1887

Abstract

The tobamovirus TMV-Cg induces an HR-like response in cv. Xanthi nn sensitive plants lacking the resistance genes. This response has been characterized by the appearance of necrotic lesions in the inoculated leaf and viral systemic spread, although the defence pathways are activated in the plant. A previous study demonstrated that the coat protein (CP) of TMV-Cg (CPCg) was the elicitor of this HR-like response. We examined the influence of four specific amino acid substitutions on the structure of CPCg, as well as on the development of the host response. To gain insights into the structural implications of these substitutions, a set of molecular dynamic experiments was performed using comparative models of wild-type and mutant CPCg as well as the CP of the U1 strain of TMV (CPU1), which is not recognized by the plants. A P21L mutation produces severe changes in the three-dimensional structure of CPCg and is more unstable when this subunit is laterally associated . This result may explain the observed incapacity of this mutant to assemble virions. Two other CPCg mutations (R46G and S54K) overcome recognition by the plant and do not induce an HR-like response. A double CPCg mutant P21L-S54K recovered its capacity to form virions and to induce an HR-like response. Our results suggest that the structural integrity of the CP proteins is important for triggering the HR-like response.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.83355-0
2008-03-01
2020-11-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/89/3/809.html?itemId=/content/journal/jgv/10.1099/vir.0.83355-0&mimeType=html&fmt=ahah

References

  1. Arce-Johnson P., Medina C., Padgett H. S., Huanca W., Espinoza C. 2003; Analysis of local and systemic spread of the crucifer-infecting TMV-Cg virus in tobacco and several Arabidopsis thaliana ecotypes. Funct Plant Biol 30:401–408 [CrossRef]
    [Google Scholar]
  2. Asseling A., Zaitlin M. 1998; Characterization of a second protein associated with virions of tobacco mosaic virus. Virology 91:173–181
    [Google Scholar]
  3. Asurmendi S., Berg R. H., Koo J. C., Beachy R. N. 2004; Coat protein regulates formation of replication complexes during tobacco mosaic virus infection. Proc Natl Acad Sci U S A 101:1415–1420 [CrossRef]
    [Google Scholar]
  4. Asurmendi S., Berg R. H., Smith T. J., Bendahmane M., Beachy R. N. 2007; Aggregation of TMV CP plays a role in CP functions and in coat-protein-mediated resistance. Virology 366:98–106 [CrossRef]
    [Google Scholar]
  5. Bendahmane M., Fitchen J., Zhang G., Beachy R. N. 1997; Studies of coat protein-mediated resistance to tobacco mosaic tobamovirus: correlation between assembly of mutant coat proteins and resistance. J Virol 71:7942–7950
    [Google Scholar]
  6. Bendahmane M., Chen I., Asurmendi S., Bazzini A. A., Szecsi J., Beachy R. N. 2007; Coat protein-mediated resistance to TMV infection of Nicotiana tabacum involves multiple modes of interference by coat protein. Virology 366:107–116 [CrossRef]
    [Google Scholar]
  7. Berendsen H. J. C., Grigera J. R., Straatsma T. P. 1987; The missing term in effective pair potentials. J Phys Chem 91:6269–6271 [CrossRef]
    [Google Scholar]
  8. Bhyravbhatla B., Watowich S. J., Caspar D. L. 1998; TMV coat protein refined atomic model of the four-layer aggregate of the tobacco mosaic virus coat protein at 2.4 Å resolution. Biophys J 74:604–615 [CrossRef]
    [Google Scholar]
  9. Caspar D. L., Namba K. 1990; Switching in the self-assembly of tobacco mosaic virus. Adv Biophys 26:157–185 [CrossRef]
    [Google Scholar]
  10. Culver J. N. 2002; Tobacco mosaic virus assembly and disassembly: determinants in pathogenicity and resistance. Annu Rev Phytopathol 40:287–308 [CrossRef]
    [Google Scholar]
  11. Culver J. N., Dawson W. O. 1989; Tobacco mosaic virus elicitor coat protein: an elicitor of the hypersensitive response but not required for the development of mosaic symptoms in Nicotiana sylvestris . Virology 173:755–758 [CrossRef]
    [Google Scholar]
  12. Culver J. N., Stubbs G., Dawson W. O. 1994; Structure-function relationship between tobacco mosaic virus coat protein and hypersensitivity in Nicotiana sylvestris . J Mol Biol 242:130–138 [CrossRef]
    [Google Scholar]
  13. Dempsey D. A., Klessig D. F. 1994; Salicylic acid, active oxygen species and systemic acquired resistance in plants. Trends Cell Biol 4:334–338 [CrossRef]
    [Google Scholar]
  14. Deom C. M., He X. Z., Beachy R. N., Weissinger A. K. 1994; Influence of heterologous tobamovirus coat protein and chimeric movement protein genes on cell-to-cell and long-distance movement. Virology 205:198–209 [CrossRef]
    [Google Scholar]
  15. Ehrenfeld N., Canon P., Stange C., Medina C., Arce-Johnson P. 2005; Tobamovirus coat protein CPCg induces an HR-like response in sensitive tobacco plants. Mol Cells 19:418–427
    [Google Scholar]
  16. Eisenberg D., Luthy R., Bowie J. U. 1997; verify3d: assessment of protein models with three-dimensional profiles. Methods Enzymol 277:396–404
    [Google Scholar]
  17. Flor H. H. 1991; Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296
    [Google Scholar]
  18. Gilardi P., García-Luque L., Serra M. T. 2004; The coat protein of tobamovirus acts as elicitor of both L2 and L4 gene-mediated resistance in Capsicum . J Gen Virol 85:2077–2085 [CrossRef]
    [Google Scholar]
  19. Hammond-Kosack K. E., Jones J. D. G. 1997; Plant disease resistance genes. Annu Rev Plant Physiol Plant Mol Biol 48:575–607 [CrossRef]
    [Google Scholar]
  20. Kang B. C., Yeam I., Jahm M. M. 2005; Genetics of plant virus resistance. Annu Rev Phytopathol 43:581–621 [CrossRef]
    [Google Scholar]
  21. Lanfermeijer F. C., Jiang G., Ferwerda M. A., Dijkhuis J., de Haan P., Yang R., Hille J. 2004; The durable resistance gene Tm-22 from tomato confers resistance against ToMV in tobacco and preserves its viral specificity. Plant Sci 167:687–692 [CrossRef]
    [Google Scholar]
  22. Laskowski R., MacArthur M., Moss D., Thornton J. 1993; procheck: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283–291 [CrossRef]
    [Google Scholar]
  23. Meyers B. C., Kozik A., Griego A., Kuang H., Michelmore R. W. 2003; Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834 [CrossRef]
    [Google Scholar]
  24. Namba K., Stubbs G. 1986; Structure of tobacco mosaic virus at 3.6 Å resolution: implications for assembly. Science 231:1401–1406 [CrossRef]
    [Google Scholar]
  25. Nimchuk Z., Eulgen T., Holt B. F., Dangl J. L. 2003; Recognition and response in the plant immune system. Annu Rev Genet 37:579–609 [CrossRef]
    [Google Scholar]
  26. Nürnberger T., Brunner F., Kemmerling B., Piater L. 2004; Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266 [CrossRef]
    [Google Scholar]
  27. Padgett H. S., Beachy R. N. 1993; Analysis of a tobacco mosaic virus strain capable of overcoming N gene-mediated resistance. Plant Cell 5:577–586 [CrossRef]
    [Google Scholar]
  28. Saito T., Yamanaka K., Okada Y. 1990; Long-distance movement and viral assembly of tobacco mosaic virus mutants. Virology 176:329–336 [CrossRef]
    [Google Scholar]
  29. Sali A., Blundell T. L. 1993; Comparative protein modeling by satisfaction of spatial restraints. J Mol Biol 234:779–815 [CrossRef]
    [Google Scholar]
  30. Stange C., Matus J. T., Elorza A., Arce-Johnson P. 2004; Identification and characterization of a novel tobacco mosaic virus resistance N gene homologue in Nicotiana tabacum plants. Funct Plant Biol 31:149–158 [CrossRef]
    [Google Scholar]
  31. Stange C., Matus J. T., Dominguez C., Perez-Acle T., Arce-Johnson P. 2008; The N-homologue LRR domain adopts a folding which explains the TMV-Cg-induced HR-like response in sensitive tobacco plants. J Mol Graph Model 26:850–860 [CrossRef]
    [Google Scholar]
  32. Taraporewala Z. F., Culver J. N. 1996; Identification of an elicitor active site within the three-dimensional structure of the tobacco mosaic tobamovirus coat protein. Plant Cell 8:169–178 [CrossRef]
    [Google Scholar]
  33. Taraporewala Z. F., Culver J. N. 1997; Structural and functional conservation of the tobamovirus coat protein elicitor active site. Mol Plant Microbe Interact 10:597–604 [CrossRef]
    [Google Scholar]
  34. Toedt J. M., Braswell E. H., Schuster T. M., Yphantis D. A., Taraporewala Z. F., Culver J. N. 1999; Biophysical characterization of a designed TMV coat protein mutant, R46G, that elicits a moderate hypersensitivity response in Nicotiana sylvestris . Protein Sci 8:261–270
    [Google Scholar]
  35. van der Spoel D., Lindahl E., Hess B., Groenhof G., Mark A. E., Berendsen H. J. C. 2005; gromacs: fast, flexible and free. J Comput Chem 26:1701–1718 [CrossRef]
    [Google Scholar]
  36. van Gunsteren W. F., Daura X., Mark A. E. 1998; GROMOS force field. In Encyclopedia of Computational Chemistry vol 2 pp 1211–1216Edited by Schleyer P., Allinger N., Clark T., Gasteiger J., Kollman P., Schaeffer H. J. New York: Wiley & Sons;
    [Google Scholar]
  37. Wang H., Culver J. N., Stubbs G. 1997; Structure of ribgrass mosaic virus at 2.9 Å resolution: evolution and taxonomy of tobamoviruses. J Mol Biol 269:769–779 [CrossRef]
    [Google Scholar]
  38. Wang H., Planchart A., Stubbs G. 1998; Caspar carboxylates: the structural basis of tobamovirus disassembly. Biophys J 74:633–638 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.83355-0
Loading
/content/journal/jgv/10.1099/vir.0.83355-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error