Archives of Virology

, Volume 159, Issue 11, pp 2853–2860 | Cite as

Luteovirus: insights into pathogenicity

  • Muhammad Ali
  • Shahid Hameed
  • Muhammad TahirEmail author
Brief Review


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.


Coat Protein Movement Protein Potato Leaf Roll Virus Aphid Transmission Subgenomic RNAs 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Ahlquist P (2006) Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nat Rev Microbiol 4:371–382PubMedCrossRefGoogle Scholar
  2. 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 57:383–385PubMedGoogle Scholar
  3. 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 253:139–144PubMedCrossRefGoogle Scholar
  4. 4.
    Andret-Link P, Fuchs M (2005) Transmission specificity of plant viruses by vectors. J Plant Pathol 87:153–165Google Scholar
  5. 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 99:11133–11138PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Baulcombe D (2002) Viral suppression of systemic silencing. Trends Microbiol 10:306–308PubMedCrossRefGoogle Scholar
  7. 7.
    Brown J (2000) Molecular markers for the identification and global tracking of whitefly vector—Begomovirus complexes. Virus Res 71:233–260PubMedCrossRefGoogle Scholar
  8. 8.
    Callaway A, Giesman-Cookmeyer D, Gillock E, Sit T, Lommel S (2001) The multifunctional capsid proteins of plant RNA viruses. Annu Rev Phytopathol 39:419–460PubMedCrossRefGoogle Scholar
  9. 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 132:449–462PubMedCrossRefPubMedCentralGoogle Scholar
  10. 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 219:57–65PubMedCrossRefGoogle Scholar
  11. 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) 39:534–543Google Scholar
  12. 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 106:789–791Google Scholar
  13. 13.
    D’Arcy CJ, Burnett PA (1995) Barley yellow dwarf virus: 40 years of progress. APS Press, St Paul, MNGoogle Scholar
  14. 14.
    den Boon JA, Diaz A, Ahlquist P (2010) Cytoplasmic viral replication complexes. Cell Host Microbe 8:77–85CrossRefGoogle Scholar
  15. 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 6:444–452CrossRefGoogle Scholar
  16. 16.
    Dinesh-Kumar S, Miller WA (1993) Control of start codon choice on a plant viral RNA encoding overlapping genes. Plant Cell Online 5:679–692CrossRefGoogle Scholar
  17. 17.
    Dolja VV, Koonin EV (1991) Phylogeny of capsid proteins of small icosahedral RNA plant viruses. J Gen Virol 72:1481–1486PubMedCrossRefGoogle Scholar
  18. 18.
    Domier L (2008) Barley yellow dwarf virus. In: Mahy BWJ, Regenmortel MHV (eds) Encyclopedia of virology. Elsevier Ltd, Oxford, pp 279–286Google Scholar
  19. 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 100–107Google Scholar
  20. 20.
    Dreher TW, Miller WA (2006) Translational control in positive strand RNA plant viruses. Virology 344:185–197PubMedCrossRefPubMedCentralGoogle Scholar
  21. 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 267:318–325PubMedCrossRefGoogle Scholar
  22. 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 125–134Google Scholar
  23. 23.
    Fan Q, Treder K, Miller WA (2012) Untranslated regions of diverse plant viral RNAs vary greatly in translation enhancement efficiency. BMC Biotechnol 12:22PubMedCrossRefGoogle Scholar
  24. 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 ElsevierGoogle Scholar
  25. 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 148:333–342CrossRefGoogle Scholar
  26. 26.
    Gildow FE (1987) Virus—membrane interactions involved in circulative transmission of luteoviruses by aphids. Current topics in vector research. Springer, Berlin, pp 93–120Google Scholar
  27. 27.
    Gill C, Chong J (1975) Development of the infection in oat leaves inoculated with barley yellow dwarf virus. Virology 66:440–453PubMedCrossRefGoogle Scholar
  28. 28.
    Gill C, Chong J (1979) Cytopathological evidence for the division of barley yellow dwarf virus isolates into two subgroups. Virology 95:59–69PubMedCrossRefGoogle Scholar
  29. 29.
    Gray S, Gildow FE (2003) Luteovirus-aphid interactions. Annu Review Phytopathol 41:539–566CrossRefGoogle Scholar
  30. 30.
    Gray SM, Banerjee N (1999) Mechanisms of arthropod transmission of plant and animal viruses. Microbiol Mol Biol Rev 63:128–148PubMedPubMedCentralGoogle Scholar
  31. 31.
    Guo L, Allen EM, Miller WA (2001) Base-pairing between untranslated regions facilitates translation of uncapped, nonpolyadenylated viral RNA. Mol Cell 7:1103–1109PubMedCrossRefGoogle Scholar
  32. 32.
    Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
  33. 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 101:6291–6296PubMedCrossRefPubMedCentralGoogle Scholar
  34. 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 88:1013–1019PubMedCrossRefGoogle Scholar
  35. 35.
    Koev G, Miller WA (2000) A positive-strand RNA virus with three very different subgenomic RNA promoters. J Virol 74:5988–5996PubMedCrossRefPubMedCentralGoogle Scholar
  36. 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 292:114–126PubMedCrossRefGoogle Scholar
  37. 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 15:1086–1094PubMedCrossRefGoogle Scholar
  38. 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 152:1365–1373PubMedCrossRefGoogle Scholar
  39. 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 93:1825–1830PubMedCrossRefGoogle Scholar
  40. 40.
    Lucas WJ, Lee J-Y (2004) Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 5:712–726PubMedCrossRefGoogle Scholar
  41. 41.
    Lucas WJ (2006) Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344:169–184PubMedCrossRefGoogle Scholar
  42. 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 15–22Google Scholar
  43. 43.
    Miller WA, Rasochová L (1997) Barley yellow dwarf viruses. Annu Rev Phytopathol 35:167–190PubMedCrossRefGoogle Scholar
  44. 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 1–8Google Scholar
  45. 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 35:1629–1633PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Miller WA, Liu S, Beckett R (2002) Barley yellow dwarf virus: luteoviridae or Tombusviridae? Mol Plant Pathol 3:177–183PubMedCrossRefGoogle Scholar
  47. 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 88:1031–1039PubMedCrossRefGoogle Scholar
  48. 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 97:147–172PubMedCrossRefGoogle Scholar
  49. 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 310:987–999PubMedCrossRefGoogle Scholar
  50. 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 83:5419–5429PubMedCrossRefPubMedCentralGoogle Scholar
  51. 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 9:168–174PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    Pogany J, Fabian MR, White KA, Nagy PD (2003) A replication silencer element in a plus-strand RNA virus. EMBO J 22:5602–5611PubMedCrossRefPubMedCentralGoogle Scholar
  53. 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 259–289Google Scholar
  54. 54.
    Reavy B, Mayo M (2002) Persistent transmission of luteoviruses by aphids. Adv Bot Res 36:21–46CrossRefGoogle Scholar
  55. 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 70:8908–8916PubMedPubMedCentralGoogle Scholar
  56. 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 16:4049–4059PubMedCrossRefPubMedCentralGoogle Scholar
  57. 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 327:196–205PubMedCrossRefGoogle Scholar
  58. 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 72:2035PubMedCrossRefGoogle Scholar
  59. 59.
    Wang D, Maule AJ (1995) Inhibition of host gene expression associated with plant virus replication. Science 267:229–231PubMedCrossRefGoogle Scholar
  60. 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 143:1005–1013PubMedCrossRefGoogle Scholar
  61. 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 16:4107–4116PubMedCrossRefPubMedCentralGoogle Scholar
  62. 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 5:728–738PubMedCrossRefPubMedCentralGoogle Scholar
  63. 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 45:249PubMedGoogle Scholar
  64. 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 48:2083–2087CrossRefGoogle Scholar
  65. 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):155–165Google Scholar
  66. 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 97–99Google Scholar
  67. 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 157:1233–1239PubMedCrossRefGoogle Scholar
  68. 68.
    Yoon J-Y, Choi S-K, Palukaitis P, Gray SM (2011) Agrobacterium-mediated infection of whole plants by yellow dwarf viruses. Virus Res 160:428–434PubMedCrossRefGoogle Scholar
  69. 69.
    Zvereva AS, Pooggin MM (2012) Silencing and innate immunity in plant defense against viral and non-viral pathogens. Viruses 4:2578–2597PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  1. 1.Atta-ur-Rahman School of Applied Biosciences (ASAB)National University of Sciences and Technology (NUST)IslamabadPakistan
  2. 2.Crop Disease Research Institute (CDRI), National Agricultural Research Center (NARC)IslamabadPakistan

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