Comparison of transcriptomes of an orthotospovirus vector and non-vector thrips species
Autoři:
Anita Shrestha aff001; Donald E. Champagne aff002; Albert K. Culbreath aff003; Mark R. Abney aff004; Rajagopalbabu Srinivasan aff001
Působiště autorů:
Department of Entomology, University of Georgia, Griffin, GA, United States of America
aff001; Department of Entomology, University of Georgia, Athens, GA, United States of America
aff002; Department of Plant Pathology, University of Georgia, Tifton, GA, United States of America
aff003; Department of Entomology, University of Georgia, Tifton, GA, United States of America
aff004
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0223438
Souhrn
Thrips transmit one of the most devastating plant viruses worldwide–tomato spotted wilt tospovirus (TSWV). Tomato spotted wilt tospovirus is a type species in the genus Orthotospovirus and family Tospoviridae. Although there are more than 7,000 thrips species, only nine thrips species are known to transmit TSWV. In this study, we investigated the molecular factors that could affect thrips ability to transmit TSWV. We assembled transcriptomes of a vector, Frankliniella fusca [Hinds], and a non-vector, Frankliniella tritici [Fitch], and performed qualitative comparisons of contigs associated with virus reception, virus infection, and innate immunity. Annotations of F. fusca and F. tritici contigs revealed slight differences across biological process and molecular functional groups. Comparison of virus cell surface receptors revealed that homologs of integrin were present in both species. However, homologs of another receptor, heperan sulfate, were present in F. fusca alone. Contigs associated with virus replication were identified in both species, but a contig involved in inhibition of virus replication (radical s-adenosylmethionine) was only present in the non-vector, F. tritici. Additionally, some differences in immune signaling pathways were identified between vector and non-vector thrips. Detailed investigations are necessary to functionally characterize these differences between vector and non-vector thrips and assess their relevance in orthotospovirus transmission.
Klíčová slova:
DNA-binding proteins – Phylogenetic analysis – Sulfates – Sequence databases – Transcriptome analysis – Gene ontologies – Tomato spotted wilt virus – Pattern recognition receptors
Zdroje
1. Scholthof KB, Adkins S, Czosnek H, Palukaitis P, Jacquot E, Hohn T, et al. Top 10 plant viruses in molecular plant pathology. Mol Plant Pathol. 2011;12: 938–954. doi: 10.1111/j.1364-3703.2011.00752.x 22017770
2. Kitajima EW, Resende RD, de Avila AC, Goldbach R, Peters, D. Immuno-electron microscopical detection of Tomato spotted wilt virus and its nucleocapsids in crude plant extracts. J Virol Meth. 1992;38: 313–322.
3. Goldbach R. and Peters D. Molecular and biological aspects of tospoviruses. In: Elliott R, editor.The Bunyaviridae. Springer US; 1996. pp.129–157.
4. Ullman DE, Sherwood JL, German TL. Thrips as vectors of plant pathogens. In: Lewis TE, editor, Thrips as Crop Pests., CAB International, New York; 1997. pp. 539–565.
5. Ullman DE, Medeiros RB, Campbell LR, Whitfield AE, Sherwood JL, German TL. Thrips as vectors of tospoviruses. Adv Bot Res. 2002; 36:113–140.
6. Riley DG, Joseph SV, Srinivasan R, Diffie S. Thrips vectors of tospoviruses. J Integ Pest Mngmt. 2011; 2: I1–I10.
7. Pappu HR, Jones RAC, Jain RK. Global status of Tospovirus epidemics in diverse cropping systems: Successes achieved and challenges ahead. Vir Res. 2009; 141: 219–236.
8. Mound LA. So many thrips—so few tospoviruses? In: Marullo R, Mound LA, editors. Thrips and Tospoviruses: Proceedings of the 7th International Symposium of Thysanoptera. Canberra: Australian National Insect Collection; 2002. pp. 3–6.
9. Inoue T, Sakurai T, Murai T, Maeda T. Specificity of accumulation and transmission of Tomato spotted wilt virus in two genera, Frankliniella and Thrips (Thysanoptera: Thripidae). Bull Entomol Res. 2004; 94: 501–507. 15541189
10. Assis Filho FM, Staviskly J, Reitz SR, Deom CM, Sherwood JL. Midgut infection by Tomato spotted wilt virus and vector incompetence of Frankliniella tritici. J Appl Entomol. 2005; 129: 548–550.
11. Nagata T, Inoue-Nagata AK, Smid HM, Goldbach R, Peters D. Tissue tropism related to vector competence of Frankliniella occidentalis for tomato spotted wilt tospovirus. J Gen Virol. 1999; 80: 507–515. doi: 10.1099/0022-1317-80-2-507 10073714
12. Kritzman A, Gera A, Raccah B, van Lent JWM, Peters D. The route of Tomato spotted wilt virus inside the thrips body in relation to transmission efficiency. Arch Virol. 2002; 147: 2143–2156. doi: 10.1007/s00705-002-0871-x 12417949
13. Assis Filho FM, Naidu RA, Deom CM, Sherwood JL. Dynamics of Tomato spotted wilt virus replication in the alimentary canal of two thrips species. Phytopathology. 2002; 92: 729–33. doi: 10.1094/PHYTO.2002.92.7.729 18943268
14. Mortiz G, Kumm S, Mound L. Tospovirus transmission depends on thrips ontogeny. Virus Res. 2004;100: 143–149. doi: 10.1016/j.virusres.2003.12.022 15036845
15. Whitfield AE, Ullman DE, German TL. Tospovirus -thrips interactions. Annu Rev Phytopathol. 2005;43: 459–489. doi: 10.1146/annurev.phyto.43.040204.140017 16078892
16. Nagata T, Inoue-Nagata AK, van Lent J, Goldbach R, Peters D. Factors determining vector competence and specificity for transmission of Tomato spotted wilt virus. J Gen Virol. 2002;83: 663–671. doi: 10.1099/0022-1317-83-3-663 11842261
17. Ullman DE, Cho JJ, Maru RFL, Wescot DM, Custer DM. A midgut barrier to Tomato spotted wilt virus acquisition by adult western flower thrips. Phytopathology. 1992;82: 1333–1342.
18. Washburn JO, Kirkpatrick BA, Volkman LE. Insect protection against viruses. Nature. 1996;383: 767–769.
19. Irving P, Troxler L, Heuer TS, Belvin M, Kopczynski C, Reichhart JM, et al. A genome-wide analysis of immune responses in Drosophila. Proc Natl Acad Sci. 2001;98: 15119–15124. doi: 10.1073/pnas.261573998 11742098
20. Tunaz H, Park Y, Buyukguzel K, Bedick JC, Nor Aliza AR, Stanley DW. Eicosanoids in insect immunity: bacterial infection stimulates hemocytic phospholipase A2 activity in tobacco hornworms. Arch Insect Biochem Physiol. 2003;52: 1–6. doi: 10.1002/arch.10056 12489129
21. Wang XH, Aliyari R, Li WX, Li HW, Kim K, Carthew R, et al. RNA interference directs innate immunity against viruses in adult Drosophila. Molecular Biosciences. 2006;312: 452–454.
22. Koizumi N, Morozumi A, Imamura M, Tanaka E, Iwahana H, Sato R. Lipo-polysaccharide-binding proteins and their involvement in the bacterial clearance fro the hemoymph of the silkwork Bombyx mori. Eur J Biochem. 1997;248: 217–224. doi: 10.1111/j.1432-1033.1997.t01-1-00217.x 9310381
23. Hultmark D. Drosophila immunity: paths and patterns. Curr Opin Immunol. 2003;15: 12–19. doi: 10.1016/s0952-7915(02)00005-5 12495727
24. Tania K, Furukawa S, Shono T, Yamakawa M. Elicitors triggering the simultaneous gene expression of antibacterial proteins of the silkworm, Bombyx mori. Biochem Biophys Res Commun. 1996;226: 783–790. doi: 10.1006/bbrc.1996.1429 8831690
25. Jiang H. and Kanost MR. The clip-domain family of serine proteinases arthropods. Insect Biochem Mol Biol. 2000;30: 95–105. 10696585
26. Imler JK. and Bulet P. Antimicrobial peptides and activation of immune responses in Drosophila: structures, activities and gene regulation. Chem Immunol Allergy. 2005;86: 1–21. doi: 10.1159/000086648 15976485
27. Grove J. and Marsh M. The cell biology of receptor-mediated virus entry. J Cell Bio. 2011;195: 1071–1082.
28. Bandla MD, Campbell LR, Ullman DE, Sherwood JL. (1998) Interaction of tomato spotted wilt tospovirus (TSWV) glycoproteins with a thrips midgut protein, a potential cellular receptor for TSWV. Phytopathology. 1998;88: 98–104. doi: 10.1094/PHYTO.1998.88.2.98 18944977
29. Garry CE and Garry RF (2004) 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. doi: 10.1186/1742-4682-1-10 15544707
30. Gavrilovskaya IN, Shepley M, Shaw R, Ginsberg MH, Mackow ER. (1998) beta3 Integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc Natl Acad Sci. 1998;95: 7074–7079. doi: 10.1073/pnas.95.12.7074 9618541
31. Lozach PY, Kuhbacher A, Meier R, Mancini R, Bitto D, Bouloy M, et al. DC-SIGN as a receptor for phleboviruses. Cell host Microb. 2011;10: 75–88.
32. Xiao X, Feng Y, Zhu Z, Dimitrov DS. Identification of a putative Crimean-congo hemorrhagic fever virus entry factor. Biochem Biophys Res Commun 2011; 411: 253–258. doi: 10.1016/j.bbrc.2011.06.109 21723257
33. de Boer SM, Kortekaas J, de Haan CAM, Rottier PJM, Moormann RJM, Bosch BJ. Heparan sulfate facilitates Rift Valley Fever Virus entry into the cell. J Virol. 2012;86: 13767–13771. doi: 10.1128/JVI.01364-12 23015725
34. 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: 226–237. doi: 10.1016/j.virol.2016.10.009 27835811
35. Shrestha A, Rotenberg D, Whitfield AE, Culbreath A, Champagne DE, Srinivasan R. Transcriptome changes associated with Tomato spotted wilt virus infection in various life stages of its thrips vector, Frankliniella fusca. J Gen Virol. 2017;98: 2156–2170. doi: 10.1099/jgv.0.000874 28741996
36. Buchmann JP. and Holmes EC. Cell walls and the convergent evolution of the viral envelope. Microbiology and Molecular Biology Reviews. 2015;79:403–418. doi: 10.1128/MMBR.00017-15 26378223
37. Plemper RK. Cell entry of enveloped viruses. Curr Opin Virol. 2011;1:92–100. doi: 10.1016/j.coviro.2011.06.002 21927634
38. Sarrazin S, Lamanna WC, Esko JD. Heparan sulfate proteoglycans. Cold Spring Harb Perspect Biol. 2011;3: a004952. doi: 10.1101/cshperspect.a004952 21690215
39. Liu J. and Thorp SC. Cell surface heparan sulfate and its roles in assisting viral infections. Med Res Rev. 2001;22: 1–25.
40. Sinnis P, Coppi A, Toida T, Toyoda H, Kinoshita-Toyoda A, Xie J, et al. Mosquito heparan sulfate and its potential role in malaria infection and transmission. J Biol Chem. 2007;282: 25376–25384. doi: 10.1074/jbc.M704698200 17597060
41. WuDunn D. and Spear PG. Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J Virol. 1989;63: 52–58. 2535752
42. Tyagi M, Rusnati M, Presta M, Giacca M. Internalization of HIV-1 Tat requires cell surface heparan sulfate proteoglycans. J Biol Chem. 2001;276: 3254–3261. doi: 10.1074/jbc.M006701200 11024024
43. Giroglou T, Florin L, Schafer F, Streeck RE, Sapp M. Human papillomavirus infection requires cell surface heparan sulfate. J. Virol. 2001;75: 1565–1570. doi: 10.1128/JVI.75.3.1565-1570.2001 11152531
44. Guibinga GH, Miyanohara A, Esko JD, Friedmann T. Cell surface heparan sulfate is a receptor for attachment of envelope protein-free retrovirus-like particles and vsv-g pseudotyped mlv-derived retrovirus vectors to target cells. Mol Ther. 2002;5: 538–546. doi: 10.1006/mthe.2002.0578 11991744
45. Hilgard P and Stockert R. Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes. Hepatology. 2000;32: 1069–1077. doi: 10.1053/jhep.2000.18713 11050058
46. Birkmann A, Mahr K, Ensser A, Yaguboglu S, Titgemeyer F, Fleckenstein B, et al. Cell surface heparan sulfate is a receptor for human herpesvirus 8 and interacts with envelope glycoprotein K8.1. J Virol. 2011;75: 11583–11593.
47. Germi R, Crance JM, Garin D, Guimet J, Lortat-Jacob H, Ruigrok RW, et al Heparan sulfate-mediated binding of infectious dengue virus type 2 and yellow fever virus. Virology. 2002;292: 162–168. doi: 10.1006/viro.2001.1232 11878919
48. Riblett AM, Blomen VA, Jae LT, Altamura LA, Doms RW, Brummelkamp TR, et al. A Haploid genetic screen identifies heparan sulfate proteoglycans supporting Rift Valley fever virus infection. J Virol. 2015;90: 1414–1423. doi: 10.1128/JVI.02055-15 26581979
49. Albornoz A, Hoffmann AB, Lozach PY, Tischler ND. Early Bunyavirus-host cell interactions. Viruses. 2016;8: 143; doi: 10.3390/v8050143 27213430
50. Sasaki M, Anindita PD, Ito N, Sugiyama M, Carr M, Fukuhara H, et al. The role of heparan sulfate proteoglycans as an attachment factor for rabies virus entry and infection. J Infect Dis. 2018;217: 1740–1749. doi: 10.1093/infdis/jiy081 29529215
51. Lahaye X, Vidy A, Fouquet B, Blondel D. Hsp70 protein positively regulates Rabies virus infection. J Virol. 2012;86: 4743–4751. doi: 10.1128/JVI.06501-11 22345440
52. Manzoor R, Kuroda K, Yoshida R, Tsuda Y, Fujikura D, Miyamoto H, et al. Heat shock protein 70 modulates Influenza A virus polymerase activity. J Biol Chem. 2014;289: 7599–614. doi: 10.1074/jbc.M113.507798 24474693
53. Johnston JB, Wang G, Barrett JW, Nazarian SH, Colwill K, Moran M, et al. Myxoma virus M-T5 protects infected cells from the stress of cell cycle arrest through its interaction with host cell cullin-1. J Virol. 2005;79: 10750–10763. doi: 10.1128/JVI.79.16.10750-10763.2005 16051867
54. Kim S, Ishida H, Yamane D, Yi M, Swinney DC, Foung S, et al. Contrasting roles of mitogen-activated protein kinases in cellular entry and replication of Hepatitis C Virus: MKNK1 facilitates cell entry. J Virol. 2012;87: 4214–4224.
55. Abbas W, Dichamp I, Herbein G. The HIV-1 Nef Protein interacts with two components of the 40S small ribosomal subunit, the RPS10 protein and the 18S rRNA. Virol J. 2012;9: 103. doi: 10.1186/1743-422X-9-103 22672539
56. Cristea IM, Rozjabek H, Molloy KR, Karki S, White LL, Rice CM, et al. Host factors associated with the Sindbis virus RNA-dependent RNA polymerase: role for G3BP1 and G3BP2 in virus replication. J Virol. 2010;84: 6720–6732. doi: 10.1128/JVI.01983-09 20392851
57. Yi Z, Pan T, Wu X, Song W, Wang S, Xu Y, et al. Hepatitis c virus co-opts ras-GTPase-activating protein-binding protein 1 for Its genome replication. J Virol 2011;85: 6996–7004. doi: 10.1128/JVI.00013-11 21561913
58. Daub H, Blencke S, Habenberger P, Kurtenbach A, Dennenmoser J, Wissing J, et al. Identification of SRPK1 and SRPK2 as the major cellular protein kinases phosphorylating Hepatitis B virus core protein. J Virol. 2002;76: 8124–8137. doi: 10.1128/JVI.76.16.8124-8137.2002 12134018
59. Copeland AM, Newcomb WW, Brown JC. Herpes simplex virus replication: roles of viral proteins and nucleoporins in capsid-nucleus attachment. J Virol. 2009;83: 1660–1668. doi: 10.1128/JVI.01139-08 19073727
60. Nelp MT, Young AP, Stepanski BM, Bandarian V. Human Viperin Causes Radical SAM-Dependent Elongation of Escherichia coli, Hinting at Its Physiological Role. Biochemistry. 2017;56: 3874–3876. doi: 10.1021/acs.biochem.7b00608 28708394
61. Seo JY, Yaneva R, Cresswell P. Viperin: a multifunctional, interferon-inducible protein that regulates virus replication. Cell Host Microbe. 2012;10: 534–539.
62. Chin KC and Cresswell P. Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus. Proc Natl Acad Sci. 2001;98: 15125–15130. doi: 10.1073/pnas.011593298 11752458
63. Wang X, Hinson ER, Cresswell P. The interferon-inducible protein Viperin inhibits Influenza virus release by porturbing lipid rafts. Cell Host Microb. 2007; 2: 96–105.
64. Zhang Y, Burke CW, Ryman KD, Klimstra WB. Identification and Characterization of Interferon-Induced Proteins That Inhibit Alphavirus Replication. J Virol. 2007;81: 11246–11255. doi: 10.1128/JVI.01282-07 17686841
65. Tang H-B, L Z-L1, Wei X-K, Zhong T-Z, Zhong Y-Z, Ouyang L-X, et al. Viperin inhibits rabies virus replication via reduced cholesterol and sphingomyelin and is regulated upstream by TLR4. Scientific Reports. 2016;6: 30529, doi: 10.1038/srep30529 27456665
66. Tang YD, Na L, Zhu C-H, Shen N, Yang F, Fu X-Q, et al. Equine Viperin Restricts Equine Infectious Anemia Virus Replication by Inhibiting the Production and/or Release of Viral Gag, Env, and Receptor via Distortion of the Endoplasmic Reticulum. J Virol. 2014;88: 12296–12310. doi: 10.1128/JVI.01379-14 25122784
67. Avadhanula V, Weasner BP, Hardy GG, Kumar JP, Hardy RW. A novel system for the launch of alphavirus RNA synthesis reveals a rold for the Imd pathways in arthropod antiviral response. PLoS Pathogens. 2009;5: e1000582. doi: 10.1371/journal.ppat.1000582 19763182
68. Costa A, Jan E, Sarnow P, Schneider D. The Imd pathways is involved in antiviral immune responses in Drosophila. PLOS ONE. 2009;4: e7436. doi: 10.1371/journal.pone.0007436 19829691
69. Myllymaki H, Valanne S, Ramet M. The Drosophila Imd signaling pathway. J Immunol. 2014;192: 3455–3462. doi: 10.4049/jimmunol.1303309 24706930
70. Mound AM and Kibby G. Thysanoptera: an identification guide. 2nd ed., CAB international, Wallingford, UK; 1998.
71. Munger F. A method of rearing citrus thrips in the laboratory. J Econ Entomol. 1942;35: 373–375.
72. Boigner AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30: 2114–2120. doi: 10.1093/bioinformatics/btu170 24695404
73. Grabherr MG, Hass BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotech. 2011;29: 644–652.
74. Parra G, Brandnam K, Korf I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genornes. Bioinformatics. 2007;23: 1061–1067. doi: 10.1093/bioinformatics/btm071 17332020
75. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. Busco: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015; doi: 10.1093/bioinformatics/btv351 26059717
76. Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, et al. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 2008.36: 3420–3435. doi: 10.1093/nar/gkn176 18445632
77. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003;13: 2178–2189. doi: 10.1101/gr.1224503 12952885
78. Shukla D, Liu J, Blaiklock P, Shworak NW, Bai X, Esko JD, et al. A novel role of 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell. 1999;99: 13–22. doi: 10.1016/s0092-8674(00)80058-6 10520990
79. Maddison WP, Maddison DR. Mesquite: a modular system for evolutionary analysis. 2011. http://mesquiteproject.org.
80. Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES science gateway for inference of large phylogenetic trees. In: Proceedings of the gateway computing environments workshop, 14 Nov., New Oreleans, LA. 2011; 1–8.
81. Rambaut A. FigTree v1.4.2. 2014; http://tree.bio.ed.ac.uk/software/figtree/
82. Zou Z, Evans JD, Lu Z, Zhao P, Williams M, Sumathipala N, et al. Comparative genomic analysis of the Tribolium immune system. Genome Biol. 2007;8: R177. doi: 10.1186/gb-2007-8-8-r177 17727709
83. Gerardo NM, Altincicek B, Anselme C, Atamian H, Barribeau SM, de vos M, et al. Immunity and other defenses in pea aphids Acrythosiphons pisum. Genome Biol. 2010;11: R21. doi: 10.1186/gb-2010-11-2-r21 20178569
84. Tanaka H, Ishibashi J, Fujita K, Nakajima Y, Sagisaka A, Tomimoto K, et al. A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem Mol Biol. 2008;38: 1087–1110. doi: 10.1016/j.ibmb.2008.09.001 18835443
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