloem tissues using fluorescence in situ hybridization (FISH) and electropenetrography (EPG) monitoring of virus acquisition. Furthermore, the virus is heterogeneously distributed in phloem tissues, as revealed by FISH and quantitative PCR of viral DNA acquired by EPG-monitored aphids. Despite the efficient ingestion of viral DNA, about 106 viral DNA copies per insect in a 15 h feeding period on ALCV-infected plants, the individual maximum transmission rate was 12 %. Transmission success was related to a critical viral accumulation, around 1.6×107 viral DNA copies per insect, a threshold that generally needed more than 48 h to be reached. Moreover, whereas the amount of acquired virus did not decrease over time in the whole aphid body, it declined in the haemolymph and heads. ALCV was not detected in progenies of viruliferous aphids and did not affect aphid fitness. Compared to geminiviruses transmitted by whiteflies or leafhoppers, or to luteoviruses transmitted by aphids, the transmission efficiency of ALCV by A. craccivora is low. This result is discussed in relation to the aphid vector of this geminivirus and the agroecological features of alfalfa, a hardy perennial host plant.

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 Circulative Nonpropagative Aphid Transmission of Nanoviruses: an Oversimplified View

2015 ◽  
Vol 89 (19) ◽  
pp. 9719-9726 ◽  
Author(s):  
Anne Sicard ◽  
Jean-Louis Zeddam ◽  
Michel Yvon ◽  
Yannis Michalakis ◽  
Serafin Gutiérrez ◽  
...  
Keyword(s):  
Salivary Glands ◽  
Faba Bean ◽  
Plant Viruses ◽  
The Body ◽  
Virus Species ◽  
Content Type ◽  
Aphid Vector ◽  
Arthropod Vectors ◽  
The Family ◽  
Aphid Vectors

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.

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 Alfalfa leaf curl virus is efficiently acquired by its aphid vector Aphis craccivora but inefficiently transmitted

2020 ◽  
Author(s):  
Faustine Ryckebusch ◽  
Michel Peterschmitt ◽  
Martine Granier ◽  
Nicolas Sauvion
Keyword(s):  
Transmission Rate ◽  
Infected Plant ◽  
Aphid Transmission ◽  
Transmission Efficiency ◽  
Aphis Craccivora ◽  
Viral Dna ◽  
Aphid Vector ◽  
Alfalfa Leaf ◽  
Leaf Curl Virus ◽  
Leaf Curl

ABSTRACTAlfalfa leaf curl virus (ALCV) is the first geminivirus for which an aphid transmission was reported. Transmission by Aphis craccivora was determined previously to be highly specific and circulative. Using various complementary techniques, the transmission journey of ALCV was monitored from its uptake in an infected plant tissue up to the head of its vector. ALCV was shown to be restricted in the phloem using fluorescent in situ hybridization (FISH) and electropenetrography (EPG) monitoring of virus acquisition. Furthermore, the virus is heterogeneously distributed in the phloem as revealed by FISH and qPCR quantification of the viral DNA acquired by aphids monitored by EPG. In spite of the efficient ingestion of viral DNA, about 106 in a 15-hour feeding on ALCV infected plants, the individual transmission rate was at a maximum of 12%. Transmission success was related to a critical viral accumulation, around 1.6×107 viral DNA copies per insect, a threshold that needs generally more than 48 hours to be reached. Moreover, whereas the amount of acquired virus does not decrease over time in the whole aphid body, it decreased in hemolymph and heads. ALCV was not detected in progenies of viruliferous aphids and had no effect on aphid fitness. Compared to geminiviruses transmitted by whiteflies or leafhoppers or to luteovirus transmitted by aphids, the transmission efficiency of ALCV by A. craccivora is low. This result is discussed in relation to the aphid vector of this geminivirus and the agroecological features of alfalfa, a hardy perennial host plant.

scholarly journals Impacts of cucurbit chlorotic yellows virus (CCYV) on biological characteristics of its vector Bemisia tabaci

2021 ◽  
Author(s):  
Haifang He ◽  
Jingjing Li ◽  
Zelong Zhang ◽  
Xuefei Tang ◽  
Danyang Song ◽  
...  
Keyword(s):  
Bemisia Tabaci ◽  
Plant Virus ◽  
Host Plants ◽  
Plant Viruses ◽  
The Body ◽  
Biological Characteristics ◽  
Adult Longevity ◽  
Male Adult ◽  
Q Biotype ◽  
Cucurbit Chlorotic Yellows Virus

Abstract It is known that plant viruses, to facilitate their transmission, can change the phenotypes and defense pathways of the host plants and the performance of their vectors. Cucurbit chlorotic yellows virus (CCYV), a newly reported virus occurring on cucurbit plants and many other plant species, is transmitted specifically by Middle East-Minor Asia 1 (B biotype) and Mediterranean (Q biotype) cryptic species of whitefly, Bemisia tabaci (Gennadius), in a semipersistent manner. This study evaluated the direct and indirect effects of CCYV on B. tabaci biology to better understand the plant-virus-vector interaction. By using CCYV-B. tabaci-cucumber as the model, we investigated whether or how a semipersistent plant virus impacts the biology of its whitefly vectors. CCYV mRNA were detectable in nymphs from 1st to 4th instars and adults of B. tabaci with different titers. Female nymph duration and female adult longevity greatly extended on CCYV-infected plants, but male nymph duration and male adult longevity were not significantly influenced. In addition, on CCYV-infected plants, the body length and oviposition of adult B. tabaci increased, but the hatching rates of eggs and survival rates of different stages were not affected. Most interestingly, the sex ratio (male:female) significantly reduced to 0.506:1 in whitefly populations on CCYV-infected plants, while the ratio remained about 0.979:1 on healthy plants. These results indicated that CCYV can significantly impact the biological characteristics of its vector B. tabaci through the host plants. It is speculated that CCYV and B. tabaci have established a typical mutualist relationship mediated by host plants.

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 A proteomic approach reveals possible molecular mechanisms and roles for endosymbiotic bacteria in begomovirus transmission by whiteflies

GigaScience ◽  
2020 ◽  
Vol 9 (11) ◽  
Author(s):  
Adi Kliot ◽  
Richard S Johnson ◽  
Michael J MacCoss ◽  
Svetlana Kontsedalov ◽  
Galina Lebedev ◽  
...  
Keyword(s):  
Plant Species ◽  
Molecular Mechanisms ◽  
Virus Transmission ◽  
Plant Viruses ◽  
Virus Species ◽  
Proteomic Approach ◽  
Efficient Vector ◽  
Vector Borne ◽  
Q Biotype ◽  
Leaf Curl Virus

Abstract Background Many plant viruses are vector-borne and depend on arthropods for transmission between host plants. Begomoviruses, the largest, most damaging and emerging group of plant viruses, infect hundreds of plant species, and new virus species of the group are discovered each year. Begomoviruses are transmitted by members of the whitefly Bemisia tabaci species complex in a persistent-circulative manner. Tomato yellow leaf curl virus (TYLCV) is one of the most devastating begomoviruses worldwide and causes major losses in tomato crops, as well as in many agriculturally important plant species. Different B. tabaci populations vary in their virus transmission abilities; however, the causes for these variations are attributed among others to genetic differences among vector populations, as well as to differences in the bacterial symbionts housed within B. tabaci. Results Here, we performed discovery proteomic analyses in 9 whitefly populations from both Middle East Asia Minor I (MEAM1, formerly known as B biotype) and Mediterranean (MED, formerly known as Q biotype) species. We analysed our proteomic results on the basis of the different TYLCV transmission abilities of the various populations included in the study. The results provide the first comprehensive list of candidate insect and bacterial symbiont (mainly Rickettsia) proteins associated with virus transmission. Conclusions Our data demonstrate that the proteomic signatures of better vector populations differ considerably when compared with less efficient vector populations in the 2 whitefly species tested in this study. While MEAM1 efficient vector populations have a more lenient immune system, the Q efficient vector populations have higher abundance of proteins possibly implicated in virus passage through cells. Both species show a strong link of the facultative symbiont Rickettsia to virus transmission.

Sign in / Sign up

Export Citation Format

Share Document