Horizontal Natural Product Transfer: Intriguing ... - ACS Publications

Subscriber access provided by BUFFALO STATE

Perspective

Horizontal Natural Product Transfer: Intriguing Insights into a Newly Discovered Phenomenon Dirk Selmar, Alzahraa Radwan, Tahani Hijazin, Sara Abouzeid, Mahdi Yahyazadeh, Laura Lewerenz, Maik Kleinwächter, and Melanie Nowak J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.9b03619 • Publication Date (Web): 23 Jul 2019 Downloaded from pubs.acs.org on July 23, 2019

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 23

Journal of Agricultural and Food Chemistry

acceptor plant

donor plant

transfer from rotting plants

transfer from living plants natural products derived from donor plants: derivatives of the imported substances: ACS Paragon Plus Environment

modification


Page 2 of 23

umbelliferone

uptake from the soil

modification H

esculetin

garden cress

barley

H3C-O

glucose glucose- O

scopoletin ACS Paragon Plus Environment

esculin

Page 3 of 23


Table 1: Uptake of natural products by acceptor plants

type

plant

literature

caffeine

purine alkaloid

barley

13

theobromine

purine alkaloid

barley

13

theophylline

purine alkaloid

barley

13

erucifoline

pyrrolizidine alkaloid

chamomile, peppermint melissa, parsley

11, 29

jacobine


chamomile, peppermint melissa, nasturtium, parsley

11, 29

monocrotaline


barley

seneciphylline



11, 29

senecionine



29

nicotine

nicotine alkaloid

parsley, chamomile

9, 10

atropine

tropane alkaloid

barley

13

noscapine

isoquinioline alkaloid

barley

13

papaverine


barley

13

harmaline

indole alkaloid

barley

our current research

harmine

indole alkaloid

barley


strychnine

indole alkaloid

barley

13

vincamine

indole alkaloid

barley


betanidine

betalain

barley, pea

16

resveratrol

stilbene

barley

15; 49

coumarin

barley, flax, radish

14

umbelliferone

pea, garden cress

ACS Paragon Plus Environment



1

Perspective

2

Horizontal Natural Product Transfer:

3

Intriguing Insights into a Newly Discovered Phenomenon

4 5

Dirk Selmar 1)*, Alzahraa Radwan 1), Tahani Hijazin1) , Sara Abouzeid 1) 2),

6

Mahdi Yahyazadeh 1), Laura Lewerenz 1), Maik Kleinwächter 1) 3), Melanie Nowak 1)

7 8

1)

TU Braunschweig, Institute for Plant Biology, Mendelssohnstr. 4, 38106 Braunschweig, Germany

2)

Present address: Pharmacognosy Department, Faculty of Pharmacy, Mansoura University, Mansoura, Egypt

12

3)

Present address: Repha GmbH, 30855 Langenhagen, Germany

13

* corresponding author: [email protected];

9 10 11

Tel: +49-(0)-531-391-5991

14 15


Page 4 of 23

Page 5 of 23


17

Abstract

18

Just recently, the ”Horizontal Natural Product Transfer” was unveiled: alkaloids, which have

19

been leached out from decomposing alkaloidal donor plants, are taken up by the roots of

20

acceptor plants. In the same manner, many other natural products, such as coumarins or

21

stilbenes, are also taken up from the soil. Recent research outlined that alkaloids are

22

transferred also from living donor into plants growing in their vicinity. In the acceptor plants

23

the imported natural products might be modified by hydroxylation and glucosylation. These

24

insights will strongly impact our understanding of contamination of plant derived

25

commodities as well as of plant-plant interaction.

26 27

Keywords:

28

horizontal transfer; natural products; pyrrolizidine alkaloids; alkaloids; coumarins;

29

allelopathy; xenobiotics.

30



32

Introduction

33

We all are aware that plants take up numerous substances from the soil; apart from inorganic

34

nutrients, many other compounds are imported by roots. With regard to chemical ecology, the

35

uptake of allelochemicals, i.e., substances affecting germination or growth of putative

36

competitors are of special interest. These substances, which are frequently exuded from donor

37

plants, exhibit their effect on plants growing in the vicinity 1,2. This however, requires an

38

uptake of the allelochemicals into the acceptor plants. In the same manner, another group of

39

compounds, i.e., xenobiotics such as systemic herbicides or fungicides, is also known to be

40

imported into plants 3. After their uptake by the roots, these compounds are generally

41

translocated into the shoots. Although the uptake of xenobiotics was well established, it was

42

never considered that typical plant-derived natural products, which are leached out from

43

rotting plant materials, could also be taken up analogously. Yet, the situation changed when it

44

became evident that a large number of plant-derived commodities are contaminated by toxic

45

alkaloids 4, 5 and the related path of contamination had been studied. Pyrrolizidine are known

46

to poison livestock, wildlife, and humans 6, 7. In the liver of vertebrates, PAs are oxidized to

47

unstable dehydropyrrolizidine alkaloids, also denoted as PA pyrroles 8.

48

The uptake of natural products from the soil

49

To identify the potential sources of the widespread alkaloid contaminations, various research

50

projects had been launched. Foremost, pot experiments unveiled that nicotine leached out

51

from dried tobacco material, was taken up by all plants tested 9. Hereafter, field experiments

52

manifested that nicotine, which was washed out into the soil from discarded cigarette butts,

53

was efficiently taken up by crop plants 10. Even one cigarette butt per square meter suffices to

54

tenfold exceed the limit value set by the EU 10. In the same manner, pyrrolizidine alkaloids

55

(PAs), which are derived from rotting PA-containing weeds, e.g. Senecio jacobaea, are also

56

imported into acceptor plants 11. Thus, the transfer of alkaloids is – at least in part –


Page 6 of 23

Page 7 of 23


57

responsible for the numerous and widespread alkaloidal contaminations of plant-derived

58

commodities 12.

59

Meanwhile the uptake of many other alkaloids from the soil 13 as well as of other natural

60

products such as coumarins 14 or stilbenes 15 had been verified (Table 1). The insights and

61

coherences constitute the basis for the concept of the “Horizontal natural product transfer” 12,

62

16,

63

decomposing plant parts - denoted as donor plants – these compounds are taken up by the

64

roots of other plants. Due to the general underlying mechanisms, all plants will take up these

65

substances; therefore they are denoted as acceptor plants. Subsequently after their uptake by

66

the roots, the substances are translocated via xylem into the leaves 16, 25.

67

In the course of this transfer, the substances have to pass the plasmalemma of root cells. In

68

contrast to the import of most ionic nutrients like nitrate, sulfate or metal ions, which requires

69

specific transporters 17, most of the xenobiotics diffuse passively through biomembranes, i.e.,

70

they are taken up by simple diffusion 3. However, a prerequisite for such diffusion is the

71

solubility of the substance in aqueous as well as in organic media. Accordingly, the ability for

72

a passive membrane transfer can roughly be estimated from the so-called KOW value,

73

representing the distribution coefficient of a substance between octanol and water, or its

74

decadal logarithm pKOW 18, which is frequently also denoted as logP 19. Substances revealing

75

logP values between -1 and 3 are generally considered to be able to diffuse easily through

76

biomembranes 20. Indeed, these coherences had been elaborated for the uptake of xenobiotics,

77

but they also apply for all natural products. This is in accordance with the analyses of Hurtado

78

et al. 21, who demonstrated that, many so-called “emerging organic contaminants” are taken

79

up by lettuce plants. Accordingly these authors confirmed that many different classes of

80

organic compounds are able to pass biomembranes. In this sense, also the uptake of

81

allelochemicals such as biochanin A or benzoxazolinone (BOA) has to be noted 22, 23.

which is displayed in Figure 1. When natural products are leached out into the soil from



82

Yahyazadeh et al. 13 reported that – as predicted - all alkaloids exhibiting a logP between -1

83

and 3 are taken up, too. In analogy to nicotine and PAs, also tropane and purine alkaloids as

84

well as benzylisoquinoline and indole alkaloids were imported by the roots of acceptor plants

85

and transferred into their leaves 13. In contrast, quaternary alkaloids such as coptisine,

86

palmatine, or berberine are not taken up, putatively because of the permanent positive charge,

87

which prevents membrane permeability. Just recently, Hijazin et al. 14 verified that

88

umbelliferone is taken up by seedlings of various plant species. As outlined below, this

89

coumarin is differentially modified in various acceptor plants after its uptake (Figure 2).

90

In the case of alkaloids, in addition to their logP values, also the pH of the medium

91

determines their membrane permeability, and thus their potential to be taken up by the

92

acceptor plants 24, 25: in acidic solutions, alkaloids are protonated. In consequence, they are not

93

able to pass biomembranes. Whereas alkaloids, leached out into neutral to slightly alkaline

94

soils, predominantly are present as free bases. In consequence, they can easily diffuse through

95

biomembranes. In contrast, in acidic soils – due to the higher degree of protonation – the

96

membrane permeability of the alkaloids is quite lower. Accordingly, the pH of the soils will

97

strongly determine the extent of alkaloids taken up by the acceptor plants.

98

In addition to the membrane permeability, a further point has to be considered when

99

evaluating the uptake of natural compounds, i.e., the microbial decomposition of natural

100

products leached out from rotting plant material. As the entire biomass of rotting plants is

101

completely decayed by microorganisms, also the relevant natural products are efficiently

102

degraded in the soil. Thus, we always have to be aware that the actual amount of natural

103

products present in the in the soil, does not solely depend on the extent of the leaching

104

processes from the donor plant, but is also highly influenced and determined by the catabolic

105

activity of the microorganisms present in the soil. Ergo, the extent of an import of a certain


Page 8 of 23

Page 9 of 23


106

compound does not rely only on the physico-chemical properties and the pH of the soil, but is

107

also determined by the velocity of its degradation by microorganisms26.

108

Transfer from living donor plants

109

Allelopathy taught us that there are basically various options how allelochemicals are released

110

into the environment 27. Apart from the leaching out from decomposing plant residues, the

111

active compounds also could be exuded from living plants either by their roots 2 or by their

112

leaves 27. Considering these options for the phenomenon of horizontal natural product

113

transfer, it seems reasonable to assume that - in analogy - also classical natural products might

114

be released from living donor plants, too. To verify this assumption, co-culture experiments

115

had been conducted. In this context, Senecio jacobaea plants containing large amounts of

116

pyrrolizidine alkaloids (PAs) were co-cultivated together with various acceptor plants in the

117

same pot. Two months after co-cultivation, the plants were harvested and the PAs were

118

quantified. It was really fascinating to realize that in all acceptor plants co-cultivated with the

119

Senecio plants, quite high concentrations of PAs were present, e.g., in parsley, in average

120

more than 200 µg PAs / kg d.w. had been accumulated 16. These results evinced clearly that the

121

PAs - originally synthesized and accumulated in the Senecio donor plants - had been relocated

122

into the parsley acceptor plants.

123

As outlined for allelochemicals, in principle also several options may account for the transfer

124

of classical secondary metabolites. Moreover, at least in the pot experiments, a further

125

possibility has to be considered, i.e., a direct transfer by root grafts. Since in the pot

126

experiments the roots of the Senecio donor plants and the parsley acceptor plants exhibited an

127

intimate contact 16, interspecific root grafting as described by Basnet 28 could not be excluded.

128

Accordingly, co-culture experiments had been repeated under field conditions employing

129

different spatial distances between the experimental plants 29. Since in all acceptor plants PAs

130

had been detected, the authors exclude a direct exchange of substances via root grafts. A ACS Paragon Plus Environment


131

further and most obvious possibility to explain the observed PA-transfer between living plants

132

is related to the shedding of Senecio leaves, from which the PAs might have been leached out.

133

However, since during the related pot experiments hardly any abscission of leaves occurred,

134

this possibility can be neglected, too. Alternatively, the PAs could have been bled out from

135

minor leaf injuries, e.g., those caused by pathogens, herbivores or by mechanical contact

136

among the leaves. Verily, the plants used in the experiments were healthy and no herbivores

137

were present. Accordingly, also any bleeding of PAs from minor injuries of leaves seems to

138

be unlikely. This assumption is underlined by the finding that the PA-spectra of donor and

139

acceptor plants are quite different: whereas in the donor plants the characteristic PA-spectrum

140

of S. jacobaea was detected, in the acceptor plants nearly exclusively jacobine and its N-oxide

141

were present 29. In case of leaching or bleeding processes, the related PA-spectra should be

142

very similar to that of the donor plant – just as it was observed in the course of the mulching

143

experiments by 11. In consequence, it has to be taken into consideration that the Senecio donor

144

plants actively exude PAs into the soil. Although any direct evidence for such exudation of

145

alkaloids is still lacking, there are some hints to support this option. In root cultures of

146

Senecio vernalis, which contain a large array of PAs, senkirkine was the sole PA present in

147

the medium. Obviously the root cells exude this PA actively into the culture medium 30.

148

Similar exudation of alkaloids has been reported for the indole alkaloid ajmalicine in the hairy

149

root cultures of Catharanthus roseus 31, for harmine and harmaline in those of Oxalis

150

tuberosa 32 or for nicotine in root culture from Nicotiana tabacum 33. Nonetheless, any direct

151

proof that alkaloids indeed are exuded from roots growing in the soil is still missing; only

152

some hints are available 34, 35. Much further research is required to elucidate whether or not

153

alkaloids are actively released into the soil.

154

Although the actual path of the PA-transfer from living donor plants into acceptor plants

155

growing in the vicinity is still unknown, the co-culture experiments approve undoubtedly that


Page 10 of 23

Page 11 of 23


156

a transfer of typical secondary metabolites from living and vital donor plants to the various

157

acceptor plants growing in the vicinity does occur. Accordingly, the concept of horizontal

158

natural product transfer has to be broadened by including the transfer from vital plants

159

(Figure 1).

160 161

Modification of the imported substances

162

With respect to the fate of xenobiotics, it is well established that the imported substances

163

could be modified within the acceptor plants, e.g., by oxidation, hydroxylation, and conju-

164

gation 36. According to the so-called “green liver concept”, these reactions are discussed to be

165

part of a deliberate detoxification system of xenobiotics 37. Consequently, we have to consider

166

that also the natural compounds taken up, could be modified within the acceptor plants. The

167

first hint for such mechanisms was given by the finding that the content of alkaloids in

168

acceptor plants strongly decreased by the time 9, 11. In a renewed studies 15 - in contrast to

169

previous investigations - the amount of PAs taken up into acceptor plants was not solely

170

determined by summing up all genuine PAs known to occur in the donor plants, but also by

171

the so-called “sum-parameter” method 38. This approach is based on a HPLC-ESI-MS/MS

172

determination of the necine base. Consequently, all PA-related structures, i.e., also putative

173

modification products of genuine PAs are determined. The corresponding results were highly

174

surprising. It turned out that two weeks after the mulching, more than two-thirds of the PAs

175

taken up had been modified to so far unknown derivatives, which are not detectable by

176

employing the standard methods for PA quantification 15. Up to now, detailed information on

177

the modification is missing as well as on potential toxicity of the unknown derivatives. Much

178

more research is required to evaluate reliably the risk of the related PA contamination.

179

Obviously, as known for xenobiotics, also PAs imported into the acceptor plants, are modified

180

to a large extent. However, this means that we have to take into consideration that far more ACS Paragon Plus Environment


181

PAs are taken up by the acceptor plants than generally estimated by the standard methods.

182

Accordingly, there is a strong need to elucidate the modified substances. Yet, corresponding

183

approaches to analyze the chemical nature of these modifications are sophisticated. Indeed, a

184

smart strategy would be the application of isotope labelled alkaloids. However, such

185

approach is very time-consuming and cost-intensive. Alternatively, for the elucidation of

186

putative modifications, the employment of other natural products seems to be far more

187

promising. In this context, coumarins are very advantageous, since the genuine substances as

188

well as most of their derivatives could easily be detected due to their fluorescence 39. Hijazin

189

et al. 14 chose umbelliferone as model compound to study the uptake of phenolic compounds

190

and their putative modifications in acceptor plants. As predicted, in all cases, a tremendous

191

uptake of umbelliferone was observed. However, in several plants the umbelliferone was just

192

translocated into the leaves, while in the seedlings of barley and garden cress, the imported

193

umbelliferone was modified effectively. In garden cress, it was hydroxylated and glucosylated

194

to yield esculin (Figure 2), whereas in barley seedlings, the imported umbelliferone was

195

modified by methoxylation to yield scopoletin. Corresponding modifications of xenobiotics

196

are known to be catalyzed by cytochrome P450 enzymes 40, 41. In order to verify the

197

involvement of P450 enzymes in the conversion of umbelliferone to scopoletin in barley and

198

to esculin in garden cress, respectively, an additional approach was performed. Umbelliferone

199

was applied together with naproxen, which is reported to reduce the activity of P450

200

enzymes 42. As assumed, the conversion of umbelliferone to scopoletin in barley as well as the

201

modification to esculin in garden cress was massively reduced by the addition of naproxen.

202

The data presented by Hijazin et al. 14 for the first time demonstrate that – in analogy to the

203

modification of xenobiotics – also the imported natural products are modified in the acceptor

204

plants. In this context, up to now, only the modification of typical allelochemicals, e.g.,

205

biochanin A or BOA, have been reported 22, 23. In consequence, the concept of horizontal


Page 12 of 23

Page 13 of 23


206

natural product transfer has to be broadened by including the modifications of imported

207

substances as outlined in Figure 1.

208

The knowledge that the fate of imported natural products is quite different in the various plant

209

species suggests that the observed modifications are not due to a general and deliberate

210

detoxification system as proposed by the “green liver concept” 36, 37. In contrast, these

211

reactions appear to be due to random “accidental” activities of enzymes generally involved in

212

the modification of natural products genuinely present in the acceptor plants. Accordingly, the

213

phenomenon of enzyme promiscuity 43, which actually is getting more and more attraction,

214

also seems to be relevant with respect to the differential modification of natural products and

215

xenobiotics in the acceptor plants. There is a tremendous demand for further research to

216

elucidate whether the modification of imported substances is due to a particular

217

“detoxification system” or to “side activities” of promiscuous enzymes involved in plant

218

specialized metabolism.

219

New implications for allelopathy

220

The data outlined so far demonstrate clearly that the “Horizontal natural product transfer”

221

represents a prevailing phenomenon in nature that is quite more spread than originally

222

assumed. In forthcoming studies on plant-plant interactions, we have to consider that natural

223

compounds derived from one plant species are taken up randomly from the soil by other

224

plants growing in their vicinity. Due to the unlimited number of permutations of donor and

225

acceptor plants and thus the tremendously high variation in natural products exchanged, for

226

most of these cases a certain or specific ecological effect of this phenomenon can be ruled out.

227

Nonetheless, we have to concede that apart from the so-called typical allelochemicals, all

228

other natural products exhibiting the appropriate physico-chemical properties (a logP value

229

between -1 and 3) are generally taken up by plants. These novel insights will strongly impact



230

our comprehension of chemical ecology, especially with respect to plant-plant interactions

231

and the definition of xenobiotics.

232

Up to now, xenobiotics are frequently defined as “non-natural substances”, which are “foreign

233

to life” 44. As the random uptake of natural products and their modification in the acceptor

234

plants is equal to the related processes for xenobiotics, a re-evaluation of the classical

235

definition of xenobiotics is required 15. In the same manner as the “classical, non-natural”

236

xenobiotics are foreign to the acceptor plants, the natural products taken up in the course of

237

horizontal natural product transfer are foreign, too. Accordingly, a new definition, or at least a

238

differentiation of the term xenobiotics, is required. Indeed, Godheja et al. 45 included already

239

“naturally occurring poisons” in the definition for xenobiotics; however, based on the

240

findings related to the horizontal natural product transfer, the definition of “xenobiotics” must

241

be broadened even more. In this manner, the denomination xenobiotics should include all

242

metabolites from other plants, which are foreign to the acceptor plants.

243

The knowledge that plants inherently take up a wide array of natural products from the soil

244

necessitates a reconsideration of our understanding of plant-plant-interactions. This concept is

245

consolidated by the cognition that many natural products are released into the environment

246

from vital and living plants. Up to now, in this context, only “typical allelochemicals”, which

247

reveal certain significance in plant-plant interactions, e.g., by affecting the growth or the

248

germination of potential competitors, have been taken into consideration. Now, we are aware

249

that a random exchange of natural products even between living plants and also among

250

individuals of different species seems to be quite common. In addition, the imported

251

compounds could be differentially modified, depending on the plant species. In this sense, it

252

has to be considered that the modification of allelochemicals like biochanin A or BOA

253

strongly influences their potential inhibitory effect 22, 23. These coherences might open new

254

doors for our understanding of the evolution of allelopathic interactions. This can nicely be ACS Paragon Plus Environment

Page 14 of 23

Page 15 of 23


255

demonstrated for the allelopathic effect of juglone, whose inhibition strongly differs between

256

various plant species 46 - 48. If we assume that – alike umbelliferone - also juglone is modified

257

differentially within the various acceptor plants, this conjuncture could explain the differences

258

in the sensitivity against this allelochemical.

259

Apart from these reflections related to basic science, the novel insights also reveal certain

260

relevance for applied plant biology and agriculture. The transfer of natural products from

261

living donor plants might actually be the bases for our understanding of several hitherto

262

unexplained processes, e.g., concerning the beneficial effects of crop rotations or of co-

263

cultivation of certain vegetables.

264

Abbreviations Used

265

BOA - Benzoxazolinone

266

HPLC-ESI-MS/MS – High-performance liquid chromatography-electrospray ionisation

267 268

tandem mass spectrometry PAs - Pyrrolizidine alkaloids



269

Literature

270

1. Bertin, C.; Yang, X.; West, L.A. The role of root exudates and allelochemicals in the

271

rhizosphere. Plant Soil, 2003, 256, 67-83.

272

2. Kalinova, J.; Vrchotova, N.; Triska, J. Exudation of allelopathic substances in buckwheat

273

(Fagopyrum esculentum Moench). J. Agric. Food Chem. 2007, 55, 6453-6459.

274

3. Trapp, S.; Legind, C.N. Uptake of organic contaminants from soil into vegetables and

275

fruits. In: Dealing with Contaminated Sites; Swartjes, F.A., Ed.; Springer, Netherlands

276

2011; 369-408.

277

4. EFSA - European Commission Decision - 2009. Concerning the non-inclusion of nicotine

278

in Annex I to Council Directive 91/414/EEC and the withdrawal of authorisations for

279

plant protection products containing that substance. Official Journal of the European

280

Union 2009; L 5/9 – 9.1.

281 282 283 284 285 286 287 288 289

5. Mulder, P.P.J.; Sánchez, P.L.; These, A.; Preiss-Weigert, A.; Castellari, M. Occurrence of pyrrolizidine alkaloids in food. EFSA supporting publication 2015. EN-859. 6. Fu, P. P.; Xia, Q.; Lin, G.; Chou, M.W. Pyrrolizidine Alkaloids-Genotoxicity, Metabolism Enzymes, Metabolic Activation, and Mechanisms. Drug Metab. Rev. 2004, 36:1. 7. Wiedenfeld, H.; Edgar, J. Toxicity of pyrrolizidine alkaloids to humans and ruminants. Phytochem. Rev. 2011, 10, 137–15. 8. Mattocks, A. R. Chemistry and Toxicology of Pyrrolizidine Alkaloids. Academic Press, New York., 1986. 9. Selmar, D.; Engelhardt, U.H.; Hänsel, S.; Thräne, C.; Nowak, M.; Kleinwächter, M.

290

Nicotine uptake by peppermint plants as a possible source of nicotine in plant-derived

291

products. Agron Sustain Dev. 2015, 35, 1185–1190.

292

10. Selmar, D.; Radwan, A.; Abdalla, N.; Taha, H.; Wittke, C.; El-Henawy, A.; Alshaal, T.;

293

Amer, M.; Nowak, M.; El-Ramady, H. Uptake of nicotine from discarded cigarette butts

294

– A so far unconsidered path of contamination of plant derived commodities. Environ.

295

Pollut. 2018, 238, 972-976.

296

11. Nowak, M.; Wittke, C.; Lederer, I.; Klier, B.; Kleinwächter, M.; Selmar, D. Interspecific

297

transfer of pyrrolizidine alkaloids: An unconsidered source of contaminations of

298

phytopharmaceuticals and plant derived commodities. Food Chem. 2016, 213, 163-168.


Page 16 of 23

Page 17 of 23

299


12. Selmar, D.; Radwan, A.; Nowak, M. Horizontal natural product transfer: A so far

300

unconsidered source of contamination of plant-derived commodities. J. Environ. Anal.

301

Toxicol. 2015, 5, 4.

302

13. Yahyazadeh, M.; Nowak, M.; Kima, H.; Selmar, D. Horizontal natural product transfer: A

303

potential source of alkaloidal contaminants in phytopharmaceuticals. Phytomedicine

304

2017, 34, 21-25.

305 306 307

14. Hijazin, T.; Radwan, A.; Abouzeid, S.; Dräger, G.; Selmar, D. Uptake and modification of umbelliferone by various seedlings. Phytochemistry 2019, 157, 194-199. 15. Selmar, D.; Abouzeid, S.; Radwan, A.; Hijazin, T.; Yahyazadeh, M.; Lewerenz, L.;

308

Nowak, M.; Kleinwächter, M. Horizontal natural product transfer - A novel attribution

309

in allelopathy. In: Reference Series in Phytochemistry. Co-Evolution of Secondary

310

Metabolite, Mérillon, J.M., Ramawat, K.G., Eds.; Springer International Publishing,

311

Cham, Switzerland, 2020; in press.

312

16. Nowak, M.; Yahyazadeh M.; Lewerenz, L.; Selmar, D. Horizontal Natural Product

313

Transfer: A so far unconsidered source of contamination of medicinal. In: Medicinal

314

Plants and Environmental Challenges. Ghorbanpour, M., Varma, A., Eds. Springer

315

International Publishing, Cham, Switzerland, 2017; 215-226.

316 317 318 319 320

17. Kobayashi, T.; Nishizawa, N.K. Iron uptake, translocation, and regulation in higher plants Ann. Rev. Plant Biol. 2012, 63, 131-52. 18. Trapp, S. Plant uptake and transport models for neutral and ionic chemicals. Environ. Sci. Pollut. R. 2004, 11, 33-39. 19. Cronin, M.T.D.; Livingstone, J. Calculation of physiochemical properties. In: Predicting

321

Chemical Toxicity and Fate, Cronin, M.T.D., Livingstone, J., Eds.; CRC Press 2004,

322

31-40.

323 324

20. Limmer, M.A.; Burken, J.G. Plant translocation of organic compounds: Molecular and physicochemical predictors. Environ. Sci. Techno. Lettl. 2014, 1, 156-161.

325

21. Hurtado, C.; Domínguez, C.; Pérez-Babace, L.; Cãnameras, N.; Comas, J.; Bayona, J.M.

326

Estimate of uptake and translocation of emerging organic contaminants from irrigation

327

water concentration in lettuce grow under controlled conditions. J. Hazard. Mater.

328

2016, 305, 139-148.



329

22. Shajib, M.T.I.; Pedersen, H.A.; Mortensen, A.G.; Kudsk, P.; Fomsgaard, I.S. Phytotoxic

330

effect, uptake, and transformation of biochanin A in selected weed species. J. Agric.

331

Food Chem. 2012, 60, 10715-10722.

332

23. Schulz, M.; Wieland, I. Variation in metabolism of BOA among species in various field

333

communities – biochemical evidence for co-evolutionary processes in plant

334

communities? Chemoecology 1999, 9, 133-141.

335 336 337 338 339 340

24. Trapp, S. Bioaccumulation of polar and ionizable compounds in plants. In: Ecotoxicology Modeling Devillers, J. Ed.; Springer, US, 2009; 1-55. 25. Nowak, M.; Selmar, D. Cellular distribution of alkaloids and their translocation via phloem and xylem: the importance of compartment. pH. Plant Biol. 2016, 18, 879-882. 26. Fetzner, S. Bacterial degradation of pyridine, indole, quinoline, and their derivatives under different redox conditions. Appl. Microbiol. Biotechnol. 1998, 49, 237-250.

341

27. Nakano, H.; Nakajima, E.; Fujii, Y.; Yamada, K.; Shigemori, H.; Hasegawa, K. Leaching

342

of the allelopathic substance L-tryptophan from the foliage of mesquite (Prosopis

343

juliflora DC.) plants by water spraying. Plant Growth Regul. 2003, 40, 49-52.

344

28. Basnet, K. Ecological consequences of root grafting in Tabonuco (Dacryodes excelsa)

345

trees in the Luquillo experimental forest, Puerto Rico. Biotropica. 1993, 25, 28-35.

346

29. Selmar, D.; Wittke, C.; Beck von Wolffersdorff, I.; Klier, B.; Lewerenz, L.; Kleinwächter,

347

M.; Nowak, M. Transfer of pyrrolizidine alkaloids between living plants: A disregarded

348

source of contaminations. Environ. Pollut. 2019, 248, 456-461.

349

30. Toppel, G.; Witte, L.; Riebesehl, B.; Borstel, K.; Hartmann, T. Alkaloid patterns and

350

biosynthetic capacity of root cultures from some pyrrolizidine alkaloid producing

351

Senecio species. Plant Cell Rep. 1987, 6, 466-9.

352

31. Ruiz-May, E.; Galaz-Ávalos, R.M.; Loyola-Vargas, V.M. Differential secretion and

353

accumulation of terpene indole alkaloids in hairy roots of Catharanthus roseus treated

354

with methyl jasmonate. Mol. Biotechnol. 2009, 41, 278-285.

355

32. Bais, H.P.; Vepachedu, R.; Vivanco, J.M. Root specific elicitation and exudation of

356

fluorescent β-carbolines in transformed root cultures of Oxalis tuberosa. Plant Physiol.

357

Biochem. 2003, 41, 345-353.


Page 18 of 23

Page 19 of 23

358


33. Zhao, B.; Agblevor, F.A.; Ritesh, K.C.; Jelesko, J.G. Enhanced production of the alkaloid

359

nicotine in hairy root cultures of Nicotiana tabacum. Plant Cell Tiss. Org. Cult. 2013,

360

113, 121-129.

361

34. Bais, H.P.; Park, S.W.; Stermitz, F.R.; Halligan, K.M.; Vivano, J.M. Exudation of

362

fluorescent β-carbolines from Oxalis tuberosa L. roots. Phytochemistry. 2002, 61, 539-

363

543. RETRACTED: doi:10.1016/S0031-9422(02)00235-2

364

35. Glinwood, R.; Pettersson, J.; Ahmed, E.; Ninkovic, V.; Birkett, M.; Pickett, J. Change in

365

acceptability of barley plants to aphids after exposure to allelochemicals from couch-

366

grass (Elytrigia repens). J. Chem. Ecol. 2003, 29, 261-274.

367

36. Burken, J.G. Uptake and metabolism of organic compounds: green-liver model. In:

368

Phytoremediation: Transformation and Control of Contaminants. McCutcheon, S.,

369

Schnoor, J.L., Eds. Wiley, New York, 2003 59-84.

370 371

37. Sandermann, H. Higher plant metabolism of xenobiotics: the ´green liver` concept. Pharmacogenetics. 1994, 4, 225–241.

372

38. Cramer, L.; Schiebel, H.M.; Ernst, L.; Beuerle, T. Pyrrolizidine alkaloids in the food

373

chain. Development, validation, and application of a new HPLC-ESI-MS/MS sum

374

parameter method. J. Agric. Food Chem. 2013, 61, 11382-11391.

375

39. Jones, G.; Rahman, M.A. Fluorescence properties of coumarin laser dyes in aqueous

376

polymer media. Chromophore isolation in poly (methacry1ic acid) hypercoils. J. Phys.

377

Chem. 1994, 98, 13028-13037.

378

40. Yun, M.-S.; Yogo, Y.; Miura, R.; Yamasue,Y.; Fischer, A.J. Cytochrome P-450

379

monooxygenase activity in herbicide-resistant and -susceptible late watergrass

380

(Echinochloa phyllopogon). Pest. Biochem. Physiol. 2005, 83, 107-114.

381 382 383

41. Siminszky, B. Plant cytochrome P450-mediated herbicide metabolism. Phytochem. Rev. 2006, 5, 445–458. 42. Miners, J.O.; Coulter, S.; Tukey, R.H.; Veronese, M.E.; Birkett, D.J. Cytochromes P450,

384

1A2, and 2C9 are responsible for the human hepatic O-demethylation of R- and S-

385

naproxen. Biochem. Pharmacol. 1996, 51, 1003-1008.

386 387

43. Kreis, W.; Munkert, J. Exploiting enzyme promiscuity to shape plant specialized metabolism. J. Exp. Bot. 2019, 70, 1435–1445.



388

44. Knapp, J.S.; Bromley-Challoner, K.C.A. Recalcitrant organic compounds. In: Handbook

389

of Water and Wastewater Microbiology. Mara, D., Horanm N. Academic Press. 2003,

390

559-596.

391

45. Godheja, J.; Shekhar, S.K.; Siddiqui, S.A.; Dr, M. Xenobiotic compounds present in soil

392

and water: A review on remediation strategies. J. Environ. Anal. Toxicol. 2016, 6: 5.

393

doi: 10.4172/2161-0525.1000392

394 395

46. Williams, R.D.; Hoagland, R.E. The Effects of naturally occurring phenolic compounds on seed germination. Weed Sci. 1982, 30, 206-212.

396

47. Kocacë Aliskan, I.; Terzi, I. Allelopathic effects of walnut leaf extracts and juglone on

397

seed germination and seedling growth. J Hortic Sci Biotech. 2001, 76, 436-440.

398 399 400

48. Rietveld, W.J. Allelopathic effects of juglone on germination and growth of several herbaceous and woody species. J. Chem. Ecol. 1982, 9, 295-308. 49. Abouzeid, S.; Beutling, U.; Selamr, D. Stress-induced modification of indole alkaloids:

401

Phytomodificines as a new category of specialized metabolites Phytochem. 2019, 159,

402

102–107.


Page 20 of 23

Page 21 of 23


Table 1: Uptake of natural products by acceptor plants

404 405

type

plant

literature

caffeine

purine alkaloid

barley

13

theobromine

purine alkaloid

barley

13

theophylline

purine alkaloid

barley

13

erucifoline


chamomile, peppermint melissa, parsley

11, 29

jacobine



11, 29

monocrotaline


barley

seneciphylline



11, 29

senecionine



29

nicotine

nicotine alkaloid

parsley, chamomile

9, 10

atropine

tropane alkaloid

barley

13

noscapine


barley

13

papaverine


barley

13

harmaline

indole alkaloid

barley


harmine

indole alkaloid

barley


strychnine

indole alkaloid

barley

13

vincamine

indole alkaloid

barley


betanidine

betalain

barley, pea

16

resveratrol

stilbene

barley

15; 49

coumarin

barley, flax, radish

14

umbelliferone

pea, garden cress 406




Figure 1: 408 409

410 411 412 413

Figure 1: The concept of Horizontal Natural Product Transfer.

414

The concept of this phenomenon originally described solely the uptake of substances

415

leached out from rotting plant material 12 Meanwhile, it was demonstrated that

416

natural products, such as alkaloids, are also transferred from vital and living donor

417

plants 7. Moreover, it became evident that the natural products could be modified

418

after their uptake in the acceptor plants 14. Accordingly, the concept has to be

419

broadened by including these both new aspects.

420


Page 22 of 23

Figure 2:

Page 23 of 23


421 422

Figure 2: Uptake and modification of umbelliferone in acceptor plants.

423

Umbelliferone is taken up by seedlings of all plant species tested. In some acceptor plants,

424

this coumarin is oxidized to yield esculetin, which subsequently, in barley is methylated to

425

scopoletin. In contrast, in garden cress, it is converted to esculin by glucosylation 14. In the

426

control plants neither umbelliferone nor the derivatives are detectable. Moreover, no

427

glucosylated derivatives had been detected in the medium, verifying that the modification

428

took place in the acceptor plants. ACS Paragon Plus Environment

Horizontal Natural Product Transfer: Intriguing ... - ACS Publications

Recommend Documents