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Plant Physiol. (1998) 118: 1389-1393
Biosynthesis of Camalexin from Tryptophan Pathway Intermediates
in Cell-Suspension Cultures of Arabidopsis1
Michael Zook*
Department of Botany and Plant Pathology, Michigan State
University, East Lansing, Michigan 48824
 |
ABSTRACT |
Camalexin (3-thiazol-2 -yl-indole) is
the principal phytoalexin that accumulates in Arabidopsis
after infection by fungi or bacteria. Camalexin
accumulation was detectable in Arabidopsis cell-suspension cultures 3 to 5 h after inoculation with Cochliobolus carbonum
(Race 1), and then increased rapidly from 7 to 24 h after inoculation. Levels of radioactivity incorporated into camalexin during
a 1.5-h pulse labeling with [14C]anthranilate also
increased with time after fungal inoculation. The levels of radioactive
incorporation into camalexin increased rapidly between 7 and 18 h
after inoculation, and then decreased along with camalexin
accumulation. Relatively low levels of radioactivity from
[14C]anthranilate incorporated into camalexin in
the noninoculated controls. Autoradiographic analysis of the
accumulation of chloroform-extractable metabolites labeled with
[14C]anthranilate revealed a transient increase in the
incorporation of radioactivity into indole in fungus-inoculated
Arabidopsis cell cultures. The time-course measurement of radioactive
incorporation into camalexin during a 1.5-h pulse labeling with
[14C]indole was similar to that with
[14C]anthranilate. These data suggest that indole
destined for camalexin synthesis is produced by a separate enzymatic
reaction that does not involve tryptophan synthase.
| |
INTRODUCTION |
One of the most intensively studied disease-resistance mechanisms
of plants is the accumulation of phytoalexins. Apart from this
function, there is interest in phytoalexins because the induction of
synthesis of these secondary metabolites provides unique experimental systems for the study of the coordinate regulation of primary and
secondary metabolic pathways. One system that likely involves the
coordinate regulation of these pathways is the biosynthesis of
phytoalexins in Arabidopsis.
Arabidopsis has several attributes that are ideal for the
genetic analysis of disease-resistance mechanisms (Meyerowitz, 1989 ; Kunkel, 1996). It accumulates the phytoalexin camalexin
(3-thiazol-2-yl-indole) (Tsuji et al., 1992), a compound originally
isolated from another crucifer, Camelina sativa (Browne et
al., 1991). This metabolite is typical of crucifer phytoalexins in
having an indole group substituted at the no. 3 position with a
sulfur-containing group (Chapple et al., 1994). In in vitro
bioassays, camalexin is inhibitory to bacterial and fungal growth
(Jejelowo et al., 1991; Tsuji et al., 1992; Rogers et al., 1996).
Mutants of Arabidopsis deficient in camalexin accumulation have been
isolated (Glazebrook and Ausubel, 1994). These pad mutants
have not yet provided clear evidence for the role of camalexin in the
disease resistance of Arabidopsis, but a recently isolated
pad4 mutant exhibits an interesting phenotype that may
provide insight into differential host plant responses between
pathogens and nonpathogens (Glazebrook et al., 1997).
Advances have been made in recent years in the study of Trp synthesis
in Arabidopsis (Radwanski and Last, 1995). The study of individual
steps in the Trp pathway is important to understand the coordinate
regulation of the Trp and camalexin pathways during the induction of
camalexin synthesis. Labeling studies have provided evidence that
anthranilate, a Trp-pathway intermediate, but not Trp itself, is a
precursor of camalexin (Tsuji et al., 1993; Zook and Hammerschmidt,
1997). Furthermore, there is a close correlation between the level of
induction of anthranilate synthase and camalexin accumulation in
response to different eliciting agents (Zhao and Last, 1996). However,
there remains uncertainty about what Trp intermediate is the branch
point between the Trp and camalexin biosynthetic pathways. In the
current study suspension cultures of Arabidopsis cells inoculated with
fungal spores were used to characterize the biosynthetic relationship
between Trp-pathway intermediates and the accumulation of the camalexin
phytoalexin.
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MATERIALS AND METHODS |
Cell-Suspension Cultures
Cell-suspension cultures of Arabidopsis (ecotype Columbia) were
obtained using a protocol originally devised by Axelos et al. (1992).
Cultures were subcultured weekly into 3.2 g/L Gamborg's basal medium
with minimal organics (Sigma), 2% (w/v) Suc, and 1.1 mg/L 2,4-D, pH
5.7.
Fungal Inoculum
Cochliobolus carbonum (Race 1) was grown on
vegetable-juice agar (163 mL/L vegetable juice, 1.0 g/L
CaCO3, and 14 g/L agar [Sigma]) for 7 to
10 d. Fifty milliliters of Arabidopsis cell cultures (3-4 d after
subculturing) was inoculated under sterile conditions with 1.5 × 106 spores.
Labeling of Cell Cultures with [14C]Anthranilate or
[14C]Indole and Quantitation of Camalexin Accumulation
Seven microliters (1.5 × 106 dpm) of
[U-14C]anthranilate (60 mCi/mmol) in ethanol or
5 µL (1.1 × 106 dpm) of
[2-14C]indole (25 mCi/mmol) in ethanol was
added to 50 mL of Arabidopsis cell-suspension culture 1.5 h before
harvesting of the cell culture for determination of levels of
radioactivity incorporated into camalexin. At the time of harvest, the
cell-suspension cultures were filtered through a single layer of
premoistened Miracloth (Calbiochem). The filtrate was then extracted
twice with an equal volume of CHCl3. The pooled
CHCl3 extracts were evaporated under reduced
pressure, and the remaining residue was redissolved in CHCl3 and applied to a TLC plate. The TLC plate
was developed with CHCl3:methanol (9:1, v/v) and
analyzed by autoradiography, or camalexin was visualized with
short-wave UV light and scraped from the TLC plate for determination of
radioactivity. For quantitation of camalexin, the TLC plate scrapings
were treated with ethyl acetate and filtered through a sintered-glass
funnel. The ethyl acetate solution was evaporated under a stream of
nitrogen, and the remaining residue was redissolved in 100 µL of 7%
isopropanol in hexane (HPLC mobile phase) before injection onto a
5-µm × 150-mm × 4.6-mm silica HPLC column (Econosphere,
Alltech, Deerfield, IL) developed with a 1.0 mL/min flow rate. The
eluent from the column was monitored at
A210 using a variable-wavelength detector. The amount of camalexin detected at A210 was
determined by comparison of known standards of camalexin.
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RESULTS |
To be useful as an experimental system for the study of camalexin
biosynthesis, a suitable eliciting agent had to be found that could
generate a sufficient amount of camalexin after treatment or
inoculation of cell-suspension cultures. Several elicitors that have
proven to be effective in other plant cell-suspension cultures were
applied. A "void-glucan elicitor" prepared by partial acid
hydrolysis of mycelial walls of Phytophthora sojae (provided by Dr. Michael Hahn, University of Georgia, Athens) and cellulase R10
(Karlan Research Products, Santa Rosa, CA), which elicit phytoalexin accumulation in parsley and tobacco cell-suspension cultures, respectively (Lois et al., 1989; Vögeli et al., 1990), were
ineffective. A variety of commercially available cell wall-degrading
enzymes were either ineffective or elicited only a relatively small
amount of camalexin. Inoculation of cell-suspension cultures with the bacterial pathogen Pseudomonas syringae pv
maculicola strain ES4326 elicited only small amounts of
camalexin. The only treatment that proved effective in eliciting a
significant accumulation of camalexin was viable spores of C. carbonum (Fig. 1). Camalexin
accumulation began to increase 5 to 7 h after inoculation, peaked
between 18 and 24 h after inoculation, and then decreased. Very
low levels of camalexin were present in untreated cell-suspension
cultures.
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| Figure 1.
Accumulation of camalexin in Arabidopsis
cell-suspension cultures after inoculation with a C. carbonum spore suspension ( ) or no treatment ( ). The
fungal inoculum and determination of the levels of camalexin
accumulation in each 50-mL culture are described in ``Materials and Methods''. All data points represent means of three
determinations ± SE (except the 0- and 3-h time
points, which represent means of two determinations ± SE).
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One of the main advantages of using a cell-suspension system for the
study of phytoalexin synthesis is that radiolabeled compounds can be
easily applied to cell-suspension cultures. Arabidopsis cultures were
pulse labeled with [14C]anthranilate for
1.5 h before determining the incorporation of radioactivity into
camalexin as a function of time after inoculation with C. carbonum (Fig. 2). The level of
incorporation of radioactivity that occurs during a relatively short
period of labeling (1.5 h) is expected to be a measure of the rate of
synthesis or substrate flow into the final product (camalexin).
Therefore, as the level of camalexin accumulation increases, the level
of incorporation of biosynthetic intermediates would be expected to
increase because of the increased rate of synthesis or flow of
substrate through the pathway.
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| Figure 2.
Incorporation of radioactivity from
[14C]anthranilate into camalexin in Arabidopsis
cell-suspension cultures after inoculation with a C. carbonum spore suspension () or no treatment ().
Radioactivity was allowed to incorporate into camalexin for 1.5 h
before each time point, as described in ``Materials and Methods''.
All data points represent means of three determinations ± SE (except the 0- and 3-h time points, which represent
means of two determinations ± SE).
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Data from previous studies (Tsuji et al., 1993; Zook and Hammerschmidt,
1997) suggest that anthranilate is an intermediate of camalexin
synthesis. Consistent with this hypothesis, the level of radioactivity
incorporated into camalexin from
[14C]anthranilate increased as the rate of
camalexin accumulation increased. The greatest increase in camalexin
accumulation occurred between 12 and 18 h after inoculation with
C. carbonum; likewise, the highest level of incorporation of
radioactivity into camalexin occurred 18 h after inoculation. The
levels of radioactivity incorporated into camalexin also decreased in a
manner similar to the levels of camalexin between 24 and 48 h
after inoculation.
An autoradiographic analysis of chloroform extracts from each time
point of the [14C]anthranilate pulse-labeling
experiments (Fig. 2) revealed the transient accumulation of a compound
with a higher RF than camalexin (Fig.
3). The compound was eluted from the TLC
plate with ethyl acetate, and after careful evaporation of the solvent
under a stream of nitrogen, the residue had the very distinctive aroma of indole. HPLC analysis of the residue revealed that more than 95% of
the radioactivity in a single peak comigrated with a pure indole
standard. Pulse labeling of C. carbonum with
[14C]anthranilate grown in plant cell culture
medium failed to reveal the presence of compounds that comigrated with
indole or camalexin by TLC analysis (data not shown).
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| Figure 3.
Autoradiogram of a TLC separation of chloroform
extracts of Arabidopsis cell-suspension culture filtrates after
inoculation with a C. carbonum spore suspension (lanes
1-9) or no treatment (lane 10). [14C]Anthranilate was
applied 1.5 h before each of the following times after fungal
inoculation: 3 h (lane 1), 5 h (lane 2), 7 h (lane 3),
9 h (lane 4), 12 h (lane 5), 18 h (lane 6), 24 h
(lane 7), 36 h (lane 8), 48 h (lane 9), and 24 h (lane
10). Preparation of chloroform extracts and TLC/autoradiography is
described in ``Materials and Methods''.
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To determine if indole is a precursor of camalexin, Arabidopsis cell
cultures were pulse labeled with [14C]indole
(Fig. 4) in the same manner as shown in
Figure 2 for [14C]anthranilate. Similar to
[14C]anthranilate incorporation, the levels of
radioactivity incorporated into camalexin increased as the rate of
camalexin accumulation increased.
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| Figure 4.
Incorporation of radioactivity from
[14C]indole into camalexin in Arabidopsis cell-suspension
cultures after inoculation with a C. carbonum spore
suspension () or no treatment (). Radioactivity was allowed to
incorporate into camalexin for 1.5 h before each time point, as
described in ``Materials and Methods''.
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DISCUSSION |
Because previous studies of camalexin biosynthesis using detached
leaves of Arabidopsis have provided evidence that anthranilate is a
biosynthetic precursor of camalexin (Tsuji et al., 1993; Zook and
Hammerschmidt, 1997), similar results were expected from these
experiments with cell-suspension cultures of Arabidopsis. The level of
radioactivity incorporated into camalexin from
[14C]anthranilate increased as the rate of
camalexin accumulation increased (Figs. 1 and 2). An unexpected result
of the pulse-labeling experiments with
[14C]anthranilate, however, was the transient
accumulation of label from anthranilate into indole (Fig. 3). Indole is
the immediate precursor of Trp in the Trp synthase complex, but there
is evidence that indole is not a "free intermediate" in Trp
synthesis (Creighton, 1970). Indole is thought to pass directly from
the  -subunit to the  -subunit though a tunnel in the Trp synthase
complex (Hyde et al., 1988). Therefore, indole is not expected to
accumulate, even if there is an increase in the flux through the
pathway.
A recent study by Frey et al. (1997) may offer an explanation for the
apparent accumulation of free indole in camalexin-synthesizing Arabidopsis cell cultures. This study identified a gene
(BX1) that encodes a Trp synthase -subunit homolog. The
encoded enzyme catalyzes the formation of a free indole destined for
2,4-dihydroxy-1,4-benzoxazin-3-one synthesis rather than for Trp
synthesis. Evidence for the formation of free indole during the
elicitation of camalexin synthesis in the present study (Fig. 3)
supports the hypothesis originally proposed by Frey et al. (1997) that
there may be a homolog of BX1 in Arabidopsis. This homolog
would encode an enzyme that catalyzes the formation of indole from
indole-3-glycerol phosphate for camalexin synthesis (Fig.
5).
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| Figure 5.
Abbreviated Trp biosynthetic pathway showing
hypothetical branch point for camalexin biosynthesis. TSA, Trp synthase
-subunit; TSB, Trp synthase -subunit.
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There is a gene in Arabidopsis that may be the homolog of
BX1 (accession no. F20005 for the 5 end of the expressed
sequence tag and accession no. F20004 for the 3 end of the expressed sequence tag). This gene is also found in a 100-kb bacterial artificial chromosome clone (T10P11, Cold Spring Harbor Laboratory;
accession no. AC002354) located in the upper portion of chromosome 4. The putative coding region of the Arabidopsis gene encodes a 275-amino acid protein (Mr = 30,000) with
approximately 80% sequence identity to the -subunit of the
Arabidopsis Trp synthase (data not shown). The presence of this homolog
may account for one or more of the additional bands that appeared under
low-stringency genomic DNA gel-blot hybridization using TSA1
cDNA as a probe (Radwanski et al., 1995).
The relative efficiency of incorporation of radioactivity from
[14C]indole into camalexin that accompanied the
increase in the accumulation rate of camalexin (Fig. 4) is consistent
with the hypothesis that indole is a biosynthetic intermediate of
camalexin. The overall efficiency of incorporation of radioactivity
into camalexin from [14C]indole was
approximately twice that for [14C]anthranilate.
If indole is the more immediate precursor of camalexin compared with
anthranilate, then the incorporation efficiency of anthranilate may be
less because of diversion of this intermediate toward the synthesis of
other secondary metabolites that do not include indole as a
biosynthetic precursor. Differences in incorporation efficiencies
between indole and anthranilate may also result from differences in
chemical properties of these two compounds.
The results of the current study and those of previous studies (Tsuji
et al., 1993; Zhao and Last, 1996; Zook and Hammerschmidt, 1997) are
consistent with the hypothesis that the synthesis of camalexin involves
steps of the Trp pathway. Also, there is good evidence for the
induction of an increase in transcript and protein levels of
Trp-pathway enzymes after microbial infection (Niyogi and Fink, 1992;
Niyogi et al., 1993; Zhao and Last, 1996). This induction of an
apparent increase in substrate flow through the Trp pathway during
camalexin synthesis is expected if biosynthetic precursors of camalexin
originate from the Trp pathway. In addition to camalexin, other
defense-related secondary metabolites derived from the Trp pathway may
be synthesized after microbial infection.
There are also results from investigations of biosynthetic pathways
that do not offer obvious explanations. Zhao and Last (1996) reported
that a phosphoribosyl-anthranilate transferase (PAT1)
mutant, trp1-100, and an anthranilate
synthase/PAT1 double mutant,
trp4/trp1-100, accumulated to near wild-type
levels of camalexin after infection with P. syringae pv
maculicola ES4326. A large reduction in the activity of
enzymes early in the Trp pathway is expected to reduce the flow of
substrate into camalexin. There was some reduction in the levels of
camalexin accumulation in the infected Trp mutants compared with
infected wild-type plants, but the percentage level of reduction was
not as large as that previously reported (Tsuji et al., 1993) using
AgNO3 as an elicitor of camalexin accumulation.
P. syringae pv maculicola ES4326 elicited about a
20-fold greater amount of camalexin compared with
AgNO3, and this greater flux of substrate through
the pathway after infection may overcome constraints caused by
enzyme-activity deficiencies in the mutants.
Analysis of an allelic series of trp1 mutants revealed that
the prototrophic mutants, including trp1-100, grew normally
with less than 1% of normal PAT1 activity (Rose et al.,
1997). If the single-copy PAT1 gene were completely knocked
out, the Trp pathway would be blocked, and the mutation would be lethal
because of auxin and Trp starvation (Rose et al., 1997). Therefore, the
amount of PAT1 activity required for normal growth and
camalexin accumulation is much less than that present in wild-type
plants. Characterization of the anthranilate synthase -subunit gene
(Niyogi et al., 1993), the defective gene in trp4 mutants,
revealed three very similar genes in the Arabidopsis genome. This gene
duplication apparently accounts for the normal growth of
trp4-1 mutants (Niyogi et al., 1993). Despite the fact that
the trp4/trp1-100 double mutant is an auxotroph,
there is apparently enough flow through the Trp pathway to support near
wild-type levels of camalexin accumulation.
The duplication of genes of the Trp pathway (Radwanski and Last, 1995),
with the exception of PAT1 (Rose et al., 1992), has been
proposed as one of the reasons for the failure to isolate Trp
auxotrophs (Radwanski et al., 1996). The existence of multiple isozymes
of Trp-pathway genes also may allow for independent regulation of
substrate flow through the Trp and camalexin pathways. In the case of
Ruta graveolens, there are two isozymes of the -subunit of anthranilate synthase (Bohlmann et al., 1995) that appear
differentially with respect to the synthesis of alkaloids and Trp
(Bohlmann et al., 1996). A similar method of regulation may exist for
camalexin synthesis (Fig. 5). The synthesis of free indole destined for camalexin synthesis may provide a means to independently regulate the
flow of substrate between the camalexin and Trp pathways.
Work is currently in progress to determine the enzymatic reactions that
might involve indole in the synthesis of camalexin. One possible
reaction is the carboxylation of indole, and it has been proposed that
indole-3-carboxaldehyde condenses with Cys to form camalexin (Browne et
al., 1991). There is evidence that Cys is involved in camalexin
biosynthesis (Zook and Hammerschmidt, 1997). Elucidation of the steps
in the camalexin biosynthetic pathway is important for gaining
additional insight into the regulation of the biosynthesis of secondary
metabolites used in plant defense mechanisms.
| |
FOOTNOTES |
1
This research was supported in part by the
Michigan State University Agricultural Experiment Station and by grant
no. IBN-9220912 from the National Science Foundation.
*
Dr. Zook passed away in July 1998. Please address all correspondence
to: Dr. Ray Hammerschmidt, Department of Botany and Plant Pathology,
Michigan State University, East Lansing, MI 48824; e-mail
hammerS1{at}pilot.msu.edu; fax 1-517-353-1926.
Received January 30, 1998;
accepted September 14, 1998.
| |
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G. Brader, E. Tas, and E. T. Palva
Jasmonate-Dependent Induction of Indole Glucosinolates in Arabidopsis by Culture Filtrates of the Nonspecific Pathogen Erwinia carotovora
Plant Physiology,
June 1, 2001;
126(2):
849 - 860.
[Abstract]
[Full Text]
[PDF]
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M. Frey, C. Stettner, P. W. Paré, E. A. Schmelz, J. H. Tumlinson, and A. Gierl
An herbivore elicitor activates the gene for indole emission in maize
PNAS,
November 29, 2000;
(2000)
260499897.
[Abstract]
[Full Text]
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N. Zhou, T. L. Tootle, and J. Glazebrook
Arabidopsis PAD3, a Gene Required for Camalexin Biosynthesis, Encodes a Putative Cytochrome P450 Monooxygenase
PLANT CELL,
December 1, 1999;
11(12):
2419 - 2428.
[Abstract]
[Full Text]
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M. Frey, C. Stettner, P. W. Pare, E. A. Schmelz, J. H. Tumlinson, and A. Gierl
An herbivore elicitor activates the gene for indole emission in maize
PNAS,
December 19, 2000;
97(26):
14801 - 14806.
[Abstract]
[Full Text]
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Top
Abstract
Introduction