1887

Abstract

The movement protein NSm of Tomato spotted wilt tospovirus (TSWV) plays pivotal roles in viral intercellular trafficking. Recently, the TSWV NSm was also identified as an avirulence (Avr) determinant during the Sw-5b-mediated hypersensitive response (HR). However, whether the cell-to-cell movement of NSm is coupled to its function in HR induction remains obscure. Here, we showed that the NSm mutants defective in targeting plasmodesmata and cell-to-cell movement were still capable of inducing Sw-5b-mediated HR. In addition, introduction of a single amino-acid substitution, C118Y or T120N, identified previously from TSWV resistance-breaking isolates, into the movement-defective NSm mutants resulted in the failure of HR induction. Collectively, our results showed that the intercellular trafficking of NSm is uncoupled from its function in HR induction. These findings shed light on the evolutionary mechanism of R-Avr recognition and may be used to explain why this uncoupled phenomenon can be observed in many different viruses.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000496
2016-08-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/8/1990.html?itemId=/content/journal/jgv/10.1099/jgv.0.000496&mimeType=html&fmt=ahah

References

  1. Bendahmane A., Farnham G., Moffett P., Baulcombe D. C. 2002; Constitutive gain-of-function mutants in a nucleotide binding site-leucine rich repeat protein encoded at the Rx locus of potato. Plant J 32:195–204[PubMed] [CrossRef]
    [Google Scholar]
  2. Benitez-Alfonso Y., Faulkner C., Ritzenthaler C., Maule A. J. 2010; Plasmodesmata: gateways to local and systemic virus infection. Mol Plant-Microbe Interact 23:1403–1412 [View Article]
    [Google Scholar]
  3. Boiteux L. S., de B. Giordano L. 1993; Genetic basis of resistance against two Tospovirus species in tomato (Lycopersicon esculentum) . Euphytica 71:151–154 [View Article]
    [Google Scholar]
  4. Brommonschenkel S. H., Frary A., Frary A., Tanksley S. D. 2000; The broad-spectrum tospovirus resistance gene Sw-5 of tomato is a homolog of the root-knot nematode resistance gene Mi. Mol Plant-Microbe Interact 13:1130–1138 [View Article][PubMed]
    [Google Scholar]
  5. de Ronde D., Pasquier A., Ying S., Butterbach P., Lohuis D., Kormelink R. 2014; Analysis of Tomato spotted wilt virus NSs protein indicates the importance of the N-terminal domain for avirulence and RNA silencing suppression. Mol Plant Pathol 15:185–195 [View Article][PubMed]
    [Google Scholar]
  6. Elliott R. M. 1990; Molecular biology of the Bunyaviridae. J Gen Virol 71:501–522 [View Article][PubMed]
    [Google Scholar]
  7. Elliott R. M. 1996 The Bunyaviridae New York: Plenum Press; [CrossRef]
    [Google Scholar]
  8. Erickson F. L., Holzberg S., Calderon-Urrea A., Handley V., Axtell M., Corr C., Baker B. 1999; The helicase domain of the TMV replicase proteins induces the N-mediated defence response in tobacco. Plant J 18:67–75[PubMed] [CrossRef]
    [Google Scholar]
  9. Feng Z., Xue F., Xu M., Chen X., Zhao W., Garcia-Murria M. J., Mingarro I., Liu Y., Huang Y. et al. 2016; The ER-membrane transport system is critical for intercellular trafficking of the NSm movement protein and tomato spotted wilt tospovirus. PLoS Pathog 12:e1005443 [View Article][PubMed]
    [Google Scholar]
  10. Goldbach R., Peters D. 1996; Molecular and biological aspects of Tospoviruses. In The Bunyaviridae pp. 129–157 Edited by Elliott R. M. New York: Plenum Press; [CrossRef]
    [Google Scholar]
  11. Hallwass M., de Oliveira A. S., de Campos Dianese E., Lohuis D., Boiteux L. S., Inoue-Nagata A. K., Resende R. O., Kormelink R. 2014; The Tomato spotted wilt virus cell-to-cell movement protein (NSm) triggers a hypersensitive response in Sw-5-containing resistant tomato lines and in Nicotiana benthamiana transformed with the functional Sw-5b resistance gene copy. Mol Plant Pathol 15:871–880 [View Article][PubMed]
    [Google Scholar]
  12. Hanssen I. M., Lapidot M., Thomma B. P. 2010; Emerging viral diseases of tomato crops. Mol Plant-Microbe Interact 23:539–548 [View Article][PubMed]
    [Google Scholar]
  13. Hu Z., Zhang T., Yao M., Feng Z., Miriam K., Wu J., Zhou X., Tao X. 2012; The 2a protein of Cucumber mosaic virus induces a hypersensitive response in cowpea independently of its replicase activity. Virus Res 170:169–173 [View Article][PubMed]
    [Google Scholar]
  14. Kormelink R., Storms M., Van Lent J., Peters D., Goldbach R. 1994; Expression and subcellular location of the NSm protein of Tomato spotted wilt virus (TSWV), a putative viral movement protein. Virology 200:56–65 [View Article][PubMed]
    [Google Scholar]
  15. Lewandowski D. J., Adkins S. 2005; The tubule-forming NSm protein from Tomato spotted wilt virus complements cell-to-cell and long-distance movement of Tobacco mosaic virus hybrids. Virology 342:26–37 [View Article][PubMed]
    [Google Scholar]
  16. Li W., Lewandowski D. J., Hilf M. E., Adkins S. 2009; Identification of domains of the Tomato spotted wilt virus NSm protein involved in tubule formation, movement and symptomatology. Virology 390:110–121 [View Article][PubMed]
    [Google Scholar]
  17. Lucas W. J. 2006; Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344:169–184 [View Article][PubMed]
    [Google Scholar]
  18. López C., Aramburu J., Galipienso L., Soler S., Nuez F., Rubio L. 2011; Evolutionary analysis of tomato Sw-5 resistance-breaking isolates of Tomato spotted wilt virus. J Gen Virol 92:210–215 [View Article][PubMed]
    [Google Scholar]
  19. Paape M., Solovyev A. G., Erokhina T. N., Minina E. A., Schepetilnikov M. V., Lesemann D. E., Schiemann J., Morozov S. Y., Kellmann J. W. 2006; At-4/1, an interactor of the Tomato spotted wilt virus movement protein, belongs to a new family of plant proteins capable of directed intra- and intercellular trafficking. Mol Plant Microbe Interact 19:874–883 [View Article][PubMed]
    [Google Scholar]
  20. Peiró A., Cañizares M. C., Rubio L., López C., Moriones E., Aramburu J., Sánchez-Navarro J. 2014; The movement protein (NSm) of Tomato spotted wilt virus is the avirulence determinant in the tomato Sw-5 gene-based resistance. Mol Plant Pathol 15:802–813 [View Article][PubMed]
    [Google Scholar]
  21. Prins M., Storms M. M. H., Kormelink R., DeHaan P., Goldbach R. 1997; Transgenic tobacco plants expressing the putative movement protein of Tomato spotted wilt tospovirus exhibit aberrations in growth and appearance. Transgenic Res 6:245–251 [CrossRef]
    [Google Scholar]
  22. Shen Y., Zhao X., Yao M., Li C., Miriam K., Zhang X., Tao X. 2014; A versatile complementation assay for cell-to-cell and long distance movements by cucumber mosaic virus based agro-infiltration. Virus Res 190:25–33 [CrossRef]
    [Google Scholar]
  23. Soellick T., Uhrig J. F., Bucher G. L., Kellmann J. W., Schreier P. H. 2000; The movement protein NSm of Tomato spotted wilt tospovirus (TSWV): RNA binding, interaction with the TSWV N protein, and identification of interacting plant proteins. Proc Natl Acad Sci U S A 97:2373–2378 [View Article][PubMed]
    [Google Scholar]
  24. Spassova M. I., Prins T. W., Folkertsma R. T., Klein-Lankhorst R. M., Hille J., Goldbach R. W., Prins M. 2001; The tomato gene Sw5 is a member of the coiled coil, nucleotide binding, leucine-rich repeat class of plant resistance genes and confers resistance to TSWV in tobacco. Mol Breed 7:151–161 [CrossRef]
    [Google Scholar]
  25. Storms M. M. H., van der Schoot C., Prins M., Kormelink R., van Lent J. W. M., Goldbach R. W. 1998; A comparison of two methods of microinjection for assessing altered plasmodesmal gating in tissues expressing viral movement proteins. Plant J 13:131–140 [CrossRef]
    [Google Scholar]
  26. Storms M. M., Kormelink R., Peters D., Van Lent J. W., Goldbach R. W. 1995; The nonstructural NSm protein of Tomato spotted wilt virus induces tubular structures in plant and insect cells. Virology 214:485–493 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000496
Loading
/content/journal/jgv/10.1099/jgv.0.000496
Loading

Data & Media loading...

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