Skip to main content
SpringerLink
Log in

The role of fungicides in the physiology of higher plants: Implications for defense responses

  • Published:
The Botanical Review Aims and scope Submit manuscript

Abstract

Plants react to pathogen attack through a variety of active and passive defense mechanisms primarily related to the metabolism of phenolic compounds and oxidative metabolism. Thus the activation of defensive reactions is associated with the increased expression of a great number of genes that encode enzymes involved in the biosynthetic pathway of phenolic compounds. Similarly, the activation of oxidative metabolism precedes the expression of defense genes during plant-pathogen interactions, so both metabolic processes must exert a major function in directing the mechanisms to resist disease. Similarly, it has been suggested that certain fungicides used to mitigate or prevent pathogen attack may be involved in activating certain defensive responses of plants. However, the fact that such substances may influence the key steps of the phenolic and oxidative processes has scarcely been studied. Our work confirms the results proposed by other authors, who suggest that certain wide-spectrum fungicides, in addition to their antibiotic action against pathogens, may be involved in the activation of some defensive responses of plants.

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

Similar content being viewed by others

Literature Cited

  • Aono, M., H. Saji, A. Sakamoto, K. Fujiyama, N. Cómodo &K. Tanaka. 1995. Paraquat tolerance of transgenicNicotiana tabaccum with enhanced activities of glutathione reductase and Superoxide dismutase. Pl. Cell Physiol. 36: 1687–1691.

    CAS  Google Scholar 

  • Apostol, I., P. F. Heinstein &P. S. Low. 1989. Rapid simulation of an oxidative burst during elicitation of cultured plant cells: Role in the defense and signal transduction. Pl. Physiol. (Lancaster) 90: 109–116.

    CAS  Google Scholar 

  • Bader, K. P. &R. Abdel-Basset. 1999. Adaptation of plants to anthropogenic and environmental stresses: The effects of air constituents and plant-protective chemicals. Pp. 973–1010in M. Pessarakli (ed.), Handbook of plant and crop stress. Marcel Dekker, New York.

    Google Scholar 

  • Barak, E., L. V. Edginton &B. D. Ripley. 1984. Bioactivity of the fungicide metalaxyl in potato tubers against some species ofPhytophthora, Fusarium, andAlternaria, related to polyohenoloxidase activity. Canad. J. Pl. Pathol. 6: 304–308.

    CAS  Google Scholar 

  • Benhamou, N. 1996. Elicitor-induced plant defence pathways. Trends Pl. Sci. 1: 233–240.

    Google Scholar 

  • Bowler, C., M. V. Van Montagu &D. Inzé. 1992. Superoxide dismutase and stress tolerance. Annual Rev. Pl. Physiol. Pl. Molec. Biol. 43: 83–116.

    Article  CAS  Google Scholar 

  • Bradley, D. J., P. Kjellbom &C. J. Lamb. 1992. Elicitor-induced and wound-induced oxidative crosslinking of a proline-rich plant-cell wall protein: A novel, a rapid defense response. Cell 70: 21–30.

    Article  PubMed  CAS  Google Scholar 

  • Brisson, L. F., R. Tenhaken &C. Lamb. 1994. Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Pl. Cell 6: 1703–1712.

    CAS  Google Scholar 

  • Cadenas, E. 1989. Biochemistry of oxygen toxicity. Annual Rev. Biochem. 58: 79–110.

    Article  CAS  Google Scholar 

  • Cakmak, I. &H. Marschner. 1993. Activities of hydrogen peroxide-scavenging enzymes in germinating wheat seed. J. Exp. Bot. 44: 127–132.

    Article  CAS  Google Scholar 

  • Chen, Z., H. Silva &D. F. Klessig. 1993. Active oxygen species in the induction of plant systematic acquired resistance by salicylic acid. Science 262: 1883.

    Article  PubMed  CAS  Google Scholar 

  • Chester, K. S. 1933. The problem of acquired physiological immunity in plants. Quart. Rev. Biol. 8: 275–324.

    Article  Google Scholar 

  • Delaney, T. P., S. Uknes, B. Vernoij, L. Friedrich, K. Weymann, D. Negrotto, T. Gaffney, M. Gut-Rella, H. Kessmann &E. Ward. 1994. A central role of salicylic acid in plant disease resistance. Science 266: 1247–1250.

    Article  PubMed  CAS  Google Scholar 

  • Delp, C. J. 1987. Benzimidazole and related fungicides. Pp. 233–244in H. Lyr (ed.), Modern selective fungicides: Properties, applications, mechanisms of action. Wiley, New York.

    Google Scholar 

  • Dixon, R. A. &C. J. Lamb. 1990. Molecular communication in interactions between plant and microbial pathogens. Annual Rev. Pl. Physiol. Pl. Molec. Biol. 41: 339–367.

    Article  CAS  Google Scholar 

  • —,M. J. Harrison &C. J. Lamb. 1994. Early events in the activation of plant defense responses. Annual Rev. Phytopathol. 32: 479–501.

    Article  CAS  Google Scholar 

  • Doke, N. 1983. Generation of Superoxide anion by potato tuber protoplast during hypersensitive response to hyphal wall components ofPhytophtora infestons and specific inhibition of the reaction with suppressors of hypersensitivity. Physiol. Pl. Pathol. 23: 359–367.

    CAS  Google Scholar 

  • — &Y. Ohashi. 1988. Involvement of an O2 generating system in the induction of necrotic lesions on tobacco leaves infected with tobacco mosaic virus. Physiol. Molec. Pl. Pathol. 32: 163–175.

    Article  CAS  Google Scholar 

  • Dominguez, F. 1998. Plagas y enfermedades de las plantas cultivadas. Ed. 9. Mundi-Prensa Libros, Madrid.

    Google Scholar 

  • Durner, J. &D. F. Klessig. 1995. Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defence responses. Proc. Natl. Acad. U.S.A. 92: 11312–11316.

    Article  CAS  Google Scholar 

  • Ebel, J. &H. Grisebach. 1988. Defense strategies of soybean against the fungusPhytophthora megasperma f. sp.glycinea: A molecular analysis. Trends Biochem. Sci. 13: 23–27.

    Article  PubMed  CAS  Google Scholar 

  • Enyedi, A., N. Yalpani, P. Silverman &I. Raskin. 1992. Localization, conjugation and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc. Natl. Acad. U.S.A. 89: 2480–2484.

    Article  CAS  Google Scholar 

  • Fisher, D. J. &A. L. Hayes. 1982. Mode of action of the systemic fungicides furalaxyl, metalaxyl, and ofurace. Pest. Sci. 13: 330–339.

    Article  CAS  Google Scholar 

  • Friend, J. 1985. Phenolic substances and plant disease. Pp. 131–137in C. F. van Sumere & P. J. Lea (eds.), The biochemistry of plant phenolics. Clarendon, Oxford.

    Google Scholar 

  • Garcia, P. C., R. M. Rivero, L. R. López-Lefebre, E. Sánchez, J. M. Ruiz &L. Romero. 2001. Direct action of the biocide carbendazim on phenolic metabolism in tobacco plants. J. Agric. Food Chem. 49: 131–137.

    Article  PubMed  CAS  Google Scholar 

  • —. 2002. Is the application of carbendazim harmful to healthy plants? Evidence of weak phytotoxicity in tobacco. J. Agric. Food Chem. 50: 279–283.

    Article  PubMed  CAS  Google Scholar 

  • Guest, D. I. 1984. Modification of defence responses in tobacco and capsicum following treatments with fosetyl-Al [aluminium tris (o-ethyl phosphonate)]. Physiol. Pl. Pathol. 25: 125–134.

    Article  CAS  Google Scholar 

  • Hammond-Kosack, K. E. &J. G. Jones. 1996. Resistance gene-dependent plant defense responses. Pl. Cell 8: 1773–1791.

    CAS  Google Scholar 

  • Hernández, J. A., E. Olmos, F. G. Corpas, F. Sevilla &L. A. del Rio. 1995. Salt-induced oxidative stress on chloroplasts of pea plants. Pl. Sci. (Elsevier) 105: 151–167.

    Article  Google Scholar 

  • Heydari, A. &I. J. Misaghi. 1999. Herbicide-mediated changes in the population and activity of root-associated microorganisms: A potential cause of plant stress. Pp. 613–624in M. Pessarakli (ed.), Handbook of plant and crop stress. Marcel Dekker, New York.

    Google Scholar 

  • Hunt, M. D. &J. A. Ryals. 1996. Systemic acquires resistance signal transduction. Critical Rev. Pl. Sci. 15(5–6): 583–606.

    Article  CAS  Google Scholar 

  • Iturbe-Omaerxe, I., J. F. Moran, C. Arrese-Igor, Y. Gorgocena, R. V. Klucas &M. Becana. 1995. Activated oxygen and antioxidant defenses in iron-deficient pea plants. Pl. Cell Environ. 18: 421–429.

    Article  Google Scholar 

  • Jones, J. B., S. S. Woltz, J. P. Jones &K. L. Portier. 1991. Population dynamics ofXanthomonas campestris pv. Vesicatoria on tomato leaflets treated with copper bactericides. Phytopathology 81: 714–719.

    Article  CAS  Google Scholar 

  • Keppler, L. D., C. J. Baker &M. M. Atkinson. 1989. Active oxygen production during a bacteria induced hypersensitive reaction in tobacco suspension cells. Phytopathology 79: 974–978.

    Article  CAS  Google Scholar 

  • Klessig, D. F. &J. Malamy. 1994. The salicylic acid signal in plants. Pl. Molec. Biol. 26: 1439–1458.

    Article  CAS  Google Scholar 

  • Kuc, J. 1995. Phytoalexins, stress metabolism, and disease resistance in plants. Annual Rev. Phytopathol. 33: 275–297.

    Article  CAS  Google Scholar 

  • Leon, J., M. A. Lawton &I. Raskin. 1995. H2O2 simulated salicylic acid biosynthesis in tobacco. Pl. Physiol. (Lancaster) 108: 1673–1678.

    CAS  Google Scholar 

  • Levine, A., R. Tenhaken, R. Dicon &C. Lamb. 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79(4): 583–593.

    Article  PubMed  CAS  Google Scholar 

  • Lydon, J. &S. O. Duke. 1989. Pesticide effects on secondary metabolism of higher plants. Pest. Sci. 25: 361–373.

    Article  CAS  Google Scholar 

  • Malamy, J., J. P. Carr, D. F. Klessig &I. Raskin. 1990. Salicylic acid: A likely endogenous signal in the resistance response of tobacco to viral infection. Science 205: 1002–1004.

    Article  Google Scholar 

  • Marc, W., V. Iersel &B. Bugbee. 1996. Phytotoxic effects of benzimidazole fungicides on bedding plants. J. Amer. Soc. Hort. Sci. 211(6): 1095–1102.

    Google Scholar 

  • ———. 1997. Dibutylurea reduces photosynthesis, growth and flowering ofPetunia andImpatiens. J. Amer. Soc. Hort. Sci. 122(4): 536–541.

    Google Scholar 

  • Mauch-Mani, B. &A. J. Slusarenko. 1996. Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance ofArabidopsis toPeronospora parasitica. Pl. Cell. 8: 203–212.

    CAS  Google Scholar 

  • Mehdy, M. C., Y. K. Sharma &K. Sathasivan. 1996. The role of activated oxygen species in plant disease resistance. Physiol. PL (Copenhagen) 98(2): 365–374.

    Article  CAS  Google Scholar 

  • Métraux, J., H. Singer, J. Ryals, E. Ward, M. Wyss-Benz, J. Gaudin, K. Raschdorf, E. Schmid, W. Blum &B. Inverardi. 1990. Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250: 1004–1006.

    Article  PubMed  Google Scholar 

  • Mishra, N. P., R. K. Mishra &G S. Singhal. 1995. Changes in the activities of antioxidant enzymes during exposure of intact wheat leaves to strong visible light at different temperatures in presence of protein synthesis inhibitors. PL Physiol. (Lancaster) 102: 903–910.

    Google Scholar 

  • Molina, A., M. D. Hunt &J. A. Ryals. 1998. Impaired fungicide activity in plants blocked in disease resistance signal transduction. PL Cell 10: 1903–1914.

    CAS  Google Scholar 

  • Monk, L. S., K. V. Fagerstedt &R. M. N. Crawford. 1987. Superoxide dismutase as an anaerobic polypeptide: A key factor in recovery from oxygen deprivation inIris pseudacorus? Plant. Physiol. 85: 1016–1020.

    PubMed  CAS  Google Scholar 

  • Nagarathna, K. C., S. A. Shetty &H. S. Shetty. 1993. Phenylalanine ammonia-lyase activity in pearl millet seedlings and its relation to downy mildew disease resistance. J. Exp. Bot. 44: 1291–1296.

    Article  CAS  Google Scholar 

  • Nemestothy, G N. &D. I. Guest. 1990. Phytoalexin accumulation, phenylalanine ammonia-lyase activity and ethylene biosynthesis in fosetyl-Al treated resistant and susceptible tobacco cultivars infected withPhytophthora nicotianae var.nicotiane. Physiol. Molec. Pl. Pathol. 37: 207–219.

    Article  CAS  Google Scholar 

  • Nicholson, R. L. &R. Hammerschmidt. 1992. Phenolic compounds and their role in disease resistance. Annual Rev. Phytopathol. 30: 369–389.

    Article  CAS  Google Scholar 

  • Olsson, M., K. Nilsson, C. Liljenberg &G A. F. Hendry. 1996. Drought stress in seedlings-lipid metabolism and lipid peroxidation during recovery from drought inLotus corniculatus andCerastium fontanum. Physiol. Pl. (Copenhagen) 96: 577–584.

    Article  CAS  Google Scholar 

  • Pallas, J. A., N. L. Pavia, C. Lamb &R. A. Dixon. 1996. Tobacco plants epigenetically suppressed in phenylalanine ammonia-lyase expression do not develop systemic acquired resistance in response to infection by tobacco mosaic virus. Pl. J. 10: 281–293.

    Article  CAS  Google Scholar 

  • Peng, M. &J. Kuc. 1992. Peroxidase-generated hydrogen peroxide as a source of antifungal activity in vitro on tobacco leaf disks. Phytopathology 82: 696–699.

    Article  CAS  Google Scholar 

  • Rainieri, A., G D’Urso, C. Nali, G Lorenzoni &G F. Soldatini. 1996. Ozone stimulates apoplastic antioxidant system in pumpkin leaves. Physiol. Pl. (Copenhagen) 97: 381–387.

    Article  Google Scholar 

  • Rasmussen, J. B., R. Hammerschmidt &M. N. Zook. 1991. Systemic induction of salicylic acid accumulation in cucumber after inoculation withPseudomonas syringae pv.Syringae. PI. Physiol. (Lancaster) 97: 1342–1347.

    CAS  Google Scholar 

  • Ryals, J. K., U. H. Neuenschwander, M. G. Willits, A. Molina, H. Steiner &M. D. Hunt. 1996. Systemic acquired resistance. Pl. Cell 8: 1809–1819.

    CAS  Google Scholar 

  • Skene, K. G M. 1972. Cytokinin-like properties of the systemic fungicide benomyl. J. Hort. Sci. 47: 179–182.

    CAS  Google Scholar 

  • Smith-Becker, J., E. Marois, E. J. Huguet, S. L. Midland, J. J. Sims &N. T. Keen. 1998. Accumulation of salicylic acid and 4-hydrobenzoic acid in phloem fluids of cucumber during systemic resistance is preceded by a transient increase in phenylalanine ammonia-lyase activity in petioles and stem. Pl. Physiol. (Lancaster) 116: 231–238.

    Article  CAS  Google Scholar 

  • Summermatter, K., L. Sticher &J. P. Métraux. 1995. Systemic response inArabidopsis thaliana infected and challenged withPseudomonas syringae pv.syringae. Pl. Physiol. (Lancaster) 108: 1379–1385.

    CAS  Google Scholar 

  • Tenhaken, R., A. Levine, L. F. Brisson, R. A. Dixon &C. J. Lamb. 1995. Function of the oxidative burst in hypersensitive disease resistance. Proc. Natl. Acad. U.S.A. 92: 4158–4163.

    Article  CAS  Google Scholar 

  • Tiburzy, R. &H. J. Reisener. 1990. Resistance of wheat toPuccinia graminis f. sp.Tritici: Association of the hypersensitive reaction with the cellular accumulation of linkin-like material and callose. Physiol. Molec. Pl. Pathol. 36: 109–120.

    Article  CAS  Google Scholar 

  • Tomlin, C. (ed.). 1994. The pesticide manual: A world compendium: Incorporating the agrochemicals handbook. Ed. 10. British Crop Protection Council, Farnham, England; Royal Society of Chemistry, Information Sciences, Cambridge.

    Google Scholar 

  • Tripathi, R. K., K. Tandon, E. Schlösser &W. M. Hess. 1982. Effects of fungicides on the physiology of plants, IV: Protection of cellular organelles of senescent wheat leaves by carbendazim. Pest. Sci. 13: 395–400.

    Article  CAS  Google Scholar 

  • Uknes, S., B. Mauch-Many, M. Moyer, S. Potter, S. Williams, S. Dincher, D. Chandler, A. Slusarenko, E. Ward. &J. Ryals. 1992. Acquired resistance inArabidopsis. Pl. Cell. 4: 645–656.

    CAS  Google Scholar 

  • Vera-Estrella, R., E. Blumwald &V. J. Higgins. 1992. Effect of specific elicitors ofCladosporium fulvum on tomato suspension cells. Pl. Physiol. (Lancaster) 99: 1208–1215.

    CAS  Google Scholar 

  • Ward, E. R., S. J. Uknes, S. C. Williams, S. S. Dincher, D. L. Wiederhold, D. C. Alexander, P. Ahl-Goy, J. Métraux &J. A. Ryals. 1991. Coordinate gene activity in response to agents that induce systemic acquired resistance. Pl. Cell. 3: 1085–1094.

    CAS  Google Scholar 

  • Ward, E. W. B., G Lazarovits, P. Stössel, S. D. Barrie &C. H. Unwin. 1980. Glyceollin production associated with the control ofPhytophthora root of soybean by the systemic fungicide, metalaxyl. Phytopathology 70: 738–740.

    CAS  Google Scholar 

  • Weckx, J. E. J. &H. M. M. Clijters. 1996. Oxidative damage and defense mechanisms in primary leaves ofPhaseolus vulgaris as a result of root assimilation of toxic amounts of copper. Physiol. Pl. (Copenhagen) 96: 506–512.

    Article  CAS  Google Scholar 

  • Wendehenne, D., J. Durner, Z. Chen &D. F. Klessig. 1998. Bezothiadiazole, an inducer of plant defenses, inhibits catralase and ascorbate peroxidase. Phytochemistry 47: 651–657.

    Article  CAS  Google Scholar 

  • Wenzel, A. A. &H. Melhorn. 1995. Zinc deficiency enhances ozone toxicity in bush beans (Phaseolus vulgaris L. cv.Saxa). J. Exp. Bot. 46: 867–872.

    Article  CAS  Google Scholar 

  • Wojtaszek, P. 1995. Oxidative burst: An early plant response to pathogen infection. Biochem. J. 332: 681–692.

    Google Scholar 

  • Wu, G., B. J. Shortt, E. B. Lawrence, J. Leon, K. C. Fitzsimmons, E. B. Levine, I. Raskin &D. M. Sha. 1997. Activation of host defense mechanisms by elevated production of H2O2 in transgenic plants. Pl. Physiol. (Lancaster) 115: 427–435.

    CAS  Google Scholar 

  • Yuste, M. P. &J. Gostincar. 1999. Handbook of agriculture. Marcel Dekker, New York.

    Google Scholar 

  • Zacheo, G. &T. Bleve-Zacheo. 1988. Involvement of Superoxide dismutases and Superoxide radicals in the susceptibility and resistance of tomato plants toMeloidogyne incognita attack. Physiol. & Molec. Pl. Pathol. 32: 313–322.

    Article  CAS  Google Scholar 

  • —. 1983. Mitochondrial peroxidase and Superoxide dismutase activities during the infection byMeloidogyne incognita of susceptible and resistant tomato plants. Nematol. Medit. 11: 107–114.

    Google Scholar 

  • Zhang, J. &M. B. Kirkham. 1995. Enzymatic responses of the ascorbate-glutathione cycle to drought in the sorghum and sunflower plants. Pl. Sci. 113: 139–147.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant Biology Faculty of Sciences, University of Granada, 18071, Granada, Spain

    Pablo C. Garcia, Rosa M. Rivero, Juan M. Ruiz & Luis Romero

Authors
  1. Pablo C. Garcia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rosa M. Rivero
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juan M. Ruiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luis Romero
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Garcia, P.C., Rivero, R.M., Ruiz, J.M. et al. The role of fungicides in the physiology of higher plants: Implications for defense responses. Bot. Rev 69, 162–172 (2003). https://doi.org/10.1663/0006-8101(2003)069[0162:TROFIT]2.0.CO;2

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1663/0006-8101(2003)069[0162:TROFIT]2.0.CO;2

Keywords

Search

Navigation