Compatibility of Plant Defense Elicitors with Aphid- and Nematode-Resistant Tomato Varieties in Integrated Pest Management

Project Overview

Project Type: Graduate Student
Funds awarded in 2003: $10,034.00
Projected End Date: 12/31/2004
Region: Southern
State: Arkansas
Graduate Student:

Annual Reports


  • Vegetables: tomatoes


  • Crop Production: application rate management
  • Farm Business Management: whole farm planning
  • Pest Management: chemical control, genetic resistance


    The goals of this project were to evaluate the effects of several forms of host-plant resistance in tomato (Lycopersicon esculentum) on potato aphids (Macrosiphum euphorbiae) and root-knot nematodes (Meloidogyne javanica), and to determine if these forms of resistance can be used simultaneously for enhanced protection against these pests. The first form of resistance we evaluated was Mi-mediated resistance. Mi-1.2 is a single dominant resistance gene (R-gene) that confers resistance against potato aphids, root-knot nematodes, and sweet-potato whiteflies. The goal of this study was to determine whether Mi-mediated resistance is compatible with induction of two different forms of acquired resistance. One form of acquired resistance we evaluated was systemic acquired resistance (SAR), a form of acquired resistance that is dependent upon salicylic acid (SA), and is primarily associated with pathogen protection. Foliar application of an SA analog, benzothiadiazole (BTH), was used to induce SAR in a susceptible tomato cultivar that lacks Mi-1.2, and a resistant cultivar that carries the gene. BTH treatment reduced the population growth of two different aphid isolates on both the susceptible and the resistant tomato cultivars. These results indicate that SAR is an effective defense against aphids, and can be combined with R-gene mediated resistance for enhanced aphid control.

    This study also examined another form of acquired resistance in tomato, jasmonate-dependent induced resistance (IR). IR is known to deter feeding by chewing insects, but its effects on piercing-sucking insects such as aphids have not previously been extensively investigated. A foliar application of synthetic jasmonic acid (JA) was used to induce IR in both susceptible (Mi-) and resistant (Mi+) tomato cultivars. Induction of IR triggered expression of a JA-inducible proteinase inhibitor in both the susceptible and the resistant tomato cultivars, although the effects of JA treatment on aphid performance differed between these cultivars. JA-treatment significantly reduced aphid population growth on the susceptible tomato cultivar, but it did not influence aphid numbers on a near-isogenic resistant tomato cultivar. Thus, although JA-dependent IR is an effective defense against aphids, it does not appear to interact synergistically with Mi-mediated aphid resistance.

    The mechanisms of different forms of resistance may influence whether they have a synergistic effect against attackers. In order to characterize the mode of action of IR, this study also examined the effects of JA application on the life parameters of individual potato aphids and their progeny on resistant (Mi+) and susceptible (Mi-) tomato plants with and without JA treatment. JA-treatment did not influence the survivorship or fecundity of aphids on resistant plants, which confirms the results of our previous population growth studies. In contrast, on the susceptible tomato cultivar, JA-dependent defenses significantly reduced the longevity and net reproduction of adult aphids, and reduced the number of juveniles to survive to maturity. These results indicate that JA application induces systemic defenses in susceptible tomato that have a direct negative effect on aphid survivorship. In an additional experiment, aphid excretion rates were used as an indirect measure of aphid feeding to determine if IR and/or Mi-mediated resistance had antixenotic effects. The average honeydew excretion per aphid was lower on resistant plants carrying Mi-1.2, confirming previous findings that Mi-mediated resistance deters aphid feeding. However, honeydew excretion was comparable on plants with and without JA treatment, indicating that JA-dependent defenses did not deter feeding. This suggests that the effect of JA on aphid performance was due to anti-digestive and/or toxic factors. These results could explain why activation of JA-dependent defenses didn’t enhance resistance conferred by Mi-1.2. Potentially, the effects that Mi-mediated resistance has on aphid feeding could inhibit aphids from coming into contact with JA-induced resistance factors.

    We also evaluated whether artificial induction of acquired resistance would enhance Mi-mediated resistance against root-knot nematodes. Mi-1.2 is the only known source of resistance against root-knot nematodes in cultivated tomato, and this resistance has remained stable throughout decades of use. Despite the importance of resistant cultivars, the effectiveness of Mi-mediated resistance is limited in certain growing regions. Mi-mediated resistance is temperature-sensitive, and becomes unstable at soil temperatures above 30°C. This could limit the use of resistant cultivars in tropical and subtropical tomato growing regions. Major goals of this study were to determine the effects of JA-dependent defenses in tomato on root-knot nematode performance, and to determine if JA treatment can enhance nematode protection offered by Mi-1.2. This study investigated whether artificial induction of JA could provide tomato plants with protection against nematode infection at high soil temperatures. The results from this study indicate that JA application induces a systemic defense response in the roots of susceptible tomato, and has a negative impact on root-knot nematodes. Furthermore, we found that JA-dependent defenses are heat-stable, and protect tomato at temperatures that reduce the effectiveness of Mi-mediated resistance. At 25°C, JA application did not significantly enhance or inhibit resistance conferred by Mi-1.2; however, JA treatment may potentially enhance nematode control on resistant plants at 30°C. These results are the first to indicate that JA-dependent defenses are effective against a parasitic nematode, and to suggest that artificial induction of JA could be used to control root-knot nematodes on tomato.


    Tomato production is an important component of American agriculture. On a list of the top 34 vegetable crops in the U.S., fresh market tomatoes rank sixth in total acreage and second in total value grossing over one billion dollars in 2001 (United States Department of Agriculture, 2002). Tomato production is particularly important to the economy of the Southern United States. Of the thirteen states that represent the Southern growing region, as defined by the Sustainable Agriculture Research and Education (SARE) program, commercial tomato production is found in nine of these states (AL, AR, FL, GA, NC, SC, TN, TX, and VA). In fact, the South comprises 49% of the country’s fresh market tomato acreage, and produces 57% of the national commodity (United States Department of Agriculture, 2002). Tomato is also important because it acts as an alternative crop for small Southern tobacco farms affected by declined profitability in tobacco production (SARE, 2002).

    Despite its economic importance, the fresh market tomato industry is currently endangered due to its dependence on pesticides that are disappearing from the market. Southern tomato growers are particularly threatened by the phase-out of methyl bromide and the proposed ban on organophosphate and carbamate pesticides. Methyl bromide is an effective soil fumigant that is widely used to control root-knot nematodes on tomato (Bloem et at. 2001). The Environmental Protection Agency (EPA) mandated the phase-out of methyl bromide fumigation by the year 2005. The loss of this pesticide could cause a substantial reduction in the nation’s total tomato acreage; for example, it is predicted that Florida could experience a 69% reduction in tomato acreage (Spreen et al., 1995). To date, no suitable alternative offers the same broad-spectrum control (Bloem et al., 2001). Tomato producers also rely heavily on organophosphates and carbamates to control insects and other pests, including the potato aphid and root knot nematodes. Many insecticides belonging to these two pesticide families have already been banned or heavily restricted. Legislation is pending that will mandate the ban of both pesticide families entirely from the market. The loss of these insecticides is predicted to result in a 13% increase in production costs for tomato growers, 15% decreased yield, and increased competition from foreign markets (FFBF, 1999). The state most vulnerable to reduced yields and increased production costs is Florida, with a predicted 21% loss in yield production and 20% cost increase (FFBF, 1999). In addition to reduced yields and increased production cost, the ban of these pesticides will result in more food imports, higher food prices for American consumers, and less consumption of nutritionally important fruits and vegetables, according to a study compiled by Texas A & M University’s Agricultural and Food Policy Center (Knutson, et al., 1999).

    The continuing loss of widely used pesticides from the market clearly demonstrates the need to develop effective alternative pest control strategies for tomato. The primary goal of this research was to identify effective alternative management strategies for two important pests of tomato: root-knot nematodes (Meloidogyne spp.), and potato aphids (Macrosiphum euphorbiae). Root-knot nematodes are soil-borne roundworms that parasitize the root systems of various vegetable crops including tomato. Symptoms include production of root galls, increased susceptibility to drought stress and pathogen attack, and premature death. Nematode infestations are known to cause substantial tomato yield reduction, making root-knot nematodes among the most significant economical pests worldwide (Williamson et. al. 1996). Potato aphids are an emerging pest of tomato that cause leaf curling, chlorosis, production of sooty mold, and increased feeding by hemipterous insects resulting in yield reduction (Walgenbach, 1997). This insect is becoming an increasingly significant problem for tomato growers because of the continuing loss of broad-spectrum insecticides from the market (Walgenbach, 1997). The combined use of resistant tomato varieties and plant defense elicitors could offer effective control against aphids and nematodes in the absence of the disappearing pesticides.

    Many commercial tomato varieties are resistant to aphids and certain species of nematodes, due to a single dominant gene (Mi-1.2) that was introduced through traditional breeding practices. Mi-1.2 is used as the only source of nematode resistance in cultivated tomato and varieties possessing this gene have been widely used for decades. These resistant varieties provide highly effective nematode control at moderate soil temperatures, but have reduced effectiveness at high temperatures. Nematode resistance begins to diminish at soil temperatures above 28°C, and is nearly 100% susceptible at 32°C (Dropkin, 1969). This suggests the use of resistant varieties could be limited to cooler spring temperatures in some southern states (Noling, 2002). Mi-mediated resistance is also effective against potato aphids with some limitations. Unlike nematode resistance that is expressed throughout the entire life of the plant, resistance against aphids is not expressed until about the plant’s reproductive age, or about six weeks after germination (Kaloshian, et al., 1995). This leaves juvenile resistant varieties susceptible to aphid infestation. Another limitation to aphid resistance is that Mi-1.2 is not effective against all biotypes of potato aphid (Goggin et al., 2000). These limitations suggest the need for additional alternative control methods.

    The use of plant defense elicitors to “immunize” plants could offer promising additional control strategies against nematodes and aphids in tomato. Plant defense elicitors are molecules that trigger induced defensive responses in plants, and thereby render plants more resistant to pests. Defense elicitors have been used to develop many new reduced risk pesticides and plant activators; for example, defense elicitors are used as active ingredients in Actigard (Syngenta Crop Protection), Messenger (Eden Bioscience), ReZist, and CaB’y (Stoller Enterprises). Of the plant elicitors that have been studied most extensively, most act by inducing one of two distinct defensive pathways in the plant: salicylic acid mediated resistance and jasmonic acid mediated resistance.

    Salicylic acid (SA) is a plant-signaling compound that plays a critical role in the induction of systemic acquired resistance to certain pests, such as many bacterial, viral, and fungal pathogens. Elicitation of SA-mediated defenses is associated with induction of pathogenesis-related proteins in the plant, and localized cell death surrounding the invading pest. Elicitors of SA-dependent defenses have been shown to reduce nematode performance on susceptible tomato varieties (K. Sitaramaiah et al., 1979; Nandi, B. et al., 1999). The effects of SA-mediated defenses on aphid performance on tomato have not yet been determined; however, SA appears to be involved in aphid resistance in winter wheat (Mohase, 2002). The first objective of this project was to determine if an SA elicitor protects susceptible tomato varieties against aphid infestation. Another objective of this work was to determine if an SA elicitor is appropriate for use on resistant varieties. Induction of SA is required for the function of Mi-1.2 (Branch et al., 2004). Potentially, prior induction of SA may enhance aphid and/or nematode resistance in tomato varieties that carry Mi-1.2. Alternatively, an SA elicitor could interfere with the function of Mi-1.2 (Vasyukova et al., 1999); therefore, it is important to determine if SA elicitors are compatible with aphid and nematode resistant varieties.

    We also tested the effects of another plant signaling compound, jasmonic acid (JA), on aphids and nematodes. JA is involved in induced resistance to many insects, and triggers increased polyphenol oxidase activity and enhanced expression of proteinase inhibitors in plants. In tomato, JA is known to play a role in induced defenses against the tobacco hornworm, corn earworm, and other chewing insects. The first goal of this study was to determine if JA application reduces aphid and/or nematode performance on a tomato cultivar lacking Mi-1.2. Another goal was to investigate whether or not JA elicitors can be used on resistant tomato varieties. Signaling conflicts are known to exist between SA and JA; for example, induction of JA-mediated insect resistance in tomato renders plants more susceptible to bacterial speck (Thaler et al., 1999). Therefore, it is important to determine whether JA elicitors will enhance or inhibit the effectiveness of aphid- and nematode-resistant tomato varieties.


    Bloem, S., Mizell, R.E. 2001. Tomato IPM in Florida. Department of Entomology and Nematology, Florida Coop. Ext. Serv., Institute of Food and Agricultural Sciences, University of Florida 1-22.

    Branch C, Hwang CF, Navarre DA and Williamson VM. 2004. Salicylic acid is part of the Mi-1-mediated defense response to root-knot nematode in tomato. Mol. Plant Microbe Interact. 17, 351-356

    Dropkin, V.H. 1969. The necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: Reversal by temperature. Phytopathol. 59, 1632-1637.

    FFBF (Floridia Farm Bureau Federation). 1999. All Pain, No Gain: FFBF News Release. 1-6.

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    euphorbiae and Myzus persicae (Hemiptera: Aphididae) to the tomato resistance gene Mi.
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    Knutson, R.D., Smith, E.G. 1999. Economic impacts of the elimination of organophosphates and carbamates onTexas Agriculture. AFPC Policy Working Paper 99-3. Agricultural and Food Policy Center, Department of Agriculture Experiment Station. Texas Agriculture Extension Service pp. 11.

    Kaloshian, I., Lange, W.H., Williamson, V.M. 1995. An aphid-resistance locus is tightly linked to the nematode-resistance gene, Mi, in tomato. Proc. Natl. Ac. Sci. 92, 662-625

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

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    Vasyukova, N.I., Zinov’eva, Il’inskaya, Gerasimova, Udalova. 1999. Salicylic acid and interaction between tomato plants and root-knot nematode, Meloidoagyne incognita. Doklady, Biol. Sci. 364, 82-84.

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    Project objectives:

    A major objective of this study was to determine if elicitors of SA- and JA-mediated plant defenses could protect tomato plants against aphid and root-knot nematode infestation. A second objective was to determine if the use of these elicitors is compatible with the use of aphid- and nematode-resistant tomato varieties. Specific objectives included:

    1. Explore the impact of SA-dependent defenses against the potato aphid on tomato cultivars with and without the resistance gene Mi-1.2

    2. Explore the impact of JA-dependent defenses against the potato aphids on tomato cultivars with and without the resistance gene Mi-1.2.

    3. Explore the impact of JA-dependent defenses against root-knot nematodes on tomato cultivars with and without the resistance gene Mi-1.2, and determine whether JA-dependent defenses protect resistant tomato at higher temperatures.

    Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture or SARE.