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First published online December 28, 2007; 10.1104/pp.107.111088 Plant Physiology 146:965-973 (2008) © 2008 American Society of Plant Biologists OPEN ACCESS ARTICLE
Effects of Feeding Spodoptera littoralis on Lima Bean Leaves: IV. Diurnal and Nocturnal Damage Differentially Initiate Plant Volatile Emission1,[W],[OA]Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, D–07745 Jena, Germany (G.-i.A., S.K., M.K., V.V., A.D., P.B., P.D., W.B.); and Department of Plant Biology and Centre of Excellence for Plant and Microbial Biosensing, University of Turin, I–10125 Turin, Italy (V.V., M.E.M.)
Continuous mechanical damage initiates the rhythmic emission of volatiles in lima bean (Phaseolus lunatus) leaves; the emission resembles that induced by herbivore damage. The effect of diurnal versus nocturnal damage on the initiation of plant defense responses was investigated using MecWorm, a robotic device designed to reproduce tissue damage caused by herbivore attack. Lima bean leaves that were damaged by MecWorm during the photophase emitted maximal levels of β-ocimene and (Z)-3-hexenyl acetate in the late photophase. Leaves damaged during the dark phase responded with the nocturnal emission of (Z)-3-hexenyl acetate, but with only low amounts of β-ocimene; this emission was followed by an emission burst directly after the onset of light. In the presence of 13CO2, this light-dependent synthesis of β-ocimene resulted in incorporation of 75% to 85% of 13C, demonstrating that biosynthesis of β-ocimene is almost exclusively fueled by the photosynthetic fixation of CO2 along the plastidial 2-C-methyl-D-erythritol 4-P pathway. Jasmonic acid (JA) accumulated locally in direct response to the damage and led to immediate up-regulation of the P. lunatus β-ocimene synthase gene (PlOS) independent of the phase, that is, light or dark. Nocturnal damage caused significantly higher concentrations of JA (approximately 2–3 times) along with enhanced expression levels of PlOS. Transgenic Arabidopsis thaliana transformed with PlOS promoter::β-glucuronidase fusion constructs confirmed expression of the enzyme at the wounded sites. In summary, damage-dependent JA levels directly control the expression level of PlOS, regardless of light or dark conditions, and photosynthesis is the major source for the early precursors of the 2-C-methyl-D-erythritol 4-P pathway.
Herbivore-induced plant volatiles (HIPVs) attract herbivore natural enemies and, hence, benefit plants indirectly. Like floral volatiles (Dudareva et al., 2003  , 2005), HIPVs display diurnal or nocturnal rhythms that may be coordinated with the habits of the parasitoids that are attracted to them (Loughrin et al., 1994; Turlings et al., 1995; Arimura et al., 2004a, 2005). Whereas floral scents or light-dependent isoprene emissions are constitutively produced according to circadian rhythms (Dudareva et al., 2005; Loivamäki et al., 2007; Roeder et al., 2007), the release of HIPVs is a phenotypically plastic response of plants to herbivory that is influenced by insect performance and environmental factors (e.g. photoperiod and temperature). Herbivorous insects likewise depend on plant volatiles for information about their food plants and the surrounding environment so that they can modulate their activity accordingly. For example, caterpillars of Mythimna separata behaved as if they were in the dark when exposed during the day to volatiles emitted from host plants (infested or uninfested) in the dark (Shiojiri et al., 2006). Likewise, regardless of the amount of light available, caterpillars behaved as if they were in the light when exposed to volatiles emitted from plants during the photophase (Shiojiri et al., 2006). Moreover, volatile compounds released at night from lepidopteran-infested tobacco (Nicotiana tabacum) plants were repellent to conspecific female moths (Heliothis virescens; De Moraes et al., 2001). These examples clearly demonstrate that plants are able to generate temporally different volatile blends that address different organisms at different times of the day in order to optimize defense. Whereas many elements of damage recognition, signal transduction, de novo biosynthesis, and metabolic regulation involved in HIPV biosynthesis are known (Arimura et al., 2005), only little is known about the mechanisms of the temporal variations underlying the synthesis and release of HIPVs. In particular, the question of whether HIPV emissions are controlled by circadian clocks or by environmental factors, such as the insect's activity level or the amount of light, remain to be addressed.
Here, we report on the results of diurnal and nocturnal leaf damage using the previously developed MecWorm device to mimic herbivore-caused tissue damage in a completely reproducible and quantifiable manner. The continuous mechanical damage effected by the robotic device was able to induce in lima bean (Phaseolus lunatus) leaves the emission of volatiles whose profiles perfectly matched those of the HIPVs induced by feeding larvae of Spodoptera littoralis (Mithöfer et al., 2005 Using this fully reproducible mode of mechanical damage, we present evidence that temporally different instances of leaf damage to the same plant during either the light phase (day) or the dark phase (night) play a decisive role in the control of HIPV emission. We demonstrate that continuous mechanical damage during the day or night is associated with an enhanced level of jasmonic acid (JA). This JA production is closely followed by up-regulation of the transcript level of the gene coding for the (E)-β-ocimene synthase. During the photophase, damage by MecWorm leads to the instantaneous emission of (E)-β-ocimene. In the dark, however, a very weak nocturnal emission is followed by a rather brief emission burst after the onset of the photophase. Studies with 13CO2 demonstrate that the early steps of the terpenoid pathway along the 2-C-methyl-D-erythritol 4-P (MEP) pathway appear to be responsible for the delayed response. We propose a schematic view of the elements of signaling and metabolic regulation required for the herbivore-induced β-ocimene emission and the light-independent Hex-Ac.
Functional Characterization of the β-Ocimene Synthase Gene in Lima Bean
The monoterpene (E)-β-ocimene, emitted from lima bean leaves after damage by the feeding larvae of S. littoralis, was one of the major volatiles (64%–69% of the total volatiles; Arimura et al., 2007
Rhythmic Emission of Herbivore-Induced Volatiles β-Ocimene and Hex-Ac
Volatiles in the headspace of induced plants were analyzed with zNose, which combines a high time resolution (10 min) with the ability to run unattended over prolonged periods (Kunert et al., 2002
Effects of Diurnal and Nocturnal Damage on Volatile Emissions
To determine temporal relation between leaf damage and emission of HIPVs, we used the recently developed MecWorm (Mithöfer et al., 2005
Evidence for de Novo Biosynthesis of β-Ocimene during the Early Morning Burst
The supply of C5 precursors for monoterpene biosynthesis via the plastidial MEP pathway is directly linked to CO2 fixation (Paré and Tumlinson, 1997
Effect of Diurnal and Nocturnal Damage on JA Production and Gene Regulation
Damage by feeding herbivores and the external application of JA (0.5 mM) to lima bean leaves (Dicke et al., 1999
Localization of JA and PlOS Transcript Accumulation in Damaged Leaves
Localization patterns of JA and the PlOS transcript in leaf sections in relation to the first and second instances of damage in the dark were then investigated (Fig. 6A
). Thirty-two hours after onset of the first nocturnal damage by MecWorm, high JA levels were found in segments 2 and 3. Increased JA levels in segments 2 and 3 reflect the increased JA levels of the consecutive treatments shown in Figure 3D. JA and PlOS transcript levels in undamaged neighbor segments 1 and 4 corresponded to the resting level, showing that JA accumulated only locally at the wounding site. PlOS expression showed a similar localization pattern; the difference in expression levels in leaf sections 2 and 3 was statistically insignificant. That PlOS was expressed only at the sites of wounding was further demonstrated with transgenic Arabidopsis (Arabidopsis thaliana) stably transformed with PlOS promoter::GUS. As shown in Figure 6A, 2 h of manual wounding led to the expression of the inducible GUS reporter gene only at the wounding sites (Fig. 6B). Treatment with MecWorm led to the same result (Fig. 6C). Overall, these results indicate that JA-induced PlOS expression is localized at the wounding site, thus facilitating terpenoid emission locally and temporally. Similar herbivory-linked local patterns were observed for TPS genes AtTPS12 (At4g13280), AtTPS13 (At4g13300; Ro et al., 2006
Analyzing the volatiles from lima bean plants damaged by MecWorm for 6 h during the day or night over a period of 3 d, we observed a clear difference between the emission of the terpenoid β-ocimene and the emission of the fatty acid-derived volatile Hex-Ac. However, emission patterns for both compounds were clearly periodic (Fig. 7 ). The total amount of volatiles increased during the day (independent of whether damage occurred in the light or dark), whereas the amount dropped at night. This pattern corresponded to the results of Loughrin et al. (1994) and Turlings et al. (1995), who studied corn (Zea mays) and cotton (Gossypium hirsutum) plants infested by caterpillars. However, our study has revealed additional details due to two major technical improvements. First, the completely reproducible mechanical damage inflicted by MecWorm when applied during the day or night to the same plant species allowed us to compare even subtle differences in the biosynthesis of HIPVs, JA, and the expression level of PlOS. Second, the high time resolution of zNose (Kunert et al., 2002) allowed close correlation to be made between the emission profiles of individual volatiles and their gene expression, as well as their levels of JA.
In lima bean, herbivore-induced emission of β-ocimene was found to be exclusively linked to light and not to the circadian clock. Rapidly diminishing levels of β-ocimene after an AD period was introduced into the photophase strikingly demonstrated this link. The light-dependent β-ocimene emission was hampered by the level of the early terpenoid precursors delivered to the MEP pathway by the photosynthetic fixation of CO2. Because the monoterpene β-ocimene is synthesized in the lima bean via the MEP pathway (Piel et al., 1998 ; Bartram et al., 2006), the very high degree of 13C-labeling of the monoterpene (70% within the first 30 min and 85% in the second 30 min after the beginning of the light phase) synthesized de novo from 13CO2 after the onset of the light period strongly supported this view. Thus, the metabolic flux from photosynthesis to terpenoid biosynthesis is a key regulatory element of the light-dependent emission of β-ocimene. This view is complemented by the observation that, after the first instance of damage, the high transcript level of nocturnally induced PlOS followed the high nocturnal level of JA. Also, all other enzymes along the MEP pathway have to be produced during the dark phase. The metabolic flow-through system begins to operate as soon as the very first photosynthates are delivered, and β-ocimene can be emitted within minutes after the onset of the light period. On the other hand, light seems also to be essential to maintain high levels of PlOS expression because an additionally introduced dark phase rapidly reduced PlOS expression levels in herbivore-damaged leaves within 4 h after the dark period began (Fig. 2B). Similar observations were made for the isoprene synthase, the 1-deoxy-D-xylulose 5-P reductoisomerase from gray poplar (Populus x canescens; Loivamäki et al., 2007), and the germin-like protein from mustard (Sinapsis alba; Heintzen et al., 1994). In both plants, the corresponding mRNAs were no longer detected in the dark even when expression was under the control of the endogenous clock.
In addition to increasing levels of JA and the presence/absence of light, other factors, such as the impact of an endogenous clock, seem to contribute to regulating PlOS. Screening the database PLACE (http://www.dna.affrc.go.jp/PLACE/signalscan.html) for cis-acting regulatory DNA elements revealed the presence of a circadian element (CAANNNNATC; Piechulla et al., 1998
Another major difference between nocturnal and daytime damage was observed in the levels of JA. JA is the major plant hormone involved in the up-regulation of volatiles, in particular, terpenoid biosynthesis (Arimura et al., 2005
Production of JA and the emission of the fatty acid-derived volatile Hex-Ac correlated closely with MecWorm damage, regardless of whether damage occurred under light or dark conditions (Fig. 3, A and B). Besides the low nocturnal emission of Hex-Ac (Fig. 3B), a second emission peak occurred during the day. This biphasic emission of Hex-Ac corresponded to previous observations in Arabidopsis. Enhanced transcript levels of CHAT (At3g03480) coincided with the highest levels of Hex-Ac, which were emitted several hours after wounding. However, the first emission of Hex-Ac was observed just 5 min after wounding (Loreto et al., 2006
Both Hex-Ac and β-ocimene, volatiles focused on in this research, are known to attract carnivorous arthropods and thus function as indirect plant defenses by increasing predation pressure on attacking herbivores (Dicke et al., 1990
Plants and Caterpillars
Lima bean (Phaseolus lunatus ‘Ferry Morse’ var. Jackson Wonder Bush) was grown in soil. Individual plants were grown in plastic pots in a growth chamber at 23°C (160 µE m–2 s–1 during a 14-h photoperiod; relative humidity 60%) for 2 weeks. Larvae of Spodoptera littoralis Boisd. (Lepidoptera, Noctuidae) were reared on an artificial diet in a plastic box (25°C ± 1°C; 14:10 LD; Bergomaz and Boppré, 1986
Primary leaves from intact lima bean plants were used for all treatments and analyses. For S. littoralis infestation, three second- and third-instar larvae were placed on a leaf. Manual wounding was performed by punching 18 6-mm-diameter holes into a leaf for a total of 508 mm2 of damaged area. MecWorm operation was programmed to generate within 6 h circles of damaged leaf area in the primary leaf, yielding 265 mm2 of total damaged area (two circle sectors;
Leaves were damaged by MecWorm during the first and second dark phases (11 PM–5 AM) and covered by a Plexiglas cabinet (approximately 500 mL) with air constantly passing through the system at 50 mL min–1. For pulse labeling, synthetic air with 380 µg mL–113CO2, 20.9% O2, and 79% N2 (Westfalen A.G.) was introduced into the cabinet with a starting flow of 200 mL min–1 for 10 min (6 AM–6:10 AM) to replace the natural 12CO2 followed by a reduced flow at 50 mL min–1. The emitted volatiles were collected by solid-phase microextraction on a polydimethylsiloxane 100 fiber (Supelco). Samples were analyzed on an Agilent 6580 gas chromatograph coupled to a Micromass GCT time-of-flight mass spectrometer (Micromass UK Ltd.). Separation was performed on a Zebron ZB-5ms capillary column (30 m x 0.25 mm i.d. x 0.25 µm; Phenomenex). Helium at a flow rate of 1.0 mL min–1 served as carrier gas and a split-mode injection (1:10) was employed. The gas chromatograph injector, transfer line, and ion source were set at 220°C, 280°C, and 280°C, respectively. Spectra were taken in the total ion-scanning mode at 70 eV. Compounds were eluted under programmed conditions starting at 40°C (2-min isotherm) followed by heating at 15°C min–1 to 200°C, then at 40°C min–1 to 280°C. The injected amount was 1 µL. The intense fragment ions at m/z 93 (control plants) and at m/z 94 to 100 (13CO2-fed plants) were used to analyze and calculate the incorporation rate of 13C. The fragment ions at m/z 94 to 100 correspond to the incorporation of one to seven 13C-atoms into β-ocimene (see Fig. 4).
A primary leaf attached to an intact lima bean plant was enclosed in a Plexiglas cabinet (552 mL) where it was subjected to insect and MecWorm damage (Mithöfer et al., 2005
Plant material was weighed (0.2–0.25 g) and shock frozen with liquid nitrogen. For analyses of spatial patterns of JA, we mixed two samples corresponding to each leaf section to obtain 0.2 g of leaf sections. JA was quantified in plant material according to a modified protocol from Schulze et al. (2006)
A whole leaf was crushed in liquid N2 and the tissue (100 mg) was used for RNA extraction. First-strand cDNA was synthesized using the SuperScript II (Invitrogen) oligo(dT)12-18 primer and 1 µg of total RNA at 50°C for 50 min. For PCR, primers for the PlOS cDNA fragment were designed using a LjEβOS cDNA sequence (GenBank accession no. AY575970). PCR was run for 2 min at 95°C, 35 cycles of 15 s at 94°C, 30 s at 50°C, and 60 s at 72°C. Further cloning of 5'- and 3'-ends was accomplished by RACE-PCR using the first-choice RLM-RACE kit (Ambion) according to the manufacturer's protocol. For functional identification of the full-length genes, the region of an open reading frame of PlOS was subcloned into pHis-8-3 expression vectors (Jez et al., 2000
First-strand cDNA was synthesized from isolated total RNA (see above) using SuperScript II reverse transcriptase, oligo(dT)12-18 primer, and 1 µg of total RNA at 42°C for 50 min. Real-time PCR was done on a Mx3000P real-time PCR system (Stratagene). The process was performed with 25 µL of reaction mixture containing 12.5 µL of 2x Brilliant SYBR Green QPCR master mix (Stratagene), cDNA (1 µL from 20 µL of each reverse transcriptase product pool), 100 nM primers, and 30 mM ROX as a passive reference dye. Initial polymerase activation: 10 min at 95°C; 40 cycles of 30 s at 95°C, 60 s at 55°C, and 30 s at 72°C. PCR conditions were determined by comparing threshold values in a dilution series of the RT product, followed by non-RT template control and nontemplate control for each primer pair. Relative RNA levels were calibrated and normalized with the level of PlACT1 mRNA (GenBank accession no. DQ159907). Primers are shown in Supplemental Table S1.
Genomic DNA was extracted from lima bean leaves using the Qiagen plant DNA extraction kit. Genomic DNA was digested with EcoRV and then circularized with T4 DNA ligase (New England Biolabs). Nested, inverse PCR was performed with circularized genomic DNA as the template, using Taq DNA polymerase (New England Biolabs). PCR protocol: 40 cycles of 15 s at 95°C, 30 s at 55°C, and 60 s at 72°C. The PCR product was ligated to a TOPO TA cloning kit (Invitrogen). Primers are shown in Supplemental Table S1. The 517-bp PlOS promoter region upstream of the start codon (GenBank accession no. EU194554) was reamplified by PCR using Pfu DNA polymerase with a pair of primers introducing restriction sites. The amplified promoter fragments were digested with BamHI and EcoRI, and digested fragments were ligated to the corresponding site of pCAMBIA1391 upstream of the GUS gene (Cambia). Constructs were transformed into the Agrobacterium GV3101 strain, which was then used to transform Arabidopsis (Arabidopsis thaliana) ecotype Columbia-0 according to the floral-dip method (Clough and Bent, 1998 Sequence data from this article can be found in the GenBank/EMBL data libraries under accession numbers EU194553 and EU194554.
The following materials are available in the online version of this article.
We thank Dr. A. Mithöfer and Dr. S. Bartram for valuable discussions and H. Uchtenhagen and S. Garms for technical assistance. Received October 16, 2007; accepted December 10, 2007; published December 28, 2007.
1 This work was supported in part by the Center of Excellence for Plant and Microbial Biosensing of the University of Turin. 
2 These authors contributed equally to the article. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Wilhelm Boland (boland{at}ice.mpg.de).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.107.111088 * Corresponding author; e-mail boland{at}ice.mpg.de.
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ABSTRACT
RESULTS
-linolenic acid, may also limit JA production during the light phase. Only comprehensive profiling of the different JA derivatives and all other products derived from 
= 13.0 mm) using 12 punches min–1. For chemical treatment, JA or salicylic acid (0.5 mM, pH 5.8–6.0) in 2 mL of water was sprayed onto intact plants in plastic pots. Alamethicin (1 mM) was applied to the petioles of detached plantlets in aqueous solutions. All treatments, except MecWorm damage in the darkness, started at 9 AM. During treatments, temperature was maintained at 25°C ± 1°C with a photoperiod of 14 h (160 µE m–2 s–1). The light period ran from 7 AM to 9 PM. 
