Botanical Studies (2006) 47: 45-50.
*
Corresponding author: e-mail: hshige@agbi.tsukuba.ac.jp;
Tel & Fax: +81-29-853-4603.
BIOCHEMISTRY
A glycolipid involved in flower bud formation of
Arabidopsis thaliana
Yosuke HisamaTsu
1
, Nobuharu GOTO
2
, Koji HasEGaWa
1
, and Hideyuki sHiGEmORi
1,
*
1
Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba 305-8572, Japan
2
Department of Biology, Miyagi University of Education, Sendai 980-0845, Japan
(Received December 21, 2004; accepted september 27, 2005)
ABSTRACT.
We searched for bioactive substances involved in flower bud formation of Arabidopsis
thaliana. some significantly decreasing HPLC peaks were detected in the extract of flower buds-forming
A. thaliana compared with that of the non-flower bud-forming stage. Compound 1, which corresponded to
the most decreased HPLC peak, was isolated from aerial parts of A. thaliana. From NmR and ms data,
compound 1 was identified as one of the monogalactosyl diacylglyceride (mGDG). Compound 1 induced
flower bud formation of A. thaliana exposed to long day condition for only 1 day. These results suggest that
compound 1 as a precursor or a substrate of flower bud-forming substances plays important roles in the flower
bud formation of A. thaliana.
Keywords: Arabidopsis thaliana; Bioactive substance; Flower bud formation; Long day condition; mGDG;
short day condition.
IntroductIon
Flower bud formation is one of the most important
physiological process for higher plants, and the flowering
time is influenced by photoperiod, vernalization, drought
stress, and so on. Chailakhyan demonstrated that
flowering was regulated by the bioactive substances,
which were produced in leaves that were subjected
to favorable photoperiods, and the substances were
transported to the shoot apex to induce flower bud
formation. He named the substances "flower-inducing
hormone" or "florigen" (Chailakhyan, 1936). Since then,
studies on isolation of substances inducing flower bud
formation have been carried out with a large number
of plant species. For example, when the water solution
prepared by immersing Lemna paucicostata exposed
to drought, heat, or osmotic stress, were incubated with
(-)-norepinephrine, the water solution showed strong
flower inducing activity of L. paucicostata (Takimoto
et al., 1994). They found that FN1, the tricyclic α-ketol
fatty acid derived from (-)-norepinephrine and 9, 10-ketol-
octadecadienoic acid (KODA), induced flower formation
of Lemna (Yamaguchi et al., 2001). On the other hand,
to analyze the molecular processes that initiate flower
bud formation and trigger the change from vegetative
to reproductive growth, biologists have performed
intensive genetic studies of flowering time in model plant
A. thaliana. as a result, there was discovery of many
genes about the regulation of flowering time and the
development of a lot of genetic models (Bastow and Dean,
2003). However, bioactive substances involved in flower
bud formation of A. thaliana have been hardly reported.
In this paper, we report the isolation and identification of
a bioactive substance (compound 1) involved in flower
bud formation of A. thaliana and the flower buds-forming
activity of compound 1.
MAterIAlS And MethodS
equipment
Optical rotations were measured with a JasCO
DiP-370 polarimeter.
1
H an d
13
C NmR spectra were
measured and recorded on a Buker aVaNCE-500 in
CD
3
OD. The resonances of CD
3
OD at δ
H
3.35 ppm and
δ
C
49.8 ppm were used as internal standards for NmR
spectra. Esims were recorded on a Waters platform
LC. HPLC was performed using a system composed
of a TOsOH DP-8020 pump and a TOsOH PD-8020
photodiodearray detector or a TOsOH Ri-8021 refractive
index detector.
Plant materials
The seeds of Arabidopsis thaliana cv. Columbia
were provided by the sendai Arabidopsis seed stock
Center (sassC, Japan). The seeds were immersed in
the water for 2 days before sowing on rock wool (Rock
fiber, NITTOBO, Japan). They have been cultured in the
growth container (24°C, ca. 3,800 lux) under short day
condition (8 h-light and 16 h-dark, sD) for 26 or 30 days.
pg_0002
46
Botanical Studies, Vol. 47, 2006
Figure 1. HPLC chromatograms of groups i, ii, and iii. Group
i: grown under long day conditions (16 h-light and 8 h-dark, LD,
ca. 2,500 lux) until the flower bud formation, Group II: grown
under sD and exposed to LD for 3 days just before extraction,
and Group iii: grown under sD throughout the course of the
experiment. They were extracted with meOH and partitioned
between EtOac and H
2
O. The EtOac-soluble materials were
analysed by HPLC. This experiment was repeated 3 times.
hPlc analyses of the extracts of groups I, II,
and III
Arabidopsis thaliana were cultured at 24°C for 26 days
under sD, and they were divided into groups i, ii, and
iii. Group i was grown under long day conditions (16
h-light and 8 h-dark, LD, ca. 2,500 lux) until the flower
bud formation, group ii was grown under sD and exposed
to LD for 3 days just before extraction, and group iii was
grown under sD throughout the course of this experiment.
The aerial parts of each group were frozen with liquid
N
2
, and ground to a fine powder in a mortar, and then
they were extracted with meOH for 3 times. The meOH
extracts were evaporated to dryness in vacuo at 30°C and
the residue was partitioned between EtOac and H
2
O. The
each equivalent amount of EtOAc-soluble material was
analysed by a reversed-phase HPLC (ODs-80Ts, φ4.6×
250 mm, TOsOH, uV detection at 195 nm) with H
2
O-
CH
3
CN under linear gradient conditions at 0.8 ml/min
(aqueous portion: 0 to 100% CH
3
CN at 1%/min, at 100%
CH
3
CN for 10 min, EtOAc-soluble portion: 50 to 100%
CH
3
CN at 1%/min, at 100% CH
3
CN for 30 min). Further
HPLC analysis (same as above) was under the condition at
95% CH
3
CN (Figure 1).
Isolation and structure identification of
compound 1
The aerial parts of A. thaliana were extracted with
meOH (200 mL), and the meOH extracts were evaporated
to dryness in vacuo at 30°C. Then the residue was
partitioned between EtOac and H
2
O. The EtOac-
soluble portion was applied to a reversed-phase column
(TOYOPAK ODS M, TOSOH, 100% CH
3
CN) to afford
a glycolipids fraction, which was purified by a reversed-
phase HPLC (ODs-80Ts, φ4.6×250 mm, TOSOH, 95%
CH
3
CN at a flow rate of 0.8 ml/min, UV detection at 195
nm). From 0.78 g of aerial parts of A. thaliana, 0.3 mg of
compound 1 was obtained.
The mass spectrum of compound 1 gave m/z 769
(m+Na)
+
.
1
H NmR (CD
3
OD): δ 1.03 (6H, t, J = 5.4 Hz),
1.38 (6H, m), 1.67 (2H, m), 2.13 (4H, m), 2.37 (2H, m),
2.86 (4H, m), 3.50 (1H, dd, J = 3.2 and 9.7 Hz, 3’-H), 3.55
(2H, m, 2’, 5’-H), 3.75 (1H, dd, J = 5.2 and 10.7 Hz, sn-
3-Hb, overlapped with 6’-H), 3.79 (2H, m, 6’-H), 3.86
(1H, d, J = 3.2 Hz, 4’-H), 4.04 (1H, dd, J = 5.5, 10.9 Hz,
sn-3-Ha), 4.26 (1H, dd, J = 6.7 and 12.0 Hz, sn-1-Hb,
overlapped with 1’-H), 4.27 (1H, d, J = 7.5 Hz, 1’-H), 4.49
(1H, dd, J = 2.8 and 12.0 Hz, sn-1-Ha), 5.31 (1H, m, sn-
2-H), and 5.40 (12H, m, 7’’-H, 8’’-H, 10’’-H, 11’’-H, 13’’
-H, 14’’-H, 9’’’-H, 10’’’-H, 12’’’-H, 13’’’-H, 15’’’-H, 16’’’
-H).
13
C NmR (CD
3
OD): δ 105.8 (C-1’), 72.8 (C-2’), 75.3
(C-3’), 70.7 (C-4’), 77.3 (C-5’), 62.9 (C-6’), 64.5 (sn-
1-C), 72.2 (sn-2-C), 69.2 (sn-3-C), 22.04, 22.17 (C-15’’,
C-17’’’), 26.42, 26.53, 26.92, 27.04 (C-9’’, C-11’’’, C-12’’,
C-14’’’), 28.57, and 28.69 (C-6’’, C-8’’’).
Enzymatic hydrolysis of compound 1. a solution of
compound 1 (1 mg) and lipase type Xi (0.72 units, sigma)
in boric acid – borax buffer [0.63 mL, containing Triton
X-100 (2.5 mg), pH 7.7] was stirred at 38°C for 12 h. The
reaction was quenched with AcOH (0.1 mL) and then
EtOH was added to the reaction mixture. The solvent was
removed by N
2
gas and the residue was purified by a silica
gel column (CHCl
3
/MeOH, 12:1→7:1) to afford linolenic
acid and sn2-O -(hexadecatrienoyl)-monogalactosyl
glyceride (morimoto et al., 1995).
Determination of absolute configuration at C-2 in
compound 1. a solution of compound 1 (9.6 mg) and
NaOMe (10 equiv.) in anhyd. MeOH (0.1 mL) was stirred
at room temperature for 1 h. The reaction mixture was
partitioned between hexane and water and the water-
soluble materials were purified by a C
18
column (sep-Pak
C
18
cartridge 12 CC, Waters, H
2
O) and HPLC (TsKgel
amide-80, φ4.6×250 mm, TOSOH, 75% CH
3
CN, flow rate:
0.8 mL/min, RI detection) to give the β-galactosylglycerol
(2, 1.75 mg, 54%). The absolute configuration of 2 was
determined by comparison with the optical rotation (son
et al., 2001).
long day treatment under weak light
Arabidopsis thaliana were cultured at 24°C for 26 days
under sD. some plants were grown under sD throughout
the course of the experiment. The others were cultured for
several days under long day conditions (16 h-light and 8
h-dark, LD, ca. 2,500 lux), and then were grown under sD
until flower bud formation. The days for forming flower
bud was measured individually and averaged. means ±
sE showed of 3 replicates of 5 plants.
Bioassay
Thirty-day-old A. thaliana plants cultured at 24°C
under sD were used for bioassay. Before application,
one group of the assayed plants was exposed to LD for
pg_0003
HISAMATSU et al. — A bioactive substance of
A. thaliana
47
Figure 2. 2D NmR correlations of compound 1 (A) and β-galactosyl glycerol (2) derived from compound 1 (B).
one day (LD-1). it was shown that exposing to long
day condition for only 1 day (LD-1) give the plants only
slight promotion of forming flower bud (Figure 1). Then,
compound 1 in 50% aqueous acetone solutions of several
concentrations was applied to the center of rosette leaves
using microsyringe at intervals of 7 days. Twenty-days
after the onset of application, the number of plants formed
flower bud was counted. This experiment was repeated
twice.
reSultS
The aerial parts of A. thaliana in groups i, ii, and
iii were extracted with meOH, and the extracts were
partitioned between EtOac and H
2
O. The EtOac-soluble
materials were analysed by HPLC. some decreased peaks
were observed in t
R
50-80 min fraction of EtOac-soluble
materials obtained from group i in comparison with
those of groups ii and iii, while no increased peaks were
observed. as the result of further analysis, peak 1 was
most decreased in HPLC chromatogram of group i (Figure
1).
To identify the structure of compound 1 corresponded
to peak 1, the aerial parts of A. thaliana were extracted
with meOH, and the extract was partitioned between
EtOac and H
2
O. The EtOac-soluble portion was
separated by a reversed-phase column and C
18
HPLC to
afford compound 1.
The Esims of compound 1 showed a pseudomolecular
ion peak at m/z 769 (m+Na)
+
. The gross structure of
compound 1 was deduced from detailed analysis of the
1
H and
13
C NmR data aided with 2D NmR experiments
(
1
H-
1
H COsY, HmQC, and HmBC). The
13
C NmR data
of compound 1 indicated that the molecule possessed two
ester carbonyl carbons, six disubstituted olefins, one acetal
carbon, five oxymethines, three oxymethylenes, eighteen
methylenes, and two methyl groups. The
1
H-
1
H COsY
connectivities of C-1 to C-3 and C-1’ to C-6’ indicated the
presence of a glycerol and a sugar component. The sugar
was assigned to be galactose by NOEsY correlations of
H-1’ to H-3’ and H-5’ and H-4’ to H-3’ and H-5’ and the
1
H-
1
H coupling constants (J
1’, 2’
= 7.3 Hz, J
2’, 3’
= 7.4 Hz, J
3’,
4’
= 2.5 Hz, J
4’, 5’
= ~0 Hz). HMBC correlations of H-1’ to
C-3 (δ
C
69.2) and H-3a and H-3b to C-1’(δ
C
105.8) and the
coupling constant (J
1’, 2’
= 7.3 Hz) of the anomeric proton
(H-1’) at δ
H
4.27 revealed that compound 1 possessed a
β-galactosyl glycerol moiety.
The
1
H-
1
H COSY connectivities of C-2’’ to C-16’’
and C-2’’’ to C-18’’’ indicated the presence of two fatty
acids which contained three double bonds, respectively.
Z-Genometiries of six double bonds at C-7’’-C-8’’, C-10’’
-C-11’’, C-13’’-C-14’’, C-9’’’-C-10’’’, C-12’’’-C-13’’’, and
C-15’’’-C-16’’’ were deduced from the carbon chemical
shifts (δ
C
< 30) of allylic carbons (Gunstone et al., 1977).
The two fatty acids were presumed to be octadecatrienoic
acid and hexadecatrienoic acid judging from Esims of
compound 1. HmBC correlations of Ha-1 and Hb-1 to
ester carbonyl carbon (δ
C
175.5 or 175.1) and chemical
shifts (δ
H
5.31; δ
C
72.2) of C-2 indicated that the linolenic
acid and hexadecatrienoic acid connected to C-1 and
C-2. In order to define the locations of these fatty acids
in the β-galactosyl glycerol moiety of compound 1,
we applied enzymatic hydrolysis. The lipase type XI
(Sigma)-catalyzed hydrolysis of compound 1 afforded
sn2-O -(hexadecatrienoyl)-monogalactosyl glyceride
and linolenic acid (morimoto et al., 1995). Therefore,
compound 1 was identified as sn1-O-(octadecatrienoyl)-
sn2-O-(hexadecatrienoyl)-monogalactosyl diglyceride
(Figure 2). The absolute configuration at C-2 in the
β-galactosylglycerol (2 ), which was derived from
compound 1 with NaOme presumed to be R, from the
basis of comparison of the optical rotation ([α]
D
-8°) of 2
with the reported values ([α]
D
-7° for C-2 R and [α]
D
+2°
for C-2 s) (son et al., 2001).
and next, we applied compound 1 to A. thaliana to
examine its affection in flower bud formation. Before
assay, we measured how long it took for forming flower
buds of A. thaliana under light conditions described in
materials and methods. as shown in Figure 3, A. thaliana
under LD for one day acquired about 23 days for forming
flower buds, but the plants exposed LD for 3 days longer
took about 15 days (Figure 3). When the solution of
pg_0004
48
Botanical Studies, Vol. 47, 2006
Table 1. The effect of compound 1 on flower bud formation.
Flower-bud forming plants
a
assayed plants
Control
b
3 (14%)
21
50% acetone
b
4 (20%)
20
Compound 1 (10 ppm)
7 (47%)
15
Compound 1 (100 ppm)
8 (53%)
15
Compound 1 (1,000 ppm)
11 (58%)
19
a
Number of flower-bud forming plants at twenty-days after the application of test solution to the assayed plants.
b
Control cultures were applied for nothing, an equal volume of 50% acetone (as negative control).
compound 1 in 50% aqueous acetone solutions of several
concentrations applied to the center of rosette leaves of
assayed plants, which were exposed to LD for one day just
before onset of the bioassay, the 58% of the plants applied
compound 1 at 1,000 ppm formed flower bud, whereas
only 14% and 20% of the plants applied for nothing or
50% acetone have flower bud (Table 1). On the other
hand, flower bud of the plants not exposed to LD were not
promoted by compound 1 (data not shown).
dIScuSSIon
in Arabidopsis thaliana, large amount of studies on
flower bud formation from genetic point of view have
been carried out. However, bioactive substances involved
in flowering of A. thaliana have been hardly reported.
in this study, therefore, we exhibited the isolation of
bioactive substances involved in flower bud formation of
A. thaliana.
The aerial parts of A. thaliana in groups i, ii, and
iii were extracted with meOH, and the extracts were
partitioned between EtOac and H
2
O. The EtOac-soluble
materials were analysed by HPLC. some decreased
peaks were observed in t
R
50-80 min fraction of EtOac-
soluble materials obtained from group i in comparison
with those of groups ii and iii, while increased peaks
weren’t observed. The decrease of peak 1 after flower
bud formation suggested that the substance including
peak 1 was metabolized to bioactive substance (s) when
flower bud was formed and in groups II and III, the peak
1 was not decreased as they were not formed flower bud.
Therefore, we further separated the fraction to afford
the substance of peak 1, which was named compound 1
(Figure 1). as a result, sn1-O-(octadecatrienoyl)-sn2-
O -(hexadecatrienoyl)-monogalactosyl diglyceride (1),
which corresponded to the most decreased HPLC peak,
was isolated from EtOac-soluble materials of A. thaliana
(Figure 2).
and next, we measured how long it took for forming
flower buds of A. thaliana under light conditions described
in materials and methods. it took about 23 days until
the flower buds under LD for one day were formed, but
the flower buds under LD for 3 days longer were formed
after about 15 days from the start of LD treatment (Figure
Figure 3. The effects of long day treatment related to flower
buds formation. sD: grown under short day condtions (8 h-light
and 16 h-dark, sD, ca. 3,800 lux) throughout the course of
the experiment, LD-1~7: cultured for 1-7 days under long day
conditions (16 h-light and 8 h-dark, LD, ca. 2,500 lux), and
were backed to sD, C-LD: cultured under LD until form ing
flower bud. The days for forming flower bud was measured
individually and averaged. means ± sE showed of 3 replicates
of 5 plants.
3). it suggested that exposing to LD for one day was
not enough for A. thaliana to change from vegetative to
reproductive growth under the long day conditions, and
slightly promoted the flower buds formation. Therefore
we assayed compound 1 to the plants exposed LD for one
day.
The solution of compound 1 in 50% aqueous acetone
of several concentrations was applied to the center of
rosette leaves of assayed plants that exposed to LD for one
day just before onset of the bioassay, and their effects on
flower bud formation was tested (Table 1). Compound
1 induced significantly flower bud formation, whereas
flower bud formation of the plants applied for nothing or
50% acetone wasn’t promoted. On the other hand, flower
bud of the plants not exposed to LD was not induced by
compound 1 (data not shown). These results suggest that
compound 1 is metabolized to the bioactive substance
(s) inducing flower bud by exposed to LD, and which
compound 1 was not metabolized to those by not exposed
to LD. so it envisaged that compound 1 is the precursor
pg_0005
HISAMATSU et al. — A bioactive substance of
A. thaliana
49
or the substrate of flower bud-inducing substance (s).
Compound 1 may play important roles in flower bud
formation of A. thaliana.
Compound 1 is one of monogalactosyl diglycerides
(mGDG), which are major constituents of the chloloplast
membrane in plants and recently, they were draw much
attention because of their various biological activity.
For example, mGDG is the stores of fatty acids that
are substrates of various bioactive substances, such as
jasmonic acid, 9, 10-ketol-octadecadienoic acid (KODa),
sn1-O-(12-oxophytodienoyl)-sn2-O-(hexadecatrienoyl)-
monogalactosyl glyceride (mGDG-O), and arabidopsides
a and B (Vick and Zimmerman, 1984; Yokoyama
et al., 2000; stelmach et al., 2001; Hisamatsu et al.,
2003). Jasmonic acid is one of the phytohormone which
stimulates or inhibits several events in plant growth and
development, while KODa was known to related to
flower induction of Lemna paucicostata and Pharbitis
nil (Miersch et al., 1999; Suzuki et al., 2003). MGDG-O
and arabidopsides a and B are rare mGDG containing
OPDa and/or dn-OPDa, which are precursors of
jasmonic acid (Baertschi et al., 1988; Weber et al., 1997).
Furthermore, as compound 1 induced flower bud of the
plants exposed to LD-1, it suggested bioactive substances
regulating flower bud formation of A. thaliana is also one
of the metabolites of mGDG. We are now studying the
substances derived from MGDG and their effect for flower
bud formation.
lIterAture cIted
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M. Mizoguchi, F. Yano, Y. Todoroki, N. Watanabe, and
M. Yokoyama. 2003. Endogenous α-ketol linolenic acid
levels in short day-induced cotyledons are closely related
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35-43.
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induced factors involved in flower formation of Lemna.
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Vick, B. and D. Zimmerman. 1984. Biosynthesis of jasmonic
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pg_0006
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Botanical Studies, Vol. 47, 2006
一種糖脂涉及阿拉伯芥之花芽形成
Yosuke HisamaTsu
1
, Nobuharu GOTO
2
, Koji HasEGaWa
1
, and Hideyuki
sHiGEmORi
1
1
Graduate school of Life and Environmental sciences,
university of Tsukuba, Tsukuba 305-8572, Japan
2
Department of Biology, miyagi university of Education,
sendai 980-0845, Japan
我們追尋阿拉伯芥 (Arabidopsis thaliana) 涉及花芽形成之生理活性物½。比較花芽形成- 及未發芽
形成- 之發育階段的抽取液於 HPLC 檢測時發現前者有下降之若干.值。化合物 1,此乃減少最明顯之
.值,係單離自阿拉伯芥之地上部。從核磁共振儀及½譜儀之數據得知化合物 1 乃單半乳糖-雙酸甘油
(mGDG)。當阿拉伯芥暴露於長日照只一天時,添加化合物1 可誘導花芽形成。這些結果顯示:化合物
1 可能為花芽形成物½之前驅體或基½,因此乃阿拉伯芥花芽形成之一重要成份。
關鍵詞:花芽形成;阿拉伯芥;短日照;長日照;單半乳糖-雙酸甘油;生理活性物½。