Skip to main content
SpringerLink
Log in

Rice Allelopathy Induced by Methyl Jasmonate and Methyl Salicylate

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Methyl jasmonate (MeJA) and methyl salicylate (MeSA) are important signaling molecules that induce plant defense against insect herbivores and microbial pathogens. We tested the hypothesis that allelopathy is an inducible defense mechanism, and that the JA and SA signaling pathways may activate allelochemicals release. Exogenous application of MeJA and MeSA to rice (Oryza sativa L.) enhanced rice allelopathic potential and led to accumulation of phenolics, an increase in enzymatic activities, and gene transcription of phenylalanine ammonia-lyase (PAL) and cinnamate 4-hydroxylase (C4H), two key enzymes in the phenylpropanoid pathway. Aqueous extracts of the leaves of rice IAC165, a putative allelopathic variety, treated with MeSA (5 mM) or MeJA (0.05 mM), showed increased inhibitory effects (25 and 21%, respectively) on root growth of barnyardgrass (Echinochloa crus-galli L.), and increased inhibitory effects (18 and 23%, respectively) on shoot growth. Aqueous extracts from leaves of Huajingxian 1 rice, a putative nonallelopathic variety treated with MeJA and MeSA, caused 63 and 24% inhibition of root growth in barnyardgrass seedlings. The root exudates of both IAC165 and Huajingxian 1 plants treated with MeJA and MeSA for 48 hr also showed significant increases in their inhibitory effects on root growth of barnyardgrass seedlings. At the four-leaf stage, levels of 3,4-hydroxybenzoic acid, vanillic acid, coumaric acid, and ferulic acid that accumulated in the leaves were 5.3-, 31.3-, 2.2-, and 1.7-fold higher in response to MeJA exposure, and 3.3-, 13.1-, 2.0-, and 2.2-fold higher in response to MeSA. Treatments of MeSA and MeJA enhanced the PAL activity in the rice leaves up to 52.3 and 80.1%, respectively, whereas C4H activity was increased by 40.2 and 67%. Gene transcription of PAL and C4H in rice leaves significantly increased after the plants were subjected to treatment with MeJA and MeSA. These results suggest that allelopathy may be an active defense mechanism, and that plant signaling compounds are potentially valuable in its regulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

MeSA:

methyl salicylate

MeJA:

methyl jasmonate

VA:

vanillic acid

CA:

caffeic acid

FA:

ferulic acid

CMA:

coumaric acid

HBA:

3,4-hydroxybenzoic acid

PAL:

phenylalanine ammonia-lyase

C4H:

cinnamate 4-hydroxylase

References

  • Ahn, J. K. and Chung, I. M. 2000. Allelopathic potential of rice hulls on germination and seedling growth of barnyardgrass. Agron. J. 92:1162–1167.

    Article  Google Scholar 

  • An, Y., Shen, Y. B., Wu, L. J., and Zhang, Z. X. 2006. A change of phenolic acids content in poplar leaves induced by methyl salicylate and methyl jasmonate. J. For. Res. 17:107–110.

    Article  CAS  Google Scholar 

  • Baldwin, I. T. 1998. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc. Natl. Acad. Sci. U S A 95:8113–8118.

    Article  PubMed  CAS  Google Scholar 

  • Bi, H. H. 2004. Rice allelopathy induced by methyl jasmonate and methyl salicylate. MS dissertation, South China Agricultural University, Guangzhou, China.

  • Brader, G., Tas, E., and Palva, E. T. 2001. Jasmonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the nonspecific pathogen Erwinia carotovora. Plant Physiol. 126:849–860.

    Article  PubMed  CAS  Google Scholar 

  • Chou, C. H. 1999. Role of allelopathy in plant biodiversity and sustainable agriculture. Crit. Rev. Plant Sci. 18:609–636.

    Article  Google Scholar 

  • Chou, C. H. and Lin, H. J. 1976. Autointoxication mechanism of Oryza sativa. I. Phytotoxic effects of decomposing rice residues in soils. J. Chem. Ecol. 2:353–367.

    Article  CAS  Google Scholar 

  • Chung, I. M., Kim, K. H., Ahn, J. K., and Ju, H. J. 1997. Allelopathic potential evaluation of rice cultivars on Echinochloa crus-galli. Korean J. Weed Sci. 17:52–58.

    Google Scholar 

  • Chung, I. M., Ahn, J. K., Kim, J. T., and Kim, C. S. 2000. Assessment of allelopathic potentiality and identification of allelopathic compounds on Korean local rice varieties. Korean J. Crop Sci. 45:44–49.

    Google Scholar 

  • Chung, I. M., Ahn, J. K., and Yun, S. J. 2001a. Identification of allelopathic compounds from rice (Oryza sativa L.) straw and their biological activity. Can J. Plant Sci. 81:815–819.

    CAS  Google Scholar 

  • Chung, I. M., Ahn, J. K., and Yun, S. J. 2001b. Assessment of allelopathic potential of barnyardgrass (Echinochloa crus-galli) on rice (Oryza sativa L.) cultivars. Crop Prot. 20:921–928.

    Article  Google Scholar 

  • Chung, I. M., Kim, J. T., and Kim, S. H. 2006. Evaluation of allelopathic potential and quantification of momilactone A, B from rice hull extracts and assessment of inhibitory bioactivity on paddy field weeds. J. Agric. Food Chem. 54:2527–2536.

    Article  PubMed  CAS  Google Scholar 

  • Creelman, R. A. and Mullet, J. E. 1997. Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:355–381.

    Article  PubMed  CAS  Google Scholar 

  • Dayan, F. E. 2006. Factors modulating the levels of the allelochemical sorgoleone in Sorghum bicolor. Planta 224:339–346.

    Article  PubMed  CAS  Google Scholar 

  • De Vos, M., Van Oosten, V. R., Van Poecke, R. M., Van Pelt, J. A., Pozo, M. J., Mueller, M. J., Buchala, A. J., Metraux, J. P., Van Loon, L. C., Dicke, M., and Pieterse, C. M. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Plant Microbe. Interact. 18:923–937.

    Article  CAS  Google Scholar 

  • Dicke, M., Gols, R., Ludeking, D., and Posthumus, M. A. 1999. Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in lima bean plants. J. Chem. Ecol. 25:1907–1922.

    Article  CAS  Google Scholar 

  • Dilday, R. H., Nastasi, P., and Smith, J. R. 1989. Allelopathic observations in rice (Oryza sativa L.) to duck salad (Heteranthera limosa (SW) Willd). Proc. Arkansas Acad. Sci. 43:21–22.

    Google Scholar 

  • Dilday, R. H., Lin, J., and Yan, W. G. 1994. Identification of allelopathy in the USDA-ARS rice germplasm collection. Aust. J. Exp. Agric. 34:901–910.

    Article  Google Scholar 

  • Dilday, R. H., Yan, W. G., Moldenhauer, K. A. K., and Gravois, K. A. 1998. Allelopathic activity in rice for controlling major aquatic weeds, pp. 7–26, in M. Olofsdotter (ed.). Allelopathy in Rice. International Rice Research Institute, Manila.

    Google Scholar 

  • Durrant, W. E. and Dong, X. 2004. Systemic acquired resistance. Annu. Rev. Phytopathol. 42:185–209.

    Article  PubMed  CAS  Google Scholar 

  • Ebana, K., Yan, W. G., Dilday, R. H., Namai, H., and Okuno, K. 2001. Analysis of QTL associated with the allelopathic effect of rice using water soluble extracts. Breed. Sci. 51:47–51.

    Article  CAS  Google Scholar 

  • Edwards, R. and Kessmann, H. 1992. Isoflavonoid phytoalexins and their biosynthetic enzymes, pp. 45–62, in S. J. Gurr, M. J. McPherson, and D. J. Bowles (eds.). Molecular Plant Pathology: A Practical Approach. IRL Press, Oxford.

    Google Scholar 

  • Fan, D. 2005. Effects of glyphosate, chlorsulfuron, and methyl jasmonate on growth and alkaloid biosynthesis of jimsonweed (Datura stramonium L.). Pestic. Biochem. Physiol. 82:16–26.

    Article  CAS  Google Scholar 

  • Fujii, Y. 1992. The potential for biological control of paddy and aquatic weeds with allelopathy: Allelopathic effect of some rice varieties, pp. 305–320, in Proceedings of the International Symposium on Biological Control and Integrated Management of Paddy and Aquatic Weeds, Tsukuba, Japan.

  • Garrity, D. P., Movillon, M., and Moddy, K. 1992. Differential weed suppression ability in upland rice cultivars. Agron. J. 84:586–591.

    Article  Google Scholar 

  • Gundlach, H., Mueller, M. J., Kutchan, T. M., and Zenk, M. H. 1992. Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc. Natl. Acad. Sci. U S A 89:2389–2393.

    Article  PubMed  CAS  Google Scholar 

  • He, H. Q., Shen, L. H., Xiong, J., Jia, X. L., Lin, W. X., and Wu, H. 2004. Conditional genetic effect of allelopathy in rice (Oryza sativa L.) under different environmental conditions. Plant Growth Reg. 44:211–218.

    Article  CAS  Google Scholar 

  • He, H. Q., Lin, W. X., Liang, Y. Y., Song, B. Q., Ke, Y. Q., Guo, Y. C. H., and Liang, K. J. 2005. Analyzing the molecular mechanism of crop allelopathy by using differential proteomics. Acta Ecol. Sin. 25:3141–3146.

    CAS  Google Scholar 

  • Inderjit, Callaway, R. M., and Vivanco, J. M. 2006. Can plant biochemistry contribute to understanding of invasion ecology? Trends Plant Sci. 11:574–580.

    Article  PubMed  CAS  Google Scholar 

  • Jensen, L. B., Courtois, B., Shin, L., Li, Z. K., Olofsdotter, M., and Mauleon, R. P. 2001. Locating genes controlling allelopathic effects against barnyardgrass in upland rice. Agron. J. 93:21–26.

    Article  CAS  Google Scholar 

  • Jörn, H., Jens, D., Siegfried, B., and Wilhelm, B. 1994. Herbivore-induced volatiles: The emission of acyclic homoterpenes from leaves of Phaseolus lunatus and Zea mays can be triggered by a glucosidase and jasmonic acid. FEBS Lett. 352:146–150.

    Article  Google Scholar 

  • Kato-Noguchi, H. 2004. Allelopathic substance in rice root exudates: Rediscovery of momilactone B as an allelochemical. J. Plant Physiol. 161:271–276.

    Article  PubMed  CAS  Google Scholar 

  • Kato-Noguchi, H. 2005. Review of progress in the chemistry of rice allelopathy, pp. 182–188, in J. D. I. Haper, M. An, H. Wu and J. H. Kent (eds.). Proceedings of the Fourth World Congress on Allelopathy, “Establishing the Scientific Base,” Wagga Wagga, Australia.

  • Kato-Noguchi, H. and Ino, K. 2003. Rice seedlings release momilactone B into the environment. Phytochemistry 63:551–554.

    Article  PubMed  CAS  Google Scholar 

  • Kato-Noguchi, H., Ino, T., Sata, N., and Yamamura, S. 2002. Isolation and identification of a potent allelopathic substance in rice root exudates. Physiol. Plant. 115:401–405.

    Article  PubMed  CAS  Google Scholar 

  • Kessler, A. and Baldwin, I. T. 2002. Plant response to insect herbivory: The emerging molecular analysis. Annu. Rev. Plant Biol. 53:299–328.

    Article  PubMed  CAS  Google Scholar 

  • Kiefer, E., Heller, W., and Ernst, D. 2000. A simple and efficient protocol for isolation of functional RNA from plant tissues rich in secondary metabolites. Plant Mol. Biol. Rep. 18:33–39.

    CAS  Google Scholar 

  • Kim, S. Y., Madrid, A. V., Park, S. T., Yang, S. J., and Olofsdotter, M. 2005. Evaluation of rice allelopathy in hydroponics. Weed Res. 45:74–79.

    Article  Google Scholar 

  • Kong, C., Liang, W., Xu, X., and Hu, F. 2004. Release and activity of allelochemicals from allelopathic rice seedlings. J. Agric. Food Chem. 52:2861–2865.

    Article  PubMed  CAS  Google Scholar 

  • Lamb, C. and Rubery, P. H. 1975. A spectrophotometric assay for trans-cinnamic acid 4-hydroxylase activity. Anal. Biochem. 68:554–561.

    Article  PubMed  CAS  Google Scholar 

  • Loivamaki, M., Holopainen, J. K., and Nerg, A. M. 2004. Chemical changes induced by methyl jasmonate in oilseed rape grown in the laboratory and in the field. J. Agric. Food Chem. 52:7607–7613.

    Article  PubMed  CAS  Google Scholar 

  • Mangas, S., Bonfill, M., Osuna, L., Moyano, E., Tortoriello, J., Cusido, R. M., Pinol, M. T., and Palazon, J. 2006. The effect of methyl jasmonate on triterpene and sterol metabolisms of Centella asiatica, Ruscus aculeatus and Galphimia glauca cultured plants. Phytochemistry 67:2041–2049.

    Article  PubMed  CAS  Google Scholar 

  • Martin, D., Tholl, D., Gershenzon, J., and Bohlmann, J. 2002. Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiol. 129:1003–1018.

    Article  PubMed  CAS  Google Scholar 

  • Martin, D. M., Gershenzon, J., and Bohlmann, J. 2003. Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce. Plant Physiol. 132:1586–1599.

    Article  PubMed  CAS  Google Scholar 

  • Mattice, J., Lavy, T., Skulman, B., and Dilday, R. H. 1998. Searching for allelochemicals in rice that control ducksalad, pp. 81–98, in M. Olofsdotter (ed.). Allelopathy in Rice. International Rice Research Institute, Manila.

    Google Scholar 

  • Métraux, J. P. 2001. Systemic acquired resistance and salicylic acid: current state of knowledge. Eur. J. Plant Pathol. 107:13–18.

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Olofsdotter, M., Navarez, D., and Moody, K. 1995. Allelopathic potential in rice (Oryza sativa L.) germplasm. Ann. Appl. Biol. 127:543–560.

    Article  Google Scholar 

  • Olofsdotter, M., Navarez, D., Rebulanan, M., and Streibig, J. C. 1999. Weed suppressing rice cultivars—does allelopathy play a role? Weed Res. 39:441–454.

    Article  Google Scholar 

  • Preston, C. A., Betts, H., and Baldwin, I. T. 2002. Methyl jasmonate as an allelopathic agent: Sagebrush inhibits germination of a neighboring tobacco, Nicotiana attenuata. J. Chem. Ecol. 28:2343–2369.

    Article  PubMed  CAS  Google Scholar 

  • Ramamoorthy, V., Raguchander, T., and Samiyappan, R. 2002. Induction of defence-related proteins in tomato roots treated with Pseudomonas fluorescens Pf1 and Fusarium oxysporum f. sp. lycopersici. Plant Soil 239:55–68.

  • Reinbothe, S., Mollenhauer, B., and Reinbothe, C. 1994. JIPs and RIPs: the regulation of plant gene expression by jasmonates in response to environmental cues and pathogens. Plant Cell 6:1197–1209.

    Article  PubMed  CAS  Google Scholar 

  • Schmelz, E. A., Alborn, H. T., Banchio, E., and Tumlinson, J. H. 2003. Quantitative relationships between induced jasmonic acid levels and volatile emission in Zea mays during Spodoptera exigua herbivory. Planta 216:665–673.

    PubMed  CAS  Google Scholar 

  • Seal, A. N., Haig, T., and Pratley, J. E. 2004a. Evaluation of putative allelochemicals in rice root exudates for their role in the suppression of arrowhead root growth. J. Chem. Ecol. 30:1663–1678.

    Article  PubMed  CAS  Google Scholar 

  • Seal, A. N., Pratley, J. E., Haig, T., and An, M. 2004b. Identification and quantitation of compounds in a series of allelopathic and non-allelopathic rice root exudates. J. Chem. Ecol. 30:1647–1662.

    Article  PubMed  CAS  Google Scholar 

  • Seal, A. N., Pratley, J. E., Haig, T., and Lewin, L. G. 2005. Allelopathic potential in rice to control important rice weeds in the Riverina. Co-operative Research Centre for Sustainable Rice Production Final Report No. 3205.

  • Shigeru, T., Randeep, R., and Osamu, K. 1997. Phytoalexin production by amino acid conjugates of jasmonic acid through induction of aringenin-7-O-methyltransferase, a key enzyme on phytoalexin biosynthesis in rice (Oryza sativa L.). FEBS Lett. 401:239–242.

    Article  Google Scholar 

  • Taguchi, G., Yazawa, T., Hayashida, N., and Okazaki, M. 2001. Molecular cloning and heterologous expression of novel glucosyltransferases from tobacco cultured cells that have broad substrate specificity and are induced by salicylic acid and auxin. Eur. J. Biochem. 268:4086–4094.

    Article  PubMed  CAS  Google Scholar 

  • Thaler, J. S., Stout, M. J., Karban, R., and Duffey, S. S. 1996. Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J. Chem. Ecol. 22:1767–1781.

    Article  CAS  Google Scholar 

  • Thelen, G. C., Vivanco, J. M., Newingham, B., Good, W., Bais, H. P., Landres, P., Caesar, A., and Callaway, R. M. 2005. Insect herbivory stimulates allelopathic exudation by an invasive plant and the suppression of natives. Ecol. Lett. 8:209–217.

    Article  Google Scholar 

  • Thomma, B. P. H. J., Eggermont, K., Penninckx, I. A. M. A., Mauch-Mani, B., Vogelsang, R., Cammue, B. P. A., and Broekart, W. F. 1998. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. U S A 95:15107–15111.

    Article  PubMed  CAS  Google Scholar 

  • Turner, J. G., Ellis, C., and Evoto, A. 2002. The jasmonate signal pathway. Plant Cell 14:S153–S164.

    PubMed  CAS  Google Scholar 

  • Wang, Y. P., Tang, L. H., Zhang, H. S., and Fang, X. W. 2005. Induction effect of some weeds on the allelopathy of rice varieties. Chin. Ecol. Environ. 14:250–252.

    Google Scholar 

  • Zeng, R. S. and Luo, S. M. 1995. Relationship between allelopathic effects of Bidens pilosa aqueous extracts and rainfall. J. South China Agric. Univ. 16(4):69–72.

    Google Scholar 

  • Zeng, R. S., Luo, S. M., Shi, M. B., Shi, Y. H., Zeng, Q., and Tan, H. F. 2001. Allelopathy of Aspergillus japonicus on crops. Agron. J. 93:60–64.

    Article  CAS  Google Scholar 

  • Zeng, D. L., Qian, Q., Teng, S., Dong, G., Fujimoto, H., Yasufumi, K., and Zhu, L. 2003. Genetic analyses on rice allelopathy. Chin. Sci. Bull. 48(1):70–73.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the National 973 project of China (2006CB100200), Natural Science Foundation of China (30370246, 30670331), and Natural Science Foundation of Guangdong Province (group project 039254, 04105977), Guangdong Science and Technology Plan Program (2004B20501010, 2002C20506) and the Program for New Century Excellent Talents in University (NCET-04-0830) to R. S. Z. We thank three anonymous reviewers for helpful comments. We also thank Reed Johnson at University of Illinois at Urbana-Champaign for language revision.

Author information

Authors and Affiliations

  1. Research Center for Chemical Ecology, South China Agricultural University, Guangzhou, People’s Republic of China

    Hai Hong Bi, Ren Sen Zeng & Shi Ming Luo

  2. Institute of Tropical and Sub-tropical Ecology, South China Agricultural University, Wushan, Guangzhou, 510642, People’s Republic of China

    Hai Hong Bi, Ren Sen Zeng, Li Ming Su & Shi Ming Luo

  3. EH Graham Centre for Agricultural Innovation, Wagga Wagga, New South Wales, 2678, Australia

    Min An

Authors
  1. Hai Hong Bi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ren Sen Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Li Ming Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Min An
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shi Ming Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ren Sen Zeng.

Additional information

EH Graham Centre for Agricultural Innovation is a collaborative alliance between Charles Sturt University and the New South Wales Department of Primary Industries

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bi, H.H., Zeng, R.S., Su, L.M. et al. Rice Allelopathy Induced by Methyl Jasmonate and Methyl Salicylate. J Chem Ecol 33, 1089–1103 (2007). https://doi.org/10.1007/s10886-007-9286-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-007-9286-1

Keywords

Search

Navigation