To determine whether SA or aspirin affect the enzymatic activity of
AOS, its capacity for conversion of 13-HPLA to 12-oxo-PDA was examined
in the presence and absence of these substances. To this end, total
protein from flax seed was isolated (Song and Brash, 1991
) and
incubated in buffer either with or without different concentrations of
SA and aspirin. None of the concentrations of SA or aspirin used showed
any effect on AOS activity (Fig. 7). Even
at higher concentrations (up to 3 mM) the ability of the enzyme to form 12-oxo-PDA was not affected (data not shown). These data
suggest that SA and aspirin do not inhibit the enzymatic activity of
flax AOS.
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[in this window]
[in a new window]
| Figure 7.
Effect of aspirin and SA on AOS activity. The
enzymatic activity of AOS was analyzed as described by Harms et al.
(1995) in the absence and presence of increasing concentrations of
either aspirin or SA. Specific AOS activity in flax leaf extracts is
given in nanograms of 12-oxo-PDA per microgram of total protein.
|
|
Wound-Induced AOS Gene Expression Is Blocked by Aspirin
Because wound-induced JA accumulation is inhibited by SA and
aspirin and neither substance affected AOS enzymatic activity, we
decided to analyze the effect of these substances on the wound-induced AOS gene expression at the RNA level. To this end, detached flax leaves
were incubated in water or pretreated with aspirin or SA and
subsequently wounded. Because wound-induced AOS gene expression reaches
its maximum 6 h after wounding (Fig. 2), total RNA was isolated
from leaves 6 and 20 h after treatment. As expected, mechanical
wounding led to an accumulation of AOS in both the directly wounded and
the systemic unwounded leaves (Fig. 8).
Surprisingly, pretreatment of the detached flax leaves with 1 mM aspirin led to a reduction of the wound-induced
accumulation of AOS transcripts. This reduction occurred in both the
damaged and the systemic nondamaged tissues. Similar results were
obtained by using SA (data not shown). These data strongly suggest that
aspirin or SA inhibit wound-induced JA biosynthesis by blocking AOS
gene expression at the transcriptional level.
View larger version (33K):
[in this window]
[in a new window]
| Figure 8.
Influence of aspirin on AOS mRNA levels in flax
leaves. Excised flax plants were preincubated with buffer or aspirin
for 2 h, as described previously, and were subsequently wounded.
RNA was isolated from flax leaves of intact plants before wounding (C)
and from directly wounded (L) and systemic unwounded (S) leaves at the
times shown after treatment. Amounts of RNA were confirmed as described
in Figure 1. Blots were probed with the flax AOS cDNA and the
corresponding densitogram is shown.
|
|
 |
DISCUSSION |
AOS has been postulated to play a key role in the biosynthesis of
JA (Vick and Zimmerman, 1987; Hamberg and Gardner, 1992). Overexpression of the flax AOS cDNA in transgenic potato plants leads
to an increase in endogenous JA levels by 8- to 12-fold compared with
nontransformed potato plants (Harms et al., 1995). These results
suggest that potato leaves possess the factors needed for JA formation
and that no previous stimuli are required for their release.
Furthermore, they suggest that the amounts of JA present in normal
plants are determined by the amount of AOS activity, which may
represent the major rate-limiting step of the biosynthetic pathway of
JA. AOS has been found to be ubiquitous in plants (Brash and Song,
1995; Simpson and Gardner, 1995) and differs in the distribution of its
activity in different tissues (Vick and Zimmerman, 1987; Simpson and
Gardner, 1995). Recently, Laudert et al. (1996) demonstrated that a
single gene for AOS is likely present in the genome of Arabidopsis.
Similar organization has been observed in flax, tomato, and potato
plants (H. P
na-Cortés, unpublished data). AOS is
constitutively expressed in most tissues of flax plants (Fig. 1), the
amounts of transcript being higher in flax seeds. Its physiological
role in this organ is unclear, because total enzyme activity is very
high in seeds compared with vegetative tissues (Vick and Zimmerman,
1987). The constitutive AOS expression seen in all tissues may be
required for the formation of AOS to maintain a certain amount of the
protein required for the formation of basal levels of JA.
It is interesting that AOS gene expression can be enhanced transiently
in flax leaves after mechanical wounding. This gene activation is not
limited to the wounded leaves; it also takes place in the unwounded
leaves located distally to the wounded leaves. The nondamaged leaves of
a wounded plant readily accumulate AOS mRNA, albeit with a short delay
compared with the directly wounded leaves, thus resulting in lower
levels of AOS at a given time in the systemically induced leaves
compared with the locally induced leaves. Elevation of AOS transcript
amounts can be detected as soon as 10 min after wounding (data not
shown), with the increase being clearly detectable after 1 h and a
maximum being reached at 5 to 7 h (about 3-fold higher than the
levels present in unwounded leaves). This increase declines to 70% of
the maximum value after 11 h, returning to values similar to those
of the nontreated leaves 26 h after treatment.
The kinetics of the wound-induced accumulation of flax AOS mRNA differ
from the wound kinetics of Arabidopsis AOS (Laudert et al., 1996).
Although Arabidopsis AOS transcripts also increase transiently after
mechanical wounding, they reach maximum levels between 60 and 90 min
and decrease rapidly in the next 30 min. As mentioned above, the
increase of flax AOS transcript levels remains elevated for several
hours, and a decline can only be observed 11 h after the start of
the treatment. AOS mRNA accumulation in Arabidopsis leaves correlates
with an increase in JA levels. This increase occurs in the first 90 min
after wounding and levels decline rapidly to basal levels in the next
2 h (Laudert et al., 1996). JA accumulation in flax leaves follows
different kinetics than in Arabidopsis leaves. The JA levels increase
and reach maximum levels 6 h after wounding and remain elevated
for the next 26 h. Both AOS gene expression and JA biosynthesis
are affected in both Arabidopsis and flax plants after mechanical
wounding.
However, there are clear differences between the genera in response to
this stimuli. Whereas Arabidopsis plants react quickly by a transient
accumulation of AOS mRNA and JA after wounding, the response in flax
leaves occurs more slowly and the accumulation of AOS transcripts and
JA remains detectable for several hours. Although such differences
could be explained by dissimilarities in the procedure used to perform
the mechanical wounding or in experimental conditions, fundamental
differences in the metabolic pathway between both plants cannot be
ruled out. For instance, the wound-induced accumulation of JA in flax
resembles the kinetics observed in potato and tomato leaves, in which
the maximum levels of JA are reached 6 h after mechanical wounding
(Peña-Cortés et al., 1993, 1995; Harms et al., 1995; Herde
et al., 1996). Furthermore, JA pools also increase transiently in
tobacco leaves after mechanical damage (Baldwin et al., 1994). Within
0.5 and 2 h after damage, the shoot and the root JA pools of
damaged tobacco plants were significantly greater than the
corresponding levels of unwounded plants. JA levels of damaged leaves
decreased to levels found in unwounded plants 10 h after harvest.
Together, these results suggest that plants may respond to the same
stimulus with some dissimilarities, which may depend on certain
differences in their metabolic (biosynthetic and/or catabolic)
pathways.
AOS involvement in JA biosynthesis has been well documented (Vick and
Zimmerman, 1987; Song and Brash, 1991; Harms et al., 1995), as has the
involvement of JA in the regulation of wound-induced gene expression in
plants (Farmer, 1994; Peña-Cortés et al., 1995). JA has
also been shown to be involved in systemic wound-induced gene
expression (Farmer and Ryan, 1992; Peña-Cortés and
Willmitzer, 1995; Bergey et al., 1996). Because AOS mRNA accumulates in
directly wounded tissues and, based on the correlation with JA
accumulation, an increase of JA in the systemic unwounded leaves as a
result of AOS gene activation is also to be expected. The local and
systemic AOS gene activation supports earlier results on the
involvement of increased levels of JA in both local and systemic
wound-induced gene activation (Bergey et al., 1996; Herde et al., 1996;
Peña-Cortés et al., 1996).
Several components of the octadecanoid pathway, such as linolenic acid,
13-HPLA, and 12-oxo-PDA, as well as JA, are able to activate
wound-responsive genes (Farmer 1994). Flax AOS gene expression is
activated by treatment with JA. This activation occurs in a dose-dependent manner, with 50 µM being the most
effective concentration. Similar results were obtained by applying the
same concentration of 12-oxo-PDA and the bacterial phytotoxin
coronatine (data not shown). Although coronatine exhibits a high
structural similarity to 12-oxo-PDA, it cannot be converted to JA
(Weiler et al., 1994). Thus, coronatine-induced AOS gene expression
strongly supports previous results postulating the involvement of the
intermediates of the JA biosynthetic pathway (i.e. 12-oxo-PDA) in the
modulation of wound-responsive genes (Weiler et al., 1994; Blechert et
al., 1995). Furthermore, these results strongly suggest that the
precursors of JA, 12-oxo-PDA, and JA itself are able to activate their
own biosynthetic pathway in flax leaves.
As mentioned previously, wound-induced AOS mRNA accumulation take place
very fast, the transcript being detectable in flax leaves within the
first 10 min after wounding (data not shown) and after 15 min in
Arabidopsis plants (Laudert et al., 1996). However, this fast
activation can be blocked with protein-synthesis inhibitors.
Cycloheximide (an inhibitor of cytoplasmic protein biosynthesis)
prevents AOS mRNA accumulation upon wounding, whereas chloramphenicol
(affecting protein biosynthesis in the chloroplasts) does not. These
results suggest that the wound-induced activation of AOS gene
expression depends on the de novo biosynthesis of cytoplasmic
protein(s) that are required in the signaling-pathway-modulating wound
response (Peña-Cortés et al., 1989).
Both SA and aspirin lead to a reduction in the wound-induced JA
accumulation in flax leaves. These results confirm the previous finding
by Peña-Cortés et al. (1993) that application of these substances inhibits the effect of wounding in JA accumulation. Evidence
obtained by analyzing pin2 gene expression using different intermediates of the JA biosynthetic pathway in the presence and absence of aspirin or SA showed that only 12-oxo-PDA and JA overcome the inhibitory effect of these substances. Thus, it was suggested that
SA and aspirin may inhibit the enzymatic activity of AOS, the enzyme
responsible for the conversion of 13-HPLA to 12-oxo-PDA. These
substances are synthesized by a pathway involving oxygenation and
cyclization steps, which shows a strong resemblance to the proposed
biosynthetic pathway of eicosanoids in animals (Needleman et al.,
1986). It has been shown that the chemical structures of JA and
12-oxo-PDA are very similar to those of animal prostaglandins (Vick and
Zimmerman, 1983). In plants 12-oxo-PDA can be produced either by an
enzymatic process involving the enzymes AOS and AOC or by spontaneous
cyclization of the allene oxide, resulting in a racemic mixture of
12-oxo-PDA, one raceme being the direct precursor of (+)-7-iso-JA
(Hamberg and Gardner, 1992). The allene oxide produced by the action of
AOS can spontaneously be converted to 12-oxo-PDA by a mechanism that
does not require the involvement of AOC. If AOC activity alone was
affected by the inhibitors, we should be able to observe a small
fraction of racemic 12-oxo-PDA as a result of spontaneous formation and
a corresponding accumulation of JA upon mechanical wounding, even in
the presence of aspirin or SA. Because we could not detect any increase
of JA after such treatments, we assume that both aspirin and SA act on
AOS and not on AOC.
Aspirin and SA were postulated to prevent the formation of 12-oxo-PDA
by negatively affecting AOS enzymatic activity (Peña-Cortés et al., 1993). In human cells aspirin acetylates a Ser residue of the
catalytic site of prostaglandin endoperoxide synthetase, causing an
irreversible inhibition of the cyclooxygenase activity and thus
preventing prostaglandin biosynthesis (Van der Ouderaa et al., 1980).
Furthermore, SA is an effective inhibitor of cyclooxygenase-2 activity,
thereby preventing the formation of prostanoids at the site of
inflammation (Mitchell et al., 1997). Examination of flax AOS activity
using a protein extract from flax seeds in the absence or presence of
increasing concentrations of SA or aspirin clearly shows that neither
substance influences the formation of 12-oxo-PDA. These data indicate
that the components (either the enzymes AOS and AOC or via a
spontaneous mechanism) allowing the formation of 12-oxo-PDA in this
system are not affected by aspirin or SA. Both substances prevent the
accumulation of AOS mRNA in flax leaves after mechanical wounding. Flax
leaves pretreated with aspirin clearly show lower levels of AOS
transcripts upon wounding than leaves of untreated plants. This effect
is not limited to local AOS gene expression but is also seen in the
systemic accumulation of AOS mRNA. These results, however, do not
permit the determination of whether both substances alter the steady
state of AOS transcript levels or the wound-induced accumulation of AOS
mRNA. Because the AOS protein levels are not changed in the treated
leaves (data not shown), the results obtained here may indicate that
both SA and aspirin suppress the wound-induced accumulation of AOS,
most likely by altering some component of the transcriptional
machinery.
Several studies have demonstrated the role of SA and aspirin in the
regulatory mechanisms involved in different biological processes. In
HeLa cells, SA activates the human heat-shock transcription factor.
Like heat shock, salicylate may interfere with protein synthesis or
lead to the accumulation of aberrant newly synthesized proteins
(Jurivich et al., 1992). It has also been reported that SA and aspirin
inhibit the activation of the transcription of NF-
B in transfected T
cells (Kopp and Ghosh, 1994). Most of the genes known to be activated
by NF-B are involved in the immune and inflammatory responses
(Grilli et al., 1993). Bestatin, an inhibitor of some aminopeptidases
in plants and animals, inhibits NF-B degradation in liver nuclei,
whereas cycloheximide blocks the activation of NF-B (Cressman and
Taub, 1994). More recently, Schaller et al. (1995) reported that
Bestatin acts as a powerful inducer in tomato leaves of defense genes
that are also induced by herbivore attack, mechanical wounding,
systemin, and JA. Because Bestatin does not influence the internal
levels of JA, it was assumed that the site of action of Bestatin is
located downstream of the octadecanoid pathway. This substance may
exert its effect at or near the levels of gene transcription by
inhibiting a regulatory protease (Schaller et al., 1995).
It has also been reported that aspirin and SA influence animal and
plant gene expression by affecting the accumulation of the
corresponding transcripts. Thus, low levels of aspirin and SA suppress
the accumulation of the 2.7-kb prostaglandin synthase mRNA after
interleukin-1 treatment (Wu et al., 1991). These substances also
inhibit the wound-inducible ACC synthase transcript in tomato fruit (Li
et al., 1992). Moreover, Kim et al. (1992) demonstrated that SA and
aspirin inhibit the Suc response of the potato pin2 promoter,
suggesting the interaction of SA with a receptor. In addition,
salicylate-like drugs have the ability to inhibit the accumulation of
steady-state levels of nitric oxide synthase mRNA and subsequent nitric
oxide synthase-2 enzymes and nitrite production in cultured neonatal
rat cardiac fibroblasts (Farivar and Brecher, 1996; Farivar et al.,
1996).
In summary, the similarity of the effects of aspirin, SA, and
cycloheximide on NF-B in animal cells and on the wound-induced AOS
gene expression in flax plants strongly suggests the presence of some
common features between the signal transduction pathway mediating
stress response in both animals and plants, as already proposed by
Bergey et al. (1996).
| |
FOOTNOTES |
1
This work was supported by Fondecyt grant no.
1970121 to H.P.-C.
*
Corresponding author; e-mail hpena{at}lauca.usach.cl; fax
56-2-681-9036.
Received March 9, 1998;
accepted August 2, 1998.
| |
ABBREVIATIONS |
Abbreviations:
AOC, allene oxide cyclase.
AOS, allene oxide
synthase.
13-HPLA, 13-hydroperoxylinolenic acid.
JA, jasmonic acid.
NF-B, nuclear factor B.
12-oxo-PDA, 12-oxo-phytodienoic acid.
SA, salicylic acid.
| |
ACKNOWLEDGMENTS |
We thank Prof. Lothar Willmitzer for continuous support and
encouragement. We also thank Dr. A. Brash for the flax cDNA and AOS
antibody and Dr. C. Wasternack and Dr. R. Atzorn (Institut für
Pflanzenbiochemie, Halle, Germany) for assistance with JA determination. We are also thankful to Regina Breitfeld for taking care
of our plants in the greenhouse and to Antje Voigt for the photographic
work. Many thanks to Dr. Nicholas Provart for useful comments on the
manuscript.
| |
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Sanduja R,
Tsai A-L,
Ferhanoglu B,
Loose-Mitchell DS
(1991)
Aspirin inhibits interleukin 1-induced prostaglandin H synthase expression in cultured endothelial cells.
Proc Natl Acad Sci USA
88:
2384-2387
[Abstract/Free Full Text]
1 fresh weight) and reached a maximum (6700 pmol JA equivalents g
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Abstract
Introduction
- and 
-ketol fatty
acids implicates this type of oxygenase in the biosynthetic pathway of
the phytohormone JA.
