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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
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)
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