Abstract
Groundnut bud necrosis virus (GBNV) is an economically important tospovirus transmitted by Thrips palmi (Thysanoptera: Thripidae). The current understanding of thrips-tospovirus interactions is largely based on the tomato spotted wilt virus-Frankliniella occidentalis relationship. Only limited information is available for the GBNV-T. palmi system. In the present study, available genome data of T. palmi and GBNV were used to predict the protein partners that may play a crucial role in the internalization of GBNV virions into thrips cells. Computational analyses showed that the GBNV precursor glycoprotein bears a signal peptide of 24 amino acids and a secondary cleavage site at position 434–435 separates the amino-terminal mature glycoprotein (GN) from the carboxyl-terminal glycoprotein (GC). Potential interactions of GBNV glycoproteins were predicted with T. palmi enolase, cathepsin, C-type lectin, clathrin and vacuolar ATP synthase subunit E. The in silico analyses suggested that C-type lectin is the primary cellular receptor to interact with GBNV-GN. After receptor binding, virus particles probably enter vector cells by clathrin-mediated endocytosis. This is the first in silico evidence of GBNV-T. palmi protein interaction.
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Albornoz A, Hoffmann AB, Lozach PY, Tischler ND. Early bunyavirus-host cell interactions. Viruses. 2016;8:143.
Andrusier N, Nussinov R, Wolfson HJ. FireDock: fast interaction refinement in molecular docking. Proteins. 2007;69:139–59.
Badillo-Vargas IE, Rotenberg D, Schneweis DJ, Hiromasa Y, Tomich JM, Whitfield AE. Proteomic analysis of Frankliniella occidentalis and differentially expressed proteins in response to Tomato Spotted Wilt Virus infection. J Virol. 2012;86:8793–809.
Chandran K, Sullivan NJ, Felbor U, Whelan SP, Cunningham JM. Endosomal proteolysis of the ebola virus glycoprotein is necessary for infection. Science. 2005;308:1643–5.
Duhovny D, Nussinov R, Wolfson HJ (2002) Efficient unbound docking of rigid molecules. In: International workshop on algorithms in bioinformatics, Springer, Berlin, pp 185–200.
Evgeny K. Crystal contacts as nature’s docking solutions. J Comput Chem. 2010;31:133–43.
Garry CE, Garry RF. Proteomics computational analyses suggest that the carboxyl terminal glycoproteins of bunyaviruses are class II viral fusion protein (beta-penetrenes). Theor Biol Med Model. 2004;1:10.
Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 2003;31:3784–8.
Ghosh A, Dey D, Timmanna, Basavaraj, Mandal B, Jain RK (2017) Thrips as the vectors of tospoviruses in Indian agriculture. In: A century of plant virology in India, Springer, Singapore, pp 537–561.
Guex N, Peitsch MC. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis. 1997;18:2714–23.
Hofmann H, Li X, Zhang X, Liu W, Kuhl A, Kaup F, Soldan SS, Gonzalez-Scarano F, Weber F, He Y, Pohlmann S. Severe fever with thrombocytopenia virus glycoproteins are targeted by neutralizing antibodies and can use DC-SIGN as a receptor for pH-dependent entry into human and animal cell lines. J Virol. 2013;87:4384–94.
Hofmann K, Stoffel W. TMbase—a database of membrane spanning proteins segments. Bio Chem Hoppe-Seyler. 1993;374:166.
Hollidge BS, Nedelsky NB, Salzano MV, Fraser JW, Gonzalez-Scarano F, Soldan SS. Orthobunyavirus entry into neurons and other mammalian cells occurs via clathrin-mediated endocytosis and requires trafficking into early endosomes. J Virol. 2012;86:7988–8001.
Kreyszig E. Advanced engineering mathematics. 4th ed. Berlin: Wiley; 1979. p. 880. ISBN 0-471-02140-7.
Krissinel E, Henrick K (2005) Detection of protein assemblies in crystals. In: International symposium on computational life science, Springer, Berlin, pp 163–174.
Krissinel E, Henrick K. Inference of macromolecular assemblies from crystalline state. J Mol Biol. 2007;372:774–97.
Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305:567–80.
Kumar R, Mandal B, Geetanjali AS, Jain RK, Jaiwal PK. Genome organisation and sequence comparison suggest intraspecies incongruence in M RNA of Watermelon bud necrosis virus Archieves of. Virology. 2010;155:1361–5.
Léger P, Tetard M, Youness B, Cordes N, Rouxel RN, Flamand M, Lozach PY. Differential use of the C-type lectins L-SIGN and DC-SIGN for Phlebovirus endocytosis. Traffic. 2016;17:639–56.
Löber C, Anheier B, Lindow S, Klenk HD, Feldmann H. The Hantaan virus glycoprotein precursor is cleaved at the conserved pentapeptide WAASA. Virology. 2001;289:224–9.
Lozach PY, Kühbacher A, Meier R, Mancini R, Bitto D, Bouloy M, Helenius A. DC-SIGN as a receptor for phleboviruses. Cell Host Microbe. 2011;10:75–88.
Mandal B, Jain RK, Krishnareddy M, Krishna Kumar NK. Emerging problems of tospoviruses (Bunyaviridae) and their management in the Indian subcontinent. Plant Dis. 2012;96:468–78.
Martoglio B, Dobberstein B. Signal sequences: more than just greasy peptides. Trends Cell Biol. 1998;8:410–5.
Mashiach E, Mashiach E, Schneidman-Duhovny D, Schneidman-Duhovny D, Andrusier N, Andrusier N, Nussinov R, Nussinov R, Wolfson HJ. FireDock: a web server for fast interaction refinement in molecular docking. Nucleic Acids Res. 2008;36:229–32.
Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, Frandsen PB, Ware J, Flouri T, Beutel RG, Niehuis O, Petersen M, Izquierdo-Carrasco F, Wappler T, Rust J, Aberer AJ, Aspöck U, Aspöck H, Bartel D, Blanke A, Berger S, Böhm A, Buckley TR, Calcott B, Chen J, Friedrich F, Fukui M, Fujita M, Greve C, GrobeP GuS, Huang Y, Jermiin LS, Kawahara AY, Krogmann L, Kubiak M, Lanfear R, Letsch H, Li Y, Li Z, Li J, Lu H, Machida R, Mashimo Y, Kapli P, McKenna DD, Meng G, Nakagaki Y, Navarrete-Heredia JL, Ott M, Ou Y, Pass G, Podsiadlowski L, Pohl H, Von Reumont BM, Schütte K, Sekiya K, Shimizu S, Slipinski A, Stamatakis A, Song W, Su X, Szucsich NU, Tan M, Tan X, Tang M, Tang J, Timelthaler G, Tomizuka S, Trautwein M, Tong X, Uchifune T, Walzl MG, Wiegmann BM, Wilbrandt J, Wipfler B, Wong TKF, Wu Q, Wu G, Xie Y, Yang S, Yang Q, Yeates DK, Yoshizawa K, Zhang Q, Zhang R, Zhang W, Zhang Y, Zhao J, Zhou C, Zhou L, Ziesmann T, Zou S, Li Y, Xu X, Zhang Y, Yang H, Wang J, Wang J, Kjer KM, Zhou X. Phylogenomics resolves the timing and pattern of insect evolution. Science. 2014;346:763–7.
Petersen TN, Brunak S, Von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8:785–6.
Pierce BG, Wiehe K, Hwang H, Kim BH, Vreven T, Weng Z. ZDOCK server: interactive docking prediction of protein-protein complexes and symmetric multimers. Bioinformatics. 2014;30:1771–3.
Ramachandran S, Kota P, Ding F, Dokholyan NV. Automated minimization of steric clashes in protein structures. Proteins. 2011;79:261–70.
Reddy DVR, Buiel AAMT, Satyanarayana SL, Dwivedi AS, Reddy AS et al. (1995) Peanut bud necrosis virus disease: an overview in Recent Studies on Peanut Bud Necrosis Disease, Patancheru, India, 20 March 1995, ICRISAT Asia Centre pp 3–7.
Sakimura K. Frankliniella fusca, an additional vector for the tomato spotted wilt virus, with notes on Thrips tabaci, a thrips vector. Phytopathology. 1963;53:412–5.
Šali A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol. 1993;234:779–815.
Schneidman-Duhovny D, Inbar Y, Nussinov R, Wolfson HJ. PatchDock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res. 2005;33:363–7.
Schneweis DJ, Whitfield AE, Rotenberg D. Thrips developmental stage-specific transcriptome response to tomato spotted wilt virus during the virus infection cycle in Frankliniella occidentalis, the primary vector. Virology. 2017;500:226–37.
Shrestha A, Champagne DE, Culbreath AK, Rotenberg D, Whitfield AE, Srinivasan R. Transcriptome changes associated with Tomato spotted wilt virus infection in various life stages of its thrips vector, Frankliniella fusca (Hinds). J Gen Virol. 2017;98:2156–70.
Steentoft C, Vakhrushev SY, Joshi HJ, Kong Y, Vester-Christensen MB, Schjoldager KTBG, Lavrsen K, Dabelsteen S, Pedersen NB, Marcos-Silva L, Gupta R, Paul Bennett E, Mandel U, Brunak S, Wandall HH, Levery SB, Clausen H. Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. The EMBO J. 2013;32:1478–88.
Švajger U, Anderluh M, Jeras M, Obermajer N. C-type lectin DC-SIGN: an adhesion, signalling and antigen-uptake molecule that guides dendritic cells in immunity. Cell Signal. 2010;22:1397–405.
Tusnády GE, Simon I. Principles governing amino acid composition of integral membrane proteins: applications to topology prediction. J Mol Biol. 1998;283:489–506.
Ullman DE, German TL, Sherwood JL, Westcot DM. Thrips biology and management. New York: Plenum; 1992. p. 135–52.
Ullman DE, Sherwood J, German TL. Thrips as vectors of plant pathogens. In: Lewis T, editor. Thrips as crop pests. New York: CAB International; 1997. p. 539–65.
Vijayalakshmi K (1994) Transmission and ecology of Thrips palmi Karny, the vector of peanut bud necrosis virus in Ph.D. thesis Andhra Pradesh Agril University, Rajendranagar, Hydarabad India, p 120.
Wheeler DL, Church DM, Federhen S, Lash AE, Madden TL, Pontius JU, Schuler GD, Schriml LM, Sequeira E, Tatusova TA, Wagner L. Database resources of the national center for biotechnology. Nucleic Acids Res. 2003;31:28–33.
Whitfield AE, Ullman DE, German TL. Expression and characterization of a soluble form of tomato spotted wilt virus glycoprotein Gn. J Virol. 2004;78:13197–206.
Whitfield AE, Ullman DE, German TL. Tomato spotted wilt virus glycoprotein Gc is cleaved at acidic pH. Virus Res. 2005;110:183–6.
Whitfield AE, Ullman DE, German TL. Tospovirus-thrips interactions. Annu Rev Phytopathol. 2005;43:459–89.
Widana Gamage SMK, Rotenberg D, Schneweis DJ, Tsai C-W, Dietzgen RG. Transcriptome-wide responses of adult melon thrips (Thrips palmi) associated with capsicum chlorosis virus infection. PLoS ONE. 2018;13:e0208538.
Wiederstein M, Sippl MJ. ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res. 2007;35:407–10.
Zhang F, Guo H, Zheng H, Zhou T, Zhou Y, Wang S, Fang R, Qian W, Chen X. Massively parallel pyrosequencing-based transcriptome analyses of small brown planthopper (Laodelphax striatellus), a vector insect transmitting rice stripe virus (RSV). BMC Genom. 2010;11:303.
Zhang Y. I-TASSER server for protein 3D structure prediction. BMC Bioinform. 2008;9:40.
Acknowledgments
The authors are thankful to Dr. Ralf. G. Dietzgen (QAAFI, the University of Queensland) for thorough read and editing of the final manuscript. We thank Dr. Dinesh Gupta (ICGEB, New Delhi) and Dr. Abhishek Mandal (IARI, New Delhi) for suggestions and discussions during the analyses. Two anonymous reviewers are thanked for critically reading the manuscript and suggesting substantial improvements. The research was supported by the research grants of IARI, and DBT (BT/PR26136/AGIII/103/1005/2018).
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Jagdale, S.S., Ghosh, A. In silico analyses of molecular interactions between groundnut bud necrosis virus and its vector, Thrips palmi. VirusDis. 30, 245–251 (2019). https://doi.org/10.1007/s13337-019-00521-w
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DOI: https://doi.org/10.1007/s13337-019-00521-w