Báo cáo khoa học: Plant oxylipins: Plant responses to 12-oxo-phytodienoic acid are governed by its specific structural and functional properties ppt

MINIREVIEW
Plant oxylipins: Plant responses to 12-oxo-phytodienoic
acid are governed by its specific structural and functional
properties
Christine Bo
¨
ttcher
1
and Stephan Pollmann
2
1 CSIRO Plant Industry, Adelaide, Australia
2 Department of Plant Physiology, Ruhr-University Bochum, Germany
Introduction
Plants are permanently exposed to a multitude of var-
iable environment cues, and thus have to cope with
changes in, for example, temperature, light quality,
exposure to UV light, mechanical forces and water
availability, as well as osmotic stress, wounding and
pathogen challenges [1–8]. Over time, plants have
evolved several physical barriers as defensive weap-
ons, i.e. the cuticula, thorns and stinging hairs, as
well as constitutively expressed toxic compounds or
enzymes. In addition to these morphological adapta-
tions, plants have established inducible systems.
Despite the fact that plants possess neither an
immune system nor a nervous system like animals,
they are able to defeat herbivore and pathogen preda-
tors and respond to changes in their environment
using highly complex inducible defense ⁄ response
mechanisms. These systems require the perception of
external stress conditions, transformation of these

Keywords
12-oxo-phytodienoic acid; cyclo-oxylipin-
galactolipids; environmental stress;
jasmonates; jasmonic acid;
mechanotransduction; oxylipins;
phytoprostanes; plant stress responses;
transcriptional regulation
Correspondence
S. Pollmann, Department of Plant
Physiology, Ruhr-University Bochum,
Universitaetsstrasse 150, D-44801 Bochum,
Germany
Fax: +49 234 321 4187
Tel: +49 234 322 4294
E-mail: stephan.pollmann@
ruhr-uni-bochum.de
(Received 7 November 2008, revised 23
March 2009, accepted 31 March 2009)
doi:10.1111/j.1742-4658.2009.07195.x
One of the most challenging questions in modern plant science is how
plants regulate their morphological and developmental adaptation in
response to changes in their biotic and abiotic environment. A comprehen-
sive elucidation of the underlying mechanisms will help shed light on the
extremely efficient strategies of plants in terms of survival and propagation.
In recent years, a number of environmental stress conditions have been
described as being mediated by signaling molecules of the oxylipin family.
In this context, jasmonic acid, its biosynthetic precursor, 12-oxo-phytodie-
noic acid (OPDA), and also reactive electrophilic species such as phyto-
prostanes play pivotal roles. Although our understanding of jasmonic
acid-dependent processes and jasmonic acid signal-transduction cascades

has made considerable progress in recent years, knowledge of the regula-
tion and mode of action of OPDA-dependent plant responses is just emerg-
ing. This minireview focuses on recent work concerned with the elucidation
of OPDA-specific processes in plants. In this context, aspects such as the
differential recruitment of OPDA, either by de novo biosynthesis or by
release from cyclo-oxylipin-galactolipids, and the conjugation of free
OPDA are discussed.
Abbreviations
cGL, cyclo-oxylipin-galactolipid; dnOPD, dinor-OPDA; GSH, glutathione; GST, glutathione S-transferase; JA, jasmonic acid; LOX,
lipoxygenase; Me-JA, methylester of JA; OPDA, 12-oxo-phytodienoic acid; RES, reactive electrophilic species; TGA, TGACG motif-binding
factor.
FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS 4693
stimuli into internal signals, and as a consequence, an
appropriate adjustment of gene expression via specific
signal-transduction cascades in answer to the altered
environment.
With regard to inducible response mechanisms of
plants and animals, compounds derived from the
metabolism of polyunsaturated fatty acids, collectively
termed oxylipins or octadecanoids, play a crucial role.
In mammals, oxylipins derive mainly from arachidonic
acid, a fourfold unsaturated C20 fatty acid, and have
pivotal functions in the inflammatory process, in gen-
eral reactions to infections and in allergic responses
[9]. By contrast, phytooxylipins derive mainly from
oxygenized C16 and C18 fatty acid precursors. Much
recent research has focused on the analysis of these
compounds. The biosynthesis of most plant oxylipins
is initiated by the action of lipoxygenases (LOX),
which are capable of introducing molecular oxygen at

either the C9 or C13 position of the C18 fatty acids
linoleic acid (18:2) and a-linolenic acid (18:3), respec-
tively [10,11]. Plants possess a number of different
LOX isoforms that can be subdivided into two groups:
type 1, containing all 9-LOX isoenzymes, which are
exclusively found outside the plastids; and type 2,
including all plastid-localized isoenzymes, such as the
13-LOXs [12,13]. Numerous biochemical studies pro-
vide evidence that the hydroperoxy reaction products
of LOX-assisted catalysis lead to a plethora of differ-
ent oxylipins, i.e. hydroxy, epoxy or divinylether fatty
acids, as well as volatile aldehydes and alcohols and
the well-established wound hormones jasmonic acid
(JA), 12-oxo-phytodienoic acid (OPDA), dinor-OPDA
(dnOPDA), traumatic acid and traumatin [4,14]. More-
over, a-dioxygenases catalyze the enantioselective 2-hy-
droperoxidation of long-chain fatty acids, giving rise
to additional oxylipins also involved in pathogen
defense [15,16].
In recent years, the main concern has been with the
13-LOX reaction, which initiates the synthesis of octa-
decanoids (Fig. 1), a compound class comprising jasm-
onates such as JA and several JA derivatives like
tuberonic acid, a 12-hydroxy analog of JA, and their
precursors, for example, the biological active OPDA.
The biosynthesis of JA, and activation of the interme-
diates by generation of the corresponding CoA esters
for b-oxidation, is deemed to be basically uncovered
with respect to the enzymes involved (for a review see
Ref. [7]).

In 1980, the senescence-promoting activity of the
methyl ester of JA (Me-JA) was first described for
leaves and shoots of Artemisia [17], followed by publi-
cations on the growth-inhibiting physiological role of
JA in higher plants [18,19]. Since then, lots of evidence
has been provided for the involvement of this phyto-
hormone in either mechanotransduction [20], the
response to osmotic stress [21], UV damage [22] and
water stress [23], or as a defense to wounding [24,25].
In particular, with regard to insect attacks [26,27] and
infections with necrotrophic fungi [28–30], respectively,
JA has been shown to play a key role. Furthermore,
essential developmental processes, such as seed matu-
ration [31,32], pollen development [33] and anther
dehiscence [34] are linked to variations in endogenous
JA levels.
Multiple gemone-wide transcript-profiling appro-
aches, utilizing differential experimental set-ups and
several corresponding Arabidopsis mutants have under-
scored the essential role of OPDA and JA [35]. Partic-
ularly, the fad3 ⁄ 2fad7⁄ 2fad8 (fatty acid desaturase)
triple mutant that is unable to produce the JA precur-
sor a-linolenic acid [33] and the coi1 (coronatine insen-
sitive) JA signal transduction mutant [36] have
revealed considerably decreased resistance towards the
herbivore Bradysia impatiens and the necrotrophic
fungus Alternaria brassicicola. Based on these results
and the JA deficiency of two null alleles in the OPR3
locus, namely opr3 [37] and dde1 (delayed dehiscence)
[38], it seemed surprising that these mutants exhibited

no altered resistance towards herbivore and pathogen
challenge. Recently, it has been reported that octadeca-
noid-dependent growth inhibition is seemingly medi-
ated by JA rather than OPDA. Consecutive treatment
of opr3 with OPDA resulted in unaffected leaf areas,
whereas in OPDA- or Me-JA-treated wild-type plants,
leaf areas were significantly reduced. By contrast, opr3
mutants infested with B. impatiens larvae were able to
survive the attack, whereas in the aos mutant the pop-
ulation was reduced to 4% [39]. This moved OPDA
center stage, and it appears to be a good candidate for
an independent signaling molecule specifically mediat-
ing resistance towards biotic foes.
Physiological processes mediated by
OPDA
Several physiological processes are known to be like-
wise stimulated by overlapping activities of OPDA and
JA. In addition, OPDA has been described in JA-inde-
pendent responses. Emphasizing its involvement in
mediating resistance to pathogens and pests, OPDA is
assumed to be the primary signal transducer in the
elicitation process [40], because OPDA strongly induces
alkaloid biosynthesis in Eschscholtzia californica cell
cultures. Furthermore, tendril coiling of Bryonia dioica
is more responsive to OPDA than JA. Although
exogenously administered JA is capable of promoting
OPDA triggered responses in plants C. Bo
¨
ttcher and S. Pollmann
4694 FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS

tendril coiling, the concentration needed to elicit the
reaction is one order of magnitude higher than with
methyl-OPDA and exhibits a slower kinetic. In addi-
tion, JA levels remain lower in mechanoreacting ten-
drils than in those of cis-(+)-OPDA and increase only
late during the coiling process. Comparable results
have been obtained in Phaseolus vulgaris
thigmomorphogenesis. In these studies, JA levels
remained below the detection limit after mechanical
stimulation. Thus, OPDA can be considered as an
endogenous signal transducer of Br. dioica and P. vul-
garis mechanotransduction (Fig. 2) [20,41–43]. In this
regard, OPDA and JA signaling is perhaps linked with
Ca
2+
signaling. It has recently been reported that
OPDA, as well as JA, induces transient Ca
2+
signals
in both the cytosol and the nucleus of a stimulated
transgenic tobacco cell culture. By contrast, JA–Ile
treatment had no detectable effect on the cellular
Ca
2+
content of the examined cell culture system [44].
Although OPDA and JA both contribute to an
Fig. 1. JA biosynthesis and OPDA metabolism in A. thaliana. 13-LOX, 13-lipoxygenase; ACX, acyl-CoA oxidase; AOC, allene oxid cyclase;
AOS, allene oxid synthase; CTS ⁄ PXA1 ⁄ PED3, ABC transporter for OPDA or OPDA–CoA import; COI1, F-box protein in JA signal transduc-
tion; GST, glutathione S-transferase; KAT,
L-3-ketoacyl-CoA thiolase; MFP, multifunctional protein; OPR, 12-oxo-phytodienoate reductase;

PLAI, plastidic acyl hydrolase.
C. Bo
¨
ttcher and S. Pollmann OPDA triggered responses in plants
FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS 4695
increase in the free cellular calcium level, it has been
shown that the response to OPDA was much quicker
(< 30 s) and the response amplitude higher (1 lm)
than in the response to JA treatment. This may be
indicative of distinct regulatory functions for the two
compounds. In terms of tendril coiling, the octadeca-
noid-dependent alteration in the Ca
2+
content may
induce ion fluxes, thereby directly affecting the turgor
pressure, or regulate the transcription of a specific sub-
set of genes (Fig. 2) [45,46]. Intriguingly, Medica-
go truncatula has recently been reported to respond
very sensitively to mechanostimulation with enhanced
JA levels and altered accumulation of AOC transcripts
[47]. Unfortunately, this study did not monitor other
genes involved in JA biosynthesis or cis -(+)-OPDA
levels during the reaction. It will be exciting to learn
whether mechanotransduction in Medicago is mediated
by JA rather than by OPDA.
Even though nyctinastic leaf movement most likely
differs mechanistically from mechanostimulated tendril
coiling, work conducted on the nyctinasty of several
plant species, such as Albizzia, has emphasized that JA
derivatives, i.e. potassium b-d-glucopyranosyl 12-hy-

droxyjasmonate, may at least contribute to this distinct
type of plant movement. In particular, nyctinastic leaf
closing is mediated by potassium b-d-glucopyranosyl
12-hydroxyjasmonate. In the case of nyctinasty, it is
suggested that the biochemical factors accounting for
leaf closing and opening directly affect K
+
channel
activity, thereby modulating turgor pressure in special-
ized flexor cells [48–50].
By analyzing a rice mutant with an impaired light
response, hebiba, it has recently been shown that
oxylipins are also involved in phototropic coleoptile
bending. Further experiments have emphasized an
auxin-antagonistic impact of JA in gravitopic reac-
tions. It is suggested that the JA gradient that is
formed in reciprocal orientation to the indole-3-acetic
acid gradient in coleoptiles inhibits growth in places
where it is already poorly promoted by indole-3-acetic
acid. Thereby, the velocity of the gravitopic movement
is seemingly accelerated [51–54]. The majority of the
effects described by the Nick group are most likely not
OPDA specific, but rather mediated by JA. However,
intriguingly, the authors described an OPDA gradient
which accompanies the JA gradient in the opposite
direction during gravitopism. This has been interpreted
as a putative second level of regulation in a late step
establishing the JA gradient. Extending this previous
interpretation, it is tempting to speculate that this may
also be indicative of OPDA-specific, JA-independent

regulatory effects. In the conducted experiments, an
independent signaling function of OPDA was not
taken into account and thus cannot be ruled out.
Extending the previous functions, OPDA and ⁄ or
16:3 fatty acid-derived dnOPDA are discussed as
inhibitors of programmed cell death in the conditional
Arabidopsis flu mutant [55]. Upon a dark-to-light shift,
flu mutants generate singlet oxygen (
1
O
2
) in their plast-
ids. This non-radical reactive oxygen species accounts
Fig. 2. Schematic representation of stress-induced processes med-
iated by reactive electrophilic species, such as phytoprostanes and
OPDA, and jasmonic acid as well as by its bioactive amino acid
conjugate, jasmonoyl–isoleucine
OPDA triggered responses in plants C. Bo
¨
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4696 FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS
for growth inhibitory effects and the development of
necrotic lesions [56]. Studies on flu and the flu ⁄ dde2-2
double mutant indicated that OPDA and ⁄ or dnOPDA
promote the inhibition of programmed cell death pro-
cesses induced by
1
O
2
, and the well-known cell death

induction by JA was suppressed. Unexpectedly, com-
parison of flu and the flu ⁄ dde2-2 double knockout,
impaired in OPDA, dnOPDA and JA production,
showed that the concurrent absence of those com-
pounds restored the wild-type sensitivity of flu to cell
death. Hence, OPDA and ⁄ or dnOPDA are seemingly
necessary and able to antagonize JA-promoted effects
on cell death (Fig. 2) (for more detail, refer to the
minireview by Reinbothe et al. [56a]).
A proposed mechanism of OPDA action
Despite being processed by the SCF
COI1
–JAZ–MYC
complex (for more detail, refer to the minireview by
Chini et al. [56b]), the major regulatory effect of
OPDA on the transcriptional machinery is determined
by its remarkable structural properties. Oxylipins with
a,b-unsaturated keto or epoxy functions can behave
like reactive electrophilic species (RES) towards cellu-
lar nucleophiles [57]. In this regard, a,b-unsaturated
keto groups can participate in nucleophilic Michael
additions in which carbanions are added to a,b-unsatu-
rated carbonyl compounds. This type of addition reac-
tion to proteins or to the tripeptide glutathione (GSH)
may cause changes in protein activity or in the cellular
redox state, which, in turn, can influence gene expres-
sion [58–60]. Such interactions have been described for
OPDA and a variety of related compounds [61–63].
Although the enzymatic production and physiological
impact of the octadecanoid-phytohormones OPDA

and JA is well-known (Fig. 1), the nonenzymatic gen-
eration of structurally related compounds and their
role in cellular stress responses is a very intriguing and
challenging matter of actual research. The latter com-
pounds comprise oxidized lipids and lipid fragments,
many of which are derived in vivo from a-linolenic acid
[64]. They range from very small compounds such as
malondialdehyde [65,66], to more complex families of
hydroxy fatty acids and phytoprostanes [67–69]. Cur-
rently, it is assumed that omega 3 fatty acids, in partic-
ular a-linolenic acid, serve in the protection of cells by
absorbing reactive oxygen species such that they are
oxidized in a free-radical-dependent manner [70]. This
trienoic fatty acid-mediated consumption of reactive
oxygen species results in the nonenzymatic generation
of oxidized polyunsaturated fatty acids and the subse-
quent production of many RES [71]. Recent work on
the impact of cyclopentenone-oxylipins, i.e. OPDA
and A
1
-phytoprostane (Fig. 2), on the proteome of
Arabidopsis leaves provides evidence for the induction
of both classical stress proteins and enzymes connected
to cellular redox and detoxification systems by those
compounds. Notably, a large portion of the identified
candidate proteins are located in plastids. Given the
fact that the two utilized oxylipins are generated in
these organelles, one may suggest that direct alteration
of enzyme activity ⁄ specificity or direct influencing of
the degradation of target proteins, triggered by enzy-

matically or nonenzymatically generated RES, may
take place in chloroplasts [72].
In mammals, the structural requirement for activity
of cyclopentenone prostaglandins, including effects on
gene expression, is already known to be determined by
their a,b-unsaturated carbonyl groups [73]. Hydroper-
oxy arachidonic acids, like leukotriene C
4
and 5-oxo-7-
glutathionyl-8,11,14-eicosatrienoic acid, are further
examples of such biologically active RES, which can
modulate the chemotaxis of neutrophiles and actin
polymerization, respectively [74]. Moreover, in animals,
covalent binding of RES is an appropriate tool with
which to regulate transcription factor activity, as
shown for nuclear factor kappa-light-chain-enhancer
of activated B cells (NF-jB), c-Jun or peroxisome pro-
liferator-activated receptor (PPARc) [75–77]. However,
experimental evidence for a covalent linkage between
RES and any specific protein in planta is yet to be pro-
vided. Nevertheless, both the examples from animals
and work on phytoprostanes allow for hypotheses in
which bioactive plant RES act as Michael acceptors,
thereby adding not only to GSH, but also directly to
enzymes and transcription factors.
OPDA: an independent regulator of
gene expression
Given the functional and structural differences between
OPDA and JA, it is exciting to presume that OPDA is
specifically able to orchestrate the expression of a sub-

set of genes, independent of those influenced by JA.
To identify such genes, and thus speculate on the phys-
iological impact of their gene products, several micro-
array approaches, using mainly the opr3 null mutant,
have been conducted. By analyzing a set of 150
defense-related genes, two general conclusions were
drawn. First, the COI1 signal transduction pathway
can be activated by both OPDA and JA. Second, com-
plete activation of the wound response needs the joint
action of OPDA and JA. Furthermore, not all COI1-
dependent genes were induced in wounded or OPDA-
treated opr3 plants, but both treatments activated the
transcription of several COI1-independent genes, which
C. Bo
¨
ttcher and S. Pollmann OPDA triggered responses in plants
FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS 4697
were not influenced by JA [78]. More recently, a
genome-wide microarray experiment identified a set of
> 150 genes that were induced by exogenously applied
OPDA, but not by JA or Me-JA [79]. The majority of
the identified genes encode for proteins involved in
stress responses, for example, heat shock proteins,
glutathione S-transferases (GSTs) or polypeptides
related to signal transduction, such as transcription
factors and kinases. In addition, genes encoding for
enzymes involved in the modulation of cellular indole-
3-acetic acid levels, such as ILR1, IAR3 and ILL5,
suggest a tight connection between stress responses
and auxin metabolism. Intriguingly, a further study

aimed at analyzing the molecular bases of phytopros-
tane activity, underlines that the regulation of gene
expression by those compounds is seemingly similar to
the regulation by OPDA and pathogens [63]. More-
over, a major part of these responses is shown to be
dependent on TGACG motif-binding factor (TGA)
transcription factors. Thus, a specific interaction of
RES, such as OPDA or nonenzymatically formed phy-
toprostanes, with TGA transcription factors seems
plausible and is reminiscent of the mentioned situation
in animals (vide ante).
However, unless direct covalent binding between
RES and any transcription factor has been proven
experimentally, the function of RES may also be more
indirect; acting through regulation of the cellular redox
state. Work conducted in the Pieterse lab underscores
the tight connection between plant defense responses
and the redox state of the cell [80,81]. For example, the
salicylic acid-induced antagonistic effect on JA-respon-
sive gene expression is facilitated by the modulation of
cellular GSH levels. The transcriptional regulator,
NPR1, undergoes conformational changes in response
to alterations in the cellular redox state [82]. Under sys-
temic acquired resistance conditions, NPR1 oligomers
are reduced to monomers, thereby allowing efficient
uptake into the nucleus where NPR1 can develop its
gene-regulatory functions. Because of the lack of
DNA-binding domains in NPR1, it is suggested that
the protein acts through protein–protein interaction
with transcription factors. Indeed, in multiple yeast

two-hybrid screens, an interaction between NPR1 and
a TGA subclass of basic leucine-zipper transcription
factors has been emphasized [83,84]. Taking into
account that oxylipins effectively induce TGA tran-
scription factor expression, it is attractive to speculate
that, as yet undetected, NPR1-like transcriptional regu-
lators are also involved in the redox-dependent trans-
mission of oxylipin signals.
Very recently, PHO1;H10, a member of the PHO1
gene family of Arabidopsis thaliana, has been described
as being transcriptionally regulated by OPDA, but not
by JA or coronatine, a bacterial polyketide metabolite
that mimics JA–Ile [85]. PHO1;H10 expression is
strongly induced by a variety of stresses, including
responses to wounding and dehydration. The corre-
sponding gene product is involved in loading inorganic
phosphate into the xylem in roots. Excitingly,
PHO1;H10 induction by wounding, as well as OPDA
treatment, made use of the COI1-dependent pathway,
which is noteworthy in that there is currently no exper-
imental evidence that OPDA can act via the SCF
COI1
–
JAZ–MYC-complex [86] (see minireview by Chini
et al. [56b]). However, these results suggest that dis-
tinct signaling cascades may emerge from the SCF
COI1
complex, depending on the presence of either OPDA
or JA.
Regulating the pool of free OPDA by

conjugation
Cell injury, for example, by pathogen attack is, in
most cases, accompanied by oxylipin bursts. These
drastic increases in cellular oxylipin content, governed
by enzymatic or nonenzymatic de novo production or
by the release of oxylipins from storage compounds
(vide infra) go hand in hand with the considerable cell
toxicity of these compounds. Rapid trapping and
sequestration of the partially toxic compounds could
prevent unintended cell damage. In this connection,
animals have evolved mechanisms for the rapid detoxi-
fication of oxylipins, e.g. by the addition of intracellu-
lar thioredoxin [87]. With respect to recently presented
data, it seems as though the conjugation and thereby
inactivation of free signaling molecules is a common
feature not only of animals, but also of plants. OPDA
and phytoprostanes are functionally inactivated by the
GST-catalyzed addition of GSH [63,72]. In underlying
studies, numerous GST genes were found to be upreg-
ulated by OPDA. One, a predicted chloroplastic GST
(GST6, At2g47730), is described as being able to cata-
lyze the conjugation of OPDA to GSH. This finding,
however, corresponds to work conducted in our labo-
ratory, in that we identified and characterized three
OPDA-induced cytoplasmic GSTs of the tau family
[88], all capable of adding OPDA, as well as trauma-
tin, to GSH in vitro (C. Bo
¨
ttcher et al., unpublished
data). Based on publicly available microarray data, the

expression of all of these GSTs responds strongly to
numerous stresses, e.g. wounding, jasmonate treat-
ment, nutrient starvation and fungal infections. Corre-
sponding OPDA–GSH conjugates have been reported
to accumulate in cryptogein-treated tobacco plants
[62], the fate of such membrane-impermeable GSH
OPDA triggered responses in plants C. Bo
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4698 FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS
adducts in plants remains unclear. Nevertheless, it may
be suggested that the addition of RES to GSH renders
them inactive or modulates their biological impact. In
addition to GST induction, the transcription of lipid
transfer proteins is strongly induced in answer to vari-
ous biotic and abiotic stresses. Such lipid transfer
Fig. 3. Structures of the currently identified cyclo-oxylipin-galactolipids from Arabidopsis thaliana.
C. Bo
¨
ttcher and S. Pollmann OPDA triggered responses in plants
FEBS Journal 276 (2009) 4693–4704 ª 2009 The Authors Journal compilation ª 2009 FEBS 4699
proteins have already been reported as a potential oxy-
lipin scavenger [89], although addition of OPDA or
bioactive phytoprostanes has yet to be explored.
In conclusion, the results point to a scenario in
which RES trigger both the regulation of a specific
cluster of genes and their own inactivation by a feed-
back loop, inducing the expression of detoxification
enzymes such as GSTs and lipid transfer proteins.
OPDA can be released from

cyclo-oxylipin-galactolipids
Cyclic oxylipins do not occur exclusively in their free
form. Rather, the major portion of these compounds,
at least in Arabidopsis and some near relatives, is
found covalently bound to galactolipids in the thyla-
koid membrane [90–95] (Fig. 3). The occurrence of
lipid-bound cyclic oxylipins is currently assumed to be
a special trait of only a very few members of the
Brassicaceae. Recently, we were able to detect lipid-
bound cyclic oxylipins in Arabidopsis arenosa, Arabid-
opsis halleri, Arabidopsis petraea, Arabidopsis thaliana,
Arabis pendula, Camelina microcarpa, Capsella rubella
and Neslia paniculata, all members of the Brassicaceae,
but not in 16 species taken from 11 other families [96].
The amount of these esterified oxylipins, collectively
termed cyclo-oxylipin-galactolipids (cGL), is not con-
stant but responds to external stimuli. Upon wound-
ing, for example, cGL levels in the thylakoids increase
[90,97]. Furthermore, senescence-promoting effects
have been described for arabidopside A (Fig. 3), a
monogalactosyldiacylglycerol species carrying OPDA
at sn1 and dnOPDA at sn2 [98]. Furthermore growth
inhibitory effects have been reported for monogalacto-
syldiacylglycerol-O, arabidopside A, B and F (Fig. 3)
[94]. Recent work also linked levels of lipid-bound
OPDA and dnOPDA with responses to pathogen
challenge, attributing antimicrobial activity to the
trioxylipin-containing monogalactosyldiacylglycerol de-
rivatives, arabidopside E and G (Fig. 3), which were
further shown to accumulate in response to dexameth-

asone-induced expression of an antivirulence protein
[93,95]. The biosynthesis of lipid-bound oxylipins is,
however, not yet fully understood, but several lines of
evidence emphasize a direct conversion of lipid-bound
polyunsaturated fatty acids into oxylipins [93]. How-
ever, the oxylipins linked to the galactosyl-moieties in
arabidopside E and G, at least, have to be covalently
linked to the molecules by transacylations. From this,
a general involvement of transacylation reactions,
introducing oxylipins into galactolipids, cannot be
excluded beyond reasonable doubt. Likewise, the par-
ticipation of enzymes of the jasmonate biosynthetic
pathway in the production of esterified cyclo-oxylipins
is yet to be discovered. Given that the majority of
OPDA and dnOPDA is found trapped in galactolipids,
there is speculation about the function of cGL as a
storage form for reactive oxylipins and that an alterna-
tive free fatty acid-independent pathway exists for the
synthesis of oxylipins. Consistent with the former
hypothesis, the lipolytic release of oxylipins from sev-
eral cGLs has already been reported [99]. Moreover,
there is an indication that cGLs may serve as sub-
strates for JA biosynthesis. Recently, a plastidic acyl
hydrolase has been identified that preferentially cata-
lyzes the hydrolyzation of cGLs (Fig. 1) and confers
resistance to Botrytis cinerea [100]. Intriguingly, the
plaI knockout mutant exhibited an expected enhanced
susceptibility to the necrotrophic fungus, without
affecting wound-induced JA accumulation. In fact, this
invites the presumption that lipid-bound and free pools

of oxylipins are differentially recruited depending on
the particular stimulus, which extends the current pic-
ture of inducible defense ⁄ response systems in planta.
Conclusions
In Arabidopsis, the majority of cyclic oxylipins are not
found the free form, but rather are covalently bound
to galactolipids. Under certain circumstances, the oxy-
lipins can be released from these lipids by lipases.
Regardless of their origin, in both plants and animals,
RES are engaged in the activation of a distinct set of
mostly defense- and stress-related genes. Transcrip-
tional regulation is possibly arranged by adding the
RES to certain transcription factors, thereby modulat-
ing their activity. It will be intriguing to discover
whether these strikingly similar regulation mechanisms
are the result of convergent evolution or whether they
constitute an ancient, conserved regulation mechanism
that is common to all beings.
Acknowledgements
The authors are grateful to Professor Dr Elmar W.
Weiler and Dr Florian Schaller for several fruitful dis-
cussions. Furthermore, the authors thank Professor
Dr Eckhard Hofmann for critical comments on the
manuscript. This work was funded by grants from the
Deutsche Forschungsgemeinschaft (DFG), Bonn
SFB480 ⁄ A10 and PO1214 ⁄ 3-2 for SP.
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