1887

Abstract

Barley stripe mosaic virus North Dakota 18 (ND18), Beijing (BJ), Xinjiang (XJ), Type (TY) and CV21 strains are unable to infect the Bd3-1 inbred line, which harbours a resistance gene designated , but the Norwich (NW) strain is virulent on Bd3-1. Analysis of ND18 and NW genomic RNA reassortants and RNAβ mutants demonstrates that two amino acids within the helicase motif of the triple gene block 1 (TGB1) movement protein have major effects on their Bd3-1 phenotypes. Resistance to ND18 correlates with an arginine residue at TGB1 position 390 (R) and a threonine at position 392 (T), whereas the virulent NW strain contains lysines (K) at both positions. ND18 TGB1 R390K (TGB1) and TGB1 single substitutions, and an TGB1 double mutation resulted in systemic infections of Bd3-1. Reciprocal TGB1 substitutions into TGB1 (TGB1 and TGB1) failed to affect virulence, implying that K and K compensate for each other. In contrast, an TGB1 double mutant exhibited limited vascular movement in Bd3-1, but developed prominent necrotic streaks that spread from secondary leaf veins. This phenotype, combined with the appearance of necrotic spots in certain ND18 mutants, and necrosis and rapid wilting of Bd3-1 plants after BJ strain (TGB1) inoculations, show that Bd3-1 resistance is elicited by the TGB1 protein and suggest that it involves a hypersensitive response.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.045880-0
2012-12-01
2021-10-27
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/12/2729.html?itemId=/content/journal/jgv/10.1099/vir.0.045880-0&mimeType=html&fmt=ahah

References

  1. Brkljacic J., Grotewold E., Scholl R., Mockler T., Garvin D. F., Vain P., Brutnell T., Sibout R., Bevan M. other authors 2011; Brachypodium as a model for the grasses: today and the future. Plant Physiol 157:3–13 [View Article][PubMed]
    [Google Scholar]
  2. Cui Y., Lee M. Y., Huo N., Bragg J., Yan L., Yuan C., Li C., Holditch S. J., Xie J. other authors 2012; Fine mapping of the Bsr1 barley stripe mosaic virus resistance gene in the model grass Brachypodium distachyon . PLoS ONE 7:e38333 [View Article][PubMed]
    [Google Scholar]
  3. Donald R. G., Jackson A. O. 1994; The barley stripe mosaic virus γ b gene encodes a multifunctional cysteine-rich protein that affects pathogenesis. Plant Cell 6:1593–1606[PubMed]
    [Google Scholar]
  4. Donald R. G., Lawrence D. M., Jackson A. O. 1997; The barley stripe mosaic virus 58-kilodalton β(b) protein is a multifunctional RNA binding protein. J Virol 71:1538–1546[PubMed]
    [Google Scholar]
  5. Edwards M. C., Bragg J., Jackson A. O. 2006; Natural resistance mechanisms to viruses in barley. In Natural Resistance Mechanisms of Plants to Viruses pp. 465–501 Edited by Loebenstein G., Carr J. P. Dordrecht: Springer; [View Article]
    [Google Scholar]
  6. Flor H. H. 1971; Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296 [View Article]
    [Google Scholar]
  7. Garvin D. F., Gu Y.-Q., Hasterok R., Hazen S. P., Jenkins G., Mockler T. C., Mur L. A. J., Vogel J. P. 2008; Development of genetic and genomic research resources for Brachypodium distachyon, a new model system for grass crop research. Crop Sci 48:S69–S84 [View Article]
    [Google Scholar]
  8. Gassmann W., Bhattacharjee S. 2012; Effector-triggered immunity signaling: from gene-for-gene pathways to protein–protein interaction networks. Mol Plant Microbe Interact 25:862–868 [View Article][PubMed]
    [Google Scholar]
  9. Gordon J. I., Duronio R. J., Rudnick D. A., Adams S. P., Gokel G. W. 1991; Protein N-myristoylation. J Biol Chem 266:8647–8650[PubMed]
    [Google Scholar]
  10. Gururani M. A., Venkatesh J., Upadhyaya C. P., Nookaraju A., Pandey S. K., Park S. W. 2012; Plant disease resistance genes: current status and future directions. Physiol Mol Plant Pathol 78:51–65 [View Article]
    [Google Scholar]
  11. Heath M. C. 2000; Hypersensitive response-related death. Plant Mol Biol 44:321–334 [View Article][PubMed]
    [Google Scholar]
  12. Jackson A. O., Lane L. C. 1981; Hordeiviruses. In Handbook of Plant Virus Infections and Comparative Diagnosis pp. 565–625 Edited by Kwistakk E. Amsterdam: Elsevier;
    [Google Scholar]
  13. Jackson A. O., Petty I. T. D., Jones R. W., Edwards M. C., French R. 1991a; Analysis of barley stripe mosaic virus pathogenicity. Semin Virol 2:107–119
    [Google Scholar]
  14. Jackson A. O., Petty I. T. D., Jones R. W., Edwards M. C., French R. 1991b; Molecular genetic analysis of barley stripe mosaic virus pathogenicity determinants. Can J Plant Pathol 13:163–177 [View Article]
    [Google Scholar]
  15. Jackson A. O., Lim H.-S., Bragg J., Ganesan U., Lee M. Y. 2009; Hordeivirus replication, movement, and pathogenesis. Annu Rev Phytopathol 47:385–422 [View Article][PubMed]
    [Google Scholar]
  16. Kalinina N. O., Rakitina D. V., Solovyev A. G., Schiemann J., Morozov S. Y. 2002; RNA helicase activity of the plant virus movement proteins encoded by the first gene of the triple gene block. Virology 296:321–329 [View Article][PubMed]
    [Google Scholar]
  17. Kang B.-C., Yeam I., Jahn M. M. 2005; Genetics of plant virus resistance. Annu Rev Phytopathol 43:581–621 [View Article][PubMed]
    [Google Scholar]
  18. Lane L. C. 1974; The components of barley stripe mosaic and related viruses. Virology 58:323–333 [CrossRef]
    [Google Scholar]
  19. Leshchiner A. D., Solovyev A. G., Morozov S. Y., Kalinina N. O. 2006; A minimal region in the NTPase/helicase domain of the TGBp1 plant virus movement protein is responsible for ATPase activity and cooperative RNA binding. J Gen Virol 87:3087–3095 [View Article][PubMed]
    [Google Scholar]
  20. Lim H.-S., Bragg J. N., Ganesan U., Lawrence D. M., Yu J., Isogai M., Hammond J., Jackson A. O. 2008; Triple gene block protein interactions involved in movement of barley stripe mosaic virus. J Virol 82:4991–5006 [View Article][PubMed]
    [Google Scholar]
  21. Lim H.-S., Bragg J. N., Ganesan U., Ruzin S., Schichnes D., Lee M. Y., Vaira A. M., Ryu K. H., Hammond J., Jackson A. O. 2009; Subcellular localization of the barley stripe mosaic virus triple gene block proteins. J Virol 83:9432–9448 [View Article][PubMed]
    [Google Scholar]
  22. Maule A. J., Caranta C., Boulton M. I. 2007; Sources of natural resistance to plant viruses: status and prospects. Mol Plant Pathol 8:223–231 [View Article][PubMed]
    [Google Scholar]
  23. McKinney H. H., Greeley L. W. 1965; Biological characteristics of barley stripe mosaic virus strains and their evolution. US Department of Agriculture Technical Bulletin no. 1324
  24. Moffett P. 2009; Mechanisms of recognition in dominant R gene mediated resistance. Adv Virus Res 75:1–33 [View Article][PubMed]
    [Google Scholar]
  25. Morozov S. Y., Solovyev A. G. 2003; Triple gene block: modular design of a multifunctional machine for plant virus movement. J Gen Virol 84:1351–1366 [View Article][PubMed]
    [Google Scholar]
  26. Opanowicz M., Vain P., Draper J., Parker D., Doonan J. H. 2008; Brachypodium distachyon: making hay with a wild grass. Trends Plant Sci 13:172–177 [View Article][PubMed]
    [Google Scholar]
  27. Petty I. T. D., Hunter B. G., Jackson A. O. 1988; A novel strategy for one-step cloning of full-length cDNA and its application to the genome of barley stripe mosaic virus. Gene 74:423–432 [View Article][PubMed]
    [Google Scholar]
  28. Petty I. T. D., Hunter B. G., Wei N., Jackson A. O. 1989; Infectious barley stripe mosaic virus RNA transcribed in vitro from full-length genomic cDNA clones. Virology 171:342–349 [View Article][PubMed]
    [Google Scholar]
  29. Petty I. T. D., Donald R. G. K., Jackson A. O. 1994; Multiple genetic determinants of barley stripe mosaic virus influence lesion phenotype on Chenopodium amaranticolor . Virology 198:218–226 [View Article][PubMed]
    [Google Scholar]
  30. Renner T., Bragg J., Driscoll H. E., Cho J., Jackson A. O., Specht C. D. 2009; Virus-induced gene silencing in the culinary ginger (Zingiber officinale): an effective mechanism for down-regulating gene expression in tropical monocots. Mol Plant 2:1084–1094 [View Article][PubMed]
    [Google Scholar]
  31. Santoso A., Edwards M. C. 2003; Identification of the nucleotide substitutions required for barley stripe mosaic hordeivirus pathogenicity to barley possessing the rsm1 gene. Phytopathology 93S75–S76
    [Google Scholar]
  32. Sun X., An D., Qing L., Yang S. 2007; Identification of the barley stripe mosaic virus (BSMV) from Beijing. J Southwest Univ (Nat Sci Ed) 29:51–54
    [Google Scholar]
  33. Timian R. G. 1974; The range of symbiosis of barley and Barley stripe mosaic virus . Phytopathology 64:342–345 [View Article]
    [Google Scholar]
  34. Traverso J. A., Meinnel T., Giglione C. 2008; Expanded impact of protein N-myristoylation in plants. Plant Signal Behav 3:501–502 [View Article][PubMed]
    [Google Scholar]
  35. van Ooijen G., Mayr G., Kasiem M. M., Albrecht M., Cornelissen B. J., Takken F. L. 2008; Structure–function analysis of the NB-ARC domain of plant disease resistance proteins. J Exp Bot 59:1383–1397 [View Article][PubMed]
    [Google Scholar]
  36. Verchot-Lubicz J., Torrance L., Solovyev A. G., Morozov S. Y., Jackson A. O., Gilmer D. 2010; Varied movement strategies employed by triple gene block-encoding viruses. Mol Plant Microbe Interact 23:1231–1247 [View Article][PubMed]
    [Google Scholar]
  37. Vogel J., Bragg J. 2009; Brachypodium distachyon, a new model for the Triticeae. In Genetics and Genomics of the Triticeae pp. 427–449 Edited by Muehlbauer G. J., Feuillet C. New York: Springer; [View Article]
    [Google Scholar]
  38. Vogel J. P., Garvin D. F., Mockler T. C., Schmutz J., Rokhsar D., Bevan M. W., Barry K., Lucas S., Harmon-Smith M. other authors 2010; Genome sequencing and analysis of the model grass Brachypodium distachyon . Nature 463:763–768 [View Article][PubMed]
    [Google Scholar]
  39. Weiland J. J., Edwards M. C. 1996; A single nucleotide substitution in the α a gene confers oat pathogenicity to barley stripe mosaic virus strain ND18. Mol Plant Microbe Interact 9:62–67 [View Article][PubMed]
    [Google Scholar]
  40. Whitham S., Dinesh-Kumar S. P., Choi D., Hehl R., Corr C., Baker B. 1994; The product of the tobacco mosaic virus resistance gene N: similarity to Toll and the interleukin-1 receptor. Cell 78:1101–1115 [View Article][PubMed]
    [Google Scholar]
  41. Xie H., Wang Z., Li W., Ni S. 1981; Occurence of barley stripe mosaic virus in Xinjiang. Acta Phytopathologica Sinica 11:11–14
    [Google Scholar]
  42. Yuan C., Li C., Yan L., Jackson A. O., Liu Z., Han C., Yu J., Li D. 2011; A high throughput barley stripe mosaic virus vector for virus induced gene silencing in monocots and dicots. PLoS ONE 6:e26468 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.045880-0
Loading
/content/journal/jgv/10.1099/vir.0.045880-0
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