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Systemic acquired resistance and induced systemic resistance in conventional agriculture.

Plant Researchers have known for over 100 yr that plants can be preconditioned against diseases caused by a variety of parasites. Initially, the debate was over the serological basis of what was then referred to as acquired physiological immunity (reviewed in Chester, 1933a, 1933b). It would take another 60 yr before Ross (1961a, 1961b), from results of experiments using Tobacco mosaic virus to sensitize tobacco (Nicotiana tabacum L.) against subsequent "challenge" inoculations of Tobacco mosaic virus on infected leaves or on distal uninfected leaves, would clearly articulate the concepts of localized acquired resistance and SAR, respectively. Cruikshank and Mandryk (1960) extended this concept to a nonviral pathogen in field-grown tobacco plants using stem injections of Peronospora tabacina (D.B. Adam, also referred to as P. hyoscyami de Bary f. sp. tabacina) to trigger SAR against subsequent inoculations of the same pathogen, the causative agent of blue mold of tobacco. These landmark studies led to the development of the classic SAR models during the 1980s in other plants, such as cucumber (Cucumis sativus L.), common bean (Phaseolus vulgaris L.), rice (Oryza sativa L.), and Arabidopsis thaliana (L.) Heynh., demonstrating that SAR was conserved across diverse plant families and was effective against a broad range of viral, bacterial, and fungal pathogens (reviewed in Sticher et al., 1997).

Additional interests in the biological control of soil-borne diseases of plants led to the serendipitous discovery of another form of induced resistance associated with the colonization of plant roots by certain plant growth promoting rhizobacteria (PGPR), referred to as induced systemic resistance (ISR) (reviewed in van Loon et al., 1998). ISR is distinct from SAR in several key physiological and biochemical phenotypes that are best defined in A. thaliana (Knoester et al., 1999; Pieterse et al., 1996, 1998; Ton et al., 1999, 2001; van Wees et al., 1997). Results of lab and field studies show that, like SAR, ISR is effective against a broad range of diseases caused by viruses, bacteria, and fungi (Murphy et al., 2000; Nandakumar et al., 2001; Niranjan Raj et al., 2003; Raupach and Kloepper, 1998, 2000; van Loon et al., 1998; Wei et al., 1996; Zehnder et al., 2001).

Over the last 20 yr, research on SAR and ISR using model systems has furthered our understanding of the molecular basis of induced resistance and promoted the development of synthetic elicitors and PGPR formulations for use in conventional agriculture (see reviews by Benhamou and Nicole, 1999; Hammerschmidt and Kuc, 1995; Kessler and Baldwin, 2002; Kessmann et al., 1994; Leroux, 1996; Lucas, 1999; Lyon et al., 1995; Sticher et al., 1997; van Loon et al., 1998; Walling, 2000). The future use of SAR and ISR to control crop pests in conventional agriculture seems promising. Since synthetic elicitors and PGPR strains, in general, do not exhibit any direct antimicrobial activity, unlike traditional pesticides, they provide a way to control disease without asserting direct selective pressure on pathogen populations. In addition, the use of synthetic elicitors and PGPR strains seems to be environmentally benign relative to current pesticides. These characteristics make SAR and ISR, and other forms of induced resistance, an attractive approach for managing crop pests in a sustainable manner within the scope of a conventional agriculture system.

Systemic Acquired Resistance and Induced Systemic Resistance

Induced resistance is a physiological "state of enhanced defensive capacity" elicited by specific environmental stimuli, whereby the plant's innate defenses are potentiated against subsequent biotic challenges (van Loon et al., 1998). This enhanced state of resistance is effective against a broad range of pathogens and parasites, including fungi, bacteria, viruses, nematodes, parasitic plants, and even insect herbivores (Benhamou and Nicole, 1999; Hammerschmidt and Kuc, 1995; Kessler and Baldwin, 2002; McDowell and Dangl, 2000; Sticher et al., 1997; van Loon et al., 1998; Walling, 2000). The two most clearly defined forms of induced resistance are SAR and ISR (Fig. 1), which can be differentiated on the basis of the nature of the elicitor and the regulatory pathways involved, as demonstrated in model plant systems (Knoester et al., 1999; Maleck et al., 2000; Pieterse et al., 1996, 1998; Schenk et al., 2000; Uknes et al., 1992; van Wees et al., 2000; Ward et al., 1991, Yan et al., 2002).

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The classic form of SAR can be triggered by exposing the plant to virulent, avirulent, and nonpathogenic microbes, or artificially with chemicals such as salicylic acid, 2,6-dichloro-isonicotinic acid (INA) or benzo (1,2,3) thiadiazole-7-carbothioic acid S-methyl ester (BTH) (reviewed in Sticher et al., 1997). Depending on the plant and elicitor, a set period of time is required for the establishment of SAR that corresponds to the time required for the coordinated accumulation of pathogenesis-related proteins (and transcripts) and salicylic acid throughout the plant (Cameron et al., 1994; Uknes et al., 1992; Ward et al., 1991). Any disruption in the plant's ability to accumulate salicylic acid results in the loss of pathogenesis-related gene expression and attenuation of the SAR response, when pathogens are used for induction (Gaffney et al., 1993; Lawton et al., 1995; Vernooij et al., 1994). BTH and INA, however, were still able to elicit SAR and pathogenesis-related gene expression in A. thaliana and tobacco plants defective in salicylic acid accumulation (Friedrich et al., 1996; Lawton et al., 1996).

ISR is potentiated by plant growth-promoting rhizobacteria (PGPR), of which the best characterized are strains within several species of Pseudomonas that cause no visible damage to the plant's root system (reviewed in van Loon et al., 1998). Unlike SAR, ISR does not involve the accumulation of pathogenesis-related proteins or salicylic acid (Pieterse et al., 1996), but instead, relies on pathways regulated by jasmonate and ethylene (Knoester et al., 1999; Pieterse et al., 1998; Yan et al., 2002). However, these molecular characterizations are based on a limited number of ISR systems. Other examples of ISR are linked to the production of siderophores or salicylic acid by PGPR strains and, therefore, have more in common with SAR (De Meyer and Hofte, 1997; Leeman et al., 1995a, 1996; Maurhofer et al., 1994). Neither the nature of the eliciting agent nor the site of elicitor action on the plant is as critical in the classification of induced resistance phenomena as the biochemical responses incited within the plant. Finally, SAR is effective across a wide array of plant species, whereas there is demonstrated specificity in the ability of PGPR strains to elicit ISR on certain plant species and genotypes (van Wees et al., 1997; Yan et al., 2002).

It is important to realize that SAR and ISR, as just defined, are probably only two outcomes out of an array of possibilities. It is likely that other forms of induced resistance exist that vary in their reliance on salicylic acid, ethylene, and jasmonate and other as yet discovered plant regulators. However, it is the availability of chemical inducers of SAR, such as BTH, and the characterization of numerous PGPR strains, that makes the applied use of induced resistance in conventional agriculture a reality. The next two sections will review published studies assessing SAR and ISR under field conditions. These studies on SAR and ISR are also examined in further detail in Tables 1 and 2, respectively. The SAR studies examined in this review cover an assortment of crop-pest interactions, but are centered on the use of BTH and INA, where the mechanism of resistance has been well established in laboratory studies. On the other hand, for ISR, 21 different strains of bacteria were investigated in field studies, of which only two of the strains (Bacillus pumilus SE34 and Pseudomonas fluorescens 89B-61) were further studied to substantiate ISR as the mechanism (Yan et al., 2002). Other up-and-coming "technologies" exist for eliciting induced resistance, such as Messenger (Eden Bioscience Corp., Bothell, WA, USA) and Oxycom (Redox Chemicals, ID, USA; see Kim et al., 2001) not covered here because of the lack, or small number, of published field studies.

Field Studies on Systemic Acquired Resistance

BTH and INA are by far the best studied chemical elicitors available; both are considered functional analogs of salicylic acid, and elicit a systemic form of induced resistance across a broad range of plant-pathogen interactions (Friedrich et al., 1996; Lawton et al., 1996; Maleck et al., 2000; Uknes et al., 1992; Ward et al., 1991). In general, neither chemical elicitor exhibits any direct antimicrobial activity; however, some examples of antimicrobial activity have been documented in association with high elicitor concentrations (Ishii et al., 1999; Rohilla et al., 2002; Tosi and Zazzerini, 2000). Plants exposed to high concentrations of BTH or INA may also exhibit signs of phytotoxicity, but this effect seems to be independent of the induced resistance response (discussed in Louws et al., 2001; Sticher et al., 1997).

Out of the 37 crop disease examples examined in the following SAR section (summarized in Table 1), 32 examples used BTH covering 12 diverse crops, while the remaining five examples used INA. BTH [also known as acibenzolar-S-methyl] is distributed by Syngenta Crop Protection (Raleigh, NC, USA; formerly Novartis Crop Protection) as Actigard in the USA and as Bion in Europe. BTH was originally marketed as a means to control powdery mildew of wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.) in Europe (Gorlach et al., 1996).

Efficacy among the Monocots

Gorlach et al. (1996) reported successful control of powdery mildew, Septoria leaf spot (caused by Septoria spp.), and leaf rust [caused by P. recondita Roberge ex Desmaz. f. sp. tritici (Eriks. & E. Henn.) D.M. Henderson] of wheat in field trials. BTH was also effective against downy mildew of maize [caused by Peronoscleropora sorghi (W. Weston & Uppal) C.G. Shaw] in the field when applied as a seed treatment (Morris et al., 1998). Stadnik and Buchenauer (1999a, 1999b) reported success in field experiments with single applications of BTH for controlling powdery mildew of wheat, but had mixed results against Septoria leaf blotch (caused by Septoria tritici Roberge in Desmaz.). However, several fungicides were superior to BTH at controlling powdery mildew and Septoria leaf blotch in the field, and improving overall wheat yields. There was no improvement in the control of powdery mildew or Septoria leaf blotch of wheat with additional applications of BTH over single applications, or with combined applications of BTH with fungicides over lone fungicide applications, and no improvements in yield were associated with the use of BTH over nontreated controls in field trials (Stadnik and Buchenauer, 1999a, 1999b).

Efficacy among Solanaceous Crops

Ample evidence exists supporting the effectiveness of BTH against a variety of fungal, bacterial, and viral diseases of solanaceous plants in experiments under field conditions (Abbasi et al., 2002; Buonaurio et al., 2002; Csinos et al., 2001; Louws et al., 2001; Matheron and Porchas, 2002; Inbar et al., 1998; Perez et al., 2003; Romero et al., 2001; Thaler et al., 1999). The eliciting activity of BTH was quite effective against foliar diseases caused by bacterial pathogens. In a series of field experiments across the eastern USA, BTH applied at a rate of 35 g a.i./ha every 7 to 10 d was as effective at reducing the severity of bacterial spot [caused by Xanthomonas axonopodis pv. vesicatoria Vauterin et al. or X. campestris pv. vesicatoria (Doidge) Dye] and bacterial speck [caused by Pseudomonas syringae pv. tomato (Okabe) Young et al.] on foliage and fruit of tomato (Lycopersicon esculentum Mill.) as standard bacterization treatments that always included copper hydroxide (Louws et al., 2001). BTH was especially effective at controlling field epidemics of bacterial speck and spot when copper resistant strains of P. syringae pv. tomato and X. axonopodis pv. vesicatoria predominated (Louws et al., 2001). Similar control was obtained with repeated applications of BTH in pepper (Capsicum spp.) against bacterial spot (caused by X. campestris pv. vesicatoria) and in tobacco against wildfire [caused by P. syringae pv. tabaci (Wolf & Foster) Young et al.] (Buonaurio et al., 2002; Cole, 1999). In the field, tomato plants treated repeatedly with BTH carried reduced population densities of X. axonopodis pv. vesicatoria and P. syringae pv. tomato on leaves until 1 mo and 2 mo, respectively, when there were no differences in bacterial leaf populations relative to the controls, suggesting a resistance mechanism based on tolerance to the pathogen rather than exclusion or inhibition of bacterial growth (Louws et al., 2001). In field-grown tomatoes, BTH was found to increase the expression level of the pathogenesis-related gene, P4 (equivalent to PR-1 of tobacco and A. thaliana), extending findings from lab-based experiments to the field (Thaler et al., 1999).

On tobacco, BTH offered effective control against blue mold and against several fungal diseases such as frogeye leaf spot (caused by Cercospora nicotianae Ellis & Everh.), brown spot [caused by Alternaria alternata (Fr.:Fr.) Keissl.] and Rhizoctonia leaf spot (caused by Rhizoctonia solani Kuhn) (Csinos et al., 2001; Perez et al., 2003). Repeated applications of BTH also controlled early blight of tomato (caused by Alternaria solani Sorauer), while others found that BTH offered little protection against the combined effects of late blight [caused by Phytophthora infestans (Mont.) de Bary] and early blight of tomato, or against blackshank of tobacco [caused by Phytophthora parasitica Dastur var. nicotianae (Breda de Haan) Tucker] (Csinos et al., 2001; Inbar et al., 1998; Louws et al., 2001). Finally, BTH was also found to protect tobacco plants against the effects of the thrip-vectored Tomato spotted will virus in field-grown tobacco, as assessed by a reduction in the number of symptomatic plants (Csinos et al., 2001).

Efficacy among Leguminous Crops

Limited field experiments involving the effects of INA and BTH on diseases of legumes have been reported (Dann and Deverall, 1996; Dann et al., 1998). Reduced densities of uredinia of the rust fungus, Uromyces appendiculatus Unger, on trifoliolates of common bean were obtained when INA was applied at least 7 d before inoculation, but not at 2 h before inoculation (Dann and Deverall, 1996). An additional application of INA during pod-set did not improve resistance of common bean plants to U. appendiculatus, as opposed to a single application to the first trifoliolate (Dann and Deverall, 1996).

Repeated applications of INA to field-grown soybean [Glycine max (L.) Merr.] partially reduced symptoms of white mold [caused by Sclerotinia sclerotiorurn (Lib.) deBary] in two out of three field trials. INA was most efficacious in suppressing white mold on the susceptible cultivars Elgin 87 and Williams 82 but not on partially resistant cultivars Corsoy 79 or NKS19-90 (Dann et al., 1998). However, the reductions in white mold observed on cultivars Elgin 87 and Williams 82 varied with field location and year. The first of two field trials that included BTH found it most effective against white mold when applied to soybean cultivar Elgin 87, but was ineffective in a second field trial where a 10-fold higher dose of BTH was applied (Dann et al., 1998).

Efficacy on Fruit Trees, Cotton, and Spinach

Of particular interest is the reported control of several diseases of apple (Malus domestica Borkh.) and Japanese pear (Pyrus pyrifolia Nakai) with BTH in field trials (Ishii et al., 1999; Maxson-Stein et al., 2002). When applied to field grown Japanese pear trees, BTH controlled scab (caused by Venturia nashicola Tanaka & Yamamoto) and rust (caused by Gymnosporangium asiaticum Mayabe ex. Yamada) with multiple applications. Control of scab with BTH was equivalent to that observed with the fungicide, polycarbamate; however, this was not the case with rust where the control exhibited by BTH was not as effective as that with polycarbamate (Ishii et al., 1999). Weekly applications of BTH as a foliar spray effectively reduced the incidence and severity of fire blight [caused by Erwinia amylovora (Burrill 1882) Winslow et al., 1920] comparable to foliar applications of the antibiotic streptomycin (Maxson-Stein et al., 2002). The ability of BTH to inhibit the extension of fire blight cankers was directly proportional to the application rate. BTH application induced the expression of several pathogenesis-related genes (PR-1, PR-2, and PR-8) in greenhouse grown apple seedlings (Maxson-Stein et al., 2002). Other greenhouse studies have found promise for the use of BTH in citrus against scab (caused by Elsinoe fawcettii Bitancourt & Jenk.), melanose (caused by Diaporthe citri F.A. Wolf), and Alternaria brown spot [caused by Alternaria alternata (Fr.:Fr) Keissl.] (Agostini et al., 2003).

Colson-Hanks and Deverall (2000) reported successful control of Alternaria leaf spot (caused by Alternaria macrospora A. Zimmerm.), bacterial blight [caused by Xanthomonas campestris pv. malvacearum (Smith) Dye], and Verticillium will (caused by Verticillium dahliae Kleb.) of cotton [Gossypium hirsutum L. or G. barbadense L. (Pima cotton)] in a series of field experiments with the use of BTH and INA. Single applications of either BTH or INA reduced the symptoms of both Alternaria leaf spot and bacterial blight. Multiple applications of BTH or a single application of INA reduced the severity of Verticillium will of cotton (Colson-Hanks et al., 2000).

In field trials, BTH use was as effective at controlling white rust (caused by Albugo occidentalis G.W. Wils.) of spinach (Spinacea oleracea L.) as a standard fungicide cocktail of mefenoxam [methyl N-(methoxyacetyl)-N-(2,6-xylyl)-D-alaninate] and copper hydroxide, relative to the nontreated control (Leskovar and Kolenda, 2002). The use of BTH to control white rust was not as effective as the fungicide trifloxistrobin or azoxystrobilurin, strobilurin derivatives that inhibit mitochondrial respiration in fungi. While the additional application of BTH with either of the strobilurin fungicides, improved the control of white rust relative to lone applications of either strobilurin fungicide (Leskovar and Kolenda, 2002).

Field Studies on Induced Systemic Resistance

A number of plant growth-promoting rhizobacteria (PGPR) have been identified as potential ISR elicitors, for their ability to control systemically various diseases when localized to plant roots, as a soil drench, transplant mix, root dip, or seed treatment (reviewed in van Loon et al., 1998). In field trials, the use of several PGPR strains was effective at controlling several diseases of cucumber, including anthracnose [caused by Colletotrichum lagenarium (Pass.) Ellis & Halst, also referred to as C. orbiculare (Berk. & Mont.) Arx], angular leaf spot [caused by Pseudomonas syringae pv. lachrymans (Smith and Bryan) Young et al.], and bacterial will [caused by Erwinia tracheiphila (Smith) Bergey et al.] (Raupach and Kloepper, 1998, 2000; Wei et al., 1996; Zehnder et al., 2001). While the protection afforded by many of these PGPR strains varied under field conditions, a few PGPR strains have shown remarkable efficacy. Bacillus pumilus INR-7 was an exemplary example of a PGPR strain that effectively protected cucumber plants against angular leaf spot and anthracnose in several field trials in three different years (Raupach and Kloepper 1998, 2000; Wei et al., 1996). Cucumber plants seed-treated with either Bacillus pumilus INR-7 or Serratia marcesens 90-166, in comparison to nontreated plants, exhibited a lower incidence of bacterial will and harbored fewer cucumber beetles (Diabrotica undecimpuctata Howardi Barber and Acalymma vittata Fabricius) in two independent field trials (Zehnder et al., 2001). Further experiments in a controlled environment attributed the protection against bacterial will to ISR and a corresponding reduction in the beetle feeding stimulant cucurbitacin in PGPR treated cucumber plants (Zehnder et al., 2001). In greenhouse and field experiments, Bacillus pumilus INR-7 was also among several PGPR strains that protected pearl millet [Pennisetum glaucum (L.) R. Br.] against downy mildew [caused by Sclerospora graminicola (Sacc.) J. Schrot] but not to the same extent as the systemic fungicide metalaxyl [N-(2,6-dimethylphenyl)-N-(methoxyacetyl)alanine methyl ester] (Niranjan Raj et al., 2003).

The use of PGPR strains to control viral diseases of tomato has shown limited success in the field (Murphy et al., 2000; Zehnder et al., 2001). While several PGPR strains were identified in greenhouse trials to induce resistance against Cucumber mosaic virus, a cucumovirus, on tomato, the effectiveness of these strains varied under field conditions when under intense disease pressure (Raupach et al., 1996; Zehnder et al., 2001). Similar results were found with Tomato mottle virus, a geminivirus, on tomato; none of the PGPR strains tested were able consistently to control disease severity in three field trials, regardless of application method (Murphy et al., 2000; Zehnder et al., 2001). The inconsistency of PGPR-mediated ISR against Tomato mottle virus in field trials was attributed to an increase in disease pressure associated with the increased density of the whitefly vector of the virus (Murphy et al., 2000).

A variety of application methods has also been evaluated in the field that should improve the integration of PGPR-mediated ISR into conventional agriculture, and in some cases with improved efficacy. For example, Raupach and Kloepper (1998) found that repeated foliar spray applications of Bacillus pumilus INR-7 or Flavomonas oryzihabitans INR-5 were as effective as seed-treatments at controlling a mixed infection of angular leaf spot and anthracnose on cucumber. Similar results were obtained when comparing seed applications of a talc-based formulation versus a fresh suspension of PGPR strains for protection against downy mildew on pearl millet (Niranjan Raj et al., 2003). Talc-based formulations would allow for easier storage and application of PGPR strains, rather than dealing with liquid bacterial suspensions. Nandakumar et al. (2001) applied PGPR strains to rice plants as a single seed, root, soil, or foliar application or in combinations of two, three and four application methods, and found that combinations of three or four application methods were more effective than single applications at controlling sheath blight (caused by Rhizoctonia solani) of rice in two field trials. Finally, Raupach and Kloepper (1998, 2000) found that applying several PGPR strains, rather than a single strain, improved the control of anthracnose and angular leaf spot in several field and greenhouse experiments, as effectively as the use of BTH.

ISR and SAR within the Context of Organic Soil Amendments

Organic soil amendments have traditionally been associated with the suppression of diseases caused by soilborne pathogens in greenhouse (Boehm and Hoitink, 1992; Zhang et al., 1996, 1998) and field environments (Drinkwater et al., 1995; Workneh et al., 1993; Workneh and van Bruggen, 1994), but there are also examples of foliar disease suppression in both environments as well. Zhang et al. (1996, 1998) demonstrated that cucumbers and A. thaliana plants grown in composted pine bark potting mixes exhibited resistance to foliar diseases caused by Colletotrichum lindemuthianum (Sacc. & Magnus) Lams.-Scrib. and Pseudomonas syringae pv. maculicola (McCulloch) Young et al., respectively, relative to plants grown in a peat mix conducive to disease. This compost-mediated plant resistance corresponded to an increase in the activities of several defense- and pathogenesis-related proteins following inoculation of the pathogen, implicating the involvement of induced plant defenses (Zhang et al., 1996, 1998).

Abbasi et al. (2002) evaluated the effects of soil amendments derived from composted yard wastes and composted cannery waste on tomato production in field trials over two growing seasons. While each amendment offered some protection against anthracnose [caused by Colletotrichum coccodes (Wallr.) S.J. Hughes] and bacterial spot (caused by Xanthomonas axonopodis pv. vesicatoria or X. campestris pv. vesicatoria) of tomato, neither was consistent over the two year duration of the field trials. Tomato plants grown in compost-amended soils consistently produced higher marketable yields. However, the addition of composted amendments also increased the progress of foliar diseases, as measured over time, relative to tomato plants grown in non-amended plots, while the application of BTH impeded disease progress by 55% to 60% regardless of soil treatment (Abbasi et al., 2002).

Field experiments focused on assessing the effects of soil amendments derived from paper mill residuals on plant health, found that soils amended with batches of composted paper mill residuals suppressed the severity of foliar brown spot (caused by Pseudomonas syringae pv. syringae van Hall) of bean and the incidence of angular leaf spot of cucumber compared to that on plants grown in nonamended soils or soils amended with batches of paper mill residuals that were not composted (Stone et al., 2003). The same field soils also conferred resistance on tomato and A. thaliana plants against bacterial speck (caused by P. syringae pv. tomato) in growth chamber experiments, as demonstrated by a 35 to 65% reduction of disease symptoms on plants grown in soils amended with batches of composted paper mill residuals relative to plants grown in nonamended soil or soil amended with batches of a noncomposted paper mill residuals (Vallad et al., 2000, 2003). The suppression of bacterial speck associated with plants grown in batches of composted paper mill residuals, in several experiments, was equivalent to that induced by treating plants with BTH.

Growth chamber experiments with A. thaliana also revealed that the resistance induced by composted paper mill residuals was associated with increases in the expression of plant pathogenesis-related genes before pathogen inoculation, and was disrupted in a npr1 defense mutant and a NahG transgenic line, which are molecular features characteristic of SAR (Vallad et al., 2000, 2003). Others have also documented beneficial cytological changes in tomato plants grown in batches of paper mill residuals suppressive to crown and root rot, as a result of the formation of physical barriers at sites of attempted penetration and reduced colonization of plant roots by Fusarium oxysporum (Schlechtend.:Fr.) f. sp. radicis-lycopersici (W.R. Jarvis & Shoemaker), the causal fungal pathogen (Pharand et al., 2002). These studies stress the importance of the soil environment, beyond crop growth, to improve the defensive potential of the crop, and the potential to use organic amendments to modify the soil environment accordingly.

Considerations for the Use of Induced Resistance

The previous sections examined how chemical and biological elicitors can be practically applied to control pathogen and parasite problems encountered in an assortment of conventional agricultural settings, in lieu of pesticides in many cases. However, like all technologies, there are benefits and drawbacks that need to be considered. There are also biological limitations that may hinder the practical use of chemical and biological elicitors without further research and development. The next section will address these topics.

Physiological Costs of Induced Resistance

The phenomenological characterization of induced plant resistance in a number of controlled and uncontrolled environments has given us an idea about the breadth of these defenses and the costs of fitness that plants incur when deploying these defenses, as measured in terms of vegetative and reproductive growth (summarized as yield in Tables 1 and 2). Most experiments evaluated a range of BTH application rates, and reported a tradeoff between effective disease control and either phytotoxic effects or reduced plant productivity (Abbasi et al., 2002; Cole, 1999; Perez et al., 2003). A consistent theme from several of the field experiments using BTH or INA was the reduction of crop yield (Louws et al., 2001; Romero et al., 2001). Often these reductions were statistically insignificant. For example, when Louws et al. (2001) summarized yield data across 22 field experiments with tomato, plots treated with BTH yielded 11% less, on average, than plots treated with a standardized bacterization treatment (that always included copper hydroxide) and 2.1% less than nontreated control plots. However, only in 1 out of the 22 field experiments was the affect of BTH on yield statistically less than obtained using a standardized bacterization treatment (an 18% reduction in yield); coincidently, only in 1 out of the 22 field experiments did the standardized bacterization treatment statistically yield more than the nontreated control treatment. They also observed that tomato seedlings treated with BTH were smaller than nontreated plants in greenhouse experiments (Louws et al., 2001).

Romero et al. (2001) found that the growth of pepper plants was also greatly influenced by the use of BTH, manifested as a reduction in yield or a delay in plant maturity. These effects on plant growth were apparent across several pepper cultivars when compared to plants treated with copper hydroxide, but only when plants were infected with Xanthomonas campestris pv. vesicatoria (causal agent of bacterial spot). In experiments that carefully excluded Xanthomonas campestris pv. vesicatoria, there were no significant yield differences between BTH treated and copper hydroxide treated plants (Romero et al., 2001). In field trials, PGPR strains generally improved plant growth and yields over nontreated controls; but improved plant growth was not associated with ISR efficacy (Murphy et al., 2000; Niranjan Raj et al., 2003; Nandakumar et al., 2001; Raupach and Kloepper, 1998, 2000; Wei et al., 1996; Yan et al., 2002).

An inherent difference between monocots and dicots exists in terms of the longevity of the induced resistance elicited by BTH. While single applications of BTH were generally sufficient at inducing resistance over the life span of a monocot crop, such as wheat, dicot crops required repeated applications of BTH to extend protection over time (Cole, 1999; Dann and Deverall, 1995; Gorlach et al., 1996; Louws et al., 2001; Morris et al., 1998; Romero et al., 2001). Regardless, there is evidence that there are physiological costs associated with the induction of resistance in monocots as well.

Stadnik and Buchenauer (1999a, 1999b) reported that the effect of BTH on disease and yield of wheat was influenced by the stage of plant growth. In field experiments, BTH treatments applied during the end of tillering (growth stage 28) controlled powdery mildew more effectively then when applied at the middle of tillering (growth stage 25), even though yields from plants treated at the later stages of tillering were numerically less (Stadnik and Buchenauer, 1999a). Several fungicide treatments also effectively controlled powdery mildew, although to a lesser extent than BTH, and improved wheat yields over a nontreated control. The combined use of BTH and fungicide treatments effectively controlled powdery mildew and Septoria leaf blotch of wheat better than either individual treatment and improved wheat yields over a nontreated control and BTH use alone (Stadnik and Buchenauer, 1999a). Foliar applications of urea with BTH also improved wheat yields without disrupting the effective control of BTH, regardless of the increased symptoms of powdery mildew associated with the increase in available nitrogen (Stadnik and Buchenauer, 1999b).

A number of hypotheses have been put forth to explain how plants reallocate resources during the induction of plant defenses and how induced resistance benefits the overall fitness of the plant relative to constitutive defense mechanisms (Coley et al., 1985; Hatcher and Paul, 2000; Heil, 1999; Heil et al., 2000; Herms and Mattson, 1992; Simms and Rausher, 1987; reviewed in Heil 2001). A few studies have tried to address these costs directly in various settings. In a series of greenhouse experiments, Stout et al. (1998) examined the expression of several constitutive and inducible defenses of tomato under different fertilization regiments that varied nitrogen availability. While nitrogen deficiency increased the level of total proteins and phenolics in tomato plants, it had little bearing on the activity levels of proteinase inhibitors or polyphenol oxidase in nontreated plants, or plants induced by a foliar application of jasmonic acid or by herbivore damage caused by Helicoverpa zea (Boddie). Increased nitrogen levels tended to decrease constitutive activity levels of polyphenol oxidase and proteinase inhibitors but did not interfere with the induction of these defenses (Stout et al., 1998). These results suggest that constitutive plant defenses are influenced more by nitrogen availability than inducible plant defenses (Stout et al., 1998).

In greenhouse and field experiments, radish (Raphanus sativus L.) plants induced by limited insect damage or a foliar application of jasmonic acid exhibited less tissue damage from subsequent insect herbivory, accumulated higher amounts of glucosinolates, and were reproductively more fit than mechanically damaged or nonmanipulated plants (Agrawal, 1998, 1999; Agrawal et al., 1999). However, in the absence of herbivore pressure, induced plants were reproductively less fit in terms of flower development and pollen production (Agrawal, 1999). Heil et al. (2000) observed effects on the vegetative growth and seed production of wheat plants induced with BTH in the absence of disease pressure, regardless of the growing conditions or fertilization regiment. However, they found that BTH impeded growth the most during the production of lateral shoots and under nitrogen-limiting conditions, demonstrating the importance of plant growth stage and nutritional status when assessing the physiological costs of induced resistance (Heil et al., 2000). Others have pointed out similar physiological costs associated with resistance induced by applications of jasmonic acid, and also the importance of induced resistance in competition among neighboring plants (Baldwin, 1998; van Dam and Baldwin, 1998). Interestingly, similar vegetative and reproductive costs have also been associated with R-gene mediated resistance (vertical resistance) (reviewed in Bergelson and Purrington, 1996; Bergelson, 1994; Tian et al., 2003).

Conflicts in Plant Signaling Pathways

In nature, plants respond to a multitude of parasites, often simultaneously, and must allocate resources to defenses and vegetative growth to ensure reproductive success. A number of laboratory studies assessing the role of defense responses dependent of salicylic acid, jasmonic acid, and ethylene have demonstrated conflictive and additive interactions among these pathways depending on the parasite(s) involved (see reviews of Bostock, 1999; Dempsey et al., 1999; Genoud and Metraux, 1999; Kessler and Baldwin, 2002; McDowell and Dangl, 2000; Walling, 2000). Interactions among defense pathways have also been studied in the field, primarily between foliar pathogens and herbivores.

Thaler et al. (1999) in a field experiment treated tomato plants with BTH, jasmonic acid, or both, in addition to nontreated controls, and then challenged plants with either a bacterial pathogen or an insect herbivore. Tomato plants treated with BTH exhibited reduced symptoms of foliar speck (caused by Pseudomonas syringae pv. tomato) compared to nontreated plants, but were also more susceptible to herbivore damage caused by larvae of the beet armyworm [Spodoptera exigua (Hubner)]. Conversely, tomato plants treated with jasmonic acid were more resistant to herbivore damage, but did not differ from the nontreated control in susceptibility to foliar speck. An analysis of several biochemical defenses found that the increased susceptibility to herbivory in BTH-treated plants was associated with the suppression of polyphenol oxidase activity and mRNA encoding the proeinase inhibitor PIN II, which are key antiherbivore responses. An increase in mRNA encoding the pathogenesis-related protein P4 was also observed in BTH-treated plants in association with suppression of symptoms of bacterial speck, but suppressed in plants treated with jasmonic acid. Interestingly, plants treated simultaneously with BTH and jasmonic acid exhibited symptoms of bacterial speck and herbivore damage intermediate of the plants treated individually with either BTH or jasmonic acid, and were associated with intermediate levels of polyphenol oxidase activity and P4 mRNA. Thaler (1999) further demonstrated that defenses induced by foliar applications of jasmonic acid on tomatoes effectively controlled insect herbivory in field trials over a 4 yr period.

Hatcher et al. (1994) and Hatcher and Paul (2000) found that undamaged leaves of the plant Rumex obtusifolius L. that received damage from the beetle Gastrophysa viridula (De Geer) were more resistant to several fungal pathogens than were plants undamaged by herbivory. Interestingly, induced resistance was not found to be a factor among the fungal pathogens studied, which included a biotrophic Basidiomycete [Uromyces rumicis (Schumach.) G. Winter], a hemibiotrophic Ascomycete [Venturia rumicis (Desm.) G. Winter], and a necrotrophic Ascomycete [Ramularia rubella (Bonord.) Nannf.] (Hatcher and Paul, 2000). It's quite possible that these fungal pathogens evolved strategies to avoid or neutralize the defenses of R. obtusifolius during pathogenesis, explaining why host defenses elicited by insect herbivory were effective against these fungi.

Genetic Variability in Plants

Results from the various field trials considered in this review demonstrate the potential of biological and chemical elicitors to control a wide variety of diseases. The crops utilized in these studies were modern cultivars selected in conventional agricultural settings, and they generally exhibited only minor, often statistically insignificant, reductions in yield in association with chemical elicitors of SAR when compared with standard pesticide treatments. Since induced resistance is a biological response, it should be amenable to breeding strategies to minimize its negative impact on agronomic traits, and perhaps even improve its overall effectiveness. However, it will be necessary to determine the amount and types of variability that may exist among domesticated crops and their wild relatives.

Currently, it is unclear what variability exists within plant populations for the induction, maintenance, and overall robustness (in terms of the number and effectiveness of individual biochemical components involved) of induced resistance responses. A great deal is known from A. thaliana about the role of the phytohormones ethylene, jasmonic acid, and salicylic acid in induced resistance responses, mostly because of mutational screens that identified genes that when disrupted prevent the plant from producing or detecting such phytochemicals. However, little data are available assessing the allelic variability of these regulatory genes among the various ecotypes of A. thaliana, let alone what variability exists among the A. thaliana ecotypes for induced resistance responses, except in a limited case involving a single ISR-eliciting PGPR strain (van Wees et al., 1997).

The induction of ISR relies on specific plant-PGPR strain interactions (Leeman et al., 1995a, 1995b; Ton et al., 1999, 2001; van Wees et al., 1997). In A. thaliana, the PGPR strain Pseudomonas fluorescens WCS417r was capable of eliciting an ISR response on most ecotypes, but not on ecotypes RLD and Wassilewskija (van Wees et al., 1997; Ton et al., 1999). Subsequent genetic studies led to the identification of the ISR1 locus that not only controls the ability to respond to P. fluorescens WCS417r, but also basal resistance to P. syringae pv. tomato. After further research, the ISR1 locus was found to play a role in the ethylene signaling pathway of A. thaliana, therefore ecotypes RLD and Wassilewskija carried a recessive trait that affected ISR by disrupting ethylene signaling while leaving SAR intact (Ton et al., 2001). This demonstrates that among A. thaliana ecotypes, allelic variability exists in regulatory genes that influence ISR pathways.

What allelic variability exists for regulatory genes of SAR? Nothing has been found that compares with the previous example of the ISR1 locus, since few studies have examined genotypic effects on SAR. Interestingly, some limited studies evaluating SAR among cultivars that differed in their level of resistance toward a particular pathogen found improved efficacy in partially resistant cultivars over susceptible cultivars, whereas others reported just the opposite or few differences among cultivars (Dann et al., 1998; Hijwegen and Verhaar, 1994; Romero et al., 2001; Stadnik and Buchenauer, 1999b). However, there is evidence from an ecological study using families of wild radish (Raphanus raphanistrum L.) derived from full- or half-sib matings that significant differences existed among families for fitness costs following induction, as measured by differences among various reproductive traits, suggesting that among the families there was either genetic variability for the induction of resistance or genetic variability for the physiological costs associated with the induced resistance response, which implies heritability (Agrawal et al., 1999).

Effects on Parasite Populations

Unlike race-specific (vertical) resistance or pesticides, induced resistance does not appear to apply selective pressure to pathogen or parasite populations on the basis of any single genetic determinant or specific mode of action, but rather is quantitative because of the cumulative effects of numerous plant defense mechanisms (Sticher et al., 1997; van Loon et al., 1998). However, because of its similarity to horizontal resistance, the effectiveness of induced resistance has the potential to "erode" over time as the pathogen or parasite population evolves (McDonald and Linde, 2002). There is a need for research evaluating the effects of SAR or ISR on the composition of pathogen or parasite populations.

In one such study, Bousset and Pons-Kuhnemann (2003) constructed a population of Blumeria graminis (DC.) E. O. Speer = Erysiphe graminis DC. f. sp. hordei Em. Marchal (causes powdery mildew on barley) derived from crosses among 30 isolates collected from barley fields treated with either BTH or the fungicide ethirimol (5-butyl-2-ethylamino-6-methylpyrimidin-4-ol). The composition of the population, on the basis of the diversity of virulence pathotypes and sensitivity to the fungicide ethirimol and triadimenol [(1RS,2RS;1RS, 2SR)-l-(4-chlorophenoxy)-3,3-dimethyl-1-(1H-1,2,4-triazol-1-yl)butan-2-ol], was monitored over several generations on barley plants treated with ethirimol, BTH or both, in addition to nontreated plants. On the basis of sensitivity to ethirimol and triadimenol, and the diversity of virulence pathotypes, the use of BTH alone did not affect the composition of the B. graminis population relative to the nontreated control beyond that attributable to genetic drift. As expected, the composition of the B. graminis population was influenced by the fungicide ethirimol, as detected by an increase in the number of isolates tolerant to the fungicide and a decrease in the diversity of virulence pathotypes. However, the combined use of ethirimol and BTH had an even larger affect on the composition of the pathogen population than ethirimol alone. This suggests that BTH alone may not have a direct effect on the genetic composition of a pathogen population, but may exert additional selective pressure either through SAR or synergy between BTH and ethirimol chemistries (Bousset and Pons-Kuhnemann, 2003).

Future Directions

Elicitors of SAR and ISR could potentially revolutionize pest management in conventional agriculture. BTH, in particular, effectively and consistently reduced diseases caused by a broad spectrum of pathogens across a diverse range of crops and plant taxa. However, the efficacy of SAR induced by BTH depended on a number of variables, such as the dose and frequency of BTH application, host genotype and in one case the growth stage of the plant. Data exist supporting heritability in the induction of plant defenses and physiological costs incurred from maintaining plant defenses, opening the possibility of breeding plants with improved inducible resistance responses or minimized fitness costs (Agrawal et al., 1999). Can the same types of genetic variability for induced resistance responses be found in domesticated plants, and applied during breeding?

The efficacy of SAR and ISR also depended on the pathogen, and some pathogens did not respond to elicitors of either. For example, SAR induced by BTH was ineffective against Fusarium wilt of cucumber (Fusarium oxysporum Schlechtend.:Fr. f. sp. cucumerinum J.H. Owen) (Ishii et al., 1999). Preinoculation of bean plants with C. lindemuthianum or foliar applications of INA was ineffective against two root pathogens, Fusarium solani (Mart.) Sacc. f. sp. phaseoli (Burkholder) W. C. Snyder & H. N. Hans. or pathogenic Rhizoctonia spp. (Dann and Deverall, 1995). Several elicitors of SAR and ISR also failed to reduce symptoms of late leaf spot [caused by Phaeoisariopsis personata (Berk. & M.A. Curtis) Arx = Cercosporidium personatum (Berk. & M.A. Curtis) Deighton] of peanut (Arachis hypogaea L.) and in some cases exacerbated symptoms (Zhang et al., 2001). It is conceivable that in the previous examples disease was unaffected because the pathogen was able to thwart host defenses or because the plant lacked effective defenses or lacked the capacity to initiate defenses against the pathogen.

In many cases, the SAR activity induced by BTH or INA was as effective at controlling specific diseases as a standardized pesticide control, especially for diseases caused by phytopathogenic bacteria. Still, some researchers found it necessary either to alternate or to combine BTH with a pesticide(s) to reduce disease to a level comparable to the standardized pesticide control, or to control other diseases not influenced by SAR.

For example, while Louws et al. (2001) found that BTH alone sufficiently controlled bacterial spot and speck of tomato, in some trials it was still necessary to add specific fungicides to control late and early blight. While one would predict that the combined use of SAR elicitors with standard pesticides should extend the effectiveness of the pesticides, experiments conducted by Bousset and Pons-Kuhnemann (2003) suggest just the opposite; SAR may actually intensify the selective pressure exerted by certain pesticides on pathogen and pest populations. Clearly this is a concern, especially when neither SAR nor ISR render the plant impervious to the pathogen, but rather seem to increase the plants overall tolerance.

Neither SAR nor ISR is a stand-alone method for pest control, but merely another tool that will need to be further integrated into pest management systems. Each crop and disease will be unique in some regard. The effective use of either SAR or ISR will also heavily depend on disease forecasting and the ability to activate plant defenses at critical developmental periods when the plant is most susceptible, since SAR and ISR are ineffective once the pathogen has established itself. There is also the risk of rendering the plant susceptible to other pathogens or insect herbivores, so it will be necessary to continuously monitor various pests in the field. On the other hand, there is evidence from the A. thaliana model system that the simultaneous induction of ISR and SAR may give additive protection against pathogens, but this approach has not been further investigated in crops or in the field (van Wees et al., 2000).

Newer and more effective elicitors of SAR and ISR will surely be developed, perhaps in part as the result of our growing understanding of the underlying mechanisms of these pathways within the plant. In the future, it may be possible to apply elicitor cocktails that induce a balance of defenses regulated by salicylic acid, jasmonic acid, ethylene, and other undefined regulators, against specific pests or complexes of threats. However, this future will require a shift in conventional agriculture away from the total reliance on pesticides to solve pest problems, and a concerted effort to manage pests as opposed to eliminating them.

Abbreviations: ISR, induced systemic resistance; PGPR, plant growth-promoting rhizobacteria: SAR, systemic acquired resistance.
Table 1. The average percentage difference in disease and yield
relative to a nontreated control in field experiments using elicitors
of systemic acquired resistance and pesticides to control crop
diseases.

                                                 SAR
                                               elicitor
Crop              Pathogen/disease            ([dagger])

Monocots
  Maize        Peronoscleropora sorghil          BTH
                 downy mildew
  Wheat        Blumeria graminis f. sp.          BTH
                 tritici/powdery mildew
               Blumeria graminis f. sp.          BTH
                 tritici/powdery mildew
               Septoria spp./Septoria leaf       BTH
                 spot
               Septoria tritici/Septoria         BTH
                 leaf blotch
               Septoria tritici/Septoria         BTH
                 leaf blotch
               Puccinia recondita/leaf rust      BTH

Dicots
  Solanaceous
    Tobacco    Pseudomonas syringae pv.          BTH
                 tabaci (tox+)/bacterial
                 wildfire
               Perenospora hyoscyami f. sp.      BTH
                 tabacina/blue mold
               Cercospora nicotiana/eyespot      BTH

               Alternaria alternata/brown        BTH
                 spot

               Thanetephorus cucumeris/          BTH
                 Rhizoctonia leaf spot

               Tomato spotted wilt virus         BTH

    Tomato     Pseudomonas syringae pv.          BTH
                 tomato/bacterial speck
               Pseudomonas syringae pv.          BTH
                 tomato/bacterial speck

               Xanthomonas axonopodis pv.        BTH
                 vesicatoria/bacterial spot
               Xanthomonas axonopodis pv.        BTH
                 vesicatoria/bacterial spot
                 and Colletotrichum
                 coccodes/Anthracnose
               Xanthomonas campestris pv.        BTH
                 vesicatoria/bacterial spot
               Alternari solani/early blight     BTH
               Fulvia fulva/leaf mold            BTH
               Alternaria solani/early           BTH
                 blight, Phtophthora
                 infestans/late blight, and
                 X. axonopodis pv.
                 vesicatoria/bacterial spot
    Pepper     Xanthomonas campestris pv.        BTH
                 vesicatoria/bacterial spot
               Xanthomonas campestris pv.        BTH
                 vesicatoria/bacterial spot
  Leguminous
    Bean       Uromyces appendiculatus/rust      INA

    Soybean    Sclerotinia sclerotiorum/         INA
                 white mold
               Sclerotinia sclerotiorum/         BTH
                 white mold

Miscellaneous
  Cotton       Xanthomonas campestris pv.        BTH
                 malvacearum/bacterial
                 blight
               Alternaria macrosporal            INA
                 Alternaria leaf spot
               Alternaria macrosporal            BTH
                 Alternaria leaf spot
               Verticillium dahliae              INA
               Verticillium dahliae              BTH
    Peanut     Cercosporidium personatum/        INA
                 late leaf spot
               Cercosporidium personatum/        BTH
                 late leaf spot
  Spinach      Albugo occidentalis/white         BTH
                 rust
  Apple        Erwinia amylovora/fire            BTH
                 blight
  Pear         Gymnosporangium asiaticum/        BTH
                 rust

               Venturia nashicola/scab           BTH

                                                 Disease (+ or - %)
                                                  ([double dagger])

                                                 SAR        Pesticide
Crop              Pathogen/disease             elicitor     standard

Monocots
  Maize        Peronoscleropora sorghil          -35           -31
                 downy mildew
  Wheat        Blumeria graminis f. sp.          -64           -55
                 tritici/powdery mildew
               Blumeria graminis f. sp.          -77           NA
                 tritici/powdery mildew
               Septoria spp./Septoria leaf       -35           NA
                 spot
               Septoria tritici/Septoria         -52           -45
                 leaf blotch
               Septoria tritici/Septoria         -46           NA
                 leaf blotch
               Puccinia recondita/leaf rust      -35           NA

Dicots
  Solanaceous
    Tobacco    Pseudomonas syringae pv.          -99           -32
                 tabaci (tox+)/bacterial
                 wildfire
               Perenospora hyoscyami f. sp.      -76           -42
                 tabacina/blue mold
               Cercospora nicotiana/eyespot      -91           -85

               Alternaria alternata/brown        -89           -61
                 spot

               Thanetephorus cucumeris/          -71           -10
                 Rhizoctonia leaf spot

               Tomato spotted wilt virus         -61           -38

    Tomato     Pseudomonas syringae pv.          -47           -27
                 tomato/bacterial speck
               Pseudomonas syringae pv.          -42           NA
                 tomato/bacterial speck

               Xanthomonas axonopodis pv.        -50           -40
                 vesicatoria/bacterial spot
               Xanthomonas axonopodis pv.        -51           NA
                 vesicatoria/bacterial spot
                 and Colletotrichum
                 coccodes/Anthracnose
               Xanthomonas campestris pv.        -47           NA
                 vesicatoria/bacterial spot
               Alternari solani/early blight     -33           NA
               Fulvia fulva/leaf mold            -52           NA
               Alternaria solani/early            -4           -94
                 blight, Phtophthora
                 infestans/late blight, and
                 X. axonopodis pv.
                 vesicatoria/bacterial spot
    Pepper     Xanthomonas campestris pv.        -64           -30
                 vesicatoria/bacterial spot
               Xanthomonas campestris pv.        -32           -43
                 vesicatoria/bacterial spot
  Leguminous
    Bean       Uromyces appendiculatus/rust      -70           -24
                                                          ([paragraph])

    Soybean    Sclerotinia sclerotiorum/         -46           NA
                 white mold
               Sclerotinia sclerotiorum/         -59           NA
                 white mold

Miscellaneous
  Cotton       Xanthomonas campestris pv.        -42           NA
                 malvacearum/bacterial
                 blight
               Alternaria macrosporal            -32           NA
                 Alternaria leaf spot
               Alternaria macrosporal            -45           NA
                 Alternaria leaf spot
               Verticillium dahliae              -38           NA
               Verticillium dahliae              -37           NA
    Peanut     Cercosporidium personatum/        +52           NA
                 late leaf spot
               Cercosporidium personatum/        +35           NA
                 late leaf spot
  Spinach      Albugo occidentalis/white         -39           -40
                 rust
  Apple        Erwinia amylovora/fire            -73           -38
                 blight
  Pear         Gymnosporangium asiaticum/        -63           -96
                 rust

               Venturia nashicola/scab           -50           -55

                                                  Yield (+ or - %)
                                                  ([double dagger])

                                                 SAR        Pesticide
Crop              Pathogen/disease             elicitor     standard

                                                          %

Monocots
  Maize        Peronoseleropora sorghil           NA           NA
                 downy mildew
  Wheat        Blumeria graminis f. sp.           +3           +28
                 tritici/powdery mildew
               Blumeria graminis f. sp.           0            NA
                 tritici/powdery mildew
               Septoria spp./Septoria leaf       +18           +17
                 spot
               Septoria tritici/Septoria          +3           +31
                 leaf blotch
               Septoria tritici/Septoria          0            NA
                 leaf blotch
               Puccinia recondita/leaf rust      +18           +17

Dicots
  Solanaceous
    Tobacco    Pseudomonas syringae pv.           NA           NA
                 tabaci (tox+)/bacterial
                 wildfire
               Perenospora hyoscyami f. sp.       NA           NA
                 tabacina/blue mold
               Cercospora nicotiana/eyespot       NA           NA

               Alternaria alternata/brown         NA           NA
                 spot

               Thanetephorus cucumeris/           NA           NA
                 Rhizoctonia leaf spot

               Tomato spotted wilt virus          NA           NA

    Tomato     Pseudomonas syringae pv.           -1           NA
                 tomato/bacterial speck
               Pseudomonas syringae pv.           NA           NA
                 tomato/bacterial speck

               Xanthomonas axonopodis pv.         0            +13
                 vesicatoria/bacterial spot
               Xanthomonas axonopodis pv.        +26           NA
                 vesicatoria/bacterial spot
                 and Colletotrichum
                 coccodes/Anthracnose
               Xanthomonas campestris pv.         NA           NA
                 vesicatoria/bacterial spot
               Alternari solani/early blight      NA           NA
               Fulvia fulva/leaf mold             NA           NA
               Alternaria solani/early           -27           NA
                 blight, Phtophthora
                 infestans/late blight, and
                 X. axonopodis pv.
                 vesicatoria/bacterial spot
    Pepper     Xanthomonas campestris pv.         NA           NA
                 vesicatoria/bacterial spot
               Xanthomonas campestris pv.         0            +50
                 vesicatoria/bacterial spot
  Leguminous
    Bean       Uromyces appendiculatus/rust       NA           NA

    Soybean    Sclerotinia sclerotiorum/          +9           NA
                 white mold
               Sclerotinia sclerotiorum/          NA           NA
                 white mold

Miscellaneous
  Cotton       Xanthomonas campestris pv.         NA           NA
                 malvacearum/bacterial
                 blight
               Alternaria macrosporal             NA           NA
                 Alternaria leaf spot
               Alternaria macrosporal             NA           NA
                 Alternaria leaf spot
               Verticillium dahliae               NA           NA
               Verticillium dahliae               NA           NA
    Peanut     Cercosporidium personatum/         NA           NA
                 late leaf spot
               Cercosporidium personatum/         NA           NA
                 late leaf spot
  Spinach      Albugo occidentalis/white         +50           +72
                 rust
  Apple        Erwinia amylovora/fire             NA           NA
                 blight
  Pear         Gymnosporangium asiaticum/         NA           NA
                 rust

               Venturia nashicola/scab            NA           NA

Crop              Pathogen/disease             Comments ([section])

Monocots
  Maize        Peronoseleropora sorghil       percent symptomatic
                 downy mildew                   plants
  Wheat        Blumeria graminis f. sp.       percent infected leaf
                 tritici/powdery mildew         area
               Blumeria graminis f. sp.       percent infected leaf
                 tritici/powdery mildew         area
               Septoria spp./Septoria leaf    values reported in
                 spot                           text
               Septoria tritici/Septoria      percent infected leaf
                 leaf blotch                    area
               Septoria tritici/Septoria      percent infected leaf
                 leaf blotch                    area
               Puccinia recondita/leaf rust   values reported in
                                                text
Dicots
  Solanaceous
    Tobacco    Pseudomonas syringae pv.       foliar symptoms
                 tabaci (tox+)/bacterial        rated as lesions/
                 wildfire                       plant
               Perenospora hyoscyami f. sp.   foliar symptoms
                 tabacina/blue mold
               Cercospora nicotiana/eyespot   foliar symptoms
                                                rated as lesions/
                                                leaf
               Alternaria alternata/brown     foliar symptoms
                 spot                           rated as lesions/
                                                leaf
               Thanetephorus cucumeris/       foliar symptoms
                 Rhizoctonia leaf spot          rated as lesions/
                                                plant
               Tomato spotted wilt virus      percent symptomatic
                                                plants
    Tomato     Pseudomonas syringae pv.       foliar symptoms
                 tomato/bacterial speck
               Pseudomonas syringae pv.       foliar symptoms
                 tomato/bacterial speck         rated as lesions/
                                                [cm.sup.2]
               Xanthomonas axonopodis pv.     foliar symptoms;
                 vesicatoria/bacterial spot     total yield
               Xanthomonas axonopodis pv.     disease assessed by
                 vesicatoria/bacterial spot     AUDPC;
                 and Colletotrichum             marketable yield
                 coccodes/Anthracnose
               Xanthomonas campestris pv.     foliar symptoms
                 vesicatoria/bacterial spot
               Alternari solani/early blight  foliar symptoms
               Fulvia fulva/leaf mold         foliar symptoms
               Alternaria solani/early        disease measured in
                 blight, Phtophthora            terms of
                 infestans/late blight, and     defoliation;
                 X. axonopodis pv.              marketable yield
                 vesicatoria/bacterial spot
    Pepper     Xanthomonas campestris pv.     percent infected leaf
                 vesicatoria/bacterial spot     area
               Xanthomonas campestris pv.     disease assessed by
                 vesicatoria/bacterial spot     AUDPC
  Leguminous
    Bean       Uromyces appendiculatus/rust   foliar symptoms
                                                rated as uridinia/
                                                leaf
    Soybean    Sclerotinia sclerotiorum/      foliar symptoms
                 white mold
               Sclerotinia sclerotiorum/      foliar symptoms;
                 white mold                     BTH was
                                                ineffective in
                                                second field trial
Miscellaneous
  Cotton       Xanthomonas campestris pv.     percent infected leaf
                 malvacearum/bacterial          area
                 blight
               Alternaria macrosporal
                 Alternaria leaf spot
               Alternaria macrosporal
                 Alternaria leaf spot
               Verticillium dahliae           foliar symptoms
               Verticillium dahliae
    Peanut     Cercosporidium personatum/     disease assessed by
                 late leaf spot                 AUDPC
               Cercosporidium personatum/
                 late leaf spot
  Spinach      Albugo occidentalis/white      percent infected leaf
                 rust                           area
  Apple        Erwinia amylovora/fire         percent infected
                 blight                         shoots/tree
  Pear         Gymnosporangium asiaticum/     foliar symptoms
                 rust                           rated as lesions/
                                                leaf
               Venturia nashicola/scab        percent leaves with
                                                symptoms

Crop              Pathogen/disease                  Source

Monocots
  Maize        Peronoseleropora sorghil       Morris et al., 1998
                 downy mildew
  Wheat        Blumeria graminis f. sp.       Stadnik and
                 tritici/powdery mildew         Buchenauer, 1999a
               Blumeria graminis f. sp.       Stadnik and
                 tritici/powdery mildew         Buchenauer, 1999b
               Septoria spp./Septoria leaf    Gorlach et al., 1996
                 spot
               Septoria tritici/Septoria      Stadnik and
                 leaf blotch                    Buchenauer, 1999a
               Septoria tritici/Septoria      Stadnik and
                 leaf blotch                    Buchenauer, 1999b
               Puccinia recondita/leaf rust   Gorlach et al., 1996

Dicots
  Solanaceous
    Tobacco    Pseudomonas syringae pv.       Cole, 1999
                 tabaci (tox+)/bacterial
                 wildfire
               Perenospora hyoscyami f. sp.   Perez et al., 2003
                 tabacina/blue mold
               Cercospora nicotiana/eyespot   Perez et al., 2003

               Alternaria alternata/brown     Perez et al., 2003
                 spot

               Thanetephorus cucumeris/       Cole, 1999
                 Rhizoctonia leaf spot

               Tomato spotted wilt virus      Csinos et al., 2001

    Tomato     Pseudomonas syringae pv.       Louws et al., 2001
                 tomato/bacterial speck
               Pseudomonas syringae pv.       Thaler et al., 1999
                 tomato/bacterial speck

               Xanthomonas axonopodis pv.     Louws et al., 2001
                 vesicatoria/bacterial spot
               Xanthomonas axonopodis pv.     Abbasi et al., 2002
                 vesicatoria/bacterial spot
                 and Colletotrichum
                 coccodes/Anthracnose
               Xanthomonas campestris pv.     Inbar et al., 1998
                 vesicatoria/bacterial spot
               Alternari solani/early blight  Inbar et al., 1998
               Fulvia fulva/leaf mold         Inbar et al., 1998
               Alternaria solani/early        Louws et al., 2001
                 blight, Phtophthora
                 infestans/late blight, and
                 X. axonopodis pv.
                 vesicatoria/bacterial spot
    Pepper     Xanthomonas campestris pv.     Buonaurio et al., 2002
                 vesicatoria/bacterial spot
               Xanthomonas campestris pv.     Romero et al., 2001
                 vesicatoria/bacterial spot
  Leguminous
    Bean       Uromyces appendiculatus/rust   Dann and Deverall,
                                                1996

    Soybean    Sclerotinia sclerotiorum/      Dann et al., 1998
                 white mold
               Sclerotinia sclerotiorum/      Dann et al., 1998
                 white mold

Miscellaneous
  Cotton       Xanthomonas campestris pv.     Colson-Hanks et al.,
                 malvacearum/bacterial          2000
                 blight
               Alternaria macrosporal
                 Alternaria leaf spot
               Alternaria macrosporal
                 Alternaria leaf spot
               Verticillium dahliae
               Verticillium dahliae
    Peanut     Cercosporidium personatum/     Zhang et al., 2001
                 late leaf spot
               Cercosporidium personatum/
                 late leaf spot
  Spinach      Albugo occidentalis/white      Leskovar and
                 rust                           Kolenda, 2002
  Apple        Erwinia amylovora/fire         Maxson-Stein et al.,
                 blight                         2002
  Pear         Gymnosporangium asiaticum/     Ishii et al., 1999
                 rust

               Venturia nashicola/scab        Ishii et al., 1999

([dagger]) BTH, benzo (1,2,3) thiadiazole-7-carbothioic acid S-methyl
ester (also known as acibenzolar-S-methyl); INA,
2,6-dichloro-isonicotinic acid.

([double dagger]) NA, not available. In those papers where data for
multiple pesticide treatments are presented, calculations are based on
the pesticide treatments that were most efficacious or most
representative.

([section]) Refer to how disease or yield was measured; AUDPC, area
under the disease progress curve.

([paragraph]) Plants treated with wetable powder and other inert
ingredients from INA formulation (INA not included).

Table 2. The average percentage difference in disease and yield
relative to a nontreated control in field experiments using strains of
plant growth-promoting rhizobacteria (PGPR) and pesticides to control
crop diseases.

                                                   Disease ([+ or -] %)
                                                        ([dagger])

                                                            %

               Pathogen/                                   ISR
Crop            disease           PGPR strain            elicitor

Monocots
  Rice      Rhizoctonia       Pseudomonas                  -51
              solani/sheath     fluorescens PF1            -57
              blight          Pseudomonas
                                fluorescens FP7
  Pearl     Sclerospora       Bacillus pumilus T4          -52
    Millet    glaucum/
              downy mildew
                              Bacillus pumilus             -63
                                INR7
                              Bacillus                     -44
                                amyloliquefaciens
                                IN937a
                              Bacillus subtilis            -46
                                IN937b
                              Bacillus pumilus             -55
                                SE34
                              Brevibacillus                -51
                                brevis
                                IPC11
                              Bacillus subtilis            -53
                                GB03
Dicots
  Tomato    Cucumber mosaic   Bacillus pumilus             -45
              virus             SE34
                              Kluyvera                     -30
                                cryocrescens
                                IN114
                              Bacillus                     -53
                                amyloliquefaciens
                                IN937a
  Tomato    Cucumber mosaic   Bacillus subtilus            -54
              virus             IN937b
            Tomato mottle     Bacillus pumilus             -30
              virus             SE34
                              Bacillus                     -58
                                amyloliquefaciens
                                IN937a
                              Bacillus subtilus            -29
                                IN937b
  Cucumber  Erwinia           Bacillus pumilis             -86
              tracheiphila/     INR-7
              bacterial wilt
                              Serratia marcesens           -89
                                90-166
            Pseudomonas       Pseudomonas putida           -34
              syringae pv.      89B-61
              lachrymans/     Serratia marcescens          -20
              angular leaf      90-166
              spot            Flavomonas                   -32
                                oryzihabitans
                                INR-5
                              Bacillus pumilus             -42
                                INR-7
                              Bacillus pumilis             -69
                                INR-7
                              Curtobacterium               -16
                                flaccumfaciens
                                ME1
                              Bacillus pumilus             -52
                                GB03
                              INR7 + ME1                   -80
                              INR7 + GB03                  -67
  Cucumber  Pseudomonas       ME1 + GB03                   -50
              syringae pv.
              lachrymans/     INR7 + ME1 + GB3             -86
              angular leaf    Bacillus pumilus             -57
              spot              INR-7
                              Curtobacterium               -38
                                flaccumfaciens
                                ME1
                              Bacillus pumilus             -38
                                GB03
                              INR7 + ME1                   -54
                              INR7 + GB03                  -57
                              ME1 + GB03                   -42
                              INR7 + MEl +                 -57
                                GB03
            Pseudomonas       Bacillus pumilus             -48
              syringae pv.      INR7
              lachrymans/
              angular leaf
              spot;
              Colletotrichum
              orbicularel     Burkholderia                 -26
              anthracnose       gladioli
                                IN26
                              INR7 + IN26                  -45
                              INR7 + ME1 + GB03            -55
                              Bacillus pumilus             -36
                                INR-7
                              Curtobacterium               -24
                                flaccumfaciens
                                ME1
                              Bacillus pumilus             -29
                                GB03
                              INR7 + ME1                   -54
  Tomato    Pseudomonas       INR7 + GB03                  -44
              syringae pv.
              lachrymans/
              angular leaf
              spot;
              Colletotrichum  ME1 + GB03                   -47
              orbiculare/     INR7 + ME1 + GB03            -56
              anthracnose
            Colletotrichum    Pseudomonas putida           -54
              orbiculare/       89B-61
              anthracnose
                              Serratia                     -37
                                marcescens
                                90-166
                              Flavomonas                   -51
                                oryzihabitans
                                INR-5
                              Bacillus pumilus             -56
                                INR-7
  Pepper    Meloidogyne       GB03 + IN937a                +12
              incognita/
              root-knot       GB03 + SE34                  -15
              nematode        GB03 + IN937b                -14
                              GB03 + INR7                   -6
                              GB03 + Bacillus              -32
                                cereus C4
  Peanut    Cercosporidium    Bacillus cereus C1           -33
              personatum/                            ([double dagger])
              late leaf spot                         ([double dagger])
                              Bacillus cereus C3            +2
                                                     ([double dagger])
                                                     ([double dagger])
                              Bacillus cereus C5           -30
                                                     ([double dagger])
                                                     ([double dagger])
                              Bacillus pumilus T4          -11
                                                     ([double dagger])
                                                     ([double dagger])

                                                   Disease ([+ or -] %)
                                                        ([dagger])

                                                            %

               Pathogen/                                Pesticide
Crop            disease           PGPR strain            standard

Monocots
  Rice      Rhizoctonia       Pseudomonas                  -54
              solani/sheath     fluorescens PF1            -53
              blight          Pseudomonas
                                fluorescens FP7
  Pearl     Sclerospora       Bacillus pumilus T4          -87
    Millet    glaucum/
              downy mildew
                              Bacillus pumilus             -87
                                INR7
                              Bacillus                     -87
                                amyloliquefaciens
                                IN937a
                              Bacillus subtilis            -87
                                IN937b
                              Bacillus pumilus             -87
                                SE34
                              Brevibacillus                -87
                                brevis
                                IPC11
                              Bacillus subtilis            -87
                                GB03
Dicots
  Tomato    Cucumber mosaic   Bacillus pumilus              NA
              virus             SE34
                              Kluyvera                      NA
                                cryocrescens
                                IN114
                              Bacillus                      NA
                                amyloliquefaciens
                                IN937a
  Tomato    Cucumber mosaic   Bacillus subtilus             NA
              virus             IN937b
            Tomato mottle     Bacillus pumilus              NA
              virus             SE34
                              Bacillus                      NA
                                amyloliquefaciens
                                IN937a
                              Bacillus subtilus             NA
                                IN937b
  Cucumber  Erwinia           Bacillus pumilis             -53
              tracheiphila/     INR-7
              bacterial wilt
                              Serratia marcesens           -53
                                90-166
            Pseudomonas       Pseudomonas putida           -38
              syringae pv.      89B-61                ([paragraph])
              lachrymans/     Serratia marcescens          -38
              angular leaf      90-166
              spot            Flavomonas                   -38
                                oryzihabitans
                                INR-5
                              Bacillus pumilus             -38
                                INR-7
                              Bacillus pumilis              NA
                                INR-7
                              Curtobacterium                NA
                                flaccumfaciens
                                ME1
                              Bacillus pumilus              NA
                                GB03
                              INR7 + ME1                    NA
                              INR7 + GB03                   NA
  Cucumber  Pseudomonas       ME1 + GB03                    NA
              syringae pv.
              lachrymans/     INR7 + ME1 + GB3              NA
              angular leaf    Bacillus pumilus              NA
              spot              INR-7
                              Curtobacterium                NA
                                flaccumfaciens
                                ME1
                              Bacillus pumilus              NA
                                GB03
                              INR7 + ME1                    NA
                              INR7 + GB03                   NA
                              ME1 + GB03                    NA
                              INR7 + MEl +                  NA
                                GB03
            Pseudomonas       Bacillus pumilus             -62
              syringae pv.      INR7                    ([dagger])
              lachrymans/                               ([dagger])
              angular leaf
              spot;
              Colletotrichum
              orbicularel     Burkholderia                 -62
              anthracnose       gladioli                ([dagger])
                                IN26                    ([dagger])
                              INR7 + IN26                  -62
                                                        ([dagger])
                                                        ([dagger])
                              INR7 + ME1 + GB03            -62
                                                        ([dagger])
                                                        ([dagger])
                              Bacillus pumilus              NA
                                INR-7
                              Curtobacterium                NA
                                flaccumfaciens
                                ME1
                              Bacillus pumilus              NA
                                GB03
                              INR7 + ME1                    NA
  Tomato    Pseudomonas       INR7 + GB03                   NA
              syringae pv.
              lachrymans/
              angular leaf
              spot;
              Colletotrichum  ME1 + GB03                    NA
              orbiculare/     INR7 + ME1 + GB03             NA
              anthracnose
            Colletotrichum    Pseudomonas putida           +153
              orbiculare/       89B-61                ([paragraph])
              anthracnose
                              Serratia                     +153
                                marcescens
                                90-166                ([paragraph])
                              Flavomonas                   +153
                                oryzihabitans         ([paragraph])
                                INR-5
                              Bacillus pumilus             +153
                                INR-7                 ([paragraph])
  Pepper    Meloidogyne       GB03 + IN937a                 NA
              incognita/
              root-knot       GB03 + SE34                   NA
              nematode        GB03 + IN937b                 NA
                              GB03 + INR7                   NA
                              GB03 + Bacillus               NA
                                cereus C4
  Peanut    Cercosporidium    Bacillus cereus C1           -37
              personatum/                            ([double dagger])
              late leaf spot                         ([double dagger])
                              Bacillus cereus C3           -37
                                                     ([double dagger])
                                                     ([double dagger])
                              Bacillus cereus C5           -37
                                                     ([double dagger])
                                                     ([double dagger])
                              Bacillus pumilus T4          -37
                                                     ([double dagger])
                                                     ([double dagger])

                                                    Yield ([+ or -] %)
                                                        ([dagger])

                                                            %

               Pathogen/                                   ISR
Crop            disease           PGPR strain            elicitor

Monocots
  Rice      Rhizoctonia       Pseudomonas                  +25
              solani/sheath     fluorescens PF1            +23
              blight          Pseudomonas
                                fluorescens FP7
  Pearl     Sclerospora       Bacillus pumilus T4          +16
    Millet    glaucum/
              downy mildew
                              Bacillus pumilus             +40
                                INR7
                              Bacillus                     +17
                                amyloliquefaciens
                                IN937a
                              Bacillus subtilis            +33
                                IN937b
                              Bacillus pumilus             +37
                                SE34
                              Brevibaeillus                +24
                                brevis
                                IPC11
                              Bacillus subtilis            +27
                                GB03
Dicots
  Tomato    Cucumber mosaic   Bacillus pumilus             +43
              virus             SE34
                              Kluyvera                     +14
                                cryocrescens
                                IN114
                              Bacillus                     +41
                                amyloliquefaciens
                                IN937a
  Tomato    Cucumber mosaic   Bacillus subtilus            +27
              virus             IN937b
            Tomato mottle     Bacillus pumilus              +5
              virus             SE34
                              Bacillus                     +19
                                amyloliquefaciens
                                IN937a
                              Bacillus subtilus            +42
                                IN937b
  Cucumber  Erwinia           Bacillus pumilis             +27
              tracheiphila/     INR-7
              bacterial wilt

                              Serratia marcesens           +35
                                90-166
            Pseudomonas       Pseudomonas putida           +27
              syringae pv.      89B-61
              lachrymans/     Serratia marcescens          +27
              angular leaf      90-166
              spot            Flavomonas                   +16
                                oryzihabitans
                                INR-5
                              Bacillus pumilus             +28
                                INR-7
                              Bacillus pumilis             +16
                                INR-7
                              Curtobacterium               +20
                                flaccumfaciens
                                ME1
                              Bacillus pumilus             +19
                                GB03
                              INR7 + ME1                    +8
                              INR7 + GB03                   +3
  Cucumber  Pseudomonas       ME1 + GB03                   +27
              syringae pv.
              lachrymans/     INR7 + ME1 + GB3             +27
              angular leaf    Bacillus pumilus           +57 (#)
              spot              INR-7
                              Curtobacterium             +32 (#)
                                flaccumfaciens
                                ME1
                              Bacillus pumilus           +22 (#)
                                GB03
                              INR7 + ME1                 +44 (#)
                              INR7 + GB03                +41 (#)
                              ME1 + GB03                 +36 (#)
                              INR7 + MEl +               +35 (#)
                                GB03
            Pseudomonas       Bacillus pumilus           +59 (#)
              syringae pv.      INR7
              lachrymans/
              angular leaf
              spot;
              Colletotrichum
              orbicularel     Burkholderia               +43 (#)
              anthracnose       gladioli
                                IN26
                              INR7 + IN26                +66 (#)
                              INR7 + ME1 + GB03          +61 (#)
                              Bacillus pumilus           +29 (#)
                                INR-7
                              Curtobacterium             +21 (#)
                                flaccumfaciens
                                ME1
                              Bacillus pumilus           +25 (#)
                                GB03
                              INR7 + ME1                 +23 (#)
  Tomato    Pseudomonas       INR7 + GB03                +27 (#)
              syringae pv.
              lachrymans/
              angular leaf
              spot;
              Colletotrichum  ME1 + GB03                 +29 (#)
              orbiculare/     INR7 + ME1 + GB03          +34 (#)
              anthracnose
            Colletotrichum    Pseudomonas putida           +27
              orbiculare/       89B-61
              anthracnose
                              Serratia                     +27
                                marcescens
                                90-166
                              Flavomonas                   +16
                                oryzihabitans
                                INR-5
                              Bacillus pumilus             +28
                                INR-7
  Pepper    Meloidogyne       GB03 + IN937a                 -5
              incognita/
              root-knot       GB03 + SE34                  -15
              nematode        GB03 + IN937b                -17
                              GB03 + INR7                  -15
                              GB03 + Bacillus               -2
                                cereus C4
  Peanut    Cercosporidium    Bacillus cereus C1            NA
              personatum/
              late leaf spot
                              Bacillus cereus C3            NA
                              Bacillus cereus CS            NA
                              Bacillus pumilus T4           NA

                                                    Yield ([+ or -] %)
                                                        ([dagger])

                                                            %

               Pathogen/                                Pesticide
Crop            disease           PGPR strain            standard

Monocots
  Rice      Rhizoctonia       Pseudomonas                  +14
              solani/sheath     fluorescens PF1            +12
              blight          Pseudomonas
                                fluorescens FP7
  Pearl     Sclerospora       Bacillus pumilus T4           NA
    Millet    glaucum/
              downy mildew
                              Bacillus pumilus              NA
                                INR7
                              Bacillus                      NA
                                amyloliquefaciens
                                IN937a
                              Bacillus subtilis             NA
                                IN937b
                              Bacillus pumilus              NA
                                SE34
                              Brevibacillus                 NA
                                brevis
                                IPC11
                              Bacillus subtilis             NA
                                GB03
Dicots
  Tomato    Cucumber mosaic   Bacillus pumilus              NA
              virus             SE34
                              Kluyvera                      NA
                                cryocrescens
                                IN114
                              Bacillus                      NA
                                amyloliquefaciens
                                IN937a
  Tomato    Cucumber mosaic   Bacillus subtilus             NA
              virus             IN937b
            Tomato mottle     Bacillus pumilus              NA
              virus             SE34
                              Bacillus                      NA
                                amyloliquefaciens
                                IN937a
                              Bacillus subtilus             NA
                                IN937b
  Cucumber  Erwinia           Bacillus pumilis              +5
              tracheiphila/     INR-7
              bacterial wilt
                              Serratia marcesens            +5
                                90-166
            Pseudomonas       Pseudomonas putida           -21
              syringae pv.      89B-61                ([paragraph])
              lachrymans/     Serratia marcescens           -2
              angular leaf      90-166
              spot            Flavomonas                    -2
                                oryzihabitans
                                INR-5
                              Bacillus pumilus              -2
                                INR-7
                              Bacillus pumilis              NA
                                INR-7
                              Curtobacterium                NA
                                flaccumfaciens
                                ME1
                              Bacillus pumilus              NA
                                GB03
                              INR7 + ME1                    NA
                              INR7 + GB03                   NA
  Cucumber  Pseudomonas       ME1 + GB03                    NA
              syringae pv.
              lachrymans/     INR7 + ME1 + GB3              NA
              angular leaf    Bacillus pumilus              NA
              spot              INR-7
                              Curtobacterium                NA
                                flaccumfaciens
                                ME1
                              Bacillus pumilus              NA
                                GB03
                              INR7 + ME1                    NA
                              INR7 + GB03                   NA
                              ME1 + GB03                    NA
                              INR7 + MEl +                  NA
                                GB03
            Pseudomonas       Bacillus pumilus              NA
              syringae pv.      INR7
              lachrymans/
              angular leaf
              spot;
              Colletotrichum
              orbicularel     Burkholderia                  NA
              anthracnose       gladioli
                                IN26
                              INR7 + IN26                   NA
                              INR7 + ME1 + GB03             NA
                              Bacillus pumilus              NA
                                INR-7
                              Curtobacterium                NA
                                flaccumfaciens
                                ME1
                              Bacillus pumilus              NA
                                GB03
                              INR7 + ME1                    NA
  Tomato    Pseudomonas       INR7 + GB03                   NA
              syringae pv.
              lachrymans/
              angular leaf
              spot;
              Colletotrichum  ME1 + GB03                    NA
              orbiculare/     INR7 + ME1 + GB03             NA
              anthracnose
            Colletotrichum    Pseudomonas putida            -2
              orbiculare/       89B-61
              anthracnose
                              Serratia                      -2
                                marcescens
                                90-166
                              Flavomonas                    -2
                                oryzihabitans
                                INR-5
                              Bacillus pumilus              -2
                                INR-7
  Pepper    Meloidogyne       GB03 + IN937a                 NA
              incognita/
              root-knot       GB03 + SE34                   NA
              nematode        GB03 + IN937b                 NA
                              GB03 + INR7                   NA
                              GB03 + Bacillus               NA
                                cereus C4
  Peanut    Cercosporidium    Bacillus cereus C1            NA
              personatum/
              late leaf spot
                              Bacillus cereus C3            NA
                              Bacillus cereus C5            NA
                              Bacillus pumilus T4           NA

               Pathogen/                                 Comments
Crop            disease           PGPR strain       ([double dagger])

Monocots
  Rice      Rhizoctonia       Pseudomonas          foliar symptoms
              solani/sheath     fluorescens PF1
              blight          Pseudomonas
                                fluorescens FP7
  Pearl     Sclerospora       Bacillus pumilus T4  disease incidence
    Millet    glaucum/                               from a single
              downy mildew                           field trial
                              Bacillus pumilus
                                INR7
                              Bacillus
                                amyloliquefaciens
                                IN937a
                              Bacillus subtilis
                                IN937b
                              Bacillus pumilus
                                SE34
                              Brevibacillus
                                brevis
                                IPC11
                              Bacillus subtilis
                                GB03
Dicots
  Tomato    Cucumber mosaic   Bacillus pumilus     viral titer
              virus             SE34
                              Kluyvera
                                cryocrescens
                                IN114
                              Bacillus
                                amyloliquefaciens
                                IN937a
  Tomato    Cucumber mosaic   Bacillus subtilus    viral titer
              virus             IN937b
            Tomato mottle     Bacillus pumilus     foliar symptoms
              virus             SE34                 from a single
                              Bacillus               field trial
                                amyloliquefaciens
                                IN937a
                              Bacillus subtilus    foliar symptoms
                                IN937b
  Cucumber  Erwinia           Bacillus pumilis     % vines wilted from
              tracheiphila/     INR-7                a single field
              bacterial wilt                         trial; insecticide
                                                     used for pesticide
                                                     standarad
                              Serratia marcesens
                                90-166
            Pseudomonas       Pseudomonas putida   foliar symptoms
              syringae pv.      89B-61
              lachrymans/     Serratia marcescens
              angular leaf      90-166
              spot            Flavomonas
                                oryzihabitans
                                INR-5
                              Bacillus pumilus
                                INR-7
                              Bacillus pumilis     disease incidence
                                INR-7
                              Curtobacterium
                                flaccumfaciens
                                ME1
                              Bacillus pumilus
                                GB03
                              INR7 + ME1
                              INR7 + GB03
  Cucumber  Pseudomonas       ME1 + GB03           disease incidence
              syringae pv.
              lachrymans/     INR7 + ME1 + GB3
              angular leaf    Bacillus pumilus     disease severity and
              spot              INR-7                yield averaged
                                                     across methyl
                                                     bromide treated
                                                     and nontreated
                                                     field trials
                              Curtobacterium
                                flaccumfaciens
                                ME1
                              Bacillus pumilus
                                GB03
                              INR7 + ME1
                              INR7 + GB03
                              ME1 + GB03
                              INR7 + MEl +
                                GB03
            Pseudomonas       Bacillus pumilus     foliar symptoms of
              syringae pv.      INR7                 angular leaf spot
              lachrymans/                            and anthracnose;
              angular leaf                           pesticide standard
              spot;                                  used plants
              Colletotrichum                         treated with BTH
              orbicularel     Burkholderia
              anthracnose       gladioli
                                IN26
                              INR7 + IN26
                              INR7 + ME1 + GB03
                              Bacillus pumilus     disease severity and
                                INR-7                yield averaged
                                                     across methyl
                                                     bromide treated
                                                      and nontreated
                                                     field trials
                              Curtobacterium
                                flaccumfaciens
                                ME1
                              Bacillus pumilus
                                GB03
                              INR7 + ME1
  Tomato    Pseudomonas       INR7 + GB03          disease severity;
              syringae pv.                           averaged across
              lachrymans/                            methyl bromide
              angular leaf                           treated and
              spot;                                  nontreated field
              Colletotrichum  ME1 + GB03             trials
              orbiculare/     INR7 + ME1 + GB03
              anthracnose
            Colletotrichum    Pseudomonas putida   foliar symptoms;
              orbiculare/       89B-61               used plants
              anthracnose                            preinoculated with
                                                     C. orbiculare
                                                     to elicit SAR for
                                                     pesticide standard
                              Serratia
                                marcescens
                                90-166
                              Flavomonas
                                oryzihabitans
                                INR-5
                              Bacillus pumilus
                                INR-7
  Pepper    Meloidogyne       GB03 + IN937a        disease severity
              incognita/
              root-knot       GB03 + SE34
              nematode        GB03 + IN937b
                              GB03 + INR7
                              GB03 + Bacillus
                                cereus C4
  Peanut    Cercosporidium    Bacillus cereus C1   disease severity
              personatum/                            based on
              late leaf spot                         defoliation at 90
                                                     d after planting;
                              Bacillus cereus C3
                              Bacillus cereus C5
                              Bacillus pumilus T4

               Pathogen/
Crop            disease           PGPR strain             Source

Monocots
  Rice      Rhizoctonia       Pseudomonas          Nandakumar et al.,
              solani/sheath     fluorescens PF1      2001
              blight          Pseudomonas
                                fluorescens FP7
  Pearl     Sclerospora       Bacillus pumilus T4  Niranjan Raj et al.,
    Millet    glaucum/                               2003
              downy mildew
                              Bacillus pumilus
                                INR7
                              Bacillus
                                amyloliquefaciens
                                IN937a
                              Bacillus subtilis
                                IN937b
                              Bacillus pumilus
                                SE34
                              Brevibacillus
                                brevis
                                IPC11
                              Bacillus subtilis
                                GB03
Dicots
  Tomato    Cucumber mosaic   Bacillus pumilus     Zehnder et al., 2001
              virus             SE34
                              Kluyvera
                                cryocrescens
                                IN114
                              Bacillus
                                amyloliquefaciens
                                IN937a
  Tomato    Cucumber mosaic   Bacillus subtilus    Zehnder et al., 2001
              virus             IN937b
            Tomato mottle     Bacillus pumilus
              virus             SE34
                              Bacillus
                                amyloliquefaciens
                                IN937a
                              Bacillus subtilus
                                IN937b
  Cucumber  Erwinia           Bacillus pumilis     Zehnder et al., 2001
              tracheiphila/     INR-7
              bacterial wilt
                              Serratia marcesens
                                90-166
            Pseudomonas       Pseudomonas putida   Wei et al., 1996
              syringae pv.      89B-61
              lachrymans/     Serratia marcescens
              angular leaf      90-166
              spot            Flavomonas
                                oryzihabitans
                                INR-5
                              Bacillus pumilus
                                INR-7
                              Bacillus pumilis     Raupach and
                                INR-7                Kloepper, 1998
                              Curtobacterium
                                flaccumfaciens
                                ME1
                              Bacillus pumilus
                                GB03
                              INR7 + ME1
                              INR7 + GB03
  Cucumber  Pseudomonas       ME1 + GB03           Raupach and
              syringae pv.                           Kloepper, 1998
              lachrymans/     INR7 + ME1 + GB3
              angular leaf    Bacillus pumilus     Raupach and
              spot              INR-7                Kloepper, 2000
                              Curtobacterium
                                flaccumfaciens
                                ME1
                              Bacillus pumilus
                                GB03
                              INR7 + ME1
                              INR7 + GB03
                              ME1 + GB03
                              INR7 + MEl +
                                GB03
            Pseudomonas       Bacillus pumilus     Raupach and
              syringae pv.      INR7                 Kloepper, 1998
              lachrymans/
              angular leaf
              spot;
              Colletotrichum
              orbicularel     Burkholderia
              anthracnose       gladioli
                                IN26
                              INR7 + IN26
                              INR7 + ME1 + GB03
                              Bacillus pumilus     Raupach and
                                INR-7                Kloepper, 2000
                              Curtobacterium
                                flaccumfaciens
                                ME1
                              Bacillus pumilus
                                GB03
                              INR7 + ME1
  Tomato    Pseudomonas       INR7 + GB03          Raupach and
              syringae pv.                           Kloepper, 2000
              lachrymans/
              angular leaf
              spot;
              Colletotrichum  ME1 + GB03
              orbiculare/     INR7 + ME1 + GB03
              anthracnose
            Colletotrichum    Pseudomonas putida   Wei et al., 1996
              orbiculare/       89B-61
              anthracnose
                              Serratia
                                marcescens
                                90-166
                              Flavomonas
                                oryzihabitans
                                INR-5
                              Bacillus pumilus
                                INR-7
  Pepper    Meloidogyne       GB03 + IN937a        Kokalis-Burelle et
              incognita/                             al., 2002
              root-knot       GB03 + SE34
              nematode        GB03 + IN937b
                              GB03 + INR7
                              GB03 + Bacillus
                                cereus C4
  Peanut    Cercosporidium    Bacillus cereus C1   Zhang et al., 2001
              personatum/
              late leaf spot
                              Bacillus cereus C3
                              Bacillus cereus C5
                              Bacillus pumilus T4

([dagger]) NA, not available. In those papers where data for multiple
pesticide treatments are presented, calculations are based on the
pesticide treatments that were most efficacious or most representative.

([double dagger]) Refer to how disease or yield was measured; AUDPC,
area under the disease progress curve.

([paragraph]) Plants preinoculated with C. orbiculare to elicit
systemic acquired resistance.

(#) Yield assessed by main runner length.

([dagger][dagger]) Plants treated with BTH, benzo (1,2,3)
thiadiazole-7-carbothioic acid S-methyl ester (also known as
acibenzolar-S-methyl).

([double dagger][double dagger]) Disease severity across pesticide and
PGPR treatments averaged +3% relative to nontreated control at 105 d
after planting.


ACKNOWLEDGMENTS

The authors wish to thank A. Bent, L. Cooperband, C. Grau, and J. Handelsman for fruitful discussions stemming from the review of an earlier version of this manuscript.

REFERENCES

Abbasi, P.A., J. Al-Dahmani, F. Sahin, H.A.J. Hoitink, and S.A. Miller. 2002. Effect of compost amendments on disease severity and yield of tomato in conventional and organic production systems. Plant Dis. 86:156-161.

Agostini, J.P., P.M. Bushong, and L.W. Timmer. 2003. Greenhouse evaluation of products that induce host resistance for control of scab, malanose, and Alternaria brown spot of citrus. Plant Dis. 87: 69-74.

Agrawal, A. 1998. Induced responses to herbivory and increased plant performance. Science 279:1201-1202.

Agrawal, A. 1999. Induced responses to herbivory in wild radish: Effects on several herbivores and plant fitness. Ecology 80:1713-1723.

Agrawal, A., S.Y. Strauss, and M.J. Stout. 1999. Costs of induced resistance and tolerance to herbivory in male and female fitness components of wild radish. Evolution 53:1093-1104.

Baldwin, I.T. 1998. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc. Natl. Acad. Sci. USA 95:8113-8118.

Benhamou, N., and M. Nicole. 1999. Cell biology of plant immunization against microbial infection: The potential of induced resistance in controlling plant diseases. Plant Physiol. Biochem. 37:703-719.

Bergelson, J. 1994. The effects of genotype and the environment on costs of resistance in lettuce. Am. Nat. 143:349-359.

Bergelson, J., and C.B. Purrington. 1996. Surveying patterns in the cost of resistance in plants. Am. Nat. 148:536-558.

Boehm, M.J., and H.A.J. Hoitink. 1992. Sustenance of microbial activity in potting mixes and its impact on severity of Pythium root rot of poinsettia. Phytopathology 82:259-264.

Bostock, R.M. 1999. Signal conflicts and synergies in induced resistance to multiple attackers. Physiol. Mol. Plant Pathol. 55:99-109.

Bousset, L., and J. Pons-Kuhnemann. 2003. Effects of acibenzolar-S-methyl and ethirimol on the composition of a laboratory population of barley powdery mildew. Phytopathology 93:305-315.

Buonaurio, R., L. Scarponi, M. Ferrara, P. Sidoti, and A. Bertona. 2002. Induction of systemic acquired resistance in pepper plants by acibenzolar-S-methyl against bacterial spot disease. Eur. J. Plant Pathol. 108:41-49.

Cameron, R.K., R.A. Dixon, and C.J. Lamb. 1994. Biologically induced systemic acquired resistance in Arabidopsis thaliana. Plant J. 5:715-725.

Chester, K.S. 1933a. The problem with acquired physiological immunity in plants. Q. Rev. Biol. 8:129-154.

Chester, K.S. 1933b. The problem with acquired physiological immunity in plants (continued). Q. Rev. Biol. 8:275-324.

Cole, D.L. 1999. The efficacy of acibenzolar-S-methyl, an inducer of systemic acquired resistance, against bacterial and fungal diseases of tobacco. Crop Prot. 18:267-273.

Coley, P.D., J.P. Bryant, and S. Chapin, III. 1985. Resource availability and plant antiherbivore defense. Science 22:895-899.

Colson-Hanks, E.S., S.J. Allen, and B.J. Deverall. 2000. Effect of 2,6-dichloroisonicotinic acid or benzothiadiazole on Alternaria leaf spot, bacterial blight and Verticillium wilt in cotton under field conditions. Australas. Plant Pathol. 29:170-177.

Colson-Hanks, E.S., and B.J. Deverall. 2000. Effect of 2,6-dichloroisonicotinic acid, its formulation materials and a benzothiadiazole on systemic resistance to Alternaria leaf spot in cotton. Plant Pathol. 118:1203-1212.

Cruikshank, I.A.M., and M. Mandryk. 1960. The effect of stem infestations of tobacco with Peronospora tabacina Adam. on foliage reaction to blue mold. J. Aust. Inst. Agric. Sci. 26:369-372.

Csinos, A.S., H.R. Pappu, R.M. McPherson, and M.G. Stephenson. 2001. Management of Tomato spotted wilt virus in flue-cured tobacco with acibenzolar-S-methyl and imidacloprid. Plant Dis. 85: 292-296.

Dann, E.K., and B.J. Deverall. 1995. Effectiveness of systemic resistance in bean against foliar and soilborne pathogens as induced by biological and chemical means. Plant Pathol. 44:458-466.

Dann, E.K., and B.J. Deverall. 1996. 2,6-dichloro-isonicotinic acid (INA) induces resistance in green beans to the rust pathogen, Uromyces appendiculatus, under field conditions. Australas. Plant Pathol. 25:199-204.

Dann, E., B. Diers, J. Byrum, and R. Hammerschmidt. 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. Eur. J. Plant Pathol. 104:271-278.

De Meyer, G., and M. Hofte. 1997. Salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 induces resistance to leaf infection by Botrytis cinerea on bean. Phytopathology 87:588-593.

Dempsey, D.M.A., J. Shah, and D.F. Klessig. 1999. Salicylic acid and disease resistance in plants. Crit. Rev. Plant Sci. 18:547-575.

Drinkwater, L.E., D.K. Letourneau, F. Workneh, A.H. van Bruggen, and C. Shennan. 1995. Fundamental differences between conventional and organic tomato agroecosystems in California. Ecol. Appl. 5:1098-1112.

Friedrich, L., K. Lawton, W. Ruess, P. Masner, N. Specker, M. Gut Rella, B. Meier, S. Dincher, T. Staub, S. Uknes, J.-P. Metraux, H. Kessmann, and J. Ryals. 1996. A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J. 10:61-70.

Gaffney, T., L. Friedrich, B. Vernooij, D. Negrotto, G. Nye, S. Uknes, E. Ward, H. Kessmann, and J. Ryals. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261: 754-756.

Genoud, T., and J.P. Metraux. 1999. Cross-talk in plant cell signaling structure and function of the genetic network. Trends Plant Sc. 4:503-507.

Gorlach, J., S. Volrath, F. Knauf-Beiter, G. Hengy, U. Beckhove, K.-H. Kogel, M. Oostendorp, T. Staub, E. Ward, H. Kessmann, and J. Ryals. 1996. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8:629-643.

Hammerschmidt, R., and J. Kuc. 1995. Induced resistance to disease in plants. Klumer, Dordrecht, the Netherlands.

Hatcher, P.E., N.D. Paul, P.G. Ayres, and J.B. Whittaker. 1994. Interactions between Rumex spp., herbivores and a rust fungus: Gastrophysa viridula grazing reduces subsequent infection by Uromyces rumicis. Func. Ecol. 8:265-272.

Hatcher, P.E., and N.D. Paul. 2000. Beetle grazing reduces natural infection of Rumex obtusifolius by fungal pathogens. New Phytol. 146:325-333.

Heil, M. 2001. The ecological concept of costs of induced systemic resistance (ISR). Eur. J. Plant Pathol. 107:137-146.

Heil, M., A. Hilpert, W. Kaiser, and K.E. Linsenmair. 2000. Reduced growth and seed set following chemical induction of pathogen defence: Does systemic acquired resistance (SAR) incur allocation costs? J. Ecol. 88:645-654.

Heil, M. 1999. Systemic acquired resistance: Available information and open ecological questions. J. Ecol. 87:341-346.

Herms, D.A., and W.J. Mattson. 1992. The dilemma of plants: To grow or defend. Q. Rev. Biol. 67:283-335.

Hijwegen, T., and M.A. Verhaar. 1994. Effects of cucumber genotype on the induction of resistance to powdery mildew, Sphaerotheca faliginea, by 2,6-dichloroisonicotinic acid. Plant Pathol. 44:756-762.

Inbar, M., H. Doostdar, R.M. Sonoda, G.L. Leibee, and R.T. Mayer. 1998. Elicitors of plant defensive systems reduce insect densities and disease incidence. J. Chem. Ecol. 24:135-149.

Ishii, H., Y. Tomita, T. Horio, Y. Narusaka, Y. Nakazawa, K. Nishimura, and S. Iwamoto. 1999. Induced resistance of acibenzolar-S-methyl (CGA 245704) to cucumber and Japanese pear diseases. Eur. J. Plant Pathol. 105:77-85.

Kessler, A., and I.T. Baldwin. 2002. Plant responses to insect herbivory: The emerging molecular analysis. Annu. Rev. Plant Biol. 53: 299-328.

Kessmann, H., T. Staub, C. Hofmann, T. Maetzke, and J. Herzog. 1994. Induction of systemic acquired disease resistance in plants by chemicals. Annu. Rev. Phytopathol. 32:439-459.

Kim, Y.C., K.A. Blee, J. Robins, and A.J. Anderson. 2001. Oxycom[TM] under field and laboratory conditions increases resistance responses in plants. Eur. J. Plant Pathol. 107:129-136.

Knoester, M., C.M.J. Pieterse, J.F. Bol, and L.C. van Loon. 1999. Systemic resistance in Arabidopsis induced by rhizobacteria requires ethylene-dependent signaling at the site of application. Mol. Plant-Microb. Interact. 12:720-727.

Kokalis-Burelle, N., C.S. Vavrina, E.N. Rosskopf, and R.A. Shelby. 2002. Field evalution of plant growth-promoting rhizobacteria amended transplant mixes and soil solarization for tomato and pepper production in Florida. Plant Soil 238:257-266.

Lawton, K., K. Weymann, L. Friedrich, B. Vernooij, S. Uknes, and J. Ryals. 1995. Systemic acquired resistance in Arabidopsis requires salicylic acid but no ethylene. Mol. Plant-Microb. Interact. 6:863-870.

Lawton, K., L. Friedrich, M. Hunt, K. Weymann, T. Delaney, H. Kessmann, T. Staub, and J. Ryals. 1996. Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J. 10:71-82.

Leeman, M., J.A. van Pelt, M.J. Hendrickx, R.J. Scheffer, and P.A.H.M. Bakker. 1995a. Biocontrol of fusarium wilt of radish in commercial greenhouse trials by seed treatment with Pseudomonas fluorescens WCS374. Phytopathology 85:1301-1305.

Leeman, M., J.A. van Pelt, F.M. den Ouden, M. Heinsbroek, P.A.H.M. Bakker, and B. Schippers. 1995b. Induction of systemic resistance by Pseudomonas fluorescens in radish cultivars differing in susceptibility to Fusarium wilt, using a novel bioassay. Eur. J. Plant Pathol. 101:655-664.

Leeman, M, F.M. den Ouden, J.A. van Pelt, F.P.M. Dirkx, H. Steijl, P.A.H.M. Bakker, and B. Schippers. 1996. Iron availability affects induction of systemic resistance to Fusarium wilt of radish by Pseudomonas fluorescens. Phytopathology 86:149-155.

Leroux, P. 1996. Recent developments in the mode of action of fungicides. Pestic. Sci. 47:191-197.

Leskovar, D.I., and K. Kolenda. 2002. Strobilurin + acibenzolar-S-methyl controls white rust without inducing leaf chlorosis in spinach. Ann. Appl. Biol. 140:171-175.

Louws, F.J., M. Wilson, H.L. Campbell, D.A. Cuppels, J.B. Jones, P.B. Shoemaker, F. Sahin, and S.A. Miller. 2001. Field control of bacterial spot and bacterial speck of tomato using a plant activator. Plant Dis. 85:481-488.

Lucas, J.A. 1999. Plant immunization: From myth to SAR. Pestic. Sci. 55:193-196.

Lyon, G.D., T. Reglinski, and A.C. Newton. 1995. Novel disease control compounds: The potential to 'immunize' plants against infection. Plant Pathol. 44:407-427.

Maleck, K., A. Levine, T. Eulgem, A. Morgan, J. Schmid, K.A. Lawton, J.L. Dangl, and R.A. Dietrich. 2000. The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat. Genet. 26:403-410.

Matheron, M.E., and M. Porchas. 2002. Suppression of Phytophthora root and crown rot on pepper plants treated with acibenzolar-S-methyl. Plant Dis. 86:292-297.

Maurhofer, M., C. Hase, P. Meuwly, J.-P. Metraux, and G. Defago. 1994. Induction of systemic resistance of tobacco to tobacco necrosis virus by the root-colonizing Pseudomonas fluorescens strain CHA0: Influence of the gacA gene and of pyoverdin production. Phytopathology 84:139-146.

Maxson-Stein, K., S.-Y. He, R. Hammerschmidt, and A.L. Jones. 2002. Effect of treating apple trees with acibenzolar-S-methyl on fire blight and expression of pathogenesis-related protein genes. Plant Dis. 86:785-790.

McDonald, B.A., and C. Linde. 2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40:349-379.

McDowell, J.M., and J.L. Dangl. 2000. Signal transduction in the plant immune response. Trends Biol. Sci. 25:79-82.

Morris, S.W., B. Vernooij, S. Titatarn, M. Starrett, S. Thomas, C.C. Wiltse, R.A. Frederiksen, A. Bhandhufalck, S. Hulbert, and S. Uknes. 1998. Induced resistance responses in maize. Mol. Plant-Microb. Interact. 7:643-658.

Murphy, J.F., G.W. Zehnder, D.J. Schuster, E.J. Sikora, J.E. Polston, and J.W. Kloepper. 2000. Plant growth-promoting rhizobacteria mediated protection in tomato against Tomato mottle virus. Plant Dis. 84:779-784.

Nandakumar, R., S. Babu, R. Viswanathan, T. Raguchander, and R. Samiyappan. 2001. Induction of systemic resistance in rice against sheath blight disease by Pseudomonas fluorescens. Soil Biol. Biochem. 33:603-612.

Niranjan Raj, S., G. Chaluvaraju, K.N. Amruthesh, H.S. Shetty, M.S. Reddy, and J.W. Kloepper. 2003. Induction of growth promotion and resistance against downy mildew on pearl millet (Pennisetum glaucum) by rhizobacteria. Plant Dis. 87:380-384.

Perez, L., M.E. Rodriguez, F. Rodriguez, and C. Roson. 2003. Efficacy of acibenzolar-S-methyl, an inducer of systemic acquired resistance against tobacco blue mould caused by Peronospora hyoscyami f. sp. tabacina. Crop Prot. 22:405-413.

Pharand, B., O. Carisse, and N. Benhamou. 2002. Cytological aspects of compost-mediated induced resistance against Fusarium crown and root rot in tomato. Phytopathology 92:424-438.

Pieterse, C.M.J., S.C.M. van Wees, E. Hoffland, J.A. van Pelt, and L.C. van Loon. 1996. Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogensis-related gene expression. Plant Cell 8:1225-1237.

Pieterse, C.M.J., S.C.M. van Wees, J.A. van Pelt, M. Knoester, R. Laan, H. Gerrits, P.J. Weisbeek, and L.C. van Loon. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571-1580.

Raupach, G.S., and J.W. Kloepper. 1998. Mixtures of plant growth-promoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology 88:1158-1164.

Raupach, G.S., and J.W. Kloepper. 2000. Biocontrol of cucumber diseases in the field by plant growth-promoting rhizobacteria with and without methyl bromide fumigation. Plant Dis. 84:1073-1075.

Raupach, G.S., L. Liu, J.F. Murphy, S. Tuzun, and J.W. Kloepper. 1996. Induced systemic resistance in cucumber and tomato against cucumber mosaic cucumovirus using plant growth promoting rhizobacteria (PGPR). Plant Dis. 80:891-894.

Rohilla, R., U.S. Singh, and R.L. Singh. 2002. Mode of action of acibenzolar-S-methyl against sheath blight of rice, caused by Rhizoctonia solani Kuhn. Pest Manag. Sci. 58:63-69.

Romero, A.M., C.S. Kousik, and D.F. Ritchie. 2001. Resistance to bacterial spot in bell pepper induced by acibenzolar-S-methyl. Plant Dis. 85:189-194.

Ross, A.F. 1961a. Localized acquired resistance to plant virus infection in hypersensitive hosts. Virology 14:329-339.

Ross, A.F. 1961b. Systemic acquired resistance induced by localized virus infections in plants. Virology 14:340-358.

Schenk, P.M., K. Kazan, I. Wilson, J.P. Anderson, T. Richmond, S.C. Somerville, and J.M. Manners. 2000. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl. Acad. Sci. USA 97:11655-11660.

Simms, E.L., and M.D. Rausher. 1987. Costs and benefits of plant resistance to herbivory. Am. Nat. 130:570-581.

Stadnik, M.J., and H. Buchenauer. 1999a. Control of wheat diseases by benzothiadiazole-derivative and modern fungicides. Zeitschrift fur Pflanzenkrankheiten und Pflanzenshutz 106:466-475.

Stadnik, M.J., and H. Buchenauer. 1999b. Effects of benzothiadiazole, kinetin and urea on the severity of powdery mildew and yield of winter wheat. Zeitschrift fur Pflanzenkrankheiten und Pflanzenshutz 106:476-489.

Sticher, L., B. Mauch-Mani, and J.-P. Metraux. 1997. Systemic acquired resistance. Annu. Rev. Phytopathol. 35:235-270.

Stone, A.G., G.E. Vallad, L.R. Cooperband, D. Rotenberg, H.R. Darby, R.V. James, W. Stevenson, and R.M. Goodman. 2003. The effect of organic amendments on soil-borne and foliar diseases in field-grown snap bean and cucumber. Plant Dis. 87:1037-1042.

Stout, M.J., R.A. Brovont, and S.S. Duffey. 1998. Effects of nitrogen availability on expression of constitutive and inducible chemical defenses in tomato, Lycopersicon esculentum. J. Chem. Ecol. 24: 945-963.

Thaler, J.S. 1999. Induced resistance in agricultural crops: Effects of jasmonic acid on herbivory and yield in tomato plants. Environ. Entomol. 28:30-37.

Thaler, J.S., A.L. Fidantsef, S.S. Duffey, and R.M. Bostock. 1999. Trade-offs in plant defense against pathogens and herbivores: A field demonstration of chemical elicitors of induced resistance. J. Chem. Ecol. 25:1597-1609.

Tian, D., M.B. Traw, J.Q. Chen, M. Kreitman, and J. Bergelson. 2003. Fitness costs of R-gene mediated resistance in Arabidopsis thaliana. Nature 423:74-77.

Ton, J., C.M.J. Pieterse, and L.C. van Loon. 1999. Identification of a locus in Arabidopsis controlling both the expression of rhizobacteria-mediated induced systemic resistnace (ISR) and basal resistance against Pseudomonas syringae pv. tomato. Mol. Plant-Microb. Interact. 12:911-918.

Ton, J., S. Davison, S.C.M. van Wees, L.C. van Loon, and C.M.J. Pieterse. 2001. The Arabidopsis ISR1 locus controlling rhizobacteria-mediated induced systemic resistance is involved in ethylene signaling. Plant Physiol. 125:652-661.

Tosi, L., and A. Zazzerini. 2000. Interactions between Plasmopara helianthi, Glomus mosseae and two plant activators in sunflower plants. Eur. J. Plant Pathol. 106:735-744.

Uknes, S., B. Mauch-Mani, M. Moyer, S. Potter, S. Williams, S. Dincher, D. Chandler, A. Slusarenko, E. Ward, and J. Ryals. 1992. Acquired resistance in Arabidopsis. Plant Cell 4:645-656.

Vallad, G.E., L.R. Cooperband, and R.M. Goodman. 2003. Plant foliar disease suppression mediated by composted forms of paper-mill residuals exhibits molecular features of induced resistance. Physiol. Mol. Plant Pathol. 63:65-77.

Vallad, G.E., A.G. Stone, R.M. Goodman, and L.R. Cooperband. 2000. Assessment of foliar disease suppression generated by paper mill sludge amendments. Phytopathology 90:S79 (Abstr.).

van Dam, N.M., and I.T. Baldwin. 1998. Costs of jasmonate-induced responses in plants competing for limited resources. Ecol. Lett. 1:30-33.

van Loon, L.C., P.A.H.M. Bakker, and C.M.J. Pieterse. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36:453-483.

van Wees, S.C.M., C.M.J. Pieterse, A. Trijssenaar, Y.A.M. van't Westende, F. Hartog, and L.C. van Loon. 1997. Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Mol. Plant-Microb. Interact. 6:716-724.

van Wees, S.C.M., E.A.M. de Swart, J.A. van Pelt, L.C. van Loon, and C.M.J. Pieterse. 2000. Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 97:8711-8716.

Vernooij, B., L. Friedrich, A. Morse, R. Reist, R. Kolkitz-Jawhar, E. Ward, S. Uknes, H. Kessmann, and J. Ryals. 1994. Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6:959-965.

Walling, L.L. 2000. The myriad plant responses to herbivores. J. Plant Growth Regul. 19:195-216.

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

Wei, G., J.W. Kloepper, and S. Tuzun. 1996. Induced systemic resistance to cucumber diseases and increased plant growth by plant growth-promoting rhizobacteria under field conditions. Phytopathology 86:221-224.

Workneh, F., and A.H.C. van Bruggen. 1994. Suppression of corky root of tomatoes in organically managed soil associated with soil microbial activity and nitrogen status of soil and tomato tissue. Phytopathology 81:688-694.

Workneh, F., A.H.C. van Bruggen, L.E. Drinkwater, and C. Sherman. 1993. Variables associated with a reduction in corky root and Phytophthora root rot of tomatoes in organic compared to conventional farms. Phytopathology 83:581-589.

Yan, Z., M.S. Reddy, C.-M. Yyu, J.A. McInroy, M. Wilson, and J.W. Kloepper. 2002. Induced systemic protection against tomato late blight by plant growth-promoting rhizobacteria. Phytopathology 92:1329-1333.

Zehnder, G.W., J.F. Murphy, E.J. Sikora, and J.W. Kloepper. 2001. Application of rhizobacteria for induced resistance. Eur. J. Plant Pathol. 107:39-50.

Zhang, S., M.S. Reddy, N. Kokalis-Burelle, L.W. Wells, S.P. Nightengale, and J.W. Kloepper. 2001. Lack of induced systemic resistance in peanut to late leaf spot disease by plant growth-promoting rhizobacteria and chemical elicitors. Plant Dis. 85:879-884.

Zhang, W., W.A. Dick, and H.A.J. Hoitink. 1996. Compost-induced systemic acquired resistance in cucumber to Pythium root rot and anthracnose. Phytopathology 86:1066-1070.

Zhang, W., D.Y. Han, W.A. Dick, K.R. Davis, and H.A.J. Hoitink. 1998. Compost and compost water extract-induced systemic acquired resistance in cucumber and Arabidopsis. Phytopathology 88:450-455.

Gary E. Vallad and Robert M. Goodman *

Gary E. Vallad, Dep. of Plant Pathology, Univ. of California-Davis, c/o U.S. Agriculture Research Station, 1636 E. Alisal St., Salinas, CA 93905; Robert M. Goodman, Dep. of Plant Pathology and Gaylord Nelson Institute for Environmental Studies, Univ. of Wisconsin, Madison, WI 53706. Received 22 Oct. 2003. * Corresponding author (rgoodman@facstaff.wisc.edu).
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Title Annotation:Review & Interpretation
Author:Vallad, Gary E.; Goodman, Robert M.
Publication:Crop Science
Date:Nov 1, 2004
Words:14601
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