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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1996 Jul 23;93(15):7470–7474. doi: 10.1073/pnas.93.15.7470

An interspecies hybrid RNA virus is significantly more virulent than either parental virus.

S W Ding 1, B J Shi 1, W X Li 1, R H Symons 1
PMCID: PMC38768  PMID: 8755497

Abstract

Cucumber mosaic cucumovirus (CMV) infects a very wide range of plant species (>1000 species). We recently demonstrated that a previously undescribed gene (2b) encoded by RNA 2 of the tripartite RNA genome of CMV is required for systemic virus spread and disease induction in its hosts. Herein we report that when this CMV gene is replaced by its homologue from tomato aspermy cucumovirus (TAV), the resultant hybrid virus is significantly more virulent, induces earlier onset of systemic symptoms, and accumulates to a higher level in seven host species from three families than either of the parents. Our results indicate that CMV and the TAV 2b protein interact synergistically despite the fact that no synergism occurs in double infections with the two parental viruses. To our knowledge, this is the first example of an interspecific hybrid made from plant or animal RNA viruses that is more efficient in systemic infection of a number of hosts than the naturally occurring parents. As CMV and the hybrid virus accumulated to a similar level in the infected tobacco protoplasts, the observed synergistic responses most likely resulted from an increased efficacy of the hybrid virus in systemic spread in host plants provided by the TAV 2b protein. The relevance of our finding to the application of pathogen-derived resistance is discussed.

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Selected References

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  1. Ahlquist P., French R., Janda M., Loesch-Fries L. S. Multicomponent RNA plant virus infection derived from cloned viral cDNA. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7066–7070. doi: 10.1073/pnas.81.22.7066. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aryan A. P., An G., Okita T. W. Structural and functional analysis of promoter from gliadin, an endosperm-specific storage protein gene of Triticum aestivum L. Mol Gen Genet. 1991 Jan;225(1):65–71. doi: 10.1007/BF00282643. [DOI] [PubMed] [Google Scholar]
  3. Banerjee N., Wang J. Y., Zaitlin M. A single nucleotide change in the coat protein gene of tobacco mosaic virus is involved in the induction of severe chlorosis. Virology. 1995 Feb 20;207(1):234–239. doi: 10.1006/viro.1995.1070. [DOI] [PubMed] [Google Scholar]
  4. Burgyán J., Tavazza M., Dalmay T., Lucioli A., Balázs E. Consequences of gene transfer between distantly related tombusviruses. Gene. 1993 Jul 30;129(2):191–196. doi: 10.1016/0378-1119(93)90268-8. [DOI] [PubMed] [Google Scholar]
  5. Cooper B., Lapidot M., Heick J. A., Dodds J. A., Beachy R. N. A defective movement protein of TMV in transgenic plants confers resistance to multiple viruses whereas the functional analog increases susceptibility. Virology. 1995 Jan 10;206(1):307–313. doi: 10.1016/s0042-6822(95)80046-8. [DOI] [PubMed] [Google Scholar]
  6. Daugherty B. L., DeMartino J. A., Law M. F., Kawka D. W., Singer I. I., Mark G. E. Polymerase chain reaction facilitates the cloning, CDR-grafting, and rapid expression of a murine monoclonal antibody directed against the CD18 component of leukocyte integrins. Nucleic Acids Res. 1991 May 11;19(9):2471–2476. doi: 10.1093/nar/19.9.2471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. De Jong W., Ahlquist P. A hybrid plant RNA virus made by transferring the noncapsid movement protein from a rod-shaped to an icosahedral virus is competent for systemic infection. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6808–6812. doi: 10.1073/pnas.89.15.6808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ding S. W., Anderson B. J., Haase H. R., Symons R. H. New overlapping gene encoded by the cucumber mosaic virus genome. Virology. 1994 Feb;198(2):593–601. doi: 10.1006/viro.1994.1071. [DOI] [PubMed] [Google Scholar]
  9. Ding S. W., Li W. X., Symons R. H. A novel naturally occurring hybrid gene encoded by a plant RNA virus facilitates long distance virus movement. EMBO J. 1995 Dec 1;14(23):5762–5772. doi: 10.1002/j.1460-2075.1995.tb00265.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ding S. W., Rathjen J. P., Li W. X., Swanson R., Healy H., Symons R. H. Efficient infection from cDNA clones of cucumber mosaic cucumovirus RNAs in a new plasmid vector. J Gen Virol. 1995 Feb;76(Pt 2):459–464. doi: 10.1099/0022-1317-76-2-459. [DOI] [PubMed] [Google Scholar]
  11. Hilf M. E., Dawson W. O. The tobamovirus capsid protein functions as a host-specific determinant of long-distance movement. Virology. 1993 Mar;193(1):106–114. doi: 10.1006/viro.1993.1107. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. KASSANIS B. INTERACTIONS OF VIRUSES IN PLANTS. Adv Virus Res. 1963;10:219–255. doi: 10.1016/s0065-3527(08)60700-9. [DOI] [PubMed] [Google Scholar]
  14. Lopez S., Yao J. S., Kuhn R. J., Strauss E. G., Strauss J. H. Nucleocapsid-glycoprotein interactions required for assembly of alphaviruses. J Virol. 1994 Mar;68(3):1316–1323. doi: 10.1128/jvi.68.3.1316-1323.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mise K., Allison R. F., Janda M., Ahlquist P. Bromovirus movement protein genes play a crucial role in host specificity. J Virol. 1993 May;67(5):2815–2823. doi: 10.1128/jvi.67.5.2815-2823.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Moriones E., Roossinck M. J., García-Arenal F. Nucleotide sequence of tomato aspermy virus RNA 2. J Gen Virol. 1991 Apr;72(Pt 4):779–783. doi: 10.1099/0022-1317-72-4-779. [DOI] [PubMed] [Google Scholar]
  17. Neeleman L., van der Kuyl A. C., Bol J. F. Role of alfalfa mosaic virus coat protein gene in symptom formation. Virology. 1991 Apr;181(2):687–693. doi: 10.1016/0042-6822(91)90902-n. [DOI] [PubMed] [Google Scholar]
  18. Peng D., Koetzner C. A., McMahon T., Zhu Y., Masters P. S. Construction of murine coronavirus mutants containing interspecies chimeric nucleocapsid proteins. J Virol. 1995 Sep;69(9):5475–5484. doi: 10.1128/jvi.69.9.5475-5484.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Petty I. T., Edwards M. C., Jackson A. O. Systemic movement of an RNA plant virus determined by a point substitution in a 5' leader sequence. Proc Natl Acad Sci U S A. 1990 Nov;87(22):8894–8897. doi: 10.1073/pnas.87.22.8894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pletnev A. G., Bray M., Huggins J., Lai C. J. Construction and characterization of chimeric tick-borne encephalitis/dengue type 4 viruses. Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10532–10536. doi: 10.1073/pnas.89.21.10532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rao A. L., Grantham G. L. A spontaneous mutation in the movement protein gene of brome mosaic virus modulates symptom phenotype in Nicotiana benthamiana. J Virol. 1995 Apr;69(4):2689–2691. doi: 10.1128/jvi.69.4.2689-2691.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rao A. L., Grantham G. L. A spontaneous mutation in the movement protein gene of brome mosaic virus modulates symptom phenotype in Nicotiana benthamiana. J Virol. 1995 Apr;69(4):2689–2691. doi: 10.1128/jvi.69.4.2689-2691.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rodríguez-Cerezo E., Klein P. G., Shaw J. G. A determinant of disease symptom severity is located in the 3'-terminal noncoding region of the RNA of a plant virus. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9863–9867. doi: 10.1073/pnas.88.21.9863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Shintaku M. H., Zhang L., Palukaitis P. A single amino acid substitution in the coat protein of cucumber mosaic virus induces chlorosis in tobacco. Plant Cell. 1992 Jul;4(7):751–757. doi: 10.1105/tpc.4.7.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Traynor P., Young B. M., Ahlquist P. Deletion analysis of brome mosaic virus 2a protein: effects on RNA replication and systemic spread. J Virol. 1991 Jun;65(6):2807–2815. doi: 10.1128/jvi.65.6.2807-2815.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tsai C. H., Dreher T. W. Increased viral yield and symptom severity result from a single amino acid substitution in the turnip yellow mosaic virus movement protein. Mol Plant Microbe Interact. 1993 May-Jun;6(3):268–273. doi: 10.1094/mpmi-6-268. [DOI] [PubMed] [Google Scholar]
  27. Vance V. B., Berger P. H., Carrington J. C., Hunt A. G., Shi X. M. 5' proximal potyviral sequences mediate potato virus X/potyviral synergistic disease in transgenic tobacco. Virology. 1995 Jan 10;206(1):583–590. doi: 10.1016/s0042-6822(95)80075-1. [DOI] [PubMed] [Google Scholar]
  28. Weiland J. J., Edwards M. C. Evidence that the alpha a gene of barley stripe mosaic virus encodes determinants of pathogenicity to oat (Avena sativa). Virology. 1994 May 15;201(1):116–126. doi: 10.1006/viro.1994.1271. [DOI] [PubMed] [Google Scholar]
  29. Wilson T. M. Strategies to protect crop plants against viruses: pathogen-derived resistance blossoms. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3134–3141. doi: 10.1073/pnas.90.8.3134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. van der Vossen E. A., Neeleman L., Bol J. F. Role of the 5' leader sequence of alfalfa mosaic virus RNA 3 in replication and translation of the viral RNA. Nucleic Acids Res. 1993 Mar 25;21(6):1361–1367. doi: 10.1093/nar/21.6.1361. [DOI] [PMC free article] [PubMed] [Google Scholar]

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