JXB Advance Access originally published online on April 12, 2007
Journal of Experimental Botany 2007 58(7):1835-1842; doi:10.1093/jxb/erm044
RESEARCH PAPER |
Reduction of ethylene emission from Scots pine elicited by insect egg secretion
1Freie Universität Berlin, Institute of Biology, Haderslebener Str. 9, D-12163 Berlin, Germany
2Radboud University Nijmegen, Institute for Molecules and Materials, Toernooiveld 1, NL-6525 ED Nijmegen, The Netherlands
* To whom correspondence should be addressed. E-mail: hilker{at}zedat.fu-berlin.de
Received 17 November 2006; Revised 12 February 2007 Accepted 19 February 2007
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Abstract |
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Pinus sylvestris L. is known to activate indirect defence in response to attack by an herbivorous sawfly. Egg deposition by the sawfly Diprion pini L. induces pine to release, three days after egg laying, locally and systemically terpenoid volatiles that attract parasitoids to kill the eggs. The elicitor of the pine's response is located in the sawfly's oviduct secretion enveloping the eggs after deposition. Application of this secretion on twigs with artificially conducted ovipositional woundings mimics the effects of egg deposition. Furthermore, jasmonic acid (JA) induces a volatile pattern similar, but not identical, to the one induced by egg deposition. To gain deeper insight into the transduction of plant signals induced by herbivore egg deposition, it was investigated whether ethylene emission from pine is affected by sawfly egg deposition. Systemically induced ethylene emission from differently treated pine twigs was monitored for a period of 3 d after treatment. Ethylene emissions from untreated control twigs were compared with those from twigs treated as follows: (i) sawfly egg secretion [= oviduct secretion (OVI)] was transferred on artificially wounded pine needles (attractive volatiles), (ii) needles were artificially wounded (non-attractive volatiles), and (iii) the twig was supplied with JA (attractive volatiles). Ethylene emission from systemically OVI-induced twigs was significantly lower than from untreated controls, whereas artificial wounding had no detectable effect. JA-treated twigs released much more ethylene and showed higher variability of ethylene emission than artificially wounded twigs and OVI-treated ones. Ethylene emissions from pine after the various treatments studied here are discussed with respect to known effects of insect feeding on ethylene release from plants.
Key words: Diprion pini, egg deposition, ethylene emission, herbivore, jasmonic acid, oviduct secretion, photoacoustic spectroscopy, Pinus sylvestris
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Introduction |
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Plants have evolved numerous constitutive and inducible defence strategies against herbivores (Karban and Baldwin, 1997; Agrawal et al., 1999; Dicke and van Loon, 2000; Turlings and Wäckers, 2004; Schoonhoven et al., 2005). Their defensive responses can be induced by both insect egg deposition and feeding. Induction of plant defence by insect egg deposition is considered to be a preventive defence strategy, since defence is induced prior to later damage by the feeding activity of insect larvae (Hilker and Meiners, 2006).
Plant responses induced by egg deposition and feeding show some parallels with respect to their effects and mechanisms. They may act directly with harmful effects on the eggs, the ovipositing female or the feeding herbivore. Moreover, the plant may defend itself indirectly by attracting predators and parasitoids of the eggs or feeding stages (Turlings and Benrey, 1998; Dicke and van Loon, 2000; Hilker and Meiners, 2002; Hilker et al., 2002b; Kessler and Baldwin, 2002; Turlings et al., 2002; Agrawal, 2005). To date, the mechanisms of oviposition-induced plant responses have not yet been studied to the same extent as feeding-induced ones. It is known that, in both types of responses, an elicitor released by the herbivore onto the plant (herbivore regurgitate or secretion on eggs) is able to induce herbivore species specific plant responses (Doss et al., 2000; Engelberth, 2000; Turlings et al., 2000; Halitschke et al., 2001; Alborn et al., 2003; Hilker et al., 2005; Mumm et al., 2005). Even though many plant responses to herbivory and egg deposition show some similarities to plant reactions induced by mechanical wounding, the effects of feeding- and oviposition-induced plant responses are often different from those of artificially wounded plants (Paré and Tumlinson, 1999; Meiners and Hilker, 2000; Hilker et al., 2002a; van Poecke and Dicke, 2004). Both feeding and oviposition are known to induce volatile patterns different from that induced by artificial damage (Dicke, 1995; Wegener et al., 2001; Kessler and Baldwin, 2002; Mumm et al., 2003; Schmelz et al., 2003). Responses to both feeding and oviposition show local and systemic effects, indicating that phytohormones may be involved in distributing the message of attack within the plant. The ecological effects of both types of responses can be mimicked by exogenous application of the phytohormone jasmonic acid which leads to the attraction of predators and parasitoids (van Poecke and Dicke, 2004; Hilker and Meiners, 2006). However, neither the volatile pattern induced by egg deposition nor the one induced by feeding is identical with the pattern induced by jasmonic acid (Dicke et al., 1999; Gols et al., 1999; Wegener et al., 2001; Hilker and Meiners, 2002; Mumm et al., 2003; Hilker and Meiners, 2006).
For signal transduction, several pathways and phytohormones like jasmonic acid (JA), salicylic acid (SA), and ethylene (ET) are known to orchestrate plant defence (Pieterse et al., 2001; Farmer et al., 2003; Rojo et al., 2003; Arimura et al., 2005; Bostock, 2005; Beckers and Spoel, 2006; Halim et al., 2006). Interactions between signalling pathways depend on the herbivore species feeding on the plant tissue (Walling, 2000; Ozawa et al., 2000; van Poecke and Dicke, 2004). Several studies show that the emission of the phytohormone ET is enhanced in response to herbivore feeding (van Poecke and Dicke, 2004, and references therein). Moreover, diverse other stress signals like mechanical wounding, chemicals such as metal ions, drought, extreme temperature, and phytopathogens are known to induce an increase in ET emissions (Popp et al., 1995; Rieske and Raffa, 1995; Bleecker and Kende, 2000; Kruzmane et al., 2002; Wang et al., 2002; Pierik et al., 2006; van Loon et al., 2006). However, so far it is not known whether ET plays a role in the induction of plant defence against egg deposition.
Therefore, this study aimed to elucidate the role of ET in the induction of defensive plant responses to insect egg deposition. Egg deposition by the herbivorous sawfly Diprion pini L. on Scots pine (Pinus sylvestris L.) induces the plant to emit volatiles that attract the eulophid parasitic wasp Chrysonotomyia ruforum Krausse, which kills the egg of the herbivore (Mumm and Hilker, 2006). The attractive volatiles are emitted not only from the site of egg deposition (local release), but also from adjacent egg-free sites (systemic emission) (Hilker et al., 2002a). Three days after egg deposition, the quantities of terpenoid volatiles released from systemically induced twigs are changed such that egg parasitoids become attracted. Likewise, three days after JA-treatment, pine twigs attract egg parasitoids by a volatile pattern similar, but not identical, to the one induced by egg deposition (Hilker et al., 2002a; Mumm et al., 2003). Mimicking the ovipositional wounding by artificial wounding (i.e. slitting or ‘sawing’ into pine needles longitudinally) does not induce pine to emit attractive volatiles (Hilker et al., 2002a, 2005). The elicitor of the pine's response to egg deposition is located in a secretion coating the sawfly eggs. The eliciting secretion originates from the sawfly's oviduct (oviduct secretion=OVI) (Hilker et al., 2002a; 2005). Moreover, D. pini egg deposition affects photosynthetic activity in pine. Systemically oviposition-induced twigs show reduced net photosynthetic rates when compared with untreated controls (Schröder et al., 2005).
To elucidate the effects of the sawfly's egg deposition on ET emission in pine, ET emissions from artificially wounded pine twigs treated with the eliciting egg secretion were quantified for a period of 3 d after treatment. The plant's response to this type of treatment with OVI is equivalent to the response to egg deposition, as shown by several studies (Hilker et al., 2002a, 2005). The treatment of plants with OVI can be highly standardized, while sawfly egg-laying activity cannot be standarized so easily. Furthermore, an application of OVI enables the starting point of induction to be clearly defined, which is important when studying ethylene emission over time. By contrast, the onset of egg-laying by sawflies cannot be influenced within a time-scale of hours. ET emissions from OVI-treated pine twigs were compared with ET emissions from untreated controls, from artificially wounded twigs (without any elicitor application), and from JA-treated twigs. The treatment of pine with OVI allowed a fine-scaled temporal investigation comparable with treatments by artificial wounding and JA.
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Materials and methods |
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Plants and insects
Large branches of Scots pine (Pinus sylvestris L.) were detached from 15–30-year-old trees in a forest near Berlin and brought into the laboratory where the stems were cleaned and sterilized according to the method of Moore and Clark (1968) prior to measurements. The sawfly Diprion pini L. was reared continuously in the laboratory on cut pine twigs as described by Bombosch and Ramakers (1976) and Eichhorn (1976) at 20±1 °C, 18/6 h light/dark cycles.
General plant treatment
Two small pine twigs (about 20 cm in length) were cut from the same branch. The cut end was immediately immersed in water. The terpenoid concentrations may vary greatly within an individual pine tree (Gershenzon and Croteau, 1991). Therefore, one of the two small twigs was used for treatment (see below), while the other twig was kept untreated as the control. Since a test and control twig was always cut from the same branch, they were considered as paired sample (see statistics, below). All pine twigs were tested systemically as described in detail by Mumm et al. (2003), i.e. the lower half of a twig was treated, while the upper half was left untreated. Ethylene release from the upper part of the twig was measured.
Treatment: artificial wounding (AW)
Eight needles from the lower part of a pine twig were slit longitudinally (2 cm length) using an insect needle, mimicking the ovipositional wounding of the sawfly (Hilker et al., 2002a). The corresponding control was kept untreated.
Treatment: oviduct secretion (OVI)
Oviduct secretion was collected by dissecting the oviduct (oviductus communis and o. lateralis) of 10 D. pini females. Oviducts were dissolved in 20 µl of ice-cold ringer solution (pH 7.2, Merck, Darmstadt, Germany), samples were centrifuged (10 min at 12 000 rpm), and the supernatant containing the oviduct secretion was kept frozen (–80 °C) until application. Previous studies have shown that oviduct secretion obtained and kept in this way is active as an elicitor of pine volatiles attracting egg parasitoids (Hilker et al., 2002a, 2005). Thus, this type of treatment can be used to simulate egg deposition, but does not depend on sawfly egg-laying activity. For treatment, eight needles from the lower part of the twig were treated. A volume of 1 µl oviduct secretion was applied to each needle that had been artificially wounded to mimic the ovipositional wounding (see above). The respective control twigs were left untreated.
Treatment: jasmonic acid (JA)
Pine twigs were supplied with an aqueous Tween 20 solution (0.05%) containing 0.3 µmol JA ml–1 in the water taken up by the twig through the cut end. This concentration and type of JA-treatment is known to elicit the emission of volatiles that lures the egg parasitoid C. ruforum (Hilker et al., 2002a). The water was changed once during the 3-d measuring period. Control twigs were supplied with Tween 20 solution.
Photoacoustic detection of ethylene emission
ET emission was monitored in real time by using a sensitive CO2 laser-based photoacoustic detector in combination with a gas flow-through system (Bijnen et al., 1996; Harren and Reuss, 1997; Harren et al., 2000). For the measurement of systemic ethylene responses of treated twigs, a glass cuvette was placed over the upper untreated part of the pine twig. The opening where the upper half of the twig entered the cuvette was closed by a sealant (Terostat; Teroson GmbH, Heidelberg, Germany). Similarly, the upper part of the control twig was placed into a cuvette with the lower half left outside.
Compressed air as carrier gas was flushed through the cuvettes containing the twigs at a constant flow of 2.0 l h–1, being regulated by mass flow controllers (Brooks Instruments type 5850 S., Veenendaal, The Netherlands). Ethylene released in the headspace of the cuvettes was thus transported to the photoacoustic cell (RUN, Nijmegen, The Netherlands), where it was measured by sensitive microphones. The gas flow through the measuring system was controlled by electrical three-way-valves that switch a particular gas stream to the photoacoustic cell (on-position) or into the laboratory (off-position). The ethylene detector and the valves were controlled automatically by a computer program. To remove carbon dioxide and water, a scrubber filled with potassium hydroxide and calcium chloride was inserted in the gas flow system before entering the photoacoustic cell. In addition, a cooling trap (–150 °C) was used to remove any possibly interfering gases.
Continuous measurement of ethylene emission
Treatment of pine twigs was conducted shortly prior to the measurements. The day when treated twigs and their respective controls (N=8 for each treatment and respective control) were placed in the glass cuvettes is referred to here as d 0. Starting with d 0, the ethylene emission was continuously measured for a period of further 3 d. Five cuvettes [two with one treated twig each, two with one control twig each, and one empty (base-line)] were used per experiment and placed into a climate chamber (20 °C, 18/6 h light/dark cycles, photosynthetic photon flux density approximately 400 µmol m–2 s–1). The measurement cycle was as follows: for a single cuvette, 25 acquisition points (about 30 min) were measured, thereafter the valve switched to the next cuvette, thus cycling through all cuvettes. One cycle was completed after approximately 2.5 h, and the next started immediately. These cycles were repeated for a period of 3 d. The last 10 acquisition data points out of 25 were considered for analysis and averaged automatically by a computer program. Thus, there was one mean ET data point every 30 min and, due to cycling, one ET data point for a cuvette every 2.5 h.
Data calculation and statistics
The measured ET signal was multiplied with the flow rate and expressed as nl h–1 g–1 needle fresh weight. To determine needle fresh weight, needles from the measured upper part of the pine twigs were removed and weighed after measurements. The ethylene levels measured in the empty cuvette (base-line) were subtracted from the emission rates obtained. ET data points within a time frame of 2.5 h were considered as comparable ET signals released by the twig.
ET emissions were statistically analysed by repeated-measures ANOVA for single effects of treatment and time, and for combined effects. Since data obtained from the treated twig and its corresponding control from the same branch were considered paired samples, two ‘within-subject’ factors were analysed, i.e. one for factor ‘treatment’ and one for factor ‘time’. The analysis was performed using Statistica 4.5. scientific software (Statsoft, Hamburg, Germany). For direct comparison, ET emission from controls of OVI-, AW-, and JA-treated twigs were analysed with repeated-measures ANOVA, thereby analysing the factor time (‘within-subject’ factor) and the factor treatment, in all three controls (‘between-subject’ factor).
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Results |
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Ethylene (ET) emission from pine twigs treated with oviduct secretion (OVI)
Treatment of twigs with OVI from D. pini females significantly affected ET emission. Systemically OVI-induced twigs showed a significantly lower emission than the corresponding control during all days and nights of the measurement (Fig. 1A, treatment, Table 1A). Both in OVI-treated and control twigs, the ET emission significantly changed during the 3-d measuring period (time, Table 1A) with a maximum after 21 h (OVI-treatment) and after 33 h (control). In addition, a combined effect of treatment and time was detected, i.e. OVI-induced twigs did not show the same pattern of ET emission from days 0–3 as the control (treatmentxtime, Table 1A).
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ET emission from artificially wounded (AW) pine twigs
Systemic ET emission was not affected by artificial wounding when comparing with the respective control (Fig. 1B; treatment, Table 1B). Furthermore, no combinatory effect of treatment and time was detected, i.e. both AW-treatment and control showed the same pattern of ET emission from days 0–3 (treatmentxtime, Table 1B). However, ET emission significantly changed during the 3-d measuring period (time, Table 1B) with a maximum after 36 h for both AW-treatment and control.
ET emission from jasmonic acid (JA) treated pine twigs
ET emission from JA-treated twigs differed from the ones of AW- and OVI-treated twigs (Fig. 1C). Overall, ethylene emission after JA treatment was much higher than after the other treatments (compare y-axis 0–5.0 nl h–1 g–1 FW for OVI- and AW-treated twigs and 0–25 nl h–1 g–1 FW for JA treated ones). Furthermore, ethylene emission from JA-treated twigs varied much stronger than ethylene release from AW- and OVI-treated twigs. Due to this high variation, no statistically significant effect of treatment on ET emission was detectable in JA-treated twigs (treatment, Table 1C). However, a strong tendency (P=0.066) of the combinatory effect of treatment and time was detected during the night and a less strong tendency (P=0.108) during the day time (treatmentxtime, Table 1C). Both in JA-treated and control twigs, ET emission significantly changed during the 3-d measuring period (time, Table 1C) with a maximum after 63 h (JA-treatment) and after 39 h (control).
For comparison, ET emissions from control twigs taken from the same branches as the respective treated twigs (paired samples) are presented in Fig. 1D. This direct comparison of control twigs shows that ethylene emissions of all controls were similar and did not differ significantly (treatment, Table 2). In addition, no combinatory effect of treatment and time was detected, i.e. all three controls show the same pattern of ET emission from days 0–3 (treatmentxtime, Table 2). All control twigs had a maximum of ET emission between 33 h and 39 h, showing that all control pine twigs changed ethylene emissions over time (time, Table 2).
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Discussion |
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These data show that pine treatment with egg secretion [= oviduct secretion (OVI)] of the sawfly D. pini affects systemic ethylene (ET) emission in Scots pine. As shown by several other studies (Hilker et al., 2002a, 2005), this treatment mimics egg deposition by the application of oviduct secretion into artificially wounded pine needles. ET emission from systemic parts of the twig adjacent to the sites of OVI-treatment decreased significantly (Fig. 1A; Table 1A). In contrast, artificial wounding mimicking the ovipositional wounding by the sawfly did not affect systemic ET emission (Fig. 1B; Table 1B). Thus, ovipositional wounding per se (without egg secretion) did not cause a decrease in ET emission.
It is well known that just cutting twigs from a plant, even without any further wounding of leaf or bark tissue, leads to accelerated ageing, water deficiency, subsequent decrease of photosynthesis, and a change in ethylene emissions (Moldau et al., 1993; Richardson and Berlyn, 2002). For example, when 6-week-old seedlings of Norway spruce (Picea abies L. Karst) were cut, they immediately responded by a decrease in ET production, while about 6 h later a slow, continuous increase of ET production was found over a period of 4 d (Ingemarsson and Bollmark, 1997). In this study, no rapid decrease of ET production was detected when measurements started shortly after cutting twigs from the branch. Instead, ET emissions from untreated control twigs showed a slight and slow increase especially during day 1 of the measurements (Fig. 1D). The finding that OVI-treatment triggered an ET response different from the other treatments indicates that the cut twigs used were able to respond sensitively to a treatment.
Several other studies show that artificial wounding of leaf or bark tissue of angiosperms and gymnosperms induces enhanced ET emissions or enhanced transcription of genes involved in ET biosynthesis (Wang et al., 2002; Hudgins and Franceschi, 2004; Hudgins et al., 2006; Ralph et al., 2006), even though exceptions exist (Kahl et al., 2000; Schmelz et al., 2003). These artificial woundings were usually conducted to mimic feeding damage, thus removing considerable parts of plant tissue. In this study, the pine needles were slit, thereby destroying the epidermis, parenchymatic tissue, and one of the vascular bundles in a pine needle (Hilker et al., 2002a). Such damage is severe damage, but different from feeding damage by sawfly larvae which remove entire needles or large parts of a needle. Thus, the lack of effects of artificial wounding on ET emissions found in this study might be due to the specific mode of ovipositional wounding that was conducted here.
While angiosperms often show a rapid increase of ET emissions a few h after wounding (Tscharntke et al., 2001; Arimura et al., 2002; Kruzmane et al., 2002), no such immediate wounding-induced ET bursts have been found so far in gymnosperms (Telewski and Jaffe, 1986; Ingemarsson and Bollmark, 1997). In Sitka spruce, the expression of genes encoding S-adenosyl-L-methionine synthase and 1-aminocyclopropane-1-carboxylate (ACC) oxidase, both key enzyme in ethylene biosynthesis (Kende, 1993), were only found to be induced 52 h after spruce budworm feeding, but not after 3 h, when compared with unwounded controls (Ralph et al., 2006). In Douglas fir, ACC oxidase protein quantities were enhanced 6 h after wounding with a continuous slow further increase until 96 h (Hudgins and Franceschi, 2004). Ingemarsson and Bollmark (1997) conclude that the absence of an early burst in ET production after wounding might be a general trait in conifers. These data support this conclusion.
Like the artificially wounded pine samples, no immediate ET burst was detectable in pine twigs treated with jasmonic acid (JA) (Fig. 1C). Treatment of pine with JA induced a very slow and highly variable increase of ET emissions. The maximum of ET emission from JA-treated twigs was only reached after 2 d. JA is well-known to induce plant ethylene emissions and genes involved in ethylene biosynthesis (Xu et al., 1994; O'Donnell et al., 1996; Penninckx et al., 1998; Howe, 2004; Hudgins and Franceschi, 2004). However, our data show no significant difference between ET emissions from JA-treated twigs and the respective controls. As terpenoid patterns of pine trees may strongly vary inter- and intra-individually (Gershenzon and Croteau, 1991), their sensitivity to JA might also vary in such a way that sampling ET emissions from 10 JA-treated pine twigs was not sufficient to detect a statistically supported increase of ET emissions after JA treatment (but compare Table 1C for tendencies).
JA and ET do not activate plant defence independently, but rather establish complex interactions with other phytohormones (Pieterse et al., 2001; Wang et al., 2002). The interaction of phytohormone-mediated signalling pathways can be antagonistic, co-operative, or even synergistic (de Bruxelles and Roberts, 2001; Arimura et al., 2005). For example, SA signalling has been found to inhibit JA-dependent defence in tobacco and Arabidopsis thaliana (L.) Heynh. plants (Preston et al., 1999; Cipollini et al., 2004). Also, abscisic acid (ABA) is known as a negative regulator of plant defences by interacting with SA-, JA,- and ET signalling pathways (Anderson et al., 2004; Fellner et al., 2005; Mauch-Mani and Mauch, 2005; Diaz and Alvarez-Buylla, 2006). Moreover, ABA is known to limit ET production during shoot growth in maize (Sharp and LeNoble, 2002; Voisin et al., 2006). This study revealed that ET emission from JA-treated pine was different from the one of OVI-treated twigs. It is proposed that egg deposition on pine triggers other and/or additional signalling pathways in pine than the octadecanoid pathway, with the interaction of the activated pathways leading to the suppression of ethylene production. This suggestion could also explain that the JA-treatment of pine induced a terpenoid volatile pattern similar, but not identical to the one released from egg-laden pine (Mumm et al., 2003). However, the match of the JA-induced volatile pattern with the egg-induced pine volatile blend was sufficient to attract the egg parasitoids (Hilker et al., 2002a).
Our results raise the question on the ecological role and effects of a decreased ET emission from pine after insect egg deposition. As will be argued below, a decrease of ET emission might imply a decrease of direct defence against the pine sawfly. Results of a study by Hudgins and Franceschi (2004) indicate that enhanced ethylene production induces the synthesis of phenolic compounds and an increase of additional resin ducts, so-called traumatic resin ducts (TD) in a gymnosperm plant. Increased levels of resin and phenolics in TD might lead to a higher toxicity, and thus, may directly impair herbivore performance (Larsson et al., 1986, 2000; Hanover, 1975; Nagy et al., 2000; Krokene et al., 2003). If enhanced emission of ethylene causes an increase of direct defence in gymnosperms, lowered ethylene production might mean a decrease of direct defence.
Based on this logic, the following possible ecological roles of ethylene decrease is suggested: (i) from the plant's perspective, egg deposition of the sawfly D. pini induces indirect defensive responses in pine at the cost of direct defence. An ecological trade-off between direct and indirect defence could be shown for several angiosperm plants (Agrawal et al., 2002; Cipollini et al., 2003). (ii) From the herbivore's perspective, the primary role to envelope the eggs in oviduct secretion might be to suppress the direct plant defence in order to provide the best diet for their larvae. So far, we are well aware that we only can speculate when searching for answers on these ecological questions. However, these further ideas, opened and supported by the ethylene data presented here, will be worthwhile analysing in future studies.
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Acknowledgements |
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We thank Ute Braun (Freie Universität Berlin) for her technical assistance in rearing the sawflies. Thanks are also due to Marco Steeghs for his helpful advice and discussion. This work was supported by the German National Science Foundation (GRK 837/1-03) and the EU-FP6-Infrastructures-5 program, project FP6-026183 ‘Life Science Trace Gas Facility’ in Nijmegen, The Netherlands.
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