1887

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Volume 105, Issue 1

WIV, a protein domain found in a wide number of arthropod viruses, which probably facilitates infection No Access

Abstract

The most powerful approach to detect distant homologues of a protein is based on structure prediction and comparison. Yet this approach is still inapplicable to many viral proteins. Therefore, we applied a powerful sequence-based procedure to identify distant homologues of viral proteins. It relies on three principles: (1) traces of sequence similarity can persist beyond the significance cutoff of homology detection programmes; (2) candidate homologues can be identified among proteins with weak sequence similarity to the query by using ‘contextual’ information, e.g. taxonomy or type of host infected; (3) these candidate homologues can be validated using highly sensitive profile–profile comparison. As a test case, this approach was applied to a protein without known homologues, encoded by ORF4 of Lake Sinai viruses (which infect bees). We discovered that the ORF4 protein contains a domain that has homologues in proteins from >20 taxa of viruses infecting arthropods. We called this domain ‘widespread, intriguing, versatile’ (WIV), because it is found in proteins with a wide variety of functions and within varied domain contexts. For example, WIV is found in the NSs protein of tospoviruses, a global threat to food security, which infect plants as well as their arthropod vectors; in the RNA2 ORF1-encoded protein of chronic bee paralysis virus, a widespread virus of bees; and in various proteins of cypoviruses, which infect the silkworm . Structural modelling with AlphaFold indicated that the WIV domain has a previously unknown fold, and bibliographical evidence suggests that it facilitates infection of arthropods.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): arthropod virus , cypovirus , distant homology detection , insect virus , remote homology detection , small protrusion domain , SPD-like domain , structure prediction , thrips , tospovirus and virulence factor
© 2024 The Authors
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2024-01-09
2024-05-03
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References

  1. Karlin DG. WIV, a protein domain found in a wide number of arthropod viruses, which probably facilitates infection Microbiology Society Figshare 2024 [View Article]
     [Google Scholar]
  2. Koonin EV, Krupovic M, Dolja VV. The global virome: How much diversity and how many independent origins?. Environ Microbiol 2023; 25:40–44 [View Article] [PubMed]
     [Google Scholar]
  3. Zayed AA, Wainaina JM, Dominguez-Huerta G, Pelletier E, Guo J et al. Cryptic and abundant marine viruses at the evolutionary origins of Earth’s RNA virome. Science 2022; 376:156–162 [View Article] [PubMed]
     [Google Scholar]
  4. Neri U, Wolf YI, Roux S, Camargo AP, Lee B et al. Expansion of the global RNA virome reveals diverse clades of bacteriophages. Cell 2022; 185:4023–4037 [View Article] [PubMed]
     [Google Scholar]
  5. Kuchibhatla DB, Sherman WA, Chung BYW, Cook S, Schneider G et al. Powerful sequence similarity search methods and in-depth manual analyses can identify remote homologs in many apparently “orphan” viral proteins. J Virol 2014; 88:10–20 [View Article] [PubMed]
     [Google Scholar]
  6. Remmert M, Biegert A, Hauser A, Söding J. HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nat Methods 2012; 9:173–175 [View Article] [PubMed]
     [Google Scholar]
  7. Varadi M, Bertoni D, Magana P, Paramval U, Pidruchna I et al. AlphaFold protein structure database in 2024: providing structure coverage for over 214 million protein sequences. Nucleic Acids Res 2023gkad1011 [View Article] [PubMed]
     [Google Scholar]
  8. Marx V. Method of the year: protein structure prediction. Nat Methods 2022; 19:5–10 [View Article] [PubMed]
     [Google Scholar]
  9. Jumper J, Evans R, Pritzel A, Green T, Figurnov M et al. Highly accurate protein structure prediction with AlphaFold. Nature 2021; 596:583–589 [View Article] [PubMed]
     [Google Scholar]
  10. van Kempen M, Kim SS, Tumescheit C, Mirdita M, Lee J et al. Foldseek: fast and accurate protein structure search. Bioinformatics 2022 [View Article]
     [Google Scholar]
  11. Aravind L. Guilt by association: contextual information in genome analysis. Genome Res 2000; 10:1074–1077 [View Article] [PubMed]
     [Google Scholar]
  12. Coin L, Bateman A, Durbin R. Enhanced protein domain discovery using taxonomy. BMC Bioinformatics 2004; 5:56 [View Article] [PubMed]
     [Google Scholar]
  13. Boekhorst J, Snel B. Identification of homologs in insignificant blast hits by exploiting extrinsic gene properties. BMC Bioinformatics 2007; 8:356 [View Article] [PubMed]
     [Google Scholar]
  14. Ahola T, Karlin DG. Sequence analysis reveals a conserved extension in the capping enzyme of the alphavirus supergroup, and a homologous domain in nodaviruses. Biol Direct 2015; 10:16 [View Article] [PubMed]
     [Google Scholar]
  15. Rehanek M, Karlin DG, Bandte M, Al Kubrusli R, Nourinejhad Zarghani S et al. The complex world of Emaraviruses—challenges, insights, and prospects. Forests 2022; 13:1868 [View Article]
     [Google Scholar]
  16. Hou C, Liang H, Chen C, Zhao H, Zhao P et al. Lake Sinai virus is a diverse, globally distributed but not emerging multi-strain honeybee virus. Mol Ecol 2023; 32:3859–3871 [View Article] [PubMed]
     [Google Scholar]
  17. Daughenbaugh KF, Martin M, Brutscher LM, Cavigli I, Garcia E et al. Honey bee infecting Lake Sinai Viruses. Viruses 2015; 7:3285–3309 [View Article] [PubMed]
     [Google Scholar]
  18. Runckel C, Flenniken ML, Engel JC, Ruby JG, Ganem D et al. Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS ONE 2011; 6:e20656 [View Article] [PubMed]
     [Google Scholar]
  19. Parmentier L, Smagghe G, de Graaf DC, Meeus I. Varroa destructor Macula-like virus, Lake Sinai virus and other new RNA viruses in wild bumblebee hosts (Bombus pascuorum, Bombus lapidarius and Bombus pratorum). J Invertebr Pathol 2016; 134:6–11 [View Article] [PubMed]
     [Google Scholar]
  20. Bigot D, Dalmon A, Roy B, Hou C, Germain M et al. The discovery of Halictivirus resolves the Sinaivirus phylogeny. J Gen Virol 2017; 98:2864–2875 [View Article] [PubMed]
     [Google Scholar]
  21. McMenamin AJ, Flenniken ML. Recently identified bee viruses and their impact on bee pollinators. Curr Opin Insect Sci 2018; 26:120–129 [View Article] [PubMed]
     [Google Scholar]
  22. Hu G, Kurgan L. Sequence similarity searching. Curr Protoc Protein Sci 2019; 95:e71 [View Article] [PubMed]
     [Google Scholar]
  23. Zimmermann L, Stephens A, Nam S-Z, Rau D, Kübler J et al. A completely reimplemented MPI bioinformatics toolkit with a new HHpred server at its core. J Mol Biol 2018; 430:2237–2243 [View Article] [PubMed]
     [Google Scholar]
  24. Mushegian AR, Elena SF. Evolution of plant virus movement proteins from the 30K superfamily and of their homologs integrated in plant genomes. Virology 2015; 476:304–315 [View Article] [PubMed]
     [Google Scholar]
  25. Hildebrand A, Remmert M, Biegert A, Söding J. Fast and accurate automatic structure prediction with Hhpred: structure prediction with Hhpred. Proteins 2009; 77:128–132 [View Article]
     [Google Scholar]
  26. Dunbrack RL. Sequence comparison and protein structure prediction. Curr Opin Struct Biol 2006; 16:374–384 [View Article] [PubMed]
     [Google Scholar]
  27. Pei J, Tang M, Grishin NV. PROMALS3D web server for accurate multiple protein sequence and structure alignments. Nucleic Acids Res 2008; 36:W30–W34 [View Article] [PubMed]
     [Google Scholar]
  28. Chen Y-M, Sadiq S, Tian J-H, Chen X, Lin X-D et al. RNA viromes from terrestrial sites across China expand environmental viral diversity. Nat Microbiol 2022; 7:1312–1323 [View Article] [PubMed]
     [Google Scholar]
  29. Medd NC, Fellous S, Waldron FM, Xuéreb A, Nakai M et al. The virome of Drosophila suzukii, an invasive pest of soft fruit. Virus Evol 2018; 4:vey009 [View Article] [PubMed]
     [Google Scholar]
  30. Kondo H, Chiba S, Maruyama K, Andika IB, Suzuki N. A novel insect-infecting virga/nege-like virus group and its pervasive endogenization into insect genomes. Virus Res 2019; 262:37–47 [View Article] [PubMed]
     [Google Scholar]
  31. Mahar JE, Shi M, Hall RN, Strive T, Holmes EC. Comparative analysis of RNA virome composition in rabbits and associated ectoparasites. J Virol 2020; 94:e02119-19 [View Article] [PubMed]
     [Google Scholar]
  32. Valles SM, Oi DH, Becnel JJ, Wetterer JK, LaPolla JS et al. Isolation and characterization of Nylanderia fulva virus 1, a positive-sense, single-stranded RNA virus infecting the tawny crazy ant, Nylanderia fulva. Virology 2016; 496:244–254 [View Article] [PubMed]
     [Google Scholar]
  33. Valles SM, Rivers AR. Nine new RNA viruses associated with the fire ant Solenopsis invicta from its native range. Virus Genes 2019; 55:368–380 [View Article] [PubMed]
     [Google Scholar]
  34. Lee C-C, Hsu H-W, Lin C-Y, Gustafson N, Matsuura K et al. First polycipivirus and unmapped RNA virus diversity in the yellow crazy ant, Anoplolepis gracilipes. Viruses 2022; 14:2161 [View Article] [PubMed]
     [Google Scholar]
  35. Webster CL, Longdon B, Lewis SH, Obbard DJ. Twenty-five new viruses associated with the Drosophilidae (Diptera). Evol Bioinform Online 2016; 12:13–25 [View Article] [PubMed]
     [Google Scholar]
  36. Hernández-Pelegrín L, Llopis-Giménez Á, Crava CM, Ortego F, Hernández-Crespo P et al. Expanding the medfly virome: viral diversity, prevalence, and sRNA profiling in mass-reared and field-derived medflies. Viruses 2022; 14:623 [View Article] [PubMed]
     [Google Scholar]
  37. He Y-J, Ye Z-X, Zhang C-X, Li J-M, Chen J-P et al. An RNA virome analysis of the pink-winged grasshopper Atractomorpha sinensis. Insects 2022; 14:9 [View Article] [PubMed]
     [Google Scholar]
  38. Charles J, Tangudu CS, Hurt SL, Tumescheit C, Firth AE et al. Discovery of a novel Tymoviridae-like virus in mosquitoes from Mexico. Arch Virol 2019; 164:649–652 [View Article] [PubMed]
     [Google Scholar]
  39. Krell PJ. Reoviruses of Invertebrates (Reoviridae). In Encyclopedia of Virology Elsevier; 2021 pp 867–882 [View Article]
     [Google Scholar]
  40. Takatsuka J. A new cypovirus from the Japanese peppered moth, Biston robustus. J Invertebr Pathol 2020; 174:107417 [View Article] [PubMed]
     [Google Scholar]
  41. Karlin D. An overlooked protein domain, WIV, is found a wide number of arthropod viruses and probably facilitates infection. Biol Life Sci 2023 [View Article]
     [Google Scholar]
  42. Katsuma S, Tanaka S, Omuro N, Takabuchi L, Daimon T et al. Novel macula-like virus identified in Bombyx mori cultured cells. J Virol 2005; 79:5577–5584 [View Article] [PubMed]
     [Google Scholar]
  43. Verdonckt T-W, Bilsen A, Van Nieuwerburgh F, De Troij L, Santos D et al. Identification and profiling of a novel Bombyx mori latent virus variant acutely infecting Helicoverpa armigera and Trichoplusia ni. Viruses 2023; 15:1183 [View Article]
     [Google Scholar]
  44. Bejerman N, Debat H. Exploring the tymovirales landscape through metatranscriptomics data. Arch Virol 2022; 167:1785–1803 [View Article] [PubMed]
     [Google Scholar]
  45. Katsuma S, Kawamoto M, Shoji K, Aizawa T, Kiuchi T et al. Transcriptome profiling reveals infection strategy of an insect maculavirus. DNA Res 2018; 25:277–286 [View Article] [PubMed]
     [Google Scholar]
  46. Feng Y, Zhang X, Kumar D, Kuang S, Liu B et al. Transient propagation of BmLV and dysregulation of gene expression in nontarget cells following BmLV infection. J Asia Pac Entomol 2021; 24:893–902 [View Article]
     [Google Scholar]
  47. Gupta R, Kwon S-Y, Kim ST. An insight into the tomato spotted wilt virus (TSWV), tomato and thrips interaction. Plant Biotechnol Rep 2018; 12:157–163 [View Article]
     [Google Scholar]
  48. Whitfield AE, Falk BW, Rotenberg D. Insect vector-mediated transmission of plant viruses. Virology 2015; 479–480:278–289 [View Article] [PubMed]
     [Google Scholar]
  49. Margaria P, Bosco L, Vallino M, Ciuffo M, Mautino GC et al. The NSs protein of tomato spotted wilt virus is required for persistent infection and transmission by Frankliniella occidentalis. J Virol 2014; 88:5788–5802 [View Article] [PubMed]
     [Google Scholar]
  50. Oliveira VC, Bartasson L, de Castro MEB, Corrêa JR, Ribeiro BM et al. A silencing suppressor protein (NSs) of a tospovirus enhances baculovirus replication in permissive and semipermissive insect cell lines. Virus Res 2011; 155:259–267 [View Article] [PubMed]
     [Google Scholar]
  51. de Oliveira VC, da Silva Morgado F, Ardisson-Araújo DMP, Resende RO, Ribeiro BM. The silencing suppressor (NSs) protein of the plant virus Tomato spotted wilt virus enhances heterologous protein expression and baculovirus pathogenicity in cells and lepidopteran insects. Arch Virol 2015; 160:2873–2879 [View Article] [PubMed]
     [Google Scholar]
  52. Garcia S, Billecocq A, Crance J-M, Prins M, Garin D et al. Viral suppressors of RNA interference impair RNA silencing induced by a Semliki forest virus replicon in tick cells. J Gen Virol 2006; 87:1985–1989 [View Article] [PubMed]
     [Google Scholar]
  53. Kim C-Y, Kim Y. In vivo transient expression of a viral silencing suppressor, NSs, derived from tomato spotted wilt virus decreases insect RNAi efficiencies. Arch Insect Biochem Physiol 2023; 112:e21982 [View Article] [PubMed]
     [Google Scholar]
  54. Nagata T, Storms MM, Goldbach R, Peters D. Multiplication of tomato spotted wilt virus in primary cell cultures derived from two thrips species. Virus Res 1997; 49:59–66 [View Article] [PubMed]
     [Google Scholar]
  55. Wijkamp I, van Lent J, Kormelink R, Goldbach R, Peters D. Multiplication of tomato spotted wilt virus in its insect vector, Frankliniella occidentalis. J Gen Virol 1993; 74:341–349 [View Article] [PubMed]
     [Google Scholar]
  56. Zhu M, van Grinsven IL, Kormelink R, Tao X. Paving the way to tospovirus infection: multilined interplays with plant innate immunity. Annu Rev Phytopathol 2019; 57:41–62 [View Article] [PubMed]
     [Google Scholar]
  57. Turina M, Kormelink R, Resende RO. Resistance to Tospoviruses in vegetable crops: epidemiological and molecular aspects. Annu Rev Phytopathol 2016; 54:347–371 [View Article] [PubMed]
     [Google Scholar]
  58. de Ronde D, Pasquier A, Ying S, Butterbach P, Lohuis D et al. Analysis of tomato spotted wilt virus NSs protein indicates the importance of the N-terminal domain for avirulence and RNA silencing suppression. Mol Plant Pathol 2014; 15:185–195 [View Article] [PubMed]
     [Google Scholar]
  59. Zhai Y, Bag S, Mitter N, Turina M, Pappu HR. Mutational analysis of two highly conserved motifs in the silencing suppressor encoded by tomato spotted wilt virus (genus Tospovirus, family Bunyaviridae). Arch Virol 2014; 159:1499–1504 [View Article] [PubMed]
     [Google Scholar]
  60. Huang C-H, Foo M-H, Raja JAJ, Tan Y-R, Lin T-T et al. A conserved helix in the C-Terminal region of watermelon silver mottle virus nonstructural protein S is imperative for protein stability affecting self-interaction, RNA silencing suppression, and pathogenicity. Mol Plant Microbe Interact 2020; 33:637–652 [View Article] [PubMed]
     [Google Scholar]
  61. Almási A, Nemes K, Sáray R, Gellért Á, Incze N et al. Self-interaction of tomato spotted wilt virus NSs protein enhances gene silencing suppressor activity, but is dispensable as avirulence determinant on pepper. Biologia plant 2023; 67:105–113 [View Article]
     [Google Scholar]
  62. Huang C-H, Hsiao W-R, Huang C-W, Chen K-C, Lin S-S et al. Two novel motifs of watermelon silver mottle virus NSs protein are responsible for RNA silencing suppression and pathogenicity. PLoS One 2015; 10:e0126161 [View Article] [PubMed]
     [Google Scholar]
  63. Yesilyurt A, Demirbag Z, van Oers MM, Nalcacioglu R. Conserved motifs in the invertebrate iridescent virus 6 (IIV6) genome regulate virus transcription. J Invertebr Pathol 2020; 177:107496 [View Article] [PubMed]
     [Google Scholar]
  64. de Faria IJS, Aguiar ERGR, Olmo RP, Alves da Silva J, Daeffler L et al. Invading viral DNA triggers dsRNA synthesis by RNA polymerase II to activate antiviral RNA interference in Drosophila. Cell Rep 2022; 39:110976 [View Article] [PubMed]
     [Google Scholar]
  65. Ince IA, Boeren SA, van Oers MM, Vervoort JJM, Vlak JM. Proteomic analysis of Chilo iridescent virus. Virology 2010; 405:253–258 [View Article] [PubMed]
     [Google Scholar]
  66. Xu C, Wang J, Yang J, Lei C, Hu J et al. NSP2 forms viroplasms during Dendrolimus punctatus cypovirus infection. Virology 2019; 533:68–76 [View Article] [PubMed]
     [Google Scholar]
  67. Pan J, Qiu Q, Kumar D, Xu J, Tong X et al. Interaction between Bombyx mori Cytoplasmic Polyhedrosis Virus NSP8 and BmAgo2 Inhibits RNA Interference and Enhances Virus Proliferation. In Yotam BO. eds Microbiol Spectr vol 11 2023 p e04938-22 [View Article] [PubMed]
     [Google Scholar]
  68. Zhao SL, Liang CY, Zhang WJ, Tang XC, Peng HY. Characterization of the RNA-binding domain in the Dendrolimus punctatus cytoplasmic polyhedrosis virus nonstructural protein p44. Virus Res 2005; 114:80–88 [View Article] [PubMed]
     [Google Scholar]
  69. Vacic V, Uversky VN, Dunker AK, Lonardi S. Composition profiler: a tool for discovery and visualization of amino acid composition differences. BMC Bioinformatics 2007; 8:211 [View Article] [PubMed]
     [Google Scholar]
  70. Jiang L, Peng Z, Guo Y, Cheng T, Guo H et al. Transcriptome analysis of interactions between silkworm and cytoplasmic polyhedrosis virus. Sci Rep 2016; 6:24894 [View Article] [PubMed]
     [Google Scholar]
  71. Chavali VRM, Ghosh AK. Molecular cloning, sequence analysis and expression of genome segment 7 (S7) of Antheraea mylitta cypovirus (AmCPV) that encodes a viral structural protein. Virus Genes 2007; 35:433–441 [View Article] [PubMed]
     [Google Scholar]
  72. Oliver JE, Whitfield AE. The genus tospovirus: emerging bunyaviruses that threaten food security. Annu Rev Virol 2016; 3:101–124 [View Article] [PubMed]
     [Google Scholar]
  73. Ribière M, Olivier V, Blanchard P. Chronic bee paralysis: a disease and a virus like no other?. J Invertebr Pathol 2010; 103:S120–S131 [View Article] [PubMed]
     [Google Scholar]
  74. Beaurepaire A, Piot N, Doublet V, Antunez K, Campbell E et al. Diversity and global distribution of viruses of the western honey bee, Apis mellifera. Insects 2020; 11:239 [View Article] [PubMed]
     [Google Scholar]
  75. Shan T, Yang S, Wang H, Wang H, Zhang J et al. Virome in the cloaca of wild and breeding birds revealed a diversity of significant viruses. Microbiome 2022; 10:60 [View Article] [PubMed]
     [Google Scholar]
  76. de Lima JGS, Lanza DCF. 2A and 2A-like sequences: distribution in different virus species and applications in biotechnology. Viruses 2021; 13:2160 [View Article] [PubMed]
     [Google Scholar]
  77. Olivier V, Blanchard P, Chaouch S, Lallemand P, Schurr F et al. Molecular characterisation and phylogenetic analysis of chronic bee paralysis virus, a honey bee virus. Virus Res 2008; 132:59–68 [View Article] [PubMed]
     [Google Scholar]
  78. Wagner I, Volkmer M, Sharan M, Villaveces JM, Oswald F et al. morFeus: a web-based program to detect remotely conserved orthologs using symmetrical best hits and orthology network scoring. BMC Bioinformatics 2014; 15:263 [View Article] [PubMed]
     [Google Scholar]
  79. Lay CL, Shi M, Buček A, Bourguignon T, Lo N et al. Unmapped RNA virus diversity in termites and their symbionts. Viruses 2020; 12:1145 [View Article] [PubMed]
     [Google Scholar]
  80. Perrakis A, Sixma TK. AI revolutions in biology: the joys and perils of AlphaFold. EMBO Rep 2021; 22:e54046 [View Article] [PubMed]
     [Google Scholar]
  81. Tokuriki N, Oldfield CJ, Uversky VN, Berezovsky IN, Tawfik DS. Do viral proteins possess unique biophysical features?. Trends Biochem Sci 2009; 34:53–59 [View Article] [PubMed]
     [Google Scholar]
  82. Lin Z, Akin H, Rao R, Hie B, Zhu Z et al. Evolutionary-scale prediction of atomic level protein structure with a language model. Synth Biol 2022 [View Article]
     [Google Scholar]
  83. Zheng W, Wuyun Q, Freddolino PL, Zhang Y. Integrating deep learning, threading alignments, and a multi-MSA strategy for high-quality protein monomer and complex structure prediction in CASP15. Proteins 2023; 91:1684–1703 [View Article] [PubMed]
     [Google Scholar]
  84. Bruley A, Mornon J-P, Duprat E, Callebaut I. Digging into the 3D structure predictions of AlphaFold2 with low confidence: disorder and beyond. Biomolecules 2022; 12:1467 [View Article] [PubMed]
     [Google Scholar]
  85. Gulyaeva AA, Sigorskih AI, Ocheredko ES, Samborskiy DV, Gorbalenya AE. LAMPA, LArge multidomain protein annotator, and its application to RNA virus polyproteins. Bioinformatics 2020; 36:2731–2739 [View Article] [PubMed]
     [Google Scholar]
  86. Floden EW, Tommaso PD, Chatzou M, Magis C, Notredame C et al. PSI/TM-Coffee: a web server for fast and accurate multiple sequence alignments of regular and transmembrane proteins using homology extension on reduced databases. Nucleic Acids Res 2016; 44:W339–W343 [View Article] [PubMed]
     [Google Scholar]
  87. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. Jalview Version 2--a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009; 25:1189–1191 [View Article] [PubMed]
     [Google Scholar]
  88. Procter JB, Thompson J, Letunic I, Creevey C, Jossinet F et al. Visualization of multiple alignments, phylogenies and gene family evolution. Nat Methods 2010; 7:S16–S25 [View Article] [PubMed]
     [Google Scholar]
  89. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402 [View Article] [PubMed]
     [Google Scholar]
  90. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S et al. NCBI BLAST: a better web interface. Nucleic Acids Res 2008; 36:W5–W9 [View Article] [PubMed]
     [Google Scholar]
  91. Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA et al. Pfam: The protein families database in 2021. Nucleic Acids Res 2021; 49:D412–D419 [View Article] [PubMed]
     [Google Scholar]
  92. Burley SK, Bhikadiya C, Bi C, Bittrich S, Chen L et al. RCSB protein data bank: powerful new tools for exploring 3D structures of biological macromolecules for basic and applied research and education in fundamental biology, biomedicine, biotechnology, bioengineering and energy sciences. Nucleic Acids Res 2021; 49:D437–D451 [View Article] [PubMed]
     [Google Scholar]
  93. Tsirigos KD, Peters C, Shu N, Käll L, Elofsson A. The TOPCONS web server for consensus prediction of membrane protein topology and signal peptides. Nucleic Acids Res 2015; 43:W401–W407 [View Article] [PubMed]
     [Google Scholar]
  94. Teufel F, Almagro Armenteros JJ, Johansen AR, Gíslason MH, Pihl SI et al. SignalP 6.0 predicts all five types of signal peptides using protein language models. Nat Biotechnol 2022; 40:1023–1025 [View Article] [PubMed]
     [Google Scholar]
  95. Mirdita M, Schütze K, Moriwaki Y, Heo L, Ovchinnikov S et al. ColabFold: making protein folding accessible to all. Nat Methods 2022; 19:679–682 [View Article] [PubMed]
     [Google Scholar]
  96. Goddard TD, Huang CC, Meng EC, Pettersen EF, Couch GS et al. UCSF chimerax: meeting modern challenges in visualization and analysis: UCSF chimerax visualization system. Protein Sci 2018; 27:14–25 [View Article]
     [Google Scholar]
  97. Dong R, Pan S, Peng Z, Zhang Y, Yang J. mTM-align: a server for fast protein structure database search and multiple protein structure alignment. Nucleic Acids Res 2018; 46:W380–W386 [View Article] [PubMed]
     [Google Scholar]
  98. Li Z, Jaroszewski L, Iyer M, Sedova M, Godzik A. FATCAT 2.0: towards a better understanding of the structural diversity of proteins. Nucleic Acids Res 2020; 48:W60–W64 [View Article] [PubMed]
     [Google Scholar]
  99. Holm L. Dali server: structural unification of protein families. Nucleic Acids Res 2022; 50:W210–W215 [View Article] [PubMed]
     [Google Scholar]
  100. Paraskevopoulou S, Käfer S, Zirkel F, Donath A, Petersen M et al. Viromics of extant insect orders unveil the evolution of the flavi-like superfamily. Virus Evol 2021; 7:veab030 [View Article] [PubMed]
     [Google Scholar]
  101. Liu S, Sappington TW, Coates BS, Bonning BC. Sequences encoding a novel toursvirus identified from southern and northern corn rootworms (Coleoptera: Chrysomelidae). Viruses 2022; 14:397 [View Article] [PubMed]
     [Google Scholar]
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WIV, a protein domain found in a wide number of arthropod viruses, which probably facilitates infection
J. Gen. Virol. 105, 001948 (2024); https://doi.org/10.1099/jgv.0.001948
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