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First published online April 30, 2004; 10.1104/pp.103.038315 Plant Physiology 135:483-495 (2004) © 2004 American Society of Plant Biologists Differential Timing of Spider Mite-Induced Direct and Indirect Defenses in Tomato Plants1,[w]Institute for Biodiversity and Ecosystem Dynamics (M.R.K., M.W.S.) and Swammerdam Institute for Life Sciences, Department of Plant Physiology, University of Amsterdam, 1098 SM Amsterdam, The Netherlands (K.A., M.A.H., R.C.S.)
Through a combined metabolomics and transcriptomics approach we analyzed the events that took place during the first 5 d of infesting intact tomato (Lycopersicon esculentum) plants with spider mites (Tetranychus urticae). Although the spider mites had caused little visible damage to the leaves after 1 d, they had already induced direct defense responses. For example, proteinase inhibitor activity had doubled and the transcription of genes involved in jasmonate-, salicylate-, and ethylene-regulated defenses had been activated. On day four, proteinase inhibitor activity and particularly transcript levels of salicylate-regulated genes were still maintained. In addition, genes involved in phospholipid metabolism were up-regulated on day one and those in the secondary metabolism on day four. Although transcriptional up-regulation of the enzymes involved in the biosynthesis of monoterpenes and diterpenes already occurred on day one, a significant increase in the emission of volatile terpenoids was delayed until day four. This increase in volatile production coincided with the increased olfactory preference of predatory mites (Phytoseiulus persimilis) for infested plants. Our results indicate that tomato activates its indirect defenses (volatile production) to complement the direct defense response against spider mites.
Plants employ diverse strategies to resist or evade arthropod herbivores. Some plants accumulate constitutively high levels of compounds that function as biochemical defenses; some minimize herbivore damage through rapid growth or development, dispersion, or choice of habitat (Gatehouse, 2002  ). When a herbivore starts feeding on a plant it inflicts mechanical damage resulting in a wound response that in general is aspecific (Schaller and Frasson, 2001). However, herbivores can also produce cues that enable plants to respond in a much more targeted fashion. Such cues can be products in herbivore saliva or regurgitant (McCloud and Baldwin, 1997) but also plant products that result from herbivore damage (Pare et al., 1998). In general, the plant's direct defense response upon herbivory is characterized by the activation of signaling cascades, which leads to the formation of specific products and physiological changes that interfere with the performance of the herbivore. Additionally, it has been found that plants can produce herbivore-induced volatile metabolites. It has been proposed that this happens when direct defenses are inadequate (Kahl et al., 2000), since in many cases it appeared that these volatiles had the property of making the plant more attractive to predators or parasitoids of herbivores (Pare and Tumlinson, 1999). The attraction of natural enemies of a pest species is referred to as the indirect defense response (Sabelis et al., 2001). It is believed that the direct and the indirect defense strategies act in concert (Baldwin and Preston, 1999). However, hardly anything is known about the properties of their interaction and their interdependence.
In tomato, the herbivore-induced direct defense response is characterized by an increase in signaling compounds like jasmonate (JA), ethylene (Et), salicylate (SA) and systemin, which results in local and systemic changes, such as the accumulation of wound-inducible proteinase inhibitors (WIPIs), polyphenol oxidase, peroxidase (POD), chitinases, and callose synthase (Walling, 2000
Li et al. (2002)
The volatiles produced by tomato plants are predominantly monoterpenes, but they also produce a variety of sesquiterpenes, aromatics, aldehydes, ketones, alcohols, and esters (Andersson et al., 1980 Here we have investigated tomato's defense responses to spider mites during the first 5 d of infestation because in this period no eggs hatched. This enabled us to simultaneously assess the temporal progress of leaf damage, spider mite performance, transcriptome changes (through microarray and RNA gel-blot analysis), changes in volatile emission, and the attraction of predatory mites.
Performance of Spider Mites Spider mites caused chlorotic lesions when feeding on tomato leaf tissue. We took the total necrotic area of an infested leaflet as a measure to determine the optimal infestation density. Figure 1A shows the average damage in millimeters squared over a period of 5 d for four different mite densities. Fifty mites necrotized approximately 24% of the leaflet area within 5 d. To retain enough viable plant material during the experiment we therefore chose an infestation-dose of 15 adult female spider mites per leaflet. Moreover, with 50 spider mites per leaflet the damage per mite per day was less than that with 15 mites. Figure 1C shows an example of the damage inflicted by 0, 1, 5, 15, and 50 spider mites per leaflet after a period of 5 d. At a density of 15 spider mites per leaflet, each individual spider mite damaged on average 1.4 ± 0.2 mm2/d. The total damage on day five corresponded to an average leaf area of approximately 14%.
In all our experiments we infested tomato plants with adult female spider mites. The number of eggs produced per adult female was used as a measure of their performance. Eggs started to hatch after 5 d (Fig. 1B), leading to a population increase. Therefore, we decided to do our experiments within a 5-day time frame. Two-day-old adult females laid on average 7.4 ± 0.5 eggs per day during this period (Fig. 1B).
A dedicated microarray with 428 tomato expressed sequence tags (ESTs) was made to investigate which genes were regulated through spider mite feeding. These ESTs were selected on the basis of their potential relevance to plant-herbivore and plant-pathogen interactions, and signaling in general. Data on the ESTs that were used and the details of the microarray can be found in the Supplemental Data (available at www.plantphysiol.org). The microarray slide also contained 839 PCR-amplified cDNA fragments and 170 ESTs from petunia (Petunia hybrida) flowers and 46 controls for unrelated experiments. To distinguish between early and late responses of tomato upon spider mite infestation, transcript levels were determined after 1 and 4 d, in 3 independent experiments.
On day one we found that the transcript levels of 60 genes (45 from tomato and 15 from petunia) were at least 1.6 times higher in plants infested by spider mites than in control plants. We have chosen a 1.6-fold difference in transcript level as reliable and relevant since this difference in transcript levels is reproducible with northern blots as shown for diacylglycerol kinase (DGK; Fig. 2). Two additional criteria, a P-value (adjusted for multiple testing) smaller than 0.05 and a signal to noise (S:N) ratio larger than 2.0 were also applicable to the data of these 45 tomato and 15 petunia clones. An adjusted P-value smaller than 0.05 corresponds to a significance level (
JA, SA, and Ethylene Responsive Genes Are Induced by Spider Mites
When the transcript levels in uninfested and spider mite-infested leaves were compared, a clear increase was observed for many members of the family of WIPIs (WIPI-I and WIP-II, Table I) during infestation. Two members of these WIPIs have previously been reported to be induced by spider mites (Li et al., 2002
Several players in lipid signaling such as phosphatidylinositol-4-kinase, phospholipase C, and DGK were also up-regulated, albeit to different extents, on day one. The combined action of these three enzymes can lead to the formation of phosphatidic acid. Phosphatidic acid levels have been shown to increase in tomato upon pathogen attack (Munnik, 2001 ). Two phospholipase D genes, PLD 1 and PLD 2, which can produce phosphatidic acid from phosphatidylcholine and are putatively involved in JA-signaling (Wang et al., 2000), were up-regulated on day one. Other miscellaneous genes related to signal transduction events such as a protein phosphatase 2C, a Leu rich protein kinase, catalase, and a petunia phototaxis-related protein were also up-regulated by spider mites. Two genes encoding zinc-finger proteins were regulated inversely, with lesion stimulated disease-1 (LSD1) down-regulated on day one and SINA-2 on day four. The zinc-finger protein encoded by the Arabidopsis LSD1 gene that acts as a negative regulator of the hypersensitive response has been previously shown to be down-regulated by methyl jasmonate and SA (Schenk et al., 2000). Interestingly, transcript levels of an MLO-2 homolog, a negative regulator of cell death (Stein and Somerville, 2002), were 2- and 3-fold higher after 1 and 4 d, respectively. Two NAM-like proteins from petunia, nh2 and nh23, were also higher on day one, indicating that tomato contains homologous transcripts. The NAM proteins belong to the family of NAC proteins, of which several are induced by elicitor or pathogen treatment (Collinge and Boller, 2001). The transcript levels of the small subunit of Rubisco were lower in spider mite-infested leaves, similar to the situation in tobacco (Nicotiana tabacum) subjected to Manduca sexta herbivory (Halitschke et al., 2003).
Genes encoding enzymes that produce precursors for terpenoid biosynthesis, such as geranylgeranyl pyrophosphate (GGPP) synthase, DOXP-synthase, and diphosphomevalonate decarboxylase were significantly up-regulated by spider mites, indicating that both the mevalonate and DOXP-routes were activated (Table I). Transcript levels of genes related to anthocyanin production such as chalcone isomerase A, dihydroflavonol 4-reductase, and flavonoid 3'-hydroxylase were only up-regulated after 4 d. Correspondingly, transcript levels of tomato genes with high homology to several of the petunia cDNAs that are involved in regulating the transcription of genes involved in the biosynthesis of anthocyanins (an1, an2, an11, and jaf13; Quattrocchio et al., 1993
From the above it was clear that spider mites induce the transcription of direct defense-related genes. In order to determine the onset of the indirect defense response, the temporal emission of volatile organic compounds by infested and uninfested intact tomato plants was analyzed by means of gas chromatography-mass spectrometry. We identified 3 phenolics (p-cymene, MeSA, and putatively di-tert-butylphenol), 9 monoterpenes (2-carene,
To test whether there was a consistent difference between infested and uninfested plants over a period of 5 d, the data of nine independent replicate experiments was analyzed by repeated measures ANOVA. Five volatiles were significantly different (P < 0.05 for all tests): MeSA (Fig. 4A), trans- -ocimene (Fig. 4B), trans-nerolidol (Fig. 4C), linalool (Fig. 4D), and TMTT. To test whether some volatiles exhibited a significant difference on only a subset of days we also tested each day separately. Apart from MeSA, TMTT, trans-nerolidol, trans--ocimene, and linalool, there were only three other volatiles that showed a significant difference on a particular day. Four times more cis-nerolidol (P = 0.03; Fig. 4F), and twice as much limonene (P = 0.02; data not shown) were produced by the control plants on the first day. -farnesene was produced in 4-fold greater quantities by control plants on the second day (P = 0.02; Fig. 4E). The significant differences between infested and uninfested plants for trans-nerolidol and linalool were apparent from day three onwards and for MeSA, TMTT, and trans--ocimene on day four and five. The total amount of monoterpenes and the total amount of sesquiterpenes produced by infested plants were not significantly different from the amounts produced by uninfested plants (results not shown).
In a separate analysis, we also tested whether the cumulative amounts of each volatile emitted by infested and uninfested plants were significantly different. For this we calculated the total amounts produced over 5 d per replicate and tested them through a one-way ANOVA. Only MeSA, TMTT, trans- -ocimene, trans-nerolidol, and linalool were significantly different (Table II). We did not find volatiles whose total production was significantly down-regulated in the infested plants compared to the uninfested plants.
To determine whether the enhanced emission of linalool and trans-nerolidol on day three and four, and the increased emission of TMTT, MeSA, and trans-
Our results indicate that when tomato plants are infested with spider mites their direct defense responses are activated within 1 d, but that their indirect defense-response takes 3 d to be mounted. The microarray results showed an early increase in transcript levels of various genes related to defense proteins and metabolites. In general, the early defense response was characterized by simultaneous activation of JA, ethylene, and SA signal transduction pathways, comparable to the response activated in Arabidopsis and tobacco by leaf-chewing insects (Reymond et al., 2000 ; Halitschke et al., 2003).
In contrast to mechanical wounding (Strassner et al., 2002
Both the microarray data (Table I) and the proteinase inhibitor assay (Fig. 3) indicated a rapid increase in inhibitory compounds upon infestation. Proteinase inhibitors as well as Leu aminopeptidase and callose synthase are all known to be up-regulated in tomato by wounding (Strassner et al., 2002
Our microarray contained many ESTs involved in lipid signaling and we saw that several of them were up-regulated in infested leaves. The transcripts of three enzymes, PI-4-kinase, phospholipase C, and DGK, whose combined action leads to the formation of phosphatidic acid, were all significantly up-regulated. Phosphatidic acid is being recognized as an important second messenger in plants and increases in this lipid have been observed during wounding, oxidative stress, and pathogen attack (Laxalt and Munnik, 2002
We also discovered that various genes that regulate flavonoid and anthocyanin synthesis were up-regulated in tomato by spider mites. These genes encode several types of transcription factors, of which some are up-regulated by gibberellic acid (GA; Weiss et al., 1993
Our microarray data showed that diphosphomevalonate decarboxylase and DOXP-synthase were induced by spider mites, indicating a higher flux through pathways leading to terpenoid synthesis. 3-hydroxy-3-methyl glutaryl coenzyme A reductase and mevalonate kinase were also up-regulated though less significantly (see Supplemental Data). What is new is our finding that GGPP-synthase was induced by spider mites. Apparently more GGPP has to be produced, since TMTT, one of the major volatiles produced by tomato infested with spider mites, is derived from the GGPP-derivate geranyllinalool (Donath and Boland, 1994
The attraction of predatory mites to infested tomato plants occurred when the emission of MeSA, TMTT, linalool, trans-
Li et al. (2002
Since the indirect defense response is delayed relative to the direct defense response, the question is whether the delay occurs in terms of function or in terms of causal mechanisms. In terms of function the delay might represent a strategy of the predators who spend energy in searching for prey and who will profit more when prey densities are high. Vice versa, it might represent a strategy of the herbivore that attempts to delay the arrival of predators. Alternatively, it might represent a strategy of the plant that only needs to attract predators when the direct defense mechanisms are insufficient. Kahl et al. (2000)
Plant Material and Arthropod Rearing Tomato (Lycopersicon esculentum Mill cv Castlemart) seedlings were grown in a greenhouse with day/night temperatures of 23° to 18°C and a 16/8 h light/dark regime. Three days prior to each experiment all plants were transferred to a climate room at 23°C to 18°C, a 16/8 h light regime with 300 µE m–2 s–1, and 60% relative humidity (RH).
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 they 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% RH. We choose to work with predatory mites reared on Castlemart tomato plants since predatory mites can learn to associate plant odors with their prey (Drukker et al., 2000
Prior to the fecundity-assay, several adult female spider mites were allowed to lay eggs on detached uninfested tomato leaves (on wet cotton wool) to produce an egg-wave. After 24 h the adults were removed and the eggs were maintained. After 16 d (2 d after the last moulting stage) the females were collected. We infested 14 plants with 7 of these 2-d-old females on 1 leaflet per plant. The plants were inspected daily by means of a stereomicroscope and all adults, eggs, and juveniles on both sides of the infested leaflet were counted during 7 d. The experiment was performed in a climate room at 23°C, a 16/8 h light regime with 100 µE m–2 s–1, and 60% RH. To assess the level of damage inflicted by different densities of spider mites, we infested 3 leaves per plant with either none, 1, 5, 15, or 50 adult females. Ten plants were infested for each density level. To assess the total leaf area that had been damaged, we harvested the infested leaves of 2 plants (6 leaves) at each density-level during 5 d. After collection the leaves were scanned digitally. Each scan included a 4 cm2 reference. The scans were processed in Photoshop 7.0 (Adobe Systems, Mountain View, CA). First the background was selected and deleted. Second, the colored pixels were transformed to black-and-white using the threshold tool in such a way that all damaged areas were set to white and the remaining undamaged leaf-area was set to black. The histogram-tool was then used to count the white pixels (chlorotic lesions) and the black pixels (intact leaf) of each separate leaflet, as well as that of the reference.
Adult female spider mites were gently placed on the adaxial surface of the fully expanded terminal leaflets using a soft-bristle paintbrush. Per leaflet 15 mites were introduced, 3 leaflets on each plant in total. Plants contained 4 fully expanded leaves, which were chosen for infestation, and 2 emerging leaves. We never observed spider mites dispersing to adjacent leaflets.
For preparation of the slide 428 ESTs clones were selected from the Institute of Genomic Research based on their relevance in plant-herbivore and plant-pathogen interactions and plant-signaling in general. These cDNAs were PCR amplified with T3 (5'-AAT TAA CCC TCA CTA AAG GG-3') and T7 (5'-GTA ATA CGA CTC ACT ATA GGG C-3') primers. The PCR products were purified with MultiScreen plates (Millipore Intertech, Bedford, MA) according to the manufacturer's instructions. The concentrations and lengths of the PCR products were checked with agarose gels. The PCR-products were printed on CMT-CAPS slides (Corning, Corning, NY) with a 12-pin arraying robot (Molecular Dynamics, Sunnyvale, CA). Each spot contained 0.25 ng cDNA. The array also contained spots with PCR products from plasmids with no inserts, bacteriophage lambda DNA in various concentrations, pBluescript DNA in several concentrations, poly-A80 oligonucleotide DNA in different concentrations, water, spotting-buffer, the MSLO cDNA from mouse, CNGC1 cDNA from Arabidopsis, and dilution series of randomly selected PCR pooled products from both petunia and tomato (46 in total). The array also contained 839 randomly selected cDNAs and 170 ESTs from petunia flowers that were also PCR amplified with T3 and T7 primers. All cDNAs were spotted four times per slide. Slides were left to dry over night at 55% RH prior to UV crosslinking (150 mJ). One slide was hybridized with SpotCheck Cy3 labeled nonameres (Genetix, New Milton, Hampshire, UK) to examine the spotting quality.
Leaves were cut at the base and 3 leaves from 3 plants were pooled in 14-mL tubes, directly frozen in liquid nitrogen, and stored at –80°C. Total RNA was isolated with a phenol-LiCl based method and RNA gel-blot analysis was done as described in Verdonk et al. (2003) The data in this article represent 6 hybridizations of 6 independent replicates. Three of these replicates were done on purified RNA of tomato plants infested with spider mites 24 h (day 1) after introduction of 15 adult female spider mites on 3 leaves per plant. The 3 other replicates were done after 96 h (day 4). Leaves from 3 plants (9 infested leaves) were harvested and pooled per replicate.
The spot signal intensities were corrected by subtracting the average background calculated from the second percentile of the petunia spot intensities. For each clone we subsequently calculated the signal-to-noise ratio (S:N) by dividing the Cy3 or the Cy5 signal of a particular clone by the SD of its local background as assessed by ArrayVision software. Data for the two fluorophores were subsequently normalized using a Lowess-normalization procedure performed in R using the Sma-package from CRAN (freely available at: http://cran.r-project.org/). The average ratios (infested to uninfested) and the SEs of these ratios were calculated from the normalized, background-subtracted intensity values for each clone. For calculation of the significance of up- or down-regulation we used a nested-design ANOVA on the separate clones, treating the read-outs of the four within-slide replicates per clone as subsamples. Prior to the analysis an irrelevant small value (by default set to 0.001) was added to each value to neutralize zeroes, after which all values were 10log transformed. The ANOVA was structured using three factors: slide, spotlabel-pair nested in slide and treatment, and was performed in Statistica 6.0 as a univariate analysis on all clones. The obtained P-values of the factor treatment for all clones were adjusted for multiple testing using Benjamini and Hochberg's (1995)
Eighteen-day-old Castlemart tomato plants were transferred to a climate room where they remained in 40-L desiccators for 3 d. The desiccators were ventilated with carbon-filtered pressure-air at 400 mL/min. Per replicate experiment, 3 plants were used for infesting with 15 adult female spider mites on 3 leaves of 3 plants (45 mites per plant) and 3 clean plants were used as control. The head space (the air surrounding a plant) was sampled during 24 h for 5 consecutive days by trapping it on 300 mg Tenax TA in 5-mm wide glass tubes. The desiccators were closed with a glass lid (no grease was used), which had a glass air-inlet and an air-outlet. The air-outlet opening was led directly into a Teflon tube that split in two; one branch was connected to a Tenax-filled sampling tube (connected to a vacuum pump that operated at 200 mL/min), the other released the remainder of the airflow. Before the junction of these two tubes there was a small hatch through which an internal standard could be added to the airstream downstream of the plants because in this set-up part of the headspace was trapped on Tenax, but part was also lost. To correct for this loss we pipetted 1.8 µg benzylacetate dissolved in 20 µL pentane:diethylether (4:1, v/v) into the air stream on a filter paper directly after connecting a new Tenax tube. All connections in the set-up were sealed with Teflon tape. After sampling the tubes were eluted with 2 mL pentane:diethylether (4:1) into amber vials.
The headspace collections were analyzed on a Trace GC-MS-Plus (ThermoFinnigan, Austin, TX). The injector port temperature was set at 250°C and the source temperature at 200°C. The HP DB-5 column (30 m long; 0.25 mm i.d.; 0.25 µm stationary phase) was held at 40°C and heated at 8°C/min to 230°C, where it was maintained for 4 min. Helium was used as carrier gas (1 mL min–1). The MS was set at 5 scans per second for a mass-range from 50 to 350 atomic mass units in electron impact mode (–70 eV).
A mixture of pure GC-grade standards of all identified terpenes (Fluka, Milwaukee, WI) was run as external standard, except for trans- All experiments were repeated 9 times. We analyzed both the absolute emission (in µg/5 d or peak area/5 d) and the relative emission. Relative emission was calculated by setting the highest amount of a volatile, measured during 5 d in each experiment, to 1 and subsequently expressing the other values of that volatile as fraction of the highest. This was done separately for each replicate. Prior to the statistical analysis, the relative data was arcsin-square-root transformed to achieve normality. The temporal emission was analyzed through a repeated measures ANOVA on the relative data using Statistica 6.0 for Windows. All volatiles were analyzed separately. Total production of each volatile compound in 5 d was tested with a one-way ANOVA.
Olfactory-choice assays for predatory mites were conducted using the Y-tube olfactometer, as previously described by Bruin et al. (1992)
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The authors thank Francel Verstappen and Harro Bouwmeester (Plant Research International, Wageningen) for contributing to the GC-MS analyses, Martijn Egas (University of Amsterdam) for discussions regarding statistical analyses, and the MicroArray Division of the University of Amsterdam for assisting in preparing and analyzing the microarrays. Prof. Dr. Wilhelm Boland (Jena, Germany) is kindly acknowledged for providing us with DMNT, TMTT, and -farnesene. Frank Koudijs (Interscience, Breda, The Netherlands) is acknowledged for his advice with Trace-MS analyses. Francesca Quattrocchio (Free University, Amsterdam) is acknowledged for providing us with 170 petunia ESTs. We are grateful to Dr. Alan Musgrave for his valuable comments on the manuscript. Received December 22, 2003; returned for revision February 12, 2004; accepted February 17, 2004.
1 This work was supported by NWO, The Netherlands Organization for Scientific Research (ALW 812.04.004 to M.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.103.038315. * Corresponding author; e-mail kant{at}science.uva.nl; fax 31–20–5257754.
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