Involvement of salicylate and jasmonate signaling pathways in arabidopsis interaction with fusarium graminearum

Molecular Plant-Microbe Interactions

Volumn 23, Issue 7, 2010, Pages 861-870

  Makandar, Ragiba ^a,b   Nalam, Vamsi ^a   Chaturvedi, Ratnesh ^c   Jeannotte, Richard ^c   Sparks, Alexis A ^c   Shah, Jyoti ^a  

^a UNIVERSITY OF NORTH TEXAS   (United States)

^b UNIVERSITY OF HYDERABAD   (India)

^c KANSAS STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CYCLOPENTANE DERIVATIVE; JASMONIC ACID; OXYLIPIN; SALICYLIC ACID;

ARABIDOPSIS; ARTICLE; FUSARIUM; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT LEAF; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYCLOPENTANES; FUSARIUM; GENE EXPRESSION REGULATION, PLANT; GENOTYPE; HOST-PATHOGEN INTERACTIONS; OXYLIPINS; PLANT LEAVES; SALICYLIC ACID; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; FUNGI; FUSARIUM; GIBBERELLA ZEAE; HORDEUM; TRITICUM AESTIVUM;

EID: 77953223985     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-23-7-0861     Document Type: Article

References (67)

1. Agrios, G. N. 2005. Plant Pathology, 5th ed. Elsevier Academic Press, Amsterdam.
2. Anand, A. Schmelz, E. A., and Muthukrishnan, S. 2003a. Development of a lesion-mimic phenotype in a transgenic wheat line overexpressing genes for pathogenesis-related PR. proteins is dependent on salicylic acid concentration. Mol. Plant-Microbe Interact. 16:96-925.
3. Anand, A., Zhou, T., Trick, H. N., Gill, B. S., and Muthukrishnan, S. 2003b. Greenhouse and field testing of transgenic wheat plants stably expressing genes for thaumatin-like protein, chitinase and glucanase against Fusarium graminearum. J. Exp. Bot. 54:1001-1111.
4. Anand, A., Lei, Z., Summer, L. W., Mysore, K. S., Arakane, Y., Bockus, W. W., and Muthukrishnan, S. 2004. Apoplastic extracts from a transgenic wheat line exhibiting lesion-mimic phenotype have multiple pathogenesis-related proteins that are antifungal. Mol. Plant-Microbe Interact. 17:1306-1317.
5. Bai, G.-H., and Shaner, G. 2004. Management and resistance in wheat and barley to Fusarium head blight. Annu. Rev. Phytopathol. 4:135-161.
6. Berrocal-Lobo, M., Molina, A., and Solano, R. 2002.. Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J. 29:23-32.
7. Bowling, S. A., Guo, A., Cao, H., Gordon, A. S., Klessig D. F., and Dong, X. 1994. A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell 6:1845-1857.
8. Brooks, D. M., Bender, C. L., and Kunkel, B. N. 2005. The Pseudomonas syringae Phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defences in Arabidopsis thaliana. Mol. Plant Pathol. 6:629-639.
9. Cao, H., Bowling, S. A., Gordon, A. S., and Dong, X. 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell:6:1583-1592.
10. Cao, H., Li, X., and Dong, X. 1998. Generation of broad spectrum disease resistance by over expression of an essential regulatory gene in systemic acquired resistance. Proc. Natl. Acad. Sci. U.S.A. 95:6531-6536.
11. Chaturvedi, R., and Shah, J. 2007. Salicylic acid in plant disease resistance. Pages 335-370 in: Salicylic Acid-A Plant Hormone. S. Hayat and A. Ahmad, eds. Springer, Dordrecht, The Netherlands.
12. Chaturvedi, R., Krothapalli, K., Makandar, R., Nandi, A., Sparks, A., Roth, M., Welti, R., and Shah, J. 2008. Plastid ω-3 desaturase-dependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. Plant J. 54:106-117.
13. Chen, C., and Chen, Z. 2002. Potentiation of developmentally regulated plant defense response by AtWRKY 18, a pathogen-induced Arabidopsis transcription factor. Plant Physiol. 129:706-716.
14. Chen, X., Steed, A., Harden, C., and Nicholson, P. 2006. Characterization of Arabidopsis thaliana-Fusarium graminearum interactions and identification of variation in resistance among ecotypes. Mol. Plant Pathol. 7:391-403.
15. Chen, X., Steed, A., Travella, S. Keller, B., and Nicholson, P. 2009. Fusarium graminearum exploits ethylene signaling to colonize dicotyledonous and monocotyledonous plants. New Phytol. 182:975-983.
16. Chomczynski, P., and Sacchi, N. 1987. Single-step method of RNA isolation by acid guanidium thiocyanate-phenol chloroform extraction. Anal. Biochem. 162:156-159.
17. Clarke, J. D., Volko, S. M., Ledford, H., Ausubel, F. M., and Dong, X. 2000. Roles of salicylic acid, jasmonic acid, and ethylene in cpr induced resistance in Arabidopsis. Plant Cell 12:2175-2190.
18. Cuzick, A., Lee, S., Gezan, S., and Hammond-Kosack, K. E. 2008. NPR1 and EDS11 contribute to host resistance against Fusarium culmorum in Arabidopsis buds and flowers. Mol. Plant Pathol. 9:697-704.
19. Delaney, T. P., Friedrich, L., and Ryals, J. A. 1995. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc. Natl. Acad. Sci. U.S.A. 92:6602-6606.
20. Diener, A. C., and Ausubel, F. M. 2005. RESISTANCE TO FUSARIUM OXYSPORUM 1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics 171:305-321.
21. Durrant, W. E., and Dong, X. 2004. Systemic acquired resistance. Annu. Rev. Phytopathol. 42:185-209.
22. Ferrari, S., Plontikova, J. M., De Lorenzo, G., and Ausubel, F. M. 2003. Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J. 35:193-205. (Pubitemid 36901066)
23. Glazebrook, J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205-227.
24. Goswami, R. S., and Kistler, H. C. 2004. Heading for disaster: Fusarium graminearum on cereal crops. Mol. Plant Pathol. 5:515-525.
25. Jayaraj, J., Anand, A., and Muthukrishnan, S. 2004. Pathogenesis-related proteins and their roles in resistance to fungal pathogens. Pages 178-205 in: Fungal Disease Resistance in Plants-Biochemistry, Molecular Biology and Genetic Engineering. Z. K. Punja, ed. Haworth Press, Binghamton, NY, U.S.A.
26. Jing, H.-C., Anderson, L., Sturre, M. J. G., Hille, J., and Dijkwel, P. P. 2007. Arabidopsis CPR5 is a senescence-regulatory gene with pleiotropic functions as predicted by the evolutionary theory of senescence. J. Exp. Bot. 58:3885-3894.
27. Kloek, A. P., Verbsky, M. L., Sharma, S. B., Schoelz, J. E., Vogel, J., Klessig, D. F., and Kunkel, B. N. 2001. Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coil) mutation occurs through two distinct mechanisms. Plant J. 26:509-522.
28. Koornneef, A., and Pieterse, C. M. J. 2008. Cross talk in defense signaling. Plant Physiol. 146:839-844.
29. Kunkel, B. N., and Brooks, D. M. 2002. Cross talk between signaling pathways in plant defense. Curr. Opin. Plant Biol. 5:325-331.
30. Leslie, J. F., and Summerell, B. A. 2006. The Fusarium Laboratory Manual. Blackwell, Ames, IA, U.S.A.
31. Li, G., and Yen, Y. 2008. Jasmonate and ethylene signaling pathway may mediate Fusarium head blight resistance in wheat. Crop Sci. 48:1888-1896.
32. Lin, W.-C., Lu, C.-R., Wu, J.-W., Cheng, M.-L., Lin, Y.-M., Yang, N.-S., Black, L., Green, S. K., Wang, J.-F., and Cheng, C.-P. 2004. Transgenic tomato plants expressing the Arabidopsis NPR1 gene display enhanced resistance to a spectrum of fungal and bacterial diseases. Transgenic Res. 13:567-581.
33. Makandar, R., Essig, J. S., Schapaugh, M. A., Trick, H. N., and Shah, J. 2006. Genetically engineered resistance to Fusarium head blight in wheat by expression of Arabidopsis NPR1. Mol. Plant-Microbe Interact. 19:123-129. (Pubitemid 43172826)
34. Métraux, J.-P., Nawrath, C., and Genoud, T. 2002. Systemic acquired resistance. Euphytica 124:237-243.
35. Nishiuchi, T., Masuda, D., Nakashita, H., Ichimura, K., Shinozaki, K., Yoshida, S., Kimura, M., Yamaguchi. I., and Yamaguchi K. 2006. Fusarium Phytotoxin trichothecenes have an elicitor-like activity in Arabidopsis thaliana, but its activity differed significantly among their molecular species. Mol. Plant-Microbe Interact. 19:512-520.
36. Pieterse, C. J. M., and van Loon, L. C. 2004. NPR1: the spider in the web of induced resistance signaling pathways. Curr. Opin. Plant Biol. 7:456-464.
37. Pritsch, C., Vance, C. P., Bushnell, W. R., Somers, D. A., Hohn, T. M., and Muehlbauer, G. J. 2001. Systemic expression of defense response genes in wheat spikes as a response to Fusarium graminearum infection. Physiol. Mol. Plant Pathol. 58:1-12.
38. Reuber, T. L., Plotnikova, J. M., Dewdney, J., Rogers, E. E., Wood, W., and Ausubel, F. M. 1998. Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. Plant J. 16:473-485.
39. Savitch, L. V., Subramaniam, R., Allard, G. C., and Singh, J. 2007. The GLK1 'regulon' encodes disease defense related proteins and confers resistance to Fusarium graminearum in Arabidopsis. Biochem. Biophys. Res. Commun. 359:234-238. (Pubitemid 46880497)
40. Schmelz, E. A., Engelberth, J., Tumlinson, J. H., Block, A., and Alborn, H. T. 2004. The use of vapor phase extraction in metabolic profiling of phyto hormones and other metabolites. Plant J. 39:790-808. (Pubitemid 39218785)
41. Shah, J., Tsui, F., and Klessig, D. F. 1997. Characterization of a salicylic acid-insensitive mutant (sail) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol. Plant-Microbe Interact. 10:69-78. (Pubitemid 27052575)
42. Shah, J., Kachroo, P., and Klessig, D. F. 1999. The Arabidopsis ssil mutation restores pathogenesis-related gene expression in npr1 plants and renders defensin gene expression salicylic acid dependent. Plant Cell 11:191-206.
43. Shah, J., Kachroo, P., Nandi, A., and Klessig, D. F. 2001. A recessive mutation in the Arabidopsis SSI2 gene confers SA- and NPR1-independent expression of PR genes and resistance against bacterial and oomycete pathogens. Plant J. 25:563-574.
44. Skadsen, R. W., and Hohn, T. M. 2004. Use of Fusarium graminearum transformed with gfp to follow infection patterns in barley and Arabidopsis. Physiol. Mol. Plant Pathol. 64:45-53.
45. Spoel, S. H., Koornneef, A., Chessens, S. M. C, Korzelius, J. P., VanPetl, J. A., Mueller, M. J., Buchala, A. J., Metaux, J.-P., Brown, R., Kazoan, K.,Van Loon, L. C., Dong, X., and Peiterse, C. M. J. 2003. NPR1 modulates cross- talk between salicylate and jasmonate dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760-770.
46. Staswick, P. E., and Tiryaki, I. 2004. The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117-2127.
47. Staswick, P. E., Yuen, G. Y., and Lehman, C. C. 1998. Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare. Plant J. 15:747-754. (Pubitemid 28463803)
48. Thatcher, L. F., Manners, J. M., and Kazan, K. 2009. Fusarium oxysporum hijacks COI1-dependent jasmonate signaling to promote disease development in Arabidopsis. Plant J. 58:927-939.
49. Thomma, B. P. H. J, Eggermont, K., Penninckx, I., Mauch-Mani, B., Vogelsang, R., Cammue, B. P. A., and Broekaert, W. F. 1998. Separate jasmonate-dependent and salicylate-dependent defense-response path-ways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. U.S.A. 95:15107-15111.
50. Thomma, B. P. H. J, Eggermont, K., Tierens, K. F., and Broekaert, W. F. 1999. Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiol. 121:1093-1102. (Pubitemid 30018496)
51. Thomma, B. P. H. J., Eggermont, K., Broekaert, W. F., and Cammue, P. A. 2000. Disease development of several fungi on Arabidopsis can be reduced by treatment with methyl jasmonate. Plant Physiol. Biochem. 38:421-427.
52. Uppalapati, S. R., Ishiga, Y., Wangdi, T., Kunkel, B. N., Anand, A., Mysore, K. S., and Bender, C. L. 2007. The Phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv. tomato DC3000. Mol. Plant-Microbe Interact. 20:955-965. (Pubitemid 47105728)
53. Urban, M., Daniels, S., Mott, E., and Hammond-Kosack, K. 2002. Arabidopsis is susceptible to the cereal ear blight fungal pathogen Fusarium graminearum and Fusarium culomorum. Plant J. 32:961-973. (Pubitemid 36108063)
54. Van Hemelrijck, W., Wouters, P. F. W., Brouwer, M., Windelinckx, A., Goderis, I. J. W. M., De Bolle, M. F. C., Thomma, B. P. H. J., Cammue, B. P. A., and Delaure, S. L. 2006. The Arabidopsis defense response mutant esal as a model to discover novel resistance traits against Fusarium diseases. Plant Sci. 171:585-595.
55. van Loon, L. C., Rep, M., and Pieterse, C. M. J. 2006. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44:135-162.
56. Walter, S., Nicholson, P., and Doohan, F. M. 2010. Action and reaction of host and pathogen during Fusarium head blight disease. New Phytol. 185:54-66.
57. Wang, D., Weaver, N. D., Kesarwani, M., and Dong, X. 2005. Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036-1040. (Pubitemid 40664417)
58. Wang, D., Amornsiripanitch, N., and Dong, X. 2006. A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathogens 2:1042-1050. (Pubitemid 44818624)
59. Wasternack, C. 2007. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann. Bot. 100:681-697.
60. Wildermuth, M. C., Dewdney, J., Wu, G., and Ausubel, F. M. 2001. Isochorismate synthase is required to synthesize acid for plant defense. Nature 414:562-565. (Pubitemid 33131541)
61. Xu, X., Chen, C., Fan, B., and Chen, Z. 2006. Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18:1310-1326.
62. Yu, G.-Y., and Muehlbauer, G. J. 2001. Benzothiadiazole-induced gene expression in wheat spikes does not provide resistance to Fusarium head blight. Physiol. Mol. Plant Pathol. 59:129-136.
63. Zhao, Y., Thilmony, R., Bender, C. L., Schaller, A., He, S. Y., and Howe, G. A. 2003. Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J. 36:485-499.
64. Zimmerli, L., Métraux, J.-P., and Macuh-Mani, B. 2001. β-Aminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiol. 126:517-523. (Pubitemid 32566608)
65. SAS website: www.sas.com
66. Promega Corp. website: www.promega.com
67. Amersham Biosciences website: www.amersham.com