Role of salicylic acid in phosphite-induced protection against Oomycetes; a Phytophthora cinnamomi - Lupinus augustifolius model system

European Journal of Plant Pathology

Volumn 141, Issue 3, 2015, Pages 559-569

  Groves, Emma ^a   Howard, Kay ^a   Hardy, Giles ^a   Burgess, Treena ^a  

^a MURDOCH UNIVERSITY   (Australia)

Author keywords

Accumulation; Induced resistance; Phytotoxicity; Signal; Synthesis

Indexed keywords

EID: 84925503434     PISSN: 09291873     EISSN: 15738469     Source Type: Journal    
DOI: 10.1007/s10658-014-0562-y     Document Type: Article

References (58)

1. Akinsanmi, O. A., & Drenth, A. (2013). Phosphite and metalaxyl rejuvenate macadamia trees in decline caused by Phytophthora cinnamomi. Crop Protection, 53, 29–36.
2. An, C., & Mou, Z. (2011). Salicylic acid and its function in plant immunity. Journal of Integrative Plant Biology, 53(6), 412–428.
3. Attaran, E., Zeier, T. E., Griebel, T., & Zeier, J. (2009). Methyl salicylate production and jasmonate signalling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell, 21, 954–971.
4. Barrett, S. R., Shearer, B. L., & Hardy, G. E. S. J. (2004). Phytotoxicity in relation to in planta concentration of the fungicide phosphite in nine Western Australian native species. Australasian Plant Pathology, 33, 521–528.
5. Boachon, B., Gamir, J., Pastor, V., Erb, M., Dean, J. V., Flors, V., et al. (2014). Role of two UDP-Glycosyltransferases from the L group of Arabidopsis in resistance against Pseudomonas syringae. European Journal of Plant Pathology. doi:10.1007/s10658-014-0424-7.
6. Boatwright, J. L., & Pajerowska-Mukhtar, K. (2013). Salicylic acid: an old hormone up to new tricks, Review. Molecular Plant Pathology, 14(6), 623–634.
7. Brown, S., Koike, S. T., Ochoa, O. E., Laemmlen, F., & Michelmore, R. W. (2004). Insensitivity to the fungicide fosetyl-aluminum in California isolates of the lettuce downy mildew pathogen, Bremia lactucae. Plant Disease, 88, 502–508.
8. Burgess, T., McComb, J. A., Hardy, G. E. S. J., & Colquhoun, I. J. (1998). Influence of low oxygen levels in aeroponics chambers on eucalypt roots infected with Phytophthora cinnamomi. Plant Disease, 82, 368–373.
9. Burgess, T., Hardy, G. E. S. J., McComb, J. A., & Colquhoun, I. J. (1999). Effects of hypoxia on root morphology and lesion development in Eucalyptus marginata infected with Phytophthora cinnamomi. Plant Pathology, 48, 786–796.
10. Camilo-Alves, C., Esteves da Clara, M. I., & Ribeiro, N. (2013). Decline of Mediterranean oak trees and its association with Phytophthora cinnamomi: a review. European Journal Forestry Research, 132, 411–432. doi:10.1007/s10342-013-0688-z.
11. Conrath, U. (2011). Molecular aspects of defence priming. Trends in Plant Science, 16(10), 524–531.
12. Dean, J. V., Mohammed, L. A., & Fitzpatrick, T. (2005). The formation, vacuolar localization, and tonoplast transport of salicylic acid glucose conjugates in tobacco cell suspension cultures. Planta, 221, 287–296.
13. Dobrowolski, M. P., Shearer, B. L., Colquhoun, I. J., O’Brien, P. A., & Hardy, G. E. S. J. (2008). Selection for decreased sensitivity to phosphite in Phytophthora cinnamomi with prolonged use of fungicide. Plant Pathology, 57, 928–936.
14. Durner, J., Shah, J., & Klessig, D. F. (1997). Salicylic acid and disease resistance in plants. Trends in Plant Science, 2, 266–274.
15. 3. Yearbook – South African Avocado Growers’ Association, 17, 35–37.
16. Fu, Z. Q., & Dong, X. (2013). Systemic acquired resistance: turning local infection into global defense. Annual Review Plant Biology, 64, 839–863.
17. Gozzo, F., & Faoro, F. (2013). Systemic acquired resistance (50 years after discovery): moving from the lab to the field. Journal of Agricultural and Food Chemistry, 61, 12473–12491.
18. Hardham, A. R. (2001). The cell biology behind Phytophthora pathogenicity. Australasian Plant Pathology, 30, 91–98.
19. Hardy, G. E., St, J., Barrett, S., & Shearer, B. L. (2001). The future of phosphite as a fungicide to control the soil borne plant pathogen Phytophthora cinnamomi in natural ecosystems. Australasian Plant Pathology, 30, 133–139.
20. Jackson, T. J. (1997). Role of host defences in controlling the growth of Phytophthora cinnamomi in phosphite treated clonal Eucalyptus marginata plants resistant and susceptible to P. cinnamomi. Honours thesis, Murdoch University.
21. Jackson, T. J., Burgess, T., Colquhoun, I. J., Hardy, G. E., & St, J. (2000). Action of the fungicide phosphite on Eucalyptus marginata inoculated with Phytophthora cinnamomi. Plant Pathology, 49, 147–154.
22. Kessmann, H., Staub, T., Hofmann, C., Maetzke, T., & Herzog, J. (1994). Induction of systemic acquired disease resistance in plants by chemicals. Annual Review of Phytopathology, 32, 439–459.
23. Klessig, D. F., & Malamy, J. (1994). The salicylic acid signal in plants. Plant Molecular Biology, 26, 1439–1458.
24. Lim, S., Borza, T., Peters, R. D., Coffin, R. H., Al-Mughrabi, K. I., Pinto, D. M., et al. (2013). Proteomics analysis suggests broad functional changes in potato leaves triggered by phosphites and a complex indirect mode of action against Phytophthora infestans. Journal of Proteomics, 93, 207–223.
25. Lobato, M., Olivieri, F., Altamiranda, E., Wolski, E., Daleo, G., Caldiz, D. O., et al. (2008). Phosphite compounds reduce disease severity in potato seed tubers and foliage. European Journal Plant Pathology, 122, 349–358.
26. Malamy, J., Carr, J. P., Klessig, D. F., & Raskin, I. (1990). Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science, 250, 1002–1004.
27. Mandal, S., Mallick, N., & Mitra, A. (2009). Salicylic acid-induced resistance to Fusarium oxysporum f. sp. lycopersici in tomato. Plant Physiol. Biochemistry, 47, 642–649.
28. Martin, J. A., Solla, A., Witzell, J., Gil, L., & Garcia-Vallejo, M. C. (2010). Antifungal effect and reduction of Ulmus minor symptoms to Ophiostoma novo-ulmi by carvacrol and salicylic acid. European Journal of Plant Pathology, 127, 21–32.
29. Massoud, K., Barchietto, T., Le Rudulier, T., Pallandre, L., Didierlaurent, L., Garmier, M., et al. (2012). Dissecting phosphite-induced priming in Arabidopsis infected with Hyaloperonospora arabidopsidis. Plant Physiology, 159, 286–298.
30. Matheron, M. E., & Matejka, J. C. (1988). Persistence of systemic activity for fungicides applied to citrus trunks to control Phytophthora gummosis. Plant Disease, 72, 170–174.
31. McMahon, P. J., Purwantara, A., Wahab, A., Imron, M., Lambert, S., Keane, P. J., et al. (2010). Phosphonate applied by trunk injection controls stem canker and decreases Phytophthora pod rot (black pod) incidence in cocoa in Sulawesi. Australasian Plant Pathology, 39, 170–175.
32. Meuwly, P., Molders, W., Buchala, A., & Metraux, J.-P. (1995). Local and systemic biosynthesis of salicylic acid in infected cucumber plants. Plant Physiology, 109, 1107–1114.
33. Molders, W., Buchala, A., & Metraux, J.-P. (1996). Transport of salicylic acid in tobacco necrosis virus-infected cucumber plants. Plant Physiology, 112, 787–792.
34. Molina, A., Hunt, M. D., & Ryals, J. (1998). Impaired fungicide activity in plants blocked in disease resistance signal transduction. The Plant Cell, 10, 1903–1914.
35. Murphy, A. M., Holcombe, L. J., & Carr, J. P. (2000). Characteristics of salicylic acid-induced delay in disease caused by a necrotrophic fungal pathogen in tobacco. Physiological and Molecular Plant Pathology, 57, 47–54.
36. Nobuta, K., Okrent, R. A., Stoutemyer, M., Rodibaugh, N., Kempema, L., Wildermuth, M. C., et al. (2007). The GH3 acyl adenylase family member PBS3 regulates salicylic acid-dependent defense responses in Arabidopsis. Plant Physiology, 144, 1144–1156.
37. Noutoshi, Y., Okazaki, M., Kida, T., Nishina, Y., Morishita, Y., Ogawa, T., et al. (2012). Novel plant immune-priming compounds identified via high-throughput chemical screening target salicylic acid glucosyltransferases in Arabidopsis. Plant Cell, 24, 3795–3804.
38. Ouimette, D. G., & Coffey, M. D. (1990). Symplastic entry and phloem translocation in phosphonate. Pesticide Biochemistry and Physiology, 38, 18–25.
39. Pilbeam, R. A., Colquhoun, I. J., Shearer, B. L., Hardy, G. E., & St, J. (2000). Phosphite concentration: its effects on phytotoxicity symptoms and colonisation by Phytophthora cinnamomi in three understorey species of Eucalyptus marginata forest. Plant Pathology, 29, 86–95.
40. Rasmussen, J. B., Hammerschmidt, R., & Zook, M. N. (1991). Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv. syringae. Plant Physiology, 97, 1342–1347.
41. Ryals, J., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H.-Y., & Hunt, M. D. (1996). Systemic acquired resistance. The Plant Cell, 8, 1809–1819.
42. Sanchez, L., Courteaux, B., Hubert, J., Kauffmann, S., Renualt, J.-H., Clement, C., et al. (2012). Rhamnolipids elicit defense responses and induce disease resistance against biotrophic, hemibiotrophic, and necrotrophic pathogens that require different signalling pathways in Arabidopsis and highlight a central role for salicylic acid. Plant Physiology, 160, 1630–1641.
43. Seskar, M., Shulaev, V., & Raskin, I. (1998). Endogenous methyl salicylate in pathogen-inoculated tobacco plants. Plant Physiology, 116, 387–392.
44. Seymour, N. P., Thompson, J. P., & Fiske, M. L. (1994). Phytotoxicity of fosetyl-Al and phosphonic acid to maize during production of vesicular-arbuscular mycorrhizal inoculum. Plant Disease, 78, 441–446.
45. Shulaev, V., Leon, J., & Raskin, I. (1995). Is salicylic acid a translocated signal of systemic acquired resistance in tobacco? The Plant Cell, 7, 1691–1701.
46. Sillero, J. C., Rojas-Molina, M. M., Avila, C. M., & Rubiales, D. (2012). Induction of systemic acquired resistance against rust, ascochyta blight and broomrape in faba bean by exogenous application of salicylic acid and benzothiadiazole. Crop Protection, 34, 65–69.
47. Sukarno, N., Smith, S. E., & Scott, E. S. (1993). The effects of fungicides on vescicular-arbuscular mycorrhizal symbiosis. New Phytologist, 25, 139–147.
48. Thomidis, T., & Elena, K. (2001). Effects of metalaxyl, fosetyl-Al, dimethomorph and cymoxanil on phytophthora cactorum of peach tree. Journal Phytopathology, 149, 97–101.
49. Ticconi, C. A., Delatorre, C. A. & Abel, S. (2001). Attenuation of phosphate starvation responses by phosphite in Arabidposis. Plant Physiology, 127, 963–972.
50. Urban, J., & Lebeda, A. (2007). Variation of fungicide resistance in Czech populations of Pseudoperonospora cubensis. Journal of Phytopathology, 155, 143–151.
51. Varadarajan, D. K., Karthikeyan, A. S., Matilda, P. D., & Raghothama, K. G. (2002). Phosphite, an analog of phosphate, suppresses the coordinated expression of genes under phosphate starvation. Plant Physiology, 129, 1232–1240.
52. Vawdrey, L. L., & Westerhuis, D. (2007). Field and glasshouse evaluations of metalaxyl, potassium phosphonate, acibenzolar and tea tree oil in managing Phytophthora root rot of papaya in far northern Queensland, Australia. Australasian Plant Pathology, 36, 270–276.
53. Vlot, A. C., Dempsey, D. A., & Klessig, D. F. (2009). Salicylic acid, a multifaceted hormone to combat disease. Annual Review of Phytopathology, 47, 177–206.
54. Wicks, T. J., & Hall, B. (1990). Control of Phytophthora canker with phosphonate in artificially inoculated almond and cherry trees. Australian Journal of Experimental Agriculture, 30, 413–420.
55. Wildermuth, M. C., Dewdney, J., Wu, G., & Ausubel, F. M. (2001). Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 414, 562–565.
56. Wilkinson, C. J., Holmes, J. M., Tynan, K. M., Colquhoun, I. J., McComb, J. A., Hardy, G. E. S. J., et al. (2001). Ability of phosphite applied in a glasshouse trial to control Phytophthora cinnamomi in five plant species native to Western Australia. Australasian Plant Pathology, 30, 343–351.
57. Wong, M.-H., McComb, J. A., Hardy, G. E., St, J., & O’Brien, P. A. (2009). Phosphite induces expression of a putative proteophosphoglycan gene in Phytophthora cinnamomi. Australasian Plant Pathology, 38, 235–241.
58. Yalpani, N., Enyedi, A. J., Leon, J., & Raskin, I. (1994). Ultraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis-related proteins and virus resistance in tobacco. Planta, 193, 372–376.