1887

Journal of General Virology header logo

Volume 104, Issue 2

Genome-wide identification of lncRNAs associated with viral infection in Open Access

Abstract

The role of lncRNAs in immune defence has been demonstrated in many multicellular and unicellular organisms. However, investigation of the identification and characterization of long non-coding RNAs (lncRNAs) involved in the insect immune response is still limited. In this study, we used RNA sequencing (RNA-seq) to investigate the expression profiles of lncRNAs and mRNAs in the fall armyworm in response to virus infection. To assess the tissue- and virus-specificity of lncRNAs, we analysed and compared their expression profiles in haemocytes and fat body of larvae infected with two entomopathogenic viruses with different lifestyles, i.e. the polydnavirus HdIV ( IchnoVirus) and the densovirus JcDV ( densovirus). We identified 1883 candidate lncRNAs, of which 529 showed differential expression following viral infection. Expression profiles differed considerably between samples, indicating that many differentially expressed (DE) lncRNAs showed virus- and tissue-specific expression patterns. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment and target prediction analyses indicated that DE-LncRNAs were mainly enriched in metabolic process, DNA replication and repair, immune response, metabolism of insect hormone and cell adhesion. In addition, we identified three DE-lncRNAs potentially acting as microRNA host genes, suggesting that they participate in gene regulation by producing miRNAs in response to virus infection. This study provides a catalogue of lncRNAs expressed in two important immune tissues and potential insight into their roles in the antiviral defence in . The results may help future in-depth functional studies to better understand the biological function of lncRNAs in interaction between viruses and the fall armyworm.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): densovirus , host-virus interactions , long non-coding RNA , polydnavirus , RNA-Seq and Spodoptera frugiperda
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001827
2023-02-09
2024-05-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/104/2/jgv001827.html?itemId=/content/journal/jgv/10.1099/jgv.0.001827&mimeType=html&fmt=ahah

References

  1. Robin S, Legai F, Jouan V, Ogliastro M, Darboux I. Genome-wide identification of lncRNAs associated to viral infection in Spodoptera frugiperda. Figshare 2022 [View Article]
     [Google Scholar]
  2. Ma H, Han P, Ye W, Chen H, Zheng X et al. The long noncoding RNA NEAT1 exerts antihantaviral effects by acting as positive feedback for RIG-I signaling. J Virol 2017; 91:e02250-16 [View Article]
     [Google Scholar]
  3. Wang J, Zhang Y, Li Q, Zhao J, Yi D et al. Influenza virus exploits an interferon-independent lncRNA to preserve viral RNA synthesis through stabilizing viral RNA polymerase PB1. Cell Rep 2019; 27:3295–3304 [View Article]
     [Google Scholar]
  4. Wang P, Xu J, Wang Y, Cao X. An interferon-independent lncRNA promotes viral replication by modulating cellular metabolism. Science 2017; 358:1051–1055 [View Article] [PubMed]
     [Google Scholar]
  5. Wang Z, Zhao Y, Zhang Y. Viral lncRNA: a regulatory molecule for controlling virus life cycle. Noncoding RNA Res 2017; 2:38–44 [View Article]
     [Google Scholar]
  6. Tycowski KT, Guo YE, Lee N, Moss WN, Vallery TK et al. Viral noncoding RNAs: more surprises. Genes Dev 2015; 29:567–584 [View Article]
     [Google Scholar]
  7. Schuessler A, Funk A, Lazear HM, Cooper DA, Torres S et al. West Nile virus noncoding subgenomic RNA contributes to viral evasion of the type I interferon-mediated antiviral response. J Virol 2012; 86:5708–5718 [View Article] [PubMed]
     [Google Scholar]
  8. Tai-Schmiedel J, Karniely S, Lau B, Ezra A, Eliyahu E et al. Human cytomegalovirus long noncoding RNA4.9 regulates viral DNA replication. PLoS Pathog 2020; 16:e1008390 [View Article]
     [Google Scholar]
  9. Ruiz-Orera J, Messeguer X, Subirana JA, Alba MM. Long non-coding RNAs as a source of new peptides. Elife 2014; 3:e03523 [View Article]
     [Google Scholar]
  10. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B et al. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 2011; 25:1915–1927 [View Article]
     [Google Scholar]
  11. Liu C, Bai B, Skogerbø G, Cai L, Deng W et al. NONCODE: an integrated knowledge database of non-coding RNAs. Nucleic Acids Res 2005; 33:D112–5 [View Article] [PubMed]
     [Google Scholar]
  12. Bu D, Yu K, Sun S, Xie C, Skogerbø G et al. NONCODE v3.0: integrative annotation of long noncoding RNAs. Nucleic Acids Res 2012; 40:D210–5 [View Article] [PubMed]
     [Google Scholar]
  13. Chen B, Zhang Y, Zhang X, Jia S, Chen S et al. Genome-wide identification and developmental expression profiling of long noncoding RNAs during Drosophila metamorphosis. Sci Rep 2016; 6:23330 [View Article]
     [Google Scholar]
  14. McCorkindale AL, Wahle P, Werner S, Jungreis I, Menzel P et al. A gene expression atlas of embryonic neurogenesis in Drosophila reveals complex spatiotemporal regulation of lncRNAs. Development 2019; 146:dev175265 [View Article]
     [Google Scholar]
  15. Schor IE, Bussotti G, Maleš M, Forneris M, Viales RR et al. Non-coding RNA expression, function, and variation during Drosophila Embryogenesis. Curr Biol 2018; 28:3547–3561 [View Article]
     [Google Scholar]
  16. Azlan A, Halim MA, Mohamad F, Azzam G. Identification and characterization of long noncoding RNAs and their association with acquisition of blood meal in Culex quinquefasciatus. Insect Sci 2021; 28:917–928 [View Article]
     [Google Scholar]
  17. Liu F, Shi T, Qi L, Su X, Wang D et al. lncRNA profile of Apis mellifera and its possible role in behavioural transition from nurses to foragers. BMC Genomics 2019; 20:393 [View Article]
     [Google Scholar]
  18. Xiao H, Yuan Z, Guo D, Hou B, Yin C et al. Genome-wide identification of long noncoding RNA genes and their potential association with fecundity and virulence in rice brown planthopper, Nilaparvata lugens. BMC Genomics 2015; 16:749 [View Article]
     [Google Scholar]
  19. Bernabò P, Viero G, Lencioni V. A long noncoding RNA acts as a post-transcriptional regulator of heat shock protein (HSP70) synthesis in the cold hardy Diamesa tonsa under heat shock. PLoS One 2020; 15:e0227172 [View Article]
     [Google Scholar]
  20. Chen Y, Singh A, Kaithakottil GG, Mathers TC, Gravino M et al. An aphid RNA transcript migrates systemically within plants and is a virulence factor. Proc Natl Acad Sci 2020; 117:12763–12771 [View Article]
     [Google Scholar]
  21. Zhang S, Shen S, Yang Z, Kong X, Liu F et al. Coding and non-coding RNAs: molecular basis of forest-insect outbreaks. Front Cell Dev Biol 2020; 8:369 [View Article]
     [Google Scholar]
  22. Liu F, Guo D, Yuan Z, Chen C, Xiao H. Genome-wide identification of long non-coding RNA genes and their association with insecticide resistance and metamorphosis in diamondback moth, Plutella xylostella. Sci Rep 2017; 7:15870 [View Article]
     [Google Scholar]
  23. Zhu B, Xu M, Shi H, Gao X, Liang P. Genome-wide identification of lncRNAs associated with chlorantraniliprole resistance in diamondback moth Plutella xylostella (L.). BMC Genomics 2017; 18:380 [View Article]
     [Google Scholar]
  24. Etebari K, Furlong MJ, Asgari S. Genome wide discovery of long intergenic non-coding RNAs in Diamondback moth (Plutella xylostella) and their expression in insecticide resistant strains. Sci Rep 2015; 5:14642 [View Article]
     [Google Scholar]
  25. Qiao H, Wang J, Wang Y, Yang J, Wei B et al. Transcriptome analysis reveals potential function of long non-coding RNAs in 20-hydroxyecdysone regulated autophagy in Bombyx mori. BMC Genomics 2021; 22:374 [View Article]
     [Google Scholar]
  26. Lopez-Ezquerra A, Mitschke A, Bornberg-Bauer E, Joop G. Tribolium castaneum gene expression changes after Paranosema whitei infection. J Invertebr Pathol 2018; 153:92–98 [View Article]
     [Google Scholar]
  27. Jayakodi M, Jung JW, Park D, Ahn Y-J, Lee S-C et al. Genome-wide characterization of long intergenic non-coding RNAs (lincRNAs) provides new insight into viral diseases in honey bees Apis cerana and Apis mellifera. BMC Genomics 2015; 16:680 [View Article]
     [Google Scholar]
  28. Ali A, Abd El Halim HM. Re-thinking adaptive immunity in the beetles: evolutionary and functional trajectories of lncRNAs. Genomics 2020; 112:1425–1436 [View Article]
     [Google Scholar]
  29. Azlan A, Obeidat SM, Theva Das K, Yunus MA, Azzam G. Genome-wide identification of Aedes albopictus long noncoding RNAs and their association with dengue and Zika virus infection. PLoS Negl Trop Dis 2021; 15:e0008351 [View Article]
     [Google Scholar]
  30. Etebari K, Asad S, Zhang G, Asgari S. Identification of Aedes aegypti long intergenic non-coding RNAs and their association with Wolbachia and Dengue virus infection. PLoS Negl Trop Dis 2016; 10:e0005069 [View Article]
     [Google Scholar]
  31. Zhang L, Xu W, Gao X, Li W, Qi S et al. lncRNA sensing of a viral suppressor of RNAi activates non-canonical innate immune signaling in Drosophila. Cell Host Microbe 2020; 27:115–128 [View Article]
     [Google Scholar]
  32. Guan R, Li H, Zhang H, An S. Comparative analysis of dsRNA-induced lncRNAs in three kinds of insect species. Arch Insect Biochem Physiol 2020; 103:e21640 [View Article]
     [Google Scholar]
  33. Legeai F, Santos BF, Robin S, Bretaudeau A, Dikow RB et al. Genomic architecture of endogenous ichnoviruses reveals distinct evolutionary pathways leading to virus domestication in parasitic wasps. BMC Biol 2020; 18:89 [View Article]
     [Google Scholar]
  34. Dorémus T, Cousserans F, Gyapay G, Jouan V, Milano P et al. Extensive transcription analysis of the Hyposoter didymator Ichnovirus genome in permissive and non-permissive lepidopteran host species. PLoS One 2014; 9:e104072 [View Article]
     [Google Scholar]
  35. Visconti V, Eychenne M, Darboux I. Modulation of antiviral immunity by the ichnovirus HdIV in Spodoptera frugiperda. Mol Immunol 2019; 108:89–101 [View Article] [PubMed]
     [Google Scholar]
  36. Barat-Houari M, Hilliou F, Jousset F-X, Sofer L, Deleury E et al. Gene expression profiling of Spodoptera frugiperda hemocytes and fat body using cDNA microarray reveals polydnavirus-associated variations in lepidopteran host genes transcript levels. BMC Genomics 2006; 7:160 [View Article] [PubMed]
     [Google Scholar]
  37. Provost B, Jouan V, Hilliou F, Delobel P, Bernardo P et al. Lepidopteran transcriptome analysis following infection by phylogenetically unrelated polydnaviruses highlights differential and common responses. Insect Biochem Mol Biol 2011; 41:582–591 [View Article] [PubMed]
     [Google Scholar]
  38. Clavijo G, Dorémus T, Ravallec M, Mannucci M-A, Jouan V et al. Multigenic families in Ichnovirus: a tissue and host specificity study through expression analysis of vankyrins from Hyposoter didymator Ichnovirus. PLoS One 2011; 6:e27522 [View Article]
     [Google Scholar]
  39. Mutuel D, Ravallec M, Chabi B, Multeau C, Salmon J-M et al. Pathogenesis of Junonia coenia densovirus in Spodoptera frugiperda: a route of infection that leads to hypoxia. Virology 2010; 403:137–144 [View Article] [PubMed]
     [Google Scholar]
  40. Legeai F, Gimenez S, Duvic B, Escoubas J-M, Gosselin Grenet A-S et al. Establishment and analysis of a reference transcriptome for Spodoptera frugiperda. BMC Genomics 2014; 15:704 [View Article]
     [Google Scholar]
  41. Gouin A, Bretaudeau A, Nam K, Gimenez S, Aury J-M et al. Two genomes of highly polyphagous lepidopteran pests (Spodoptera frugiperda, Noctuidae) with different host-plant ranges. Sci Rep 2017; 7:11816 [View Article]
     [Google Scholar]
  42. Poitout S, Bues R. Linolenic acid requirements of lepidoptera Noctuidae Quadrifinae Plusiinae: Chrysodeixis chalcites Esp., Autographa gamma L.’ Macdunnoughia confusa Stph., Trichoplusia ni Hbn. reared on artificial diets. Ann Nutr Aliment 1974; 28:173–187
     [Google Scholar]
  43. Ewels PA, Peltzer A, Fillinger S, Patel H, Alneberg J et al. The nf-core framework for community-curated bioinformatics pipelines. Nat Biotechnol 2020; 38:276–278 [View Article] [PubMed]
     [Google Scholar]
  44. Legeai F, Derrien T. Identification of long non-coding RNAs in insects genomes. Curr Opin Insect Sci 2015; 7:37–44 [View Article] [PubMed]
     [Google Scholar]
  45. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 2014; 30:923–930 [View Article] [PubMed]
     [Google Scholar]
  46. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26:139–140 [View Article] [PubMed]
     [Google Scholar]
  47. Alexa A JR. 2021; TopGO: enrichment analysis for gene ontology. version 2.48.0. ed2022. p. R package.
  48. Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 2021; 38:5825–5829 [View Article]
     [Google Scholar]
  49. Rau A, Maugis-Rabusseau C. Transformation and model choice for RNA-seq co-expression analysis. Brief Bioinform 2018; 19:425–436 [View Article]
     [Google Scholar]
  50. Wucher V, Legeai F, Hédan B, Rizk G, Lagoutte L et al. FEELnc: a tool for long non-coding RNA annotation and its application to the dog transcriptome. Nucleic Acids Res 2017; 45:e57 [View Article]
     [Google Scholar]
  51. Le Béguec C, Wucher V, Lagoutte L, Cadieu E, Botherel N et al. Characterisation and functional predictions of canine long non-coding RNAs. Sci Rep 2018; 8:13444 [View Article]
     [Google Scholar]
  52. Moné Y, Nhim S, Gimenez S, Legeai F, Seninet I et al. Characterization and expression profiling of microRNAs in response to plant feeding in two host-plant strains of the lepidopteran pest Spodoptera frugiperda. BMC Genomics 2018; 19:804 [View Article]
     [Google Scholar]
  53. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26:841–842 [View Article] [PubMed]
     [Google Scholar]
  54. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25:402–408 [View Article] [PubMed]
     [Google Scholar]
  55. Dumas B, Jourdan M, Pascaud AM, Bergoin M. Complete nucleotide sequence of the cloned infectious genome of Junonia coenia densovirus reveals an organization unique among parvoviruses. Virology 1992; 191:202–222 [View Article] [PubMed]
     [Google Scholar]
  56. Gimenez S, Abdelgaffar H, Goff GL, Hilliou F, Blanco CA et al. Adaptation by copy number variation increases insecticide resistance in the fall armyworm. Commun Biol 2020; 3:664 [View Article]
     [Google Scholar]
  57. Hess AM, Prasad AN, Ptitsyn A, Ebel GD, Olson KE et al. Small RNA profiling of Dengue virus-mosquito interactions implicates the PIWI RNA pathway in anti-viral defense. BMC Microbiol 2011; 11:45 [View Article]
     [Google Scholar]
  58. Léger P, Lara E, Jagla B, Sismeiro O, Mansuroglu Z et al. Dicer-2- and Piwi-mediated RNA interference in Rift Valley fever virus-infected mosquito cells. J Virol 2013; 87:1631–1648 [View Article] [PubMed]
     [Google Scholar]
  59. Santos D, Verdonckt T-W, Mingels L, Van den Brande S, Geens B et al. PIWI proteins play an antiviral role in lepidopteran cell lines. Viruses 2022; 14:1442 [View Article]
     [Google Scholar]
  60. Salasc F, Mutuel D, Debaisieux S, Perrin A, Dupressoir T et al. Role of the phosphatidylinositol-3-kinase/Akt/target of rapamycin pathway during ambidensovirus infection of insect cells. J Gen Virol 2016; 97:233–245 [View Article] [PubMed]
     [Google Scholar]
  61. Pruijssers AJ, Falabella P, Eum JH, Pennacchio F, Brown MR et al. Infection by a symbiotic polydnavirus induces wasting and inhibits metamorphosis of the moth Pseudoplusia includens. J Exp Biol 2009; 212:2998–3006 [View Article] [PubMed]
     [Google Scholar]
  62. Cusson M, Laforge M, Miller D, Cloutier C, Stoltz D. Functional significance of parasitism-induced suppression of juvenile hormone esterase activity in developmentally delayed Choristoneura fumiferana larvae. Gen Comp Endocrinol 2000; 117:343–354 [View Article] [PubMed]
     [Google Scholar]
  63. Wolfe CJ, Kohane IS, Butte AJ. Systematic survey reveals general applicability of “guilt-by-association” within gene coexpression networks. BMC Bioinformatics 2005; 6:227 [View Article]
     [Google Scholar]
  64. Scherfer C, Tang H, Kambris Z, Lhocine N, Hashimoto C et al. Drosophila Serpin-28D regulates hemolymph phenoloxidase activity and adult pigmentation. Dev Biol 2008; 323:189–196 [View Article] [PubMed]
     [Google Scholar]
  65. Dykes IM, Emanueli C. Transcriptional and post-transcriptional gene regulation by long non-coding RNA. Genomics, Proteomics & Bioinformatics 2017; 15:177–186 [View Article]
     [Google Scholar]
  66. Zhang Z, Zhao Z, Lin S, Wu W, Tang W et al. Identification of long noncoding RNAs in silkworm larvae infected with Bombyx mori cypovirus. Arch Insect Biochem Physiol 2021; 106:1–12 [View Article] [PubMed]
     [Google Scholar]
  67. Mayer KA, Stöckl J, Zlabinger GJ, Gualdoni GA. Hijacking the supplies: metabolism as a novel facet of virus-host interaction. Front Immunol 2019; 10:1533 [View Article]
     [Google Scholar]
  68. Weitzman MD, Fradet-Turcotte A. Virus DNA replication and the host DNA damage response. Annu Rev Virol 2018; 5:141–164 [View Article]
     [Google Scholar]
  69. Chevignon G, Periquet G, Gyapay G, Vega-Czarny N, Musset K et al. Cotesia congregata Bracovirus circles encoding PTP and Ankyrin genes integrate into the DNA of parasitized Manduca sexta hemocytes. J Virol 2018; 92:e00438-18 [View Article]
     [Google Scholar]
  70. Muller H, Chebbi MA, Bouzar C, Périquet G, Fortuna T et al. Genome-wide patterns of Bracovirus chromosomal integration into multiple host tissues during parasitism. J Virol 2021; 95:e0068421 [View Article]
     [Google Scholar]
  71. Wang Z, Ye X, Zhou Y, Wu X, Hu R et al. Bracoviruses recruit host integrases for their integration into caterpillar’s genome. PLoS Genet 2021; 17:e1009751 [View Article]
     [Google Scholar]
  72. Wang Z-H, Zhou Y-N, Yang J, Ye X-Q, Shi M et al. Genome-wide profiling of Diadegma semiclausum ichnovirus integration in parasitized Plutella xylostella hemocytes identifies host integration motifs and insertion sites. Front Microbiol 2020; 11:608346 [View Article]
     [Google Scholar]
  73. Kerr AG, Wang Z, Wang N, Kwok KHM, Jalkanen J et al. The long noncoding RNA ADIPINT regulates human adipocyte metabolism via pyruvate carboxylase. Nat Commun 2022; 13:2958 [View Article]
     [Google Scholar]
  74. Feldstein O, Nizri T, Doniger T, Jacob J, Rechavi G et al. The long non-coding RNA ERIC is regulated by E2F and modulates the cellular response to DNA damage. Mol Cancer 2013; 12:131 [View Article]
     [Google Scholar]
  75. Valanne S, Salminen TS, Järvelä-Stölting M, Vesala L, Rämet M. Immune-inducible non-coding RNA molecule lincRNA-IBIN connects immunity and metabolism in Drosophila melanogaster. PLoS Pathog 2019; 15:e1007504 [View Article]
     [Google Scholar]
  76. Zhou H, Li S, Pan W, Wu S, Ma F et al. Interaction of lncRNA-CR33942 with Dif/Dorsal facilitates antimicrobial peptide transcriptions and enhances Drosophila toll immune responses. J Immunol 2022; 208:1978–1988 [View Article]
     [Google Scholar]
  77. Zhou H, Wu S, Liu L, Li R, Jin P et al. Drosophila relish activating lncRNA-CR33942 transcription facilitates antimicrobial peptide expression in imd innate immune response. Front Immunol 2022; 13:905899 [View Article]
     [Google Scholar]
  78. Lanzrein B, Treiblmayr K, Meyer V, Pfister-Wilhelm R, Grossniklaus-Bürgin C. Physiological and endocrine changes associated with polydnavirus/venom in the parasitoid-host system Chelonus inanitus-Spodoptera littoralis. J Insect Physiol 1998; 44:305–321 [View Article] [PubMed]
     [Google Scholar]
  79. Valzania L, Romani P, Tian L, Li S, Cavaliere V et al. A polydnavirus ANK protein acts as virulence factor by disrupting the function of prothoracic gland steroidogenic cells. PLoS One 2014; 9:e95104 [View Article]
     [Google Scholar]
  80. Ignesti M, Ferrara R, Romani P, Valzania L, Serafini G et al. A polydnavirus-encoded ANK protein has a negative impact on steroidogenesis and development. Insect Biochem Mol Biol 2018; 95:26–32 [View Article]
     [Google Scholar]
  81. Chen J, Liang Z, Liang Y, Pang R, Zhang W. Conserved microRNAs miR-8-5p and miR-2a-3p modulate chitin biosynthesis in response to 20-hydroxyecdysone signaling in the brown planthopper, Nilaparvata lugens. Insect Biochem Mol Biol 2013; 43:839–848 [View Article] [PubMed]
     [Google Scholar]
  82. Skalsky RL, Vanlandingham DL, Scholle F, Higgs S, Cullen BR. Identification of microRNAs expressed in two mosquito vectors, Aedes albopictus and Culex quinquefasciatus. BMC Genomics 2010; 11:119 [View Article]
     [Google Scholar]
  83. Ling L, Ge X, Li Z, Zeng B, Xu J et al. MicroRNA Let-7 regulates molting and metamorphosis in the silkworm, Bombyx mori. Insect Biochem Mol Biol 2014; 53:13–21 [View Article] [PubMed]
     [Google Scholar]
  84. Fu Y, Wang Y, Huang Q, Zhao C, Li X et al. Long noncoding RNA lncR17454 regulates metamorphosis of silkworm through let-7 miRNA cluster. J Insect Sci 2022; 22:12 [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001827
Loading
Genome-wide identification of lncRNAs associated with viral infection in Spodoptera frugiperda
J. Gen. Virol. 104, 001827 (2023); https://doi.org/10.1099/jgv.0.001827
/content/journal/jgv/10.1099/jgv.0.001827
/content/journal/jgv/10.1099/jgv.0.001827
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

Supplementary material 2

EXCEL

Supplementary material 3

EXCEL

Supplementary material 4

EXCEL

Supplementary material 5

EXCEL

Supplementary material 6

EXCEL

Supplementary material 7

EXCEL

Supplementary material 8

EXCEL

Supplementary material 9

EXCEL

Supplementary material 10

EXCEL

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error