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Physiology and Development |
2School of Biological Science, Washington State University, Pullman, Washington 99164-4236 USA; 3Institute of Chemistry and Biotechnology, Electron Microscopy Laboratory, Agricultural University of Norway, N-1432 Ås, Norway; 4Department of Forest Ecology, Norwegian Forest Research Institute, N-1432 Ås, Norway
Received for publication August 9, 2001. Accepted for publication October 25, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: bark • conifer • methyl jasmonate • phenolics • phloem • Picea abies • Pinaceae • plant defense • resin ducts • xylem
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Franceschi et al., 1998
; Christiansen and Krokene, 1999
; Krekling et al., 2000
). In addition to these constitutive defenses, defense-related anatomical changes are induced by bark beetle attack or experimental treatments with pathogenic fungi. Upon an attack by bark beetles and infection by fungi, distinct anatomical changes are up-regulated in Norway spruce bark, including activation of polyphenolic parenchyma cells (PP cells) in the secondary phloem and formation of traumatic resin ducts (TDs) in the xylem (Christiansen et al., 1999a
; Franceschi et al., 2000
; Nagy et al., 2000
). These reactions appear to aid the plant in fending off subsequent attacks and providing sustained resistance to fungal growth in the initially infected region (Christiansen and Krokene, 1999
; Christiansen et al., 1999b
; Krokene et al., 1999
; Franceschi et al., 2000
; Krokene, Solheim, and Christiansen, 2001
).
It is of interest to determine how these fairly complex anatomical changes are induced and regulated because such information may be of use in strategies for chemical or genetic manipulation of conifer resistance. While the mechanism of induction of PP cell formation has not been characterized, there is quite a bit known about factors that can induce TD formation. A number of different biotic and abiotic factors have been found to induce TD formation in conifers, including insect and fungal attack, wounding, frost, and other physical trauma (Thomson and Sifton, 1926
; Bannan and Thomson, 1933
; Bannan, 1936
; Lenely and Moore, 1977
; Fahn, Werker, and Ben-Tzur, 1979
; Alfaro, 1995
; Tomlin et al., 1998
; Yonenobu and Takenaka, 1998
; Nagy et al., 2000
). The signaling agents for these changes are not known, but various phytohormones have been shown to be capable of inducing TD formation and thus are possible candidates for control of this process (Fahn and Zamski, 1970
; Fahn, Werker, and Ben-Tzur, 1979
; Pardos, 1980
). Unfortunately, most of these studies with hormones included shallow wounding during application of the compounds, which in itself can induce TD formation (Franceschi et al., 2000
). As dramatic and important as these inducible anatomically based defenses are in conifers, the biochemical mechanisms leading to their induction and formation remain unknown. Along with characterizing general defense responses and structures in conifers, it is important to determine the chemical agents or other signals involved in generating various aspects of the defense response, as this knowledge will provide tools for further understanding of these defensive processes.
Jasmonates, which are endogenous plant phytohormones (Koda, 1992
; Creelman and Mullet, 1997
), are potent elicitors or signaling agents, and it is well known that they are involved in a host of defense responses (Seo, Sano, and Ohashi, 1997
; Thaler et al., 2001
). While most of the work with these compounds has been done with angiosperms, there is growing evidence of jasmonate induction of defensive compounds in gymnosperms (Yukimune et al., 1996
; Ketchum et al., 1999
; Richard et al., 1999, 2000
; Lapointe, Luckevich, and Séguin, 2001
), as well as jasmonate involvment in conifer developmental phenomena such as mycorrhization of roots (Regvar and Gogala, 1996
; Regvar, Gogala, and Znidarsic, 1997
). Of particular importance to our work is the Kozlowski, Buchala, and Métraux (1999)
study, which demonstrated that methyl jasmonate treatment can make 8–10-d-old Norway spruce seedlings more resistant to the root pathogen Pythium ultimum. However, there are no studies showing jasmonates are capable of inducing the rather complex anatomical changes seen in Norway spruce in response to bark-beetle attack or wounding.
The purpose of this study was to determine if methyl jasmonate can induce the previously characterized cellular defense reactions in Norway spruce. Exogenous application of this compound to the surface of trees overcomes the problem of experimental treatments typically requiring wounding, which complicates the analysis of defense response to fungi or other agents. We examined the effect of methyl jasmonate on the anatomy of bark in both mature trees and small saplings and we show that this compound strongly induces anatomical changes related to defense in spruce.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The experiment was repeated twice, 44 d apart, giving a total of four treatments and four controls from two different trees of the same clone. On 15 June 2000, a healthy Norway spruce tree (clone #504) was selected for exogenous treatment with methyl jasmonate. Four squares, approximately 4 x 4 cm, were outlined on the stem surface between 1.3 and 2 m above the ground, two on each side of the tree, approximately 0.5 m apart. The two squares on one side were coated with a solution of 100 mmol/L methyl jasmonate (Aldrich, catalog #39,270-7, Steinheim, Germany) in water with 0.1% Tween 20, using a cotton pad to keep the bark wet for 5 min before allowing the liquid to dry. Tween 20 is a nonbiologically active detergent used to solubalize the methyl jasmonate and to act as a surfactant to help spread the solution evenly on the hydrophobic bark surface. The two squares on the opposite side (controls) were left untreated. On 18 July 2000, six samples (approximately 1 x 3 cm) including the bark, cambium, and outer annual rings of sapwood were removed from the tree: two samples were taken from inside the control squares, two from inside the methyl jasmonate-treated squares, and two samples from 5 cm above the upper edge of the methyl jasmonate squares. Samples were prepared for microscopy as detailed below. On 28 July 2000, another tree of the same clone (#504) was given the same treatment as described above. Samples were collected on 1 September 2000 following the same procedure as before, except samples were taken 5 and 15 cm above the treated bark section.
Methyl jasmonate treatment of 2-yr-old saplings
Two-year-old saplings were used to determine if methyl jasmonate can induce defense responses in young stems. For this experiment, 2-yr-old saplings of two full-sib families of Norway spruce were treated with 100 mmol/L methyl jasmonate +0.1% Tween 20. On 7 August 2000, the lower internode (of 1999) of eight plants from each family was carefully coated with the methyl jasmonate using a small, soft paintbrush, while the upper internode (2000) was left untreated. Two plants from each family were left as untreated controls. The plants stood in individual 1-L pots in a greenhouse. On 1 September 2000, two treated plants of both families plus two control plants were harvested. Stem sections from both internodes were fixed and embedded in acrylic resin as described below. The remaining plants were kept under the natural light and temperature conditions of the unheated greenhouse until 3 January 2001, when they were exposed to a regime of approximately 20°C and 24 h daylight to initiate an early growth season. By early May 2001, they had completed new shoot elongation, and on 10 May 2001, one plant of both families from each treatment was examined for TD formation in all three main stem internodes and branches coming off the internodes, using fresh sections of the living tissue. Traumatic resin ducts, when present, can be easily seen in fresh samples with a dissecting microscope.
Microscopy preparation of stem samples
The samples were placed directly in fixative (2% paraformaldehyde and 1.25% glutaraldehyde buffered in 50 mmol/L L-piperazine-N-N'-bis [2-ethane sulfonic] acid, pH 7.2). In the laboratory, a strip of bark and wood 20 mm long by 4 mm wide was taken from each sample and placed into a drop of fresh fixative and a 1 mm wide slice (cross sections) was cut out. The slice was fixed overnight at room temperature, rinsed with the same buffer, and embedded in L. R. White acrylic resin (TAAB Laboratories, Aldermatson, Berkshire, UK). Sections (1 µm thick) were cut on a diamond knife, dried onto gelatin-coated slides, and stained with Stevenel's blue (Del Cerro, Cogen, and Del Cerro, 1980
). A drop of immersion oil was placed on the sections followed by a coverslip that was sealed to the slide with nail polish. The sections were examined and photographed with a Leitz Aristoplan photomicroscope.
Methyl jasmonate treatment followed by fungal inoculation
To determine if methyl jasmonate can affect relative resistance to a phytopathogenic fungus, on 31 July 2000 the trunk of one tree (clone #2359; 30+ yr old) was treated with methyl jasmonate between 1 and 2 m above ground. A solution of 100 mmol/L methyl jasmonate (aqueous, with 0.1% Tween 20) was applied with a hand sprayer so that the bark was kept wet for 5 min. Another tree of the same clone, of the same size and appearance, and growing 4 m away from the treated tree was designated a control tree, on which the stem section between 1 and 2 m was marked but to which no treatment was given. On 24 August, an 80-cm section within the marked region of both trees (between 1.1 and 1.9 m) was mass inoculated with Ceratocystis polonica on malt agar at a density of 400 inoculations/m2, using a 5-mm cork borer (see Christiansen, 1985
). The two trees were felled in mid-October and three 20-cm bolts were cut from the inoculated stem section. After peeling away the outer bark, the length of the necrotic zones at each inoculation site in the phloem was measured.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The cambial zone was quite large, and no axial resin ducts were present in the cambial or sapwood region of the control samples (Fig. 2A). The PP cells, which occur as annual rings in the phloem (Krekling et al., 2000
), showed features normal for bark of trees that had not undergone stress (Fig. 2A). One month after application, samples from the middle of the methyl jasmonate-treated areas showed the symptoms previously demonstrated to occur in response to wounding, fungal infection, and bark-beetle attack (Franceschi et al., 2000
; Nagy et al., 2000
). Well-developed TDs were present in a tangential band along the bottom of the cambial zone at the treatment site (Fig. 2B). Within the annual phloem rings, the PP cells were swollen, resulting in considerable crushing of the older sieve cell layers, and contained denser staining phenolic bodies than in control tissues (Figs. 2B and 3A–B). In addition, extra PP cells were formed interior to the normal current-year layer of PP cells in the methyl jasmonate-treated region but not in control bark (Figs. 3C–D). These same features (TDs, swollen PP cells with denser phenolics, and extra PP cells) were present in samples taken 5 cm above the edge of the methyl jasmonate-treated area of the tree (Fig. 2C). However, the TDs were somewhat smaller in size and were closer to the cambium, indicating they were induced later than those in the treated area and/or that the inductive stimulus may have been less strong.
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). The cambial zone was greatly reduced in size in this later experiment (see Krekling et al. [2000]
for seasonal features of cambial zone activity), as indicated by comparing the control sections from the two experiments (Fig. 2A, D). While a distinct ring of small TDs was produced in treated areas (Fig. 2E), only an occasional TD was found 5 cm above the treated area (Fig. 2F) and no TDs were formed in samples taken at 15 cm away.
No indication of a toxic effect of application of the methyl jasmonate could be seen in any of the samples examined. The periderm of control and treated areas looked the same, and while in the treated zone the PP cells of the secondary phloem appeared in an activated stage, there was no evidence of PP cell death or phloem necrosis. There was also no induction of a wound periderm or lignification in the sections examined, both of which were previously found to occur very close to a wound site (Nagy et al., 2000
; Franceschi et al., 2000
) where the damage is severe.
Effect of methyl jasmonate application on relative resistance to Ceratocystis polonica
Nine days after mass inoculation with C. polonica, copious amounts of resin was observed flowing from the inoculation sites of the methyl jasmonate-treated tree but not the control tree (Fig. 4A–B). The amount and uniformity of resin flow observed is not typical of Norway spruce this soon after inoculation. Examination using a dissecting microscope of stem discs taken at the time of felling showed that a continuous ring of TDs was present in the methyl jasmonate-treated tree but not in the control tree (Fig. 4C–D). Lesion lengths, which are an indication of the ability of the plant to inhibit growth of the fungus, were found to be significantly different between the methyl jasmonate and control trees. Lesion lengths in the methyl jasmonate-treated tree averaged less than half of the lesion lengths in the untreated control tree (7.9 ± 1.9 mm vs. 17.5 ± 5.9 mm, mean ± SD).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Franceschi et al., 2000
; Nagy et al., 2000
). This result is consistent with the role of jasmonates in defense responses in a host of plants that have been studied. Although there is no information on jasmonates in conifer defense mechanisms operating in mature stem tissue and no data about induction of anatomical features in conifers by jasmonates, there is data indicating that production of defensive chemicals in conifers, including spruce, can be induced by jasmonates. Kozlowski, Buchala, and Métraux (1999)
found that methyl jasmonate treatment enhanced resistance of Norway spruce seedlings to Pythium ultimum via activation of the salicylic acid pathway and subsequent induction of chitinase. Other studies have shown induction of various potential defense-related proteins in white spruce by jasmonate treatment (Richard et al., 1999, 2000
; Lapointe, Luckevich, and Séguin, 2001
), but in neither of these studies was the cell biology of the process determined. Our results indicate jasmonates may be involved in defense-related signaling in Norway spruce and specifically in the regulation of complicated anatomical changes that can occur in bark and cambial zone tissues in response to attack.
Formation of TDs after treatment with methyl jasmonate followed the same time scale (3–4 wk) previously found in a number of experiments we have conducted on mature trees treated with sterile or fungal inoculations (Christiansen et al., 1999a
; Franceschi et al., 2000
; Nagy et al., 2000
). Traumatic resin ducts are formed through activation of the cambial zone, which results in an altered developmental program for cells that would normally become xylem. It is unlikely that methyl jasmonate is directly inducing this change, as auxins seem to be more directly involved in TD induction (Fahn and Zamski, 1970
; Fahn, Werker, and Ben-Tzur, 1979
; Pardos, 1980
). Alternatively, ethylene, either induced by auxin (Yamamoto and Kozlowski, 1987
) or directly by elicitor (Popp, Lesney, and Davis, 1996
) in conifer systems, may be the agent initiating TD formation. Thus, it is possible that methyl jasmonate induces changes in auxin or ethylene production that in turn result in activation of TD formation, but this remains to be proven.
Polyphenolic parenchyma cell activation was also seen after external application of methyl jasmonate to bark. Jasmonates have been shown to induce chalcone synthase expression in white pine (Richard et al., 2000
) and phenylalanine ammonia lyase in cultured tobacco cells (Sharan et al., 1998
), and both of these enzymes are important in phenolic compound biosynthesis in Norway spruce (Brignolas et al., 1995
; Nagy et al., 2000
). Polyphenolic parenchyma cells are the primary site of phenolic biosynthesis in the secondary phloem, and so the activation of PP cells and increase in their phenolic contents is consistent with studies showing jasmonate induction of enzymes of the phenylpropanoid pathway (Sharan et al., 1998
; Richard et al., 2000
).
Methyl jasmonate treatment induced the whole range of responses that are elicited by inoculation with the exceptions of wound periderm formation and the lignification seen at the necrotic zone immediately surrounding the inoculation hole (Nagy et al., 2000
). Similarly, lignification was not induced in methyl jasmonate-treated seedlings (Kozlowski, Buchala, and Métraux, 1999
). Although we show that jasmonates can induce the general activation of PP cells and activation of cambial zone cells to form TDs, the concentration used here did not induce the responses we associate with severe wounding and necrosis, such as PP cell death, proliferation and lignification of cells around the wound site, and wound periderm formation. While we used very high concentrations of methyl jasmonate in our applications, it is likely that the quantity reaching the living cells of the phloem was very low, given the combination of thick, lignified walls, suberized layers and phenolics that make up the periderm. In support of this, we never saw any indication of a toxic effect of the treatments, such as cell death or necrosis or browning or loss of needles, on either mature trees or saplings.
The sapling study showed the methyl jasmonate-induced response was not persistent, as only a single layer of TDs was formed the year of treatment and no new TDs were formed in the subsequent year. In contrast, bark-beetle attacks and fungal inoculation can lead to formation of multiple rows of TDs close to the wound in the year of damage and also in subsequent years (see Franceschi et al., 2000
). In the immediate vicinity of a wound, an active callus-like tissue is formed and the signaling agent for TD formation is likely continuously produced over a long period of time giving rise to the potential for multiple bands of TDs within a season and during subsequent seasons. Exogenously applied methyl jasmonate, however, appears to act as a one-time signal. Methyl jasmonate treatment elicited defense responses, but the compound, or its active products, were either sequestered or metabolized quickly and thus could not induce sequential activation of the cambial zone after it is reorganized following TD formation.
The induction of defense responses by methyl jasmonate was found to extend a considerable distance beyond the actual treatment zone. This extended induction is similar to the effects seen in response to a single inoculation 5 mm in diameter, which can lead to induction of recognizable young TDs 10 cm away after a period of 18 d (Nagy et al., 2000
). In the case of the sapling study, the responses were induced across nodes (between treated and untreated internodes). We do not believe that this was due to gaseous methyl jasmonate diffusing to untreated parts of the stem for the following reasons. (1) Branches of the saplings would be exposed to equal amounts of gaseous methyl jasmonate but did not produce TDs, though they are capable of this with direct treatment. (2) A previous experiment where we placed methyl jasmonate on a cotton ball in a glass container sealed to the bark demonstrated that gaseous methyl jasmonate does not induce TDs in mature stems, probably because it cannot reach a concentration high enough to effectively penetrate the periderm (unpublished data). (3) The mature trees were in a relatively open stand and methyl jasmonate vapors were unlikely to build up around the application site. (4) Spraying of 15-yr-old trees with 100 µmol/L methyl jasmonate in Tween had no effect on these older trees (unpublished data). Our results indicate that either jasmonates or some agent produced in response to jasmonates is transported some distance away from the application zone, probably internally by the vascular system, where these agents are then capable of inducing the defense responses. The TDs produced further away from the application site are also smaller, indicating a dose-response phenomenon.
The anatomical changes induced by methyl jasmonate application appear to be relevant to defense, as indicated with the fungal inoculation of mature trees. First, resin flow after a few days was considerable in the treated but not the control tree. This demonstrates the TDs produced in response to methyl jasmonate application were actually functional. With respect to resin flow, it would also be interesting to determine if the existing radial resin canals of the secondary phloem are activated by methyl jasmonate. There is a general lack of information about the activity of constitutive resin canals in the conifers, although a study of Pinus pinaster indicates existing resin canal epithelial cells can be activated by wounding (Walter et al., 1989
). Secondly, lesion lengths were significantly reduced in the treated tree. This indicates that growth of the pathogenic fungus was severely inhibited by the changes in the tree induced by methyl jasmonate. Further studies are in progress to determine the strength of this treatment relative to the vaccination effect we have shown can be induced with preinoculations (Christiansen and Krokene, 1999
; Christiansen et al., 1999b
; Krokene et al., 1999
; Krokene, Solheim, and Christiansen, 2001
).
The current study shows that exogenous application of methyl jasmonate mimics effects of wounding or bark-beetle attack with respect to induction of a complex of cellular-based defense responses, and methyl jasmonate alone can induce locally enhanced resistance in mature trees in the absence of wounding. In both mature bark and small saplings, the suite of anatomical responses is also found some distance from the application site, indicating that methyl jasmonate, or some product of it, is transported axially and has an inductive effect. This is relevant to induced responses with respect to both local acquired resistance (Christiansen and Krokene, 1999
; Christiansen et al., 1999b
; Krokene et al., 1999
; Krokene, Solheim, and Christiansen, 2001
) and possibly systemic acquired resistance (SAR). However, in trees, SAR may have to be evaluated in a different context than typically used for much smaller herbaceous plants. In summary, this is the first report of a single compound that can give rise to all the structures previously characterized in response to wounding, fungal infection, and bark-beetle attack in Norway spruce and which are related to induced resistance. Future studies will determine if jasmonates are part of the endogenous signaling system in Norway spruce or if they are just able to activate a nonjasmonate-based system in conifers.
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FOOTNOTES |
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5 Author for reprint requests: (FAX: +47 64 94 29 80; email: Erik.Christiansen{at}skogforsk.no
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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A. Byun-McKay, K.-A. Godard, M. Toudefallah, D. M. Martin, R. Alfaro, J. King, J. Bohlmann, and A. L. Plant Wound-Induced Terpene Synthase Gene Expression in Sitka Spruce That Exhibit Resistance or Susceptibility to Attack by the White Pine Weevil Plant Physiology, March 1, 2006; 140(3): 1009 - 1021. [Abstract] [Full Text] [PDF]
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B. Miller, L. L. Madilao, S. Ralph, and J. Bohlmann Insect-Induced Conifer Defense. White Pine Weevil and Methyl Jasmonate Induce Traumatic Resinosis, de Novo Formed Volatile Emissions, and Accumulation of Terpenoid Synthase and Putative Octadecanoid Pathway Transcripts in Sitka Spruce Plant Physiology, January 1, 2005; 137(1): 369 - 382. [Abstract] [Full Text] [PDF]
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G. W. Turner and R. Croteau Organization of Monoterpene Biosynthesis in Mentha. Immunocytochemical Localizations of Geranyl Diphosphate Synthase, Limonene-6-Hydroxylase, Isopiperitenol Dehydrogenase, and Pulegone Reductase Plant Physiology, December 1, 2004; 136(4): 4215 - 4227. [Abstract] [Full Text] [PDF]
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J.W. Hudgins and V. R. Franceschi Methyl Jasmonate-Induced Ethylene Production Is Responsible for Conifer Phloem Defense Responses and Reprogramming of Stem Cambial Zone for Traumatic Resin Duct Formation Plant Physiology, August 1, 2004; 135(4): 2134 - 2149. [Abstract] [Full Text] [PDF]
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D. M. Martin, J. Faldt, and J. Bohlmann Functional Characterization of Nine Norway Spruce TPS Genes and Evolution of Gymnosperm Terpene Synthases of the TPS-d Subfamily Plant Physiology, August 1, 2004; 135(4): 1908 - 1927. [Abstract] [Full Text] [PDF]
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S. A. B. McKay, W. L. Hunter, K.-A. Godard, S. X. Wang, D. M. Martin, J. Bohlmann, and A. L. Plant Insect Attack and Wounding Induce Traumatic Resin Duct Development and Gene Expression of (--)-Pinene Synthase in Sitka Spruce Plant Physiology, September 1, 2003; 133(1): 368 - 378. [Abstract] [Full Text] [PDF]
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D. M. Martin, J. Gershenzon, and J. Bohlmann Induction of Volatile Terpene Biosynthesis and Diurnal Emission by Methyl Jasmonate in Foliage of Norway Spruce Plant Physiology, July 1, 2003; 132(3): 1586 - 1599. [Abstract] [Full Text] [PDF]
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