Skip to main content
SpringerLink
Log in

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

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Phosphite is used to control Oomycetes in a wide range of horticultural and native plant species worldwide. However, phosphite can be phytotoxic, and some pathogens have exhibited a reduction in the effectiveness of phosphite due to prolonged use. In this study, salicylic acid (SA) was investigated as an alternative, or supplementary, treatment to be used to protect plant species. With the use of aeroponics chambers, foliar application of phosphite, SA, and phosphite/SA to Lupinus augustifolius was assessed in relation to root tip damage, in planta phosphite and SA concentration and lesion development. Both phosphite and SA were measurable at the root tip within 24 h of application, and all treatments significantly (P ≤ 0.05) reduced the lesion length at 7 days. However, while phosphite and SA application increased the in planta SA concentration, phosphite caused significantly more damage to the root tip by reducing root cap layers and length than the SA, or phosphite/SA application. This study supports the notion that phosphite-induced sensitivity may be SA-dependent, as both phosphite and SA were found to control P. cinnamomi and stimulate SA accumulation. A combination of phosphite and SA may be more beneficial to plants if it can reduce phytotoxic effects and reduce the chance of pathogen sensitivity to phosphite.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Akinsanmi, O. A., & Drenth, A. (2013). Phosphite and metalaxyl rejuvenate macadamia trees in decline caused by Phytophthora cinnamomi. Crop Protection, 53, 29–36.

    Article  CAS  Google Scholar 

  • An, C., & Mou, Z. (2011). Salicylic acid and its function in plant immunity. Journal of Integrative Plant Biology, 53(6), 412–428.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Boatwright, J. L., & Pajerowska-Mukhtar, K. (2013). Salicylic acid: an old hormone up to new tricks, Review. Molecular Plant Pathology, 14(6), 623–634.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Conrath, U. (2011). Molecular aspects of defence priming. Trends in Plant Science, 16(10), 524–531.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Durner, J., Shah, J., & Klessig, D. F. (1997). Salicylic acid and disease resistance in plants. Trends in Plant Science, 2, 266–274.

    Article  Google Scholar 

  • Duvenhage, J. A. (1994). Monitoring the resistance of Phytophthora cinnamomi to fosetyl-Al and H3PO3. Yearbook – South African Avocado Growers’ Association, 17, 35–37.

    Google Scholar 

  • Fu, Z. Q., & Dong, X. (2013). Systemic acquired resistance: turning local infection into global defense. Annual Review Plant Biology, 64, 839–863.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Hardham, A. R. (2001). The cell biology behind Phytophthora pathogenicity. Australasian Plant Pathology, 30, 91–98.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Klessig, D. F., & Malamy, J. (1994). The salicylic acid signal in plants. Plant Molecular Biology, 26, 1439–1458.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Molders, W., Buchala, A., & Metraux, J.-P. (1996). Transport of salicylic acid in tobacco necrosis virus-infected cucumber plants. Plant Physiology, 112, 787–792.

    PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ouimette, D. G., & Coffey, M. D. (1990). Symplastic entry and phloem translocation in phosphonate. Pesticide Biochemistry and Physiology, 38, 18–25.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Seskar, M., Shulaev, V., & Raskin, I. (1998). Endogenous methyl salicylate in pathogen-inoculated tobacco plants. Plant Physiology, 116, 387–392.

    Article  CAS  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Sukarno, N., Smith, S. E., & Scott, E. S. (1993). The effects of fungicides on vescicular-arbuscular mycorrhizal symbiosis. New Phytologist, 25, 139–147.

    Article  Google Scholar 

  • Thomidis, T., & Elena, K. (2001). Effects of metalaxyl, fosetyl-Al, dimethomorph and cymoxanil on phytophthora cactorum of peach tree. Journal Phytopathology, 149, 97–101.

    Article  CAS  Google Scholar 

  • Ticconi, C. A., Delatorre, C. A. & Abel, S. (2001). Attenuation of phosphate starvation responses by phosphite in Arabidposis. Plant Physiology, 127, 963–972.

  • Urban, J., & Lebeda, A. (2007). Variation of fungicide resistance in Czech populations of Pseudoperonospora cubensis. Journal of Phytopathology, 155, 143–151.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Rob Trengove and Gavin Survey are thanked for their assistance with HPLC analysis.

Author information

Authors and Affiliations

  1. Centre of Phytophthora Science and Management, Veterinary and Life Sciences, Murdoch University, Murdoch, 6150, Australia

    Emma Groves, Kay Howard, Giles Hardy & Treena Burgess

Authors
  1. Emma Groves
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kay Howard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Giles Hardy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Treena Burgess
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Treena Burgess.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Groves, E., Howard, K., Hardy, G. et al. Role of salicylic acid in phosphite-induced protection against Oomycetes; a Phytophthora cinnamomi - Lupinus augustifolius model system. Eur J Plant Pathol 141, 559–569 (2015). https://doi.org/10.1007/s10658-014-0562-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-014-0562-y

Keywords

Search

Navigation