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First published online August 13, 2004; 10.1104/pp.104.048694 Plant Physiology 135:2025-2037 (2004) © 2004 American Society of Plant Biologists Jasmonic Acid Is a Key Regulator of Spider Mite-Induced Volatile Terpenoid and Methyl Salicylate Emission in Tomato1,[w]Swammerdam Institute for Life Sciences, Department of Plant Physiology (K.A., M.A.H., R.C.S.) and Institute for Biodiversity and Ecosystem Dynamics (M.R.K., M.W.S.), University of Amsterdam, 1098 SM Amsterdam, The Netherlands
The tomato (Lycopersicon esculentum) mutant def-1, which is deficient in induced jasmonic acid (JA) accumulation upon wounding or herbivory, was used to study the role of JA in the direct and indirect defense responses to phytophagous mites (Tetranychus urticae). In contrast to earlier reports, spider mites laid as many eggs and caused as much damage on def-1 as on wild-type plants, even though def-1 lacked induction of proteinase inhibitor activity. However, the hatching-rate of eggs on def-1 was significantly higher, suggesting that JA-dependent direct defenses enhanced egg mortality or increased the time needed for embryonic development. As to gene expression, def-1 had lower levels of JA-related transcripts but higher levels of salicylic acid (SA) related transcripts after 1 d of spider mite infestation. Furthermore, the indirect defense response was absent in def-1, since the five typical spider mite-induced tomato-volatiles (methyl salicylate [MeSA], 4,8,12-trimethyltrideca-1,3,7,11-tetraene [TMTT], linalool, trans-nerolidol, and trans-  -ocimene) were not induced and the predatory mite Phytoseiulus persimilis did not discriminate between infested and uninfested def-1 tomatoes as it did with wild-type tomatoes. Similarly, the expression of the MeSA biosynthetic gene salicylic acid methyltransferase (SAMT) was induced by spider mites in wild type but not in def-1. Exogenous application of JA to def-1 induced the accumulation of SAMT and putative geranylgeranyl diphosphate synthase transcripts and restored MeSA- and TMTT-emission upon herbivory. JA is therefore necessary to induce the enzymatic conversion of SA into MeSA. We conclude that JA is essential for establishing the spider mite-induced indirect defense response in tomato.
Plants protect themselves against herbivores through a combination of constitutive and inducible defenses that decrease herbivore performance. Induced defenses are characterized by changes in morphology and increases in secondary metabolites or defense-associated proteins. If such changes lower the food quality for herbivores they are referred to as direct defense. Plants may also acquire protection indirectly, for example via the production of herbivore-induced volatiles that attract the natural enemies of the herbivores, such as predators and parasitoids (for review, see Dicke et al., 1998  ; Baldwin and Preston, 1999; Sabelis et al., 1999).
In tomato (Lycopersicon esculentum), jasmonic acid (JA) and Systemin (Sys) are the key molecules that mediate local and systemic signaling, leading to direct defense-related gene expression. In the model proposed by Li et al. (2002a)
The role of jasmonate in tomato defense signaling has been studied by making use of the JA-biosynthesis mutants def-1, spr-1 and spr-2 and the JA-perception mutant jai1-1 (Li et al., 2002a
It has been established that jasmonate precursors and derivatives or JA itself can induce the emission of volatiles similar to those induced by herbivory such as 4,8-dimethyl-1,3,7-nonatriene (DMNT) and 4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT) as well as the monoterpenes linalool and
The beet army worm (Spodoptera exigua) induced lower amounts of Here we report that tomato-reared spider mites induced transcription of direct defense genes related to SA primarily, and no indirect defenses in def-1. Nevertheless, the spider mites performed only as well on def-1 as on the wild type. Through combined transcriptomics, volatile-metabolomics and behavioral analyses, we characterized the tomato response to spider mites and we were able to demonstrate that the indirect defense response of tomato to spider mites is orchestrated by JA. Moreover, we provide preliminary evidence for cross talk between JA and SA at the interface of direct and indirect defenses through JA-mediated volatilization of SA.
Spider Mites Perform Equally Well on def-1 and Wild Type In order to assess whether the def-1 mutation affected the rate in which spider mites damaged leaves and produced offspring, we measured the area of chlorotic lesions caused by spider mite-feeding and counted the number of eggs they produced. Figure 1A shows the damage in mm2 of chlorotic leaf area per mite over a period of 5 d on wild-type and def-1 plants. The damage was 1.06 ± 0.21 mm2 per mite per day on the wild type and 1.16 ± 0.10 mm2 per mite per day on def-1. Each 2-d-old adult female laid on average 38.1 ± 2.3 eggs in 5 d on the wild type and 44 ± 3.7 on def-1 (Fig. 1B).
Spider Mite Eggs Produced on def-1 Are More Viable To determine whether the def-1 mutation affected spider mite-egg viability, we counted the number of juveniles (protonymphs) that had emerged on day 5 (the 1st d eggs hatched), 6, and 7 after infesting wild-type and def-1 plants. Repeated measures ANOVA (df = 1) revealed that the hatching rate from day 5 to day 7 on def-1 was significantly higher than on the wild type (F = 7.4; P = 0.014). The ratio of juveniles to eggs on day 7 was 0.37 ± 0.05 on the wild type and 0.58 ± 0.07 on def-1 (Fig. 1C).
As a measure of the direct defense, we determined the proteinase activity in infested and uninfested leaves. We performed a full factorial ANOVA on the data, discriminating between plant-type (wild type and def-1), treatment (control and infested), and time (day 1 and day 4). ANOVA (df = 1) showed that all three factors were significantly different (plant-type, F = 31.76; P = 0.0001; treatment, F = 11.74; P = 0.009; time, F = 8.04; P = 0.022). We subsequently performed a Fisher post hoc test (df = 8) on the separate samples. The infested wild-type samples from day 1 differed significantly from all other samples (P < 0.05), except from the uninfested wild-type sample for day 4 (P = 0.3). The infested wild type day 4 samples differed from all other samples (P < 0.007). No other samples were significantly different from each other (Fig. 2). These data confirm that def-1, unlike wild-type tomato, was unable to produce proteinase inhibitor activity in response to spider mite herbivory, as previously reported (Li et al., 2002b
SA-Related Transcript Accumulation Is Higher in def-1
DNA microarray analyses were used to determine the effect of spider mite-infestation on the induction of gene-expression, in def-1 and wild-type plants. A dedicated microarray with 428 tomato expressed sequence tags (ESTs) was used, as described by Kant et al. (2004)
To identify genes regulated by DEF-1, microarray slides were hybridized simultaneously with probes from def-1 and Castlemart, the corresponding wild type, after 1 d of spider mite infestation, in three independent experiments. Only nine genes were induced or repressed in the wild type compared to def-1 (Table II). Wound inducible-proteinase inhibitor I and II and Leu aminopeptidase were more highly expressed in the wild type, illustrating their dependence on JA. Remarkably, two SA-inducible PR-genes (PR-P4, Fidantsef et al., 1999 ; and PR-P6, Tornero et al., 1997) were higher expressed in def-1 after 1 d. For P6 we confirmed this by RNA gel-blot analysis for the three sets of RNA used for the microarrays (ratio def-1:wild type 2.3 ± 0.7). This finding indicates that DEF-1 is important in up-regulating JA-responsive genes and down-regulating SA-regulated genes. Moreover, the def-1 mutation seems to affect only a specific set of genes since the differences between the transcriptome of def-1 and wild type were very limited (Table II).
To visualize transcript levels for a selection of genes over 5 d, the whole period of spider mite-infestation, RNA gel-blot analysis was used and the difference in expression between wild type and def-1 was evaluated by means of ANOVA. Expression of the Phe ammonia lysase (PAL) gene, identified by microarray analysis, remained higher in wild type over the period of 5 d (Fig. 3A; P < 0.001), confirming that the expression of this gene is influenced by the def-1 mutation. The transcript levels of the SA-related gene PR-P23 (Rodrigo et al., 1993 ), were different in def-1 and wild type (Fig. 3B; P = 0.0013), with the largest difference on day 4 (Fisher post hoc P = 0.01). Expression of PR-P6 was also different between wild type and def-1 (Fig. 3C; P = 0.007) with the largest difference also on day 4 (P = 0.04). This indicates that the deficiency of inducible JA--accumulation in def-1 (Li et al., 2002b) leads to higher expression levels of SA-related genes. For spider mite infested lima beans it is known that SA levels increase between day 1 and day 3 while JA levels remain constant during that period after an initial increase during the 1st d of infestation (Arimura et al., 2002). This increase in SA levels during the later periods of spider mite-infestation could correspond with the expression of SA-related genes in tomato (Fig. 3, B and C). We also analyzed the transcript levels of a member of the diacylglycerol kinase (DGK) family (Fig. 3D), since this gene was induced by spider mites in wild-type tomato (Kant et al., 2004). Transcript levels of DGK were higher in the wild type on all days during spider mite infestation (Fisher post hoc test; P < 0.001 for all days), indicating that the expression of this gene this is DEF1-dependent. This illustrates that the rigorous criteria of our microarray analysis can eliminate clones with low and variable expression levels.
Spider Mites Do Not Induce Emission of Volatiles in def-1 Plants
Because jai1-1 has low constitutive levels of (mono) terpenes (Li et al., 2004
As a marker for the indirect defense, we assessed the temporal emission of volatile organic compounds by infested and uninfested intact plants over a period of 5 d (n = 9). We identified 9 monoterpenes, 13 sesquiterpenes, 2 aromatics, and 2 homoterpenes. Uninfested wild-type plants emitted higher amounts of -caryophyllene and -phellandrene while uninfested def-1 plants emitted more of  -gurjunene, although none of these differences were significant. The emitted compounds -myrcene, linalool, and limonene (Table IV) were not identified in the internal pools (Table III), while -phellandrene and cis--ocimene were not detected in the headspace of tomato. We did not find significant differences between volatiles emitted by spider mite-infested and uninfested def-1. The sesquiterpene -copaene was emitted in higher amounts by def-1 than by wild type (Fisher post hoc test: P = 0.009) but its emission was independent of spider mite infestation (Fisher post hoc test: P = 0.99). -Copaene was present at very low amounts in the internal pool of volatiles (Table III). When expressed in microgram emission per gram fresh weight per 5 d, over 75% of the tomato headspace consisted of TMTT and MeSA while the internal pool of wild type and def-1 consisted primarily out of the monoterpenes 2-carene (±11%), -terpinene (±7%), and -phellandrene (±54%). However, 2-carene and -terpinene were only present in low amounts in the headspace of tomato.
We did not find volatiles that were emitted exclusively by wild type or def-1 but for several volatiles we found significant quantitative differences. The emission of 5 volatiles (trans- -ocimene, linalool, trans-nerolidol, TMTT, and MeSA) were induced by spider mites in wild type plants (Table IV). Moreover, none of these volatiles were induced by spider mites in def-1. Full factorial ANOVA showed that induced-emission of all five compounds was mutually dependent on induction by spider mites and on DEF1 (Table IV), strongly suggesting that their induction by spider mites is JA-dependent.
We investigated whether predatory mites (the natural enemies of spider mites) discriminated between odors from infested and uninfested wild-type plants and odors from infested and uninfested def-1 plants. We recorded the behavioral response of predatory mites submitted to the odors of plants infested with spider mites and uninfested plants, by using a Y-tube olfactometer (Bruin et al., 1992
Exogenous JA Restores Induction of MeSA and TMTT Emission in def-1 To test whether volatile emission by def-1 could be restored, we pretreated intact def-1 plants with three different JA concentrations and infested them with spider mites. We sprayed intact plants with 3 mL JA (treatment) or with 3 mL water (control) 2 h prior to infesting them with spider mites. The absolute amounts of emitted volatiles were evaluated by means of ANOVA and Dunnett's post hoc test. We found a significant increase in MeSA (Fig. 5A) and TMTT (Fig. 5B) emission by plants treated with 0.25 mM JA. TMTT emission was approximately nine times higher than from the infested def-1 control, but approximately three times lower than from infested wild-type plants. Induced emission of none of the other identified volatiles was significantly affected by the JA-pretreatments.
Exogenous JA Restores Induction of SAMT and GGPPS Transcripts in def-1
In addition to measuring induction of MeSA emission, we investigated whether spider mites could induce transcription of SAMT in def-1 and wild type. SAMT was up-regulated in wild-type plants (approximately 4-fold after 2 d) but not in def-1 (Fig. 6; Fisher post hoc test; for all days of infestation P < 0.02), indicating a dependence on JA for induction. We then determined the effect of exogenous JA on the transcript levels of SAMT. We sprayed intact plants with 3 mL 0.25 mM JA (treatment) or with 3 mL water (control) 2 h prior to infesting them with spider mites and sampled after 24 h. Quantitative reverse transcription (RT)-PCR analysis showed that SAMT was expressed on average 1.7-times higher in untreated, spider mite-infested wild type than def-1 after 24 h (Fig. 7). In plants treated with JA, levels of SAMT increased in both wild type and def-1 to matching levels (Fig. 7). JA also induced the expression of WIPI but expression levels in def-1 were not as high as in wild-type plants. We also investigated the transcript levels of a putative geranylgeranyldiphosphate synthase (GGPPS). Geranylgeranyldiphosphate is a precursor of diterpenes and TMTT (Boland et al., 1998
In this study we have shown that the spider mite-induced indirect defense response in tomato is JA-dependent. First, we have shown that tomato-reared spider mites perform equally well on def-1 and wild-type tomato, but that the offspring is more viable on def-1. Second, spider mite-induced gene expression in def-1 was predominantly related to the SA-mediated defense-response. Third, predatory mites were only attracted to spider mite-infested wild-type plants but not to def-1. Fourth, transcription of SAMT and GGPPS was enhanced in spider mite-infested def-1 after pretreatment with JA, concomitant with restoration of spider mite-induced MeSA and TMTT emission.
In our experiments, spider mites performed equally well on def-1 and wild-type plants (±40 eggs per mite after 5 d; see Fig. 1B). This result contrasts with that of Li et al. (2002b)
The function of DEF-1 is not yet clear, but Howe et al. (1996)
This study shows that the def-1 mutation prevented tomato from mounting its indirect defense. The mutation did not result in an overall terpene deficiency in leaves, as in jai1 tomato fruits and sepals (Table III; Li et al., 2004
Although the def-1 mutation allowed for higher expression of SA-related genes, emission of MeSA in def-1 only increased after treatment with JA. This is striking since emission of MeSA has been shown to be positively dependent on levels of SA in tobacco (Shulaev et al., 1997
The emission of TMTT coincided with that of MeSA and was not induced in def-1 (Table IV). In addition, the emission of TMTT by spider mite-infested def-1 increased significantly after the plants had been treated with exogenous JA (Fig. 5). TMTT is a volatile homoterpene-derivate of geranylgeranyl diphosphate (Boland et al., 1998
Predatory mites are the natural enemies of spider mites and since they are blind they use induced plant-odors to locate plants containing prey. Thaler et al. (2002)
Plant Material and Arthropod Rearing
Tomato (Lycopersicon esculentum Mill cv Castlemart, cv Moneymaker, and def-1) seedlings were grown in a greenhouse with day/night temperatures of 23°C to 18°C and a 16/8-h light/dark regime. Def-1 was kindly provided by Greg Howe (Department of Energy-Plant Research Laboratory, Michigan, USA) and was previously described in Howe and Ryan (1999)
The two-spotted spider mite Tetranychus urticae Koch was originally obtained in 1993 from tomato plants in a greenhouse (Houten, The Netherlands; Gotoh et al., 1993 The colony of the predatory mite Phytoseiulus persimilis was originally maintained in the laboratory on detached lima bean-leaves infested with spider mites for more than 3 years. Prior to all experiments predatory mites were transferred to intact tomato plants (cultivar Castlemart) infested with spider mites and maintained for approximately 1 month in a climate room at 23°C, a 16/8-h light regime with 100 µE m–2 s–1 and 70% relative humidity. Adult female predatory mites were collected from this culture for the olfactory-choice assays.
For the microarray, RNA gel-blot and volatile-sampling experiments, adult female spider mites were collected from the base culture. The mites were placed gently on the adaxial surface of the fully expanded terminal leaflets using a soft-bristle paintbrush. In each experiment 15 mites were introduced per leaflet, on each plant 3 leaflets in total, except for the leaf damage and fecundity assay where respectively 4 and 7 mites were introduced per leaflet. Plants were always 3 weeks old and contained 4 fully expanded leaves, which were chosen for infestation, and 2 emerging leaves. The infestation procedure was performed without wounding or damaging the plant. We never observed spider mites dispersing to adjacent leaflets during the period of the experiment.
The total area of chlorotic lesions on spider mite-infested leaves was measured as described in Kant et al. (2004)
PI activity assays were performed in duplo on wild-type plants and def-1 as described in Kant et al. (2004)
Olfactory-choice assays for predatory mites were conducted using the Y-tube olfactometer, as previously described by Bruin et al. (1992)
Microarray analysis was performed as described in Kant et al. (2004)
The spot signal intensities of the arrays were corrected by subtracting the local background as assessed by ArrayVision software. In addition, we calculated for each clone the average signal-to-noise ratio (S:N). The background-subtracted spot signal intensities were normalized using a Lowess-normalization procedure. From this data, the average signal intensity ratio (infested wild type versus infested def-1 and infested def-1 versus uninfested def-1) and SE of these ratios was calculated. For calculation of the significance of up- or down-regulation we used a nested-design ANOVA. The obtained P-values for all clones were adjusted for multiple testing, using Benjamini and Hochberg's (1995)
Northern analysis on wild-type cv Castlemart and def-1 were performed as described in Verdonk et al. (2003) For RT-PCR determination of transcript levels, 10 µg of total RNA was used to synthesize first-strand cDNA using an 18-mer dT-primer and SuperScript II RNase H-reverse transcriptase (Invitrogen, Carlsbad, CA) in the supplied buffer at 42°C. For each gene we determined the range of PCR amplification that was still linear in order to quantify the amounts of PCR product. Therefore various number of PCR-cycles were run for each gene after which the PCR products were separated on agarose gels, blotted onto nylon membranes and hybridized with the corresponding radioactively labeled probe. Subsequently the PCR products were quantified by phosphoimaging (see above) to determine the number of cycles at which linear amplification occurred. PCR amplification of UBQ (TC116081) fragments (0.723 kb) comprised 15, 18, and 20 cycles (each cycle: 94°C for 60 s, 55°C for 45 s, and 72°C for 75 s) with forward primer, 5'-GATTCTCTCTCATCAATCAATTCG-3' and reverse primer, 5'-GCATCCAAACTTTACAGACTCTC-3'; for WIPI-2 (0.601 kb) 10, 14, and 17 cycles with forward primer, 5'-GACAAGGTACTAGTAATCAATTAT-3' and reverse primer, 5'-CACATAACACACAACTTTGATGCC-3'; for SAMT (0.440 kb) 18, 20, and 25 cycles with forward primer, 5'-CAATAAGAGATCAAGCCATAAG-3' and reverse primer, 5'-CTTGGTGGACTTGTACTTGCC-3' and 25, 30, and 35 cycles for GGPPS (0.323 kb) with forward primer, 5'-GCAATCAATGTAAACAAAGCAC-3' and reverse primer, 5'-CAAAGATATAAGTGCATCCCATC-3'. The cDNA for SAMT (TC 125218) and for GGPPS (TC 130320) were obtained from The Institute for Genomic Research (TIGR).
Volatiles of def-1 and Castlemart wild-type plants were collected, identified, and quantified on the basis of an internal standard and synthetic external standards of known concentration as described in Kant et al. (2004)
For determination of total terpene content, 250 mg leaf material was harvested, frozen in liquid nitrogen, and ground to a fine powder. Care was taken to select leaves from the same age. After addition of 0.1 µg benzyl acetate as an internal standard, samples were extracted in 2 mL pentane while vigorous shaking for 1 h. Pentane extracts were dehydrated with 250 mg Na2SO4 and 10 times concentrated by a stream of N2 at 4°C. One µL was injected into an Optic (ATAS, GL International, Zoetermeer, The Netherlands) injection port at 50°C, which was heated to 275°C at 4°C s–1. The split flow was 0 mL min–1 for 2 min and then 25 mL min–1 until the end of the run. Compounds were separated on a capillary DB-5 column (10 m x 180 µm, film thickness 0.18 µm; Hewlett-Packard, Palo Alto, CA) at 40°C for 3 min and then at 30°C min–1 to 250°C with He (37 kPa) as the carrier gas. The column flow was 3 mL min–1 for 2 min and 1.5 mL min–1 thereafter. Mass spectra of eluting compounds were collected on a Time-of-Flight-MS (Leco, Pegasus III) with a 60 s solvent delay at –1597 eV (ion source at 200°C), at an acquisition rate of 20 spectra s–1. Compounds were identified and quantified on the basis of the internal standard and synthetic external standards of known concentration as described in Kant et al. (2004)
A stock solution of 0.1 M JA was prepared by dissolving (±)-jasmonic acid (Duchefa, Haarlem, The Netherlands) in ethanol and diluting the solution 10 times with water. A solution of 10% ethanol was used as a stock for the control. The 0-, 0.05-, 0.25-, and 0.5-mM working solutions were prepared by diluting the stock solutions with water. For measuring the volatiles emitted by JA-treated plants, sets of three plants were misted with 3 mL of solution in such a way that all leaflets carried clearly visible droplets. The plants were allowed to dry in a climate room for 2 h before the introduction of spider mites. The volatiles emitted during the first 24 h after infestation were collected as described in the volatile analysis section. To obtain leaves from intact plants treated with JA for RNA extraction, the same procedure was followed as described above, except that only the 0.25 mM JA solution and the water control were used for spraying. Two plants were used per treatment. After 24 h plants were removed from the volatile-sampling set up and leaves were harvested, frozen in liquid nitrogen and stored at –80°C.
Upon request, all novel materials described in this publication will be made available in a timely manner for noncommercial research purposes, subject to the requisite permission from any third-party owners of all or parts of the material. Obtaining any permission will be the responsibility of the requestor.
We thank Greg Howe (Department of Energy-Plant Research Laboratory, East Lansing, Michigan) for providing us with def-1. We also thank Rene Braakman (ATAS Benelux, Zoetermeer, The Netherlands) and Alan Musgrave for their valuable comments. Natali Rianika Mustafa (RUL, Leiden, The Netherlands) is kindly thanked for the SA and SAG assays. Received June 24, 2004; returned for revision June 29, 2004; accepted June 29, 2004.
1 This work was supported by NWO, The Netherlands Organization for Scientific Research (ALW 812.04.004 to M.R.K.). 
2 These authors contributed equally to the paper.
[w] The online version of this article contains Web-only data. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.048694. * Corresponding author; e-mail kant{at}science.uva.nl; fax 31–20–5257754.
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0.05); (2) an average S/N 
2; and (3) the minimal treatment-1/treatment-2 ratio of >1.6 or <-1.6 on the basis of our RNA gel-blot controls. All cDNAs in 
