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Endogenous and induced monooxygenase activity in gypsy moth larvae feeding on natural and artificial diets.

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Archives of Insect Biochemistry and Physiology 10:47-56 (1 989)
Endogenous and Induced Monooxygenase
Activity in Gypsy Moth larvae Feeding on
Natural and Artificial Diets
Carol A. Sheppard and Stanley Friedman
Department of Entomology, University of lllinois at Urbana-Champaign
NADPH oxidase activity was measured in third to sixth instar gypsy moth larvae fed oak or pine foliage. Activity levels ranged from 400 t o 1,900 prnol
NADPH oxidized/min/mg microsomal protein, but enzyme activity was not
correlated with host plant ingested. Similarly, activity levels in larvae fed diets
containing inducers, such as the terpenoid a-pinene or pentamethylbenzene,
ranged from 700 to 1,500 pmol NADPH oxidized/min/rng protein, levels that
were comparable to those measured for larvae fed control diets. 0-demethylase
activity in older instar gypsy moth larvae fed pine averaged 109 pmol p-nitrophenol/min/mg protein, and activity levels in those fed diet containing apinene ranged from 22 to 55 pmol/min/mg protein. Although statistically significant, these induced 0-demethylase levels are well below those observed
for Hehothis zea larvae. Our findings indicate that monooxygenases play a
minor, if any, role i n the ability of later instar gypsy moth larvae to develop
successfully on pine foliage.
Key words: Lymantria dispar, Heliothis zea, Estigmene acrea, Diptera, a-pinene,pine, oak, MFO
INTRODUCTION
Larvae of the gypsy moth, Lyrnuntriu dispar, are major defoliators of northeastern United States shade and forest trees. Although generally considered
to be polyphagous herbivores, the larvae show strong host plant preferences.
These have been categorized by Mosher [l]as follows: class I, in which oaks
predominate, species preferred by all larval instars; class 11, which includes
the gymnosperms, favored ”after the early larval stages”; class I11 and IV species,
least preferred.
Recent research has shown Mosher’s class I and I1 categories to be correctly
separated. First instar larvae suffer 100%mortality on coniferous foliage, whereas
larvae switched at the fourth instar from black oak to pine foliage achieve development rates and female fecundities that are comparable to or better than those
Received August 4,1988; accepted November 7,1988.
Carol A. Sheppard’s current address is USDA, ARS, BARC-East, Insect Reproduction Laboratory, Building 306, Room 323, Beltsville, MD 20705. Address reprint requests there.
01989 Alan R. Liss, Inc.
48
Sheppard and Friedman
of nonswitched larvae [2]. It is well to note that this ontogenetic broadening
of larval host plant range contains serious economic implications, in that deciduous trees can withstand two or three defoliations, but conifers die after a
single such incident [ 3 ] .
The striking contrast between oak and pine foliar chemistry raises the question of what larval functional changes underlie its ability in later life to utilize
pine as an alternative host plant. Pine is characterized by high concentrations
of potentially toxic terpenoids such as a- and P-pinene [4, and references
therein], which may be detoxified enzymatically by cytochrome P-450-dependent monooxygenases(polysubstratemonooxygenases,mixed-function oxidases)
[5,6]. In contrast, oak foliage is rich in tannins, compounds whose ability to
form complexes with proteins accounts for their putative role as digestibility
reducers [7,8]. However, it has been argued that the strongly alkaline pH conditions of gypsy moth larval midgut would dissociate such complexes [9].
The insect literature is rife with reports that MFO* activity is induced following ingestion of natural or artificial diets containing terpenes [5,6,10-181. Therefore, to investigate the role played by these enzymes in gypsy moth utilization
of pine foliage, we determined NADPH oxidase and O-demethylase activity
levels in larvae fed oak and pine foliage and artificial diets containing known
inducers of monooxygenase activity. The results of our studies, which include
comparative assays performed with other lepidopterous larvae and adult Diptera, are the subject of this report.
MATERIALS AND METHODS
Insect Rearing and Feeding
Gypsy moth larvae used in this study were maintained at 24"C, 40-50% relative humidity, on a 16:s L/D cycle. Eggs from which larvae were reared were
obtained from facilities in Otis Air Force Base, Otis, MA. Other lepidopterous
larvae used in these experiments were reared from matings among feral
individuals-Hyalophora cecropia-or from laboratory colonies-Heliothis zea and
Estigmenearea.
For experiments in which larvae were fed fresh foliage, bur oak (Quercus
macrocarpa), white pine (Pinus strobus), and wild cherry (Prunus serotina) were
collected from the same location in a forest preserve, in which trees are free
from direct chemical treatment and "drift" from agricultural fields is considered to be minimal. The cut ends of branches or stem ends of leaves were
inserted into a water bottle to maintain turgidity, and foliage was replaced every
2 to 3 days. Since gypsy moths perish in the first instar if fed a diet of pine
needles, in spite of feeding vigorously and producing copious amounts of feces
for a limited period of time, larvae were reared through the first two instars
on HWG diet, and transferred to either oak or pine as newly molted third
instar larvae. When reared on artificial diet, the HWG diet formulated by Bell
et al. [19], was used. Either 0.2% (+)-a-pineneor PMB was incorporated into
*Abbreviations: HWG = high w h e a t germ; MFO = mixed-function oxidase; PMB
methylbenzene; PMSF = phenlymethanesulfonyl fluoride.
=
penta-
Monooxygenase Activity in Gypsy Moth larvae
49
the diet as an MFO inducer. The same batch of diet without addition served
as a control in these experiments.
Adult Diptera (Phorrnia regina and Musca dornestica) of both sexes were
taken for experiments from laboratory stocks maintained on a diet of sucrose
and water.
Chemicals
( + )-a-Pinene, p-nitroanisole, p-nitrophenol, and PMB were purchased from
Aldrich Chemical Co., Milwaukee. P-NADPH was obtained from the United
States Biochemical Corp. , Cleveland. All other biochemicals were purchased
from Sigma Chemical Co., St. Louis.
Enzyme Preparation and Activity Assays
Midgut tissue was obtained from ”full gut” larvae that had been feeding on
a given diet or foliar type for 3 days prior to enzyme assay. The tissue was
prepared by removing it whole and transferring it to ice-cold sucrose medium
(0.25 M sucrose containing 1mM EDTA, 1%polyvinylpyrrolidone and 2 mM
PMSF [20]). After cutting the gut lengthwise, the tissue was gently shaken to
free it of its contents and was rinsed in fresh sucrose medium prior to homogenization in sucrose medium containing 0.5 mM PMSF. The method of Crankshaw et al. [20] yielded the most active larval enzyme preparations and was
used to isolate microsomal fractions.For adult dipteran abdominal microsomes,
the procedure described by Folsom and Hodgson [21] was employed.
In assays of microsomal MFO activity as measured by NADPH oxidation,
the following procedure was employed [21,22]. Duplicate amounts of microsomal protein ranging from 0.05 to 1.0 mg were incubated in 10-mlErlenmeyer
flasks with 0.13 pmol NADPH contained in a final volume of 1.0 ml of 50
mM Tris buffer, pH 7.4. Flasks containing corresponding amounts of microsomal protein but no NADPH served as blanks. Incubations were carried out
in a shaking water bath at 30°C. Absorbance at 340 nm was recorded on a
dual beam spectrophotometer at zero time and at 30 min after initiation of the
reaction, and NADPH oxidation was calculated from the decrease in absorption through that time span.
0-Demethylation of p-nitroanisole to p-nitrophenol was measured by slight
modification of a procedure previously reported [23]. Microsomal fractions
were isolated as described above, and the reaction was carried out in 10-ml
Erlenmeyer flasks for 30 min at 32°C in a shaking water bath. Microsomal protein ranging from 1.5 to 5 mg (in the case of gypsy moths) or 0.8 to 3 mg (H.
zea) was added to initiate the reaction in “experimental” flasks, which contained the following in a final volume of 1.6ml: 0.5 mM NADP, 2.5 mM glucose6-phosphate, 2 units glucose-6-phosphatedehydrogenase, 7.5 mM MgCI2, 0.5
mM p-nitroanisole, and 100 mM Tris-HC1, pH 7.8. The reaction was terminated by the addition of 400 pl of 1 N HCl. “Control” flasks contained the
same reaction mixture and final volume as did experimental flasks, except that
HCl was added immediately after the addition of the microsomal protein at
zero time. Upon termination of the reaction, the acidified reaction mixture
was “vortexed” with 2 ml chloroform, and after centrifugation, 1 ml of the
chloroform layer was “vortexed” with 1ml of 0.5 N NaOH. Following centrif-
Sheppard and Friedman
50
ugation, the absorbance of the NaOH layer at 400 nm was determined for experimental vs. control samples, and results were calculated as mean p-nitrophenol
produced/min/mg microsomal protein.
Protein was determined by the method of Bradford [24], with human yglobulin Fraction I1 serving as a standard and protein dye reagent purchased
from BioRad Corp., Richmond, CA.
Experiments with adult Diptera were repeated at least twice, and all other
experiments were replicated three or more times. A two-tailed Student's t-test
was used for statistical analysis of the difference between the means of two
groups, probability < .05 being considered significant.
RESULTS
Table 1summarizes the NADPH oxidase activities of three cohorts of larvae
fed fresh oak or pine foliage through the 1985 season. In four comparisons,
pine-fed larvae have significantlyhigher levels of endogenousNADPH-oxidation
activity than do their oak-fed counterparts, and in three comparisons the reverse
is true. Gypsy moth microsomal MFO activity also appears to be unaffected
by seasonal variations in foliage [25, and references therein], since there is no
evident correlation between the phenology of the ingested foliage and NADPH
oxidase levels.
NADPH oxidase activities in two species of Diptera and two additional species of Lepidoptera are shown in Table 2. Enzyme activity levels in the lepidopterous species, H. cecropia and E. acrea, fed cherry foliage are comparable,
averaging about 3,600 pmol NADPH oxidized/min/mgprotein. The basal activities of microsomal enzymes isolated from housefly (M. domesticu) and blowfly (P. regina) abdomens range from nearly 5,000 to 13,000 pmoYmin/mg protein.
For comparative purposes, NADPH oxidase levels in gypsy moth and
saltmarsh caterpillar ( E . acrea) larvae fed a diet containing either of two known
monooxygenase inducers, a-pinene or PMB, are presented in Table 3. No differences in enzyme activity are observed between gypsy moth larvae reared
on control and inducer diets. In contrast, activity levels of salt marsh larvae
TABLE 1. NADPH Oxidase Activity in Gypsy Moth Larvae Fed Fresh Foliage
Cohort
1
2
3
Instar
Date"
5th
6th
3rd
4th
5th
3rd
4th
5th
6th
June 7
July 10
August 24
Enzyme Activityb
Oak leaves
Pine needles
1,933
567
1,400
600
767
867
600
833
1,400
t 203
*
t
k
t
*
t
t
t
93
153
20
43
167
133
117
80
'Date when newly molted 3rd instar larvae were transferred from diet to foliage.
bData expressed as pmol NADPH oxidized/min/mg protein S.E.
'Indicates P < .05%. Comparisons are within rows of a given cohort.
x
*
933
1,200
1,200
1,033
1,567
433
967
1,000
1,167
2
57'
t 133*
2
t
2
t
t
*
t
140
76*
107'
67*
100"
70
60"
51
MonooxygenaseActivity in Gypsy Moth larvae
TABLE 2. NADPH Oxidase Activity in Representative Species of Diptera and Lepidoptera
Insect
Age
M. dornestica
(adult abdomen)
P. regina
(adult abdomen)
H . cecropia
(midgut)
E . acrea
(midgut)
“Data expressed as
9 days
11days
2 days
4 days
4th instar
5th instar
5th instar
5th instar
Diet
Enzyme activity”
Sucrose
Sucrose
Cherry foliage
Cherry foliage
Oak foliage
10,600
13,467
7,000
4,933
3,327
2,627
3,927
3,420
t 800
f 1,267
t
f
t
f
t
f
333
300
233
99
567
467
x pmol NADPH oxidizediminlmgprotein t S.E.
fed either of the inducer diets average 1.6 times more than those of their noninducer-fed counterparts. In addition, basal (noninduced)activity levels in salt
marsh larvae are higher than the corresponding values for gypsy moth larvae
fed the same batch of HWG diet.
Measurements of 0-demethylase activity in older instar gypsy moth larvae
fed fresh foliage or HWG diet with and without a-pinene are given in Table 4.
The enzyme activity of fifth instar larvae fed pine foliage is significantly greater
than that of larvae fed oak foliage. Fifth and sixth instar larvae fed HWG diet
containing 0.2% a-pinene show a comparatively small, although statistically
significant (see below and “Discussion”), increase in 0-demethylase activity
over those fed HWG without inducer.
0-Demethylase activity in Heliofhiszeu larvae fed HWG diet containing 0.2%
a-pinene is presented in Table 5 for comparative purposes. After 2 days of
feeding, activity levels are 1.7 times greater in larvae fed the inducer-containing
diet than those fed control diet. Enzyme activity levels in a-pinene-fed larvae
rise from 290 to 800 pmol p-nitrophenollminlmgprotein prior to gut purging
at day 3. Larvae in the empty gut stage fed a-pinene for 3 days have activity
TABLE 3. NADPH Oxidase Activity in Larvae Fed Inducer Compounds
Insect
Instar
L. dispar
E . acrea
3rd
4th
5th
6th
4th
Insect
Instar
L. dispar
4th
6th
4th
5th
E. acrea
x
HWG diet
767 f
734 t
900 f
837 t
1,531 f
Enzyme Activity
HWG w/0.2% a-pinene
694
759
630
731
2,232
68
193
34
83
29
HWG diet
t 200
f
230
t 103
f 50
t 91*
Enzyme Activitf
HWG w/0.2% PMB
1,030 t 137
1,531 f 328
4,234 t 430
313
3,587
*
“Data expressed as pmol NADPH oxidizediminlmg protein f S.E.
*IndicatesP < .05%. Comparisons are within rows.
1,397
1,301
7,268
5,020
f
t
f
t
237
135
800*
386*
52
Sheppard and Friedman
TABLE 4. 0-Demethylase Activity in Gypsy Moth Larvae
Instar
5th
5th
6th
Diet
Enzyme activity
Oak foliage
Pine foliage
HWG diet
HWG w/0.2%a-pinene
HWG diet
HWG w/0.2%a-pinene
57 2 1
109 2 4*
13 2 4
22 2 4*
18 2 1
55 2 2*
"Data expressed as X pmol p-nitrophenollminlmg protein i S.D.
'Indicates P < .05%. Comparisons are within larval instars, within
a given dietary regime.
levels comparable to those measured for larvae with full guts fed the pinene
diet for 2 days.
Table 6 shows development time and pupal weights for L. dispar larvae reared
from egg eclosion to pupation on HWG diet or diet containing 0.2% a-pinene.
In the first experiment, male pupae from HWG diet weighed more than those
from the HWG w/pinene diet. Other than this, no appreciable differences were
observed between insects reared on control and inducer-containingdiet.
DISCUSSION
The importance of microsomal cytochromeP-450-dependentmonooxygenases
in the biotransformation of lipophilic xenobiotics, particularly drugs, became
apparent with mammalian studies conducted in the mid-1950s. These enzymes
are now known to be ubiquitous in aerobic organisms; in insects, MFOs play
a primary role in hormone metabolism, pesticide resistance, and response to
plant allelochemicals [see 11, 12,26-28 for review].
Although a large array of reactions is catalyzed by the cytochrome P-450
monooxygenases, e.g., epoxidation, hydroxylation, N-demethylation, 0demethylation, etc., all reactions require reducing equivalents in the form of
NADPH. NADH is usually an ineffective substitute for NADPH, although it
may have a synergistic effect when used in conjunction with the latter [27].
Hence, demonstration of increased NADPH oxidation activity should serve
TABLE 5. 0-Demethylase Activity in Fifth Instar Heliothis zea Larvae
Day
Gut lumen
Diet
Enzyme activityb
2
2
2.5
2.5
3
3
Full
Full
Full
Full
Empty
Empty
HWG
HWG ~ 1 0 . 2 %
a-pinene
HWG
HWG ~ 1 0 . 2 %
a-pinene
HWG
HWG w/0.2% a-pinene
172 2 10
290
8"
268 2 6
818 2 7*
642 4
255 2 50*
*
"Day indicates number of days on diet, from day of eclosion to 5th instar to day of
experiment.
bData expressed as % pmol p-nitrophenoliminlmg protein 2 S.D.
*IndicatesP < .05%. Comparisons are within a given day.
Monooxygenase Activity in Gypsy Moth larvae
53
TABLE 6. Gypsy Moth Development on Normal and Inducer Diets
Diet
Experiment 1
HWG
HWG w/0.2% a-pinene
Experiment 2
HWG
HWG w/0.2% a-pinene
Days"
20.3
22.9
2
23.0
23.1
4
4
2
Malesb
1.8
1.7
451 & 83
358 2 67
1.3
1.4
376
343
2
F
PuDal weights
(N)
Females
(9)"
(6)
52 (12)
31 (13)
1,047
993
?
k
(N)
243 (16)
259 (20)
1,090 t 262 (12)
941 ? 267 (9)
days t S1D. from day of egg eclosion to day of molt to 5th instar.
bValues are X weight in mg & S.D.; (N) indicates number of individuals.
*Indicates P < .05% in a two-tailed t-test. Comparisons are within columns, within a given
experiment.
as a reasonable indicator of monooxygenase activity. Given this, our results
suggest that monooxygenases play only a minor role, if any, in the ability of
later instar gypsy moth larvae to feed successfully on pine. A summary of
experiments conducted through the 1985 season reveals no consistent pattern among NADPH oxidase activities of gypsy moths fed oak or pine foliage
(Table 1). There is neither a correlation between NADPH oxidase activity and
foliar type or phenology nor an ontogenetic increase in activity levels.
The highest NADPH oxidase activity observed in fifth instar gypsy moth
larvae fed oak leaves averages about 1,900pmol NADPH oxidizedmidmg microsoma1 protein (Table l), which is less than 50% that of fifth instar salt marsh
larvae fed the same foliage (Table 2). That suitable assay conditions existed for
NADPH oxidation may be seen by the values obtained for the cyclorrhaphous
Diptera using the same assay system. These amounts, ranging from 5,000 to
over 13,000 pmol NADPH oxidized/min/mgprotein (Table 2), are comparable
to those reported in the literature [21].
Artificial diet containing 0.2% a-pinene, the concentration commonly
employed to induce monooxygenase activity in insects, fails to elicit enhanced
activity levels in gypsy moth larvae from the third through the sixth instar
(Table 3). In contrast, a 1.6-fold increase in endogenous NADPH oxidase activity is observed in fourth instar salt marsh larvae fed the pinene diet. Similarly,
sixth instar southern armyworms fed this same dietary level of a-pinene exhibit
significant increases in endogenous NADPH oxidation [17].
In keeping with the results obtained with a-pinene in the diet, 0.2% PMB
has no effect on gypsy moth NADPH oxidase activity (Table 3). However, fourth
and fifth instar salt marsh larvae show 1.5- to 1.7-fold increases in activity following ingestion of the HWG w/PMB diet. And, as was expected from experiments involving Lepidoptera fed foliage (Tables 1and 2), salt marsh larvae fed
HWG diet have higher basal activities than do gypsy moth larvae fed the
same diet.
Using larvae that originated from field-collected egg masses and that were
fed pin oak foliage, Ahmad and Forgash [29] reported NADPH oxidase levels
in fifth instar gypsy moth larvae that were significantly lower than those of
larvae fed a basal, i.e., wheat germ diet. This would indicate, as have our stud-
54
Sheppard and Friedman
ies, that feeding on pine foliage, which might be expected to induce higher
levels of monooxygenase than would a HWG diet, does not do so in this insect.
However, the specific activity levels reported in their paper were higher than
those we found in our preparations. There is no reason to doubt their work,
and the difference may lie in the fact that their strain, originating from fieldcollected egg masses, might be genetically different from ours, a laboratory
strain obtained from the facility at Otis AFB. It should also be noted that in
the same report they state that their wheat germ diets might be contaminated
with DDT, a compound that would be expected to stress the larvae generally,
leading to a number of metabolic changes.
Since we were unable to obtain significant andlor consistent induction of
NADPH oxidase levels with gypsy moths fed pine foliage or artificial diet containing monooxygenase inducers, we employed another assay commonly used
to measure monooxygenase activity in insects. Results obtained with the
0-demethylation assay show that activity levels in fifth instar gypsy moth larvae fed pine foliage are more than 1.5 times greater than those of larvae fed
oak foliage (Table 4).Fifth and sixth instar larvae feeding on artificial diet also
show a significant increase in 0-demethylase activity following ingestion of
0.2% dietary a-pinene.
The induced activity levels of fifth and sixth instar gypsy moth larvae using
the 0-demethylase assay represent the highest we have observed for this insect
under any conditions. However, using the same dietary regime and assay conditions, basal and induced activity levels in fifth instar "full gut" H. zeu larvae
range from 172 to over 800 pmol p-nitrophenollminlmg microsomal protein,
levels that are five- to 15-fold higher than the corresponding values for late
instar gypsy moths (cf. Tables 4 and 5). In view of these comparative findings, it is questionable whether the 0-demethylase induction levels we observe
in gypsy moth larvae are physiologically meaningful.
Perusal of the literature reveals that the 0-demethylase activity levels we
obtain with H . zeu larvae are within the range reported for other Lepidoptera
with the exception of the gypsy moth. For example, after 2 days of feeding on
corn foliage, 0-demethylase activity in sixth instar fall armyworms rises to 290
pmol p-nitrophenollminlmg protein, representing a 6.3-fold increase in activity over that of larvae fed soybean foliage [16]. Similarly, basal activity levels in
Munduca sextu larvae during fifth instar development to the prepupal stage
range upward from 86 to 270 pmol p-nitrophenollminlmgprotein [30].
Monooxygenase activity in gypsy moth larvae as measured by N-demethylation of p-chloro-N-methylaniline is also relatively low compared with that
reported for other Lepidoptera. In gypsy moth larvae fed pin oak or a wheat
germ-based artificial diet, peak activity levels occur in the final instar and average 0.13-0.15 nmol N-demethylated product (p-chloroani1ine)lminlmgmicrosoma1 protein [31]. In contrast, basal activity levels in sixth instar southern
armyworm larvae average 1.7 nmol p-chloroanilinelminlmg protein [6]. Using
the same substrate, N-demethylase activity in sixth instar fall armyworm larvae fed various host plants ranges from 0.31 to 0.96 nmol p-chloroanilinelminlmg
protein [32], and activity levels in fifth instar H. cecropia larvae fed cherry foliage
average 0.8 nmol p-chloroanilinelminlmg protein (C. Sheppard and S. Friedman, personal observations using assay conditions described in [33]).
Monooxygenase Activity in Gypsy Moth Larvae
55
Normal larval development has been observed with gypsy moths reared on
artificial diets containing terpenes and on pine foliage, which is rich in terpenoids. When reared from eclosion to pupation on a HWG diet containing 0.2%
a-pinene, gypsy moth larvae have development rates and, except in one comparison, pupal weights that are not different from those for larvae fed HWG
diet without addition (Table 6). Hence, little if any deleterious developmental
effects are associated with this level of dietary terpenoid.
Barbosa et al. [2] have reported that gypsy moth larvae switched at the fourth
instar from black oak foliage to coniferous foliage may have faster larval development times and greater fecundities than larvae maintained on black oak
foliage. Our own findings indicate, as well, that third instar larvae can, at times,
feed successfully on coniferous foliage [25]. Thus, it appears that if terpenoids
are responsible for the restricted host plant range of very young gypsy moth
larvae, some detoxication mechanism(s) other than MFOs must be utilized by
gypsy moths. There are a number of ways in which insects may deal with
toxins, ranging from sequestrationand immobilization, through various energyrequiring activities to nonabsorption. As Dowd et al. 1341 have stated, current
research trends are biased toward the microsomal monooxygenases because
of their induction by plant compounds. Our findings emphasize the need for
investigations of alternative mechanisms whereby insect herbivores counteract plant defensive compounds.
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