Phytochemistry 71 (2010) 1445–1449

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Phytochemistry
journal homepage: www.elsevier.com/locate/phytochem

Molecules of Interest

Plant defense elicitors: Analogues of jasmonoyl–isoleucine conjugate

Jiří Svoboda, Wilhelm Boland *
Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, 07745 Jena, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Our understanding of plant defensive mechanisms against herbivore and pathogen attack has signifi-
Received 6 January 2010 cantly increased over the past decade. The complex cascade of defensive events is initiated and controlled
Received in revised form 28 April 2010 by a network of interacting plant hormones. Especially, the conjugate of jasmonate and isoleucine is a
major regulator which controls gene expression and production of secondary metabolites after (a)biotic
challenges. This review offers a survey of both natural and synthetic mimetics of the natural hormone
Keywords: which can be used for a selective manipulation and the study of the plant’s secondary metabolism.
Plant defense
Ó 2010 Elsevier Ltd. All rights reserved.
Secondary metabolism
Jasmonic acid
Jasmonoyl–isoleucine
Coronalon

1. Introduction JAZ protein family in the achievement of specific palette of re-

Plants have developed highly sophisticated strategies to cope
with the challenges of microbial and herbivore attack (Chessin
and Zipf, 1990; Harborne, 1993; Hutcheson, 1998; Kessler and
Baldwin, 2001; Gatehouse, 2002; Schulze-Lefert and Panstruga,
2003; Innes, 2004; Howe and Jander, 2008; Koo and Howe,
2009). Their direct defence is based, e.g., on the use of thorns,
waxes or secondary metabolites (Wittstock and Gershenzon,
2002), and their indirect defences use, among others, the release
of volatile organic compounds to attract predators of their herbi-
vores (De Moraes et al., 1998; Paré and Tumlinson, 1999; Arimura
et al., 2000; Dicke and van Loon, 2000). The broad spectrum of
defensive responses (e.g., qualitative and quantitative composition
of volatile blends and other metabolite families) is finely tuned to
fight the particular invader. They are orchestrated by a suite of
phytohormones among which jasmonic acid (3) and its conjugate
with isoleucine (6) play a major role.
Apart from the jasmonate-based hormone, the defensive re-
sponse can be triggered by natural (Weiler et al., 1994), and syn-
thetic (Lauchli and Boland, 2003, and references therein)
structural and functional analogues. The aim of this review is to of-
fer a survey of both natural and synthetic analogues of the natural
hormone, along with a discussion of their biological activity which
is often overlapping but not quite identical to that of the natural
jasmonate. This indicates how important the difference in the rec-
ognition of the hormone analogue structure by the members of the
* Corresponding author.
E-mail addresses: jsvoboda@ice.mpg.de (J. Svoboda), boland@ice.mpg.de (W.
Boland).
sponses could be.
2. The signalling cascade
Octadecanoids are central actors in the defensive responses
when the plant faces insect, mite or fungal attackers (Weber,
2002; Santner et al., 2009). The ability to induce the defenses only
when necessary conserves the plant energy in the absence of po-
tential aggressors (Baldwin et al., 2000). The cascade, initiated by
the mechanical wounding of cellular membranes (Hamann et al.,
2009), e.g., by the caterpillar mandibles, begins by the conversion
of linolenic acid (1) released from the membrane (Fig. 1; Weiler,
1997; Walling, 2000; Dicke et al., 2003; Arimura et al., 2005) into
a cyclopentenone structure, such as 12-oxophytodienoic acid
(12-OPDA, 2; Schaller and Stintzi, 2009). This intermediate is ex-
ported from the plastid into the cytosol, reduced and its chain is
shortened by b-oxidation to yield jasmonic acid 3. Alternatively,
reactive oxygen species resulting from an oxidative burst can con-
vert linolenic acid into, e.g., phytoprostanes (such as phytopros-
tane B1 type II, 5) which are considered stable final products of
the free-radical-catalysed cascade (Imbusch and Mueller,
2000a,b; Thoma et al., 2003; Mueller, 2004; Schulze et al., 2006;
Schmidt and Boland, 2007; Schaller and Stintzi, 2009). Both 12-
OPDA and the oxylipins may interact with their molecular target
and cross-talk to other signalling pathways (Pieterse et al., 2001,
2009; Kunkel and Brooks, 2002; Rojo et al., 2003).
After conjugation of jasmonic acid 3 to L-isoleucine, the now-ac-
tive hormone 6 binds to the SCFCOI1 protein (COI1 is an F-box com-
ponent of SKIP-CULLIN-F-box complex) and so assists in its binding
to a jasmonate ZIM domain (JAZ) protein (Thines et al., 2007; Yan

0031-9422/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.phytochem.2010.04.027
1446 J. Svoboda, W. Boland / Phytochemistry 71 (2010) 1445–1449

O
The biological effect of jasmonic acid is also mimicked by coron-
atine (7, Fig. 1), a bacterial phytotoxin originally described in Pseu-
COOH domonas coronafaciens by Ichihara et al. (1977, 1979) which
COOH
facilitates proliferation of the bacterium by weakening the plant
12-oxophytodienoic acid 2
linolenic acid 1 host (Bender et al., 1987, and references therein; Uppalapati
et al., 2005). Coronatine 7 is composed of coronafacic acid pro-
reactive oxygen species duced by the polyketide pathway, and coronamic acid, a rare ami-
no acid containing a cyclopropane ring and produced from
O O O isoleucine (Ichihara et al., 1979; Mitchell et al., 1994). Its structure
7
closely resembles that of the natural hormone 6; however, the ste-
COOH COOH
COOH
3
reochemistry at the cyclopentanone ring is fixed and no epimerisa-
OH (3R,7S)-jasmonic acid (3R,7R)-jasmonic acid tion is possible. Additionally, the a-branching makes coronamic
phytoprostane B1 type II (+)-epi-jasmonic acid (–)-jasmonic acid acid resistant to amide bond cleavage. This makes the compound
5 3 4
phytotoxic as the plant cannot attenuate the signal of the mimic
by a transformation to the less active form, and overreacts (Lauchli
O O
and Boland, 2003).
The biological activities triggered by coronatine include tendril
structural analogues
coiling (Weiler et al., 1994), biosynthesis of terpenoids and other
volatiles (Boland et al., 1995a,b; Baldwin et al., 2002; Schüler
HN O HN O et al., 2004), expression of specific genes (Wasternack et al.,
HO
HOOC 1998), accumulation of alkaloids (Haider et al., 2000) and isoflava-
O noid–phytoalexins (Fliegmann et al., 2003). The phytotoxin
jasmonoyl–isoleucine conjugate coronatine 7 matches the activity profile of both jasmonic acid and 12-OPDA
6 (Mithöfer et al., 2005), and to some extent shares common struc-
SCFCOI1
degradation tural features with phytoprostans (Mueller, 2004). Despite of sub-
stantial research efforts, no current synthetic route offers a rapid
6
JAZ SCFCOI1 approach to larger quantities of the phytotoxin or to structural
MYC2 JAZ
analogues (Nara et al., 1997; Ichihara and Toshima, 1999). Syn-
MYC2
thetic analogues of this important elicitor have therefore been pre-
early response genes early response genes pared by simplification and modification of the parent structure
(vide infra).
Fig. 1. Natural elicitors of plant defensive responses, the structure of coronatine,
the natural mimic, and their mode of action. 3.2. Synthetic elicitors

Systematic structural modification of jasmonic acid provided

et al., 2009). The complex is then degraded by the ubiquitin ligase-
dependent 26S proteasome pathway (Fonseca et al., 2009, and ref-
erences therein; Chung et al., 2009). This interrupts the repression
of jasmonate-responsive genes (by the release of MYC2 and possi-
bly other transcription factors) and eventually leads to the local
and systemic defensive response, such as the emission of preda-
tor-attractive volatiles (Boland et al., 1995a,b; Dicke et al., 1999;
Kessler and Baldwin, 2001; Weiler, 2003a,b).
The defenses triggered by the elicitor depend on the elicitor
type even within the octadecanoid family, and there are significant
differences between the responses induced by the action of 12-
OPDA and jasmonic acid (Blechert et al., 1999; Koch et al., 1999;
Stintzi et al., 2001; Fliegmann et al., 2003) and between the biolog-
ical models used (Lauchli and Boland, 2003, and references therein;
Pauwels et al., 2009).
3. Elicitors
3.1. Natural elicitors
Although often generically called ‘jasmonate’, the active form of
the plant hormone is in fact the conjugate of the (3R, 7S)-stereoiso-
mer of jasmonic acid with L-isoleucine (6; Wang et al., 2008; Stas-
wick, 2008; Fonseca et al., 2009). To a minor extent, it also occurs
as conjugate with L-leucine and L-valine. Nevertheless, the required
stereoisomer 3, produced by the b-oxidation of 12-OPDA 2 (Fig. 1),
rapidly epimerises to the less active (3R, 7R)-stereoisomer 4 which
may serve as a mechanism for signal attenuation to avoid an exag-
gerated response (Acree et al., 1985; Beale and Ward, 1998; Lauchli
and Boland, 2003).
information about the fundamental structural features required
for the biological activity (Kiyota et al., 1996, 1997; Miersch
et al., 1999). Generally, structural changes in the pentenyl side
chain (compounds 8–9, Fig. 2) led to loss of activity (Miersch
et al., 1999; Kiyota et al., 2001), with the notable exception of a tri-
fluorinated analogue 8a (Kiyota et al., 1996). Flattening of the
three-dimensional architecture of jasmonate by the introduction
of a double bond (compound 10) had the same effect (Koch et al.,
1997). On the other hand, certain modifications on the cyclopenta-
none ring were tolerated (compounds 12–13), as well as substitu-
tion the a-position to the carboxylic acid group (11). Conjugation
of jasmonic acid to an (R)-amino acid or an aromatic amino acid
compromised its activity. Derivatives with modified ester group
(14), prepared as coronatine analogues to induce the production
of taxanes in cell cultures (Yukimune and Hara, 1996; Qian et al.,
2004, 2005), were slightly (8–67%) more active than parent methyl
jasmonate. Different biological models were less structurally strict
(Haider et al., 2000).
Considering the synthetically poorly accessible structure of the
phytotoxin coronatin, efforts have led to the development of par-
tially simplified, yet biologically active structures containing, for
example, L-isoleucine instead of the rare coronamic acid and an
analogue without the ethyl substituent on the bicyclic skeleton
(Haider et al., 2000), along with dihydrocoronatine (Suzuki et al.,
2004) and analogues based on the reduction of the ring-located
carbonyl group and conversion to esters (Uppalapati et al., 2005).
3.3. Indanone–amino acid conjugates
Further structural simplification of coronatine led to the devel-
opment of highly active indanone–isoleucine conjugates (e.g.,
 J. Svoboda, W. Boland / Phytochemistry 71 (2010) 1445–1449 1447

R = CH2CF3 a R R
O R
CHFCH3 b R = =O a R= H a
CH=CH2 c H b Cl b
C(CH3)=CH2 d F c
COOMe CH(OH)CH3 e OH d
CH3 f HN O SAc e HN O
CHBr2 g =N–OH f
8 O O
(E,Z)-I h
CH(CH3)2 i O O
15 16
O O O
R1 R
COOMe COOR COOMe R2

(CH2)nCOOMe 17 18
9 10 11
n = 0, 2, 3 R1 = C(O)CH3, R2 = H a R = –OH a
HN O HN O =O b
R1 = R2 = OCH3 b
O O
X = CF2 a
X AcO O O
CH2 b
O R
COOMe c COOMe H O O
O N N
N
12 13 S n

HN O HN O HN O HN O
R= D-glucose a F F O O O O
OH d
O F O O O O
OH b
F F 19 20 21 22
c n = 1, 2
R = –OH a
COOR O F e =O b
O
14 F F
Fig. 3. Aromatic elicitor conjugates.

Fig. 2. Examples of modified jasmonates. For complete list of tested structures, see
Kiyota et al. (1996, 1997), Miersch et al. (1999), Haider et al. (2000).
for which the name ‘coronalon’ was coined (Schüler et al., 2004).
Interestingly, the profile of volatiles induced by coronalon 24 and
15a–f, Fig. 3; Hopke et al., 1994; Boland et al., 1995a,b; Lauchli and the parent unsubstituted indanone–isoleucine conjugate 15a was
Boland, 2003). Short, modular and straightforward approach to the significantly different (Schüler et al., 2001). Alkoxylated derivatives
synthesis of the indanone–amino acid conjugates 15–24 brought (23d–f, h–i) and methyl derivative (23a) were little or not active,
the possibility to systematically modify particular fragments of with the exception of 6-allyloxy derivative (23g) which combined
the structure and obtain information on the structure–activity high activity and improved water solubility. The vinyl (23b) and al-
relationship. lyl derivatives (23c) were active, but did not exceed the activity of
The amino acid residue is an essential constituent as the biolog- coronalon. Furyl (23n) and thiofuryl derivatives (23o) are presum-
ical activity can only be attributed to the intact conjugates, not to ably too large and do not bind efficiently to the receptors (Yan
the hydrolysed building blocks (i.e., free amino acid and free inda- et al., 2009); additionally, they suffered from poor solubility. The
none-4-carboxylic acid). Only isoleucine, leucine and valine were
tolerated for conjugation (Krumm et al., 1995; Krumm and Boland,
O
1996; Krumm, 1998). Both allyl and methyl esters of the amino R R =Me, CH=CH2, allyl a,b,c
acid could be used – the ester group is cleaved in vivo by the action OMe, OEt, OPr, O–allyl, O(CH2)4CH3 d,e,f,g,h
of esterases (Fonseca et al., 2009); however, the latter was pre- O(CH2CH2O)2CH3 i
OSO2CF3 j
ferred for synthetic reasons. Br, I, N3 k,l,m
There is little structural flexibility in the fused bicyclic system HN O
(Fig. 3; Krumm et al., 1995; Winscheidt, 1997; Krumm, 1998): O S
O
monocyclic (17) and tricyclic systems (18) are not tolerated at
all, and no heteroatom substitution is allowed (19–20). Expansion O
23 n o
of the five-membered ring to six-membered (21–22) decreased the
biological activity. The presence of the double bond is not advanta- O
geous (16a). Substitution of the cyclopentanone ring (15b–f) does
not compromise the biological activity, but it is lower than that of
the parent structure 15a. An exception are the 1-acetylthio (15e)
and the 1-chloro-1-ene (16b) analogues which exhibit a different
HN O
activity and induce the emission of otherwise not observed volatile
O
compounds.
Biological activity of the molecule can be increased by a substi- O
tution at the position 6 of the aromatic ring (23–24), thus resem-
coronalon 24
bling the structure of coronatine more closely (Fig. 4; for
syntheses, see Schüler et al. (2001), Lauchli et al. (2002), Lauchli Fig. 4. Aromatic-ring-substituted analogues of the indanone–isoleucine conjugate
and Boland (2003)). The most active was the ethyl analogue 24 and the structure of coronalon.
1448 J. Svoboda, W. Boland / Phytochemistry 71 (2010) 1445–1449
6-azido derivative (23m) was designed as a photoaffinity label to
search for the cellular receptors of jasmonates, and was success-
fully used with myoglobin as a test substance (Schüler et al.,
1999). The 6-iodo derivative (23l) was intended for the use as a
135
I-labelled radioactive probe.
4. Structure–activity relationship
In a number of biological models, differences between the defen-
sive responses induced by jasmonate or coronatine and the syn-
thetic analogues have been observed (Lauchli and Boland, 2003,
and references therein). In some cases, the activity of the com-
pounds differed. For example, unsubstituted indanoyl isoleucine
15a did not induce the accumulation of poppy alkaloids while coron-
alon 24 did (Haider et al., 2000), although in other models the activ-
ity of several analogues was comparable (for example, both indanoyl
isoleucine 15a and coronalon 24 induce the production of nicotine in
tobacco plant; Zhang et al. (1997), Schüler et al. (2001); indanoyl
isoleucine 15a as well as the 6-azido analogue 23m and coronalon
24 induced glyceollin production in soybean cell cultures; Schüler
et al. (2001)). However, in other cases, the response induced by
the elicitor differed. For example, in a bioassay based on the emis-
sion of volatile organic compounds from Lima bean plants exposed
to the solution of the tested substance, there were differences in
the composition of the volatile blend (Schüler et al., 1999). The emis-
sion of three volatiles could only be elicited by herbivory itself or by
coronatine and coronalon which represent the closest analogues of
jasmonates. The activity of other analogues including the unsubsti-
tuted indanoyl isoleucine 15a varied, but so did the composition of
the blend. Similarly, jasmonates and its mimics differentially elicit
the systemic response in the tobacco plant (Pluskota et al., 2007;
Wang et al., 2008) and to induce resistance against downy mildew
pathogen in pearl millet (Deepak et al., 2007).
The differential effects cannot be simply attributed to the struc-
ture of the conjugated amino acid or to the nature of the substitu-
ent in position 6. This indicates the recognition process is more
complex, and the hormone or its analogues do not interact with
just one, but rather several members of the JAZ protein family,
and the differential recognition by the JAZ proteins may result in
the triggering of a slightly different defensive response. Research
in this area will continue by the identification and importance of
the differences between the JAZ proteins, and in fact, synthetic
analogues which can interact selectively with the signalling path-
way could play a great role here. Apart from their role in the re-
search of the jasmonate signalling cascades, the analogues also
have industrial importance (Burns, 2001; Yukimune and Hara,
1996; Qian et al., 2004, 2005).
5. Conclusion
The activity of the natural phytohormone, jasmonoyl–isoleu-
cine conjugate 6, can be efficiently mimicked by easily accessible
synthetic analogues such as 15a or 24. Differences in the responses
triggered prove the importance of the hormone interaction with
several members of the JAZ protein family. Each member then en-
sures a different aspect of the response, thus tailoring the response
to the invader. Future research in this field will lead to the design
of analogues capable of a selective interaction with the JAZ pro-
teins, and of plants with modified response abilities.
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