1887

Abstract

(BSBV) is a sugar beet pomovirus frequently associated with , the causal agent of the rhizomania disease. BSBV has been detected in most of the major beet-growing regions worldwide, yet its impact on this crop remains unclear. With the aim to understand the life cycle of this virus and clarify its putative pathogenicity, agroinfectious clones have been engineered for each segment of its tripartite genome. The biological properties of these clones were then studied on different plant species. Local infection was obtained on agroinfiltrated leaves of . On leaves of , similar results were obtained, but only when heterologous viral suppressors of RNA silencing were co-expressed or in a transgenic line down regulated for both dicer-like protein 2 and 4. On sugar beet, local infection following agroinoculation was obtained on cotyledons, but not on other tested plant parts. Nevertheless, leaf symptoms were observed on this host via sap inoculation. Likewise, roots were efficiently mechanically infected, highlighting low frequency of root necrosis and constriction, and enabling the demonstration of transmission by the vector . Altogether, the entire viral cycle was reproduced, validating the constructed agroclones as efficient inoculation tools, paving the way for further studies on BSBV and its related pathosystem.

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2020-11-20
2024-04-25
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References

  1. Henry CM, Jones RAC, Coutts RHA. Occurrence of a soil-borne virus of sugar beet in England. Plant Pathol 1986; 35:585–591 [View Article]
    [Google Scholar]
  2. Barbarossa L, Vetten HJ, Kaufmann A, Lesemann D-E, Koenig R. Monoclonal antibodies to beet soil-borne virus. Annals of Applied Biology 1992; 121:143–150 [View Article]
    [Google Scholar]
  3. Koenig R, Loss S. Beet soil-borne virus RNA 1: genetic analysis enabled by a starting sequence generated with primers to highly conserved helicase-encoding domains. J Gen Virol 1997; 78:3161–3165 [View Article][PubMed]
    [Google Scholar]
  4. Koenig R, Commandeur U, Loss S, Beier C, Kaufmann A et al. Beet soil-borne virus RNA 2: similarities and dissimilarities to the coat protein gene-carrying RNAs of other furoviruses. J Gen Virol 1997; 78:469–477 [View Article][PubMed]
    [Google Scholar]
  5. Koenig R, Beier C, Commandeur U, Lüth U, Kaufmann A et al. Beet soil-borne virus RNA 3-a further example of the heterogeneity of the gene content of furovirus genomes and of triple gene block-carrying RNAs. Virology 1996; 216:202–207 [View Article][PubMed]
    [Google Scholar]
  6. Adams MJ, Antoniw JF, Kreuze J. Virgaviridae: a new family of rod-shaped plant viruses. Arch Virol 2009; 154:1967–1972 [View Article][PubMed]
    [Google Scholar]
  7. Savenkov EI, Sandgren M, Valkonen JPT. Complete sequence of RNA 1 and the presence of tRNA-like structures in all RNAs of potato mop-top virus, genus Pomovirus. J Gen Virol 1999; 80 (Pt 10:2779–2784 [View Article][PubMed]
    [Google Scholar]
  8. Lu X, Yamamoto S, Tanaka M, Hibi T, Namba S. The genome organization of the broad bean necrosis virus (BBNV). Arch Virol 1998; 143:1335–1348 [View Article]
    [Google Scholar]
  9. Gil JF, Adams I, Boonham N, Nielsen SL, Nicolaisen M. Molecular and biological characterisation of two novel pomo-like viruses associated with potato (Solanum tuberosum) fields in Colombia. Arch Virol 2016; 161:1601–1610 [View Article][PubMed]
    [Google Scholar]
  10. Koenig R, Pleij CW, Beier C, Commandeur U. Genome properties of beet virus Q, a new furo-like virus from sugarbeet, determined from Unpurified virus. J Gen Virol 1998; 79:2027–2036 [View Article][PubMed]
    [Google Scholar]
  11. Scott KP, Kashiwazaki S, Reavy B, Harrison BD. The nucleotide sequence of potato mop-top virus RNA 2: a novel type of genome organization for a furovirus. J Gen Virol 1994; 75:3561–3568 [View Article][PubMed]
    [Google Scholar]
  12. Kalyandurg PB, Tahmasebi A, Vetukuri RR, Kushwaha SK, Lezzhov AA et al. Efficient RNA silencing suppression activity of potato Mop-Top virus 8K protein is driven by variability and positive selection. Virology 2019; 535:111–121 [View Article][PubMed]
    [Google Scholar]
  13. Lukhovitskaya NI, Thaduri S, Garushyants SK, Torrance L, Savenkov EI. Deciphering the mechanism of defective interfering RNA (di RNA) biogenesis reveals that a viral protein and the di RNA act antagonistically in virus infection. J Virol 2013; 87:6091–6103 [View Article][PubMed]
    [Google Scholar]
  14. Savenkov EI, Germundsson A, Zamyatnin AA, Sandgren M, Valkonen JPT. Potato mop-top virus: the coat protein-encoding RNA and the gene for cysteine-rich protein are dispensable for systemic virus movement in Nicotiana benthamiana . J Gen Virol 2003; 84:1001–1005 [View Article][PubMed]
    [Google Scholar]
  15. Meunier A, Schmit J-F, Stas A, Kutluk N, Bragard C. Multiplex reverse transcription-PCR for simultaneous detection of beet necrotic yellow vein virus, beet soilborne virus, and beet virus Q and their vector polymyxa betaE KESKIN on sugar beet. Appl Environ Microbiol 2003; 69:2356–2360 [View Article][PubMed]
    [Google Scholar]
  16. Yilmaz NDK, Sokmen MA, Kaya R, Sevik MA, Tunali B et al. The widespread occurrences of beet soil borne virus and RNA-5 containing beet necrotic yellow vein virus isolates in sugar beet production areas in turkey. Eur J Plant Pathol 2016; 144:443–455 [View Article]
    [Google Scholar]
  17. Mouhanna AM, Nasrallah A, Langen G, Schlösser E. Surveys for beet necrotic yellow vein virus (the cause of Rhizomania), other viruses, and soil-borne fungi infecting sugar beet in Syria. Journal of Phytopathology 2002; 150:657–662 [View Article]
    [Google Scholar]
  18. Mouhanna AM, Choueiri E. First report of beet soil-borne virus in Rhizomania-infested soils of sugar beet fields in Lebanon. J Plant Pathol 2009; 91:S108
    [Google Scholar]
  19. Farzadfar S, Pourrahim R, Golnaraghi AR, Shahraeen N. First report of beet soil-borne virus on sugar beet in Iran. Plant Dis 2002; 86:187 [View Article][PubMed]
    [Google Scholar]
  20. Lindsten K, Rush CM. First report of beet soilborne virus in the United States. Plant Disease 1994; 78:316C [View Article]
    [Google Scholar]
  21. Wang B, Li M, Zhang J, Han C, Li D et al. First report of beet soil-borne virus on sugar beet in China. Plant Pathol 2008; 57:389 [View Article]
    [Google Scholar]
  22. Ratti C, Bianchi L, Resca R, De Biaggi M, Harju VA et al. Incidence of sugar beet soil-borne viruses in sugar beet growing countries. In: Proceedings of the Sixth Symposium of the International Working group on Plant Viruses with Fungal Vectors
    [Google Scholar]
  23. Nouayti F, Tahiri A, Madani I, Blenzar A, Lahlali R. Detection and prevalence of viruses associated with sugarbeet in the Tadla region of Morocco. J Plant Pathol 2019; 101:173–177 [View Article]
    [Google Scholar]
  24. Camelo-García VM, Rezende JAM, Nagata T. First report of beet soil-borne virus on red table beet in Brazil. Plant Dis 2019; 103:2146 [View Article]
    [Google Scholar]
  25. McGrann GRD, Grimmer MK, Mutasa-Göttgens ES, Stevens M. Progress towards the understanding and control of sugar beet rhizomania disease. Mol Plant Pathol 2009; 10:129–141 [View Article][PubMed]
    [Google Scholar]
  26. Hill SA, Torrance L. Rhizomania disease of sugar beet in England. Plant Pathology 1989; 38:114–122 [View Article]
    [Google Scholar]
  27. Gaafar Y, Sieg-Müller A, Lüddecke P, Hartrick J, Seide Y et al. First report of natural infection of beetroot with Beet soil-borne virus . New Dis Rep 2019; 40:5 [View Article]
    [Google Scholar]
  28. Kaufmann A, Koenig R, Rohloff H. Influence of beet soil-borne virus on mechanically inoculated sugar beet. Plant Pathology 1993; 42:413–417 [View Article]
    [Google Scholar]
  29. Crutzen F, Mehrvar M, Gilmer D, Bragard C. A full-length infectious clone of beet soil-borne virus indicates the dispensability of the RNA-2 for virus survival in planta and symptom expression on Chenopodium quinoa leaves. J Gen Virol 2009; 90:3051–3056 [View Article][PubMed]
    [Google Scholar]
  30. Grimsley N, Hohn B, Hohn T, Walden R. “Agroinfection,” an alternative route for viral infection of plants by using the Ti plasmid. Proc Natl Acad Sci U S A 1986; 83:3282–3286 [View Article]
    [Google Scholar]
  31. Pasin F, Menzel W, Daròs J-A. Harnessed viruses in the age of metagenomics and synthetic biology: an update on infectious clone assembly and biotechnologies of plant viruses. Plant Biotechnol J 2019; 17:1010–1026 [View Article][PubMed]
    [Google Scholar]
  32. Delbianco A, Lanzoni C, Klein E, Rubies Autonell C, Gilmer D et al. Agroinoculation of Beet necrotic yellow vein virus cDNA clones results in plant systemic infection and efficient Polymyxa betae transmission. Mol Plant Pathol 2013; 14:422–428 [View Article][PubMed]
    [Google Scholar]
  33. Laufer M, Mohammad H, Maiss E, Richert-Pöggeler K, Dall'Ara M et al. Biological properties of beet soil-borne mosaic virus and beet necrotic yellow vein virus cDNA clones produced by isothermal in vitro recombination: insights for reassortant appearance. Virology 2018; 518:25–33 [View Article][PubMed]
    [Google Scholar]
  34. Laufer M, Mohammad H, Christ DS, Riedel D, Maiss E et al. Fluorescent labelling of beet necrotic yellow vein virus and beet soil-borne mosaic virus for Co- and superinfection experiments in Nicotiana benthamiana . J Gen Virol 2018; 99:1321–1330 [View Article][PubMed]
    [Google Scholar]
  35. Liebe S, Wibberg D, Maiss E, Varrelmann M. Application of a reverse genetic system for beet necrotic yellow vein virus to study Rz1 resistance response in sugar beet. Front Plant Sci 2019; 10:10 [View Article][PubMed]
    [Google Scholar]
  36. Lindbo JA. TRBO: a high-efficiency tobacco mosaic virus RNA-based overexpression vector. Plant Physiol 2007; 145:1232–1240 [View Article][PubMed]
    [Google Scholar]
  37. Blawid R, Nagata T. Construction of an infectious clone of a plant RNA virus in a binary vector using one-step Gibson assembly. J Virol Methods 2015; 222:11–15 [View Article]
    [Google Scholar]
  38. Uhrig JF, Canto T, Marshall D, MacFarlane SA. Relocalization of nuclear ALY proteins to the cytoplasm by the tomato bushy stunt virus P19 pathogenicity protein. Plant Physiol 2004; 135:2411–2423 [View Article][PubMed]
    [Google Scholar]
  39. Tena Fernández F, González I, Doblas P, Rodríguez C, Sahana N et al. The influence of cis-acting P1 protein and translational elements on the expression of potato virus Y helper-component proteinase (HCPro) in heterologous systems and its suppression of silencing activity. Mol Plant Pathol 2013; 14:530–541 [View Article][PubMed]
    [Google Scholar]
  40. González I, Martínez L, Rakitina DV, Lewsey MG, Atencio FA et al. Cucumber mosaic virus 2B protein subcellular targets and interactions: their significance to RNA silencing suppressor activity. Mol Plant Microbe Interact 2010; 23:294–303 [View Article][PubMed]
    [Google Scholar]
  41. Koenig R, Stein B. Distribution of beet necrotic yellow vein virus in mechanically inoculated sugarbeet plantlets of cultivars with different degrees of rizomania resistance. In Braunschweig 1990
    [Google Scholar]
  42. Dadami E, Boutla A, Vrettos N, Tzortzakaki S, Karakasilioti I et al. Dicer-Like 4 but not Dicer-like 2 may have a positive effect on potato spindle tuber viroid accumulation in Nicotiana benthamiana . Mol Plant 2013; 6:232–234 [View Article]
    [Google Scholar]
  43. Katsarou K, Mitta E, Bardani E, Oulas A, Dadami E et al. DCL-suppressed Nicotiana benthamiana plants: valuable tools in research and biotechnology. Mol Plant Pathol 2019; 20:432–446 [View Article][PubMed]
    [Google Scholar]
  44. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680–685 [View Article][PubMed]
    [Google Scholar]
  45. Roberts IM, Harrison BD. Detection of potato leafroll and potato mop-top viruses by immunosorbent electron microscopy. Ann Appl Biol 1979; 93:289–297 [View Article]
    [Google Scholar]
  46. Khankhum S, Escalante C, de Souto and ER, Valverde RA. Extraction and electrophoretic analysis of large dsRNAs from desiccated plant tissues infected with plant viruses and biotrophic fungi. Eur J Plant Pathol 2017; 147:431–441 [View Article]
    [Google Scholar]
  47. Legrève A, Delfosse P, Vanpee B, Goffin A, Maraite H. Differences in temperature requirements between polymyxa sp. of Indian origin and polymyxa graminis and polymyxa betaE from temperate areas. Eur J Plant Pathol 1998; 104:195–205 [View Article]
    [Google Scholar]
  48. Hutchinson PJ, Henry CM, Coutts RH, comparison A. A comparison, using dsRNA analysis, between beet soil-borne virus and some other tubular viruses isolated from sugar beet. J Gen Virol 1992; 73:1317–1320 [View Article][PubMed]
    [Google Scholar]
  49. Cui T, Bin Y, Yan J, Mei P, Li Z et al. Development of infectious cDNA clones of citrus yellow vein clearing virus using a novel and rapid strategy. Phytopathology 2018; 108:1212–1218 [View Article][PubMed]
    [Google Scholar]
  50. Feng M, Zhang H, Pan Y, Hu Y, Chen J et al. Complete nucleotide sequence of strawberry vein banding virus Chinese isolate and infectivity of its full-length DNA clone. Virol J 2016; 13:164 [View Article][PubMed]
    [Google Scholar]
  51. Yang S-J, Carter SA, Cole AB, Cheng N-H, Nelson RS. A natural variant of a host RNA-dependent RNA polymerase is associated with increased susceptibility to viruses by Nicotiana benthamiana . Proc Natl Acad Sci U S A 2004; 101:6297–6302 [View Article][PubMed]
    [Google Scholar]
  52. Ambrós S, El-Mohtar C, Ruiz-Ruiz S, Peña L, Guerri J et al. Agroinoculation of citrus tristeza virus causes systemic infection and symptoms in the presumed nonhost Nicotiana benthamiana . Mol Plant Microbe Interact 2011; 24:1119–1131 [View Article][PubMed]
    [Google Scholar]
  53. Yoon J-Y, Choi S-K, Palukaitis P, Gray SM. Agrobacterium-mediated infection of whole plants by yellow dwarf viruses. Virus Res 2011; 160:428–434 [View Article][PubMed]
    [Google Scholar]
  54. Fukuzawa N, Itchoda N, Ishihara T, Goto K, Masuta C et al. Hc-Pro, a potyvirus RNA silencing suppressor, cancels cycling of cucumber mosaic virus in Nicotiana benthamiana plants. Virus Genes 2010; 40:440–446 [View Article][PubMed]
    [Google Scholar]
  55. Norkunas K, Harding R, Dale J, Dugdale B. Improving agroinfiltration-based transient gene expression in Nicotiana benthamiana . Plant Methods 2018; 14:71 [View Article][PubMed]
    [Google Scholar]
  56. Fukudome A, Fukuhara T. Plant Dicer-like proteins: double-stranded RNA-cleaving enzymes for small RNA biogenesis. J Plant Res 2017; 130:33–44 [View Article][PubMed]
    [Google Scholar]
  57. Matsuo K, Matsumura T. Repression of the DCL2 and DCL4 genes in Nicotiana benthamiana plants for the transient expression of recombinant proteins. J Biosci Bioeng 2017; 124:215–220 [View Article][PubMed]
    [Google Scholar]
  58. Cordero T, Cerdán L, Carbonell A, Katsarou K, Kalantidis K et al. Dicer-Like 4 is involved in restricting the systemic movement of Zucchini yellow mosaic virus in Nicotiana benthamiana . MPMI 2017; 30:63–71 [View Article]
    [Google Scholar]
  59. Rysanek P, Stocky G, Haeberle AM, Putz C. Immunogold labelling of beet necrotic yellow vein virus particles inside its fungal vector, polymyxa betae K. Agronomie; 1992; 8651–659
  60. Goodin MM, Zaitlin D, Naidu RA, Lommel SA. Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions. Mol Plant Microbe Interact 2008; 21:1015–1026 [View Article][PubMed]
    [Google Scholar]
  61. Andika IB, Kondo H, Sun L. Interplays between soil-borne plant viruses and RNA Silencing-Mediated antiviral defense in roots. Front Microbiol 2016; 7:1458 [View Article][PubMed]
    [Google Scholar]
  62. Andika IB, Maruyama K, Sun L, Kondo H, Tamada T et al. Differential contributions of plant Dicer-like proteins to antiviral defences against potato virus X in leaves and roots. Plant J 2015; 81:781–793 [View Article][PubMed]
    [Google Scholar]
  63. Li L, Andika IB, Xu Y, Zhang Y, Xin X et al. Differential characteristics of viral siRNAs between leaves and roots of wheat plants naturally infected with wheat yellow mosaic virus, a soil-borne virus. Front Microbiol 2017; 8:1802 [View Article][PubMed]
    [Google Scholar]
  64. Gurel E, Gurel S, Lemaux PG. Biotechnology applications for sugar beet. CRC Crit Rev Plant Sci 2008; 27:108–140 [View Article]
    [Google Scholar]
  65. Stephan D, Maiss E. Biological properties of beet mild yellowing virus derived from a full-length cDNA clone. J Gen Virol 2006; 87:445–449 [View Article][PubMed]
    [Google Scholar]
  66. Klein E, Brault V, Klein D, Weyens G, Lefèbvre M et al. Divergence of host range and biological properties between natural isolate and full-length infectious cDNA clone of the beet mild yellowing virus 2ITB. Mol Plant Pathol 2014; 15:22–30 [View Article][PubMed]
    [Google Scholar]
  67. Jiang N, Zhang C, Liu J-Y, Guo Z-H, Zhang Z-Y et al. Development of beet necrotic yellow vein virus-based vectors for multiple-gene expression and guide RNA delivery in plant genome editing. Plant Biotechnol J 2019; 17:1302–1315 [View Article][PubMed]
    [Google Scholar]
  68. Inouye T, Asatani M. Broadbean necrosis virus. Jpn J Appl Phys 1968; 34:317–322 [View Article]
    [Google Scholar]
  69. Harrison BD, Jones RAC, C JRa. Effects of light and temperature on symptom development and virus content of tobacco leaves inoculated with potato mop-top virus. Ann Appl Biol 1971; 67:377–387 [View Article]
    [Google Scholar]
  70. Andika IB, Sun L, Xiang R, Li J, Chen J. Root-specific role for Nicotiana benthamiana RDR6 in the inhibition of Chinese wheat mosaic virus accumulation at higher temperatures. Mol Plant Microbe Interact 2013; 26:1165–1175 [View Article][PubMed]
    [Google Scholar]
  71. Ohsato S, Miyanishi M, Shirako Y. The optimal temperature for RNA replication in cells infected by soil-borne wheat mosaic virus is 17 degrees C. J Gen Virol 2003; 84:995–1000 [View Article][PubMed]
    [Google Scholar]
  72. Prillwitz H, Schlösser E. Temperature requirements of beet necrotic yellow vein virus (BNYVV) and beet soil-borne virus (BSBV-2) / Temperaturansprüche des Aderngelbfleckigkeitsvirus (BNYVV) und des beet soilborne virus (BSBV-2). J Plant Dis Protect 1993; 100:665–669
    [Google Scholar]
  73. Tamada T, Abe H. Evidence that beet necrotic yellow vein virus RNA-4 is essential for efficient transmission by the fungus polymyxa betaE. J Gen Virol 1989; 70:3391–3398 [View Article]
    [Google Scholar]
  74. Rahim MD, Andika IB, Han C, Kondo H, Tamada T. RNA4-encoded p31 of beet necrotic yellow vein virus is involved in efficient vector transmission, symptom severity and silencing suppression in roots. J Gen Virol 2007; 88:1611–1619 [View Article][PubMed]
    [Google Scholar]
  75. D'Alonzo M, Delbianco A, Lanzoni C, Autonell CR, Gilmer D et al. Beet soil-borne mosaic virus RNA-4 encodes a 32kDa protein involved in symptom expression and in virus transmission through polymyxa betaE. Virology 2012; 423:187–194 [View Article]
    [Google Scholar]
  76. Kanyuka K, Ward E, Adams MJ. Polymyxa graminis and the cereal viruses it transmits: a research challenge. Molecular Plant Pathol 2003; 4:393–406 [View Article][PubMed]
    [Google Scholar]
  77. Dieryck B, Weyns J, Doucet D, Bragard C, Legrève A. Acquisition and transmission of peanut clump virus by polymyxa graminis on cereal species. Phytopathology 2011; 101:1149–1158 [View Article][PubMed]
    [Google Scholar]
  78. Lubicz JV, Rush CM, Payton M, Colberg T. Beet necrotic yellow vein virus accumulates inside resting spores and zoosporangia of its vector polymyxa betae BNYVV infects P. betae . Virol J 2007; 4:37 [View Article][PubMed]
    [Google Scholar]
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