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Journal of Plant Physiology 169 (2012) 1471–1476

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Journal of Plant Physiology


journal homepage: www.elsevier.de/jplph

Absorption of momilactone A and B by Arabidopsis thaliana L. and the growth


inhibitory effects
Hisashi Kato-Noguchi ∗ , Katsumi Ota, Hiroya Kujime
Department of Applied Biological Science, Faculty of Agriculture, Kagawa University, Miki, Kagawa 761-0795, Japan

a r t i c l e i n f o a b s t r a c t

Article history: Although most allelochemicals can potentially cause growth inhibition in receiver plants, there is little
Received 31 January 2012 information available about the absorption of these allelochemicals by the receiver plants. The present
Received in revised form 22 May 2012 research describes the absorption of momilactone A and B by Arabidopsis thaliana (L.) and effects of the
Accepted 23 May 2012
absorption on Arabidopsis growth. Exogenously applied momilactone A and B inhibited the growth of
Arabidopsis hypocotyls and roots at concentrations greater than 10 and 1 ␮mol/L, respectively. The levels
Keywords:
of momilactone A and B in Arabidopsis hypocotyls were approximately 3.2 and 2.4% of momilactone A
Allelochemical
and B, respectively, in the medium and those in Arabidopsis roots were about 3.9–3.4%, respectively.
Arabidopsis
Absorption
The absorption rates of momilactone A and B by Arabidopsis were not significantly different. The present
Growth inhibitor research suggests that momilactone A and B may be absorbed in proportion to their applied levels,
Momilactone and the growth inhibitory effects of momilactone A and B may also correlated with their endogenous
levels. However, the effectiveness of momilactone B on growth inhibition was much greater than that of
momilactone A, and the sensitivities of hypocotyls to momilactone A and B were greater than those of
roots. This is the first report describing the absorption of potent rice allelochemicals, momilactone A and
B by receiver plants.
© 2012 Elsevier GmbH. All rights reserved.

Introduction Several phenolic acids have been found in rice root exudates.
However, considering the inhibitory activity of phenolic acids, the
A large number of rice cultivars have been found to inhibit the secretion level of these phenolic acids from rice was insufficient to
growth of several plant species when these rice cultivars were cause growth inhibition of neighboring plants. In addition, allelo-
grown together with these plants under field and/or laboratory con- pathic rice cultivars did not secrete significantly greater amounts
ditions (Dilday et al., 1989, 1994, 1998; Kim et al., 1999; Olofsdotter of phenolic acids than non-allelopathic cultivars (Olofsdotter et al.,
et al., 1999; Azmi et al., 2000; Gealy et al., 2003; Seal et al., 2004a; 2002; Seal et al., 2004b).
Kim et al., 2005). These findings suggest that living rice may possess A potent growth inhibitory substance has been isolated from
allelopathic potential and secrete allelochemicals into its neighbor- root exudates of the rice cultivar Koshihikari and identified as
ing environment. momilactone B (Kato-Noguchi et al., 2002). Momilactone B inhibits
Many secondary compounds, such as hydroxamic acids, fatty the growth of the typical rice weed, Echinochloa crus-galli (L.) Beauv.
acids, terpenes and indoles, have been isolated from rice plants by at concentrations greater than 1 ␮mol/L. Rice plants secrete momi-
organic and aqueous solvents as candidates for rice allelochem- lactone B from the roots into the rhizosphere over their entire
icals (Rimando and Duke, 2003). However, it is not yet clear if life cycle (Kato-Noguchi et al., 2008b). Considering the growth
these compounds are secreted from living rice plants and act as inhibitory activity and secretion level, momilactone B is enough
rice allelochemicals. Although most plant tissues contain poten- to cause growth inhibition of neighboring plants (Kato-Noguchi
tial allelochemicals, only compounds released from the plants into et al., 2010). The secretion of momilactone B has also been con-
the environment have the potential to inhibit the germination and firmed for other rice cultivars (Kong et al., 2004; Kato-Noguchi
growth of neighboring plant species and act as allelochemicals et al., 2010). These observations suggest that momilactone B,
(Putnam and Tang, 1986). among other rice allelochemicals, may play a critical role in rice
allelopathy. This hypothesis was recently supported strongly by
the findings of a genetic approach (Xu et al., 2012). In addition,
momilactone A was later found to be secreted by rice into the
∗ Corresponding author. Tel.: +81 87 891 3086; fax: +81 87 891 3086. rhizosphere and inhibited the growth E. crus-galli at concentra-
E-mail address: hisashi@ag.kagawa-u.ac.jp (H. Kato-Noguchi). tions greater than 10 ␮mol/L (Kato-Noguchi et al., 2008a). Thus,

0176-1617/$ – see front matter © 2012 Elsevier GmbH. All rights reserved.
http://dx.doi.org/10.1016/j.jplph.2012.05.022
1472 H. Kato-Noguchi et al. / Journal of Plant Physiology 169 (2012) 1471–1476

momilactone A cannot be excluded as a possible rice allelochemi- Determination of momilactone A and B


cal.
However, there has been no information available about the Ten Arabidopsis seedlings were extracted with 10 mL of 50%
mode of action of momilactone A and B on growth inhibition or aqueous methanol for 24 h. After filtration, the extracts were then
allelopathic activity. The very first event causing the growth inhi- loaded onto a reverse-phase C18 Sep-Pak cartridge (Waters). The
bition on receiver plants by momilactone A and B is probably cartridge was first eluted with 50% aqueous methanol to remove
the absorption by the receiver plants. There is also no informa- impurities, and then eluted with methanol to release momilac-
tion available about the absorption of momilactone A and B by tone A and B. Methanol eluate were concentrated to 1 mL and
receiver plants. This study focused on understanding the absorption analyzed by liquid chromatography–tandem mass spectrometry
of momilactone A and B by the receiver plants. Therefore, allelo- (LC–MS/MS) with the positive-ion mode and nitrogen for the col-
pathic activities of momilactone A and B against the typical model lision gas (10–50 ␮L injection volume). Momilactone A and B,
plant, Arabidopsis, and the absorption level of exogenously applied respectively, were detected in the multiple-reaction monitoring
momilactone A and B by Arabidopsis were determined as the first mode by the combination of m/z 315 and 217, and the combina-
event causing the growth inhibition. tion of m/z 331 and 268. Quantification of momilactone A and B
was performed as described by Obara et al. (2002). The determina-
tion of momilactone A and B was performed for seven independent
Materials and methods experiments with three injections to LC–MS/MS per experiment.
The overall recovery of momilactone A and B added to the solution
Isolation of momilactone A and B for the extraction before filtration was 87 and 85% as calculated
from five replications.
Momilactone A and B were isolated from husks of rice (Oryza
sativa L. cv. Koshihikari) and identified by 1 H and 13 C NMR spectra
Results and discussion
as described by Kato-Noguchi et al. (2002, 2008b).

Effects of momilactone A and B on Arabidopsis


Bioassay of momilactone A and B
The biological activities of momilactone A and B isolated from
rice husks were determined with the model plant Arabidop-
Seeds of Arabidopsis thaliana (L.) ecotype Columbia (Co-0) were
sis. Momilactone A and B inhibited the growth of Arabidopsis
surface sterilized in a 2% (w/v) solution of sodium hypochlorite for
hypocotyls and roots at concentrations greater than 30 and
15 min and rinsed four times in distilled water. The seeds were ger-
1 ␮mol/L (P < 0.01, Tukey’s test), respectively (Figs. 1 and 2).
minated on two sheets of moist filter paper (No. 1; Toyo Ltd., Tokyo)
Increasing concentrations of momilactone A and B increased inhi-
at 4 ◦ C in dark for three days and at 22 ◦ C with a 12-h photoperiod
bitions, but maximum inhibition by momilactone A was about
for another one day.
60–70% at the concentrations tested.
Momilactone A and B were dissolved in 1 mL methanol (0,
When inhibition of Arabidopsis hypocotyls and roots were plot-
0.03, 0.1, 0.3, 1, 3, 10, 30, 100, 300, 1000, 3000, 10,000 and
ted against the logarithm of momilactone A and B concentrations
30,000 ␮mol/L), added to two sheets of filter paper (No. 2) in a 5.5-
as described by Streibig (1998), significant logistic functions were
cm Petri dish. Methanol was subsequently evaporated and the filter
obtained. The equations of the functions of momilactone A were Y =
paper in the Petri dishes was moistened with 3 mL of a 0.05% (v/v)
[(0.414 − 76.699)/{1 + (X/54.592)1.423 }] + 76.699; (r2 = 0.958) and
aqueous solution of Tween 20. The final concentrations of momilac-
Y = [(0.091 − 64.655)/{1 + (X/62.214)1.035 }] + 64.655; (r2 = 0.973) for
tone A and B were 0, 0.01, 0.03, 0.1, 0.3, 1, 3, 10, 30, 100, 300, 1000,
hypocotyls and roots, respectively, and those of momilactone
3000 and 10,000 ␮mol/L. Ten uniform Arabidopsis seedlings, germi-
B were Y = [(−0.198 − 95.571)/{1+ (X/5.898)0.942 }]+ 95.571; (r2 =
nated as describe above, were then transferred to 5.5-cm Petri dish,
0.987) and Y = [(−0.183 − 90.995)/{1 + (X/9.459)0.843 }] + 90.995;
and grown at 22 ◦ C with a 12-h photoperiod for three days. Only
(r2 = 0.958) for hypocotyls and roots, respectively.
roots of Arabidopsis seedlings were immersed in the solution during
The concentrations required for 50% growth inhibition (I50 ) of
the incubation. The lengths of hypocotyls and roots of the Arabidop-
Arabidopsis hypocotyls and roots in the bioassay were calculated
sis seedlings were measured. Control seedlings were grown on the
from the equations and are summarized in Table 1A. Comparing
filter paper moistened with 3 mL of a 0.05% (v/v) aqueous solution
I50 values, the inhibitory activity of momilactone B on Arabidopsis
of Tween 20. Percentage inhibition was determined by the formula:
hypocotyls and roots, respectively, was 13- and 17-fold greater than
[(control plant length − plant length incubated with momilactone
that of momilactone A. Momilactone A and B have been shown to
A or B)/control plant length] × 100. The experiments were repeated
inhibit several plant species and the activity of momilactone B was
five times independently with three Petri dishes (10 plants for each
also much greater than that of momilactone A in all other bioassays
Petri dish) (n = 150).
(Takahashi et al., 1976; Kato et al., 1977; Lee et al., 1999; Kato-
The inhibition of Arabidopsis hypocotyls and roots were then
Noguchi et al., 2008b).
plotted against the logarithm of momilactone A and B con-
centrations and the dose–response curves were drawn using a
logistic function (sigmoid curves) as described by Streibig (1988): Absorption of momilactone A and B by Arabidopsis
Y = (A1 –A2 )/{1 + (X/Xo ) p } + A2 . Y: growth inhibition (%), X: concen-
tration (␮mol/L) of momilactone A or B, A1 : initial value (lower There was no endogenous momilactone A and B in Arabidop-
asymptote), A2 : final value (higher asymptote), Xo ; values at Y50 . sis hypocotyls or roots (data not shown), which indicates that
The concentrations required for 50% growth inhibition (I50 ) of Ara- Arabidopsis does not have a pathway of momilactone A and B
bidopsis hypocotyls and roots in the bioassay were calculated by production. However, when Arabidopsis was incubated with momi-
the equations (X value at Y50 ). lactone A and B, momilactone A and B were found in the hypocotyls
For determination of momilactone A and B concentrations in and roots (Figs. 3 and 4). In addition, only Arabidopsis roots were
Arabidopsis, the Arabidopsis seedlings were washed in distilled contacted with the test solution and, thus, it is suggested that
water, dried with filter paper, frozen immediately in liquid nitrogen Arabidopsis may absorb both momilactones by roots and transport
and stored at −80 ◦ C. momilactone A and B to hypocotyls.
H. Kato-Noguchi et al. / Journal of Plant Physiology 169 (2012) 1471–1476 1473

Fig. 1. Effects of momilactone A on hypocotyl and root growth of Arabidopsis seedlings. Percentage inhibition was determined by the formula: [(control plant length − plant
length incubated with momilactone A)/control plant length] × 100. Means ± SE from five independent experiments with three replicates for each treatment are shown
(n = 150).

Fig. 2. Effects of momilactone B on hypocotyl and root growth of Arabidopsis seedlings. Percentage inhibition was determined by the formula: [(control plant length − plant
length incubated with momilactone B)/control plant length] × 100. Other details as for Fig. 1.

Momilactone A and B levels in Arabidopsis hypocotyls and Thus, the absorption levels of momilactone A and B by Arabidopsis
roots (Figs. 3 and 4) were significantly (P < 0.01) correlated with increased in proportion to the exogenous levels of momilactone A
exogenously applied momilactone A and B. The regression coeffi- and B.
cient (r2 ) of momilactone A was 0.943 and 0.962 for Arabidopsis When 10 seedlings of Arabidopsis were incubated in 3 mL
hypocotyls and roots, respectively, and that of momilactone B was medium of 1000 ␮mol/L momilactone B, 3000 nmol molecules of
0.972 and 0.954 for Arabidopsis hypocotyls and roots, respectively. momilactone B were in the medium. After incubation for three

Table 1
I50 values of momilactone A and B for hypocotyl and root growth of Arabidopsis. (A) I50 (␮mol/L) calculated from the equations of Figs. 1 and 2. (B) I50 (nmol/plant) calculated
from the equations of Figs. 5 and 6.

(A) Exogenous level (Figs. 1 and 2) (B) Endogenous level (Figs. 5 and 6)

Hypocotyl Root Hypocotyl Root

Momilactone A 84.4 203.3 0.93 8.5


Momilactone B 6.5 12.0 0.09 0.95
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Fig. 3. Momilactone A level in Arabidopsis hypocotyls and roots. Ten Arabidopsis seedlings were incubated with momilactone A in 3 mL medium for three days and the
momilactone A level in Arabidopsis was then determined. Control Arabidopsis hypocotyls and roots (0 ␮mol/L momilactone A application) did not contain momilactone A.
Means from seven independent experiments with three replicates for each cultivar are shown (n = 21).

days, 9.7 and 7.4 nmol molecules of momilactone A and B, respec- were significantly greater than those in the hypocotyls at 5% level
tively, were found in one Arabidopsis hypocotyl (Fig. 4). Thus, 10 of probability (ANOVA).
hypocotyls contained 97 and 74 nmol molecules of momilactone A
and B, respectively, which was 3.2 and 2.4% of momilactone A and Effectiveness of momilactone A and B on Arabidopsis
B molecules in the medium, respectively, with no consideration of
momilactone degradation in Arabidopsis because those degradation Exogenously applied momilactone A and B was absorbed
and detoxification processes are unknown. Momilactone A and B in by Arabidopsis (Figs. 3 and 4) and caused growth inhibition
Arabidopsis roots were 3.9 and 3.4%, respectively. (Figs. 1 and 2). Therefore, the relationship between the momi-
In addition, momilactone A levels in the hypocotyls and roots lactone A and B levels in Arabidopsis and the magnitude of the
were not significantly different from momilactone B levels in growth inhibition was determined. As a result, logistic functions
the hypocotyls and roots (Figs. 3 and 4), which suggest that the were obtained (Figs. 5 and 6) when exogenously applied momi-
absorption rates of momilactone A and B by Arabidopsis were lactone A and B concentrations on the X-axis in Figs. 1 and 2,
similar. However, the levels of momilactone A and B in the roots respectively, were replaced by corresponding momilactone A

Fig. 4. Momilactone B level in Arabidopsis hypocotyls and roots. Ten Arabidopsis seedlings were incubated with momilactone B in 3 mL medium for three days and momilactone
B level in Arabidopsis was then determined. Control Arabidopsis hypocotyls and roots (0 ␮mol/L momilactone B application) did not contain momilactone B. Other details as
for Fig. 3.
H. Kato-Noguchi et al. / Journal of Plant Physiology 169 (2012) 1471–1476 1475

Fig. 5. The potential growth inhibition of momilactone A found in Arabidopsis on Arabidopsis hypocotyl and root growth. Exogenously applied momilactone A concentrations
in X-axis in Fig. 1 were replaced by momilactone A and B concentrations found in Arabidopsis hypocotyls and roots on Y-axis in Fig. 3.

and B levels in Arabidopsis based on results in Figs. 3 and 4. 0.93 and 8.5 nmol of momilactone A inhibited 50% of Arabidopsis
The equations of logistic functions of momilactone A were hypocotyl and root growth, respectively, and 0.09 and 0.95 nmol of
Y = [(0.667 − 76.507)/{1 + (X/0.625)1.548 }] + 76.507; (r2 = 0.962) and momilactone B inhibited 50% of Arabidopsis hypocotyl and root
Y = [(1.326 − 69.177)/{1 + (X/4.521)1.474 }] + 69.177; (r2 = 0.957) for growth, respectively. With respect to I50 values, the inhibitory
hypocotyls and roots, respectively, and those of momilactone activity of momilactone B on Arabidopsis hypocotyls and roots,
B were Y = [(−146.42 − 97.081)/{1 + (X/0.007)0.564 }] + 97.081; respectively, was 10- and 8.9-fold greater than that of momilac-
(r2 = 0.939) and Y = [(−26.435 − 131.14)/{1 + (X/1.097)0.429 }] + tone A, which is consistent with previously findings that growth
2
131.14; (r = 0.968) for hypocotyls and roots, respectively. Y in inhibitory activity of exogenously applied momilactone B was
the equations indicates the growth inhibition (%) and X indicates much greater than that of momilactone A (Takahashi et al., 1976;
momilactone A or B level in Arabidopsis (nmol/plant). These Kato et al., 1977; Lee et al., 1999; Kato-Noguchi et al., 2008b). Fur-
results suggest that the growth inhibition by momilactone A and B thermore, the effectiveness of momilactone A and B in Arabidopsis
depends on the endogenous levels of momilactone A and B in the hypocotyls, respectively, was 9.1- and 11-fold greater than that in
seedlings. Arabidopsis roots.
I50 values of Arabidopsis hypocotyls and roots were calculated The ratios of I50 values for hypocotyls calculated from momi-
from the equations and summarized in Table 1B, which shows lactone A and B in Arabidopsis (Table 1B) against I50 values for

Fig. 6. The potential growth inhibition of momilactone B found in Arabidopsis on Arabidopsis hypocotyl and root growth. Exogenously applied momilactone B concentrations
in X-axis in Fig. 2 were replaced by momilactone B concentrations found in Arabidopsis hypocotyls and roots in Y-axis in Fig. 4.
1476 H. Kato-Noguchi et al. / Journal of Plant Physiology 169 (2012) 1471–1476

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