Silicon-mediated resistance of Arabidopsis against powdery mildew involves mechanisms other than the salicylic acid (SA)-dependent defence pathway

Molecular Plant Pathology

Volumn 16, Issue 6, 2015, Pages 572-582

  Vivancos, Julien ^a   Labbé, Caroline ^a   Menzies, James G ^b   Bélanger, Richard R ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

Arabidopsis; Defence genes; Induced resistance; Powdery mildew; Priming; Salicylic acid; Silicon

Indexed keywords

ARABIDOPSIS; ERYSIPHALES; GOLOVINOMYCES CICHORACEARUM; TRITICUM AESTIVUM;

SALICYLIC ACID; SILICON;

ARABIDOPSIS; ASCOMYCETES; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MUTATION; PATHOGENICITY;

ARABIDOPSIS; ASCOMYCOTA; GENE EXPRESSION REGULATION, PLANT; MUTATION; SALICYLIC ACID; SILICON;

EID: 84934756052     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/mpp.12213     Document Type: Article

References (60)

1. Adam, L. and Somerville, S.C. (1996) Genetic characterization of five powdery mildew disease resistance loci in Arabidopsis thaliana. Plant J. 9, 341-356.
2. Bauer, P., Elbaum, R. and Weiss, I.M. (2011) Calcium and silicon mineralization in land plants: transport, structure and function. Plant Sci. 180, 746-756.
3. Bélanger, R.R., Bowen, P.A., Ehret, D.L. and Menzies, J.G. (1995) Soluble silicon: its role in crop and disease management of greenhouse crops. Plant Dis. 79, 329-336.
4. Bélanger, R.R., Benhamou, N. and Menzies, J.G. (2003) Cytological evidence of an active role of silicon in wheat resistance to powdery mildew (Blumeria graminis f. sp. tritici). Phytopathology, 93, 402-412.
5. Benhamou, N. (2009) La Résistance chez les Plantes. Principes de la Stratégie Défensive et Applications Agronomiques. Paris: Éditions TEC and DOC, Lavoisier.
6. Bi, Y., Tian, S.P., Guo, Y.R., Ge, Y.H. and Qin, G.Z. (2006) Sodium silicate reduces postharvest decay on Hami melons: induced resistance and fungistatic effects. Plant Dis. 90, 279-283.
7. Bozkurt, T.O., Schornack, S., Banfield, M.J. and Kamoun, S. (2012) Oomycetes, effectors, and all that jazz. Curr. Opin. Plant Biol. 15, 483-492.
8. Chain, F., Côté-Beaulieu, C., Belzile, F., Menzies, J.G. and Bélanger, R.R. (2009) A comprehensive transcriptomic analysis of the effect of silicon on wheat plants under control and pathogen stress conditions. Mol. Plant-Microbe Interact. 22, 1323-1330.
9. Chérif, M., Benhamou, N., Menzies, J.G. and Bélanger, R.R. (1992a) Silicon induced resistance in cucumber plants against Pythium ultimum. Physiol. Mol. Plant Pathol. 41, 411-425.
10. Chérif, M., Menzies, J.G., Benhamou, N. and Bélanger, R.R. (1992b) Studies of silicon distribution in wounded and Pythium ultimum infected cucumber plants. Physiol. Mol. Plant Pathol. 41, 371-385.
11. Chérif, M., Asselin, A. and Bélanger, R.R. (1994) Defense responses induced by soluble silicon in cucumber roots infected by Pythium spp. Phytopathology, 84, 236-242.
12. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
13. Conrath, U., Pieterse, C.M.J. and Mauch-Mani, B. (2002) Priming in plant-pathogen interactions. Trends Plant Sci. 7, 210-216.
14. Côté-Beaulieu, C., Chain, F., Menzies, J.G., Kinrade, S.D. and Bélanger, R.R. (2009) Absorption of aqueous inorganic and organic silicon compounds by wheat and their effect on growth and powdery mildew control. Environ. Exp. Bot. 65, 155-161.
15. Delaney, T.P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kessmann, H., Ward, E. and Ryals, J. (1994) A central role of salicylic acid in plant disease resistance. Science, 266, 1247-1250.
16. Deshmukh, R.K., Vivancos, J., Guérin, V., Sonah, H., Labbé, C., Belzile, F. and Bélanger, R.R. (2013) Identification and functional characterization of silicon transporters in soybean using comparative genomics of major intrinsic proteins in Arabidopsis and rice. Plant Mol. Biol. 83, 303-315.
17. Dewdney, J., Reuber, T.L., Wildermuth, M.C., Devoto, A., Cui, J., Stutius, L.M., Drummond, E.P. and Ausubel, F.M. (2000) Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant J. 24, 205-218.
18. Diogo, R.V.C. and Wydra, K. (2007) Silicon-induced basal resistance in tomato against Ralstonia solanacearum is related to modification of pectic cell wall polysaccharide structure. Physiol. Mol. Plant Pathol. 70, 120-129.
19. Durrant, W.E. and Dong, X. (2004) Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185-209.
20. Epstein, E. (1999) Silicon. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 641-664.
21. Fauteux, F., Rémus-Borel, W., Menzies, J.G. and Bélanger, R.R. (2005) Silicon and plant disease resistance against pathogenic fungi. FEMS Microbiol. Lett. 249, 1-6.
22. Fawe, A., Abou-Zaid, M., Menzies, J.G. and Bélanger, R.R. (1998) Silicon-mediated accumulation of flavonoid phytoalexins in cucumber. Phytopathology, 88, 396-401.
23. Fawe, A., Menzies, J.G., Chérif, M. and Bélanger, R.R. (2001) Silicon and disease resistance in dicotyledons. In: Silicon in Agriculture (Datnoff, L.E., Snyder, G.H. and Korndörfer, G.H., eds), pp. 323-341. Amsterdam: Elsevier Science.
24. Feys, B.J., Moisan, L.J., Newman, M.-A. and Parker, J.E. (2001) Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J. 20, 5400-5411.
25. Ghanmi, D., McNally, D.J., Benhamou, N., Menzies, J.G. and Bélanger, R.R. (2004) Powdery mildew of Arabidopsis thaliana: a pathosystem for exploring the role of silicon in plant-microbe interactions. Physiol. Mol. Plant Pathol. 64, 189-199.
26. Giraldo, M.C. and Valent, B. (2013) Filamentous plant pathogen effectors in action. Nat. Rev. Microbiol. 11, 800-814.
27. Glazebrook, J. (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205-227.
28. Grégoire, C., Rémus-Borel, W., Vivancos, J., Labbé, C., Belzile, F. and Bélanger, R.R. (2012) Discovery of a multigene family of aquaporin silicon transporters in the primitive plant Equisetum arvense. Plant J. 72, 320-330.
29. Guo, C., Wu, G., Xing, J., Li, W., Tang, D. and Cui, B. (2013) A mutation in a coproporphyrinogen III oxidase gene confers growth inhibition, enhanced powdery mildew resistance and powdery mildew-induced cell death in Arabidopsis. Plant Cell Rep. 32, 687-702.
30. Hodson, M.J., White, P.J., Mead, A. and Broadley, M.R. (2005) Phylogenetic variation in the silicon composition of plants. Ann. Bot. 96, 1027-1046.
31. Jones, J.D.G. and Dangl, J.L. (2006) The plant immune system. Nature, 444, 323-329.
32. Kanto, T., Maekawa, K. and Aino, M. (2007) Suppression of conidial germination and appressorial formation by silicate treatment in powdery mildew of strawberry. J. Gen. Plant Pathol. 73, 1-7.
33. Katz, V.A., Thulke, O.U. and Conrath, U. (1998) A benzothiadiazole primes parsley cells for augmented elicitation of defense responses. Plant Physiol. 117, 1333-1339.
34. Liang, Y. (1999) Effects of silicon on enzyme activity and sodium, potassium and calcium concentration in barley under salt stress. Plant Soil, 209, 217-224.
35. Liang, Y., Zhu, J., Li, Z., Chu, G., Ding, Y., Zhang, J. and Sun, W. (2008) Role of silicon in enhancing resistance to freezing stress in two contrasting winter wheat cultivars. Environ. Exp. Bot. 64, 286-294.
36. Ma, J.F. (2010) Silicon transporters in higher plants. In: MIPS and their Role in the Exchange of Metalloids (Jahn, P.T. and Bienert, G., eds), pp. 99-109. New York: Springer.
37. Ma, J.F. and Yamaji, N. (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci. 11, 392-397.
38. Massoud, K., Barchietto, T., Le Rudulier, T., Pallandre, L., Didierlaurent, L., Garmier, M., Ambard-Bretteville, F., Seng, J.-M. and Saindrenan, P. (2012) Dissecting phosphite-induced priming in Arabidopsis infected with Hyaloperonospora arabidopsidis. Plant Physiol. 159, 286-298.
39. Menzies, J.G., Ehret, D.L., Glass, A.D.M. and Samuels, A.L. (1991) The influence of silicon on cytological interactions between Sphaerotheca fuliginea and Cucumis sativus. Physiol. Mol. Plant Pathol. 39, 403-414.
40. Mitani, N., Yamaji, N., Ago, Y., Iwasaki, K. and Ma, J.F. (2011) Isolation and functional characterization of an influx silicon transporter in two pumpkin cultivars contrasting in silicon accumulation. Plant J. 66, 231-240.
41. Montpetit, J., Vivancos, J., Mitani-Ueno, N., Yamaji, N., Rémus-Borel, W., Belzile, F., Ma, J.F. and Bélanger, R.R. (2012) Cloning, functional characterization and heterologous expression of TaLsi1, a wheat silicon transporter gene. Plant Mol. Biol. 79, 35-46.
42. Pfaffl, M.W., Horgan, G.W. and Dempfle, L. (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36.
43. Qin, G.Z. and Tian, S.P. (2005) Enhancement of biocontrol activity of Cryptococcus laurentii by silicon and the possible mechanisms involved. Phytopathology, 95, 69-75.
44. 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.
45. Reynolds, O.L., Keeping, M.G. and Meyer, J.H. (2009) Silicon-augmented resistance of plants to herbivorous insects: a review. Ann. Appl. Biol. 155, 171-186.
46. Richmond, K.E. and Sussman, M. (2003) Got silicon? The non-essential beneficial plant nutrient. Curr. Opin. Plant Biol. 6, 268-272.
47. Rodrigues, F., Datnoff, L.E., Korndörfer, G.H., Seebold, K.W. and Rush, M.C. (2001) Effect of silicon and host resistance on sheath blight development in rice. Plant Dis. 85, 827-832.
48. Rodrigues, F., McNally, D.J., Datnoff, L.E., Jones, J.B., Labbé, C., Benhamou, N., Menzies, J.G. and Bélanger, R.R. (2004) Silicon enhances the accumulation of diterpenoid phytoalexins in rice: a potential mechanism for blast resistance. Phytopathology, 94, 177-183.
49. Rogers, E.E., Glazebrook, J. and Ausubel, F.M. (1996) Mode of action of the Arabidopsis thaliana phytoalexin camalexin and its role in Arabidopsis-pathogen interactions. Mol. Plant-Microbe Interact. 9, 748-757.
50. Shanner, G. and Finney, R.E. (1977) The effect of nitrogen fertilization on the expression of slow-mildewing resistance in Knox wheat. Phytopathology, 67, 1051-1056.
51. Tocquin, P., Corbesier, L., Havelange, A., Pieltain, A., Kurtem, E., Bernier, G. and Perilleux, C. (2003) A novel high efficiency, low maintenance, hydroponic system for synchronous growth and flowering of Arabidopsis thaliana. BMC Plant Biol. 3, 2.
52. Van Bockhaven, J., De Vleesschauwer, D. and Höfte, M. (2013) Towards establishing broad-spectrum disease resistance in plants: silicon leads the way. J. Exp. Bot. 64, 1281-1293.
53. Van Hulten, M., Pelser, M., van Loon, L.C., Pieterse, C.M.J. and Ton, J. (2006) Costs and benefits of priming for defense in Arabidopsis. Proc. Natl. Acad. Sci. USA, 103, 5602-5607.
54. Vogel, J. and Somerville, S. (2000) Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proc. Natl. Acad. Sci. USA, 97, 1897-1902.
55. Walters, D.R., Ratsep, J. and Havis, N.D. (2013) Controlling crop diseases using induced resistance: challenges for the future. J. Exp. Bot. 64, 1263-1280.
56. Win, J., Chaparro-Garcia, A., Belhaj, K., Saunders, D.G.O., Yoshida, K., Dong, S., Schornack, S., Zipfel, C., Robatzek, S., Hogenhout, S.A. and Kamoun, S. (2012) Effector biology of plant-associated organisms: concepts and perspectives. Cold Spring Harb. Symp. Quant. Biol. 77, 235-247.
57. Ye, M., Song, Y., Long, J., Wang, R., Baerson, S.R., Pan, Z., Zhu-Salzman, K., Xie, J., Cai, K., Luo, S. and Zeng, R. (2013) Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon. Proc. Natl. Acad. Sci. USA, 110, E3631-E3639.
58. Zhang, C., Wang, L., Nie, Q., Zhang, W. and Zhang, F. (2008) Long-term effects of exogenous silicon on cadmium translocation and toxicity in rice (Oryza sativa L.). Environ. Exp. Bot. 62, 300-307.
59. Zhang, C., Wang, L., Zhang, W. and Zhang, F. (2013) Do lignification and silicification of the cell wall precede silicon deposition in the silica cell of the rice (Oryza sativa L.) leaf epidermis? Plant Soil, 372, 137-149.
60. Zhou, N., Tootle, T.L., Tsui, F., Klessig, D.F. and Glazebrook, J. (1998) PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. Plant Cell, 10, 1021-1030.