ADP ribosylation factor 1 facilitates spread of wheat dwarf virus in its insect vector
Language English Country United States Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
Grant support
LTACH-17010
Research Program of the Ministry of Education, Youth and Sports of the Czech Republic - International
31861133020
National Natural Science Foundation of China - International
2016YFE0131000
Inter-Governmental S&T Cooperation Project of China - International
PubMed
31099153
DOI
10.1111/cmi.13047
Knihovny.cz E-resources
- Keywords
- ADP ribosylation factor, Psammotettix alienus, transmission mechanism, transport, wheat dwarf virus,
- MeSH
- ADP-Ribosylation Factor 1 genetics metabolism MeSH
- Cell Line MeSH
- Geminiviridae pathogenicity MeSH
- Hemiptera genetics metabolism virology MeSH
- Insect Vectors genetics MeSH
- Plant Diseases virology MeSH
- RNA Interference MeSH
- Salivary Glands metabolism virology MeSH
- Intestines virology MeSH
- Two-Hybrid System Techniques MeSH
- Virion metabolism MeSH
- Capsid Proteins metabolism MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- ADP-Ribosylation Factor 1 MeSH
- Capsid Proteins MeSH
Many plant viruses are vectored by insects in a persistent circulative manner. The insect gut and salivary gland are important barriers limiting virus spread, but the mechanisms by which viruses are able to cross the gut escape barriers of the insect remain largely unknown. Wheat dwarf virus (WDV), transmitted by Psammotettix alienus in a persistent, circulative, and nonpropagative manner, causes the most economically important virus disease in wheat. In this study, ADP ribosylation factor 1 (ARF1) was found to interact with the coat protein of WDV in a yeast two-hybrid, pull-down assay and to colocalise with virions in the gut and salivary glands of P. alienus. When transcription of ARF1 was suppressed by RNA interference, the WDV titre decreased in the haemolymph and salivary glands, and transmission efficiency decreased, but titre in the gut did not differ from that of the control. These data suggest that ARF1 of P. alienus binds to the WDV virion and helps virus spread from gut to haemolymph. Our study provides direct experimental evidence that WDV can use the existing membrane trafficking mechanism to aid its spread within the insect vector. This first analysis of the molecular interaction between WDV and its vector P. alienus contributes to understanding the mechanisms involved in circulative transmission of the virus by the leafhopper vector.
See more in PubMed
Balasubramaniam, M., & Freed, E. O. (2011). New insights into HIV assembly and trafficking. Physiology, 26, 236-251. https://doi.org/10.1152/physiol.00051.2010
Behjatnia, S. A. A., Afsharifar, A. R., Tahan, V., Motlagh, M. H. A., Gandomani, O. E., & Niazi, A. (2011). Widespread occurrence and molecular characterization of wheat dwarf virus in Iran. Australasian Plant Pathology, 40, 12-19. https://doi.org/10.1007/s13313-010-0008-8
Bonifacino, J. S., & Glick, B. S. (2004). The mechanisms of vesicle budding and fusion. Cell, 116, 153-166. https://doi.org/10.1016/S0092-8674(03)01079-1
Boulakirba, S., Macia, E., Partisani, M., Lacas-Gervais, S., Brau, F., Luton, F., & Franco, M. (2014). Arf6 exchange factor EFA6 and endophilin directly interact at the plasma membrane to control clathrin-mediated endocytosis. Proceedings of the National Academy of Sciences of the United States of America, 111, 9473-9478. https://doi.org/10.1073/pnas.1401186111
Brown, H. A., Gutowski, S., Moomaw, C. R., Slaughter, C., & Sternweis, P. C. (1993). ADP-ribosylation factor, a small GTP-dependent regulatory protein, stimulates phospholipase D activity. Cell, 75, 1137-1144. https://doi.org/10.1016/0092-8674(93)90323-I
Deretic, D., Williams, A. H., Ransom, N., Morel, V., Hargrave, P. A., & Arendt, A. (2005). Rhodopsin C terminus, the site of mutations causing retinal disease, regulates trafficking by binding to ADP-ribosylation factor 4 (ARF4). Proceedings of the National Academy of Sciences of the United States of America, 102, 3301-3306. https://doi.org/10.1073/pnas.0500095102
Donaldson, J. G., & Jackson, C. L. (2011). ARF family G proteins and their regulators: Roles in membrane transport, development and disease. Nature Reviews. Molecular Cell Biology, 12, 533-533. https://doi.org/10.1038/nrm3159
D'Souza-Schorey, C., & Chavrier, P. (2006). ARF proteins: Roles in membrane traffic and beyond. Nature Reviews. Molecular Cell Biology, 7, 347-358. https://doi.org/10.1038/nrm1910
Farhat, R., Seron, K., Ferlin, J., Feneant, L., Belouzard, S., Goueslain, L., … Rouillé, Y. (2016). Identification of class II ADP-ribosylation factors as cellular factors required for hepatitis C virus replication. Cellular Microbiology, 18, 1121-1133. https://doi.org/10.1111/cmi.12572
Garcia-Exposito, L., Barroso-Gonzalez, J., Puigdomenech, I., Machado, J. D., Blanco, J., & Valenzuela-Fernandez, A. (2011). HIV-1 requires Arf6-mediated membrane dynamics to efficiently enter and infect T lymphocytes. Molecular Biology of the Cell, 22, 1148-1166. https://doi.org/10.1091/mbc.e10-08-0722
Ghanim, M. (2014). A review of the mechanisms and components that determine the transmission efficiency of tomato yellow leaf curl virus (Geminiviridae; Begomovirus) by its whitefly vector. Virus Research, 186, 47-54. https://doi.org/10.1016/j.virusres.2014.01.022
Gray, S., Cilia, M., & Ghanim, M. (2014). Circulative, “nonpropagative” virus transmission: An orchestra of virus-, insect-, and plant-derived instruments. Advances in Virus Research, 89, 141-199. https://doi.org/10.1016/B978-0-12-800172-1.00004-5
Gray, S., & Gildow, F. E. (2003). Luteovirus-aphid interactions. Annual Review of Phytopathology, 41, 539-566. https://doi.org/10.1146/annurev.phyto.41.012203.105815
Gray, S. M., & Banerjee, N. (1999). Mechanisms of arthropod transmission of plant and animal viruses. Microbiology and Molecular Biology Reviews, 63, 128-148.
Grove, J., & Marsh, M. (2011). The cell biology of receptor-mediated virus entry. The Journal of Cell Biology, 195, 1071-1082. https://doi.org/10.1083/jcb.201108131
Hajano, J. U. D., Wang, B., Ren, Y. D., Lu, C. T., & Wang, X. F. (2015). Quantification of southern rice black streaked dwarf virus and rice black streaked dwarf virus in the organs of their vector and nonvector insect over time. Virus Research, 208, 146-155. https://doi.org/10.1016/j.virusres.2015.06.015
Huang, H. C., Chen, C. C., Chang, W. C., Tao, M. H., & Huang, C. (2012). Entry of hepatitis B virus into immortalized human primary hepatocytes by clathrin-dependent endocytosis. Journal of Virology, 86, 9443-9453.
Huo, Y., Liu, W., Zhang, F., Chen, X., & Li, L. (2014). Transovarial transmission of a plant virus is mediated by vitellogenin of its insect vector. PLoS Pathogens, 10, e1003949.
Huth, W. (2000). Viruses of Graminae in Germany-A short overview. Journal of Plant Diseases and Protection, 107, 406-414.
Hyodo, K., Mine, A., Taniguchi, T., Kaido, M., Mise, K., Taniguchi, H., & Okuno, T. (2013). ADP ribosylation factor 1 plays an essential role in the replication of a plant RNA virus. Journal of Virology, 87, 163-176.
Jia, D., Chen, Q., Mao, Q., Zhang, X., Wu, W., Chen, H., … Wei, T. (2018). Vector mediated transmission of persistently transmitted plant viruses. Current Opinion in Virology, 28, 127-132. https://doi.org/10.1016/j.coviro.2017.12.004
Jia, D. S., Chen, H., Mao, Q., Liu, Q., & Wei, T. Y. (2012). Restriction of viral dissemination from the midgut deter-mines incompetence of small brown planthopper as a vector of Southern rice black-streaked dwarf virus. Virus Research, 167, 404-408. https://doi.org/10.1016/j.virusres.2012.05.023
Joshi, A., Garg, H., Nagashima, K., Bonifacino, J. S., & Freed, E. O. (2008). GGA and Arf proteins modulate retrovirus assembly and release. Molecular Cell, 30, 227-238. https://doi.org/10.1016/j.molcel.2008.03.015
Kahn, R. A., Volpicelli-Daley, L., Bowzard, B., Shrivastava-Ranjan, P., Li, Y., Zhou, C., & Cunningham, L. (2005). Arf family GTPases: Roles in membrane traffic and microtubule dynamics. Biochemical Society Transactions, 33, 1269-1272. https://doi.org/10.1042/BST0331269
Kudelko, M., Brault, J. B., Kwok, K., Li, M. Y., Pardigon, N., Peiris, J. S., … Wang, P. G. (2012). Class II ADP-ribosylation factors are required for efficient secretion of dengue viruses. The Journal of Biological Chemistry, 287, 767-777. https://doi.org/10.1074/jbc.M111.270579
Lan, H., Chen, H., Liu, Y., Jiang, C., Mao, Q., Jia, D., … Wei, T. (2015). Small interfering RNA pathway modulates initial viral infection in midgut epithelium of insect after ingestion of virus. Journal of Virology, 90, 917-929.
Linz, L. B., Liu, S., Chougule, N. P., & Bonning, B. C. (2015). In vitro evidence supports membrane alanyl aminopeptidase N as a receptor for a plant virus in the pea aphid vector. Journal of Virology, 89, 11203-11212.
Liu, W., Gray, S., Huo, Y., Li, L., Wei, T., & Wang, X. (2015). Proteomic analysis of interaction between a plant virus and its vector insect reveals new functions of hemipteran cuticular protein. Molecular & Cellular Proteomics, 14, 2229-2242. https://doi.org/10.1074/mcp.M114.046763
Liu, W., Hajano, J. U., & Wang, X. (2018). New insights on the transmission mechanism of tenuiviruses by their vector insects. Current Opinion in Virology, 33, 13-17. https://doi.org/10.1016/j.coviro.2018.07.004
Liu, Y., Wang, B., Vida, G., Cseplo-Karolyi, M., Wu, B. L., Wu, Y. H., & Wang, X. F. (2012). Genomic analysis of the natural population of wheat dwarf virus in wheat from China and Hungary. Journal of Integrative Agriculture, 11, 2020-2027. https://doi.org/10.1016/S2095-3119(12)60459-6
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods, 25, 402-408. https://doi.org/10.1006/meth.2001.1262
MacDowell, S. W., Macdonald, H., Hamilton, W. D. O., Coutts, R. H. A., & Buck, K. W. (1985). The nucleotide sequence of cloned wheat dwarf virus DNA. The EMBO Journal, 4, 2173-2180. https://doi.org/10.1002/j.1460-2075.1985.tb03912.x
Marsh, M., & Helenius, A. (2006). Virus entry: Open sesame. Cell, 124, 729-740. https://doi.org/10.1016/j.cell.2006.02.007
Matto, M., Sklan, E. H., David, N., Melamed-Book, N., Casanova, J. E., Glenn, J. S., & Aroeti, B. (2011). Role for ADP ribosylation factor 1 in the regulation of hepatitis C virus replication. Journal of Virology, 85, 946-956.
Mazelova, J., Astuto-Gribble, L., Inoue, H., Tam, B. M., Schonteich, E., Prekeris, R., … Deretic, D. (2009). Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4. The EMBO Journal, 28, 183-192. https://doi.org/10.1038/emboj.2008.267
Mercer, J., Schelhaas, M., & Helenius, A. (2010). Virus entry by endocytosis. Annual Review of Biochemistry, 79, 803-833. https://doi.org/10.1146/annurev-biochem-060208-104626
Morin, S., Ghanim, M., Sobol, I., & Czosnek, H. (2000). The GroEL protein of the whitefly Bemisia tabaci interacts with the coat protein of transmissible and non-transmissible begomoviruses in the yeast two-hybrid system. Virology, 276, 404-416. https://doi.org/10.1006/viro.2000.0549
Najar, A., Makkouk, K. M., Boudhir, H., Kumari, S. G., Zarouk, R., & Bessai, R. (2000). Viral diseases of cultivated legume and cereal crops in Tunisia. Phytopathology, 39, 423-432.
Nault, L. R., & Ammar, E. D. (1989). Leafhopper and planthopper transmission of plant viruses. Annual Review of Entomology, 34, 503-529. https://doi.org/10.1146/annurev.en.34.010189.002443
Nie, Z., Hirsch, D. S., & Randazzo, P. A. (2003). Arf and its many interactors. Current Opinion in Cell Biology, 15, 396-404. https://doi.org/10.1016/S0955-0674(03)00071-1
Qin, F., Liu, W., Wu, N., Zhang, L., Zhang, Z., Zhou, X., & Wang, X. (2018). Invasion of midgut epithelial cells by a persistently transmitted virus is mediated by sugar transporter 6 in its insect vector. PLoS Pathogens, 14, e1007201. https://doi.org/10.1371/journal.ppat.1007201
Rana, V. S., Popli, S., Saurav, G. K., Raina, H. S., Chaubey, R., Ramamurthy, V. V., & Rajagopal, R. (2016). A Bemisia tabaci midgut protein interacts with begomoviruses and plays a role in virus transmission. Cellular Microbiology, 18, 663-678. https://doi.org/10.1111/cmi.12538
Rosen, R., Surapathrudu, K., & Kliot, A. (2015). Persistent, circulative transmission of begomoviruses by whitefly vectors. Current Opinion in Virology, 15, 1-8. https://doi.org/10.1016/j.coviro.2015.06.008
Seddas, P., Boissinot, S., Strub, J. M., Van Dorsselaer, A., Van Regenmortel, M. H. V., & Pattus, F. (2004). Rack-1, GAPDH3, and actin: Proteins of Myzus persicae potentially involved in the transcytosis of beet western yellows virus particles in the aphid. Virology, 325, 399-412. https://doi.org/10.1016/j.virol.2004.05.014
Shen, Q. T., Ren, X., Zhang, R., Lee, I. H., & Hurley, J. H. (2015). HIV-1 Nef hijacks clathrin coats by stabilizing AP-1:Arf1 polygons. Science, 350, aac5137. https://doi.org/10.1126/science.aac5137
Tamborindeguy, C., Monsion, B., Brault, V., Hunnicutt, L., Ju, H. J., Nakabachi, A., & Van Fleet, E. (2010). A genomic analysis of transcytosis in the pea aphid, Acyrthosiphon pisum, a mechanism involved in virus transmission. Insect Molecular Biology, 19, 259-272. https://doi.org/10.1111/j.1365-2583.2009.00956.x
Timmermans, M. C., Das, O. P., & Messing, J. (1994). Geminiviruses and their uses as extrachromosomal replicons. Annual Review of Plant Physiology, 45, 79-112. https://doi.org/10.1146/annurev.pp.45.060194.000455
Wang, C., Timmons, C. L., Shao, Q., Kinlock, B. L., Turner, T. M., Iwamoto, A., … Liu, B. (2015). GB virus type C E2 protein inhibits human immunodeficiency virus type 1 Gag assembly by downregulating human ADP-ribosylation factor 1. Oncotarget, 6, 43293-43309. https://doi.org/10.18632/oncotarget.6537
Wang, H., Wu, K., Liu, Y., Wu, Y., & Wang, X. (2015). Integrative proteomics to understand the transmission mechanism of Barley yellow dwarf virus-GPV by its insect vector Rhopalosiphum padi. Scientific Reports, 5, 10971. https://doi.org/10.1038/srep10971
Wang, Y., Mao, Q., Liu, W., Mar, T., Wei, T., Liu, Y., & Wang, X. (2014). Localization and distribution of wheat dwarf virus in its vector leafhopper, Psammotettix alienus. Phytopathology, 104, 897-904. https://doi.org/10.1094/PHYTO-09-13-0251-R
Wei, T., & Li, Y. (2016). Rice reoviruses in insect vectors. Annual Review of Phytopathology, 54, 99-120. https://doi.org/10.1146/annurev-phyto-080615-095900
Whitfield, A. E., Ullman, D. E., & German, T. L. (2005). Tospovirus-thrips interactions. Annual Review of Phytopathology, 43, 459-489. https://doi.org/10.1146/annurev.phyto.43.040204.140017
Xia, W. Q., Liang, Y., Chi, Y., Pan, L. L., Zhao, J., Liu, S. S., & Wang, X. W. (2018). Intracellular trafficking of begomoviruses in the midgut cells of their insect vector. PLoS Pathogens, 14, e1006866. https://doi.org/10.1371/journal.ppat.1006866
Xu, Y., Wu, J. X., Fu, S., Li, C. Y., Zhu, Z. R., & Zhou, X. P. (2015). Rice stripe tenuivirus nonstructural protein 3 hijacks the 26s proteasome of the small brown planthopper via direct interaction with regulatory particle non-ATPase subunit 3. Journal of Virology, 89, 4296-4310. https://doi.org/10.1128/JVI.03055-14
Zhang, X., Zhou, G., & Wang, X. (2010). Detection of wheat dwarf virus (WDV) in wheat and vector leafhopper (Psammotettix alienus Dahlb.) by real-time PCR. Journal of Virological Methods, 169, 416-419. https://doi.org/10.1016/j.jviromet.2010.07.029