Genomic and Proteomic Analysis of Schizaphis graminum Reveals Cyclophilin Proteins Are Involved in the Transmission of Cereal Yellow Dwarf Virus

Tamborindeguy, Cécilia; Bereman, Michael S.; DeBlasio, Stacy L.; Igwe, David Okeh; Smith, Dawn; White, Frank F.; MacCoss, Michael J.; Gray, Stewart M.; Cilia, Michelle

doi:10.1371/journal.pone.0071620

Cited by 50 publications

(58 citation statements)

References 51 publications

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“…Recently, peptidyl-prolyl isomerases proteins (PPIases or Cyps) have been implicated in B/CYDV circulation and transmission by aphids (Tamborindeguy et al, 2013), and were hypothesized to play a role in chaperoning these viruses to various membrane bound vesicles (Yang et al, 2008). Cyps are important in the proper folding of proteins and as modulators for human virus replication (Frausto et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…The search for such proteins in many cases is based on results described in other circulative virus-vector systems in which other proteins facilitating virus transmission have been identified. One such example was demonstrated in recent studies in which genetic and proteomic analyses suggested that virus-binding aphid proteins belonging to the peptidyl-prolyl isomerases proteins (PPIases or Cyps) were specifically inherited and conserved in different aphid vector genotypes (Tamborindeguy et al, 2013). This suggested that they play a major role in regulating Cereal yellow dwarf virus - RPV (CYDV-RPV) transmission (Yang et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

“…This suggested that they play a major role in regulating Cereal yellow dwarf virus - RPV (CYDV-RPV) transmission (Yang et al, 2008). Tamborindeguy et al (2013) showed that both CypA and B interact with CYDV-RPV, and these interactions may be important but not sufficient to mediate virus transport from the hindgut lumen into the hemocoel.…”

Section: Introductionmentioning

confidence: 99%

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Implication of the Whitefly Bemisia tabaci Cyclophilin B Protein in the Transmission of Tomato yellow leaf curl virus

Kanakala

Ghanim

2016

Front. Plant Sci.

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Tomato yellow leaf curl virus (TYLCV) is a single-stranded (ssDNA) begomoviruses that causes severe damage to tomato and several other crops worldwide. TYLCV is exclusively transmitted by the sweetpotato whitefly, Bemisia tabaci in a persistent circulative and propagative manner. Previous studies have shown that the transmission, retention, and circulation of TYLCV in its vector involves interaction with insect and endosymbiont proteins, which aid in the transmission of the virus, or have a protective role in response to the presence of the virus in the insect body. However, only a low number of such proteins have been identified. Here, the role of B. tabaci Cyclophilin B (CypB) in the transmission of TYLCV protein was investigated. Cyclophilins are a large family of cellular prolyl isomerases that have many molecular roles including facilitating protein-protein interactions in the cell. One cyclophilin protein has been implicated in aphid-luteovirus interactions. We demonstrate that the expression of CypB from B. tabaci is altered upon TYLCV acquisition and retention. Further experiments used immunocapture-PCR and co-immunolocalization and demonstrated a specific interaction and colocalization between CypB and TYLCV in the the midgut, eggs, and salivary glands. Membrane feeding of anti-CypB antibodies and TYLCV-infected plants showed a decrease in TYLCV transmission, suggesting a critical role that CypB plays in TYLCV transmission. Further experiments, which used membrane feeding with the CypB inhibitor Cyclosporin A showed decrease in CypB-TYLCV colocalization in the midgut and virus transmission. Altogether, our results indicate that CypB plays an important role in TYLCV transmission by B. tabaci.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Implication of the Whitefly Bemisia tabaci Cyclophilin B Protein in the Transmission of Tomato yellow leaf curl virus

Kanakala

Ghanim

2016

Front. Plant Sci.

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“…Similarly, a small aphid gut binding peptide was shown to interfere with enamovirus uptake from pea aphid gut into the hemocoel; the peptide also bound to gut epithelia of two other aphid species suggesting potential broader applicability [175]. Aphid vector genomic and proteomic analysis identified cyclophilin proteins as potential novel control targets based on their involvement in luteovirus transmission [176]. Vector populations may be specifically controlled by delivery of insecticidal molecules to the insect hemolymph, such as fusing a toxin to the CP of a luteovirus [177].…”

Section: Experimental Approaches To Facilitate Further Insights Anmentioning

confidence: 99%

Plant Virus–Insect Vector Interactions: Current and Potential Future Research Directions

Dietzgen

Mann

Johnson

2016

Viruses

195

142

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Acquisition and transmission by an insect vector is central to the infection cycle of the majority of plant pathogenic viruses. Plant viruses can interact with their insect host in a variety of ways including both non-persistent and circulative transmission; in some cases, the latter involves virus replication in cells of the insect host. Replicating viruses can also elicit both innate and specific defense responses in the insect host. A consistent feature is that the interaction of the virus with its insect host/vector requires specific molecular interactions between virus and host, commonly via proteins. Understanding the interactions between plant viruses and their insect host can underpin approaches to protect plants from infection by interfering with virus uptake and transmission. Here, we provide a perspective focused on identifying novel approaches and research directions to facilitate control of plant viruses by better understanding and targeting virus–insect molecular interactions. We also draw parallels with molecular interactions in insect vectors of animal viruses, and consider technical advances for their control that may be more broadly applicable to plant virus vectors.

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“…In contrast, the components of the insect vector that participate in viral transmission have been difficult to study, although some insect proteins have been identified that interact with circulative viruses and are linked to successful transmission (10 -13). Insect proteins are expected to play a role as virus receptors, in the uptake and transport of virus through various tissues, and in replication of the viruses (1,3,14). In our recent study, vitellogenin of Laodelphax striatellus (small brown planthopper) was demonstrated to play a critical role in transovarial transmission of Rice stripe virus (RSV) (15).…”

mentioning

confidence: 99%

Proteomic Analysis of Interaction between a Plant Virus and Its Vector Insect Reveals New Functions of Hemipteran Cuticular Protein

Liu

Gray

Huo

et al. 2015

Molecular & Cellular Proteomics

101

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Numerous viruses can be transmitted by their corresponding vector insects; however, the molecular mechanisms enabling virus transmission by vector insects have been poorly understood, especially the identity of vector components interacting with the virus. Here, we used the yeast two-hybrid system to study proteomic interactions of a plant virus (Rice stripe virus, RSV, genus Tenuivirus) with its vector insect, small brown planthopper (Laodelphax striatellus). Sixty-six proteins of L. striatellus that interacted with the nucleocapsid protein (pc3) of RSV were identified. A virus-insect interaction network, constructed for pc3 and 29 protein homologs of Drosophila melanogaster, suggested that nine proteins might directly interact with pc3. Of the 66 proteins, five (atlasin, a novel cuticular protein, jagunal, NAC domain protein, and vitellogenin) were most likely to be involved in viral movement, replication, and transovarial transmission. This work also provides evidence that the novel cuticular protein, CPR1, from L. striatellus is essential for RSV transmission by its vector insect. CPR1 binds the nucleocapsid protein (pc3) of RSV both in vivo and in vitro and colocalizes with RSV in the hemocytes of L. striatellus. Knockdown of CPR1 transcription using RNA interference resulted in a decrease in the concentration of RSV in the hemolymph, salivary glands and in viral transmission efficiency. These data suggest that CPR1 binds RSV in the insect and stabilizes the viral concentration in the hemolymph, perhaps to protect the virus or to help move the virus to the salivary tissues. Our studies provide direct experimental evidence that viruses can use existing vector proteins to aid their survival in the hemolymph. Identifying these pu-

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Genomic and Proteomic Analysis of Schizaphis graminum Reveals Cyclophilin Proteins Are Involved in the Transmission of Cereal Yellow Dwarf Virus

Cited by 50 publications

References 51 publications

Implication of the Whitefly Bemisia tabaci Cyclophilin B Protein in the Transmission of Tomato yellow leaf curl virus

Implication of the Whitefly Bemisia tabaci Cyclophilin B Protein in the Transmission of Tomato yellow leaf curl virus

Plant Virus–Insect Vector Interactions: Current and Potential Future Research Directions

Proteomic Analysis of Interaction between a Plant Virus and Its Vector Insect Reveals New Functions of Hemipteran Cuticular Protein

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