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RAPID COMMUNICATION
METHYL JASMONATE APPLICATION INDUCES
INCREASED DENSITIES OF GLANDULAR
TRICHOMES ON TOMATO,
Lycopersicon esculentum
ANTHONY J. BOUGHTON,* KELLI HOOVER, and GARY W. FELTON
Department of Entomology, Pennsylvania State University, University Park,
PA 16802, USA
(Received March 21, 2005; revised May 31, 2005; accepted June 2, 2005)
Published Online July 5, 2005
Abstract—This study was designed to address whether applications of methyl
jasmonate (MJ) or Benzothiadiazole (BTH) to cultivated tomato, Lycopersi-
con esculentum, induced elevated densities of defense-related glandular
trichomes on new leaves. Four-leaf tomato plants were sprayed with MJ,
BTH, or control solutions, and the density of type VI glandular trichomes on
new leaves was subsequently determined at 3, 7, 14, 21, and 28 d. At 7, 14,
and 21 d, the density of type VI glandular trichomes on new leaves was
significantly higher on MJ-treated plants than on BTH- or control-treated
plants. At 7 and 14 d after treatment, the mean density of glandular trichomes
on new leaves of MJ-treated plants was ninefold higher than on leaves of
control-treated plants. We observed entrapment of immature western flower
thrips in trichomes on MJ-treated plants at higher rates than on BTH or
control plants. Studies to evaluate potential trade-offs between reductions in
pest populations by increased trichome density and possible negative impacts
of trichome induction on biological control agents are needed.
Key WordsVLycopersicon esculentum, tomato, methyl jasmonate, induced
resistance, glandular trichomes.
0098-0331/05/0900-2211/0
#
2005 Springer Science + Business Media, Inc.
2211
Journal of Chemical Ecology, Vol. 31, No. 9, September 2005 (
#
2005)
DOI: 10.1007/s10886-005-6228-7
* To whom correspondence should be addressed. E-mail: ajb25@psu.edu
INTRODUCTION
Plants have evolved numerous defensive strategies to reduce herbivory or its
effects on plant fitness (Karban and Baldwin, 1997). These defenses may be
constitutively expressed or may be induced following attack by herbivorous
arthropods. Induced responses to herbivory have been widely documented and
may involve changes in plant secondary chemistry, reductions in plant
nutritional quality, emission of volatiles that attract predators and parasitoids
of herbivores (Kessler and Baldwin, 2002), or increases in trichome density
(Traw and Dawson, 2002). Responses to herbivores may be mediated by the
jasmonic acid (JA) or salicylic acid (SA) signaling pathways (Kessler and
Baldwin, 2002).
Trichomes occur on the surfaces of many plants and can make a
contribution to plant resistance against herbivores (Simmons and Gurr, 2004).
Trichomes play important roles in arthropod resistance within the plant family
Solanaceae and particularly within the genus Lycopersicon (Kennedy, 2003).
Seven types of trichomes occur on Lycopersicon spp., including glandular
trichomes (types I, IV, VI, and VII) and nonglandular trichomes (types II, III,
and V) (Luckwill, 1943). Glandular trichomes have heads containing various
sticky and/or toxic exudates that may be secreted onto the plant surface or may
rupture on contact with herbivores, causing irritation, entrapment, or death
(Simmons and Gurr, 2004). Nonglandular trichomes do not have heads and
affect herbivores by mechanically obstructing their movement across the plant
surface (Simmons and Gurr, 2004). Four-lobed type VI glandular trichomes are
associated with high levels of arthropod resistance in L. esculentum (Kennedy,
2003).
Recent studies of the tomato mutant jasmonic acid insensitive 1[jai1],
which is defective in JA-based signaling, revealed several defense-related
phenotypes, including abnormal glandular trichome production, suggesting a
role for JA in glandular trichome-based defenses (Li et al., 2004). JA was
recently shown to induce trichomes in Arabidopsis (Traw and Bergelson,
2003).
To our knowledge, jasmonates have not previously been demonstrated
to induce elevated trichome densities in tomato. In preliminary studies, we
found applications of methyl jasmonate (MJ) and BTH (Actigardi)to
tomato reduced populations of Myzus persicae (Sulzer) (Homoptera: Aphidi-
dae) in the greenhouse (Boughton et al., unpublished data). Here, we
present evidence showing that exogenous application of methyl jasmonate,
but not BTH, induced dramatic increases in densities of type VI glandu-
lar trichomes on new leaves of L. esculentum. We suggest that resistance to
herbivores induced by these elicitors probably operate by different
mechanisms.
2212 BOUGHTON ET AL.
METHODS AND MATERIALS
Plants. Tomato plants (L. esculentum c.v. Trust) (DeRuiter Seeds) were
grown in 4-in. plastic pots in sterile soil mix (peatYperliteYvermiculite,
55Y20Y25; Penn State Seed, Dallas, PA, USA). Plants were grown in the
greenhouse under natural lighting with day and night temperatures varying
between 21 and 33-C. Plants were irrigated daily with fertilizer solution
(NYPYK, 4Y18Y38, Chem-Gro Tomato Formula; Hydro-Gardens Inc., Colorado
Springs, CO, USA) containing supplemental magnesium sulphate and calcium
nitrate.
Effect of Elicitors on Induction of Glandular Trichomes. Fourth-leaf
tomato plants (45 per treatment) selected at random were treated with (1) 7.5
mM MJ (Bedoukian Research, Danbury, CT, USA), or (2) 0.1 mM BTH
(Actigard
\
-Syngenta, Greensboro, NC, USA) (both in 0.8% ethanol and water),
or (3) control solution (0.8% ethanol and water). Elicitor concentrations were
within the range used in other studies and were selected in dose response trials
as the lowest concentrations that induced resistance. Plants receiving different
treatments were moved to opposite sides of the greenhouse and sprayed until
leaves were saturated. After 24 hr, plants were arranged on three benches ac-
cording to a randomized block design. At 3, 7, 14, 21, and 28 days post-
treatment (DPT), three plants from each treatment were selected at random on
each of the three benches, and the youngest terminal leaflet at least 5 cm in
length on each plant was removed for sampling. This leaf selection process
yielded terminal leaflets of similar sizes, which ranged from 5.8 to 8.0 cm
in length, and 11.7 to 21.8 cm
2
in area. Two leaf disks (0.6 cm diam.) were
punched midway between the leaf tip and leaf base, one on either side of the
midrib, taking care to preserve trichomes on the upper leaf surface. Numbers of
FIG. 1. Type VI glandular trichomes on upper surface of leaves from (A) control or (B)
MJ-treated tomato plant at 12 DPT. Photographs show same field of view at 15
magnification.
2213
TRICHOME INDUCTION BY METHYL JASMONATE
type VI trichomes were determined by using a dissecting scope. Preliminary
observations had suggested MJ treatments increase type VI trichome density.
Other trichome types were not examined in this study. Plants were sampled only
once. Trichome density data were evaluated with one-way ANOVA.
RESULTS
Results showed that application of MJ to tomato plants induced increased
densities of type VI glandular trichomes on new leaves expanding after treat-
ment (Figure 1). BTH treatment had no effect on trichome densities (Table 1).
Highest densities of trichomes were present on leaves produced 14 d after
MJ treatment. At 7 and 14 DPT, trichome densities were ninefold higher on
MJ- than control-treated plants. Trichome densities were significantly higher
(Tukey’s test, P < 0.05) on MJ plants than on BTH or control plants at 7, 14 and
21 DPT. MJ-treated plants were observed to entrap higher numbers of im-
mature western flower thrips than BTH- or control-treated plants (Boughton
et al., unpublished data).
DISCUSSION
Increasing interest has focused on the use of elicitors of natural plant
defensive responses, such as JA and MJ, to induce resistance to herbivores and
TABLE 1. EFFECT OF ELICITOR TREATMENT ON GLANDULAR TRICHOME DENSITY ON
NEW TOMATO LEAVES
Mean trichome density
a
(no./mm
2
T SE)
Time point
b
(DPT) Control-treated BTH-treated MJ-treated P value
c
3 0.7 T 0.1 a 0.8 T 0.1 a 0.9 T 0.1 a 0.105
7 1.1 T 0.2 a 1.5 T 0.3 a 9.4 T 0.9 b <0.001
14 2.1 T 0.2 a 2.2 T 0.4 a 17.9 T 1.8 b <0.001
21 3.1 T 0.4 a 3.7 T 0.4 a 12.5 T 1.0 b <0.001
28 5.3 T 0.7 ab 4.7 T 0.6 a 7.2 T 0.5 b 0.027
MJ = Methyl jasmonate, BTH = Benzothiadiazole.
a
Mean density of type VI glandular trichomes on upper surface of new leaves. N = 9 plants per
treatment. One leaf examined per plant. Plants sampled only once. Densities calculated from counts
of trichomes on two leaf disks per leaf. Means within the same row followed by different letters are
significantly different by Tukey’s-test (P < 0.05).
b
Days post-treatment (DPT).
c
One-way ANOVA evaluating effect of treatment on trichome density.
2214 BOUGHTON ET AL.
plant pathogens (Thaler, 1999). In tomato, jasmonate-induced resistance to
herbivores has been documented in several field studies and has frequently been
attributed to the action of defensive proteins such as polyphenol oxidase and
proteinase inhibitors (Thaler, 1999). These proteins are induced within 24 hr of
elicitor treatment, before any changes in type VI trichome density are
detectable. However, over subsequent weeks it seems likely that a component
of jasmonate-induced resistance may be a result of increased densities of type
VI glandular trichomes, contributing to elevated polyphenol oxidase levels and
increased repellency, entrapment, or mortality of arthropod herbivores. We
suggest that elevated trichome densities were likely responsible for increased
thrips entrapment observed in our studies.
Although it is likely that jasmonate-induced resistance in crop plants will
have direct negative impacts on arthropod pests, which may be beneficial from a
pest management perspective, it is also possible that induced plant defenses may
have indirect effects on natural enemies, such as insect parasitoids and pred-
ators, which contribute to the regulation of pest populations (Thaler, 1999;
Simmons and Gurr, 2004). Trichomes, for example, may have differing impacts
on natural enemies ranging from positive effects, such as increased searching
efficiency, to negative effects, such as hindered movement, irritation by tri-
chome exudates, and entrapment (Obrycki, 1986).
The use of jasmonates to induce plant resistance to arthropod pests as a
management tactic will require careful evaluation to ensure that benefits arising
from negative impacts on pest fitness are not outweighed by adverse effects that
might reduce the efficacy of biological control.
AcknowledgmentsVThis research was funded by Pennsylvania Department of Agriculture
(Contract ME 442289).
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