Oxylipin Signaling: A Distinct Role for the Jasmonic Acid Precursor cis-(+)-12-Oxo-Phytodienoic Acid (cis-OPDA).
ABSTRACT Oxylipins are lipid-derived compounds, many of which act as signals in the plant response to biotic and abiotic stress. They include the phytohormone jasmonic acid (JA) and related jasmonate metabolites cis-(+)-12-oxo-phytodienoic acid (cis-OPDA), methyl jasmonate, and jasmonoyl-L-isoleucine (JA-Ile). Besides the defense response, jasmonates are involved in plant growth and development and regulate a range of processes including glandular trichome development, reproduction, root growth, and senescence. cis-OPDA is known to possess a signaling role distinct from JA-Ile. The non-enzymatically derived phytoprostanes are structurally similar to cis-OPDA and induce a common set of genes that are not responsive to JA in Arabidopsis thaliana. A novel role for cis-OPDA in seed germination regulation has recently been uncovered based on evidence from double mutants and feeding experiments showing that cis-OPDA interacts with abscisic acid (ABA), inhibits seed germination, and increases ABA INSENSITIVE5 (ABI5) protein abundance. Large amounts of cis-OPDA are esterified to galactolipids in A. thaliana and the resulting compounds, known as Arabidopsides, are thought to act as a rapidly available source of cis-OPDA.
Article: Direct infusion mass spectrometry of oxylipin-containing Arabidopsis membrane lipids reveals varied patterns in different stress responses.[show abstract] [hide abstract]
ABSTRACT: Direct infusion electrospray ionization triple quadrupole precursor scanning for three oxidized fatty acyl anions revealed 86 mass spectral peaks representing polar membrane lipids in extracts from Arabidopsis (Arabidopsis thaliana) infected with Pseudomonas syringae pv tomato DC3000 expressing AvrRpt2 (PstAvr). Quadrupole time-of-flight and Fourier transform ion cyclotron resonance mass spectrometry provided evidence for the presence of membrane lipids containing one or more oxidized acyl chains. The membrane lipids included molecular species of phosphatidylcholine, phosphatidylethanolamine, phosphatidylglycerol, digalactosyldiacylglycerol, monogalactosyldiacylglycerol, and acylated monogalactosyldiacylglycerol. The oxidized chains were identified at the level of chemical formula and included C(18)H(27)O(3) (abbreviated 18:4-O, to indicate four double bond equivalents and one oxygen beyond the carbonyl group), C(18)H(29)O(3) (18:3-O), C(18)H(31)O(3) (18:2-O), C(18)H(29)O(4) (18:3-2O), C(18)H(31)O(4) (18:2-2O), and C(16)H(23)O(3) (16:4-O). Mass spectral signals from the polar oxidized lipid (ox-lipid) species were quantified in extracts of Arabidopsis leaves subjected to wounding, infection by PstAvr, infection by a virulent strain of P. syringae, and low temperature. Ox-lipids produced low amounts of mass spectral signal, 0.1% to 3.2% as much as obtained in typical direct infusion profiling of normal-chain membrane lipids of the same classes. Analysis of the oxidized membrane lipid species and normal-chain phosphatidic acids indicated that stress-induced ox-lipid composition differs from the basal ox-lipid composition. Additionally, different stresses result in the production of varied amounts, different timing, and different compositional patterns of stress-induced membrane lipids. These data form the basis for a working hypothesis that the stress-specific signatures of ox-lipids, like those of oxylipins, are indicative of their functions.Plant physiology 11/2011; 158(1):324-39. · 6.53 Impact Factor
[show abstract] [hide abstract]
ABSTRACT: Jasmonates are essential phytohormones for plant development and survival. However, the molecular details of their signalling pathway remain largely unknown. The identification more than a decade ago of COI1 as an F-box protein suggested the existence of a repressor of jasmonate responses that is targeted by the SCF(COI1) complex for proteasome degradation in response to jasmonate. Here we report the identification of JASMONATE-INSENSITIVE 3 (JAI3) and a family of related proteins named JAZ (jasmonate ZIM-domain), in Arabidopsis thaliana. Our results demonstrate that JAI3 and other JAZs are direct targets of the SCF(COI1) E3 ubiquitin ligase and jasmonate treatment induces their proteasome degradation. Moreover, JAI3 negatively regulates the key transcriptional activator of jasmonate responses, MYC2. The JAZ family therefore represents the molecular link between the two previously known steps in the jasmonate pathway. Furthermore, we demonstrate the existence of a regulatory feed-back loop involving MYC2 and JAZ proteins, which provides a mechanistic explanation for the pulsed response to jasmonate and the subsequent desensitization of the cell.Nature 09/2007; 448(7154):666-71. · 36.28 Impact Factor
Article: Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development.[show abstract] [hide abstract]
ABSTRACT: Jasmonates are ubiquitously occurring lipid-derived compounds with signal functions in plant responses to abiotic and biotic stresses, as well as in plant growth and development. Jasmonic acid and its various metabolites are members of the oxylipin family. Many of them alter gene expression positively or negatively in a regulatory network with synergistic and antagonistic effects in relation to other plant hormones such as salicylate, auxin, ethylene and abscisic acid. This review summarizes biosynthesis and signal transduction of jasmonates with emphasis on new findings in relation to enzymes, their crystal structure, new compounds detected in the oxylipin and jasmonate families, and newly found functions. Crystal structure of enzymes in jasmonate biosynthesis, increasing number of jasmonate metabolites and newly identified components of the jasmonate signal-transduction pathway, including specifically acting transcription factors, have led to new insights into jasmonate action, but its receptor(s) is/are still missing, in contrast to all other plant hormones.Annals of Botany 11/2007; 100(4):681-97. · 4.03 Impact Factor
MINI REVIEW ARTICLE
published: 08 March 2012
Oxylipin signaling: a distinct role for the jasmonic acid
precursor cis-( )-12-oxo-phytodienoic acid (cis-OPDA)
Anuja Dave and IanA. Graham*
Department of Biology, Centre for Novel Agricultural Products, University ofYork,York, UK
Kent D. Chapman, University of North
Clay Carter, University of Minnesota
Ian A. Graham, Department of
Biology, Centre for Novel Agricultural
Products, University ofYork,
Heslington,YorkYO10 5DD, UK.
biotic and abiotic stress.They include the phytohormone jasmonic acid (JA) and related jas-
monate metabolites cis-(+)-12-oxo-phytodienoic acid (cis-OPDA), methyl jasmonate, and
jasmonoyl-L-isoleucine (JA-Ile). Besides the defense response, jasmonates are involved
in plant growth and development and regulate a range of processes including glandular
trichome development, reproduction, root growth, and senescence. cis-OPDA is known to
possess a signaling role distinct from JA-Ile.The non-enzymatically derived phytoprostanes
are structurally similar to cis-OPDA and induce a common set of genes that are not
responsive to JA in Arabidopsis thaliana. A novel role for cis-OPDA in seed germination
regulation has recently been uncovered based on evidence from double mutants and feed-
ing experiments showing that cis-OPDA interacts with abscisic acid (ABA), inhibits seed
germination, and increases ABA INSENSITIVE5 (ABI5) protein abundance. Large amounts
of cis-OPDA are esterified to galactolipids in A. thaliana and the resulting compounds,
known as Arabidopsides, are thought to act as a rapidly available source of cis-OPDA.
dormancy, lipid signaling
SYNTHESIS OF OXYLIPINS
Oxylipins are a diverse group of lipid-derived signaling com-
fatty acids (PUFAs) such as linoleic acid (18:2), octadecatrienoic
acid (18:3n-3), and hexadecatrienoic acid (16:3n-3; Wasternack,
2007; Mosblech et al., 2009; Wasternack and Kombrink, 2010).
These fatty acids are released from plastidial membrane lipids
by lipases including DEFECTIVE IN ANTHER DEHISCENCE1
(DAD1) and DONGLE (DGL; Ishiguro et al., 2001; Hyun et al.,
2008; Ellinger et al., 2010) and are subsequently oxidized by
lipoxygenases (LOX) to form hydroperoxides (Vick and Zimmer-
man, 1983; Bell et al., 1995). As shown in Figure 1, the octade-
canoid pathway in Arabidopsis thaliana that gives rise to jasmonic
acid (JA), initiates in the plastid with the oxidation of octade-
catrienoic acid (18:3n-3) by 13-lipoxygenase (13-LOX) to form
oxo-phytodienoic acid (cis-OPDA). cis-OPDA then travels via the
cytosol to the peroxisome with uptake into this organelle being
mediated, at least in part, by the ATP binding cassette (ABC)
transporter protein,COMATOSE (CTS; Theodoulou et al.,2005).
Schaller et al.,2000;Stintzi and Browse,2000) and activated to the
CoA ester (Schneider et al., 2005; Koo et al., 2006; Kienow et al.,
2008) prior to undergoing three rounds of β-oxidation to form JA
(Cruz Castillo et al., 2004; Pinfield-Wells et al., 2005; Schilmiller
et al.,2007; Figure 1).
In addition to the action of AOS on plastidial fatty
acid hydroperoxides, they are also cleaved by hydroperoxide
lyases (HPLs) to produce C6-aldehydes such as (2E)-hexenal,
(3Z)-hexenal and their volatile derivatives termed collectively as
green leaf volatiles (GLVs; Chehab et al., 2008). HPL and AOS
compete for hydroperoxide substrates and it has been shown that
JA and cis-OPDA accumulation are reduced upon HPL overex-
pression (Chehab et al., 2008). These authors also showed that JA
is involved in the direct defense response while the GLV hexenyl
acetate mediates the indirect defense response. Moreover, HPL
activity is not indispensable for normal growth, development, or
defense since it has been shown that functional HPL activity is
absent in the A. thaliana ecotype Col-0 (Duan et al.,2005).
from plastidial hydroperoxides originates through the activity of
divinyl ether synthases that produce divinyl ether oxylipins which
have also been shown to play a role in plant defense in a number
of systems (Weber et al., 1999; Itoh and Howe, 2001). However,
Eschen-Lippold et al. (2010) have more recently reported that
oxylipins resulting from the action of divinyl ether synthase are
not required for the R-gene-mediated resistance in potato.
mechanistic basis of how jasmonate signaling operates (Browse,
2009), much less is understood about the biological functions
of the other oxylipins. This mini-review will summarize recent
developments in our understanding of the role played by the JA
precursor cis-OPDA and the structurally similar phytoprostanes,
which are synthesized by a non-enzymatic route.
A DISTINCT ROLE FOR cis-OPDA IN PLANT SIGNALING
referred to as jasmonates which in addition to the involvement in
March 2012 | Volume 3 | Article 42 | 1
Dave and Grahamcis-OPDA-mediated responses in plants
FIGURE 1 | Oxylipin biosynthesis pathway and signal transduction in
Arabidopsis thaliana. JA biosynthesis initiates in the plastid with release
of octadecatrienoic acid or hexadecatrienoic acid from membrane lipids
by lipases such as DAD1 and DGL. cis-OPDA and dn-OPDA are formed
following sequential steps catalyzed by 13-LOX, 13-AOS, and AOC.
cis-OPDA is transported to the peroxisome via the CTS transporter, where
after reduction by OPR3, OPC-8:0 is formed.This is activated to its CoA
ester by OPCL1, which then undergoes three rounds of β-oxidation
catalyzed by ACX, KAT, and MFP to give (+)-7-iso-JA. JAR1 catalyzes
formation of the amino acid conjugate JA-Ile from JA in the cytosol, which
is the active form of the hormone involved in JA signaling. JAZ proteins
repress expression of JA-responsive genes. In response to JA-Ile, the JAZ
proteins are targeted by SCFCOI1for degradation, thus leading to
JA-dependent gene expression and ultimately the regulation of various
physiological processes.The model proposes formation of the COI1-JAZ
complex in the nucleus. cis-OPDA’s regulation of gene expression can be
COI1-dependent or COI1 independent, although cis-OPDA has not been
shown to promote binding of COI1 and JAZ. Enzyme names are shown in
red. Dashed arrows indicate route to JA biosynthesis via dn-OPDA, where
these steps are yet to be proven experimentally. DAD1, DEFECTIVE IN
ANTHER DEHISCENCE1; DGL, DONGLE; 13-LOX, 13-lipoxygenase;
13-AOS, 13-allene oxide synthase; AOC, allene oxide cyclase; OPR3,
12-oxophytodienoate reductase3; OPCL1, OPC-8:CoA ligase1; CTS,
COMATOSE; ACX, acyl CoA oxidase; KAT, 3-l-ketoacyl-CoA-thiolase; MFP ,
multifunctional protein; JA, jasmonic acid; cis-OPDA,
cis-(+)-12-oxo-phytodienoic acid; dn-OPDA, dinor-oxo-phytodienoic acid;
JA-Ile, jasmonoyl-L-isoleucine; COI1, CORONATINE-INSENSITIVE1; JAZ,
jasmonate ZIM domain.
opment, and reproduction (Staswick et al., 1992; Feys et al., 1994;
Xie et al.,1998;Li et al.,2004;Balbi and Devoto,2008;Wasternack
and Kombrink,2010). By far the best characterized jasmonate sig-
naling mechanism is the transcriptional control of JA-responsive
encoded by JAR1 (Staswick and Tiryaki, 2004). One such conju-
gate,jasmonoyl-l-isoleucine (JA-Ile),rather than JA or cis-OPDA
plays the crucial role in transcriptional control via the jasmonate
ZIM domain (JAZ) repressor proteins (Chini et al., 2007; Thines
et al., 2007; Yan et al., 2007). JA-Ile promotes binding of the
F-box protein CORONATINE-INSENSITIVE1 (COI1) and JAZ
proteins resulting in the degradation of JAZ proteins by the 26S-
proteasome (Chini et al.,2007; Thines et al.,2007). A cytochrome
P450 encoded by CYP94B3 metabolizes JA-Ile to 12OH-JA-Ile
(Kitaoka et al., 2011; Koo et al., 2011; Heitz et al., 2012) which
is less effective than JA-Ile at promoting COI1-JAZ binding (Koo
et al., 2011), thus suggesting a role for this enzyme in the inacti-
vation of JA-Ile and attenuation of the jasmonate response (Koo
oxidative catabolism of JA-Ile,by converting it to 12COOH-JA-Ile
(Heitz et al., 2012).
Frontiers in Plant Science | Plant Physiology
March 2012 | Volume 3 | Article 42 | 2
Dave and Grahamcis-OPDA-mediated responses in plants
That signals other than JA-Ile are involved in oxylipin sig-
naling was suggested through the use of a mutant defective in
12-oxophytodienoate reductase3 (opr3), which is compromised in
the conversion of cis-OPDA to JA (Stintzi et al., 2001), yet it still
undergoes a defense response. Treating the opr3 mutant with cis-
OPDA revealed two separate downstream signaling pathways,one
dependent on COI1 and the other independent (Stintzi et al.,
2001). In the case of the A. thaliana defense response, JA, and
cis-OPDA appear to act in concert to fine tune the expression of
defense genes. However, in other cases the roles of JA and cis-
OPDA are distinct as demonstrated for example by the fact that
the male sterility phenotype of opr3 is rescued by JA but not cis-
OPDA (Stintzi and Browse, 2000). A recent publication reports
that opr3 is not a complete null mutant and concludes that the
defense response displayed by opr3 plants against a necrotrophic
fungus is likely due to JA and not cis-OPDA (Chehab et al.,2011).
Nevertheless, data from other publications do strongly suggest
that cis-OPDA is capable of distinct signaling (Weiler et al., 1993;
Blechert et al., 1999; Taki et al., 2005; Mueller et al., 2008; Ribot
et al., 2011). In the tendril coiling response of Bryonia dioica,
(Weiler et al., 1993; Blechert et al., 1999), the cis-OPDA-methyl
ester acts faster and requires a much lower concentration than
MeJA to elicit the response (Weiler et al., 1993). Taki et al. (2005)
showed that in addition to a set of genes whose expression is
induced by both JA and cis-OPDA, a subset of 157 of the 21,500
genes analyzed were found to be induced by cis-OPDA but not JA
or MeJA. Half of these cis-OPDA-specific response genes (ORGs)
were induced by wounding but their regulation was found to be
COI1 independent (Taki et al., 2005). Similarly, the PHO1;H10
gene in A. thaliana which is induced by various abiotic and biotic
stresses,responds to cis-OPDA application,but not JA and in this
While a number of signaling roles have been demonstrated for
cis-OPDA, the 16 carbon homolog dinor-oxo-phytodienoic acid
(dn-OPDA) which is synthesized from hexadecatrienoic acid via
a parallel hexadecanoid pathway (Weber et al., 1997; Acosta and
Farmer, 2010; Figure 1) has not as yet had any signaling function
cis-OPDA AS A NEW PLAYER IN SEED GERMINATION
We recently uncovered an additional role for cis-OPDA when
investigating the mechanism by which the ABC transporter
(Dave et al., 2011). The severely impaired germination pheno-
type of cts mutants is also observed in other mutants that are
compromised in peroxisomal β-oxidation, including kat2, acx1
acx2,and csy2 csy3 (Pinfield-Wells et al.,2005;Pracharoenwattana
et al., 2005; Footitt et al., 2006). Since JA synthesis is dependent
on the uptake of cis-OPDA into peroxisomes (Acosta and Farmer,
et al., 2004; Pinfield-Wells et al., 2005; Schilmiller et al., 2007)
we analyzed oxylipin levels in mutant seed to establish if there is
elevated levels of not only cis-OPDA but also JA and JA-Ile in the
cts and β-oxidation mutants compared to wild type. Previously,
we had quantified JA in wounded and unwounded leaves of the
cts mutant and found that although levels were reduced relative to
transporter is involved in peroxisome import, another transport
mechanism such as ion trapping may also operate (Theodoulou
et al.,2005).Analysis of developing seeds revealed that the oxylip-
ins accumulate during late seed maturation and double mutant
analysis revealed that cis-OPDA rather than JA or JA-Ile con-
tributes to the block in seed germination in A. thaliana (Dave
et al., 2011). Seed treatments revealed that cis-OPDA is much
more effective than JA at inhibiting wild type seed germination
germination antagonist, abscisic acid (ABA). The ABA INSENSI-
TIVE5 (ABI5) locus rescues the impaired germination phenotype
of ped3, an allele of cts (Kanai et al., 2010). Consistent with these
observations we found that cis-OPDA treatment increased ABI5
protein abundance in a manner that parallels the inhibitory effect
of cis-OPDA and cis-OPDA+ABA on seed germination. Previ-
ous results from our laboratory showed that ABI5 is expressed
specifically in the micropylar region of the single cell endosperm
layer through which the radicle has to emerge for germination to
proceed in A. thaliana (Penfield et al., 2006). The work of Kanai
et al. (2010) highlights the correlation between ABI5 transcripts
which reduce cell wall pectin degradation. Thus we can propose
a mechanism by which cis-OPDA together with ABA controls
protein levels of the ABI5 transcription factor and this in turn
regulates abundance of the PGIPs at the micropylar region of the
can break through the endosperm barrier leading to seed germi-
and what regulates cis-OPDA levels in developing wild type seeds.
CHEMICALLY REACTIVE CYCLOPENTENONE OXYLIPINS
Various stress stimuli, such as wounding and pathogen infection,
result in the activation of biosynthetic enzymes responsible for
accumulation of cis-OPDA and JA (Wasternack, 2007; Mosblech
et al.,2009). In addition to this enzymatic route,a non-enzymatic
route for oxylipin formation triggered by reactive oxygen species
(ROS) and free radicals also operates to produce an array of oxi-
dized lipids including phytoprostanes and hydroxy fatty acids
(Imbusch and Mueller, 2000; Mosblech et al., 2009). Phyto-
prostanes and cis-OPDA are structurally similar cyclopentenones
that contain a chemically reactive α,β-unsaturated carbonyl struc-
This has led to their classification as reactive electrophilic species
(RES) and it has been proposed that this RES subgroup of oxylip-
ins induce a common cluster of defense genes (Almeras et al.,
2003; Weber et al., 2004; Farmer and Davoine, 2007) but other
reports indicate that chemical reactivity and gene expression do
expression of genes associated with cellular detoxification, stress
responses, and secondary metabolism with 60 and 30% of the
dependent on the basic leucine zipper containing TGA class of
March 2012 | Volume 3 | Article 42 | 3
Dave and Grahamcis-OPDA-mediated responses in plants
transcription factors in A. thaliana (Mueller et al., 2008; Mos-
blech et al., 2009). JA, which is a cyclopentanone and much less
chemically reactive, does not induce this same group of genes.
Furthermore, there was no significant overlap observed between
the cyclopentenone oxylipin regulated genes described by Mueller
that have high levels of both JA and cis-OPDA (Dave et al.,2011).
Much remains to be done to establish the details of how these var-
variety of observed responses.
Galactolipids containing esterified cis-OPDA and dn-OPDA have
been found in A. thaliana and some other related species of the
genus Arabidopsis,and these complex lipids are referred to asAra-
bidopsides (Stelmach et al., 2001; Hisamatsu et al., 2003, 2005;
Andersson et al., 2006; Buseman et al., 2006; Böttcher and Weiler,
2007; Kourtchenko et al., 2007). A number of Arabidopsides have
been identified and named according to the position at which
cis-OPDA is found esterified to the monogalactosyl diacylglyc-
erol (MGDG) or digalactosyl diacylglycerol (DGDG) instead of
the fatty acyl moiety. For example Arabidopside A and Arabidop-
side C are MGDG and DGDG derivatives respectively containing
cis-OPDA esterified at positions sn-1 and dn-OPDA at sn-2 posi-
accumulate following wounding of leaves (Buseman et al., 2006;
et al. (2007) also demonstrated that Arabidopsides accumulate
during the hypersensitive response to bacterial pathogens. More-
over, they show that in both the wounding and hypersensitive
responses,Arabidopside formation is dependent on intact JA sig-
naling as levels of Arabidopsides are severely reduced in the coi1
RecentlyVu et al. (2012) have reported that the basal composition
of these complex oxidized lipids is different from those that are
formed following various stress treatments. Based on the rapid
et al. (2006) hypothesize that galactolipids are the substrates of
cis-OPDA/dn-OPDA synthesizing enzymes rather than free fatty
acids being converted to cis-OPDA/dn-OPDA and then esteri-
fied to the galactolipids. This suggests that enzymes involved in
cis-OPDA/dn-OPDA biosynthesis can act not only on free fatty
acids, but also on lipid-bound fatty acids.
A number of functions have been described forArabidopsides.
It has been hypothesized that they may function as a storage pool
production of JA (Kourtchenko et al., 2007; Ibrahim et al., 2011).
Stelmach et al. (2001) have shown that cis-OPDA at the sn-1 posi-
Rhizopus arrhizus. Schäfer et al. (2011) report that lipase activ-
ity of grasshopper oral secretions are instrumental in release of
cis-OPDA from Arabidopsides and hence play a role in defense
response to herbivory. Some of theArabidopsides display growth-
inhibiting effects on bacterial and fungal pathogens (Andersson
et al., 2006; Kourtchenko et al., 2007). A senescence promoting
ited range of species from the genus Arabidopsis it would appear
that either these compounds are present in miniscule amounts
in other plants or are completely absent (Mosblech et al., 2009).
Based on current evidence it appears that this intriguing class of
complex lipids do not have a generic role across species but have
arisen by adaptation in just a few (Böttcher and Weiler, 2007).
A wide array of oxylipins are generated in response to various
environmental stimuli and developmental cues. In some cases,
such as plant defense, multiple oxylipins are involved while in
others, such as reproductive development and seed germination,
JA, and cis-OPDA respectively play the main role. Fine-tuning of
opmental stage of the tissue is obviously important in eliciting a
of different oxylipins. Our recent demonstration of a specific role
for cis-OPDA in regulating germination potential in developing
seeds provides an opportunity to further dissect the underlying
mechanism. Establishing the role played by oxylipin signaling
in the environmental and genetic control of seed dormancy and
germination is an important challenge for the future.
We acknowledge financial support from the UK Biotechnology
and Biological Sciences Research Council (BBSRC) grant number
BB/J00216X/1 for work on cis-OPDA.
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Conflict of Interest Statement: The
authors declare that the research was
conducted in the absence of any com-
mercial or financial relationships that
could be construed as a potential con-
flict of interest.
Received: 20 December 2011; accepted:
19 February 2012; published online: 08
Citation: Dave A and Graham IA
(2012) Oxylipin signaling: a distinct
role for the jasmonic acid precursor
cis-(+)-12-oxo-phytodienoic acid (cis-
OPDA). Front. Plant Sci. 3:42. doi:
This article was submitted to Frontiers in
Plant Physiology, a specialty of Frontiers
in Plant Science.
Copyright © 2012 Dave and Graham.
This is an open-access article distributed
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