1887

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Volume 89, Issue 8

Small deletions in the potato leafroll virus readthrough protein affect particle morphology, aphid transmission, virus movement and accumulation Free

Abstract

Potato leafroll virus (PLRV) capsid comprises 180 coat protein (CP) subunits, with some percentage containing a readthrough domain (RTD) extension located on the particle's surface. The RTD N terminus is highly conserved in luteovirids and this study sought to identify biologically active sites within this region of the PLRV RTD. Fourteen three-amino-acid-deletion mutants were generated from a cloned infectious PLRV cDNA and delivered to plants by inoculations. All mutant viruses accumulated locally in infiltrated tissues and expressed the readthrough protein (RTP) containing the CP and RTD sequences in plant tissues; however, when purified, only three mutant viruses incorporated the RTP into the virion. None of the mutant viruses were aphid transmissible, but the viruses persisted in aphids for a period sufficient to allow for virus transmission. Several mutant viruses were examined further for systemic infection in four host species. All mutant viruses, regardless of RTP incorporation, moved systemically in each host, although they accumulated at different rates in systemically infected tissues. The biological properties of the RTP are sensitive to modifications in both the RTD conserved and variable regions.

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2008-08-01
2024-04-26
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References

  1. Alvarez J. M., Srinivasan R. 2005; Evaluation of hairy nightshade as an inoculum source for aphid-mediated transmission of potato leafroll virus. J Econ Entomol 98:1101–1108 [CrossRef]
     [Google Scholar]
  2. Bahner I., Lamb J., Mayo M., Hay R. 1990; Expression of the genome of potato leafroll virus: readthrough of the coat protein termination codon in vivo . J Gen Virol 71:2251–2256 [CrossRef]
     [Google Scholar]
  3. Baumann P., Baumann L., Lai C., Rouhbakhsh D., Moran N. A., Clark M. A. 1995; Genetics, physiology and evolutionary relationships of the genus Buchnera : intracellular symbionts of aphids. Annu Rev Microbiol 49:55–94 [CrossRef]
     [Google Scholar]
  4. Brault V., van den Heuvel J. F. J. M., Verbeek M., Ziegler-Graff V., Reutenauer A., Herrbach E., Garaud J. C., Guilley H., Richards K., Jonard G. 1995; Aphid transmission of beet western yellows luteovirus requires the minor capsid read-through protein P74. EMBO J 14:650–659
     [Google Scholar]
  5. Brault V., Mutterer J., Scheidecker D., Simonis M. T., Herrbach E., Richards K., Ziegler-Graff V. 2000; Effects of point mutations in the readthrough domain of the beet western yellows virus minor capsid protein on virus accumulation in planta and on transmission by aphids. J Virol 74:1140–1148 [CrossRef]
     [Google Scholar]
  6. Brault V., Bergdoll M., Mutterer J., Prasad V., Pfeffer S., Erdinger M., Richards K. E., Ziegler-Graff V. 2003; Effects of point mutations in the major capsid protein of beet western yellows virus on capsid formation, virus accumulation, and aphid transmission. J Virol 77:3247–3256 [CrossRef]
     [Google Scholar]
  7. Brault V., Perigon S., Reinbold C., Erdinger M., Scheidecker D., Herrbach E., Richards K., Ziegler-Graff V. 2005; The polerovirus minor capsid protein determines vector specificity and intestinal tropism in the aphid. J Virol 79:9685–9693 [CrossRef]
     [Google Scholar]
  8. Brault V., Herrbach E., Reinbold C. 2007; Electron microscopy studies on luteovirid transmission by aphids. Micron 38:302–312 [CrossRef]
     [Google Scholar]
  9. Brown C. M., Dinesh-Kumar S. P., Miller W. A. 1996; Local and distant sequences are required for efficient readthrough of the barley yellow dwarf virus PAV coat protein gene stop codon. J Virol 70:5884–5892
     [Google Scholar]
  10. Bruyere A., Brault V., Ziegler-Graff V., Simonis M. T., van den Heuvel J. F. J. M., Richards K., Guilley H., Jonard G., Herrbach E. 1997; Effects of mutations in the beet western yellows virus readthrough protein on its expression and packaging and on virus accumulation, symptoms, and aphid transmission. Virology 230:323–334 [CrossRef]
     [Google Scholar]
  11. Chay C. A., Gunasinge U. B., Dinesh-Kumar S. P., Miller W. A., Gray S. M. 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 [CrossRef]
     [Google Scholar]
  12. Filichkin S. A., Lister R. M., Mcgrath P. F., Young M. J. 1994; In vivo expression and mutational analysis of the barley yellow dwarf virus readthrough gene. Virology 205:290–299 [CrossRef]
     [Google Scholar]
  13. Fukatsu T., Ishikawa H. 1992; Synthesis and localization of symbionin an aphid endosymbiont protein. Insect Biochem Mol Biol 22:167–174 [CrossRef]
     [Google Scholar]
  14. Garret A., Kerlan C., Thomas D. 1993; The intestine is a site of passage for potato leafroll virus from the gut lumen into the haemocoel in the aphid vector, Myzus persicae Sulz. Arch Virol 131:377–392 [CrossRef]
     [Google Scholar]
  15. Gildow F. E., Reavy B., Mayo M. A., Duncan G. H., Woodford J. A. T., Lamb J. W., Hay R. T. 2000; Aphid acquisition and cellular transport of potato leafroll virus-like particles lacking P5 readthrough protein. Phytopathology 90:1153–1161 [CrossRef]
     [Google Scholar]
  16. Gray S. M., Power A. G., Smith D. M., Seaman A. J., Altman N. S. 1991; Aphid transmission of barley yellow dwarf virus: acquisition access periods and virus concentration requirements. Phytopathology 81:539–545 [CrossRef]
     [Google Scholar]
  17. Guilley H., Wipf-Scheibel C., Richards K., Lecoq H., Jonard G. 1994; Nucleotide sequence of cucurbit aphid-borne yellows luteovirus. Virology 202:1012–1017 [CrossRef]
     [Google Scholar]
  18. Hammond J., Lister R. M., Foster J. E. 1983; Purification, identity and some properties of an isolate of barley yellow dwarf virus from Indiana. J Gen Virol 64:667–676 [CrossRef]
     [Google Scholar]
  19. Harrison B. D. 1999; Steps in the development of luteovirology. In The Luteoviridae pp 1–14Edited by Smith H. G., Barker H. Wallingford, UK: CABI Publishing;
     [Google Scholar]
  20. Hogenhout S. A., van der Wilk F., Verbeek M., Goldbach R. W., van den Heuvel J. F. J. M. 2000; Identifying the determinants in the equatorial domain of Buchnera GroEL implicated in binding Potato leafroll virus . J Virol 74:4541–4548 [CrossRef]
     [Google Scholar]
  21. Jolly C. A., Mayo M. A. 1994; Changes in the amino-acid-sequence of the coat protein readthrough domain of potato leafroll luteovirus affect the formation of an epitope and aphid transmission. Virology 201:182–185 [CrossRef]
     [Google Scholar]
  22. Kaplan I. B., Lee L., Ripoll D. R., Palukaitis P., Gildow F., Gray S. M. 2007; Point mutations in the potato leafroll virus major capsid protein alter virion stability and aphid transmission. J Gen Virol 88:1821–1830 [CrossRef]
     [Google Scholar]
  23. Lee L., Palukaitis P., Gray S. M. 2002; Host-dependent requirement for the Potato leafroll virus 17-kDa protein in virus movement. Mol Plant Microbe Interact 15:1086–1094 [CrossRef]
     [Google Scholar]
  24. Lee L., Kaplan I. B., Ripoll D. R., Liang D., Palukaitis P., Gray S. M. 2005; A surface loop of the potato leafroll virus coat protein is involved in virion assembly, systemic movement, and aphid transmission. J Virol 79:1207–1214 [CrossRef]
     [Google Scholar]
  25. Liang D., Gray S. M., Kaplan I., Palukaitis P. 2004; Site-directed mutagenesis and generation of chimeric viruses by homologous recombinations in yeast to facilitate analysis of plant–virus interactions. Mol Plant Microbe Interact 17:571–576 [CrossRef]
     [Google Scholar]
  26. Mayo M., Miller W. A. 1999; The structure and expression of luteovirus genomes. In The Luteoviridae pp 23–42Edited by Smith H. G., Barker H. Wallingford, UK: CABI Publishing;
     [Google Scholar]
  27. Mueller W. C., Rochow W. F. 1961; An aphid-injection method for the transmission of barley yellow dwarf virus. Virology 14:253–258 [CrossRef]
     [Google Scholar]
  28. Mutterer J. D., Stussi-Garaud C., Michler P., Richards K. E., Jonard G., Ziegler-Graff V. 1999; Role of the beet western yellows virus readthrough protein in virus movement in Nicotiana clevelandii . J Gen Virol 80:2771–2778
     [Google Scholar]
  29. Reinbold C., Gildow F. E., Herrbach E., Ziegler-Graff V., Goncalves M. C., van den Heuvel J. F. J. M., Brault V. 2001; Studies on the role of the minor capsid protein in transport of beet western yellows virus through Myzus persicae . J Gen Virol 82:1995–2007
     [Google Scholar]
  30. Seddas P., Boissinot S. 2006; Glycosylation of beet western yellows virus proteins is implicated in the aphid transmission of the virus. Arch Virol 151:967–984 [CrossRef]
     [Google Scholar]
  31. Torrance L. 1992; Analysis of epitopes on potato leafroll virus capsid protein. Virology 191:485–489 [CrossRef]
     [Google Scholar]
  32. van den Heuvel J. F., Bruyere A., Hogenhout A., Ziegler-Graff V., Brault V., Verbeek M., van der Wilk F., Richards K. 1997; The N-terminal region of the luteovirus readthrough domain determines virus binding to Buchnera GroEL and is essential for virus persistence in the aphid. J Virol 71:7258–7265
     [Google Scholar]
  33. Wang J. Y., Chay C., Gildow F. E., Gray S. M. 1995; Readthrough protein associated with virions of barley yellow dwarf luteovirus and its potential role in regulating the efficiency of aphid transmission. Virology 206:954–962 [CrossRef]
     [Google Scholar]
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Small deletions in the potato leafroll virus readthrough protein affect particle morphology, aphid transmission, virus movement and accumulation
J. Gen. Virol. 89, 2037 (2008); https://doi.org/10.1099/vir.0.83625-0
/content/journal/jgv/10.1099/vir.0.83625-0
/content/journal/jgv/10.1099/vir.0.83625-0
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