Eucommia ulmoides Oliver: A Potential Feedstock for Bioactive Products

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Eucommia ulmoides Oliver: a Potential Feedstock for Bioactive Products Ming-Qiang Zhu, and Run-Cang Sun J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.8b01312 • Publication Date (Web): 10 May 2018 Downloaded from http://pubs.acs.org on May 12, 2018

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Journal of Agricultural and Food Chemistry

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Eucommia ulmoides Oliver: a Potential Feedstock for Bioactive Products

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Ming-Qiang Zhu†‡, Run-Cang Sun ‡*

3 4 5

†

6

Utilization of Rural Renewable Energy, Northwest A&F University, Yangling, China.

7

‡

8

Western Scientific Observation and Experiment Station of Development and

Beijing Key Laboratory of Lignocellulosic Chemistry, Beijing Forestry University, Beijing, China.

9 10 11 12 13 14 15 16 17

*To whom correspondence should be addressed. Beijing Forestry University, Beijing

18

Key Laboratory of Lignocellulosic Chemistry, Beijing 100083, China. Tel: +86 10

19

62336972; fax: +86 10 62336972 (R.C. Sun).

20

E-mail address: [email protected].

ACS Paragon Plus Environment


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ABSTRACT:

22 23

Eucommia ulmoides Oliver (EUO), a traditional Chinese herb, contains a variety of

24

bioactive chemicals including lignans, iridoids, phenolics, steroids, terpenoids,

25

flavonoids, etc. These bioactive chemicals possess the effective function in nourishing

26

liver and kidney and regulating blood pressure. The composition of bioactive

27

chemicals extracted from EUO vary to the different functional parts (leaves, seeds,

28

bark and staminate flower) and planting models. The bioactive parts of EUO are

29

widely utilized as raw materials for medicine and food, powdery extracts, herbal

30

foumulations and tinctured extracts. These capabilities hold potential for future

31

development and commercial exploitation of the bioactive products from EUO.

32 33

KEYWORDS: Eucommia ulmoides Oliver; Phytochemistry; Biological activities;

34

Bioactive products.


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■ INTRODUCTION

36

Eucommia ulmoides Oliver (EUO) is named as Dù-zhòng (in Chinese), Yusipi, Gutta

37

percha tree, Sizhong, and Sixian with a long history in the Chinese medical classic

38

Shen Nong Ben Cao Jing and Ben Cao Gang Mu.1 It is a unique deciduous and

39

dioecious tree belonging to the genus Eucommia, the sole member of the family

40

Eucommiaceae. EUO tree has been widely cultivated in wide area of China at an

41

altitude range of 300-1300 m such as Shanxi, Neimeng, Xinjiang, Gansu, Zhejiang,

42

Henan, Hubei, Sichuan, Guizhou, and Yunnan province.2 Simultaneously, a limited

43

number of EUO has also been planted in Japan, Korea, and some other countries. As

44

listed in the traditional Chinese medicine (TCM), the bark, cortex Eucommiae,

45

together with its leaves, folium Eucommiae, have been listed in “China

46

Pharmacopoeia” 3. With the pharmacological activities, the EUO were used as a tonic

47

for liver and kidney, preventing miscarriage and senescence, regulating blood

48

pressure etc.4, 5 In China, the extracts of the aerial parts of EUO have been widely

49

used as popular botanical tonics and antirheumatic supplements since 2000 years ago.

50

It can be used alone or mixed with other Chinese medicinal materials in the

51

prescription

52

spermatorrhoea, prospermia, forgetfulness, osteoporosis, menopause syndrome,

53

hypertension, rheumatoid arthritis, lumbago, ischialgia, aching knees, kidney

54

deficiency pain, weak bones, bone fractures and joint diseases, and lower back pain. 3

of

traditional

Chinese

medicine

(TCM)

to

treat

impotence,

55

In modern pharmacology, the in vivo and in vitro activities of EUO against

56

hypertension, osteoporosis, hyperglycemia, obesity, Alzheimer's disease, aging,

57

diabetes, and sexual dysfunction have garnered much attention.

58

researches on the chemical components of EUO have guided the identification of 138

59

chemical compounds, which include lignans, flavonoids, iridoids, phenolics, steroids,


5-10

The extensive


11

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60

terpenoids, and guttapercha.

61

two major constituents which are normally used as key chemotaxonomic markers.

62

The

63

di-O-β-D-glucopyranoside,

64

anti-hypertensive effects; aucubin, genipin, and geniposidic acid are the major

65

components of iridoids with properties of anti-hypertensive and anti-aging. Recently,

66

the aqueous extract of EUO, widely known as EUO tea, is a favorite beverage in

67

Asian countries and has also been utilized as a superfood, with special function for

68

remission of hypertension. 9 As a potential feedstock, EUO has rich natural bioactive

69

ingredients with multiple functions for healthcare, which prompt the development and

70

utilization of EUO as human health food, drug and animal feed additives. Moreover,

71

EUO also has commercial benefits as the tree can be used to manufacture guttapercha,

72

which can be extracted from the entire parts of certain tissues or organs (such as seed

73

coats, bark, root bark, and leaves) of EUO tree. The guttapercha is resistant to acids

74

and alkalies and then is extensively used as electrical insulation and filling material of

75

false tooth. 12, 13

primary

Among these compounds, lignans and iridoids are the

components and

of

lignans,

liriodendrin,

(+)-syringaresinol

were

(+)-pinoresinol

exhibited

to

show

76

Up to now, a lot of research work are still needed to be done to clarify which

77

compound has a distinct effect on a disease or which compounds should work

78

together for treating diseases. The purpose of the perspective is to systematically

79

summarize the botanical description, ethnopharmacology, phytochemistry, and

80

biological activities of EUO and to discuss possible trends for further research and the

81

industrial exploitation of the bioactive products of EUO.

82 83

■ THE USEFULL PARTS OF EUO TREE FOR BIOACTIVE APPLICATION

84

The functional parts of EUO including the bark, leaves, seeds, and flowers can be


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applied as the feedstocks for production of bioactive materials in the industrial scale

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(Table 1 and Figure 1). 5, 14, 15, 16

87

The EUO bark is beige and rough. The leaves that grow alternately, are single and

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egg shaped with length of 5–21 cm and width of 3–15 cm, and have a serrated margin

89

and acuminate tip. When a leaf is torn across, strands of latex that are observed from

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the leaf veins form the guttapercha to keep the different parts of the leaf together.

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Strands of latex can also be found after the bark is broken and can be used to identify

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the material in TCM. The leaves of this tree can be converted into refined powder and

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then widely used as functional food with anti-obesity properties in China and Japan.

94

The EUO seeds can be refined to obtain oil and guttapercha 12. The seed oil, with

95

rich in linoleic acid and α-linolenic acid, is proved with high physiological and

96

antioxidant activities

97

supplement or nutritional vegetable oil 12.

16

. Therefore, it has great potential to be exploited as food

98

The flower of EUO is monotropic, inconspicuous, small, and greenish and displays

99

heterothallism, stamen of up to 1 cm, and female flower of up to 8 mm. The staminate

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flower simultaneously bloom before the germination of the leaf during the April with

101

abundance of flavonoid, vitamins and amino acids. Therefore, it is very worthful to be

102

processed into natural food supplement (such as flower tea, oral liquid and capsule),

103

which are proved with pharmacological effects for treatment of

104

immunity promotion 4, 17.

sedation and

105

Notably, the widely-used EUO planting model include arbor forest model,

106

orchard-like model, male flower model, bark coppice model and leaf-using model

107

(Figure 2). These EUO planting models supply plenty of feedstocks for further

108

utilization. This perspective describe an approach to convert the leaves, bark, seeds

109

and flower from EUO into high value-added products such as function food, drugs



18

110

and animal feed additives.

111

pharmacological actions of EUO should be identified.

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Primarily, the chemical components and relative

112 113

■ PHYTOCHEMISTRY

114

A total of 138 kinds of chemical compounds are identified from EUO bark and

115

leaves and include 32 lignans, 29 iridoids, 27 phenolics, 6 steroids, 10 terpenoids, 18

116

flavonoids and 16 other compounds (Figure 1). 5, 11, 19

117

As a representative of a class of secondary metabolites, lignans and their

118

derivatives are the main chemical compounds of EUO. Lignans consist of two

119

phenyl-propanoid

120

bisepoxylignans, monoepoxylignans, neolignans and sesquilignans, which have been

121

extracted mainly from the bark, and little amount can also be detected in seeds and

122

leaves of EUO.20, 21 The perfusion experiment proved that lignan fractions isolated

123

from EUO can rapidly relax mesenteric arteries in a dose-dependent fashion. This

124

phenomenon indicated that lignan fractions of EUO may effectively lower blood

125

pressure, which is most likely associated with regulation of nitric oxide and the renin–

126

angiotensin system, and directly relaxing arteries.

127

serve as a new therapeutic agent for treating hypertension by improving vascular

128

remodeling. 23

molecules

connected

by

8-8′

22

carbon

atoms,

including

Therefore, lignans of EUO may

129

Iridoid glycosides are also the main component of EUO as typical monoterpenoid

130

with a glucose moiety attached to C1 in the pyran ring. 29 iridoids have been isolated

131

and identified from EUO. Among these compounds, geniposidic acid, aucubin and

132

asperuloside have been confirmed to possess various pharmacological activities in

133

vivo and in vitro. A previous research isolated and identified 17 components from

134

Tochu tea including five iridoids with an α-unsaturated carbonyl group (geniposide,


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135

geniposidic acid, deacetyl asperulosidic acid, asperulosidic acid, and asperuloside),

136

and three phenols (pyrogallol, protocatechuic acid, and p-trans-coumaric acid) that

137

had significant anti-clastogenic activity. 5, 24

138

As a major group of nonessential dietary components, phenolics possess the

139

functions such as antioxidant, antimutagenic, anti-inflammatory, and anticancer

140

activities. Up to now, 27 phenolics have been isolated and identified from EUO.

141

Among them, chlorogenic acid, with neuroprotective effects, has been regularly

142

utilized as the standard marker for EUO and its medicinal extracts and preparations. 25

143

Only six steroids and ten terpenoids have been purified and characterized from

144

EUO.5 These compounds include β-sitosterol, daucosterol, ulmoprenol, betalin,

145

betulic

146

7α-tetrahydro-7-hydroxymethyl-cyclopenta [c] pyran-4-carboxylic methyl ester,

147

which were extracted from the EUO bark by Hua et al. 26 Loliolide has been separated

148

from the leaves of EUO by Okada et al. 27

acid,

ursolic

acid,

eucommidiol,

rehmaglutin

C

and

1,

4α,

5,

149

As very common and important secondary metabolites in nature, to date, 18

150

flavonoids have been extracted and identified from the bark, leaves and seeds of EUO,

151

28

152

kaempferol 3-O-rutinoside, astragalin, quercetin, quercetin 3-O-sambubioside,

153

quercetin

154

pyranosyl-(1-2)-β-D-glucopyranoside, isoquercetin, rutin, hirsutin and wogonside.

155 156

These compounds inlcude kaempferol, kaempferol 3-O-6″-acetyl-glucoside,

3-O-galactoside

(hyperin),

quercetin

3-O-α-L-arabino-

Fatty acids, polysaccharides, amino acids, microelements, vitamins, and gutta-percha have also been identified from EUO.

8

In a previous research, two new



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157

polysaccharides named eucomman A and eucomman B, were isolated by Tomoda et

158

al.

159

tetraeosanoie-2, 3-dihydroxy- propylester were isolated from EUO.

30

160

(αR)-α-O-β-D-glucopyranosyl-4,2′,4′-trihydroxy-dihydrochalcone,

4,

161

4′-trihy-droxychalcone,

162

isolated from the bark of EUO.

163

acids from the seed oil of EUO by using fraction chain length and mass spectrometry.

164

The main components of polyunsaturated fatty acids are α-linolenic acid (57 % of

165

total fatty acids, TFAs) and linolelaidic acid (13 % of TFAs). Simultaneously, oleic

166

acid (16 % of TFAs) was identified as the main monounsaturated fatty acid. The

167

dominant saturated fatty acids are palmitic acid (10 % of TFAs) and stearic acid (3 %

168

of TFAs). 31

29

A publication also showed that ethylglucopyranoside, n-oetaeosanoic acid, and

and

Recently,

(αR)-α,4,2′,4′-tetrahydroxy-dihydrochalcone 5

Zhang et al.

31

2′, were

analyzed the constituents of fatty

169 170

■ BIOLOGICAL ACTIVITIES

171

The ways of utilization bioactive parts of EUO are presented in the form as the

172

following (Figure 1):

173

1) Raw material for medicine and food - The plant raw material, such as the bark

174

usually used in large pieces to avoid the exsiccation of the latex substance for

175

Chinese medicine, the leaves and flower normally used in the initial state for

176

superfood, the seeds need to separate the kernel from the shell and serve as

177

functional oil.

178

2) The powdery extracts - These are water extracts that are dissolved, separated,

179

purified and dried into powder for further utilization as a bulk powder, capsule


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or tablet. 3) Herbal formulations - These are herbal preparations applying EUO extracts as either the primary or secondary ingredient. 4) Tinctured extracts - A liquid solution prepared by extracting EUO in ethanol to refine its bioactive ingredients.

185

The pharmacological actions of EUO have gained much attention on account of the

186

chemical components. Recently, EUO has been used in anti-hypertensive,

187

hypolipidemic,

188

anti-inflammatory, anti-viral and anti-bacterial, neuroprotective, antioxidative,

189

improving erectile function, anti-fatigue, anti-aging, anti-tumor, hepatoprotective,

190

enhancing immune-function activities and so on.

191

treating the diseases is still not be fully acknowledged or understood due to

192

complexity of the chemical components from EUO. Several fundamental principles of

193

the activities of the EUO compounds still remain uncovered including: 1) what the

194

active ingredients of the EUO are; 2) what explicit functions the active ingredients

195

possess; and 3) how these active ingredients exert effects on various diseases.

196

Therefore, it is worth doing further research about which active ingredient has a

197

distinct effect on a disease or which compounds should work together for treating

198

diseases.

anti-obesity,

anti-diabetic,

effect

10, 32-35

on

bone

metabolism,

Actually, the mechanism for

199 200

■ FUTURE DEVELOPMENT OF BIOACTIVE PRODUCTS

201

The bark and leaves of EUO have been recorded in the Pharmacopoeia of China. The

202

leaves of EUO have been used for treating diabetes and anti-obesity and have also

203

been used commonly as a popular beverage and/or health food. Even the staminate



204

flower has been widely used to prepare tea and/or nutraceuticals. Almost all aerial

205

parts of EUO can be used for health care. Thus, EUO tree is one of the most

206

promising plants and stimulates agricultural and industrial economics in the following

207

points (Figure 3).

208

For pharmaceuticals, since the EUO bark and leaves are commonly known to help

209

strengthen sinews and bones and alleviate fatigue, regulate blood pressure and remit

210

Alzheimer's disease, in the future, the bioactive extracts of EUO can be widely used

211

to synthesize targeted drugs for anti-hypertensive, anti-obesity, and anti-diabetic

212

activities.

213

For superfood, the EUO leaves have been listed as new basic food sources instead

214

of herb sources in China since 2018. Thus, it can be been used as a functional food or

215

diet supplement in the future. Due to the abundant content of α-linolenic acid in EUO

216

seeds kernel, it can be processed to produce superfood such as soft capsules and

217

nutrient oil. EUO male flowers are also rich in nutrients and bioactive constituents

218

and can be developed as nutrition tea.

219

For animal feed additives, with the properties of anti-viral and anti-bacterial

220

activities, EUO leaves and bark can be used as additives in animal feed to cut down

221

the dose usage of the hormones and antibiotics during the breeding process. EUO has

222

been used as feed additives for hens in China, the eggs produced with high quality are

223

rich in vitamins and amino acids.

224

For cosmetics, EUO extracts can also be used as feedstock for producing cosmetic

225

products such as facial mask and cream with functions of antioxidative activity and


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ati-aging activity.

227 228

■ ACKNOWLEDGEMENTS

229

The authors wish to express their gratitude for the financial support from Northwest

230

A&F University Education Development Foundation (A289021701), the State

231

Forestry Administration of China (948-2015459), and China Youth Science and

232

Technology Innovation Award Projects (10900-A189021502).

233 234

■ REFERENCES

235

(1) Cronquist, A., An integrated system of classification of flowering plants.

236

Columbia University Press: 1981.

237

(2) Nakazawa, Y.; Toda, Y., Eucommia ulmoides Oliv. (Eucommiaceae): In vitro

238

culture and the production of Iridoids, lignans, and other secondary metabolites. In

239

Medicinal and Aromatic Plants VIII, Bajaj, Y. P. S., (Ed), Biotechnology in

240

Agriculture and Forestry, Springer Berlin Heidelberg. 1995, pp 215-231.

241

(3) Committee, N.P. Chinese pharmacopoeia. China Med. Sc. Press, Beijing, 2010, pp

242

154-155.

243

(4) Dong, J. E.; Ma, X. H.; Fu, Z. R.; Guo, Y., Effects of microwave drying on the

244

contents of functional constituents of Eucommia ulmoides flower tea. Ind. Crop. Prod.

245

2011, 34, 1102-1110.

246

(5) He, X. R.; Wang, J. H.; Li, M. X.; Hao, D. J.; Yang, Y.; Zhang, C. L.; He, R.; Tao,

247

R.

248

pharmacology of an important traditional Chinese medicine. J. Ethnopharmacol. 2014,

Eucommia

ulmoides

Oliv.:

Ethnopharmacology,


phytochemistry

and


249

151, 78-92.

250

(6) Bai, M. M.; Shi, W.; Tian, J. M.; Lei, M.; Kim, J. H.; Sun, Y. N.; Kim, Y. H.; Gao,

251

J. M. Soluble epoxide hydrolase inhibitory and anti-inflammatory components from

252

the leaves of Eucommia ulmoides Oliver (Duzhong). J. Agric. Food Chem. 2015, 63,

253

2198-2205.

254

(7) Luo, D.; Or, T. C. T.; Yang, C. L. H.; Lau, A. S. Y., Anti-inflammatory activity of

255

iridoid and catechol derivatives from Eucommia ulmoides Oliver. Acs Chem. Neurosci.

256

2014, 5, 855-866.

257

(8) Li, Q.; Feng, Y.; He, W.; Wang, L.; Wang, R.; Dong, L.; Wang, C., Post-screening

258

characterisation and in vivo evaluation of an anti-inflammatory polysaccharide

259

fraction from Eucommia ulmoides. Carbohyd. Polym. 2017, 169, 304-314.

260

(9) Hosoo, S.; Koyama, M.; Watanabe, A.; Ishida, R.; Hirata, T.; Yamaguchi, Y.;

261

Yamasaki, H.; Wada, K.; Higashi, Y.; Nakamura, K., Preventive effect of Eucommia

262

leaf extract on aortic media hypertrophy in Wistar-Kyoto rats fed a high-fat diet.

263

Hypertens. Res. 2017, 40, 546-551.

264

(10) Cho, S.; Hong, R.; Yim, P.; Yeom, M.; Lee, B.; Yang, W. M.; Hong, J.; Lee, H. S.;

265

Hahm, D. H., An herbal formula consisting of Schisandra chinensis (Turcz.) Baill,

266

Lycium chinense Mill and Eucommia ulmoides Oliv alleviates disuse muscle atrophy

267

in rats. J. Ethnopharmacol. 2018, 213, 328-339.

268

(11) Zhang, Y. P.; Peng, M. J.; Liu, L. L.; Shi, S. Y.; Peng, S., Screening, identification,

269

and potential interaction of active compounds from Eucommia ulmodies leaves

270

binding with bovine serum albumin. J. Agric. Food Chem. 2012, 60, 3119-3125.


Page 12 of 21

Page 13 of 21


271

(12) Su, Y. Q.; Ren, Z.; Du, S. T.; Chi, M.; Ding, F. X.; Nakazawa, Y.; Tsutsumi, M.;

272

Lu, T. Screening parameters for the extraction of Eucommia rubber (EU-rubber) by

273

microbial solid fermentation. J. Northwest Agr. For. Univ. 2010, 38, 155-160.

274

(13) Zhu, M. Q.; Wen, J. L.; Zhu, Y. H.; Su, Y. Q.; Sun, R. C. Isolation and analysis of

275

four constituents from barks and leaves of Eucommia ulmoides Oliver by a multi-step

276

process. Ind. Crops Prod. 2016, 83, 124-132.

277

(14) Dong, J. E.; Ma, X. H.; Wei, Q.; Peng, S. B.; Zhang, S. C. Effects of growing

278

location on the contents of secondary metabolites in the leaves of four selected

279

superior clones of Eucommia ulmoides. Ind. Crops Prod. 2011, 34, 1607-1614.

280

(15) Deyama T.; Nishibe S.; Nakazawa Y., Constituents and pharmacological effects

281

of Eucommia and Siberian ginseng. Acta Pharmacol Sin 2001, 22, 1057-1070.

282

(16) Liang, S. F.; Zhang, K. J., Chemical constituents of Eucommia fruit. J. Northwest

283

For. Coll. 1997, 12, 43-47.

284

(17) Huang, H. Y.; Du, H. Y.; Li, Q.; Fu, J. M.; Du, N. Y.; Ma, Y. F., Promotion of the

285

function of inhibited mouse lymphocyte by aqueous extracts of Eucommia male

286

flower. Chin. Med. Mater. 2010, 33, 231-235.

287

(18) Xu, Z.; Tang, M.; Li, Y.; Liu, F.; Li, X.; Dai, R., Antioxidant properties of

288

Du-zhong (Eucommia ulmoides Oliv.) extracts and their effects on color stability and

289

lipid oxidation of raw pork patties. J. Agric. Food Chem. 2010, 58, 7289-7296.

290

(19) He, M.; Jia, J.; Li, J.; Wu, B.; Huang, W.; Liu, M.; Li, Y.; Yang, S.; Ouyang, H.;

291

Feng, Y., Application of characteristic ion filtering with ultra-high performance liquid

292

chromatography quadrupole time of flight tandem mass spectrometry for rapid



Page 14 of 21

293

detection and identification of chemical profiling in Eucommia ulmoides Oliv. J.

294

Chromatogr. A 2018, 1554, 81-91.

295

(20) Moss, G., Nomenclature of lignans and neolignans (IUPAC Recommendations

296

2000). Pure Appl. Chem. 2000, 72, 1493-1523.

297

(21) Lourith, N.; Katayama, T.; Suzuki, T., Stereochemistry and biosynthesis of 8-O-4′

298

neolignans

299

guaiacylglycerol-8-O-4′-(sinapyl alcohol) ether. J. Wood Sci. 2005, 51, 370-378.

300

(22) Luo, L. F.; Wu, W. H.; Zhou, Y. J.; Yan, J.; Yang, G. P.; Ouyang, D. S.,

301

Antihypertensive effect of Eucommia ulmoides Oliv. extracts in spontaneously

302

hypertensive rats. J. Ethnopharmacol. 2010, 129, 238-243.

303

(23) Li, C. P.; Qiu, G. Z.; Liu, B.; Chen, J. L.; Fu, H. T., Neuroprotective effect of

304

lignans

305

neurodegeneration. Neurol. Sci. 2016, 37, 755-762.

306

(24) Nakamura, T.; Nakazawa, Y.; Onizuka, S.; Satoh, S.; Chiba, A.; Sekihashi, K.;

307

Miura, A.; Yasugahira, N.; Sasaki, Y. F., Antimutagenicity of Tochu tea (an aqueous

308

extract of Eucommia ulmoides leaves) .1. The clastogen-suppressing effects of Tochu

309

tea in CHO cells and mice. Mutat. Res-gen. Tox. En. 1997, 388, 7-20.

310

(25) Zhou, Y. Q.; Liang, M.; Li, W. Z.; Li, K.; Li, P.; Hu, Y. Z.; Yang, Z. L., Protective

311

effects of Eucommia ulmoides Oliv. bark and leaf on amyloid beta-induced

312

cytotoxicity. Environ. Toxicol. Phar. 2009, 28, 342-349.

313

(26) Hua, H. M.; Yin, H. Q.; Li, B. Q.; Pei, Y. H, Study on the constituents of the bark

314

of Eucommia ulmoides. Mol. Plant Breeding 2003, 1, 801-803.

in

extracted

Eucommia

from

ulmoides:

Eucommia

diastereoselective

ulmoides

Oliv.


on

formation

of

glaucoma-related

Page 15 of 21


315

(27) Okada, N.; Shirata, K.; Niwano, M.; Koshino, H.; Uramoto, M.,

316

Immunosuppressive

317

Phytochemistry 1994, 37, 281-282.

318

(28) Chai, X.; Wang, Y. F.; Su, Y. F.; Bah, A. J.; Hu, L. M.; Gao, Y.; Gao, X. M., A

319

rapid ultra performance liquid chromatography-tandem mass spectrometric method

320

for the qualitative and quantitative analysis of ten compounds in Eucommia ulmodies

321

Oliv. J. Pharmaceut. Biomed. 2012, 57, 52-61.

322

(29) Tomoda, M.; Shimizu, N.; Ohara, N.; Gonda, R.; Ishii, S.; Otsuki, H., A

323

Reticuloendothelial

324

Astragalus-Membranaceus. Phytochemistry 1992, 31, 63-66.

325

(30) Sun, Y.; Dong, J.; Wu, S., Studies on chemical constituents from Eucommia

326

ulmoides Oliv. J. Chinese Med. Mater. 2004, 27, 341-3.

327

(31) Zhang, L. X.; Ji, X. Y.; Tan, B. B.; Liang, Y. Z.; Liang, N. N.; Wang, X.L.; Dai,

328

H., Identification of the composition of fatty acids in Eucommia ulmoides seed oil by

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fraction chain length and mass spectrometry. Food Chem. 2010, 121, 815-819.

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(32) Lee, G. H.; Lee, H. Y.; Choi, M. K.; Choi, A. H.; Shin, T. S.; Chae, H. J.,

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Eucommia ulmoides leaf (EUL) extract enhances NO production in ox-LDL-treated

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human endothelial cells. Biomed. Pharmacother. 2018, 97, 1164-1172.

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(33) Fujiwara, A.; Nishi, M.; Yoshida, S.; Hasegawa, M.; Yasuma, C.; Ryo, A.; Suzuki,

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Y., Eucommicin A, a beta-truxinate lignan from Eucommia ulmoides, is a selective

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inhibitor of cancer stem cells. Phytochemistry 2016, 122, 139-145.

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(34) Hussain, T.; Tan, B.; Rahu, N.; Hussain Kalhoro, D.; Dad, R.; Yin, Y., P 067 -

activity

of a

monoterpene

System-Activating

from Eucommia

Glycan


from

the

ulmoides.

Roots

of


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Protective mechanism of Eucommia ulmoids flavone (EUF) on enterocyte damage

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induced by LPS. Free Radical Bio. Med. 2017, 108, S40.

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(35) Liu, H. W.; Li, K.; Zhao, J. S.; Deng, W., Effects of polyphenolic extract from

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Eucommia ulmoides Oliver leaf on growth performance, digestibility, rumen

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fermentation and antioxidant status of fattening lambs. Anim. Sci. J. 2018, 238, 47-56.

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Figure Captions

345 346 347

Figure 1. The chemical compounds and biological activities from bioactive parts of

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EUO.

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Figure 2. The five different planting model of Eucommia ulmoides Oliver and

350

corresponding products.

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Figure 3. Bright ﬁeld images of EUO cross-section.


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Figure 1.



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Figure 2.


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Figure 3.



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Table 1

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The chemical components of secondary metabolite in different parts from EUO (%)

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Gutta-percha Bark Leaves Fruits Male Flower

1.84 1.43 8.25

Aucubin (A) 1.14 1.34 7.90 1.13

Chlorogenic acid (B) 0.41 1.75 0.20 1.11

Flavonoids (C) 0.36 1.67 0.30 1.82

Total (A+B+C) 1.91 4.76 8.41 4.06

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Notes: The secondary metabolite of bark and leaves are measured based on the mean

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value of male and female individuals. The value of fruits are measured based on the

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mean of female trees; and the value obtained from the male flowers based on the

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mean of male trees.

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Graphic for Manuscript

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Eucommia ulmoides Oliver: a Potential Feedstock for Bioactive Products

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Eucommia ulmoides Oliver: A Potential Feedstock for Bioactive Products

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