Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-23T09:12:43.580Z Has data issue: false hasContentIssue false

Practical application of induced resistance to plant diseases: an appraisal of effectiveness under field conditions

Published online by Cambridge University Press:  23 June 2009

D. R. WALTERS*
Affiliation:
Crop and Soil Systems Research Group, Scottish Agricultural College, King's Buildings, West Mains Road, EdinburghEH9 3JG, UK
J. M. FOUNTAINE
Affiliation:
Crop and Soil Systems Research Group, Scottish Agricultural College, King's Buildings, West Mains Road, EdinburghEH9 3JG, UK
*
*To whom all correspondence should be addressed. Email: dale.walters@sac.ac.uk

Summary

Plants resist pathogen attack through a combination of constitutive and inducible defences. Different types of induced resistance have been defined based on differences in signalling pathways and spectra of effectiveness. Systemic acquired resistance (SAR) occurs in distal plant parts following localized infection by a necrotizing pathogen. It is controlled by a signalling pathway that depends upon the accumulation of salicylic acid (SA) and the regulatory protein NPR1. In contrast, induced systemic resistance (ISR) is promoted by selected strains of non-pathogenic plant growth-promoting rhizobacteria (PGPR). ISR functions independently of SA, but requires NPR1 and is regulated by jasmonic acid (JA) and ethylene (ET).

Resistance can be induced by treatment with a variety of biotic and abiotic inducers. The resistance induced is broad spectrum and can be long-lasting, but is rarely complete, with most inducing agents providing between 0·20 and 0·85 disease control. In the field, expression of induced resistance is likely to be influenced by the environment, genotype, crop nutrition and the extent to which plants are already induced. Unfortunately, understanding of the impact of these influences on the expression of induced resistance is rudimentary. So too is understanding of how best to use induced resistance in practical crop protection. This situation will need to change if induced resistance is to fulfil its potential in crop protection.

Type
Review
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ajlan, A. M. & Potter, D. A. (1992). Lack of effect of tobacco mosaic virus-induced systemic acquired resistance on arthropod herbivores in tobacco. Phytopathology 82, 647651.CrossRefGoogle Scholar
Altamiranda, E. A. G., Andreu, A. B., Daleo, G. R. & Olivieri, F. P. (2008). Effect of β-aminobutyric acid (BABA) on protection against Phytophthora infestans throughout the potato crop cycle. Australasian Plant Pathology 37, 421427.CrossRefGoogle Scholar
Andreu, A. B., Guevara, M. G., Wolski, E. A., Daleo, G. R. & Caldiz, D. O. (2006). Enhancement of natural disease resistance in potatoes by chemicals. Pest Management Science 62, 162170.Google Scholar
Bostock, R. M. (2005). Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annual Review of Phytopathology 43, 545580.Google Scholar
Carlen, C., Faby, R., Karjalainen, R., Pommier, J. J. & Steffek, R. (2004). Control of airborne diseases in strawberries with natural and synthetic elicitors. Acta Horticulturae 649, 237240.Google Scholar
Chen, L., Qian, J., Qu, S., Long, J., Yin, Q., Zhang, C., Wu, X., Sun, F., Wu, T., Hayes, M., Beer, S. V. & Dong, H. (2008 a). Identification of specific fragments of HpaGXooc, a harpin from Xanthomonas oryzae pv. oryzicola, that induce disease resistance and enhance growth in plants. Phytopathology 98, 781791.CrossRefGoogle ScholarPubMed
Chen, L., Zhang, S.-J., Zhang, S.-S., Qu, S., Ren, X., Long, J., Yin, Q., Qian, J., Sun, F., Zhang, C., Wang, L., Wu, X., Wu, T., Zhang, Z., Cheng, Z., Hayes, M., Beer, S. V. & Dong, H. (2008 b). A fragment of Xanthomonas oryzae pv. oryzicola Harpin HpaGXooc reduces disease and increases yield of rice in extensive grower plantings. Phytopathology 98, 792802.Google Scholar
Cipollini, D. (2002). Does competition magnify the fitness costs of induced resistance in Arabidopsis thaliana? A manipulative approach. Oecologia 131, 514520.CrossRefGoogle ScholarPubMed
Cole, D. L. (1999). The efficacy of acibenzolar-S-methyl, an inducer of systemic acquired resistance, against bacterial and fungal diseases of tobacco. Crop Protection 18, 267273.Google Scholar
Cruickshank, I. A. M. & Mandryk, M. (1960). The effect of stem infection of tobacco with Peronospora tabacina on foliage reaction to blue mold. Journal of the Australian Institute of Agricultural Research 26, 369372.Google Scholar
Csinos, A. S., Pappu, H. R., McPherson, R. M. & Stephenson, M. G. (2001). Management of Tomato spotted wilt virus in flue-cured tobacco with acibenzolar-S-methyl and imidacloprid. Plant Disease 85, 292296.Google Scholar
da Rocha, A. B. & Hammerschmidt, R. (2005). History and perspectives on the use of disease resistance inducers in horticultural crops. HortTechnology 15, 518529.Google Scholar
Daayf, F., Schmitt, A. & Belanger, R. R. (1995). The effects of plant extracts of Reynoutria sachalinensis on powdery mildew development and leaf physiology of long English cucumber. Plant Disease 79, 577580.Google Scholar
Dann, E., Diers, B., Byrum, J. & Hammerschmidt, R. (1998). Effect of treating soybean with 2,6-dichloroisonicotinic acid (INA) and benzothiadiazole (BTH) on seed yields and the level of disease caused by Sclerotinia sclerotiorum in field and greenhouse studies. European Journal of Plant Pathology 104, 271278.Google Scholar
de Capdeville, G., Beer, S. V., Watkins, C. B., Wilson, C. L., Tedeschi, L. O. & Aist, J. R. (2003). Pre- and post-harvest harpin treatments of apples induce resistance to blue mold. Plant Disease 87, 3944.CrossRefGoogle ScholarPubMed
De Vos, M., Van Oosten, V. R., Van Poecke, R. M. P., Van Pelt, J. A., Pozo, M. J., Mueller, M. J., Buchala, A. J., Metraux, J.-P., Van Loon, L. C., Dicke, M. & Pieterse, C. M. J. (2005). Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Molecular Plant-Microbe Interactions 18, 923937.Google Scholar
Dietrich, R., Ploss, K. & Heil, M. (2004). Constitutive and induced resistance to pathogens in Arabidopsis thaliana depends on nitrogen supply. Plant, Cell and Environment 27, 896906.Google Scholar
Dietrich, R., Ploss, K. & Heil, M. (2005). Growth responses and fitness costs after induction of pathogen resistance depend on environmental conditions. Plant, Cell and Environment 28, 211222.CrossRefGoogle Scholar
Durrant, W. E. & Dong, X. (2004). Systemic acquired resistance. Annual Review of Phytopathology 42, 185209.Google Scholar
Fofana, B., McNally, D. J., Labbe, C., Boulanger, R., Benhamou, N., Seguin, A. & Belanger, R. R. (2002). Milsana-induced resistance in powdery mildew-infected cucumber plants correlates with the induction of chalcone synthase and chalcone isomerase. Physiological and Molecular Plant Pathology 61, 121132.Google Scholar
Gaffney, T., Friedrich, L., Vernooij, B., Nye, G., Uknes, S., Ward, E., Kessman, H. & Ryals, J. (1993). Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261, 754756.Google Scholar
Glazebrook, J., Chen, W., Estes, B., Chang, H.-S., Nawrath, C., Metraux, J.-P., Zhu, T. & Katagiri, F. (2003). Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant Journal 34, 217228.Google Scholar
Goellner, K. & Conrath, U. (2008). Priming: it's all the world to induced disease resistance. European Journal of Plant Pathology 121, 233242.CrossRefGoogle Scholar
Gorlach, J., Volrath, S., Knauf-Beiter, G., Hengy, G., Beckhove, U., Kogel, K.-H., Oostendorp, M., Staub, T., Ward, E., Kessmann, H. & Ryals, J. (1996). Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8, 629643.Google Scholar
Graham, J. H. & Leite, R. P. Jr ( 2004). Lack of control of citrus canker by induced systemic resistance compounds. Plant Disease 88, 745750.Google Scholar
Hadwiger, L. A. (1999). Host–parasite interactions: elicitation of defense responses in plants with chitosan. In Chitin and Chitinases (Eds Jolles, P. & Muzzarelli, R. A. A.), pp. 185200. Switzerland: Birkhauser Verlag.Google Scholar
Hammerschmidt, R. (1999). Induced disease resistance: how do induced plants stop pathogens? Physiological and Molecular Plant Pathology 55, 7784.Google Scholar
Hammerschmidt, R. (2007). Introduction: definitions and some history. In Induced Resistance for Plant Defence: A Sustainable Approach to Crop Protection (Eds Walters, D., Newton, A. & Lyon, G.), pp. 18. Oxford, UK: Blackwell Publishing.Google Scholar
Harish, S., Kavino, M., Kumar, N., Saravanakumar, D., Soorianathasundaram, K. & Samiyappan, R. (2008). Biohardening with plant growth promoting rhizosphere and endophytic bacteria induces systemic resistance against banana bunchy top virus. Applied Soil Ecology 39, 187200.Google Scholar
Hatcher, P. E. & Paul, N. D. (2000). Beetle grazing reduces natural infection of Rumex obtusifolius by fungal pathogens. New Phytologist 146, 325333.CrossRefGoogle ScholarPubMed
Heil, M. (2001). Induced systemic resistance (ISR) against pathogens – a promising field for ecological research. Perspectives in Plant Ecology, Evolution and Systematics 4, 6579.Google Scholar
Heil, M. (2002). Ecological costs of induced resistance. Current Opinion in Plant Biology 5, 345350.Google Scholar
Heil, M. & Baldwin, I. T. (2002). Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends in Plant Science 7, 6167.Google Scholar
Heil, M. & Ploss, K. (2006). Induced resistance enzymes in wild plants – do ‘early birds’ escape from pathogen attack? Naturwissenschaften 93, 455460.Google Scholar
Heil, M., Hilpert, A., Kaiser, W. & Linsenmair, K. E. (2000). Reduced growth and seed set following chemical induction of pathogen defence: does systemic acquired resistance (SAR) incur allocation costs? Journal of Ecology 88, 645654.Google Scholar
Heo, K. R., Lee, K. Y., Lee, S. H., Jung, S. J., Lee, S. W. & Moon, B. J. (2008). Control of crisphead lettuce damping-off and bottom rot by seed coating with alginate and Pseudomonas aeruginosa LY-11. Plant Pathology Journal 24, 6773.Google Scholar
Herman, M. A. B., Restrepo, S. & Smart, C. D. (2007). Defense gene expression patterns of three SAR-induced tomato cultivars in the field. Physiological and Molecular Plant Pathology 71, 192200.Google Scholar
Herms, D. A. & Mattson, W. J. (1992). The dilemma of plants: to grow or to defend. Quarterly Review of Biology 67, 283335.Google Scholar
Hijwegen, T. & Verhaar, M. A. (1994). Effects of cucumber genotype on the induction of resistance to powdery mildew, Sphaerotheca fuliginea, by 2,6-dichloroisonicotinic acid. Plant Pathology 44, 756762.Google Scholar
Huth, W. & Balke, K. (2002). Bion® – without effect on the development of BYDV infected plants of winter barley. Journal of Plant Diseases and Protection 109, 286290.Google Scholar
Inbar, M., Doostdar, H., Sonoda, R. M., Leibee, G. L. & Mayer, R. T. (1998). Elicitors of plant defensive systems reduce insect densities and disease incidence. Journal of Chemical Ecology 24, 135149.Google Scholar
Iriti, M. & Faoro, F. (2003). Does benzothiadiazole-induced resistance increase fitness cost in bean? Journal of Plant Pathology 85, 265270.Google Scholar
Ishii, H. (2008). Fungicide research in Japan – an overview. In Modern Fungicides and Antifungal Compounds V. Proceedings of the 15th International Reinhardsbrunn Symposium on Modern Fungicides and Antifungal Compounds, 2007 (Eds Dehne, H. W., Deising, H. B., Gisi, U., Kuck, K. H., Russell, P. E. & Lyr, H.), pp. 1117. Braunschweig, Germany: The German Phytomedical Society (DPG).Google Scholar
Iwata, M. (2001). Probenazole – a plant defence activator. Pesticide Outlook 12, 2831.Google Scholar
Iwata, M., Suzuki, Y., Watanabe, T., Mase, S. & Sekizawa, Y. (1980). Effect of probenazole on the activities of enzymes related to the resistant reaction in rice plant. Annals of the Phytopathological Society of Japan 46, 297306.Google Scholar
Jakab, G., Cottier, V., Toquin, V., Rigoli, G., Zimmerli, L., Metraux, J.-P. & Mauch-Mani, B. (2001). β-aminobutyric acid-induced resistance in plants. European Journal of Plant Pathology 107, 2937.Google Scholar
Jetiyanon, K., Fowler, W. D. & Kloepper, J. W. (2003). Broad-spectrum protection against several pathogens by PGPR mixtures under field conditions in Thailand. Plant Disease 87, 13901394.Google Scholar
Kang, S. H., Cho, H. S., Cheong, H., Ryu, C. M., Kim, J. F. & Park, S. H. (2007). Two bacterial endophytes eliciting both plant growth promotion and plant defense on pepper (Capsicum annuum L.). Journal of Microbiology and Biotechnology 17, 96103.Google Scholar
Katz, V. A., Thulke, O. U. & Conrath, U. (1998). A benzothiadiazole primes parsley cells for augmented elicitation of defence responses. Plant Physiology 117, 13331339.Google Scholar
Kohler, A., Schwindling, S. & Conrath, U. (2002). Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiology 128, 10461056.Google Scholar
Konstantinidou-Doltsinis, S., Markellou, E., Kasselaki, A.-M., Fanouraki, M. N., Koumakis, C. M., Schmitt, A., Liopa-Tsakalidis, A. & Malathrakis, N. E. (2006). Efficacy of Milsana®, a formulated plant extract from Reynoutria sachalinensis, against powdery mildew of tomato (Leveillula taurica). Biocontrol 51, 375392.Google Scholar
Konstantinidou-Doltsinis, S., Markellou, E., Kasselaki, A. M., Siranidou, E., Kalamarakis, A., Tzembelikou, K., Schmitt, A., Koumakis, C. & Malathrakis, N. E. (2007). Control of powdery mildew of grape in Greece using Sporodex® L and Milsana®. Journal of Plant Diseases and Protection 114, 256262.Google Scholar
Kosaka, H., Aikawa, T., Ogura, N., Tabata, K. & Kiyohara, T. (2001). Pine wilt disease caused by the pine wood nematode: the induced resistance of pine trees by the avirulent isolates of nematode. European Journal of Plant Pathology 107, 667675.Google Scholar
Kuć, J. (1982). Induced immunity to plant disease. Bioscience 32, 854860.Google Scholar
Latunde-Dada, A. O. & Lucas, J. A. (2001). The plant defence activator acibenzolar-S-methyl primes cowpea [Vigna unguiculata (L.) Walp.] seedlings for rapid induction of resistance. Physiological and Molecular Plant Pathology 58, 199208.CrossRefGoogle Scholar
Lawton, K., Weymann, K., Friederich, L., Vernooij, B., Uknes, S. & Ryals, J. A. (1995). Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Molecular Plant-Microbe Interactions 8, 863870.Google Scholar
Lian, B., Zhou, X., Miransari, M. & Smith, D. L. (2000). Effects of salicylic acid on the development and root nodulation of soybean seedlings. Journal of Agronomy and Crop Science 185, 187192.CrossRefGoogle Scholar
Liu, S. Y., Liu, Z., Fitt, B. D. L., Evans, N., Foster, S. J., Huang, Y. J., Latunde-Dada, A. O. & Lucas, J. A. (2006). Resistance to Leptosphaeria maculans (phoma stem canker) in Brassica napus (oilseed rape) induced by L. biglobosa and chemical defence activators in field and controlled environments. Plant Pathology 55, 401412.Google Scholar
Lyon, G. (2007). Agents that can elicit induced resistance. In Induced Resistance for Plant Disease Control: a Sustainable Approach to Crop Protection (Eds Walters, D., Newton, A. & Lyon, G.), pp. 929. Oxford, UK: Blackwell Publishing.CrossRefGoogle Scholar
Martenelli, J. A., Brown, J. K. M. & Wolfe, M. S. (1993). Effects of barley genotype on induced resistance to powdery mildew. Plant Pathology 42, 195202.Google Scholar
Martínez-Abarca, F., Herrera-Cervera, J. A., Bueno, P., Sanjuan, J., Bisseling, T. & Olivares, J. (1998). Involvement of salicylic acid in the establishment of the Rhizobium meliloti-alfalfa symbiosis. Molecular Plant-Microbe Interactions 11, 153155.Google Scholar
Meszka, B. & Bielenin, A. (2004). Possibilities of integrated grey mould control on strawberry plantations in Poland. Bulletin OILB/SROP 27, 4145.Google Scholar
Murray, D. C. & Walters, D. R. (1992). Increased photosynthesis and resistance to rust infection in upper, uninfected leaves of rusted broad bean (Vicia faba L.). New Phytologist 120, 235242.CrossRefGoogle Scholar
Niki, T., Mitsuhara, I., Seo, S., Ohtsubo, N. & Ohashi, Y. (1998). Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant and Cell Physiology 39, 500507.CrossRefGoogle Scholar
Oerke, E. C., Steiner, U. & Schonbeck, F. (1989). Zur Wirksamkeit der induzierten Resistenz unter praktischen Anbaubedingungen. V. Mehltaubefall und Ertag von Winter- und Sommergerste in Abhangigkeit von der Stickstoffdungung. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz 96, 140153.Google Scholar
Ogallo, J. L. & McClure, M. A. (1996). Systemic acquired resistance and susceptibility to root-knot nematodes in tomato. Phytopathology 86, 498501.Google Scholar
Pasquer, F., Isidore, E., Zarn, J. & Keller, B. (2005). Specific patterns of changes in wheat gene expression after treatment with three antifungal compounds. Plant Molecular Biology 57, 693707.CrossRefGoogle ScholarPubMed
Paterson, L., Walsh, D. J. & Walters, D. R. (2008). Effect of resistance elicitors on Rhynchosporium secalis infection of barley. In Proceedings Crop Protection in Northern Britain 2008, Dundee, Scotland, 26th–27th February 2008, pp. 163168. Dundee, UK: The Association for Crop Protection in Northern Britain.Google Scholar
Perez, L., Rodriguez, M. E., Rodriguez, F. & Roson, C. (2003). Efficacy of acibenzolar-S-methyl, an inducer of systemic acquired resistance, against tobacco blue mold caused by Peronospora hyoscyami f. sp. tabacina. Crop Protection 22, 405413.CrossRefGoogle Scholar
Pernezny, K., Stoffella, P., Collins, J., Carroll, A. & Beaney, A. (2002). Control of target spot of tomato with fungicides, systemic acquired resistance activators, and a biocontrol agent. Plant Protection Science 38, 8188.Google Scholar
Pieterse, C. M. J. & Van Loon, L. C. (2007). Signalling cascades involved in induced resistance. In Induced Resistance for Plant Defence: A Sustainable Approach to Crop Protection (Eds Walters, D., Newton, A. & Lyon, G.), pp. 6588. Oxford, UK: Blackwell Publishing.Google Scholar
Plessl, M., Heller, W., Payer, H. D., Elstner, E. F., Habermeyer, J. & Heiser, I. (2005). Growth parameters and resistance against Drechslera teres of spring barley (Hordeum vulgare L. cv. Scarlett) grown at elevated ozone and carbon dioxide concentrations. Plant Biology 7, 694705.Google Scholar
Pozo, M. J. & Azcón-Aguilar, C. (2007). Unravelling mycorrhiza-induced resistance. Current Opinion in Plant Biology 10, 393398.Google Scholar
Prats, E., Rubiales, D. & Jorrin, J. (2002). Acibenzolar-S-methyl-induced resistance to sunflower rust (Puccinia helianthi) is associated with an enhancement of coumarins on foliar surface. Physiological and Molecular Plant Pathology 60, 155162.Google Scholar
Ramamoorthy, V., Viswanathan, R., Raguchander, T., Prakasam, V. & Samiyappan, R. (2001). Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop Protection 20, 111.Google Scholar
Ramanujam, M. P., Abdul Jaleel, V. & Kumara Velu, G. (1998). Effect of salicylic acid on nodulation, nitrogenous compounds and related enzymes of Vigna mungo. Biologia Plantarum 41, 307311.Google Scholar
Raupach, G. S. & Kloepper, J. W. (2000). Biocontrol of cucumber diseases in the field by plant growth promoting rhizobacteria with and without methyl bromide fumigation. Plant Disease 84, 10731075.Google Scholar
Reglinski, T., Lyon, G. D. & Newton, A. C. (1994). Assessment of the ability of yeast-derived elicitors to control barley powdery mildew in the field. Journal of Plant Diseases and Protection 101, 110.Google Scholar
Reglinski, T., Dann, E. & Deverall, B. (2007). Integration of induced resistance in crop production. In Induced Resistance for Plant Defence: a Sustainable Approach to Crop Protection (Eds Walters, D., Newton, A. & Lyon, G.), pp. 201228. Oxford, UK: Blackwell Publishing.Google Scholar
Resende, M. L. V., Nojosa, G. B. A., Cavalcanti, L. S., Aguilar, M. A. G., Silva, L. H. C. P., Perez, J. O., Andrade, G. C. G., Carvalho, G. A. & Castro, R. M. (2002). Induction of resistance in cocoa against Crinipellis perniciosa and Verticillium dahliae by acibenzolar-S-methyl (ASM). Plant Pathology 51, 621628.Google Scholar
Reuveni, M., Zahavi, T. & Cohen, Y. (2001). Controlling downy mildew (Plasmopara viticola) in field-grown grapevine with beta-aminobutyric acid (BABA). Phytoparasitica 29, 125133.Google Scholar
Ross, A. F. (1961 a). Localized acquired resistance to plant virus infection in hypersensitive hosts. Virology 14, 329339.Google Scholar
Ross, A. F. (1961 b). Systemic acquired resistance induced by localized virus infection in plants. Virology 14, 340358.Google Scholar
Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H. Y. & Hunt, M. D. (1996). Systemic acquired resistance. Plant Cell 8, 18091819.Google Scholar
Schilder, A. M. C., Gillet, J. M., Sysak, R. W. & Wise, J. C. (2002). Evaluation of environmentally friendly products for control of fungal diseases of grapes. In Proceedings of the 10th International Conference on Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing and Viticulture, Weinsberg, Germany, 4–7 February 2002, pp. 163167.Google Scholar
Schmitt, A., Kunz, S., Nandi, S., Seddon, B. & Ernst, A. (2002). Use of Reynoutria sachalinensis plant extracts, clay preparations and Brevibacillus brevis against fungal diseases of grape berries. In Proceedings of the 10th International Conference on Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing and Viticulture, 4–7 February. Weinsberg, Germany, pp. 146151.Google Scholar
Shah, J., Tsui, F. & Klessig, D. F. (1997). Characterization of a salicylic acid-insensitive mutant (sai 1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Molecular Plant-Microbe Interactions 10, 6978.Google Scholar
Sharathchandra, R. G., Niranjan Raj, S., Shetty, N. P., Amruthesh, K. N. & Shekar Shetty, H. (2004). A chitosan formulation Elexa induces downy mildew disease resistance and growth promotion in pearl millet. Crop Protection 23, 881888.Google Scholar
Siegrist, J., Muhlenbeck, S. & Buchenauer, H. (1998). Cultured parsley cells, a model system for the rapid testing of abiotic and natural substances as inducers of systemic acquired resistance. Physiological and Molecular Plant Pathology 53, 223238.Google Scholar
Smedegaard-Petersen, V. & Stolen, O. (1981). Effect of energy requiring defense reactions on yield and grain quality in powdery mildew Erysiphe graminis sp. hordei resistant Hordeum vulgare cultivar Sultan. Phytopathology 71, 396399.CrossRefGoogle Scholar
Somssich, I. E. & Hahlbrock, K. (1998). Pathogen defence in plants – a paradigm of biological complexity. Trends in Plant Science 3, 8690.Google Scholar
Sonnemann, I., Finkhaeuser, K. & Wolters, V. (2002). Does induced resistance in plants affect the belowground community? Applied Soil Ecology 21, 179185.CrossRefGoogle Scholar
Sonnemann, I., Streicher, N. M. & Wolters, V. (2005). Root associated organisms modify the effectiveness of chemically induced resistance in barley. Soil Biology and Biochemistry 37, 18371842.CrossRefGoogle Scholar
Sparla, F., Rotino, L., Valgimigli, M. C., Pupillo, P. & Trost, P. (2004). Systemic resistance induced by benzothiadiazole in pear inoculated with the agent of fire blight (Erwinia amylovora). Scientia Horticulturae 101, 269279.Google Scholar
Stadnik, M. J. & Buchenauer, H. (1999). Control of wheat diseases by a benzothiadiazole-derivative and modern fungicides. Journal of Plant Disease and Protection 106, 466475.Google Scholar
Steiner, U., Oerke, E. C. & Schonbeck, F. (1988). Zur Wirksamkeit der induzierten Resistenz unter praktischen Anbaubedingungen. IV. Befall und Ertag von Wintergertsensorten mit induzierter Resistenz und nach Fungizibehandlung. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz 95, 506517.Google Scholar
Stout, M. J., Fidantsef, A. L., Duffey, S. S. & Bostock, R. M. (1999). Signal Interactions in pathogen and insect attack: systemic plant-mediated interactions between pathogens and herbivores of the tomato, Lycopersicon esculentum. Physiological and Molecular Plant Pathology 54, 115130.Google Scholar
Thaler, J. S., Fidantsef, A. L., Duffey, S. S. & Bostock, R. M. (1999). Trade-offs in plant defense against pathogens and herbivores: a field demonstration of chemical elicitors of induced resistance. Journal of Chemical Ecology 25, 15971609.CrossRefGoogle Scholar
Thaler, J. S., Fidantsef, A. L. & Bostock, R. M. (2002). Antagonism between jasmonate- and salicylate-mediated induced plant resistance: effects of concentration and timing of elicitation on defense-related proteins, herbivore, and pathogen performance in tomato. Journal of Chemical Ecology 28, 11311159.CrossRefGoogle ScholarPubMed
Ton, J. & Mauch-Mani, B. (2004). β-aminobutyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant Journal 38, 119130.Google Scholar
Ton, J., Pieterse, C. M. J. & Van Loon, L. C. (1999). Identification of a locus in Arabidopsis controlling both the expression of rhizobacteria-mediated induced systemic resistance (ISR) and basal resistance against Pseudomonas syringae pv. tomato. Molecular Plant-Microbe Interactions 12, 911918.Google Scholar
Ton, J., Davison, S., Van Wees, S. C. M., Van Loon, L. C. & Pieterse, C. M. J. (2001). The Arabidopsis ISR1 locus controlling rhizobacteria-mediated induced systemic resistance is involved in ethylene signalling. Plant Physiology 125, 652661.Google Scholar
Ton, J., Jakab, G., Toquin, V., Flors, V., Iavicoli, A., Maeder, M. N., Metraux, J.-P. & Mauch-Mani, B. (2005). Dissecting the β-aminobutyric acid induced priming phenomenon in Arabidopsis. The Plant Cell 17, 987999.Google Scholar
Vallad, G. E. & Goodman, R. M. (2004). Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Science 44, 19201934.CrossRefGoogle Scholar
van Hulten, M., Pelser, M., Van Loon, L. C., Pieterse, C. M. J. & Ton, J. (2006). Costs and benefits of priming for defense in Arabidopsis. Proceedings of the National Academy of Sciences, USA 103, 56025607.Google Scholar
Van Wees, S. C. M., Pieterse, C. M. J., Trijssenaar, A., Van't Westende, Y. A. M., Hartog, F. & Van Loon, L. C. (1997). Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Molecular Plant-Microbe Interactions 6, 716724.Google Scholar
Waller, F., Achatz, B., Baltruschat, H., Fodor, J., Becker, K., Fischer, M., Heier, T., Huckelhoven, R., Neumann, C., von Wettstein, D., Franken, P. & Kogel, K.-H. (2005). The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proceedings of the National Academy of Sciences, USA 102, 1338613391.Google Scholar
Walters, D. & Heil, M. (2007). Costs and trade-offs associated with induced resistance. Physiological and Molecular Plant Pathology 71, 317.CrossRefGoogle Scholar
Walters, D., Walsh, D., Newton, A. & Lyon, G. (2005). Induced resistance for plant disease control: Maximizing the efficacy of resistance elicitors. Phytopathology 95, 13681373.Google Scholar
Walters, D. R., Cowley, T. & Weber, H. (2006). Rapid accumulation of trihydroxyoxylipins and resistance to the bean rust pathogen Uromyces fabae following wounding in Vicia faba. Annals of Botany 97, 779784.Google Scholar
Watanabe, T. (1977). Effect of probenazole (oryzemate) on each stage of rice blast fungus (Pyricularia oryzae Cavara) in its life cycle. Journal of Pesticide Science 2, 395404.Google Scholar
Watanabe, T., Igarashi, H., Matsumoto, K., Seki, S., Mase, S. & Sekizawa, Y. (1977). The characteristics of probenazole (oryzemate) for the control of rice blast. Journal of Pesticide Science 2, 291296.CrossRefGoogle Scholar
Wei, Z. M., Laby, R. J., Zumoff, C. H., Bauer, D. W., He, S. Y., Collmer, A. & Beer, S. V. (1992). Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257, 8588.Google Scholar
Wei, G., Yao, G. W., Zehnder, S., Tuzun, S. & Kloepper, J. W. (1995). Induced systemic resistance by select plant growth promoting rhizobacteria against bacterial wilt of cucumber and the beetle vectors. Phytopathology 85, 1154.Google Scholar
Wei, G., Kloepper, J. W. & Tuzun, S. (1996). Induced systemic resistance to cucumber diseases and increased plant growth by plant growth promoting rhizobacteria under field conditions. Phytopathology 86, 221224.Google Scholar
Wiese, J., Kranz, T. & Schubert, S. (2004). Induction of pathogen resistance in barley by abiotic stress. Plant Biology 6, 529536.Google Scholar
Zavala, J. A., Patankar, A. G., Gase, K., Hui, D. Q. & Baldwin, I. T. (2004). Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiology 134, 11811190.Google Scholar
Zehnder, G. W., Murphy, J. F., Sikora, E. J. & Kloepper, J. W. (2001). Application of rhizobacteria for induced resistance. European Journal of Plant Pathology 107, 3950.CrossRefGoogle Scholar
Zhang, S., Reddy, M. S., Kokalis-Burelle, N., Wells, L. W., Nightengale, S. P. & Kloepper, J. W. (2001). Lack of induced systemic resistance in peanut to late leaf spot disease by plant growth-promoting rhizobacteria and chemical elicitors. Plant Disease 85, 879884.Google Scholar
Ziadi, S., Barbedette, S., Godard, J. F., Monot, C., Le Corre, D. & Silue, D. (2001). Production of pathogenesis-related proteins in the cauliflower (Brassica oleracea var. botrytis)-downy mildew (Peronospora parasitica) pathosystem treated with acibenzolar-S-methyl. Plant Pathology 50, 579586.CrossRefGoogle Scholar
Zimmerli, L., Jakab, G., Métraux, J.-P. & Mauch-Mani, B. (2000). Potentiation of pathogen-specific defense mechanisms in Arabidopsis by beta-aminobutyric acid. Proceedings of the National Academy of Sciences, USA 97, 1292012925.Google Scholar
Zimmerli, L., Metraux, J.-P. & Mauch-Mani, B. (2001). β-aminobutyric acid-induced protection of Arabidopsis against the necrotrophic pathogen Botrytis cinerea. Plant Physiology 126, 517523.CrossRefGoogle Scholar