Skip to content
1887

Journal of General Virology header logo Journal of General Virology

Volume 105, Issue 9

Insights into the molecular basis of beet curly top resistance in sugar beet through a transcriptomic approach at the early stage of symptom development No Access

Abstract

Curly top disease caused by (BCTV) is a limiting factor for sugar beet production. The most economical and sustainable control of BCTV in sugar beet would be via the growth of resistant cultivars, although most commercial cultivars possess only low-to-moderate quantitative resistance. A double haploid line (KDH13) showed a high level of resistance to BCTV infection. However, the mechanism of resistance and response of this line to BCTV infection is unknown. Here, we tested the response of this line to both local and systemic BCTV infections. The virus replicated at a high level in locally infected tissue but lower than in susceptible KDH19 plants. Resistant KDH13 plants systemically infected with BCTV showed only mild enation without leaf curling after 30 days. In contrast, severe leaf curling appeared after 12 days in susceptible plants with higher virus accumulation. Transcriptome analysis of the BCTV-infected KDH13 plants at the early stage of symptom development showed only 132 genes that were exclusively deregulated compared to the regulation of a large number of genes (1018 genes) in KDH19 plants. Pathway enrichment analysis showed that differentially expressed genes were predominantly involved in hormone metabolism, DNA methylation, immune response, cell cycle, biotic stress and oxidative stress. The auxin level in both resistant and susceptible plants increased in response to BCTV infection. Remarkably, exogenous application of auxin caused leaf curling phenotype in the absence of the virus. This study demonstrates the response of resistant and susceptible plants to BCTV infection at both local and systemic infections and highlights the defence-related genes and metabolic pathways including auxin for their contribution towards BCTV symptom development and resistance in sugar beet.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): auxin , beet curly top disease , geminivirus , resistance and transcriptome
Funding
This study was supported by the:
  • Deutsche Forschungsgemeinschaft (Award 672769/ EL1191-1-1)
    • Principal Award Recipient: OmidEini
© 2024 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.002026
2024-09-23
2025-11-12

Metrics

Loading full text...

Full text loading...

References

  1. Gharouni Kardani S, Heydarnejad J, Zakiaghl M, Mehrvar M, Kraberger S et al. Diversity of beet curly top Iran virus isolated from different hosts in Iran. Virus Genes 2013; 46:571–575 [View Article]
     [Google Scholar]
  2. Strausbaugh CA, Wintermantel WM, Gillen AM, Eujayl IA. Curly top survey in the Western United States. Phytopathology 2008; 98:1212–1217 [View Article] [PubMed]
     [Google Scholar]
  3. Stenger DC, Carbonaro D, Duffus JE. Genomic characterization of phenotypic variants of beet curly top virus. J Gen Virol 1990; 71 (Pt 10):2211–2215 [View Article] [PubMed]
     [Google Scholar]
  4. Bennett CW. The Curly Top Disease of Sugarbeet and Other Plants American Phytopathological Society, St Paul,MN; 1971
     [Google Scholar]
  5. Strausbaugh CA, Gillen AM, Camp S, Shock CC, Eldredge EP et al. Relationship of beet curly top foliar ratings to sugar beet yield. Plant Dis 2007; 91:1459–1463 [View Article] [PubMed]
     [Google Scholar]
  6. Stenger DC. Complete nucleotide sequence of the hypervirulent CFH strain of beet curly top virus. molecular plant-microbe interactions. Mol Plant-Microbe Interact 1994; 7:154–157
     [Google Scholar]
  7. Briddon RW, Stenger DC, Bedford ID, Stanley J, Izadpanah K et al. Comparison of a beet curly top virus isolate originating from the old world with those from the new world. Eur J Plant Pathol 1998; 104:77–84 [View Article]
     [Google Scholar]
  8. Stanley J, Markham PG, Callis RJ, Pinner MS. The nucleotide sequence of an infectious clone of the geminivirus beet curly top virus. EMBO J 1986; 5:1761–1767 [View Article] [PubMed]
     [Google Scholar]
  9. Stenger DC. Replication specificity elements of the worland strain of beet curly top virus are compatible with those of the CFH strain but not those of the cal/logan strain. Phytopathology 1998; 88:1174–1178 [View Article] [PubMed]
     [Google Scholar]
  10. Varsani A, Martin DP, Navas-Castillo J, Moriones E, Hernández-Zepeda C et al. Revisiting the classification of curtoviruses based on genome-wide pairwise identity. Arch Virol 2014; 159:1873–1882 [View Article] [PubMed]
     [Google Scholar]
  11. Duffus JE. Relationship of age of plants and resistance to a severe isolate of the beet curly top virus. Phytopathology 1977; 67:151 [View Article]
     [Google Scholar]
  12. Gillen AM, Strausbaugh CA, Tindall KV. Evaluation of beta corolliflora for resistance to curly top in Idaho. JSBR 2008; 45:99–118 [View Article]
     [Google Scholar]
  13. Eujayl IA. Beet curly top resistance in USDA-ARS kimberly germplasm lines evaluated in idaho, 2017. Plant Dis Manag Rep 2018; 12:CF152 [View Article]
     [Google Scholar]
  14. Eujayl I, Strausbaugh C, Lu C. Registration of sugarbeet doubled haploid line KDH13 with resistance to beet curly top. J Plant Regist 2016; 10:93–96 [View Article]
     [Google Scholar]
  15. Galewski PJ, Eujayl I. A roadmap to durable BCTV resistance using long-read genome assembly of genetic stock KDH13. Plant Mol Biol Rep 2022; 40:176–187 [View Article]
     [Google Scholar]
  16. Loriato VAP, Martins LGC, Euclydes NC, Reis PAB, Duarte CEM et al. Engineering resistance against geminiviruses: a review of suppressed natural defenses and the use of RNAi and the CRISPR/Cas system. Plant Sci 2020; 292:110410 [View Article] [PubMed]
     [Google Scholar]
  17. Fan H, Zhang Y, Sun H, Liu J, Wang Y et al. Transcriptome analysis of beta macrocarpa and identification of differentially expressed transcripts in response to beet necrotic yellow vein virus infection. PLoS One 2015; 10:e0132277 [View Article]
     [Google Scholar]
  18. Fernando Gil J, Wibberg D, Eini O, Savenkov EI, Varrelmann M et al. comparative transcriptome analysis provides molecular insights into the interaction of beet necrotic yellow vein virus and beet soil-borne mosaic virus with their host sugar beet. Viruses 2020; 12:1–21 [View Article] [PubMed]
     [Google Scholar]
  19. Fan H, Zhang Y, Sun H, Liu J, Wang Y et al. Transcriptome analysis of beta macrocarpa and identification of differentially expressed transcripts in response to beet necrotic yellow vein virus infection. PLoS One 2015; 10:1–17 [View Article] [PubMed]
     [Google Scholar]
  20. Sahu PP, Rai NK, Chakraborty S, Singh M, Chandrappa PH et al. Tomato cultivar tolerant to Tomato leaf curl New Delhi virus infection induces virus-specific short interfering RNA accumulation and defence-associated host gene expression. Mol Plant Pathol 2010; 11:531–544 [View Article] [PubMed]
     [Google Scholar]
  21. Majumdar R, Galewski PJ, Eujayl I, Minocha R, Vincill E et al. Regulatory roles of small non-coding RNAs in sugar beet resistance against beet curly top virus. Front Plant Sci 2021; 12:780877 [View Article] [PubMed]
     [Google Scholar]
  22. Ghosh D, Chakraborty S. Molecular interplay between phytohormones and geminiviruses: a saga of a never-ending arms race. J Exp Bot 2021; 72:2903–2917 [View Article] [PubMed]
     [Google Scholar]
  23. Müllender M, Varrelmann M, Savenkov EI, Liebe S. Manipulation of auxin signalling by plant viruses. Mol Plant Pathol 2021; 22:1449–1458 [View Article] [PubMed]
     [Google Scholar]
  24. Yu Z, Zhang F, Friml J, Ding Z. Auxin signaling: research advances over the past 30 years. J Integr Plant Biol 2022; 64:371–392 [View Article] [PubMed]
     [Google Scholar]
  25. Gupta K, Rishishwar R, Dasgupta I. The interplay of plant hormonal pathways and geminiviral proteins: partners in disease development. Virus Gen 2022; 58:1–14 [View Article]
     [Google Scholar]
  26. Park J, Hwang H, Shim H, Im K, Auh C-K et al. Altered cell shapes, hyperplasia, and secondary growth in Arabidopsis caused by beet curly top geminivirus infection. Mol Cells 2004; 17:117–124 [PubMed]
     [Google Scholar]
  27. Jia Q, Liu N, Xie K, Dai Y, Han S et al. CLCuMuB βC1 subverts ubiquitination by interacting with NbSKP1s to enhance geminivirus infection in Nicotiana benthamiana. PLoS Pathog 2016; 12:e1005668 [View Article]
     [Google Scholar]
  28. Vinutha T, Vanchinathan S, Bansal N, Kumar G, Permar V et al. Tomato auxin biosynthesis/signaling is reprogrammed by the geminivirus to enhance its pathogenicity. Planta 2020; 252:1–14 [View Article] [PubMed]
     [Google Scholar]
  29. Hennegan KP, Danna KJ. pBIN20: an improved binary vector for Agrobacterium-mediated transformation. Plant Mol Biol Rep 1998; 16:129–131 [View Article]
     [Google Scholar]
  30. 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]
  31. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 2013; 29:15–21 [View Article] [PubMed]
     [Google Scholar]
  32. Dohm JC, Minoche AE, Holtgräwe D, Capella-Gutiérrez S, Zakrzewski F et al. The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature 2014; 505:546–549 [View Article] [PubMed]
     [Google Scholar]
  33. 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]
  34. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014; 15:1–21 [View Article] [PubMed]
     [Google Scholar]
  35. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Series B 1995; 57:289–300 [View Article]
     [Google Scholar]
  36. Minoche AE, Dohm JC, Schneider J, Holtgräwe D, Viehöver P et al. Exploiting single-molecule transcript sequencing for eukaryotic gene prediction. Genome Biol 2015; 16:184 [View Article] [PubMed]
     [Google Scholar]
  37. Riley ML, Schmidt T, Artamonova II, Wagner C, Volz A et al. PEDANT genome database: 10 years online. Nucleic Acids Res 2007; 35:D354–D357 [View Article] [PubMed]
     [Google Scholar]
  38. Kanehisa M, Sato Y, Kawashima M. KEGG mapping tools for uncovering hidden features in biological data. Protein Sci 2022; 31:47–53 [View Article] [PubMed]
     [Google Scholar]
  39. Alexa A, Rahnenführer J. Gene set enrichment analysis with topgo. Bioconductor Improv 2009; 27:1–26
     [Google Scholar]
  40. Freeborough W, Gentle N, Rey MEC. WRKY transcription factors in cassava contribute to regulation of tolerance and susceptibility to cassava mosaic disease through stress responses. Viruses 2021; 13:1820 [View Article] [PubMed]
     [Google Scholar]
  41. Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S et al. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 2004; 37:914–939 [View Article] [PubMed]
     [Google Scholar]
  42. Friedmann M, Lapidot M, Cohen S, Pilowsky M. A novel source of resistance to tomato yellow leaf curl virus exhibiting a symptomless reaction to viral infection. J Am Soc Hort Sci 1998; 123:1004–1007 [View Article]
     [Google Scholar]
  43. Arunachalam P. Reaction of bitter gourd genotypes against distortion mosaic virus. Veg Sci 2002; 29:55–57
     [Google Scholar]
  44. Pierce EJ, Rey MEC. Assessing global transcriptome changes in response to South African cassava mosaic virus [ZA-99] infection in susceptible Arabidopsis thaliana. PLoS One 2013; 8:e67534 [View Article] [PubMed]
     [Google Scholar]
  45. Mason G, Noris E, Lanteri S, Acquadro A, Accotto GP et al. Potentiality of methylation-sensitive amplification polymorphism (MSAP) in identifying genes involved in tomato response to tomato yellow leaf curl sardinia virus. Plant Mol Biol Rep 2008; 26:156–173 [View Article]
     [Google Scholar]
  46. Buchmann RC, Asad S, Wolf JN, Mohannath G, Bisaro DM. Geminivirus AL2 and L2 proteins suppress transcriptional gene silencing and cause genome-wide reductions in cytosine methylation. J Virol 2009; 83:5005–5013 [View Article] [PubMed]
     [Google Scholar]
  47. Raja P, Jackel JN, Li S, Heard IM, Bisaro DM. Arabidopsis double-stranded RNA binding protein DRB3 participates in methylation-mediated defense against geminiviruses. J Virol 2014; 88:2611–2622 [View Article] [PubMed]
     [Google Scholar]
  48. Torchetti EM, Pegoraro M, Navarro B, Catoni M, Di Serio F et al. A nuclear-replicating viroid antagonizes infectivity and accumulation of a geminivirus by upregulating methylation-related genes and inducing hypermethylation of viral DNA. Sci Rep 2016; 6:35101 [View Article] [PubMed]
     [Google Scholar]
  49. Raja P, Sanville BC, Buchmann RC, Bisaro DM. Viral genome methylation as an epigenetic defense against geminiviruses. J Virol 2008; 82:8997–9007 [View Article] [PubMed]
     [Google Scholar]
  50. Brough CL, Gardiner WE, Inamdar NM, Zhang XY, Ehrlich M et al. DNA methylation inhibits propagation of tomato golden mosaic virus DNA in transfected protoplasts. Plant Mol Biol 1992; 18:703–712 [View Article]
     [Google Scholar]
  51. Butt H, Graner S, Luschnig C. Expression analysis of Arabidopsis XH/XS-domain proteins indicates overlapping and distinct functions for members of this gene family. J Exp Bot 2014; 65:1217–1227 [View Article] [PubMed]
     [Google Scholar]
  52. Matzke MA, Mosher RA. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 2014; 15:394–408 [View Article] [PubMed]
     [Google Scholar]
  53. Song Z-T, Liu J-X, Han J-J. Chromatin remodeling factors regulate environmental stress responses in plants. J Integr Plant Biol 2021; 63:438–450 [View Article] [PubMed]
     [Google Scholar]
  54. Eamens AL, Wook Kim K, Waterhouse PM. DRB2, DRB3 and DRB5 function in a non-canonical microRNA pathway in Arabidopsis thaliana. Plant Signal Behav 2012; 7:1224–1229 [View Article] [PubMed]
     [Google Scholar]
  55. Hwang IS, Hwang BK. Role of the pepper cytochrome P450 gene CaCYP450A in defense responses against microbial pathogens. Planta 2010; 232:1409–1421 [View Article] [PubMed]
     [Google Scholar]
  56. Zhang J-H, Zhao M, Zhou Y-J, Xu Q-F, Yang Y-X. Cytochrome P450 monooxygenases CYP6AY3 and CYP6CW1 regulate rice black-streaked dwarf virus replication in laodelphax striatellus (Fallén). Viruses 2021; 13:1576 [View Article]
     [Google Scholar]
  57. Yang L-P, Fang Y-Y, An C-P, Dong L, Zhang Z-H et al. C2-mediated decrease in DNA methylation, accumulation of siRNAs, and increase in expression for genes involved in defense pathways in plants infected with beet severe curly top virus. Plant J 2013; 73:910–917 [View Article] [PubMed]
     [Google Scholar]
  58. Padmanabhan C, Ma Q, Shekasteband R, Stewart KS, Hutton SF et al. Comprehensive transcriptome analysis and functional characterization of PR-5 for its involvement in tomato Sw-7 resistance to tomato spotted wilt tospovirus. Sci Rep 2019; 9:7673 [View Article] [PubMed]
     [Google Scholar]
  59. Butterbrodt T, Thurow C, Gatz C. Chromatin immunoprecipitation analysis of the tobacco PR-1a- and the truncated CaMV 35S promoter reveals differences in salicylic acid-dependent TGA factor binding and histone acetylation. Plant Mol Biol 2006; 61:665–674 [View Article] [PubMed]
     [Google Scholar]
  60. Schiermeyer A, Thurow C, Gatz C. Tobacco bZIP factor TGA10 is a novel member of the TGA family of transcription factors. Plant Mol Biol 2003; 51:817–829 [View Article] [PubMed]
     [Google Scholar]
  61. von Dahlen JK, Schulz K, Nicolai J, Rose LE. Global expression patterns of R-genes in tomato and potato. Front Plant Sci 2023; 14:1216795 [View Article]
     [Google Scholar]
  62. Chakraborty S, Nguyen B, Wasti SD, Xu G. Plant leucine-rich repeat receptor kinase (LRR-RK): structure, ligand perception, and activation mechanism. Molecules 2019; 24:3081 [View Article] [PubMed]
     [Google Scholar]
  63. Fontes EPB, Teixeira RM, Lozano-Durán R. Plant virus-interactions: unraveling novel defense mechanisms under immune-suppressing pressure. Curr Opin Biotechnol 2021; 70:108–114 [View Article] [PubMed]
     [Google Scholar]
  64. Zhu Q, Feng Y, Xue J, Chen P, Zhang A et al. Advances in receptor-like protein kinases in balancing plant growth and stress responses. Plants 2023; 12:427 [View Article] [PubMed]
     [Google Scholar]
  65. Sun L, Zhang J. Regulatory role of receptor-like cytoplasmic kinases in early immune signaling events in plants. FEMS Microbiol Rev 2020; 44:845–856 [View Article] [PubMed]
     [Google Scholar]
  66. Garnelo Gómez B, Zhang D, Rosas-Díaz T, Wei Y, Macho AP et al. The C4 protein from tomato yellow leaf curl virus can broadly interact with plant receptor-like kinases. Viruses 2019; 11:1009 [View Article] [PubMed]
     [Google Scholar]
  67. Li H, Zeng R, Chen Z, Liu X, Cao Z et al. S-acylation of a geminivirus C4 protein is essential for regulating the CLAVATA pathway in symptom determination. J Exp Bot 2018; 69:4459–4468 [View Article] [PubMed]
     [Google Scholar]
  68. Rosas-Diaz T, Zhang D, Fan P, Wang L, Ding X et al. A virus-targeted plant receptor-like kinase promotes cell-to-cell spread of RNAi. Proc Natl Acad Sci U S A 2018; 115:1388–1393 [View Article] [PubMed]
     [Google Scholar]
  69. Carluccio AV, Prigigallo MI, Rosas-Diaz T, Lozano-Duran R, Stavolone L. S‐acylation mediates Mungbean yellow mosaic virus AC4 localization to the plasma membrane and in turns gene silencing suppression. PLoS Pathog 2018; 14:e1007207 [View Article]
     [Google Scholar]
  70. Zorzatto C, Machado JPB, Lopes KVG, Nascimento KJT, Pereira WA et al. NIK1-mediated translation suppression functions as a plant antiviral immunity mechanism. Nature 2015; 520:679–682 [View Article] [PubMed]
     [Google Scholar]
  71. Arroyo-Mateos M, Sabarit B, Maio F, Sánchez-Durán MA, Rosas-Díaz T et al. Geminivirus replication protein impairs SUMO conjugation of proliferating cellular nuclear antigen at two acceptor sites. J Virol 2018; 92:e00611–00618 [View Article] [PubMed]
     [Google Scholar]
  72. Morilla G, Castillo AG, Preiss W, Jeske H, Bejarano ER. A versatile transreplication-based system to identify cellular proteins involved in geminivirus replication. J Virol 2006; 80:3624–3633 [View Article] [PubMed]
     [Google Scholar]
  73. Bagewadi B, Chen S, Lal SK, Choudhury NR, Mukherjee SK. PCNA interacts with Indian mung bean yellow mosaic virus rep and downregulates Rep activity. J Virol 2004; 78:11890–11903 [View Article] [PubMed]
     [Google Scholar]
  74. Mandal A, Mishra AK, Dulani P, Muthamilarasan M, Shweta S et al. Identification, characterization, expression profiling, and virus-induced gene silencing of armadillo repeat-containing proteins in tomato suggest their involvement in tomato leaf curl New Delhi virus resistance. Funct Integr Genomics 2018; 18:101–111 [View Article]
     [Google Scholar]
  75. Albertini V, Jain A, Vignati S, Napoli S, Rinaldi A et al. Novel GC-rich DNA-binding compound produced by a genetically engineered mutant of the mithramycin producer Streptomyces argillaceus exhibits improved transcriptional repressor activity: implications for cancer therapy. Nucleic Acids Res 2006; 34:1721–1734 [View Article] [PubMed]
     [Google Scholar]
  76. Ascencio-Ibáñez JT, Sozzani R, Lee T-J, Chu T-M, Wolfinger RD et al. Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol 2008; 148:436–454 [View Article] [PubMed]
     [Google Scholar]
  77. Jeevalatha A, Siddappa S, Kumar A, Kaundal P, Guleria A et al. An insight into differentially regulated genes in resistant and susceptible genotypes of potato in response to tomato leaf curl New Delhi virus-[potato] infection. Virus Res 2017; 232:22–33 [View Article] [PubMed]
     [Google Scholar]
  78. Yang L, Meng D, Wang Y, Wu Y, Lang C et al. The viral suppressor HCPro decreases DNA methylation and activates auxin biosynthesis genes. Virology 2020; 546:133–140 [View Article] [PubMed]
     [Google Scholar]
  79. Zhang Z, Chen H, Huang X, Xia R, Zhao Q et al. BSCTV C2 attenuates the degradation of SAMDC1 to suppress DNA methylation-mediated gene silencing in Arabidopsis. Plant Cell 2011; 23:273–288 [View Article] [PubMed]
     [Google Scholar]
  80. Lee SC. Auxin effects on symptom development of beet curly top virus infected Arabidopsis thaliana. J Bot Soc 1996; 39:249–256
     [Google Scholar]
  81. Xu J, Li J, Cui L, Zhang T, Wu Z et al. New insights into the roles of cucumber TIR1 homologs and miR393 in regulating fruit/seed set development and leaf morphogenesis. BMC Plant Biol 2017; 17:1–14 [View Article]
     [Google Scholar]
  82. Dharmasiri N, Dharmasiri S, Estelle M. The F-box protein TIR1 is an auxin receptor. Nature 2005; 435:441–445 [View Article] [PubMed]
     [Google Scholar]
  83. Wilmoth JC, Wang S, Tiwari SB, Joshi AD, Hagen G et al. NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 2005; 43:118–130 [View Article] [PubMed]
     [Google Scholar]
  84. Brackmann K, Qi J, Gebert M, Jouannet V, Schlamp T et al. Spatial specificity of auxin responses coordinates wood formation. Nat Commun 2018; 9:875 [View Article] [PubMed]
     [Google Scholar]
  85. Latham JR, Saunders K, Pinner MS, Stanley J. Induction of plant cell division by beet curly top virus gene C4. Plant J 1997; 11:1273–1283 [View Article]
     [Google Scholar]
  86. Song L, Wang Y, Zhao L, Zhao T. Transcriptome profiling unravels the involvement of phytohormones in tomato resistance to the Tomato Yellow Leaf Curl Virus (TYLCV). Horticulturae 2022; 8:143 [View Article]
     [Google Scholar]
/content/journal/jgv/10.1099/jgv.0.002026
Loading
Insights into the molecular basis of beet curly top resistance in sugar beet through a transcriptomic approach at the early stage of symptom development
J. Gen. Virol. 105, 002026 (2024); https://doi.org/10.1099/jgv.0.002026
/content/journal/jgv/10.1099/jgv.0.002026
/content/journal/jgv/10.1099/jgv.0.002026
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

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