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Insecticidal and enzyme inhibitory activities of sparassol and its analogs against Drosophila suzukii Junheon Kim, Miyeon Jang, Kyoung-Tae Lee, Kyungjae Andrew Yoon, and Chung Gyoo Park J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.6b01528 • Publication Date (Web): 21 Jun 2016 Downloaded from http://pubs.acs.org on June 24, 2016

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Journal of Agricultural and Food Chemistry

Insecticidal and enzyme inhibitory activities of sparassol and its analogs against Drosophila suzukii

Junheon Kim1, †, Miyeon Jang 3, †, Kyoung-Tae Lee4, Kyungjae Andrew Yoon5, Chung Gyoo Park1,2,3,*

1

Institute of Agriculture and Life Science, 2Institute of Life Science, and 3Division of Applied Biology (BK 21+ Program), Gyeongsang National University, Jinju 52828, Republic of Korea. 4

Southern Forest Resources Research Center, National Institute of Forest Science, Jinju 52817, Republic of Korea. 5

†

Department of Agricultural Biotechnology, Seoul National University, Seoul 08826, Republic of Korea.

These authors contributed equally to this study.

*Corresponding author: Prof. Park, Chung Gyoo Institute of Agriculture and Life Science, Gyeongsang National University, Jinju 52828, Republic of Korea. E-mail: [email protected], Tel: +82-55-772-1925, Fax: +82-55-772-1929

ACS Paragon Plus Environment


1

Abstract

2

Drosophila suzukii is an economically important pest in America and Europe as well

3

as in Asia. Sparassol and methyl orsellinate are naturally produced by the cultivating

4

mushrooms; Sparassis cripta and S. latifolia. Fumigant and contact toxicities of synthetic

5

sparassol and its analogs, methyl orsellinate and methyl 2,4-dimethoxy-6-methylbenzoate

6

(DMB), were investigated. Negligible fumigant activity was observed from the tested

7

compounds. However, DMB showed the strongest contact toxicity followed by sparassol and

8

methyl orsellinate. The possible modes of action of the compounds were assessed for their

9

acetylcholinesterase (AChE) and glutathione S-transferase (GST) inhibiting activities. AChE

10

activity was weakly inhibited by methyl orsellinate and DMB, but the GST was inhibited by

11

sparassol, methyl orsellinate, and DMB. Thus, DMB could be a promising alternative to

12

common insecticides as it can be easily synthesized from sparassol which is the natural

13

product of Sparassis species. Sparassis species could be an industrial resource of DMB.

14 15

Keywords: Spotted wing drosophila; Asian vinegar fly; sparassol; methyl orsellinate; methyl

16

2,4-dimethoxy-6-methylbenzoate;

17

1


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1. Introduction

19

Sparassis species (Polyporales: Sparassidaceae), known as cauliflower mushrooms,

20

are edible and distributed throughout the northern temperate forests.1 Cultivation of

21

cauliflower mushrooms is increasing in Korea, Japan, USA and Australia. Sparassia cripta

22

has been reported for many pharmacological activities, such as antitumor, antimetastatic,

23

antihypertensive and anti-diabetic effects.2 In culture, S. cripta and S. latifolia produce two

24

metabolites

25

orsellinate (methyl 2,4-dihydroxy-6-methylbenzoate).2,

26

have antimicrobial, antifungal and nematicidal activities.2, 4 However, insecticidal activities

27

of these compounds are not documented yet.

sparassol

(methyl

2-hydroxy-4-methoxy-6-methylbenzoate) 3

and

methyl

These compounds are known to

28

Spotted wing drosophila (SWD), Drosophila suzukii Matsumura (Diptera:

29

Drosophilidae), is a native fruit fly of south-eastern Asia. It recently invaded in North and

30

South America and European continents.5-7 SWD larvae mostly develop in unripe and

31

ripening fruits, because the female adults can lay eggs in healthy ripening fruits as well as in

32

damaged or split fruits with its unique, long and serrated ovipositor.8 It infests cherries and

33

berries leading into crop damage and potential economic loss. The annual economic loss

34

caused by SWD was estimated as $US 511 million only in three western US states.9 De Ros

35

and co-workers estimated that 13.7% and 6.7% of potential revenue losses would occur

36

annually without and with management of SWD, respectively, in the small fruit industry at

37

Trento, Italy.10 And, among the management strategies, the costs for insecticides occupied

38

0.25% of potential annual revenue (ca €60,000) .10

39

Because SWD is new to American and European continents, limited researches are

40

available for its control. In case of chemical sprays, adults should be targeted to kill well

41

before their oviposition, as sprays are not effective against mining larvae.11 Control of insect 2



42

pests is commonly dependent on continued applications of synthetic pesticides. Although

43

effective, there are concerns regarding the use of such pesticides leading to resistance

44

development, environmental pollution and health disorders. To address these issues, a lot of

45

efforts are made to exploit natural alternates such as essential oils.12 Fungal-produced

46

compounds have many biological activities such as antimicrobial and antifungal activities13, 14,

47

however, little is reported on their insecticidal activities.

48

This study investigated the fumigant and contact toxicity of sparassol and its analogs

49

against SWD. For determining the mode of actions of these compounds, their activity was

50

also assessed against acetylcholinesterase (AChE) and glutathione S-transferase (GST) of

51

both sexes of SWD adults. The objective of this research was to find alternatives to

52

conventional insecticides by assessing structure-activity relationships among the sparassol

53

and its analogs, and by determining target sites of the compounds.

54 55

2. Materials and Methods

56

2.1. Insects

57

The colony of SWD has been maintained in a netted cage (25 × 25 × 20 cm3,

58

BugDorm, Taiwan) with an artificial diet for larvae and 50% sugar solution for adults under

59

24-26°C, 60-70% RH and a photoperiod of 16:8 (L:D).15 Only the adults (5-7 days old) were

60

used for bioassay.

61 62

2.2. Chemicals

63

Sparassol, methyl orsellinate, and methyl 2,4-dimethoxy-6-methylbenzoate (DMB)

64

(Fig. 1) were synthesized by the methods modified from previous reports.16, 17 Abamectin

65

(98.7% pure) was purchased from Sigma-Aldrich (St. Louis, MO). The synthetic scheme is 3


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presented in Scheme 1 (Supporting Information) and the detailed procedure has been

67

described in the supplemental materials. The purities of sparassol, methyl orsellinate, and

68

DMB were 98.8%, 94.3%, and 95.0%, respectively. Their structures were confirmed by mass

69

spectrum and NMR. 1H and

70

performed with a Bruker DRX-500 spectrometer using TMS in CDCl3 as an internal standard

71

at Center for Research Facilities of GNU. All NMR data were in agreement with those

72

reported in the literatures.3, 16

73

Sparassol: 1H NMR (500 MHz, CDCl3, δ) 2.494 (3H, s), 3.796 (3H, s), 3.922 (3H, s), 6.282

74

(1H, m), 6.330 (1H, d, J=2.5), 11.765 (1H, s); 13C (126 MHz, CDCl3, δ) 24.34, 51.83, 55.29,

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98.71, 105.26, 111.17, 143.12, 163.95, 165.56, 172.22.

76

Methyl orsellinate: 1H NMR (500 MHz, CDCl3, δ) 2.488 (3H, s), 3.925 (3H, s), 5.381 (1H, s),

77

6.228 (1H, m), 6.279 (1H, d, J=2.5), 11.753 (1H, s); 13C (126 MHz, CDCl3, δ) 24.27, 51.91,

78

101.28, 105.70, 111.34, 144.03, 160.26, 165.32, 172.14.

79

DMB: 1H NMR (500 MHz, CDCl3, δ) 6.305 (2H, br. S), 3.867 (3H, s), 3.773 (3H, s), 2.273

80

(3H, s);

81

55.83, 55.26, 51.95, 19.88.

13

13

C NMR (500 and 126 MHz, respectively) analyses were

C (126 MHz, CDCl3, δ) 168.68, 161.37, 158.20, 138.21, 116.36, 106.66, 96.11,

82 83

2.3. Fumigant toxicity

84

The assay on fumigant toxicity followed method using glass cylinder (11 cm in

85

height with a sieve at the mid-point, 4.5 cm inner diameter; 170 mL) previously reported.18

86

Synthetic compounds, each dissolved in acetone (20 µL) were applied on a filter paper disk

87

(8 mm, Advantech, Japan). After 10 min (time for evaporating the solvent), the disk was

88

placed on the bottom lid of the cylinder. The concentrations tested ranged from 2.94 to 11.76

89

mg/L air. Acetone alone was applied as a control. 4



90

Twenty SWD adults (10 males and 10 females) were placed on the sieve having a

91

cotton wick soaked with 10% sugar solution, thereby preventing their direct contact with the

92

test compounds. The top and bottom lids were then sealed with Parafilm to prevent leakage of

93

the fumigants. The insects were maintained at 24–26°C and 70% relative humidity. After 24 h

94

of treatment, they were moved to a mesh-lidded plastic Petri dish for 10 min. The adult flies

95

were considered dead if their appendages did not move after gentle touch of a fine brush. All

96

treatments were replicated 5 times.

97 98

2.4. Contact toxicity

99

Assay on contact toxicity was performed as follows: The adults of SWD were

100

directly exposed to topical application of the synthetic compounds (1.25–20 µg/fly) dissolved

101

in acetone (1 µL) using a micro syringe with repeating dispenser (Hamilton, Reno, NV). As a

102

positive control, abamectin was applied at a range of 0.025–50 ng/fly. Abamectin was

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selected because it is isolated from fermentation of Streptomyces avermitilis, a naturally

104

occurring soil Actinomycete, and its effect on SWD has never been reported, although it has

105

insecticidal activity. Then, the adults were placed in a mesh-lidded plastic Petri dish with

106

cotton wick soaked with 10% sugar solution, thereby preventing fumigant effect of the tested

107

compounds. After 24 h treatment, mortality was checked as above. Each treatment was

108

performed 5 times each with 20 adults of SWD (10 males and 10 females).

109 110

2.5. Extraction of crude protein

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Crude protein was extracted from 50 SWD females and males using a glass tissue

112

grinder. SWD adults were soaked in 300 µL of 0.1 M Tris-HCl (pH 7.8) containing 20 mM

113

NaCl, 0.5% Triton X-100, and protease inhibitor cocktail (Sigma-Aldrich). The SWD adults 5


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were ground in ice with a glass tissue grinder. Protein from the insect tissue debris was

115

purified by centrifuging the extract at 15,000 ×g for 15 min at 4 °C.

116 117

2.6. Inhibition of acetylcholinesterase (AChE) and glutathione-S-transferase (GST)

118

AChE and GST inhibitory activities of the compounds were analyzed by modified

119

methods of Ellman et al. (1961) and Kang et al. (2013), respectively.19, 20 Chemicals were

120

prepared by diluting in acetone. One microliter chemicals and 79 µL crude protein were

121

mixed in a 96-well microplate). Acetone without any chemical was treated as a positive

122

control. The concentrations of tested chemicals were 1, 0.5, 0.2, and 0.1 mg/mL.

123

For AChE inhibition, after pre-incubation period of 10 min, 10 µL of 10 mM

124

acethylthiocholine iodide (ASChI) and 10 µL of 4 mM 5,5’-dithiobis(2-nitrobenzoic acid)

125

(DTNB) were added. The AChE inhibitory activity was estimated by measuring the

126

maximum velocity (Vmax) for 30 min at 30 sec intervals at 405 nm at room temperature by

127

using a VersaMax ELISA Microplate Reader (Molecular Devices, Sunnyvale, CA, USA).

128

For GST inhibition, the substrate solution, which included 10 µL of 20 mM reduced

129

glutathione (Sigma–Aldrich) and 10 µL of 10 mM 1-chloro-2,4-dinitrobenzene (CDNB,

130

Sigma–Aldrich) diluted in 0.1 M Tris–HCl (pH 7.8), was added to the pre-incubated mixtures

131

of proteins and the synthetic compounds. The GST inhibitory activity was estimated by

132

measuring the maximum velocity (Vmax) for 30 min at 30 sec intervals at 340 nm at room

133

temperature by using a VersaMax ELISA Microplate Reader.

134

The inhibitory activity was estimated as:

135

Inhibitory activity (%) = 100 – (Vmax of treatment/Vmax of control × 100).

136

These assays were triplicated.

137

6



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2.7. Statistics

139

The corrected mortality was calculated using Abbott’s formula.21 The LD50 and IC50

140

values were estimated by probit analysis. Statistical analysis was performed using JMP ver.

141

9.0.2 (SAS Institute Inc., Cary, NC). Mean (±SEM) values are reported.

142 143

3. Results and Discussion

144

3.1. Fumigant toxicity

145

Sparassol and its two analogs showed negligible fumigant activities against SWD

146

adults. At the concentration of 11.76 mg/L air, respective mortalities by sparassol, methyl

147

orsellinate and DMB were 2.0%, 78% mortality of both the sexes of SWD adults (Table

151

1) at the concentration of 20 µg/fly. But, methyl orsellinate of same concentration exhibited

152

as low as 35% and 24% mortality against male and female adults of SWD, respectively. The

153

active compounds, sparassol and DMB were further tested at stepwise lower concentrations

154

(Table 1). The estimated LD50 values of mortality data revealed that DMB was around 5

155

times more toxic than sparassol in its contact toxicity against both sexes of SWD adults

156

(Table 2). Abamectin, which was used as a positive control was most toxic among the

157

compounds tested. Males were more susceptible to the tested compounds than female in term

158

of LD50 values.

159

This might be the first report of fumigant and contact toxicities of sparassol, methyl

160

orsellinate and DMB against insect pest even though nematicidal activity of sparassol has

161

been recently reported.4 Sparassol and its analogs exhibited strong contact toxicities in 7


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opposite of their fumigant activities against the SWD adults. Badaway and co-workers

163

reported that higher vapor pressure of monoterpenoids has a positive coefficient of fumigant

164

toxicity.22 The vapor pressures of sparassol, methyl orsellinate, and DMB were predicted as

165

5.48×10-4, 3.23×10-4, and 4.80×10-5 mmHg, respectively at 25 ºC.23 These values were

166

relatively lower than the structurally similar compounds such as eugenol (0.04×10-2 mmHg)

167

and methyl salicylate (7.0×10-2 mmHg) which showed strong fumigant activity against

168

adzuki bean beetle, Callosobruchus chinensis24 and Japanese termite, Reticulitermes

169

speratus.25 It is also reported that the compounds which showed insignificant fumigant

170

activities but having significant contact toxicity have lower vapor pressure than the

171

compounds which showed both fumigant and contact toxicities. Thus, the reason for trifling

172

fumigant activity of sparassol and its analogs may be due to their lower vapor pressure.

173

To assess structure-activity relationships among sparassol and its analogs, DMB

174

which is not biosynthesized by Sparassis species was synthesized and evaluated for their

175

insecticidal activity. Interestingly, DMB exhibited 5 times stronger toxicity than sparassol in

176

term of LD50, while methyl orsellinate showed lower insecticidal activity. However, the

177

compounds having phenolic hydroxy group were reported to have similar contact toxicity to

178

the corresponding compounds that where the phenolic hydroxy group was converted into

179

methoxy group. For example, similar contact toxicities were shown between methyl eugenol

180

and eugenol against American cockroach26 and methyl 2-hydroxybenzoate and methyl 2-

181

methoxybenzoate against adzuki bean weevil.24 Although the reason for difference between

182

these reports and ours could not be explained from this study, it may be attributed to the

183

permeability of the tested compounds thorough the cuticle or membrane of the tested insect

184

pests. That is because increase of hydrophobicity of a compound enables it to dissolve more

185

easily in the lipids of the cell membrane.27 8



186

3.3. Inhibition of acetylcholinesterase (AChE) and glutathione S-transferase (GST) activity

187

To evaluate the mode of actions of sparassol and its analogs, activities of AChE and

188

GST were assayed for each compound. Sparassol exhibited insignificant AChE inhibitory

189

activity in both sexes of SWD (data not shown). Methyl orsellinate and DMB showed 22.4-

190

31.7% inhibitory range against male and female SWD at the concentration of 1 mg/mL (data

191

not shown). However, values of IC50 based on the inhibition ratios showed that methyl

192

orsellinate inhibited AChE activity more strongly than DMB (Table 3).

193

Sparassol and methyl orsellinate were equally effective for GST inhibitory activity in

194

both sexes of SWD, while DMB exhibited less GST inhibitory activity in male adults of

195

SWD at the concentration of 1 mg/mL (data not shown). Values of IC50 based on the

196

inhibition ratios showed that methyl orsellinate inhibited GST activity more strongly than

197

sparassol and DMB (Table 4).

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Inhibition of AChE is one of the modes of actions of many insecticides such as

199

organophosphates and carbamates. A variety of compounds derived from plants and fungi are

200

also known to inhibit the AChE activity.28 But, little is known about inhibitors of insect GST,

201

which is partly responsible for the resistance development to some chemicals.29, 30 Inhibition

202

of AChE and GST by sparassol and its analogs was assayed to evaluate their mode of action.

203

DMB, which was most effective in contact toxicity showed lower AChE inhibitory activity

204

than methyl orsellinate, as well as lower GST inhibitory activity than sparassol and methyl

205

orsellinate in both sexes of SWD. In contrast, methyl orsellinate which showed lowest

206

contact toxicity (Table 1) inhibited the AChE and GST activities more strongly than DMB in

207

both sexes of SWD. The reason why DMB showed high contact toxicity but low enzyme

208

inhibitory activities could not be confirmed from this study. Probably, AChE and GST are not

209

the target sites of DMB. Toxicity of monoterpenoids and phenylpropanoids may not 9


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necessarily be correlated with ability of AChE inhibitory activity.18, 31, 32 α-Pinene, β-pinene

211

and limonene inhibited AChE of Japanese termite,32 for which they were weak in fumigant

212

activity.25 On the contrary to this, trans-cinnamyl alcohol which showed contact toxicity did

213

not inhibit AChE of SWD.18 Further investigations are required to identify the modes of

214

actions of DMB on SWD mortality. Polyhydroxylation substitutes of flavonoid was reported

215

to enhance their GST inhibitory potency in fall armyworm.29 This is also proved by our study

216

that the GST inhibitory activity was increased along with the number of hydroxy group of the

217

tested compound. The reason why methyl orsellinate showed the highest GST inhibitory

218

activity might be related to hydroxy group in the compound.

219

Abamectin derived from a soil actinomyces microorganism, Streptomes avermitillis,

220

is mainly used as an insecticide, acaricide, and nematicide.33, 34 Abamectin and its derivatives

221

are known as interacting with ion chloride channels, such as glutamate-gated chloride

222

channels (GluCls), γ-aminobutyric acid chloride channels and histamine-gated chloride

223

channels.35 To prevent resistance development and to achieve long lasting control of SWD,

224

diverse alternative agents which have different mode of actions should be employed.36

225

Although abamectin is effective and safe to the environment37, its extensive and continuous

226

use, like other groups of insecticides, could develop resistance to the agent.38, 39 In our study,

227

sparassol and its analogs showed lower contact toxicity against SWD adults than abamectin.

228

But, they showed AChE and GST inhibitory activities. Therefore we suggest the sparassol

229

and its analogs as the alternatives to prevent resistance development. Among the tested

230

compounds, DMB could be an effective, economic and comparative alternative to common

231

insecticides including abamectin as it can be synthesized easily from sparassol, the natural

232

compound from cultivated S. crispa or S. latifolia.

233

10



234

4. Conclusions

235

In conclusion, methyl 2,4-dimethoxy-6-methylbenoate (DMB) exhibited promising

236

contact toxicity against the adults of Drosophila suzukii. It could be an alternative agent for

237

controlling insect pests as it can be easily synthesized from sparassol which is produced as a

238

metabolite by the edible cauliflower mushroom, Sparassis species in culture. Thus the

239

Sparassis species could be an industrial resource of this compound.

240 241

Acknowledgements

242

MJ was supported by the BK21 plus program, Ministry of Education, Republic of Korea. We

243

appreciated to Prof. S. H. Lee (SNU) for valuable advice on enzyme inhibitory assay, and to

244

Mr. K. Chiluwal (GNU) for editing the manuscript.

245 246

Author Contribution

247

JK, KTL, CGP were conceived and designed the experiments; JK, MJ, KAY performed the

248

experiments; JK, MJ analyzed the data; JK, MJ, CGP wrote the paper.

249 250

Supporting Information

251

Supporting Information Available: [Synthetic methods and NMR spectra] This material is

252

available free of charge via the Internet at http://pubs.acs.org.

253 254

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ammi), allspice (Pimenta dioica), caraway (Carum carvi), dill (Anethum graveolens),

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American Chemical Society, https://scifinder.cas.org. (Accessed Feb. 01, 2016);

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16



372

Figure caption.

373

Fig. 1. Chemical structures of sparassol, methyl orsellinate, and methyl 2,4-dimethoxy-6-

374

methylbenzoate (DMB).

17


Page 18 of 24

Page 19 of 24

375 376

Table 1. Contact toxicity of sparassol and its analogs against SWD adults Sex Male

Female

377


1

Treatment

Mortality (%, Mean±SEM, N=5) at doses (µg/fly) 20

15

10

7.5

5

2.5

1.25

Sparassol

88.4±6.4

95.8±4.2

85.3±5.4

72.9±9.7

23.8±10.7

13.3±4.7

13.3±4.7

Methyl orsellinate

34.9±7.0

-

-

-

-

-

-

DMB1

97.7±2.3

97.9±2.1

100

100

100

95.8±2.6

37.5±5.7

Control

0

0

0

0

0

0

0

Sparassol

78.0±8.6

56.3±6.9

56.3±6.9

23.2±6.9

15.4±5.0

11.5±5.7

3.6±2.2

Methyl orsellinate

24.0±6.0

-

-

-

-

-

-

DMB

100

100

95.8±2.6

89.9±3.2

89.9±3.2

81.8±8.7

3.6±2.2

0

0

0

0

0

0

Control 0 DMB; Methyl 2,4-dimethoxy-6-methylbenzoate

18



378 379

Table 2. LD50 values for contact toxicity of sparassol, methyl orsellinate, methyl 2,4dimethoxy-6-methylbenzoate (DMB) and abamectin against SWD adults Sex

Treatment

LD50 (µg/fly)

95% cla (µg/fly)

slope±SE

χ2b (dfc)

Male

Sparassol

5.29bd

2.86–8.49

1.13±0.32

7.69 (33)

-

-

-

Female

380 381 382 383 384

Page 20 of 24

e

Methyl orsellinate

-

DMB

1.18a

0.02–2.19

1.20±0.51

5.01 (33)

Abamectin

0.02a

NA–0.22

0.27±0.14

2.5 (18)

Sparassol

11.14c

6.51–3.46

0.95±0.34

4.64 (33)

-

-

-

e

Methyl orsellinate

-

DMB

2.27b

0.91–3.57

1.46±0.47

5.17 (33)

Abamectin

0.05a

NA–0.39

0.34±0.15

3.37 (18)

a

Confidence limit, bPearson’s Chi-square goodness-of-fit test, cDegree of freedom, dThe same letters within a column in each sex are not significantly different when the 95% cl fail to overlap, eLD50 value could not be estimated because of low mortality, NA: not available.

19


Page 21 of 24

385 386


Table 3. IC50 values of AChE inhibitory activity of sparassol, methyl orsellinate, and methyl 2,4-dimethoxy-6-methylbenzoate (DMB) Slope±SE

χ2b (dfc)

2.07ae

1.51-3.27

0.60±0.06

17.30 (9)

DMB

6.78b

3.40-23.63

0.35±0.05

1.700 (9)

Sparassol

-

Methyl orsellinate

1.69a

1.34-2.49

0.86±0.13

2.541 (5)

Compound

IC50 (mg/mL)

Male

Sparassol

-d

Methyl orsellinate Female

387 388 389 390

95% cla

Sex

DMB 4.38b 2.67-10.05 0.50±0.07 4.534 (9) Confidence limit, bPearson’s Chi-square goodness-of-fit test, cDegree of freedom, dIC50 value could not be estimated because of low inhibition ratio, eThe same letters within a column in each sex are not significantly different when the 95% cl fail to overlap. a

20



391 392

Table 4. IC50 values of GST inhibitory activity of sparassol, methyl orsellinate and methyl 2,4-dimethoxy-6-methylbenzoate (DMB) Sex

Compound

IC50 (mg/mL)

95% cla

Slope±SE

χ2b (dfc)

Male

Sparassol

0.24ad

0.20-0.30

0.60±0.07

83.98 (3)

Methyl orsellinate

0.18a

0.13-0.23

0.39±0.05

15.36 (6)

DMB

2.34b

1.21-8.84

0.28±0.05

56.66 (6)

Sparassol

0.69a

0.43-1.86

0.31±0.07

9.27 (3)

Methyl orsellinate

0.80a

0.55-1.42

0.31±0.07

49.33 (3)

DMB

1.34a

0.98-2.11

0.44±0.05

95.73 (7)

Female

393 394 395

Page 22 of 24

a

b

c

d

Confidence limit, Pearson’s Chi-square goodness-of-fit test, Degree of freedom, The same letters within a column in each sex are not significantly different when the 95% cl fail to overlap.

21


Page 23 of 24


396 397

Fig. 1. Chemical structures of sparassol, methyl orsellinate, and methyl 2,4-dimethoxy-6-

398

methylbenzoate (DMB).

399

22



400

Graphical Abstract

401 402

23


Page 24 of 24

Insecticidal and Enzyme Inhibitory Activities of ... - ACS Publications

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