Resistance of Cultivated Tomato to Cell Content-Feeding Herbivores Is Regulated by the Octadecanoid-Signaling Pathway

Abstract

The octadecanoid signaling pathway has been shown to play an important role in plant defense against various chewing insects and some pathogenic fungi. Here, we examined the interaction of a cell-content feeding arachnid herbivore, the two-spotted spider mite (Tetranychus urticae Koch), with cultivated tomato (Lycopersicon esculentum) and an isogenic mutant line (defenseless-1 [def-1]) that is deficient in the biosynthesis of the octadecanoid pathway-derived signal, jasmonic acid (JA). Spider mite feeding and fecundity on def-1 plants was significantly greater than on wild-type plants. Decreased resistance of def-1 plants was correlated with reduced JA accumulation and expression of defensive proteinase inhibitor (PI) genes, which were induced in mite-damaged wild-type leaves. Treatment of def-1 plants with methyl-JA restored resistance to spider mite feeding and reduced the fecundity of female mites. Plants expressing a 35S::prosystemin transgene that constitutively activates the octadecanoid pathway in a Def-1-dependent manner were highly resistant to attack by spider mites and western flower thrips (Frankliniella occidentalis), another cell-content feeder of economic importance. These findings indicate that activation of the octadecanoid signaling pathway promotes resistance of tomato to a broad spectrum of herbivores. The techniques of amplified fragment length polymorphism (AFLP) and bulk segregant analysis were used to map the Def-1 gene to a region on the long arm of chromosome 3 that is genetically separable from the map position of known JA biosynthetic genes. Tight linkage of Def-1 to a T-DNA insertion harboring the maize (Zea mays) Dissociation transposable element suggests a strategy for directed transposon tagging of the gene.Plant resistance to arthropod herbivores is often mediated by phytochemicals that negatively affect the feeding, growth, or reproduction of the attacking pest (Karban and Baldwin, 1997; Walling, 2000). Although many defensive compounds have been identified from diverse plant species, relatively little is known about the underlying genetic mechanisms that control their biosynthesis in response to developmental and environmental cues. Lycopersicon spp. provide an attractive model system to address this question. Cultivated tomato (Lycopersicon esculentum) is a natural host to over 100 arthropod herbivores that feed on roots, leaves, or fruit (Lange and Bronson, 1981). Included among the major pests of tomato are adult and larval stages of Coleoptera (beetles), Lepidoptera (moths), Diptera (flies), Thysanoptera (thrips), Heteroptera (true bugs), Homoptera (aphids and whiteflies), and Acari (spider mites).Natural resistance of tomato to many herbivores is attributed to both constitutive and inducible defensive phytochemicals (Farrar and Kennedy, 1992). Among the most thoroughly studied inducible defenses in tomato are proteinase inhibitor (PI) proteins that inhibit digestive enzymes in the gut of some insect herbivores (Green and Ryan, 1972; Broadway and Duffey, 1986). Wound-induc...

The Tomato Homolog of CORONATINE-INSENSITIVE1 Is Required for the Maternal Control of Seed Maturation, Jasmonate-Signaled Defense Responses, and Glandular Trichome Development[W]

“…Third, the reduced density of type-VI trichomes on jai1 leaves was correlated with a profound loss of resistance to two-spotted spider mites. This observation is in agreement with studies showing that type-VI trichomes mediate the effective resistance of wild tomato species to spider mites and that the defense of cultivated tomato to this herbivore is regulated by endogenous JAs derived from the octadecanoid pathway (Kennedy, 2002;Li et al, 2002a). Finally, a role for LeCOI1 in glandular trichome function is supported by the effect of jai1 on defense-related exudate chemistry, including the reduced accumulation of monoterpenes that exert defensive action against insect pests (Mahmoud and Croteau, 2002;Pichersky and Gershenzon, 2002).…”

Testing for reproductive interference in the population dynamics of two congeneric species of herbivorous mites

“…This suggests that T. urticae induces plant defences that hamper the reproductive performance of other spider mites, not only through JA signalling. Previous studies showed higher reproductive performance of spider mites on a def-1 tomato mutant compared with a wild tomato (Li et al, 2002;Ament et al, 2004), but recent studies show circumstantial evidence for antiherbivore defences mediated by salicylic acid, another signal transducer mediating the expression of plant defence genes (Farouk and Osman, 2011, but see Kawazu et al, 2011). Although we recognize the possibility of a role for plant defences that are not mediated by JA, we emphasize that this does not change our conclusion regarding the impact of RI.…”

“…In a parallel experiment, we created a strong RI treatment in the founder generation by releasing heterospecific and conspecific males with virgin females, which can then mate with conspecific and heterospecific males, the latter of which can potentially result in decreased reproduction. A second advantage of using the two species of spider mites is that there is much knowledge of the impact they have on host plant defences: within leaves of tomato plants many strains of T. urticae induce the jasmonate(JA)-mediated plant defences (Li et al, 2002;Ament et al, 2004;Kant et al, 2004Kant et al, , 2008, whereas T. evansi downregulates these defences, even below household levels (Sarmento et al, 2011a), thereby making the host plant more profitable for both T. evansi and T. urticae (Sarmento et al, 2011b). By using mutant def-1 tomato plants that are deficient in mounting JA-mediated plant defences (Howe et al, 1996;Li et al, 2002;Ament et al, 2004;Kant et al, 2008), we were able to reduce the effect of JA-mediated plant defences in our competition experiments, thereby gaining more analytic power to detect RI.…”

Tomato MAPKs LeMPK1, LeMPK2, and LeMPK3 function in the systemin-mediated defense response against herbivorous insects

“…Our reduction-of-function study demonstrates that LeMPK1 and LeMPK2 are required for systemin-mediated resistance to M. sexta larvae. Antisense expression of prosystemin in transgenic tomato plants resulted in reduced defense protein accumulation and thus loss of resistance to M. sexta (6), whereas 35S::prosys plants exhibited high constitutive levels of defense proteins and increased resistance to M. sexta (1) and other insects (46). MPK1 and MPK2 play an essential role for systemin-induced defense protein synthesis, and the presence of MPK3 cannot compensate for the loss of MPK1 and MPK2 (Fig.…”