1887

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Volume 105, Issue 2

Evolutionary analysis and biological characterization of a novel alphabaculovirus isolated from No Access

Abstract

Baculoviruses are insect-specific pathogens. Novel baculovirus isolates provide new options for the biological control of pests. Therefore, research into the biological characteristics of newly isolated baculoviruses, including accurate classification and nomenclature, is important. In this study, a baculovirus was isolated from and its complete genome sequence was determined by next-generation sequencing. The double-stranded DNA genome was 153 882 bp in length, encoding 163 open reading frames. The virus was identified as a variant of Mamestra brassicae multiple nucleopolyhedrovirus (MbMNPV) and designated Mamestra brassicae multiple nucleopolyhedrovirus CHN1 (MbMNPV-CHN1) according to ultrastructural analysis, genome comparison and phylogenetic analysis. Phylogenetic inference placed MbMNPV-CHN1 in a clade containing isolates of MacoNPV-A, MacoNPV-B and MbMNPV, which we have designated the Mb-McNPV group. The genomes of isolates in the Mb-McNPV group exhibited a high degree of collinearity with relatively minor differences in the content of annotated open reading frames. The development of codon usage bias in the Mb-McNPV group was affected mainly by natural selection. MbMNPV-CHN1 shows high infectivity against seven species of Lepidoptera. The yield of MbMNPV-CHN1 in the fourth- and fifth-instar larvae was 6.25×10–1.23×10 OBs/cadaver. Our data provide insights into the classification, host range and virulence differences among baculoviruses of the Mb-McNPV group, as well as a promising potential new baculoviral insecticide.

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Keyword(s): comparative genomics , host range , infectivity , Mamestra brassicae multiple nucleopolyhedrovirus , novel alphabaculovirus and phylogeny
Funding
This study was supported by the:
  • the Science and Technology Innovation Fund Project of Henan Agricultural University (Award KJCX2020A13)
    • Principle Award Recipient: XiangyangLiu
  • the Earmarked Fund for China Agriculture Research System (Award CARS-27)
    • Principle Award Recipient: XiangyangLiu
  • the Henan Province Science and Technology Research and Development Plan Joint Fund (Application Research) Project (Award 222103810001)
    • Principle Award Recipient: XiangyangLiu
© 2024 The Authors
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2024-02-20
2024-05-04
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References

  1. Rohrmann GF. Baculovirus molecular biology. Corvallis, Oregon: Bethesda (MD): National library of medicine (US). NCBI 2019 [PubMed]
     [Google Scholar]
  2. Harrison RL, Herniou EA, Jehle JA, Theilmann DA, Burand JP et al. ICTV virus taxonomy profile: Baculoviridae. J Gen Virol 2018; 99:1185–1186 [View Article] [PubMed]
     [Google Scholar]
  3. Thézé J, Lopez-Vaamonde C, Cory JS, Herniou EA. Biodiversity, evolution and ecological specialization of baculoviruses: a treasure trove for future applied research. Viruses 2018; 10:366–383 [View Article] [PubMed]
     [Google Scholar]
  4. Mukawa S, Goto C. In vivo characterization of a group II nucleopolyhedrovirus isolated from Mamestra brassicae (Lepidoptera: Noctuidae) in Japan. J Gen Virol 2006; 87:1491–1500 [View Article] [PubMed]
     [Google Scholar]
  5. Aruga H, Yoshitake N, Watanabe H, Hukuhara T. Studies on nuclear polyhedroses and their inductions in some Lepidoptera. Jpn J Appl Entomol 1960; 4:51–56 [View Article]
     [Google Scholar]
  6. Brown DA, Evans HF, Allen CJ, Kelly DC. Biological and biochemical investigations on five European isolates of Mamestra brassicae nuclear polyhedrosis virus. Arch Virol 1981; 69:209–217 [View Article] [PubMed]
     [Google Scholar]
  7. Choi JB, Heo WI, Shin TY, Bae SM, Kim WJ et al. Complete genomic sequences and comparative analysis of Mamestra brassicae nucleopolyhedrovirus isolated in Korea. Virus Genes 2013; 47:133–151 [View Article] [PubMed]
     [Google Scholar]
  8. Black BC, Brennan LA, Dierks PM, Gard IE. Commercialization of baculoviral insecticides. In Miller LK. eds The Baculoviruses New York: Plenum Press; 1997 pp 341–387 [View Article]
     [Google Scholar]
  9. Choi JB, Young ST, Bae S, Woo S-D. Formulation of mamestra brassicae Nucleopolyhedrovirus-K1 as viral insecticide. Int J Indust Entomol 2010; 21:139–143 [View Article] [PubMed]
     [Google Scholar]
  10. Abrol DP, Shankar U. Integrated pest management: principles and practice. In Abrol DP, Shankar U. eds Microbial Control of Crop Pests Using Insect Viruses UK: CAB International; 2012 pp 281–298 [View Article]
     [Google Scholar]
  11. Wiegers FP, Vlak JM. Physical map of the DNA of a Mamestra brassicae nuclear polyhedrosis virus variant isolated from Spodoptera exigua. J Gen Virol 1984; 65:2011–2019 [View Article]
     [Google Scholar]
  12. Doyle CJ, Hirst ML, Cory JS, Entwistle PF. Risk assessment studies: detailed host range testing of wild-type cabbage moth, Mamestra brassicae (Lepidoptera: Noctuidae), nuclear polyhedrosis virus. Appl Environ Microbiol 1990; 56:2704–2710 [View Article] [PubMed]
     [Google Scholar]
  13. Kouassi LN, Tsuda K, Goto C, Mukawa S, Sakamaki Y et al. Biological activity and identification of nucleopolyhedroviruses isolated from Mythimna separata and Spodoptera litura in Japan. BioControl 2009; 54:537–548 [View Article]
     [Google Scholar]
  14. Tang P, Zhang H, Li Y, Han B, Wang G et al. Genomic sequencing and analyses of HearMNPV--a new Multinucleocapsid nucleopolyhedrovirus isolated from Helicoverpa armigera. Virol J 2012; 9:1–18 [View Article] [PubMed]
     [Google Scholar]
  15. Rowley DL, Popham HJR, Harrison RL. Genetic variation and virulence of nucleopolyhedroviruses isolated worldwide from the heliothine pests Helicoverpa armigera, Helicoverpa zea, and Heliothis virescens. J Invertebr Pathol 2011; 107:112–126 [View Article] [PubMed]
     [Google Scholar]
  16. Simón O, Erlandson MA, Frayssinet M, Williams T, Theilmann DA et al. Lacanobia oleracea nucleopolyhedrovirus (LaolNPV): A new European species of alphabaculovirus with a narrow host range. PLoS One 2017; 12:e0176171 [View Article] [PubMed]
     [Google Scholar]
  17. Belda IM, Beperet I, Williams T, Caballero P. Genetic variation and biological activity of two closely related alphabaculoviruses during serial passage in permissive and semi-permissive heterologous hosts. Viruses 2019; 11:660–679 [View Article] [PubMed]
     [Google Scholar]
  18. Li L, Donly C, Li Q, Willis LG, Keddie BA et al. Identification and genomic analysis of a second species of nucleopolyhedrovirus isolated from Mamestra configurata. Virology 2002; 297:226–244 [View Article] [PubMed]
     [Google Scholar]
  19. Du EQ, Yan F, Jin WX, Lu N, Xiao HZ et al. P13 of Leucania separata multiple nuclear polyhedrosis virus affected the polyhedra and budded virions yields of AcMNPV. Virus Res 2007; 124:160–167 [View Article] [PubMed]
     [Google Scholar]
  20. Lei C, Yang S, Lei W, Nyamwasa I, Hu J et al. Displaying enhancing factors on the surface of occlusion bodies improves the insecticidal efficacy of a baculovirus. Pest Manag Sci 2020; 76:1363–1370 [View Article] [PubMed]
     [Google Scholar]
  21. Harrison RL, Rowley DL, Mowery JD, Bauchan GR, Burand JP. The Operophtera brumata nucleopolyhedrovirus (OpbuNPV) represents an early, divergent lineage within genus Alphabaculovirus. Viruses 2017; 9:307 [View Article] [PubMed]
     [Google Scholar]
  22. Quince C, Walker AW, Simpson JT, Loman NJ, Segata N. Shotgun metagenomics, from sampling to analysis. Nat Biotechnol 2017; 35:833–844 [View Article] [PubMed]
     [Google Scholar]
  23. Coil D, Jospin G, Darling AE. A5-miseq: an updated pipeline to assemble microbial genomes from illumina MiSeq data. Bioinformatics 2015; 31:587–589 [View Article] [PubMed]
     [Google Scholar]
  24. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
     [Google Scholar]
  25. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al. Versatile and open software for comparing large genomes. Genome Biol 2004; 5:1–9 [View Article] [PubMed]
     [Google Scholar]
  26. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article] [PubMed]
     [Google Scholar]
  27. Grant JR, Arantes AS, Stothard P. Comparing thousands of circular genomes using the CGView comparison tool. BMC Genomics 2012; 13:202–209 [View Article] [PubMed]
     [Google Scholar]
  28. Javed MA, Biswas S, Willis LG, Harris S, Pritchard C et al. Autographa californica multiple nucleopolyhedrovirus AC83 is a Per Os infectivity factor (PIF) protein required for Occlusion-Derived Virus (ODV) and budded virus nucleocapsid assembly as well as assembly of the PIF complex in ODV envelopes. J Virol 2017; 91:e02115-16 [View Article] [PubMed]
     [Google Scholar]
  29. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
     [Google Scholar]
  30. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article] [PubMed]
     [Google Scholar]
  31. Zhang D, Gao F, Jakovlić I, Zou H, Zhang J et al. PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol Ecol Resour 2020; 20:348–355 [View Article] [PubMed]
     [Google Scholar]
  32. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 2017; 14:587–589 [View Article] [PubMed]
     [Google Scholar]
  33. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A et al. MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 2012; 61:539–542 [View Article] [PubMed]
     [Google Scholar]
  34. Harrison RL, Mowery JD, Rowley DL, Bauchan GR, Theilmann DA et al. The complete genome sequence of a third distinct baculovirus isolated from the true armyworm, Mythimna unipuncta, contains two copies of the lef-7 gene. Virus Genes 2017; 54:297–310 [View Article] [PubMed]
     [Google Scholar]
  35. Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 2017; 34:3299–3302 [View Article] [PubMed]
     [Google Scholar]
  36. Xu W, Zhang Q, Yuan W, Xu F, Muhammad Aslam M et al. The genome evolution and low-phosphorus adaptation in white lupin. Nat Commun 2020; 11:1069 [View Article] [PubMed]
     [Google Scholar]
  37. Darling AE, Treangen TJ, Messeguer X, Perna NT. Analyzing patterns of microbial evolution using the mauve genome alignment system. Methods Mol Biol 2007; 396:135–152 [View Article] [PubMed]
     [Google Scholar]
  38. Zhang L-J, Li Y-J, Ge X-Y, Li X-Y, Yang Y-X et al. Mitochondrial genomes of Sternochetus species (Coleoptera: Curculionidae) and the phylogenetic implications. Arch Insect Biochem Physiol 2022; 111:e21898 [View Article] [PubMed]
     [Google Scholar]
  39. Aslam F, Rehman MU, Saleem G, Ashraf K, Hafeez A. Effects of Trypanosoma evansi and Theileria annulata infection on Hemato- biochemical parameters of one humped camels (Camelus dromedaries) in Punjab, Pakistan. Pak J Agric Sci 2023; 60:177–183 [View Article]
     [Google Scholar]
  40. Patil AB, Dalvi VS, Mishra AA, Krishna B, Azeez A. Analysis of synonymous codon usage bias and phylogeny of coat protein gene in banana bract mosaic virus isolates. Virusdisease 2017; 28:156–163 [View Article] [PubMed]
     [Google Scholar]
  41. Wang P, Mao Y, Su Y, Wang J. Comparative analysis of transcriptomic data shows the effects of multiple evolutionary selection processes on codon usage in Marsupenaeus japonicus and Marsupenaeus pulchricaudatus. BMC Genomics 2021; 22:781–794 [View Article] [PubMed]
     [Google Scholar]
  42. Tyagi A, Nagar V. Genome dynamics, codon usage patterns and influencing factors in Aeromonas hydrophila phages. Virus Res 2022; 320:198900 [View Article] [PubMed]
     [Google Scholar]
  43. Sharp PM, Matassi G. Codon usage and genome evolution. Curr Opin Genet Dev 1994; 4:851–860 [View Article] [PubMed]
     [Google Scholar]
  44. Wang H, Liu S, Lv Y, Wei W. Codon usage bias of Venezuelan equine encephalitis virus and its host adaption. Virus Res 2023; 328:199081 [View Article] [PubMed]
     [Google Scholar]
  45. Wang Z, Cai Q, Wang Y, Li M, Wang C et al. Comparative analysis of codon bias in the chloroplast genomes of theaceae species. Front Genet 2022; 13:824610 [View Article] [PubMed]
     [Google Scholar]
  46. Zhao Y, Zheng H, Xu A, Yan D, Jiang Z et al. Analysis of codon usage bias of envelope glycoprotein genes in nuclear polyhedrosis virus (NPV) and its relation to evolution. BMC Genomics 2016; 17:677 [View Article] [PubMed]
     [Google Scholar]
  47. Moberly JG, Bernards MT, Waynant KV. Key features and updates for origin 2018. J Cheminform 2018; 10:5–6 [View Article] [PubMed]
     [Google Scholar]
  48. Shorey HH, Hale RL. Mass-rearing of the larvae of nine Noctuid species on a simple artificial medium12. J Econ Entomol 1965; 58:522–524 [View Article]
     [Google Scholar]
  49. Hughes PR, van Beek NAM, Wood HA. A modified droplet feeding method for rapid assay of Bacillus thuringiensis and baculoviruses in noctuid larvae. J Invertebr Pathol 1986; 48:187–192 [View Article]
     [Google Scholar]
  50. Finney D. Probit analysis, 3rd. edn Cambridge, London: Cambridge University Press; 1971
     [Google Scholar]
  51. Sueoka N. Wide intra-genomic G+C heterogeneity in human and chicken is mainly due to strand-symmetric directional mutation pressures: dGTP-oxidation and symmetric cytosine-deamination hypotheses. Gene 2002; 300:141–154 [View Article] [PubMed]
     [Google Scholar]
  52. Sueoka N. Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci U S A 1988; 85:2653–2657 [View Article] [PubMed]
     [Google Scholar]
  53. Hassan M, Anal JMH, Singh R. Comprehensive analysis of codon usage pattern in Eisenia fetida and its correlation with gene expression. Bio Agri Biotechnol 2023; 52:102810 [View Article]
     [Google Scholar]
  54. Erlandson MA. Biological and biochemical comparison of Mamestra configurata and Mamestra brassicae nuclear polyhedrosis virus isolates pathogenic for the bertha armyworm, Mamestra configurata (Lepidoptera: Noctuidae). J Invert Pathol 1990; 56:47–56 [View Article]
     [Google Scholar]
  55. Wennmann JT, Keilwagen J, Jehle JA. Baculovirus kimura two-parameter species demarcation criterion is confirmed by the distances of 38 core gene nucleotide sequences. J Gen Virol 2018; 99:1307–1320 [View Article] [PubMed]
     [Google Scholar]
  56. Burden JP, Possee RD, Sait SM, King LA, Hails RS. Phenotypic and genotypic characterisation of persistent baculovirus infections in populations of the cabbage moth (Mamestra brassicae) within the British Isles. Arch Virol 2006; 151:635–649 [View Article] [PubMed]
     [Google Scholar]
  57. Jehle JA, Lange M, Wang H, Hu Z, Wang Y et al. Molecular identification and phylogenetic analysis of baculoviruses from Lepidoptera. Virology 2006; 346:180–193 [View Article] [PubMed]
     [Google Scholar]
  58. Yang Z, Bielawski JP. Statistical methods for detecting molecular adaptation. Trends Ecol Evol 2000; 15:496–503 [View Article] [PubMed]
     [Google Scholar]
  59. Hurst LD. Genetics and the understanding of selection. Nat Rev Genet 2009; 10:83–93 [View Article]
     [Google Scholar]
  60. Li S, Song KS, Koh SS, Kikuchi A, Lisanti MP. Baculovirus-based expression of mammalian caveolin in Sf21 insect cells. A model system for the biochemical and morphological study of caveolae biogenesis. J Biol Chem 1996; 271:28647–28654 [View Article] [PubMed]
     [Google Scholar]
  61. Li K, Dong Z, Dong F, Hu Z, Huang L et al. Transcriptome analysis reveals that knocking out BmNPV iap2 induces apoptosis by inhibiting the oxidative phosphorylation pathway. Int J Biol Macromol 2023; 233:123482 [View Article] [PubMed]
     [Google Scholar]
  62. Chen F, Wu P, Deng S, Zhang H, Hou Y et al. Dissimilation of synonymous codon usage bias in virus-host coevolution due to translational selection. Nat Ecol Evol 2020; 4:589–600 [View Article] [PubMed]
     [Google Scholar]
  63. Li Q, Donly C, Li L, Willis LG, Theilmann DA et al. Sequence and organization of the Mamestra configurata nucleopolyhedrovirus genome. Virology 2002; 294:106–121 [View Article] [PubMed]
     [Google Scholar]
  64. Li L, Li Q, Willis LG, Erlandson M, Theilmann DA et al. Complete comparative genomic analysis of two field isolates of Mamestra configurata nucleopolyhedrovirus-A. J Gen Virol 2005; 86:91–105 [View Article] [PubMed]
     [Google Scholar]
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Evolutionary analysis and biological characterization of a novel alphabaculovirus isolated from Mythimna separata
J. Gen. Virol. 105, 001958 (2024); https://doi.org/10.1099/jgv.0.001958
/content/journal/jgv/10.1099/jgv.0.001958
/content/journal/jgv/10.1099/jgv.0.001958
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