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Plant Physiology 132:1586-1599 (2003) © 2003 American Society of Plant Biologists Induction of Volatile Terpene Biosynthesis and Diurnal Emission by Methyl Jasmonate in Foliage of Norway Spruce1Biotechnology Laboratory (D.M.M., J.B.) and Departments of Botany (D.M.M., J.B.) and Forest Sciences (J.B.), University of British Columbia, 6174 University Boulevard, Vancouver, British Columbia, Canada V6T 1Z3; and Max Planck Institute for Chemical Ecology, Winzerlaer Strasse 10, 07745 Jena, Germany (D.M.M., J.G., J.B.)
Terpenoids are characteristic constitutive and inducible defense chemicals of conifers. The biochemical regulation of terpene formation, accumulation, and release from conifer needles was studied in Norway spruce [Picea abies L. (Karst)] saplings using methyl jasmonate (MeJA) to induce defensive responses without inflicting physical damage to terpene storage structures. MeJA treatment caused a 2-fold increase in monoterpene and sesquiterpene accumulation in needles without changes in terpene composition, much less than the 10- and 40-fold increases in monoterpenes and diterpenes, respectively, observed in wood tissue after MeJA treatment (D. Martin, D. Tholl, J. Gershenzon, J. Bohlmann [2002  ] Plant Physiol 129:
1003–1018). At the same time, MeJA triggered a 5-fold increase in total
terpene emission from foliage, with a shift in composition to a blend
dominated by oxygenated monoterpenes (e.g. linalool) and sesquiterpenes [e.g.
(E)- -farnesene] that also included methyl salicylate. The rate
of linalool emission increased more than 100-fold and that of sesquiterpenes
increased more than 30-fold. Emission of these compounds followed a pronounced
diurnal rhythm with the maximum amount released during the light period. The
major MeJA-induced volatile terpenes appear to be synthesized de novo after
treatment, rather than being released from stored terpene pools, because they
are almost completely absent from needle oleoresin and are the major products
of terpene synthase activity measured after MeJA treatment. Based on
precedents in other species, the induced emission of terpenes from Norway
spruce foliage may have ecological and physiological significance.
Terpenes contribute to the characteristic defense chemistry of conifers in many forms. Monoterpenes (C10) and diterpenes (C20) are major components of conifer oleroresins (Bohlmann and Croteau, 1999 ;
Seybold et al., 2000;
Trapp and Croteau, 2001),
whereas sesquiterpenes (C15), though less abundant in resin, have
enormous structural diversity (Steele et
al., 1998b; Fig.
1). Terpene-containing oleoresin is mobilized to wound and
infection sites and serves to protect conifers against herbivore and pathogen
invasion because of its toxicity and deterrency
(Phillips and Croteau, 1999).
After exposure to the atmosphere, the volatile mono- and sesquiterpenes
evaporate, whereas the diterpene acids polymerize, sealing the wound.
Oleoresin terpenes are products of constitutive and inducible pathways that
have been characterized in some detail at the biochemical and molecular level
in grand fir (Abies grandis;
Lewinsohn et al., 1991
Research on conifer oleoresin biosynthesis to date has focused primarily on
induced resin biosynthesis in the stem tissues. For example, it was shown
recently that treatment of Norway spruce with methyl jasmonate (MeJA) induces
a complex, traumatic oleoresin response including de novo differentiation of
traumatic resin ducts in the developing xylem, increased accumulation of
monoterpenes and diterpenes, and induced enzyme activities and gene expression
of monoterpene synthases and diterpene synthases
(Martin et al., 2002
In Norway spruce and other conifers, terpenes are accumulated not only in
stems but also in needles (Schönwitz
et al., 1987
Besides their storage of terpenes, conifer needles also release a profusion
of volatile terpenes into the environment, a topic studied by numerous
researchers seeking to inventory the volatile organic compounds of the
atmosphere (Kesselmeier and Staudt,
1999
The present study examines the biochemical regulation of terpene formation,
accumulation, and release in the needles of Norway spruce. Based on the
success of previous work with stems of this species
(Martin et al., 2002
MeJA Induces a 2-Fold Increase in Terpene Accumulation in Needles
Based on recent reports that MeJA induces terpene biosynthesis in stem
tissues of Norway spruce (Martin et al.,
2002
To determine if MeJA-induced terpene accumulation was due to de novo biosynthesis, we measured the activities of TPSs in cell-free extracts of needles of MeJA-treated and control saplings (clone IA) over a 25-d time course after treatment. Although the accumulation of monoterpenes and sesquiterpenes increased 2-fold in needles over this period in response to MeJA (Fig. 2), the activities of monoterpene synthases and sesquiterpene synthases increased over 5-fold, reaching a peak at d 10 or 12 and then declining precipitously after d 15 (Fig. 3). Diterpene synthase activity was not detectable in needle extracts from either treated or control trees, consistent with the lack of induction of diterpene accumulation in needles. The constitutive levels of diterpenes in mature needles (Fig. 2) could be due to enzyme activity in young needles and their accumulation and longevity in resin ducts.
To investigate the discrepancy between the rates of TPS activity and
terpene accumulation in needles after MeJA treatment, products of monoterpene
synthase assays and sesquiterpene synthase assays were analyzed by gas
chromatography (GC)-mass spectrometry (MS). Two clonal lines of different
genetic background (IA and II) were used for these experiments thereby
allowing us to address variation that might exist between these individual
lines. In clone IA, the major product (55.4%) of the monoterpene synthase
assays of MeJA-treated needles was the alcohol linalool
(Table II), with an
enantiomeric ratio of approximately 1:2 (3R:3S;
Fig. 1). The terpene
hydrocarbons,
The only product of the sesquiterpene synthase assays of MeJA-treated
needles of clone IA was (E)-
Because the major products of the induced needle monoterpene synthase and sesquiterpene synthase enzyme activities (Table II) in clone IA were not observed to accumulate in the needles (Table I), we analyzed volatile terpene emissions from Norway spruce saplings after MeJA treatment to access whether significant amounts of these products were released. Because of limited numbers of trees of the identical genetic background, we used a related (similar chemotype) clone IB for volatile analysis. Headspace collections revealed that the rate of terpene emission after MeJA treatment was approximately 5-fold that of unsprayed control saplings, 281.4 versus 54.3 µg g needle fresh weight h–1, averaged over a collection period of 4 d after treatment for two replicates of each treatment with two saplings in each (Fig. 6).
MeJA treatment also had a dramatic effect on the composition of volatile
terpenes emitted by Norway spruce saplings measured at peak emission at around
24 to 30 h, or approximately 1 d, after treatment. During this peak emission,
composition of volatiles collected over a period of 2 h (26.5–28.5 h
after treatment) was analyzed (Table
III). The rate of sesquiterpene emission was increased
approximately 30-fold by MeJA 1 d after treatment, whereas that of
monoterpenes was increased only 2.2-fold. Hence, sesquiterpenes, which made up
only 19% of the terpene emission of untreated saplings, were 77% of the total
terpene at peak emission after MeJA treatment. These compositional changes
were largely maintained throughout the time course of up to 7 d. Among all
terpenes emitted, the sesquiterpene (E)-
It was surprising to find that the major TPS assay products were
volatilized rather than accumulating in the needles. To confirm this
unexpected result, we investigated saplings of a second clone (clone II) from
a completely different genetic background. After spraying with MeJA, the
principal emitted monoterpenes, sampled by solid-phase microextraction (SPME),
were
Over a time course of 7 d after MeJA treatment, the emission of induced
volatiles of clone IB followed a day-night cycle with increased release rates
during the light period and lower emission during the dark period
(Fig. 7). Maximum levels of
monoterpene and sesquiterpene emission were detected during the light period
approximately 24 or 48 h after MeJA treatment
(Fig. 7). Over the rest of the
time course, the amplitude of the daytime maximum slowly declined. The more
strongly induced classes of terpenes, the oxygenated monoterpenes and
sesquiterpenes, followed a much more pronounced diurnal rhythm than the
monoterpene olefins. When rhythmic emission profiles of individual oxygenated
monoterpenes and sesquiterpenes were monitored, we found that few compounds
such as terpinen-4-ol peaked very early within the first 12 h after treatment
and then diminished rapidly during subsequent light periods, whereas other
compounds such as linalool, 1,8-cineole, and (E)-
Induced Terpene Accumulation in Needles Is Much Lower Than in Wood
MeJA treatment of Norway spruce had profound effects on the synthesis,
accumulation, and emission of terpenes in foliage that were quite different
from the effects of MeJA on the synthesis and accumulation of terpenes in the
stems of this species. The increases in terpene accumulation in foliage were
much less dramatic than in stems. In saplings sprayed with a 10 mM
solution of MeJA, the wood tissue of the stems showed a 12-fold increase in
monoterpene concentration and a nearly 40-fold increase in diterpene
concentration, peaking 15 to 25 d after treatment, but no change in
sesquiterpene levels (Martin et al.,
2002
The relatively small increase in terpene accumulation in needles was not
accompanied by any significant changes in terpene composition, unlike in
stems. The major needle monoterpenes detected in this study were similar to
those previously reported for Norway spruce
(Schönwitz et al., 1987
Monoterpene and sesquiterpene synthase activities in Norway spruce foliage
jumped 5-fold after MeJA treatment. Increases in monoterpene synthase activity
of a similar magnitude (up to 4-fold) have been measured in the foliage of
other conifer species after real or simulated herbivory
(Litvak and Monson, 1998
Although the 5-fold increases in monoterpene and sesquiterpene synthase
activities in Norway spruce foliage after MeJA treatment are sufficient to
account for the 2-fold increase in monoterpene and sesquiterpene accumulation,
the major products of MeJA-induced TPS activity in Norway spruce needles
[linalool and (E)-
Two lines of evidence indicate that the terpenes emitted in abundance after
MeJA treatment are products of de novo synthesis and not released from storage
reservoirs. First, these substances represent the principal products of
induced TPS activities in needles present after treatment, and, second, they
are nearly completely absent from stored needle oleoresin. This conclusion is
corroborated by 13CO2 feeding experiments with Norway
spruce that showed that volatilized terpenes were rapidly labeled from newly
assimilated photosynthate (Schürmann
et al., 1993
Several previous studies of terpene volatilization also attempted to
distinguish between volatilization from preformed pools of resin terpenes and
de novo synthesis and release. In some cases, both processes may be occurring.
For example, in grand fir, volatilization of monoterpenes after stem wounding
was accompanied by increased monoterpene synthase activity suggesting de novo
synthesis (Lewinsohn et al.,
1993
In several other conifer species, wounding of needles also reduced the pool
of accumulated terpenes while increasing both monoterpene emission and
monoterpene synthase activity (Litvak and
Monson, 1998
The volatilization of terpenes from Norway spruce saplings in our study
followed a diurnal cycle, with total emission greater during the light periods
than the dark periods regardless of treatment. Similar diurnal rhythms have
been reported in previous studies of Norway spruce monoterpene emission
(Bufler and Wegmann, 1991
The emission of volatile terpenes by Norway spruce seems likely to have an
important physiological or ecological function in this species because the
rate of release after MeJA treatment is 5-fold higher than before treatment
with a vastly different composition dominated by sesquiterpene and oxygenated
monoterpenes and a strong diurnal rhythm. The major components of the
volatilized blend, linalool, (E)-
In addition to (or instead of) an ecological role, the terpene volatiles of
Norway spruce could have a physiological function that is fulfilled inside the
plant before emission. Other plant terpene volatiles, such as the simple
C5 terpene, isoprene, and various monoterpenes, are thought to have
internal roles also, either serving to increase the thermal tolerance of
photosynthesis (Delfine et al.,
2000 In summary, we have demonstrated that terpene metabolism in Norway spruce needles responds to MeJA induction very differently than terpene metabolism in the stems of this species. Although needles showed only relatively small increases in terpene accumulation compared with stems, MeJA triggered emission of a novel blend of volatiles that is rich in sesquiterpenes and linalool, synthesized de novo, and released in a diurnal rhythm.
Plant Materials
Young saplings of three clonal lines of Norway spruce (Picea abies
Karst) were employed in these investigations. Clones IA (no. 3166-728) and IB
(no. 273-728) were propagated in 1998 from lateral branches of current and
previous year growth at the Niedersächsische Forstliche Versuchsanstalt
(Escherode, Germany). These clones represent similar terpenoid chemotypes.
Fully regenerated, 2-year-old, rooted saplings were grown and maintained in
growth chambers as previously described
(Martin et al., 2002
Reagents were from Sigma-Aldrich (Steinheim, Germany) or Roth (Karlsruhe, Germany). Terpene standards were from Sigma-Aldrich, Roth, Bedoukian Research (Danbury, CT), and Helix Biotech (Richmond, BC, Canada) and were of the highest purity available. All solvents were GC grade. The substrates, [1-3H]GPP (20 Ci mol–1) and [1-3H]GGPP, were from Biotrend (Köln, Germany). [1-3H]FPP (125 Ci mol–1) was the gift of Rodney Croteau (Washington State University, Pullman). Unlabeled GPP and FPP were from Echelon Research Laboratories Inc. (Salt Lake City).
Saplings were sprayed with a 10 mM solution of 95% pure (w/w)
MeJA (Sigma-Aldrich) in distilled water as described previously
(Martin et al., 2002
Dynamic headspace sampling was carried out with an automated collection
system built by Analytical Research Systems (Gainesville, FL) as described
(Degenhardt and Gershenzon,
2000 The time course was repeated three times with a separate pair of treated and control saplings, each time with similar results. Results of two experiments are shown in Figure 6, and one experiment is shown in detail in Table III. Plants of another clone (IB) were used because insufficient material of clone IA was available. These two clones had nearly identical terpene profiles in their needles. For comparison with IB, an additional clone (II) was treated with MeJA, and its volatiles were monitored by SPME analysis over a 4-d period after treatment. Saplings were enclosed in an oven bag (LookTerinex Ltd., Bedford, UK) for a 30-min equilibration period. SPME fibers were inserted into the bag, left for 1 h, and then analyzed immediately by GC-MS.
Extraction of terpenes was essentially as previously described
(Martin et al., 2002
Super Q eluates from automated volatile collection and ethereal extracts from needles were analyzed using a Hewlett-Packard 6890 GC-MS system (70 eV) with a DB-WAX column (0.25 mm x 0.25 µm x 30 m, J&W Scientific, Folsom, CA). Split injections (1 µL) were made at a ratio of 5:1 with an injector temperature of 220°C. The instrument was programmed from an initial temperature of 40°C (3-min hold) and increased at a rate of 1.5°C min–1 until 45°C, 3°C min–1 until 80°C, 5°C min–1 until 180°C, followed by an additional ramp of 10°C min–1 up to 240°C (5-min hold). Helium was used at a constant flow of 1 mL min–1. For routine quantification, monoterpene and sesquiterpene analysis of ethereal extracts was also accomplished with a Hewlett-Packard 6890 GC equipped with a flame ionization detector (FID) fitted with a DB-WAX column as described above. The flow rate was 2 mL H2 min–1, and the FID was operated at 300°C. One microliter of extract was introduced into the injection port at 220°C and a split ratio of 5:1. The GC was programmed with an initial oven temperature of 40°C (3-min hold), a ramp of 3°C min–1 until 80°C, then a ramp of 5°C min–1 until 180°C, followed by a final ramp of 15°C min–1 until 240°C (5-min hold). For SPME analysis, the fiber was inserted directly into the injection port (200°C) of a GC-MS (6890 Agilent GC equipped with a 5973N quadrapole, 70 eV, Agilent, Palo Alto, CA), the program was immediately started, and the SPME fiber was removed after a period of 45 s. The GC was fitted with an HP-5 column (0.25 mm x 0.25 µm x 30 m, Hewlett-Packard), and the He carrier gas flowed at 0.7 mL min–1. The program had an initial oven temperature of 40°C (2-min hold), a ramp of 3°C min–1 until 160°C, then a ramp of 10°C min–1 until 200°C, followed by a final ramp of 20°C min–1 until 300°C (5-min hold). For analysis of chiral compounds, a Cyclodex-B (0.25 mm x 0.25 µm x 30 m, J&W Scientific) column was used with 1 µL of splitless injection. The oven was programmed with an initial temperature of 40°C (2-min hold), a ramp of 1°C min–1 until 80°C, a ramp of 5°C min–1 until 120°C, and a final ramp of 20°C min–1 until 200°C (5-min hold). GC-FID- and GC-MS-generated peaks were integrated using Hewlett-Packard Chemstation software. Concentrations of monoterpenes and sesquiterpenes were calculated by comparing the integrated peak area with that of the internal standard isobutylbenzene. Identification of terpenes was based on comparison of retention times and mass spectra with authentic standards or with mass spectra in the Wiley library.
TPSs were extracted from needles essentially as previously described
(Martin et al., 2002
TPS activities were determined according to published procedures
(Lewinsohn et al., 1991 Conditions for all enzyme assays, including pH optimum, incubation time, substrate concentration, and temperature optimum, were optimized for this system such that maximum activity was achieved in a linear range of product generation. In addition, the possibility that enzyme activities in induced tissues might have been inhibited by additional resin or phenolic substances was ruled out by experiments in which extracts from different stages of the time course were mixed together. In all cases, the resulting enzyme activity was additive, implying that additional compounds found in induced tissues had no effect on enzyme activity.
The extracts of enzyme assays were combined and evaporated to approximately 50 µL. From this, 2 µL was analyzed by GC-MS (6890 Agilent GC equipped with a 5973N quadrupole, 70 eV). The GC was fitted with an HP-5 column (0.25 mm x 0.25 µm x 30 m, Hewlett-Packard), the injection port was operated splitless at 200°C, and the He carrier gas flowed at 0.7 mL min–1. Both monoterpene and sesquiterpene synthase assays were analyzed by the same program. The oven temperature was programmed from 40°C (2-min hold) at 3°C min–1 until 160°C, then at 10°C min–1 until 200°C, followed by 20°C min–1 until 300°C (5-min hold). Chiral analysis of the monoterpene synthase assays was also carried out on GC-MS using a Cyclodex-B (0.25 mm x 0.25 µm x 30 m, J&W Scientific) column with 1-µL splitless injections. The oven temperature was programmed from 40°C (2-min hold) at 1°C min–1 until 80°C, then at 5°C min–1 until 120°C, followed by 20°C min–1 until 200°C (5-min hold). Products were identified by comparing retention times and mass spectra with those of authentic standards.
We thank Drs. Jürgen Schmidt and Armand Seguin for trees, Dr. Rodney Croteau for substrates, and Gazmed Zeneli, Tina Letsch, and Antje Thamm for excellent technical assistance. We would like to thank two anonymous reviewers and the editor for their insightful comments and suggestions that helped to improve an earlier version of the manuscript. Received January 29, 2003; returned for revision February 17, 2003; accepted March 25, 2003.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.021196.
1 This work was supported by the Natural Sciences and Engineering Research
Council of Canada (funds to J.B.), by the Canadian Foundation for Innovation
and the BC Knowledge and Development Funds (funds to J.B.), by the Human
Sciences Frontier Program (funds to J.B.), by the Max Planck Society (funds to
J.G. and fellowship to D.M.), and by the University of British Columbia
(Walter C. Koerner Fellowship to D.M.). * Corresponding author; e-mail bohlmann{at}interchange.ubc.ca; fax 604–822–2114.
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ABSTRACT
RESULTS
-pinene, camphene, and limonene) and the diterpenes (manool and
dehydroabietate) were the most abundant. 
) and control (
) trees.
-terpinene (0.7%); 11, linalool (72.9%); 12, borneol (1.1%); and
13, 
-selinene
synthase and 
