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Luteovirus: insights into pathogenicity

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Abstract

Luteoviruses are economically important plant viruses, infecting almost all cereals throughout the world. Idiosyncrasies related to this virus group may be a strategic consequence of viral genome compression. However, many fundamental questions have yet to be resolved. This review summarizes selected findings covering molecular aspects of pathogenesis relating to plant-infecting RNA viruses in general, and luteoviruses in specific. These studies enhance our understanding of the replication structures and the virus infection pathways.

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References

  1. Ahlquist P (2006) Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nat Rev Microbiol 4:371–382

    Article  PubMed  CAS  Google Scholar 

  2. Ali M, Tahir M, Hameed S, Ashraf M (2013) Coat protein based molecular characterization of Barley yellow dwarf virus isolates identified on oat plants in Pakistan. Acta Virol 57:383–385

    PubMed  CAS  Google Scholar 

  3. Allen E, Wang S, Miller WA (1999) Barley yellow dwarf virus RNA requires a cap-independent translation sequence because it lacks a 5′ cap. Virology 253:139–144

    Article  PubMed  CAS  Google Scholar 

  4. Andret-Link P, Fuchs M (2005) Transmission specificity of plant viruses by vectors. J Plant Pathol 87:153–165

    Google Scholar 

  5. Barry JK, Miller WA (2002) A −1 ribosomal frameshift element that requires base pairing across four kilobases suggests a mechanism of regulating ribosome and replicase traffic on a viral RNA. Proc Natl Acad Sci 99:11133–11138

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  6. Baulcombe D (2002) Viral suppression of systemic silencing. Trends Microbiol 10:306–308

    Article  PubMed  CAS  Google Scholar 

  7. Brown J (2000) Molecular markers for the identification and global tracking of whitefly vector—Begomovirus complexes. Virus Res 71:233–260

    Article  PubMed  CAS  Google Scholar 

  8. Callaway A, Giesman-Cookmeyer D, Gillock E, Sit T, Lommel S (2001) The multifunctional capsid proteins of plant RNA viruses. Annu Rev Phytopathol 39:419–460

    Article  PubMed  CAS  Google Scholar 

  9. Caplan JL, Mamillapalli P, Burch-Smith TM, Czymmek K, Dinesh-Kumar S (2008) Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell 132:449–462

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  10. Chay CA, Gunasinge UB, Dinesh-Kumar SP, Miller WA, Gray SM (1996) Aphid transmission and systemic plant infection determinants of barley yellow dwarf luteovirus-PAV are contained in the coat protein readthrough domain and 17-kDa protein, respectively. Virology 219:57–65

    Article  PubMed  CAS  Google Scholar 

  11. Cheng Z, He X, Wu M, Zhou G, Keese P, Waterhouse P (1996) Nucleotide sequence of coat protein gene for GPV isolate of barley yellow dwarf virus and construction of expression plasmid for plant. Sci China Ser C Life Sci (English Edition) 39:534–543

    CAS  Google Scholar 

  12. Coudriet D, Kishaba A, Bohn G (1981) Inheritance of resistance to muskmelon necrotic spot virus in a melon aphid-resistant breeding line of muskmelon [Cucumis melo, Aphis gossypii]. J Am Soc Hortic Sci 106:789–791

  13. D’Arcy CJ, Burnett PA (1995) Barley yellow dwarf virus: 40 years of progress. APS Press, St Paul, MN

  14. den Boon JA, Diaz A, Ahlquist P (2010) Cytoplasmic viral replication complexes. Cell Host Microbe 8:77–85

    Article  Google Scholar 

  15. Di R, Dinesh-Kumar SP, Miller WA (1993) Translational frameshifting by barley yellow dwarf virus RNA (PAV serotype) in Escherichia coli and in eukaryotic cell-free extracts. Mol Plant Microbe Interact MPMI 6:444–452

    Article  CAS  Google Scholar 

  16. Dinesh-Kumar S, Miller WA (1993) Control of start codon choice on a plant viral RNA encoding overlapping genes. Plant Cell Online 5:679–692

    Article  CAS  Google Scholar 

  17. Dolja VV, Koonin EV (1991) Phylogeny of capsid proteins of small icosahedral RNA plant viruses. J Gen Virol 72:1481–1486

    Article  PubMed  Google Scholar 

  18. Domier L (2008) Barley yellow dwarf virus. In: Mahy BWJ, Regenmortel MHV (eds) Encyclopedia of virology. Elsevier Ltd, Oxford, pp 279–286

  19. Domier L (2009) Barley yellow dwarf viruses. In: Mahy BWJ, Regenmortel MHV (eds) Desk encyclopedia of plant and fungal virology. Elsevier Ltd, Oxford, pp 100–107

    Google Scholar 

  20. Dreher TW, Miller WA (2006) Translational control in positive strand RNA plant viruses. Virology 344:185–197

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  21. Escaler M, Aranda MA, Thomas CL, Maule AJ (2000) Pea embryonic tissues show common responses to the replication of a wide range of viruses. Virology 267:318–325

    Article  PubMed  CAS  Google Scholar 

  22. Falk B, Tian T, Harrison B (1999) Transcapsidation interactions and dependent aphid transmission among luteoviruses, and luteovirus-associated RNAs. In: Smith HG, Barker H (eds) Luteoviridae. CAB International, Wallingford, UK, pp 125–134

  23. Fan Q, Treder K, Miller WA (2012) Untranslated regions of diverse plant viral RNAs vary greatly in translation enhancement efficiency. BMC Biotechnol 12:22

    Article  PubMed  CAS  Google Scholar 

  24. Fauquet CM, Mayo M, Maniloff J, Desselberger U, Ball LA (2005) Virus taxonomy: VIIIth report of the International Committee on Taxonomy of Viruses. Access Online via Elsevier

  25. Gildow F, Damsteegt V, Stone A, Smith O, Gray S (2000) Virus-vector cell interactions regulating transmission specificity of soybean dwarf luteoviruses. J Phytopathol 148:333–342

    Article  Google Scholar 

  26. Gildow FE (1987) Virus—membrane interactions involved in circulative transmission of luteoviruses by aphids. Current topics in vector research. Springer, Berlin, pp 93–120

    Google Scholar 

  27. Gill C, Chong J (1975) Development of the infection in oat leaves inoculated with barley yellow dwarf virus. Virology 66:440–453

    Article  PubMed  CAS  Google Scholar 

  28. Gill C, Chong J (1979) Cytopathological evidence for the division of barley yellow dwarf virus isolates into two subgroups. Virology 95:59–69

    Article  PubMed  CAS  Google Scholar 

  29. Gray S, Gildow FE (2003) Luteovirus-aphid interactions. Annu Review Phytopathol 41:539–566

    Article  CAS  Google Scholar 

  30. Gray SM, Banerjee N (1999) Mechanisms of arthropod transmission of plant and animal viruses. Microbiol Mol Biol Rev 63:128–148

    PubMed  CAS  PubMed Central  Google Scholar 

  31. Guo L, Allen EM, Miller WA (2001) Base-pairing between untranslated regions facilitates translation of uncapped, nonpolyadenylated viral RNA. Mol Cell 7:1103–1109

    Article  PubMed  CAS  Google Scholar 

  32. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  33. Kawakami S, Watanabe Y, Beachy RN (2004) Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc Natl Acad Sci USA 101:6291–6296

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  34. Koev G, Mohan BR, Dinesh-Kumar SP, Torbert KA, Somers DA, Miller WA (1998) Extreme reduction of disease in oats transformed with the 5’ half of the barley yellow dwarf virus-PAV genome. Phytopathology 88:1013–1019

    Article  PubMed  CAS  Google Scholar 

  35. Koev G, Miller WA (2000) A positive-strand RNA virus with three very different subgenomic RNA promoters. J Virol 74:5988–5996

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  36. Koev G, Liu S, Beckett R, Miller WA (2002) The 3′-terminal structure required for replication of barley yellow dwarf virus RNA contains an embedded 3′ end. Virology 292:114–126

    Article  PubMed  CAS  Google Scholar 

  37. Lee L, Palukaitis P, Gray SM (2002) Host-dependent requirement for the Potato leafroll virus 17-kDa protein in virus movement. Mol Plant Microbe Interact 15:1086–1094

    Article  PubMed  CAS  Google Scholar 

  38. Liu F, Wang X, Liu Y, Xie J, Gray S, Zhou G, Gao B (2007) A Chinese isolate of barley yellow dwarf virus-PAV represents a third distinct species within the PAV serotype. Arch Virol 152:1365–1373

    Article  PubMed  CAS  Google Scholar 

  39. Liu Y, Zhai H, Zhao K, Wu B, Wang X (2012) Two suppressors of RNA silencing encoded by cereal-infecting members of the family luteoviridae. J Gen Virol 93:1825–1830

    Article  PubMed  CAS  Google Scholar 

  40. Lucas WJ, Lee J-Y (2004) Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 5:712–726

    Article  PubMed  CAS  Google Scholar 

  41. Lucas WJ (2006) Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344:169–184

    Article  PubMed  CAS  Google Scholar 

  42. Mayo M, D’Arcy C (1999) Family Luteoviridae: a reclassification of luteoviruses. In: Smith HG, Barker H (eds) Luteoviridae. CAB International, Wallingford, UK, pp 15–22

  43. Miller WA, Rasochová L (1997) Barley yellow dwarf viruses. Annu Rev Phytopathol 35:167–190

    Article  PubMed  CAS  Google Scholar 

  44. Miller W, Beckett R, Liu S (2002) Structure, function and variation of the Barley yellow dwarf virus and Cereal yellow dwarf virus genomes. In: Henry M, McNab A (eds) Barley yellow dwarf disease: recent advances and future strategies. CIMMYT, Mexico, DF, pp 1–8

  45. Miller W, Wang Z, Treder K (2007) The amazing diversity of cap-independent translation elements in the 3′-untranslated regions of plant viral RNAs. Biochem Soc Trans 35:1629–1633

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  46. Miller WA, Liu S, Beckett R (2002) Barley yellow dwarf virus: luteoviridae or Tombusviridae? Mol Plant Pathol 3:177–183

    Article  PubMed  CAS  Google Scholar 

  47. Nass PH, Domier LL, Jakstys BP, D’Arcy CJ (1998) In situ localization of barley yellow dwarf virus-PAV 17-kDa protein and nucleic acids in oats. Phytopathology 88:1031–1039

    Article  PubMed  CAS  Google Scholar 

  48. Novoa RR, Calderita G, Arranz R, Fontana J, Granzow H, Risco C (2005) Virus factories: associations of cell organelles for viral replication and morphogenesis. Biol Cell 97:147–172

    Article  PubMed  CAS  Google Scholar 

  49. Paul CP, Barry JK, Dinesh-Kumar SP, Brault V, Miller WA (2001) A sequence required for −1 ribosomal frameshifting located four kilobases downstream of the frameshift site. J Mol Biol 310:987–999

    Article  PubMed  CAS  Google Scholar 

  50. Peter KA, Gildow F, Palukaitis P, Gray SM (2009) The C terminus of the polerovirus p5 readthrough domain limits virus infection to the phloem. J Virol 83:5419–5429

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  51. Plant EP, Jacobs KLM, Harger JW, Meskauskas A, Jacobs JL, Baxter JL, Petrov AN, Dinman JD (2003) The 9-Å solution: How mRNA pseudoknots promote efficient programmed −1 ribosomal frameshifting. RNA 9:168–174

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  52. Pogany J, Fabian MR, White KA, Nagy PD (2003) A replication silencer element in a plus-strand RNA virus. EMBO J 22:5602–5611

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  53. Power A, Gray S (1995) Aphid transmission of barley yellow dwarf viruses: interactions between viruses, vectors, and host plants. In: D’Arcy CJ, Burnett PA (eds) Barley yellow dwarf virus: 40 years of progress. APS Press, St Paul, MN, pp 259–289

  54. Reavy B, Mayo M (2002) Persistent transmission of luteoviruses by aphids. Adv Bot Res 36:21–46

    Article  CAS  Google Scholar 

  55. Restrepo-Hartwig MA, Ahlquist P (1996) Brome mosaic virus helicase-and polymerase-like proteins colocalize on the endoplasmic reticulum at sites of viral RNA synthesis. J Virol 70:8908–8916

    PubMed  CAS  PubMed Central  Google Scholar 

  56. Schaad MC, Jensen PE, Carrington JC (1997) Formation of plant RNA virus replication complexes on membranes: role of an endoplasmic reticulum-targeted viral protein. EMBO J 16:4049–4059

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  57. Shen R, Miller WA (2004) Subgenomic RNA as a riboregulator: negative regulation of RNA replication by Barley yellow dwarf virus subgenomic RNA 2. Virology 327:196–205

    Article  PubMed  CAS  Google Scholar 

  58. Tacke E, Prüfer D, Schmitz J, Rohde W (1991) The potato leafroll luteovirus 17 K protein is a single-stranded nucleic acid-binding protein. J Gen Virol 72:2035

    Article  PubMed  CAS  Google Scholar 

  59. Wang D, Maule AJ (1995) Inhibition of host gene expression associated with plant virus replication. Science 267:229–231

    Article  PubMed  CAS  Google Scholar 

  60. Wang M-B, Cheng Z, Keese P, Graham M, Larkin P, Waterhouse P (1998) Comparison of the coat protein, movement protein and RNA polymerase gene sequences of Australian, Chinese, and American isolates of barley yellow dwarf virus transmitted by Rhopalosiphum padi. Arch Virol 143:1005–1013

    Article  PubMed  CAS  Google Scholar 

  61. Wang S, Browning KS, Miller WA (1997) A viral sequence in the 3′-untranslated region mimics a 5′ cap in facilitating translation of uncapped mRNA. EMBO J 16:4107–4116

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  62. Wang S, Guo L, Allen E, Miller WA (1999) A potential mechanism for selective control of cap-independent translation by a viral RNA sequence in cis and in trans. RNA 5:728–738

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  63. Wang X, Chang S, Jin Z, Li L, Zhou G (2001) Nucleotide sequences of the coat protein and readthrough protein genes of the Chinese GAV isolate of barley yellow dwarf virus. Acta Virol 45:249

    PubMed  CAS  Google Scholar 

  64. Wang X, Zhou G (2003) Identification of a protein associated with circulative transmission of Barley yellow dwarf virus from cereal aphids, Schizaphis graminum and Sitobion avenae. Chin Sci Bull 48:2083–2087

    Article  CAS  Google Scholar 

  65. Wang X, Liu Y, Chen L, Zhao D, Wang X, Zhang Z (2013) Wheat resistome in response to barley yellow dwarf virus infection. Funct Integr Genomics 13(2):155–165

  66. Waziri H, El Gaffar MA, Allam E, El Din AG (2002) Coat protein sequence of an Egyptian BYDV-PAV isolate. In: Henry M, McNab A (eds) Barley yellow dwarf disease: recent advances and future strategies. CIMMYT, Mexico, DF, pp 97–99

  67. Xia Z, Cao R, Sun K, Zhang H (2012) The movement protein of barley yellow dwarf virus-GAV self-interacts and forms homodimers in vitro and in vivo. Arch Virol 157:1233–1239

    Article  PubMed  CAS  Google Scholar 

  68. Yoon J-Y, Choi S-K, Palukaitis P, Gray SM (2011) Agrobacterium-mediated infection of whole plants by yellow dwarf viruses. Virus Res 160:428–434

    Article  PubMed  CAS  Google Scholar 

  69. Zvereva AS, Pooggin MM (2012) Silencing and innate immunity in plant defense against viral and non-viral pathogens. Viruses 4:2578–2597

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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Ali, M., Hameed, S. & Tahir, M. Luteovirus: insights into pathogenicity. Arch Virol 159, 2853–2860 (2014). https://doi.org/10.1007/s00705-014-2172-6

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