Allelopathic Potential of Rhus Chinensis on Seedling Growth of Radish, Semen Cassiae and Black Soyabean

J. For. Res. DOI 10.1007/s11676-015-0041-0

ORIGINAL PAPER

Allelopathic potential of Rhus chinensis on seedling growth of radish, semen cassiae and black soyabean

Long-yuan Liu • Hong-zhi He • Shi-ming Luo • Hua-shou Li

Received: 23 September 2013 / Accepted: 14 January 2014 Ó Northeast Forestry University and Springer-Verlag Berlin Heidelberg 2015

Abstract The allelopathic potential of Rhus chinensis semen cassiae and black soyabean seedling growth were Mill on seedling growth of radish (Raphanus sativus L.), -0.88, -0.93 and -0.98 respectively. The results sug- semen cassiae (seed of Cassia obtusifolia L.) and black gested that it is important to minimize the negative alle- soyabean [Glycine max (L.) Merr.] was investigated under lopathic potential of R. chinensis in agroforestry systems, laboratory conditions. The water extracts of seed, leaf and and to exploit this traditional Chinese medicinal tree for the bark of R. chinensis inhibited the germination and the production of natural bio-pesticides. growth of roots and shoots of radish, semen cassiae, and black soyabean. Significant increasing reductions in the Keywords Allelopathy Rhus chinensis Water extracts germination and growth of roots and shoots were observed Seedling growth as the concentration of water extract increased in all bioassays. The order of allelopathic potentials of the three parts from R. chinensis plant on seed germination of these Introduction receptors was leaf [ seed [ bark. However, the inhibition of water extracts from R. chinensis seed on root activity of The species Rhus chinensis Mill (Anacardiaceae) is an semen cassiae was more severe than from the other two important species of the genus Rhus, which contains over parts. The allelopathic potential on the germination of 250 individual species, with six species found in China radish was higher than that of black soyabean and semen (Djakpo and Yao 2010). It is an important economic tree cassiae. The integrated effect index for allelopathic not only widely grown in China, but also widely distributed potential of water extracts of leaf of R. chinensis on radish, in temperate, subtropical, and tropical regions, including Japan, Malaysia and India (Rayne and Mazza 2007; Ren Project funding: The work was financially supported by the Major et al. 2008). As a traditional Chinese medicinal plant, R. State Basic Research Development Program (973) of China (No. chinensis has long been used to treat diseases, such as 2011CB100400) and Sci-technology Program of Guangdong Province inflammation, impaludism, endocrine disorder, rheumatism (No. 0203-E12147). and peptic ulcer disease (Rayne and Mazza 2007; Djakpo The online version is available at http://www.link.springer.com and Yao 2010). R. chinensis can also be used as a host plant for the production of gallnut which is also used in tradi- Corresponding editor: Hu Yanbo tional Chinese medicine and as a dyeing material (Tian et al. 2009). R. chinensis has been applied in agroforestry L. Liu systems by intercropping with other plants. It has been School of Chemistry and Chemical Engineering, Guangdong Pharmaceutical University, Zhongshan 528458, China revealed that extracts of R. chinensis possess strong anti- viral, antibacterial, anticancer, hepatoprotective, antidiar- L. Liu H. He S. Luo H. Li (&) rheal and antioxidant capacities (Ahn et al. 1998; Kim et al. Key Laboratory of Tropical Agricultural Environment in South 2005; Gu et al. 2007; Wang et al. 2008; Chen et al. 2009; China, the Ministry of Agriculture, People’s Republic of China, South China Agricultural University, Guangzhou 510642, China Djakpo and Yao 2010). Moreover, the root, leaf, stem and e-mail: [email protected] fruit of R. chinensis have been used as pesticides by 123 L. Liu et al.

(a)Leaf (b) 100.00 Leaf 100.00

80.00 80.00

60.00 60.00

40.00 40.00 Percent germination Percent germination

20.00 20.00

0.00 0.00 1234567 1234567 Days after sowing Days after sowing

CK 200mg•l ¹ 100mg•l ¹ CK 200mg•l ¹ 100mg•l ¹ 50mg•l ¹ 33mg•l ¹ 25mg•l ¹ 50mg•l ¹ 33mg•l ¹ 25mg•l ¹

Bark 100.00 90.00 80.00 100.00 Bark 70.00 60.00 80.00 50.00 60.00 40.00 Percent germination Percent germination 30.00 40.00 20.00 20.00 10.00 0.00 0.00 1234567 1234567 Days after sowing Days after sowing

CK 200mg•l ¹ 100mg•l ¹ CK 200mg•l ¹ 100mg•l ¹ 50mg•l ¹ 33mg•l ¹ 25mg•l ¹ 50mg•l ¹ 33mg•l ¹ 25mg•l ¹

100.00 Seed

80.00 Seed 100.00 60.00 80.00

40.00 60.00

Percent germination 40.00 20.00

Percent germination 20.00

0.00 0.00 1234567 1234567 Days after sowing Days after sowing

CK 200mg•l ¹ 100mg•l ¹ CK 200mg•l ¹ 100mg•l ¹ 50mg•l ¹ 33mg•l ¹ 25mg•l ¹ 50mg•l ¹ 33mg•l ¹ 25mg•l ¹

Fig. 1 a Effects of water extracts of leaf, bark and seed of R. germination of semen cassiae. Data are the means of three replicates chinensis at different concentrations (200, 100, 50, 33 and 25 mg with standard errors shown by vertical bars. c Effects of water fresh weight of sample per L distilled water) on the germination trend extracts of leaf, bark and seed of R. chinensis at different concen- of radish. Data are the means of three replicates with standard errors trations (200, 100, 50, 33 and 25 mg fresh weight of sample per L shown by vertical bars. b Effects of water extracts of leaf, bark and distilled water) on the germination of black soyabean. Data are the seed of R. chinensis at different concentrations (200, 100, 50, 33 and means of three replicates with standard errors shown by vertical 25 mg fresh weight of sample per L distilled water) on the bars

123 Allelopathic potential of R. chinensis

Leaf soyabean [Glycine max (L.) Merr.] were acquired from a CK 200mg•l ¹ 100.00 local market. 100mg•l ¹ 50mg•l ¹ 33mg•l ¹ 25mg•l ¹ R. chinensis plants were isolated from other trees with at 80.00 least 1 year of normal growth. Bark of R. chinensis was removed from trunks at heights C50 cm above the ground. 60.00 Only half of the bark was scraped from the trunk in order to 40.00 ensure survival of the trees. Healthy leaves in dark green

Percent germination and seeds with white coats were collected. Dried bark, 20.00 seeds and leaves were separately cut into 6 cm long pieces 0.00 and then powdered in a grinder until 98 % of the powder 1234567 could pass through No. 1 sieve (10 mesh) and 30 % of the Days after sowing powder could pass through No. 2 sieve (24 mesh). The

Bark powder samples were extracted with five times their weight of distilled water in an 8 L beaker with oscillation of CK 200mg•l ¹ 100.00 100mg•l ¹ 50mg•l ¹ 30 min every 12 h for 48 h in the dark. And then the 80.00 33mg•l ¹ 25mg•l ¹ mixture was filtered through a paper filter. The filtrates were collected and adjusted to five levels: 200, 100, 50, 33 60.00 and 25 mg fresh weight of sample per L distilled water. 40.00 The solutions were preserved in brown bottles at 4 °C.

Percent germination 20.00 Bioassays 0.00 1234567 Days after sowing For seed germination tests, seeds were soaked with 5.25 % (w/v) sodium hypochlorite solution for 15 min, rinsed three 100.00 Seed times with distilled water and then evenly placed on a two-

80.00 layer paper filter in sterilized 9 cm Petri dishes. Extracts of CK 200mg•l ¹ different parts of the donor plant were added to dishes until 100mg•l ¹ 50mg•l ¹ 60.00 2 mm above the seed layer. Each treatment with three 33mg•l ¹ 25mg•l ¹ replicates and an additional distilled water treatment as 40.00 control were used. Dishes were put in an incubator at Percent germination constant temperature of 25 °C, 85 % humidity and 12 h 20.00 light per day. The volume of the test solutions was made up to maintain the original level every day and the numbers of 0.00 germinated seeds were recorded every day for 7 days. The 1234567 root lengths were also measured each day. The root activity Days after sowing vigor of semen cassiae was measured by TTC Method (Li 2009) on day 7. Fig. 1 continued farmers in South China. Could R. chinensis impose alle- Statistical analyses lopathic effects on its neighboring species within a plant community? We report here on the allelopathic potential of Data were analyzed by one-way analysis of variance R. chinensis on seedling growth of radish, semen cassiae (ANOVA) using SPSS PASW Statistics v18.0 software and black soyabean. (SPSS Statistics, Shanghai, China). Duncan’s new multiple range tests were calculated when treatments were significantly different at a = 0.05. Materials and methods GerminationÀ rateðÞ GR, % Extraction ¼ number ofÁ germinated seeds by day 7 / total number of test seeds 100: Rhus chinensis Mill and semen Cassiae (seed of Cassia obtusifolia L.) were obtained from the medicine nursery on The equations for calculation of relative inhibition index the Zhongshan campus of Guangdong Pharmaceutical (RI) for receptor plant according to Williamson and University. Radish (Raphanus sativus L.) and black Richardson (1988) were as follows: 123 L. Liu et al. 1 C=T when T C three receptor species. The increase of water extract con- RI ¼ ; T=C 1 when T\C centrations resulted in decreasing germination rates. The order of inhibitory intensity of the same concentration of where C and T represent the response of control and donor water extracts on germination rates of the receptors treatment, respectively. When RI C 0, it represents stimu- was leaf [ seed [ bark. Inhibitory effects were stronger on lation effects and when RI \ 0, it shows inhibitory effects. radish than on black soyabean or semen cassiae (Fig. 1). The absolute value of RI represents the magnitude of the effects. The integrated effects were assessed using inte- Allelopathic potential of donor water extracts grated effect index (IEI), which is the average value of on receptors response indexes (RI). Seeds of the three receptor species had different sensitivities to the water extracts of leaf, bark, and seed of R. Chinensis Results (Table 1). The increase of water extract concentrations resulted in increasing inhibitory effects. The IEI values of Effects of donor water extracts on receptors’ seed water extracts of leaf on radish, semen cassiae, and black germination soyabean were -0.88, -0.93 and -0.98, respectively. The IEI values of water extracts of bark on these three receptors As shown in Fig. 1, the extracts from different tissues of R. were -0.36, -0.32 and -0.45, respectively. The IEI values chinensis significantly inhibited and delayed seed germi- of water extracts of seed on these three receptors were -0.69, nation of the three receptors. The intensity of inhibition -0.65 and -0.95, respectively. increased with increasing extract concentration. High concentrations of extracts at 100 and 200 mgL-1 appar- ently totally inhibited the germination of radish. Radish Effects of donor water extracts on receptors seedlings’ seed completed its germination at the 4th day in the control root length treatment, but germination of other treatments was delayed up to the 7th day (Fig. 1a). Inhibitory effects were stronger Comparison of the five longest seedling root lengths by on radish than on black soyabean or semen cassiae. treatment, showed that water extracts of leaf, bark and seed The extracts of different tissues of R. chinensis had of R. chinensis significantly inhibited the root growth of significant inhibitory effects on germination rates of the radish, semen cassiae and black soyabean (Fig. 2). Increase

Table 1 Relative inhibition Plant part Extraction RI index (RI) and integrated effect concentration (mgL-1) index (IEI) of the three receptor Radish Semen cassiae Black soyabean plants by R. chinensis water extracts Leaf 200 -1.00 -1.00 -1.00 100 -0.99 -1.00 -1.00 50 -0.99 -1.00 -0.97 33 -0.88 -0.86 -0.99 25 -0.54 -0.80 -0.96 IEI -0.88 -0.93 -0.98 Bark 200 -0.81 -0.86 -0.75 100 -0.41 -0.19 -0.54 50 -0.29 -0.27 -0.33 33 -0.08 -0.14 -0.42 25 -0.19 -0.12 -0.20 IEI -0.36 -0.32 -0.45 Seed 200 -0.98 -0.99 -1.00 100 -0.97 -0.91 -1.00 50 -0.71 -0.43 -0.95 33 -0.31 -0.49 -0.89 25 -0.51 -0.42 -0.94 IEI -0.69 -0.65 -0.95 IEI integrated effect index

123 Allelopathic potential of R. chinensis

(a) 20.00 a Effects of donor water extracts on semen cassiae root 18.00 activity 16.00 14.00 Leaf Bark Seed All tissues from R. chinensis exhibited signiﬁcant inhibition 12.00 effects on root activity vigor of seedlings of semen cassiae. 10.00 The greatest inhibition effect was associated with the seeds b 8.00 of R. chinensis and the least inhibition effect was associated 6.00 c c with the leaves of R. chinensis. Water extracts at 25 mgL-1 Rootstock length (cm) Rootstock 4.00 d d from leaf, bark and seed of R. chinensis reduced root activity 2.00 d d d d d 0.00 vigor to 82.43, 32.97 and 27.28 %, respectively. The root CK 200 100 50 33 25 activity vigor of semen cassiae decreased to 22.98, 21.68 and 5.74 % respectively at 50 mgL-1 concentration from leaf, Concentration (mg·L-1) bark, and seed (Table 2). (b) 16.00 a 14.00 Discussion Leaf Bark Seed 12.00

10.00 This study demonstrated that R. chinensis displayed allelopathic activity and inﬂuenced the emergence and seedling 8.00 b b b growth of radish, semen cassia and black soyabean. The 6.00 c effects varied depending on the tissue and extract concen- c tration, the target species and the growth parameters mea-

Rootstock length(cm) 4.00 d c b b sured. With increasing concentration, leaf extracts of R. 2.00 d e c d b chinensis caused more significant delay and reduction of 0.00 seed germination of target species than extracts from barks CK 200 100 50 33 25 and seeds extracts. Delayed seed germination by allelopathic Concentration (mg·L-1) extract could be further strengthened by osmotic effects on rate of absorption, delayed initiation of germination and (c) 16.00 a especially cell elongation (Black 1989). At the same con- 14.00 centration, RI on germination of leaf extract treatment was 12.00 lower than that of bark or seed extract treatment. The IEI of Leaf Bark Seed 10.00 b water extracts of leaves on black soyabean was -0.98, the lowest of all treatments. Seeds of R. chinensis affected 8.00 c b b 6.00 d seedling development and growth of the three species, but b their effect was especially strong on radish. 4.00 e c c Rootstock length(cm) 2.00 Seed extracts of R. chinensis displayed more consistent d d effects than did extracts of leaf or bark on target species. Root 0.00 CK 200 100 50 33 25 length was reduced in all species by the water extracts of seed, leaf and bark of R. chinensis. Inhibitory effect on root Concentration (mg·L-1) length, also reported in other experiments (Tongma et al. Fig. 2 Effects of water extracts of leaf, bark and seed of R. chinensis 2001; Shiraishi et al. 2002), may affect the competitive at different concentrations on root length of radish a semen cassiae balance between species during the establishment stage. b black soyabean c seedlings. Bars are standard errors and values Allelopathy is the effect of one species (especially plant) sharing a common lowercase letter are not significantly different at p \ 0.05 on the growth and development of other species through the release of chemical substances (Kohli et al. 1998; Re- igosa et al. 1999). Allelopathy has been shown to play an of water extract concentration resulted in increasing important role in forests, influencing the composition of inhibitory effects on seedling root growth. The average root vegetation, and also providing an explanation for the pat- lengths of semen cassia and black soyabean declined to terns of forest regeneration. Several reports addressed the 50.92 and 62.26 % at least. However, the five longest allelopathic effects of trees on other trees or natural veg- average root length of radish were significantly reduced to etation in the field (Rietveld et al. 1983; Klionsky et al. 41 % of the control even at 25 mgL-1. The inhibition 2011). The allelopathic potential of trees on other trees or rates were much higher with higher concentrations. natural vegetation has also been assessed (Chou et al. 1989; 123 L. Liu et al.

Table 2 Effect of R. chinensis water extracts on semen cassiae root activity vigor (mgg-1h-1) Plant part Extraction concentrations (mgL-1) CK 200 100 50 33 25

Leaf 1108.4 ± 1.19a ND 177.4 ± 1.51e 254.7 ± 1.19d 683.7 ± 8.31c 913.7 ± 8.53b Bark ND 159.7 ± 4.96e 240.3 ± 5.82d 286.0 ± 8.22c 365.4 ± 6.51b Seed ND ND 63.60 ± 1.88d 200.3 ± 6.66c 302.4 ± 5.46b Data are means (±SD) of three replicates. Different lowercase letters in the same row indicate signiﬁcant difference at p \ 0.05 ND not detected, root material was not enough

Souto et al. 2001; Fang et al. 2009; Zhang et al. 2010; potentially useful to manage R. chinensis communities and Valera-Burgos et al. 2012). There are also some research agro-forest systems based on R. chinensis. on the allelopathic effect of trees on agricultural crops. A In most studies of trees, phenolics were identified as significant allelopathic effect of trees on growth and yield potential allelochemical compounds. Chou et al. (1989) of agricultural crops was noticed in the field, such as identified phytotoxic phenolics as the allelopathic chemicals Populus deltoides on wheat and winter season crops (Singh of Z. formosana and Chinese fir. Singh et al. (2001) con- et al. 1998, 2001), and E. tereticornis on crops (Singh and cluded that the allelopathic interference of P. detoides with Kohli 1992). Moreover, the allelopathic potentials of trees crops was effected by release of phytotoxin phenolics from were also tested using laboratory bioassay with crops, such leaves and litter and accumulation of these phytotoxins in the as Adina cordifolia, A. nepalensis, Celtis australis and soil. Fernandez et al. (2006) documented that the potential Prunus cerasoides on Eleusine coracana, G. max and allelochemical compounds of P. halepensis were several Hordeum vulgare (Bhatt and Todaria 1990), Picea halep- phenolic acids (e.g. 4-hydroxybenzoic acid and p-coumaric ensis on Lactuca sativa and Linum strictum (Fernandez acid). Ruan et al. (2011) also isolated a potential allelo- et al. 2006), P. halepensis and Quercus coccifera (Alr- chemical phenolic compound 3,4-dihydroxyacetophenone ababah et al. 2009), E. grandis on R. sativus and Phaseolus (DHAP) from P. schrenkiana. However, Braine et al. (2012) aureus (Zhang et al. 2010), Araucaria angustifolia (Braine documented that the potential allelochemical compounds of et al. 2012), P. schrenkianan (Ruan et al. 2011). Yu et al. A. angustifolia were ent-kaurene and phyllocladene. R. (2003) found that crude root exudates and extracts of chinensis also contains various chemical substances with cucumber, as well as compounds purified from these biological activity, including terpenes, flavonoids, tannins, sources, increased the activity of SOD and POD in resin, starch, and organic acids (Parveen and Khan 1985; cucumber plants, and decreased stomatal conductance, Taniguchi et al. 2000). These results suggest that, in some transpiration and net photosynthesis. Their work also sug- cases, an allelochemical may be directly involved in the gested that the presence of superoxide anions also production of reactive oxygen species (ROS) whereas the increased in treated roots as the concentrations of root increase in oxidizing enzymes is a secondary response to the extracts/exudates increased. Root activity can reflect the increase in free radicals. In other cases, the allelochemical level of dehydrogenase activity (Zhao et al. 1998), which is might directly inhibit oxidizing enzymes in some way and an important physiological parameter of root activity. Our cause oxidative damage to the plant (Weir et al. 2004). This results indicated that root activity vigor of semen cassiae might also explain the allelopathy of donor water extracts on was reduced by the water extracts of seeds, leaves and bark receptor seedling root length and root activity in our study. of R. chinensis. The root activities of semen cassiae were In conclusion, this study is the first to demonstrate the significantly reduced to 82.43, 32.97 and 27.28 % of the allelopathic potential of R. chinensis. The results of the CK under 25 mgL-1 extracts from leaf, bark and seed of bioassay in this work may contribute to our understanding R. chinensis respectively. Seed extracts of R. chinensis of the allelopathic potential of R. chinensis. It is important displayed more consistent effects than did extracts of leaf to ascertain the allelopathic compounds of R. chinensis and and bark on root activity of semen cassiae. to minimize their negative effects on cultural systems. Most trees were reported in published studies to have inhibitory effects on crops. In the present study, the water extracts of leaf, bark and seed of R. chinensis also showed significant inhibitory effects on seedling growth of radish, References semen cassiae, and black soyabean. This work reveals the Ahn YJ, Lee CO, Kweon JH, Ahn JW, Park JH (1998) Growth existence of different sensitivity of plant species to alle- inhibitory effects of Galla Rhois-derived tannins on intestinal lopathic chemicals from R. chinensis. It makes these results bacteria. J Appl Microbiol 84:439–443

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