Previous PageTable Of Contents

Review of progress in the chemistry of rice allelopathy

Hisashi Kato-Noguchi

Department of Biochemistry and Food Science, Faculty of Agriculture, Kagawa University, Miki, Kagawa 761-0795, Japan.
Email hisashi@ag.kagawa-u.ac.jp

Abstract

Allelopathy is the direct influence of an organic chemical released from one living plant on the growth and development of other plants. It is a generally accepted definition that allelochemicals are secondary metabolites released by source plants into the environment, causing detrimental effects on the growth and development of recipient plants. Rice plants possibly release allelochemicals into neighboring environment because rice plants inhibited the growth of several plant species when rice and these plants are grown together. A large number of compounds, such as phenolic acids, fatty acids, indoles and terpenes were identified in rice root exudates and decomposing rice residues as putative allelochemicals. This paper summarizes compounds released from living rice plants and discusses possible involvement of these compounds in rice allelopathy.

Media Summary

This paper summarizes compounds released from living rice plants and discusses possible involvement of these compounds in rice allelopathy.

Key Words

Oryza sativa; allelopathy; allelochemical; growth inhibitor; momilactone B; phenolic acid; pytotoxity; root exudates.

Introduction

A large number of rice varieties were found to inhibit the growth of several plant species when the rice varieties were grown together with the plants under field and/or laboratory conditions (Dilday et al. 1998; Hassan et al. 1998 Olofsdotter et al. 1999). These findings suggest that living rice may produce and release allelochemical(s) into the neighboring environment.

A number of secondary metabolites, phenolic acids, phenylalkanoic acids, hydroxamic acids, fatty acids, terpenes and indoles, were identified in rice extracts (Rimando and Duke 2003). These compounds are ubiquitous in plants and some of these compounds have growth inhibitory activity against several plant species. It is not clear, however, whether these compounds are released from living rice plants into the neighboring environment, and act as allelochemicals in natural ecosystems. In addition, it was found that there was no significant correlation between the level of growth inhibitory substances in plants and their level in the root exudates (Wu et al. 2001).

To date, in the trials searching for putative allelochemicals released from living rice plants, dozens of compounds were found and identified in rice roots exudates and decomposing rice residues. This paper summarizes these compounds and discussed possible involvement of those compounds in rice allelopathy.

Allelopathic substances in decomposing rice residues

It is well known that the crop residues left in soil are sometimes harmful to plant growth. The plant residues in soil could release phytotoxic substances during decomposition period. Chou and Lin (1976) observed decrease in plant productivity of the second rice crop in a paddy field containing residues from the first rice crop. They found that aqueous extracts of decomposing rice residues in soil inhibited the growth of mungbean and lettuce as well as rice. Several phenolic acids, 2-hydroxyphenylacetic acid (3), 4-hydroxybenzoic acid (11), vanillic acid (16), p-coumaric acid (23) and ferulic acid (25) were found in aqueous extracts of decomposing rice residues (Chou and Lin 1976) and in soil from paddy fields which rice was grown (Chou and Chiou 1979).

Kuwatsuka and Shindo (1973) isolated 13 different phenolic acids in decomposition of rice straw; benzoic acid (10), 4-hydroxybenzoic acid (11), protocatechuic acid (13), gallic acid (14), vanillic acid (16), syringic acid (17), salicylic acid (18), gentisic acid (19), β-resorcylic acid (20), p-coumaric acid (23), caffeic acid (24), ferulic acid (25) and sinapinic acid (26). They found that p-coumaric acid (23) was released in the greatest amount from decomposing rice straw. However, Tanaka et al. (1990) doubt that the involvement of phenolic acid in rice allelopathy, as the levels of phenolic acids found in rice soil are not sufficient to cause phytotoxic effects. In support of this view, phenolic acids were usually present in rice soils at concentrations below 5 mg Kg-1 soil, which is below the bioactive threshold (Olofsdotter et al. 2002)

Allelopathic substances in rice root exudates

Several phenolic acids and fatty acids were found in water obtained from soils in which allelopathic or non-allelopathic rice plants were incubated for 48 h (Mattice et al. 1998). Concentrations of 4-hydroxybenzaldehyde (9), 4-hydroxybenzoic acid (11), 3-hydroxybenzoic acid (12), p-coumaric acid (23) and caffeic acid (24) were greater in water obtained from soils containing allelopathic rice plants than water obtained from soils containing non-allelopathic rice plants. Mattice et al. (1998) also identified compounds contained in these soils, and found that concentrations of 4-hydroxybenzaldehyde (9), 4-hydroxybenzoic acid (11), 3-hydroxy-4-methoxybenzoic acid (15), valeric acid (30), tetradecanoic acid (31) and stearic acid (32) were greater in soils of allelopathic rice than soils of non-allelopathic rice plants. Based on these experiments, it was suggested that allelopathy of rice against weeds was correlated with the amount of phenolic acids released by living rice roots (Mattice et al. 1998). Phenolic acids are shown phytotoxicity against various plants at concentrations greater than about 1 mM (Hartley and Whitehead 1985; Dalton 1999). However, Mattice et al. (1998) did not provide the exact values of phenolic acid concentrations in the water and soils containing rice plants. Thus, it is impossible to evaluate whether phenolic acids are responsible for the allelopathy of rice.

Kim and Kim (2000) identified several compounds in the acidic fraction isolated from root exudates of allelopathic rice cv. Kouketsmochi. These compounds were 2-methyl-1,4-benzenediol (4), 1-ethyl-3,5-dimethylbenzene (5), 4-ethylbenzaldehyde (8), cinnamic aldehyde (21), octadecane (27), 3-epicosene (28), 1-eicosanol (29), 9,12-octadecadienoic acid (33), 7-hexadecenoic acid methyl ester (34), 12-octadecenoic acid methyl ester (35), 12-methyl-tridecanoic acid methyl ester (36), cis-1-butyl-2-methylcyclopropane (37), dehydroabietic acid (43) and cholest-5-en-3(β)-ol (45). They considered that 2-methyl-1,4-benzenediol (4), 4-ethylbenzaldehyde (8), cinnamic aldehyde (21) and cholest-5-en-3(β)-ol (45) were candidates for allelochemicals of rice plants. However, the concentrations of these compounds were not provided and inhibitory activities of these compounds were relatively weak.

Fifteen compounds were identified and quantified in the root exudates of allelopathic and non-allelopathic rice cultivars (Seal et al. 2004a). The concentrations of 4-hydroxybenzoic acid (11), caffeic acid (24) and ferulic acid (25) were greater in the exudates of allelopathic rice cultivars than those of non-allelopathic rice cultivars, while the concentration of abietic acid (42) was greater in those of non-allelopathic rice cultivars than those of allelopathic rice cultivars. The other 11 compounds, resorcinol (2), 2-hydroxyphenylacetic acid (3), 4-hydroxyphenylacetic acid (6), 4-phenylbutyric acid (7), cinnamic acid (22), vanillic acid (16), syringic acid (17), salicylic acid (18), p-coumaric acid (23), 5-hydroxyindole-3-acetic acid (38) and indole-5-carboxylic acid (39) did not differ in the concentrations between allelopathic and non-allelopathic rice cultivars (Seal et al. 2004a). 5-(12-Heptadecenyl)-resorcinol (1) was also found in rice root exudates (Bouillant et al. 1994).

About 5,000 rice seedlings, cv. Koshihikari, were hydroponically grown for 14 days in order to find out an allelochemical in rice root exudates. Keeping track of the biological activity, the culture solution was purified by several chromatographic fractionations and finally 2.1 mg of putative compound causing the inhibitory effect of the rice seedlings was isolated (Kato-Noguchi et al. 2002; Kato-Noguchi and Ino 2003a). The chemical structure of the inhibitor was determined from its high-resolution MS, and 1H- and 13C-NMR spectral data and has been identified as momilactone B (44). Momilactone B is quite active at sub-millimolare concentrations (Takahashi et al. 1976; Kato et al. 1977; Lee et al. 1999b). Momilactone B was later found in the rice root exudes of another allelopathic rice cultivars in addition to 5,7,4’-trihydroxy-3’,5’-dimethoxyflavone (40) and 3-isopropyl-5-acetoxycyclohexene-2-one-1(41) (Kong et al. 2004).

 

R1

R2

R3

R4

R5

   

R1

R2

R3

R4

R5

8

H

H

H

CH2CH3 

H

 

21

H

H

H

H

H

9

H

H

H

OH

H

 

22

OH

H

H

H

H

10

OH

H

H

H

H

 

23

OH

H

H

OH

H

11

OH

H

H

OH

H

 

24

OH

H

OH

OH

H

12

OH

H

OH

H

H

 

25

OH

H

OCH3

OH

H

13

OH

H

OH

OH

H

 

26

OH

H

OCH3

OH

OCH3

14

OH

H

OH

OH

OH

             

15

OH

H

OH

OCH3

H

             

16

OH

H

OCH3

OH

H

             

17

OH

H

OCH3

OH

OCH3

             

18

OH

OH

H

H

H

             

19

OH

OH

H

H

OH

             

20

OH

OH

H

OH

H

             

1, 5-(12-heptadecenyl)-resorcinol; 2, resorcinol; 3, 2-hydroxyphenylacetic acid; 4, 2-methyl-1,4-benzenediol; 5, 1-ethyl-3,5-dimethylbenzene; 6, 4-hydroxyphenylacetic acid; 7, 4-phenylbutyric acid; 8, 4-ethylbenzaldehyde; 9, 4-hydroxybenzaldehyde; 10, benzoic acid; 11, 4-hydroxybenzoic acid; 12, 3-hydroxybenzoic acid; 13, protocatechuic acid; 14; gallic acid; 15, 3-hydroxy-4-methoxybenzoic acid; 16, vanillic acid; 17, syringic acid; 18, salicylic acid; 19, gentisic acid; 20, β-resorcylic acid; 21, cinnamic aldehyde; 22, cinnamic acid; 23, p-coumaric acid; 24, caffeic acid; 25, ferulic acid; 26, sinapinic acid.

27, octadecane; 28, 3-epicosene; 29, 1-eicosanol; 30, valeric acid; 31, tetradecanoic acid; 32, stearic acid; 33, 9,12-octadecadienoic acid; 34, 7-hexadecenoic acid methyl ester; 35, 12-octadecenoic acid methyl ester, 36, 2-methyl-tridecanoic acid methyl ester; 37, cis-1-butyl-2-methylcyclopropane; 38, 5-hydroxyindole-3-acetic acid; 39, indole-5-carboxylic acid; 40, 5,7,4’-trihydroxy-3’,5’-dimethoxyflavone; 41, 3-isopropyl-5-acetoxycyclohexene- 2-one-1; 42, abietic acid; 43, dehydroabietic acid; 44, momilactone B; 45, cholest-5-en-3(β)-ol.

Volatile compounds from rice callus

It was found that the growth of soybean callus was inhibited by rice callus when both callus tissues were incubated together (Yang and Futsuhara 1991). The experimental system was designed to prevent the substance diffusion through culture medium. Thus, only volatile compounds could affect the growth of soybean callus. Involvement of ethylene in the growth inhibition was ruled out, but further analysis of the volatiles was not carried out.

Phenolic acids

Phenolic acids are often mentioned as putative allelochemicals and the most commonly investigated compounds among potential allelochemicals since they have been found in a wide range of soils (Hartley and Whitehead 1985; Inderjit 1996; Dalton 1999). Hsu et al. (1989) evaluated the inhibitory activities of phenolic acids against germination of lettuce and alfalfa. 4-hydroxybenzoic acid (11) and salicylic acid (18) were the most active and they inhibited the germination at concentrations greater than 0.5 - 1.5 mM.

Olofsdotter et al. (2002) evaluated whether phenolic acids are responsible for rice allelopathy. They found that allelopathic rice cultivars did not release significantly greater amount of phenolic acids than non-allelopathic cultivars. The maximum release rate of phenolic acids from rice plants was approximately 10 μg plant-1 day-1. Therefore, at a conventional plant density (100 rice plants m-2), the release rate of phenolic acids would be approximately 1 mg m-2 day-1. Considering the inhibitory activity of phenolic acids, it was concluded that, even if all phenolic acids were as phytotoxic as 4-hydroxybenzoic acid (11), the release level of phenolic acids from rice is not sufficient to cause growth inhibition of neighboring plants (Olofsdotter et al. 2002).

Five major phenolic acids in rice root exudates, 4-hydroxybenzoic acid (11), vanillic acid (16), syringic acid (17), p-coumaric acid (23) and caffeic acid (24), were mixed and their biological activities were determined against Sagittaria monotevidensis (Seal et al. 2004b). The concentration required for 50 % growth inhibition (I50) of the mixture of these five phenolic acids was 502 μM. The concentrations of these phenolic acids detected in the rice roots exudates were considerably less than 500 μM (Seal et al. 2004b). Inhibitory activity of a mixture of all 15 compounds identified in rice roots exudates was also determined and I50 was found to be 569 μM (Seal et al. 2004a; 2004b). In addition, it was clarified that synergistic action of phenolic acids on growth inhibition did not work well (Seal et al. 2004b). These studies indicate that none of the quantified compounds in rice root exudates including phenolic acids are not responsible for the allelopathy of rice.

All information available suggests that phenolic acid concentrations in rice root exudates were much lower than the required threshold of these compounds, and phenolic acids are unlikely rice allelochemicals.

Momilactone B

Momilactone B (44) was originally isolated from rice husks together with momilactone A (Kato et al. 1973; Takahashi et al. 1976) and has also been found in rice leaves and straw (Cartwright et al. 1977; 1981; Kodama et al. 1988; Lee et al. 1999a). Thereafter, the function of momilactone A as a phytoalexin has been extensively studied and several lines of evidence indicate that momilactone A has an important role in rice defense system against pathogens (Nojiri et al. 1996; Araki and Kurahashi 1999; Takahashi et al. 1999; Tamogami and Kodama 2000; Agrawal et al. 2002). Although the growth inhibitory activity of momilactone B was much greater than that of momilactone A (Takahashi et al. 1976; Kato et al. 1977), the function of momilactone B is obscure.

The inhibitory activities of momilactone B against the germination and growth of several plant species have been reported. A 5 μM solution of momilactone B inhibited the germination of Amaranthus lividus by 50 %, and a 50 μM solution of momilactone B inhibited root and shoot growth of Digitaria sanguinalis and seed germination of Poa annua by more than 50 % (Lee et al. 1999b). The compounds also inhibited the root and hypocotyl growth of cress seedlings at concentrations greater than 3 μM. Inhibition was increased with increasing concentrations of momilactone B. The concentrations required for 30 % inhibition of cress roots and hypocotyls were 12 and 16 μM, respectively, and 36 and 41 μM, for 50 % inhibition of cress roots and hypocotyls, respectively (Kato-Noguchi et al. 2002; Kato-Noguchi and Ino 2003a). Judging from its inhibitory activity, momilactone B was considered to be a candidate for a rice allelochemical (Rimando and Duke 2003).

Rice plants were hydroponically grown for 130 days and the release level of momilactone B released from their plants into the medium was determined (Kato-Noguchi and Ino 2003b). Rice plants released momilactone B throughout its life cycle. The release rate of momilactone B increased with plant growth until initiation of flowering. The release rate of momilactone B at the beginning of flowering was 2.1 μg plant-1 day-1. On average, a single rice plant released about 100 μg of momilactone B into the medium over its life cycle (Kato-Noguchi and Ino 2003b). At a conventional plant density (100 rice plants m-2), approximately 10 mg m-2 of momilactone B would be released. Thus, accumulation of momilactone B may occur under field conditions sufficiently to inhibit germination and growth of neighboring plants.

References

Agrawal GK, Rakwal R, Tamogami S, Yonekura M, Kubo A, Saji H (2002) Chitosan activates defense/stress response(s) in the leaves of Oryza sativa seedlings. Plant Physiology and Biochemistry 40, 1061-1069.

Araki Y, Kurahashi Y (1999) Enhancement of phytoalexin synthesis during rice blast infection of leaves by pre-treatment with carpropamid. Journal of Pesticide Science 24, 369-374.

Bouillant ML, Jacoud C, Zanella I, Favre-Bonvin J, Bally R (1994) Identification of 5-(12-heptadecenyl)-resorcinol in rice root exudates. Phytochemistry 35, 769-771.

Cartwright D, Langcake P, Pryce RJ, Leworthy DP, Ride JP (1977) Chemical activation of host defence mechanisms as a basis for crop protection. Nature 267, 511-513.

Cartwright DW, Langcake P, Pryce RJ, Leworthy DP, Ride JP (1981) Isolation and characterization of two phytoalexins from rice as momilactones A and B. Phytochemistry 20, 535-537.

Chou C-H, Lin H-J (1976) Autointoxication mechanism of Oryza sativa. I. Phytotoxic effects of decomposing rice residues in soil. Journal of Chemical Ecology 2, 353-367.

Chou C-H, Chiou S-J (1979) Autointoxication mechanism of Oryza sativa. II. Effects of culture treatments on the chemical nature of paddy soil and on rice productivity. Journal of Chemical Ecology 5, 839-859.

Dalton BR (1999) The occurrence and behavior of plant phenolic acids in soil environments and their potential involvement in allelochemical interference interactions: Methodological limitations in establishing conclusive proof of allelopathy. In ‘Principals and Practices in Plant Ecology: Allelochemical Interactions’. (Eds. Inderjit, KMM Dakshini, CL Foy) pp. 57-74, (CRC Press: Boca Raton, Florida).

Dilday RH, Yan WG, Moldenhauer KAK, Gravois KA (1998) Allelopathic activity in rice for controlling major aquatic weeds. In ‘Allelopathy in Rice’. (Ed. M Olofsdotter) pp 7-26, (International Rice Research Institute: Manila).

Ebana K, Yan W, Dilday RH, Namai H, Okuno K (2001)Variation in the allelopathic effect of rice with water soluble extracts. Agronomy. Journal. 93, 12-16.

Hartley RD, Whitehead DC (1985) Phenolic acids in soils and their influence on plant growth and soil microbial processes. In ‘Soil Organic Matter and Biological Activity. Development in Plant and Soil Sciences.’ (Eds. DVaugham, RE Malcolm) Vol. 16, pp. 109-262, (Martinus Nijhoff/Dr W. Junk Publishers: Dordrecht, The Netherlands).

Hassan SM, Aidy IR, Bastawisi AO, Draz AE (1998) Weed management using allelopathic rice varieties in Egypt. In ‘Allelopathy in Rice’. (Ed. M Olofsdotter) pp 27-37, (International Rice Research Institute: Manila).

Hsu F-H, Chiu C-Y, Chou C-H (1989) Action model of allelopthic compounds on seed germination. In ‘Phytochemical Ecology: Allelochemicals, Mycotoxins and Insect Pheromones and Allomones’. (Eds. CH Chou, GR Waller) pp. 315-327, (Institute of Botany, Academia Sinica: China).

Inderjit (1996) Plant phenolics in allelopathy. Botanical Review 62, 186-202.

Kato T, Kabuto C, Sasaki N, Tsunagawa M, Aizawa H, Fujita K, Kato Y, Kitahara Y (1973) Momilactones, growth inhibitors from rice, Oryza sativa L. Tetrahedron Letter 39, 3861-3864.

Kato T, Tsunakawa M, Sasaki N, Aizawa H, Fujita K, Kitahara Y, Takahashi N (1977) Growth and germination inhibitors in rice husks. Phytochemistry 16, 45-48.

Kato-Noguchi H, Ino T, Sata N, Yamamura S (2002) Isolation and identification of a potent allelopathic substance in rice root exudates. Physiologia Plantrum 115, 401-405.

Kato-Noguchi H, Ino T (2003a) Rice seedlings release momilactone B into the environment. Phytochemistry 63, 551-554.

Kato-Noguchi H, Ino T, Ichii M (2003b) Changes in release level of momilactone B into the environment from rice throughout its life cycle. Functional Plant Biology 30, 995 - 997.

Kim KW, Kim KU (2000) Searching for rice allelochemicals. In ‘Rice Allelopathy’. (Eds. KU Kim, DH Shin) pp. 83-95, (Kyungpook National University: Korea).

Kodama O, Suzuki T, Miyakawa J, Akatsuka T (1988) Ultraviolet-induced accumulation of phytoalexins in rice leaves. Agricultural and Biological Chemistry 52, 2469-2473.

Kong C, Liang W, Xu X, Hu F (2004) Release and activity of allelochemicals from allelopthic rice seedlings. Journal of Agricultural and Food Chemistry 52, 2861-2865.

Kuwatsuka S, Shindo H (1973) Behavior of phenolic substances in the decaying process of plants. I. Identification and quantitative determination of phenolic acids in rice straw and its decayed product by gas chromatography. Soil Science and Plant Nutrition 19, 219-227.

Lee CW, Yoneyama K, Takeuchi Y, Konnai M, Tamogami S, Kodama O (1999a) Momilactones A and B in rice straw harvested at different growth stages. Bioscience, Biotechnology,and Biochemistry 63, 1318-1320.

Lee CW, Yoneyama K, Ogasawara M, Takeuchi Y, Konnai M (1999b) Allelochemicals in rice straw. ‘Proceedings of the 17th Asian-Pacific Weed Science Society Conference’. pp 22-27. Bangkok. Thailand.

Mattice J, Lavy T, Skulman B, Dilday RH (1998) Searching for allelochemicals in rice that control ducksalad. In ‘Allelopathy in Rice’. (Ed. M Olofsdotter) pp 81-98, (International Rice Research Institute: Manila).

Nojiri H, Sugimori M, Yamane H, Nishimura Y, Yamada A, Shibuya N, Kodama O, Murofushi N, Omori T (1996) Involvement of jasmonic acid in elicitor-induced phytoalexin production in suspension-cultured rice cells. Plant Physiology 110, 387-392.

Olofsdotter M, Navarez D, Rebulanan M, Streibig JC (1999) Weed-suppressing rice cultivars: Does allelopathy play a role? Weed Research 39, 441-454.

Olofsdotter M, Rebulanan M, Madrid A, Dali W, Navarez D, Olk DC (2002) Why phenolic acids are unlikely primary allelochemicals in rice. Journal of Chemical Ecology 28, 229-242.

Rimando AM, Duke SO (2003) Studies on rice allelochemicals. In ‘Rice; Origin, History, Technology and Production’. (Eds. CW Smith, RH Dilday) pp. 221-244, (John Wiley & Sons, Inc.: Hoboken, New Jersey).

Seal AN, Pratley JE, Haig T, An M (2004a) Identification and quantitation of compounds in a series of allelopathic and non-allelopathic rice root exudates. Journal of Chemical Ecology 30, 1647-1662.

Seal AN, Haig T, Pratley JE (2004b) Evaluation of putative allelochemicals in rice roots exudates for their role in the suppression of arrowhead root growth. Journal of Chemical Ecology 30, 1663-1678.

Takahashi N, Kato T, Tsunagawa M, Sasaki N, Kitahara Y (1976) Mechanisms of dormancy in rice seeds. II. New growth inhibitors, momilactone-A and -B isolated from the hulls of rice seeds. Japanese Journal of Breeding 26, 91-98.

Takahashi A, Kawasaki T, Henmi K, Shii K, Kodama O, Satoh H, Shimamoto K (1999) Lesion mimic mutants of rice with alterations in early signaling events of defense. The Plant Journal 17, 535-545.

Tamogami S, Kodama O (2000) Coronatine elicits phytoalexin production in rice leaves (Oryza sativa L.) in the same manner as jasmonic acid. Phytochemistry 54, 689-694.

Tanaka F, Ono S, Hayasaka T (1990) Identification and evaluation of toxicity of rice root elongation inhibitors in flooded soils with added wheat straw. Soil Science and Plant Nutrition 36, 97-103.

Wu H, Haig T, Pratley J, Lemerle D, An M (2001) Allelochemicals in wheat (Triticum aestivum L.): Production and exudation of 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one. Journal of Chemical Ecology 27, 1691-1700.

Yang Y-S, Futsuhara Y (1991) Inhibitory effects of volatile compounds released from rice callus on soybean callus growth: allelopathic evidence observed using in vitro culture. Plant Science 77, 103-110.

Previous PageTop Of Page