Phenylpropanoid amides of serotonin accumulate in witches' broom diseased bamboo

Article abstract of DOI:10.1016/S0031-9422(03)00429-1

Aciculosporium take (Ascomycota; Clavicipitaceae), causes the witches' broom disease in bamboo, particularly Phyllostachys bambusoides. Since it was observed that endogenous indole-3-acetic acid is reduced in the twigs of the diseased bamboo, the symptoms

Full text of DOI:10.1016/S0031-9422(03)00429-1

Phytochemistry 64 (2003) 965–969
www.elsevier.com/locate/phytochem
Phenylpropanoid amides of serotonin accumulate in
witches’ broom diseased bamboo
Eiji Tanakaa, Chihiro Tanakaa,*, Naoki Morib,
Yasumasa Kuwaharab, Mitsuya Tsudaa
aDivision of Environmental Science and Technology, Graduate School of Agriculture, Kyoto University,
Kitashirakawa Oiwake-Cho, Sakyo-Ku, Kyoto, 606-8502, Japan
bDivision of Applied Life Sciences, Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake-Cho,
Sakyo-Ku, Kyoto, 606-8502, Japan
Received 29 October 2002; received in revised form 4 June 2003
Abstract
Aciculosporium take (Ascomycota; Clavicipitaceae), causes the witches’ broom disease in bamboo, particularly Phyllostachys
bambusoides. Since it was observed that endogenous indole-3-acetic acid is reduced in the twigs of the diseased bamboo, the
symptoms (bushy appearance) may be induced by reduction in auxin levels. Furthermore, two indolic compounds accumulated in
diseased twigs, these being identified as N-p-coumaroylserotonin and N-feruloylserotonin by LC-MS, 1H NMR and 13C NMR
spectroscopic analyses. N-p-Coumaroylserotonin possesses antifungal activity against A. take.
# 2003 Elsevier Ltd. All rights reserved.
Keywords: Phyllostachys bambusoides; Poaceae; Indole-3-acetic acid; N-p-Coumaroylserotonin; N-Feruloylserotonin; Antifungal activity;
Aciculosporium take; Witches’ broom of bamboo
1. Introduction
In this article, we analyzed indolic compounds in dis-
eased and healthy bamboo twigs. The bamboo with
witches’ broom contained significantly less IAA (indole-
3-acetic acid) (1) than healthy twigs. Furthermore, we
confirmed that diseased twigs accumulated two indolic
compounds, N-p-coumaroylserotonin (2) and N-fer-
uloylserotonin (3). We studied the antifungal activity of
these two compounds.
Witches’ broom is the disease most destructive to
bamboo forests in Japan, China and Taiwan (Tsuda et
al., 1997; Zhu and Huang, 1988; Chen, 1970). The
symptoms of this disease include a bushy appearance
with dwarfed leaves numerous twigs growing succes-
sively. The symptoms in P. bambusoides Sieb. et Zucc.
are especially severe, although the causal agent Acicu-
losporium take Miyake (Ascomycota, Clavicipitaceae;
Anamorph: Albomyces take Miyake) can infect many
other bamboo species (Tsuda et al., 1997). In order to
investigate the cause of development of the symptoms, it
is necessary to examine the physiological changes in
diseased bamboo. Auxin (indole-3-acetic acid, 1) deficit
led to a bushy phenotype in Arabidopsis mutants (Lin-
coln et al., 1990; Bak et al., 2001). Thus, a reduction in
auxin 1 may be implicated in the witches’ broom
appearance of infected bamboo plants.
* Corresponding author. Tel.: +81-75-753-6466; fax: +81-75-753-
6312.
E-mail address: chihiro@remach.kais.kyoto-u.ac.jp (C. Tanaka).
0031-9422/$ - see front matter # 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/S0031-9422(03)00429-1

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E. tanaka et al. / Phytochemistry 64 (2003) 965–969
2. Results and discussion
in all bamboo species we studied, including P. bambu-
soides var. marliacea Makino, P. pubescens Maz.ex
Houz.de Le. and Shibataea kumasaca (Zoll.) Nakai
(Table 2). N-p-Coumaroylserotonin (2) was detected
even in P. pubescens and S. kumasaca, which showed no
symptoms in response to the witches’ broom fungus.
Previously, both phenylpropanoid amides of ser-
otonin (2 and 3) had been identified from safflower
seeds and oil cake (Sakamura et al., 1978; Sakamura et
al., 1980; Zhang et al., 1997). N-p-Coumaroylserotonin
(2) was isolated from Japanese barnyard millet grains
(Watanabe, 1999) and a powder of konnyaku-imo
(Amorphophallus konjac) (Niwa et al., 2000). N-Fer-
uloylserotonin (3) was reported in Sweet Sultan (Cen-
taurea moschata) (Sarker et al., 1997) and Cornflower
(Centaurea cyanus) as moschamine (Sarker et al., 2001).
N-p-Coumaroylserotonin (2) has been reported as hav-
ing strong antioxiditant activity (Zhang et al., 1997;
Watanabe et al., 1999) and inhibiting the production of
proinflammatory cytokines by human monocytes (Takii
et al., 1999; Kawashima et al., 1998). It is, however, not
known whether N-p-coumaroyl- and N-feruloylser-
otonin (2 and 3) are important for the plant. Some
amides of hydroxycinnamic acids possess antifungal
activity, e.g. avenanthramides (Miyagawa et al., 1995)
and feruloylagmatine (Stoessl and Unwin, 1970). We
therefore investigated the antifungal activity of N-p-
coumaroyl- and N-feruloylserotonin (2 and 3).
2.1. IAA (1) amount related to the symptoms of witches’
broom
The amount of free IAA (1) in diseased and healthy
bamboo twigs were 5.4Æ1.8 mg/g (N=5) and 31.2Æ21.2
mg/g (N=4) dry wt of twigs, respectively (Table 1).
Features of witches’ broom resemble the phenotype of
some bushy mutants of Arabidopsis, e.g. a reduced
auxin 1 sensing mutant (Lincoln et al., 1990) and a
CYP83B1 over-expression mutant, which may conse-
quently reduce free auxin 1 (Bak et al., 2001). The low
concentration of free IAA (1) in the twigs possibly
explains the bushy appearance.
2.2. Diseased bamboo accumulated N-p-coumaroyl- and
N-feruloylserotonin (2 and 3)
Two indole-related compounds accumulated in dis-
eased bamboo twigs. These compounds were isolated
and identified as N-p-coumaroyl- and N-feruloylsero-
1
tonin (2 and 3) on the basis of LC-MS, H NMR and
13C NMR spectroscopic analyses. The identity of each
amide was established by chemical synthesis from the
corresponding hydroxycinnamic acids and serotonin
using dicyclohexylcarbodiimide. Next, the amounts of
N-p-coumaroyl- and N-feruloylserotonin (2 and 3) were
measured in diseased and healthy bamboo twigs
(Table 1). Both compounds (2 and 3) accumulated in
diseased twigs, compared to healthy twigs. The detec-
tion of the compounds (2 and 3) in bamboo has not
been reported before, although the occurrence of cin-
namic acid derivatives in bamboo has been carefully
examined (Tachibana et al., 1992). N-p-Coumaroylser-
otonin (2) was detected in significant amount in the
diseased twigs but only at trace levels in healthy twigs,
wherease N-feruloylserotonin (3) was detected in trace
amounts in both diseased and healthy bamboo twigs.
These observations imply that N-p-coumaroyl- and N-
feruloylserotonin (2 and 3) are produced by the bamboo
plant and not by the pathogenic fungi.
2.3. N-p-coumaroylserotonin (2) possesses antifungal
activity against Aciculosporium take
The antifungal activities of N-p-coumaroyl- and N-
feruloylserotonin (2 and 3) were tested against three
fungi pathogenic to bamboo, A. take, Heteroepichloe
¨
bambusae and Shiraia bambusicola (Fig. 1). The con-
centrations of these amides were set at 100 mg/ml or less
as in most examinations of antifungal activity. Acicu-
losporium take was unable to grow at concentrations
higher than 100 mg/ml of N-p-coumaroylserotonin (2)
(MIC=100 mg/ml), and the EC50 value for mycelial
grow was 84 mg/ml. However, A. take grew at 100 mg/ml
of N-feruloylserotonin (3) (MIC>100 mg/ml,
We then searched for N-p-coumaroyl- and N-fer-
uloylserotonin (2 and 3) in bamboo species other than
Phyllostachys bambusoides. Both amides were detected
EC >100 mg/ml). Heteroepichloe bambusae and Shiraia
¨
bambusicola grew on complete medium amended with
50
Table 1
The amounts of IAA (indole-3-acetic acid) (1), N-p-coumaroylserotonin (2) and N-feruloylserotonin (3) in bamboo twigsa
Amount (mg/g)
Sample bamboo twigs
IAA (1)
N-p-coumaroylserotonin (2)
N-feruloylserotonin (3)
Healthy bamboo (N=4)
Witches’ broom diseased bamboo (N=5)
31.2Æ21.2
5.4Æ1.8
Trace
3.4Æ1.4
2.8Æ1.0
9.6Æ6.4
a
Phyllostachys bambusoides was used. Statistically significant differences were confirmed with the Mann–Whitney U test.

E. tanaka et al. / Phytochemistry 64 (2003) 965–969
967
Table 2
Relative amounts of N-p-coumaroylserotonin (2) and N-feruloylserotonin (3) in selected bamboo species
Bamboo species
Witches’ broom
symptoms
Amount (mg/g)
N-p-coumaroylserotonin (2)
N-feruloylserotonin (3)
Phyllostachys bambusoides
Healthy
Diseased
Healthy
Diseased
Healthy
Healthy
Trace
3.4Æ1.4
Trace
2.8Æ1.0
9.6Æ6.4
1.6Æ1.0
4.2Æ2.4
6.0Æ2.2
12.8Æ7.4
P. bambusoides var. marliacea
0.8Æ0.4
1.6Æ0.8
11.0Æ5.0
P. pubescens
Shibataea kumasaca
Fig. 1. Inhibition of mycelial growth by N-p-coumaroylserotonin (2) and N-feruloylserotonin (3). The mycelial growth is the diameter of the colony
from which the diameter of the inoculum disk (4 mm) was subtracted. The colony diameter 7-days after incubation was measured and its growth
compared to that of the corresponding control, Aciculosporium take (5.3 mm), Heteroepichloe bambusae (20.7 mm) and Shiraia bambusicola (12.1
mm). Results are the mean of 3 replicates.
¨
100 mg/ml of N-p-coumaroyl- and N-feruloylserotonin (2
and 3) (MIC>100 mg/ml, EC50>100 mg/ml), respectively.
This is the first report of N-p-coumaroylserotonin (2)
possessing antifungal activity. This activity is much
stronger than the activity of several indole derivatives or
serotonin (Yue et al., 2000; Cornelia et al., 2002).
On the other hand, the witches’ broom disease rarely
occurred in P. pubescens and S. kumasaca, although
these two species were reported as a host of A. take
(Tsuda et al., 1997). Our studies showed that healthy P.
pubescens and S. kumasaca also produced N-p-coumar-
oylserotonin (2) (Table 2). From this, it is expected that
these species have a greater capacity to produce N-p-
coumaroylserotonin (2) than P. bambusoides. When
these bamboo species are attacked by A. take, they may
produce sufficient amounts of N-p-coumaroylserotonin
(2) to prevent invasion. Thus, the development of wit-
ches’ broom symptoms may be affected by the accumu-
lation of N-p-coumaroylserotonin (2).
Hydroxycinnamic acid amides have been implicated
in the inducible defense of plants. Avenanthramides, N-
cinnamoylanthramides, were characterized as oat phy-
toalexins (Mayama et al., 1981; Miyagawa et al., 1995).
N-Hydroxycinnamoyltyramine in solanaceous plants
was produced in response to various environmental sti-
muli (Clarke, 1982; Negrel and Martin, 1984; Pearce et
al., 1988). N-p-Coumaroylserotonin (2) accumulates in
diseased bamboo plants, and possesses antifungal
activity. Thus N-p-coumaroylserotonin (2) can be con-
sidered as a defense compound of bamboo plants.
The witches’ broom disease frequently occurs in P.
bambusoides and related species, and symptoms are espe-
cially severe among the host species of A. take (Tsuda et
al., 1997). In our research, the amount of N-p-coumar-
oylserotonin (2) in diseased P. bambusoides was less than
the level effective against A. take. Thus, P. bambusoides
produces insufficient amounts of antifungal compounds.
3. Experimental
3.1. Plant materials
Diseased and healthy bamboo twigs were obtained in
Kyoto, Japan. One-year-old-twigs were sampled, and the
leaves and sheaths were removed. The plant materials
were freeze-dried and ground in liquid nitrogen using a
mortar and pestle. The powdered material was then

968
E. tanaka et al. / Phytochemistry 64 (2003) 965–969
extracted three times with MeOH containing 1%
HOAc. All voucher specimens (PRI-Cla-087; PRI-Cla-088)
are deposited at the herbarium of the Kyoto University
Museum (KYO).
fraction eluted with 10% MeOH was concentrated in
vacuo. The solution was loaded on a Sep-pak C18 car-
tridge (Waters) and eluted with MeOH–H2O. The
MeOH–H2O (40:60) fraction, containing the com-
pounds of interest, was concentrated in vacuo and sub-
jected to HPLC (column, Wakosil II 5C18-HG 250Â4.6
mm; solvent, MeCN–H2O (23:77ꢀ); flow rate, 1.2 ml /
min; detection, UV 280 nm; 50 C). Each compound
gave a single peak on reversed phase HPLC, at Rt 9.8
min (A) and Rt 11.5 min (B). The purified compounds
were subjected to LC-MS (LCMS-2010A, SHI-
MADZU) analyses. The following HPLC conditions
were used: linear gradient: 30–60% AcCN for 15 min
(column, Cadenza CD-C18 75Â30 mm Imatakt; flow
rate, 0.2 ml/min; detection, UV 280 nm; 50 ꢀC). LC-MS
analysis of each compound revealed a molecular ion at
3.2. Quantification of IAA (1), N-p-coumaroyl- and
N-feruloylserotonin (2 and 3) in host plants
The MeOH-extract from bamboo twigs (1 g dry weight)
ꢀ
was evaporated in vacuo at 40 C, and dissolved in dis-
tilled water (10 ml). The aqueous phase was extracted with
EtOAc (10 ml). The EtOAc layer was concentrated in
vacuo and dissolved in distilled water (10 ml). The solu-
tion was loaded on a Sep-pak C18 cartridge (Waters) and
eluted with MeOH–H2O. The MeOH–H2O (6:4) fraction,
containing IAA (1) and the other indole compounds was
analyzed by HPLC (column, Wakosil II 5C18-HG
250Â4.6 mm; solvent, MeCN–H2O (18:88); flow rate,
1.2 ml/min), with monitoring of UV (280 nm) and fluo-
rescence intensity (excitation wavelength of 280 nm and
emission wavelength of 355 nm). The calibration curve
was linear in the concentration range from 0 to 10 mg/l.
The recovery yield of IAA (1) and serotonin conjugates (2
and 3) was determined by the following recovery experi-
ments. The concentrations of these compounds in the
powdered plant materials were determined by the method
described above. Then each compound (10 mg) was mixed
with the powdered plant materials (1 g), and the con-
centrations were again determined. The recoveries of the
compounds were calculated from differences of the
concentrations in the samples with or without additions
of exogenous IAA (1) and serotonin conjugates (2 and
3). The numeric values in Tables 1 and 2 were corrected
using recovery yield. Non parametric statistical methods
(Mann–Whitney U test) were used for analysis. Each
study shows a significant difference between diseased
and healthy twigs.
1
m/z 323 (A) and m/z 353 (B) [M+H]+. H- and 13C
NMR spectra were recorded on a Bruker AC-300 spec-
trometer in MeOH-d4 solution using TMS as an internal
1
standard. The H NMR spectral data and other results,
including the 13C NMR spectrum, compound A and
compound B were identified as N-p-coumaroylserotonin
(2) and N-feruloylserotonin (3), respectively. Compar-
isons were made with synthetic compounds and data
from the literature (Zhang et al., 1997).
3.4. Preparation of synthetic N-p-coumaroyl- and
N-feruloylserotonin (2 and 3)
Synthesis of N-p-coumaroylserotonin (2) was carried
out according to the method of caffeoyl DOPA synthesis
(Tebayashi et al., 2000) with a slight modification.
p-Coumaric acid (3.0 mmol), serotonin (1.5 mmol) and
dicyclohexylcarbodiimide (3.3 mmol) were dissolved in
dry pyridine (10 ml) and the mixture was stirred at room
temperature for 24 h. After evaporation of pyridine in
vacuo, the residue was dissolved in MeOH (20 ml). The
solution was cooled in an ice-bath and then 2 M KOH
(200 ml) was added. The mixture was stirred at room
temperature for 4 h and then neutralized with HOAc.
The solvent was extracted with EtOAc (200 ml). The
extract was evaporated in vacuo and the residue was
dissolved in MeOH (50 ml). Dicyclohexylurea and salts
were removed by filtration. After evaporation of solvent,
the filtrate was fractionated using a silica-gel column by
eluting with EtOAc–hexane (3:1, v/v) to give N-P-cou-
maroylserotonin (0.14 mmol). N-Feruloylserotonin (3)
was also synthesized using the same procedure with
ferulic acid and serotonin to give N-p-coumaroyl- and N-
feruloylserotonin (2 and 3) (0.30 mmol).
3.3. Purification and identification of N-p-coumaroyl-
and N-feruloylserotonin (2 and 3)
The MeOH-extracts were developed by silica gel TLC
(Merck) with CHCl3–MeOH (1:9). The developed plate
was sprayed with Ehrlich’s reagent (4-dimethylamino-
benzaldehyde 1 g, MeOH 75 ml, 36% HCl 25 ml). From
diseased bamboo extracts, two major violet spots
appeared at Rf 0.3 (A) and Rf 0.35 (B). From healthy
bamboo extracts, the spot corresponding to compound
B was faint. These two compounds were purified by the
following procedures, while the fraction that contains
the compounds was checked by TLC. The extract cor-
responding to 250 g dry weight of bamboo twigs was
evaporated in vacuo, and the residue was dissolved in
distilled water (250 ml) and partitioned with EtOAc
(250 ml). The EtOAc extract was applied to a silica gel
(10 g) column, and eluted with CHCl3–MeOH. The
3.5. Antifungal activities of N-p-coumaroyl- and
N-feruloylserotonin (2 and 3)
The antifungal activities of N-p-coumaroyl- and N-fer-
uloylserotonin (2 and 3) were tested against three bamboo

E. tanaka et al. / Phytochemistry 64 (2003) 965–969
969
pathogenic fungi, A. take, Heteroepichloe bambusae and
¨
production of phytoalexins by oat Avena sativa in response to crown
rust Puccinia coronata f. sp. avenae. Physiol. Plant Pathol. 19, 217–226.
Miyagawa, H., Ishihara, A., Nishimoto, T., Ueno, T., Mayama, S.,
1995. Induction of avenanthramides in oat leaves inoculated with
crown rust fungus, Puccinia coronata f. sp. avenae. Biosci. Bio-
technol. Biochem. 59, 2305–2306.
Shiraia bambusicola. Sensitivity to the compounds was
evaluated as the minimum inhibitory concentration
(MIC) and effective concentration to inhibit 50% of
mycelial growth (EC50), using the plate dilution method.
Each synthetic compound was dissolved in MeOH and
incorporated into a series of complete media [0.15%
Ca(NO3)2–4H2O, 0.05% KCl, 0.05% MgSO4–7H2O,
0.04% KH2PO4, 0.003% K2HPO4, 0.1% yeast extract,
0.1% tryptone, 1% glucose (w/v)] (Nakada et al., 1994) to
yield final concentrations of 1–100 mg/ml. Each medium
was poured into petri dishes. Mycelial discs (4 mm in dia-
meter) were cut with a sterilized cork borer from the mar-
gin of 1-week-old colonies. The EC50 value was
Nakada, M., Tanaka, C., Tsunewaki, K., Tsuda, M., 1994. RFLP
analysis for species separation in genera Bipolaris and Curvularia.
Mycoscience 35, 271–278.
Negrel, J., Martin, C., 1984. The biosynthesis of feruloyltyramine in
Nicotiana tabacum. Phytochemistry 23, 2797–2801.
Niwa, T., Etoh, H., Shimizu, A., Shimizu, Y., 2000. cis-N-(p-coumar-
oyl)serotonin from Konnyaku, Amorphophallus konjak K. Koch.
Biosci. Biotechnol. Biochem. 64, 2269–2271.
Pearce, G., Marchand, P.A., Griswold, J., Lewis, N.G., Ryan, C.A.,
1998. Accumulation of feruloyltyramine and p-coumaroyltyramine in
tomato leaves in response to wounding. Phytochemistry 47, 659–664.
Sakamura, S., Terayama, Y., Kawakatsu, S., Ichihara, A., Saito, H.,
1978. Conjugated serotonins related to cathartic activity in safflower
seeds (Carthamus tincrotorius L.). Agric. Biol. Chem. 42, 1805–1806.
Sakamura, S., Terayama, Y., Kawakatsu, S., Ichihara, A., Saito, H.,
1980. Conjugated serotonins and phenolic constituents in safflower
seeds (Carthamus tincrotorius L.). Agric. Biol. Chem. 44, 2951–2954.
Sarker, S.D., Savchenko, T., Whiting, P., Sik, V., Dinan, L.N., 1997.
Moschamine, cis-moschamine, moschamindole and moschamindo-
lol: four novel indole alkaloids from Centaurea moschata. Nat.
Prod. Lett. 9, 189.
ꢀ
determined 7 days after incubation at 25 C by plotting
the percentage decrease in colony diameter against the log
concentration of the chemicals. Each experiment was
done in triplicate.
Acknowledgements
We thank Dr. A. Ishihara, Dr. N. Shimidzu, Dr. S.
Kugimiya and Dr. M. Takemura, Division of Applied
Life Sciences, Graduate School of Agriculture, Kyoto
University, for suggestions on the chemical synthesis and
analyses. We also thank the two anonymous reviewers for
their kind suggestions on the revision of the manuscript.
Sarker, S.D., Laird, A., Nahar, L., Kumarasamy, Y., Jaspars, M.,
2001. Indole alkaloids from the seeds of Centaurea cyanus (Aster-
aceae). Phytochemistry 57, 1273–1276.
Stoessl, A., Unwin, C.H., 1970. The antifungal factors in barley. V.
Antifungal activity of the hordatines. Can. J. Botany 48, 465–470.
Tachibana, S., Ohkubo, K., Towers, G.H.N., 1992. Cinnamic acid
derivatives in cell walls of bamboo and bamboo grass. Phytochem-
istry 31, 3207–3209.
Takii, T., Hayashi, M., Hiroma, H., Chiba, T., Kawashima, S., Zhang,
H.L., Nagatsu, A., Sakakibara, J., Onozaki, K., 1999. Serotonin deri-
vative, N-(p-coumaroyl)serotonin, isolated from safflower (Carthamus
tinctorius L.) oil cake augments the proliferation of normal human and
mouse fibroblasts in synergy with basic fibroblast growth factor
(bFGF) or epidermal growth factor (EGF). J. Biochem. 125, 910–915.
Tebayashi, S., Ishihara, A., Tsuda, M., Iwamura, H., 2000. Induction
of clovamide by jasmonic acid in red clover. Phytochemistry 54,
387–392.
References
Bak, S., Tax, F.E., Feldmann, K.A., Galbraith, D.W., Feyereisen, R.,
2001. CYP83B1, a cytochrome P450 at the metabolic branch point
in auxin and indole glucosinolate biosynthesis in Arabidopsis. Plant
Cell 13, 101–111.
Chen, C.C., 1970. Witches’ broom, a new disease of bamboo in Taiwan.
Mem. Coll. Agric. Natl.Taiwan Univ. 11, 101–111. (in Chinese).
Clarke, D.D., 1982. The accumulation of cinnamic acid amides in the
cell walls of potato tissue as an early response to fungal attack. In:
Wood, R.K.S. (Ed.), Active Defence Mechanisms in Plants. Plenum
Press, New York, pp. 321–322.
Tsuda, M., Shimizu, K., Matsumura, K., Tanaka, E., Tanaka, C.,
Doi, Y., 1997. Host range of Aciculosporium take, the causal agent
of witches’ broom of bamboo plants. Bull. Nat. Sci. Mus., Tokyo
Ser. B 23, 25–34.
Cornelia, L.F., Wiedauer, B., Mayr, A., Kirchmair, M., Jenewein, I.,
Ledochowski, M., Dierich, M.P., 2002. Antifungal properties of 5-
hydroxytryptamine (serotonin) against Aspergillus spp. in vitro. Int.
J. Med. Microbiol. 291, 655–657.
Watanabe, M., 1999. Antioxidative phenolic compounds from Japa-
nese barnyard millet (Echinochloa utilis) grains. J. Agric. Food
Chem. 47, 4500–4505.
Yue, Q., Miller, C.J., White Jr., J.F., Richardson, M.D., 2000. Isolation
and characterization of fungal inhibitors from Epichloe festucae. J.
Agric. Food Chem. 48, 4687–4692.
Kawashima, S., Hayashi, M., Takii, T., Kimura, H., Zhang, H.L.,
Nagatsu, A., Sakakibara, J., Murata, K., Oomoto, Y., Onozaki, K.,
1998. Serotonin derivative N-(p-coumaroyl) serotonin, inhibits the
production of TNF-a, IL-1a, IL-1b and IL-6 by endotoxin-stimulated
human blood monocytes. J. Interferon Cytokine Res. 18, 423–428.
Lincoln, C., Britton, J.H., Estelle, M., 1990. Growth and development
of the axr1 mutants of Arabidopsis. Plant Cell 2, 1071–1080.
Mayama, S., Tani, T., Matsuura, Y., Ueno, T., Fukami, H., 1981. The
¨
Zhang, H., Nagatsu, A., Watanabe, T., Sakakibara, J., Okuyama, H.,
1997. Antioxidative compounds isolated from safflower (Carthamus
tinctorius L.) oil cake. Chem. Pharm. Bull. 45, 1910–1914.
Zhu, X., Huang, H., 1988. Studies on witches’ broom of bamboo I.
Symptoms, isolation of pathogen and inoculation test. Scientica
Silvae Sinicae 24, 483–487.