Skip to main content
NCBI home page
The EMBO Journal logoLink to The EMBO Journal
. 1992 Feb;11(2):479–488. doi: 10.1002/j.1460-2075.1992.tb05078.x

Two proteins encoded by beet necrotic yellow vein virus RNA 3 influence symptom phenotype on leaves.

I Jupin 1, H Guilley 1, K E Richards 1, G Jonard 1
PMCID: PMC556478  PMID: 1537331

Abstract

RNA 3 of the beet necrotic yellow vein virus (BNYVV) quadripartite RNA genome is not essential for virus multiplication on leaves of Tetragonia expansa but has dramatic effects on symptom expression. Virus isolates containing RNA 3 produce bright yellow local lesions while isolates lacking RNA 3 produce much milder symptoms. Using directed mutagenesis of cDNA clones followed by in vitro synthesis of biologically active transcripts, a 25 kDa open reading frame (ORF) of RNA 3 was shown to be responsible for the yellow local lesion phenotype. In addition, two deletion mutants of RNA 3 were found to elicit the appearance of severe necrotic local lesions. Analysis of one of these mutants revealed that necrosis was due to the overexpression of a second short ORF, N, overlapping the 3'-terminal portion of the 25 kDa ORF. As shown by gene fusion studies, gene N is not detectably expressed from full-length RNA 3 but is translationally activated by deletion of upstream sequences. Introduction of gene N into the genome of the unrelated DNA virus, cauliflower mosaic virus, elicits a necrotic response instead of the typical mosaic symptoms, demonstrating that gene N can induce necrosis outside of the context of a BNYVV infection.

Full text

PDF
479

Images in this article

481Image
on p.481
482Image
on p.482
483Image
on p.483
484Image
on p.484

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baughman G. A., Jacobs J. D., Howell S. H. Cauliflower mosaic virus gene VI produces a symptomatic phenotype in transgenic tobacco plants. Proc Natl Acad Sci U S A. 1988 Feb;85(3):733–737. doi: 10.1073/pnas.85.3.733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berg J. M. Zinc fingers and other metal-binding domains. Elements for interactions between macromolecules. J Biol Chem. 1990 Apr 25;265(12):6513–6516. [PubMed] [Google Scholar]
  3. Bonneville J. M., Sanfaçon H., Fütterer J., Hohn T. Posttranscriptional trans-activation in cauliflower mosaic virus. Cell. 1989 Dec 22;59(6):1135–1143. doi: 10.1016/0092-8674(89)90769-1. [DOI] [PubMed] [Google Scholar]
  4. Bouzoubaa S., Niesbach-Klösgen U., Jupin I., Guilley H., Richards K., Jonard G. Shortened forms of beet necrotic yellow vein virus RNA-3 and -4: internal deletions and a subgenomic RNA. J Gen Virol. 1991 Feb;72(Pt 2):259–266. doi: 10.1099/0022-1317-72-2-259. [DOI] [PubMed] [Google Scholar]
  5. Culver J. N., Dawson W. O. Tobacco mosaic virus coat protein: an elicitor of the hypersensitive reaction but not required for the development of mosaic symptoms in Nicotiana sylvestris. Virology. 1989 Dec;173(2):755–758. doi: 10.1016/0042-6822(89)90592-8. [DOI] [PubMed] [Google Scholar]
  6. Daubert S., Routh G. Point mutations in cauliflower mosaic virus gene VI confer host-specific symptom changes. Mol Plant Microbe Interact. 1990 Sep-Oct;3(5):341–345. doi: 10.1094/mpmi-3-341. [DOI] [PubMed] [Google Scholar]
  7. Daubert S. Sequence determinants of symptoms in the genomes of plant viruses, viroids, and satellites. Mol Plant Microbe Interact. 1988 Nov-Dec;1(8):317–325. doi: 10.1094/mpmi-1-317. [DOI] [PubMed] [Google Scholar]
  8. Daubert S., Shepherd R. J., Gardner R. C. Insertional mutagenesis of the cauliflower mosaic virus genome. Gene. 1983 Nov;25(2-3):201–208. doi: 10.1016/0378-1119(83)90224-x. [DOI] [PubMed] [Google Scholar]
  9. De Zoeten G. A., Penswick J. R., Horisberger M. A., Ahl P., Schultze M., Hohn T. The expression, localization, and effect of a human interferon in plants. Virology. 1989 Sep;172(1):213–222. doi: 10.1016/0042-6822(89)90123-2. [DOI] [PubMed] [Google Scholar]
  10. Dixon L. K., Hohn T. Initiation of translation of the cauliflower mosaic virus genome from a polycistronic mRNA: evidence from deletion mutagenesis. EMBO J. 1984 Dec 1;3(12):2731–2736. doi: 10.1002/j.1460-2075.1984.tb02203.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Eisenberg D., Schwarz E., Komaromy M., Wall R. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J Mol Biol. 1984 Oct 15;179(1):125–142. doi: 10.1016/0022-2836(84)90309-7. [DOI] [PubMed] [Google Scholar]
  12. Franck A., Guilley H., Jonard G., Richards K., Hirth L. Nucleotide sequence of cauliflower mosaic virus DNA. Cell. 1980 Aug;21(1):285–294. doi: 10.1016/0092-8674(80)90136-1. [DOI] [PubMed] [Google Scholar]
  13. French R., Janda M., Ahlquist P. Bacterial gene inserted in an engineered RNA virus: efficient expression in monocotyledonous plant cells. Science. 1986 Mar 14;231(4743):1294–1297. doi: 10.1126/science.231.4743.1294. [DOI] [PubMed] [Google Scholar]
  14. Holt C. A., Hodgson R. A., Coker F. A., Beachy R. N., Nelson R. S. Characterization of the masked strain of tobacco mosaic virus: identification of the region responsible for symptom attenuation by analysis of an infectious cDNA clone. Mol Plant Microbe Interact. 1990 Nov-Dec;3(6):417–423. doi: 10.1094/mpmi-3-417. [DOI] [PubMed] [Google Scholar]
  15. Horvath C. M., Williams M. A., Lamb R. A. Eukaryotic coupled translation of tandem cistrons: identification of the influenza B virus BM2 polypeptide. EMBO J. 1990 Aug;9(8):2639–2647. doi: 10.1002/j.1460-2075.1990.tb07446.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ishikawa M., Meshi T., Watanabe Y., Okada Y. Replication of chimeric tobacco mosaic viruses which carry heterologous combinations of replicase genes and 3' noncoding regions. Virology. 1988 May;164(1):290–293. doi: 10.1016/0042-6822(88)90648-4. [DOI] [PubMed] [Google Scholar]
  17. Jaegle M., Devic M., Longstaff M., Baulcombe D. Cucumber mosaic virus satellite RNA (Y strain): analysis of sequences which affect yellow mosaic symptoms on tobacco. J Gen Virol. 1990 Sep;71(Pt 9):1905–1912. doi: 10.1099/0022-1317-71-9-1905. [DOI] [PubMed] [Google Scholar]
  18. Jupin I., Richards K., Jonard G., Guilley H., Pleij C. W. Mapping sequences required for productive replication of beet necrotic yellow vein virus RNA 3. Virology. 1990 Sep;178(1):273–280. doi: 10.1016/0042-6822(90)90403-e. [DOI] [PubMed] [Google Scholar]
  19. Karnell M. P., Morris H. L. Multiview videoendoscopic evaluation of velopharyngeal physiology in 15 normal speakers. Ann Otol Rhinol Laryngol. 1985 Jul-Aug;94(4 Pt 1):361–365. [PubMed] [Google Scholar]
  20. Kozak M. Effects of intercistronic length on the efficiency of reinitiation by eucaryotic ribosomes. Mol Cell Biol. 1987 Oct;7(10):3438–3445. doi: 10.1128/mcb.7.10.3438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  22. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  23. Lemaire O., Merdinoglu D., Valentin P., Putz C., Ziegler-Graff V., Guilley H., Jonard G., Richards K. Effect of beet necrotic yellow vein virus RNA composition on transmission by Polymyxa betae. Virology. 1988 Jan;162(1):232–235. doi: 10.1016/0042-6822(88)90412-6. [DOI] [PubMed] [Google Scholar]
  24. Liu C. C., Simonsen C. C., Levinson A. D. Initiation of translation at internal AUG codons in mammalian cells. Nature. 1984 May 3;309(5963):82–85. doi: 10.1038/309082a0. [DOI] [PubMed] [Google Scholar]
  25. Masuta C., Takanami Y. Determination of sequence and structural requirements for pathogenicity of a cucumber mosaic virus satellite RNA (Y-satRNA). Plant Cell. 1989 Dec;1(12):1165–1173. doi: 10.1105/tpc.1.12.1165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Niesbach-Klösgen U., Guilley H., Jonard G., Richards K. Immunodetection in vivo of beet necrotic yellow vein virus-encoded proteins. Virology. 1990 Sep;178(1):52–61. doi: 10.1016/0042-6822(90)90378-5. [DOI] [PubMed] [Google Scholar]
  28. Peabody D. S., Subramani S., Berg P. Effect of upstream reading frames on translation efficiency in simian virus 40 recombinants. Mol Cell Biol. 1986 Jul;6(7):2704–2711. doi: 10.1128/mcb.6.7.2704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Quillet L., Guilley H., Jonard G., Richards K. In vitro synthesis of biologically active beet necrotic yellow vein virus RNA. Virology. 1989 Sep;172(1):293–301. doi: 10.1016/0042-6822(89)90131-1. [DOI] [PubMed] [Google Scholar]
  30. Saito T., Yamanaka K., Watanabe Y., Takamatsu N., Meshi T., Okada Y. Mutational analysis of the coat protein gene of tobacco mosaic virus in relation to hypersensitive response in tobacco plants with the N' gene. Virology. 1989 Nov;173(1):11–20. doi: 10.1016/0042-6822(89)90217-1. [DOI] [PubMed] [Google Scholar]
  31. Sleat D. E., Palukaitis P. Site-directed mutagenesis of a plant viral satellite RNA changes its phenotype from ameliorative to necrogenic. Proc Natl Acad Sci U S A. 1990 Apr;87(8):2946–2950. doi: 10.1073/pnas.87.8.2946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Stratford R., Covey S. N. Segregation of cauliflower mosaic virus symptom genetic determinants. Virology. 1989 Oct;172(2):451–459. doi: 10.1016/0042-6822(89)90187-6. [DOI] [PubMed] [Google Scholar]
  33. Vieira J., Messing J. Production of single-stranded plasmid DNA. Methods Enzymol. 1987;153:3–11. doi: 10.1016/0076-6879(87)53044-0. [DOI] [PubMed] [Google Scholar]
  34. Wilbur W. J., Lipman D. J. Rapid similarity searches of nucleic acid and protein data banks. Proc Natl Acad Sci U S A. 1983 Feb;80(3):726–730. doi: 10.1073/pnas.80.3.726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Witmer L. A., Rosenthal K. L., Graham F. L., Friedman H. M., Yee A., Johnson D. C. Cytotoxic T lymphocytes specific for herpes simplex virus (HSV) studied using adenovirus vectors expressing HSV glycoproteins. J Gen Virol. 1990 Feb;71(Pt 2):387–396. doi: 10.1099/0022-1317-71-2-387. [DOI] [PubMed] [Google Scholar]
  36. Woolston C. J., Covey S. N., Penswick J. R., Davies J. W. Aphid transmission and a polypeptide are specified by a defined region of the cauliflower mosaic virus genome. Gene. 1983 Jul;23(1):15–23. doi: 10.1016/0378-1119(83)90212-3. [DOI] [PubMed] [Google Scholar]
  37. Zhang H., Scholl R., Browse J., Somerville C. Double stranded DNA sequencing as a choice for DNA sequencing. Nucleic Acids Res. 1988 Feb 11;16(3):1220–1220. doi: 10.1093/nar/16.3.1220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Zoller M. J., Smith M. Oligonucleotide-directed mutagenesis: a simple method using two oligonucleotide primers and a single-stranded DNA template. DNA. 1984 Dec;3(6):479–488. doi: 10.1089/dna.1.1984.3.479. [DOI] [PubMed] [Google Scholar]
  39. van Loon L. C. Disease induction by plant viruses. Adv Virus Res. 1987;33:205–255. doi: 10.1016/s0065-3527(08)60319-x. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES