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Herbivore-Induced Volatiles from Tea (Camellia sinensis) Plants and Their Involvement in Intraplant Communication and Changes in Endogenous Nonvolatile Metabolites Fang Dong,† Ziyin Yang,† Susanne Baldermann,† Yasushi Sato,§ Tatsuo Asai,‡ and Naoharu Watanabe*,†,‡ †
Graduate School of Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan National Institute of Vegetable and Tea Science, 2769 Kanaya, Shizuoka 428-8501, Japan ‡ Faculty of Agriculture, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan §
bS Supporting Information ABSTRACT: As a defense response to attacks by herbivores such as the smaller tea tortrix (Adoxophyes honmaiYasuda), tea (Camellia sinensis) leaves emit numerous volatiles such as (Z)-3-hexen-1-ol, linalool, α-farnesene, benzyl nitrile, indole, nerolidol, and ocimenes in higher concentration. Attack of Kanzawa spider mites (Tetranychus kanzawai Kishida), another major pest insect of tea crops, induced the emission of α-farnesene and ocimenes from tea leaves. The exogenous application of jasmonic acid to tea leaves induced a volatile blend that was similar, although not identical, to that induced by the smaller tea tortrix. Most of these herbivore-induced plant volatiles (HIPV) were not stored in the tea leaves but emitted after the herbivore attack. Both the adaxial and abaxial epidermal layers of tea leaves emitted blends of similar composition. Furthermore, HIPV such as α-farnesene were emitted mostly from damaged but not from undamaged leaf regions. A principal component analysis of metabolites (m/z 70 1000) in undamaged tea leaves exposed or not to HIPV suggests that external signaling via HIPV may lead to more drastic changes in the metabolite spectrum of tea leaves than internal signaling via vascular connections, although total catechin contents were slightly but not significantly increased in the external signaling via HIPV. KEYWORDS: herbivore-induced plant volatiles, jasmonic acid, signaling, tea, tea tortrix
’ INTRODUCTION In response to herbivore attack, many plants emit volatiles.1 Various ecological functions have been demonstrated for herbivoreinduced plant volatiles (HIPV), including direct deterrence of herbivores, attraction of the herbivore’s enemies, plant-to-plant communication,2,3 and within-plant signaling.4,5 Tea (Camellia sinensis) is an important crop in Japan, China, India, Kenya, and other countries. The use of the tender tea leaves for manufacturing infusions has a long history. During tea plant growth, many herbivorous insects such as tea aphids and tea green leafhoppers attack tea leaves and affect the yield and quality of the crop. To avoid contamination of the commercial tea product, insecticides are generally undesired in the control of tea pests. Therefore, it is of interest to understand the responses of tea plants to herbivore attack and possibly to improve the natural antiherbivore defense system. A typical example for the interactions between tea plants and insects is the famous Formosa oolong tea, Oriental Beauty, which possesses a unique aroma of ripe fruit and honey. Intriguingly, leaves infested by the tea green leafhopper are used in manufacturing Oriental Beauty products, suggesting that unique volatiles formed in tea leaves under insect attack may play a role.6 Volatiles emitted from tea leaves attacked by insects (e.g., Tetranychus kanzawai, tea aphid) attract natural enemies of the pest insects.7,8 However, details of the responses of tea plants to insect attacks remain to be discovered. In this study, we characterized profiles of volatiles emitted by tea leaves infested by major pest insects and investigated herbivore-induced local and systemic responses of tea plants. r 2011 American Chemical Society
’ MATERIALS AND METHODS Chemicals. Acetic acid, benzaldehyde, benzyl alcohol, indole, methyl salicylate, and phenylethyl alcohol were purchased from Wako Pure Chemical Industries Ltd., Japan. Benzyl nitrile, farnesene, (Z)-3hexen-1-ol, linalool, linalool oxide (furanoid), methyl jasmonate, and nerolidol were purchased from Sigma-Aldrich Co. Ltd. (()-Jasmonic acid and geraniol were purchased from Tokyo Chemical Industry Co., Ltd., Japan. Ethyl n-decanoate was purchased from Kanto Chemical Co., Inc., Japan. Gallocatechin and catechin-3-gallate were purchased from Nagara Science Co., Ltd., Japan. Catechin, epicatechin, epigallocatechin, epicatechin-3-gallate, and epigallocatechin-3-gallate were kindly provided by Mitsui Norin Co., Ltd., Japan. Reagents used for chromatography analysis were of LC-MS analytical grade and purchased from Wako Pure Chemical Industries Ltd., Japan. Experimental Design. Leaves of C. sinensis var. Yabukita, which is the most popular tea cultivar in Japan, were exposed to the following treatments: (1) nondamaged (control); (2) 24 h after single mechanical damage by needle (6 holes/leaf); (3) 24 h smaller tea tortrix (Adoxophyes honmai Yasuda, third or fourth instar larvae, 6 insects/ treatment) continuous attack; (4) 96 h Kanzawa spider mites (Tetranychus kanzawai Kishida, adult, 40 insects/treatment) continuous attack; and (5) 24 h jasmonic acid (2.5 mM, 30 μL/6 holes/leaf) treatment. After the treatments, headspace volatiles were collected by Received: August 23, 2011 Revised: November 8, 2011 Accepted: November 12, 2011 Published: November 12, 2011 13131
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Figure 1. Experimental setup for investigating herbivore-induced local responses.
Figure 2. Experimental setups for investigations into herbivore-induced systemic responses. HIPV, herbivore-induced plant volatiles. a dynamic headspace volatile sampling system (Figure S1, Supporting Information). Herbivore-induced local responses of the tea plants were investigated using the experimental setups shown in Figure 1. After 24 h of treatment, four sets of solid phase microextraction (SPME) devices (with 100 μm polydimethylsiloxane coating fiber) were employed to simultaneously collect volatiles emitted from the adaxial and abaxial epidermal layers of undamaged and damaged regions of a tea leaf treated with jasmonic acid (2.5 mM, 20 μL/4 holes/leaf). The sampling time was 2 h. Healthy undamaged leaves and mechanically damaged leaves were studied for comparison. Herbivore-induced systematic responses of the tea plants were investigated using the experimental setups shown in Figure 2. Jasmonic acid (2.5 mM, 30 μL/6 holes/leaf) was used to simulate herbivore attacks. Setup A (healthy plant) was used as a control; setup B excluded the influence of HIPV on neighboring leaves and was used as a model for internal signaling via vascular connections; setup C served as a model for external signaling via HIPV. After 24 h of treatment, headspace volatiles of the neighboring leaves were sampled for 1 h using a dynamic headspace volatile sampling technique as shown in Figure S1 of the Supporting Information. Endogenous nonvolatile metabolites of the neighboring leaves were analyzed by ultraperformance liquid chromatography time-of-flight mass spectrometry (UPLC-TOFMS) and highperformance liquid chromatography (HPLC).
Determination of Volatile Compounds by Gas Chromatography Mass Spectrometry (GC-MS). Headspace volatiles were trapped on Tenax TA and analyzed with an Agilent 7890 gas chromatograph and a 5975 mass spectrometer controlled by a GC-MSD Chemstation. The GC was equipped with an InertCap PureWAX column, 60 m 0.25 mm i.d., and 0.25 μm film thickness. The oven temperature program was as follows: 40 °C ramped at 5 °C/min to 250 °C and held for 10 min. Helium was used as a carrier gas at a flow rate of 2.05 mL/min. The Tenax traps were thermally desorbed by
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running the thermal desorption unit from 30 °C (held for 0.5 min) to 260 °C (held for 5 min) at 360 °C/min with a 50 mL/min desorption flow. Desorbed compounds were cryofocused at 100 °C on a quartz wool-packed liner in the programmed temperature vaporization (PTV) inlet for subsequent GC-MS analysis. After desorption, the CIS 4 PTV inlet was run from 100 to 260 °C (held for 5 min) at 720 °C/min to inject trapped compounds into the analytical column. The injection was performed in the PTV solvent venting mode. MS analyses were carried out in a full scan mode, with the scan range m/z 20 300. An electron impact ionization energy of 70 eV was used for all measurements. The ion source and quadrupole analyzer temperatures were fixed at 230 and 150 °C, respectively. Analyses of volatile compounds collected by SPME were performed using a GC-MS QP5000 (Shimadzu), which was controlled by a Class-5000 workstation. Desorption of volatiles from the fiber was performed in the hot GC injector at 230 °C, for 1 min. The GC was equipped with a capillary Supelcowax 10 column (Supelco Inc.), 30 m 0.25 mm i.d., and 0.25 μm film thickness. Helium was used as a carrier gas at a flow rate of 1.6 mL/min. The GC oven was maintained at 40 °C for 3 min. The temperature of the oven was raised at 4 °C/min to 220 °C and then at 10 °C/min to 240 °C and kept at this temperature for 5 min. The mass spectrometer was operated in the full scan mode (mass range m/z 50 280). To determine endogenous volatiles, 1.5 g (fresh weight) of finely powdered leaf tissues crushed by a Multi-Beads Shocker (2000 rpm, 15 s) was extracted with 5 mL of diethyl ether containing 42 nmol of ethyl n-decanoate as an internal standard for 17 h in the dark. The extract was filtered through a short plug of anhydrous sodium sulfate. One microliter of the filtrate was subjected to GC-MS analyses as described above. Acetic acid, benzyl alcohol, benzaldehyde, benzyl nitrile, farnesene, geraniol, (Z)-3-hexen-1-ol, indole, linalool, linalool oxide (furanoid), methyl jasmonate, methyl salicylate, nerolidol, and phenylethyl alcohol were identified by authentic standards, and other volatile compounds were tentatively identified by comparison with the commercial NIST library, using Agilent probability base matching (PBM) software for mass spectrometry search.
Analysis of Endogenous Nonvolatile Metabolites by UPLC-TOFMS. Fifty milligrams (fresh weight) of finely powdered leaf tissues crushed by a Multi-Beads Shocker (2000 rpm, 15 s) was extracted with 1 mL of 70% methanol by vortexing for 1 min followed by an ultrasonic extraction in ice-cold water for 10 min. The extract was filtered through a 0.2 μm membrane filter prior to UPLC-TOFMS (Acquity UPLC- LCT Premier XETM) analysis. Samples (2 μL) were injected into a Waters Acquity UPLC HSS T3 column (2.1 100 mm, 1.8 μm). Sample and column temperatures were maintained at 4 and 35 °C, respectively. The samples were eluted at a flow rate of 0.3 mL/min using a chromatographic gradient of two mobile phases (A, 0.1% aqueous formic acid; B, 0.1% formic acid in acetonitrile). Solvent B was linearly increased from 5 to 30% over 18 min and then to 95% over 26 min. Afterward, 95% of solvent B was maintained for 4 min and subsequently brought back to 5% within 0.1 min and then held for another 5.9 min to allow for column equilibration. An electrospray source was used. Sample cone voltage was set to 30 V, and capillary voltage was set to 2.4 kV. The source and desolvation temperatures were 120 and 450 °C, respectively, and the desolvation and nebulizer gas flow rates were 900 and 50 L/h, respectively. Spectra were collected in the negative ionization W mode (ES ) at a mass resolution of approximately 10000 (full width at half-maximum). Data were acquired over the m/z range 70 1000. The raw data from the UPLCTOFMS analysis were transformed to peak tables (a matrix of m/z and retention time pairs with associated intensities) using MarkerLynx, an application manager of MassLynx v. 4.1. These data were processed by principal component analysis (PCA) via the MarkerLynx software. Analysis of Total Catechins by HPLC. Two hundred microliters of the filtered 70% methanolic extract from tea leaves (described above) 13132
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Figure 3. Major volatile compounds emitted from tea leaves induced by jasmonic acid (JA), smaller tea tortrices, and Kanzawa spider mites. Healthy tea leaves were used as a control. In our study single mechanical damage showed no significant effects on the profile of volatiles emitted from the tea leaves in contrast to the healthy tea leaves. Data are expressed as the mean ( SD (n = 4). After 24 or 96 h of treatment, the headspace volatiles were collected using a headspace volatile sampling system (Figure S1of the Supporting Information, 3 h/sampling). In the graphs, only the major volatile compounds that showed significantly increased contents compared to the control are indicated. Ocimenes were tentatively identified by comparison with the commercial NIST library, and other volatile compounds were identified by the authentic standards. was diluted with 100 μL of 70% methanol and 900 μL of 1 mM ascorbic acid (dissolved in 70% methanol) and then subjected to HPLC analysis. Two microliters of the sample solution was applied onto a Cadenza CLC18 (4.6 100 mm, 3 μm) column. Column temperature was maintained at 40 °C. The samples were eluted using a flow rate of 1 mL/min with a chromatographic gradient of two mobile phases (A, 0.1% aqueous formic acid; B, 0.1% formic acid in acetonitrile). Elution was started with isocratic conditions of 5% solvent B and 95% solvent A for 4 min. Solvent A was increased to 15% over 10 min and maintained for 5 min, then increased to 23% over 20 min and maintained for 17 min, then increased to 60% over 37.5 min and maintained for 10 min, subsequently brought back to 5% within 0.5 min, and held for another 12 min to allow for column equilibration. The effluent was monitored at 280 nm.
’ RESULTS AND DISCUSSION HIPV from Leaves of Tea Plants. The major volatiles emitted from tea leaves in response to jasmonic acid, mechanical damage, smaller tea tortrices, and Kanzawa spider mites (two major pest insects of tea crops) were characterized and are shown in Figure 3. The smaller tea tortrix induced the emission of (Z)-3-hexen-1-ol, linalool, α-farnesene, benzyl nitrile, indole, ocimenes, and nerolidol
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in high amounts, whereas Kanzawa spider mites induced the emission of α-farnesene and ocimenes (Figure 3). These fatty acid-derived green leaf volatiles, aromatic volatiles, and volatile terpenoids are also commonly found in other herbivore-attacked crops such as maize.3,9 Plants attacked by herbivores can induce the formation of phytohormones including jasmonic acid and ethylene, which are known to regulate a large number of genes related to plant defense responses.10 12 The jasmonic acid pathway is the most important signal transduction pathway underlying the induction of HIPV (reviewed in ref 13). In the present work, the exogenous application of jasmonic acid to tea leaves induced a volatile blend that was similar, although not identical, to the blend induced by the smaller tea tortrix (Figure 3). In our study single mechanical damage showed no significant effects on the profile of volatiles emitted from the tea leaves (Figure S2, Supporting Information). A continuous mechanical wounding resembling insect feeding can induce emission of herbivory-related volatiles.14 However, simple mechanical wound stimuli did not usually mimic plant responses to insect attacks. Herbivore-specific compounds from oral secretions of feeding insects, for example, certain enzymes (β-glucosidase) or fatty acid amino acid conjugates such as volicitin, are important elicitors for plant defense mechanisms including the emission of herbivory-related volatiles (reviewed in ref 10). More recently, Allmann and Baldwin reported that a heat-labile constituent of herbivore oral secretions induced a rapid (Z)/(E) isomeric change in the green leaf volatiles emitted from Nicotiana plants, which increased the predation rate of predators feeding on eggs of the herbivore.15 It remains to be discovered whether herbivore-specific compounds from oral secretions of the smaller tea tortrix elicit an accumulation of jasmonic acid, which could further regulate the biosynthesis and emission of herbivoryrelated volatiles. Herbivore-Induced Local Responses of Tea Plants. The jasmonic acid treatment induced increases in some endogenous volatile compounds in tea leaves such as 2-hexenal, methyl jasmonate, benzaldehyde, benzyl alcohol, benzyl nitrile, and α-farnesene. The Kanzawa spider mite treatment increased the amounts of (Z)-3-hexen-1-ol and α-farnesene. However, the small tea tortrice treatment had no significant effects on the endogenous pool of volatile compounds in the tea leaves (Figure S3, Supporting Information). This suggested that small tea tortriceinduced volatile compounds may not be stored but emitted after herbivore attack. Such rapid emission of HIPV indicates a rapid initiation of plant defense against insect attacks. Among the emitted HIPV (Figure 3), some compounds such as (Z)-3hexen-1-ol, linalool, benzyl alcohol, and nerolidol were emitted when feeding ruptured cellular structures in which the volatiles are synthesized and stored (Figure S3, Supporting Information). Other volatiles including α-farnesene, benzyl nitrile, indole, and ocimenes were formed at the moment of damage or soon thereafter. A setup as shown in Figure 1 was used to investigate herbivoreinduced local responses of tea plants. Both the adaxial and abaxial epidermal layers of the tea leaf can emit volatile compounds with similar profiles (Figure S4, Supporting Information). The epidermal cells of various floral parts, especially the petals, are important sites for the production and emission of floral scents.16 Moreover, in rose flowers, both epidermal layers of floral petals are capable of producing and emitting scent volatiles despite distinct morphologies of the cells.17 Volatile production and emission from vegetative organs involve specialized structures 13133
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Figure 4. GC-MS chromatogram (A) and mass spectra (B) of volatile compounds emitted from undamaged and damaged leaf regions (Figure 1), respectively. The experimental setup is shown as Figure 1. After 24 h of jasmonic acid treatment, headspace volatiles emitted from undamaged and damaged regions were collected simultaneously.
such as trichomes, oil glands, oil ducts, and cavities.16 In most cases, significant amounts of volatile compounds accumulate in leaf trichomes, which are important components of plant resistance to herbivores.3 Many plants defend themselves against insect damage by increasing the density or number of trichomes on new leaves.16 Phytohormones including jasmonic acid and gibberellins can regulate such systemic increases in physical defenses.18,19 Both epidermal layers of tea leaves may carry trichomes in which identical volatiles are stored, and after insect damage, these volatiles are emitted from all leaf trichomes in the same manner. It will be interesting to investigate whether different mechanisms of volatile emission are elicited when herbivores attack different leaf layers. The earliest events in plant insect interaction are rapid changes of the plasma membrane potential, immediately followed by variations of cytosolic Ca2+ concentration and the generation of H2O2.20 The downstream responses include the activation of kinases such as mitogen-activated protein kinase (MAPK) and calcium-dependent protein kinases.20 Recently, Wu et al. reported that herbivore attacks rapidly release a shortdistance mobile signal that enhances the activities of MAPKs such as salicylic acid-induced protein kinase and wound-induced protein kinase in wounded regions and adjacent nonwounded regions of the leaf. Subsequently, these kinases enhance transcript levels of genes involved in phytohormone biosynthesis, which results in increased levels of jasmonic acid, salicylic acid, and ethylene. These phytohormones act as signals to activate herbivore attack-related gene expression, eventually leading to indirect and direct plant responses.11 We found that HIPV such as α-farnesene was mostly emitted from damaged, but not from undamaged, regions (Figure 4). This suggests that mobile signaling in the damaged leaf may not elicit HIPV emission, but may initiate the biosynthesis of other defense compounds in nondamaged regions. The HIPV emission from wounded regions may decrease the possibility of further damage from insects and attract natural enemies of the insects, or even protect the wounded region against pathogen infection. Herbivore-Induced Systematic Responses of Tea Plants. A setup shown in Figure 2 was used to investigate herbivoreinduced systemic responses of tea plants. Metabolomics involves
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Figure 5. Principal component analysis of metabolite compositions ([M H] m/z 70 1000) of tea leaves induced by internal signaling via vascular connection and external signaling via HIPV. The experimental setup is shown as Figure 2. Undamaged tea leaves were used as control. The principal component analysis was performed using combinations of m/z and retention time in the spectra by MarkerLynx, an application manager of MassLynx v. 4.1.
a rapid and systematical characterization of small molecule metabolites found in an organism. Using the UPLC-TOFMS technique and multivariate data analysis, it is possible to determine small differences in the metabolite composition between groups or treatments.21 This approach has been successfully applied to discover unexpected bioactive compounds involved in ecological interactions between plants, their herbivores, and members of higher trophic levels.22 In the present study, the metabolomic approach was employed to study effects of HIPV signaling on tea leaves. PCA of metabolites ([M H] m/z 70 1000) indicated that the metabolite composition of tea leaves induced by external signaling was different from that induced by internal signaling and that in control leaves (Figure 5). The metabolite composition induced by internal signaling and that in the control leaves were similar (Figure 5). This may suggest that external signaling via HIPV might trigger more drastic changes than internal signaling via vascular connections. In contrast, 24 h internal signaling via vascular connections or external signaling via HIPV did not induce significant changes of the volatiles emitted from neighboring undamaged leaves as compared to the control (data not shown). Because catechins are the major polyphenols in tea leaves, total catechins were also studied. Total catechin contents were slightly but not significantly increased in the external signaling via HIPV in contrast to the internal signaling via vascular connection (Figure S5, Supporting Information). This indicates that HIPV signaling may result in changes in other unidentified metabolites. This finding suggests various lines of further investigations including (1) the identification of the metabolites that are affected by external signaling via HIPV and their functions in the defense against insect attack; (2) the evaluation of the influences of HIPV quantity and quality on external signaling and the plant defensive system; and (3) the analysis of the effects of long-term within-plant signaling on the plant defensive system. Airborne communication between neighboring plants has been a controversial topic for many years, but now there are multiple examples in the literature of plants responding to volatile chemical signals emitted from neighboring plants under herbivore attack.23,24 The controversy about plant-to-plant interactions also stimulated research into intraplant signaling between different organs. Since Narvaez-Vasquez and Ryan showed how wounding triggers defense responses in distant leaves, herbivore-induced 13134
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Journal of Agricultural and Food Chemistry within-plant signals have usually been assumed to be transmitted via vascular connections.25 Recently, Heil and Bueno4 established that herbivore-induced plant volatiles also can serve in signaling processes within leaves of the same plant. Moreover, Frost and co-workers5 showed that within-plant (hybrid poplar) signaling mediated by volatiles can overcome vascular constraints on systemic signaling and suggested that within-plant signaling may have ecological significance equal to or greater than that of signaling between plants. This information supports our conclusions regarding intraplant communication in tea. Furthermore, our study provides evidence that external signaling via HIPV stimulates biochemical responses in neighboring undamaged leaves (Figure 5). The results of this research will advance our understanding of plant defense systems and will also be essential for the future development of the biological control of pest insects in tea plants.
’ ASSOCIATED CONTENT
bS
Supporting Information. Additional figures. This material is available free of charge via the Internet at http://pubs.acs.org.
’ AUTHOR INFORMATION Corresponding Author
*Phone: +8154-2384870. Fax: +8154-2384870. E-mail: acnwata@ ipc.shizuoka.ac.jp. Funding Sources
This study was supported by a Sasakawa Scientific Research Grant (21-637) from the Japan Science Society and by Shizuoka Prefecture and Shizuoka City Collaboration of Regional Entities for the Advancement of Technological Excellence, Japan Science and Technology Agency (JST). Z.Y. acknowledges support from the Japanese Society for the Promotion of Science (P10101).
’ ABBREVIATIONS USED GC-MS, gas chromatography mass spectrometry; HIPV, herbivore-induced plant volatiles; HPLC, high-performance liquid chromatography; MAPK, mitogen-activated protein kinase; SPME, solid phase microextraction; UPLC-TOFMS, ultraperformance liquid chromatography time-of-flight mass spectrometry. ’ REFERENCES (1) Pare, P. W.; Tumlinson, J. H. Induced synthesis of plant volatiles. Nature 1997, 385, 30–31. (2) Baldwin, I. T.; Schultz, J. C. Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science 1983, 221, 277–279. (3) Pichersky, E.; Gershenzon, J. The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr. Opin. Plant Biol. 2002, 5 (3), 237–243. (4) Heil, M.; Bueno, J. C. S. With-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (13), 5467–5472. (5) Frost, C. J.; Appel, H. M.; Carlson, J. E.; Moraes, C. M.; Mescher, M. C.; Schultz, J. C. Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol. Lett. 2007, 10 (6), 490–498. (6) Cho, J. Y.; Mizutani, M.; Shimizu, B.; Kinoshita, T.; Ogura, M.; Tokoro, K.; Lin, M. L.; Sakata, K. Chemical profiling and gene expression profiling during the manufacturing process of Taiwan Oolong Tea “Oriental Beauty. Biosci., Biotechnol., Biochem. 2007, 71 (6), 1476–1486.
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