Journal of Chemical Ecology

, Volume 39, Issue 2, pp 204–212 | Cite as

Changes in Rice Allelopathy and Rhizosphere Microflora by Inhibiting Rice Phenylalanine Ammonia-lyase Gene Expression

  • Changxun Fang
  • Yuee Zhuang
  • Tiecheng Xu
  • Yingzhe Li
  • Yue Li
  • Wenxiong Lin
Article

Abstract

Gene expression of phenylalanine ammonia-lyase (PAL) in allelopathic rice PI312777 was inhibited by RNA interference (RNAi). Transgenic rice showed lower levels of PAL gene expression and PAL activity than wild type rice (WT). The concentrations of phenolic compounds were lower in the root tissues and root exudates of transgenic rice than in those of wild type plants. When barndyardgrass (BYG) was used as the receiver plant, the allelopathic potential of transgenic rice was reduced. The sizes of the bacterial and fungal populations in rice rhizospheric soil at the 3-, 5-, and 7-leaf stages were estimated by using quantitative PCR (qPCR), which showed a decrease in both populations at all stages of leaf development analyzed. However, PI312777 had a larger microbial population than transgenic rice. In addition, in T-RFLP studies, 14 different groups of bacteria were detected in WT and only 6 were detected in transgenic rice. This indicates that there was less rhizospheric bacterial diversity associated with transgenic rice than with WT. These findings collectively suggest that PAL functions as a positive regulator of rice allelopathic potential.

Keywords

Allelopathy Phenylalanine ammonia-lyase Rhizospheric microbes Rice 

References

  1. Bastiaans, L. and Kropff, M. J. 2003. WEEDS | Weed Competition. Elsevier, Oxford.Google Scholar
  2. Belz, R. G. 2007. Allelopathy in crop/weed interactions: an update. Pest Manag. Sci. 63:308–326.Google Scholar
  3. Bertin, C., Yang, X. H., and Weston, L. A. 2003. The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83.CrossRefGoogle Scholar
  4. Bi, H. H., Zeng, R. S., Su, L. M., An, M., and Luo, S. M. 2007. Rice allelopathy induced by methyl jasmonate and methyl salicylate. J. Chem. Ecol. 33:1089–1103.PubMedCrossRefGoogle Scholar
  5. Camacho-Cristal, J. J., Anzellotti, D., and Gonzez-Fontes, A. 2002. Changes in phenolic metabolism of tobacco plants during short-term boron deficiency. Plant Physiol. Biochem. 40:997–1002.CrossRefGoogle Scholar
  6. Chauhan, B. S. and Johnson, D. E. 2011. Row spacing and weed control timing affect yield of aerobic rice. Field Crops. Res. 121:226–231.CrossRefGoogle Scholar
  7. 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.PubMedCrossRefGoogle Scholar
  8. Cipollini, D., Rigsby, C. M., and Barto, E. K. 2012. Microbes as targets and mediators of allelopathy in plants. J. Chem. Ecol. 38:714–727.PubMedCrossRefGoogle Scholar
  9. Dickerson, D. P., Pascholati, S. F., Hagerman, A. E., Butler, L. G., and Nicholson, R. L. 1984. Phenylalanine ammonia-lyase and hydroxycinnamate: CoA ligase in maize mesocotyls inoculated with Helminthosporium maydis or Helminthosporium carbonum. Physiol. Plant Pathol. 25:111–123.CrossRefGoogle Scholar
  10. Dilday, R. H., Lin, J., and Yan, W. 1994. Identification of allelopathy in USDA-ARS 320 rice germplasm collection. Aust. J. Exp. Agric. 34:907–910.CrossRefGoogle Scholar
  11. Fang, C. X., Xiong, J., Qiu, L., Wang, H. B., Song, B. Q., He, H. B., Lin, R. Y., and Lin, W. X. 2009. Analysis of gene expressions associated with increased allelopathy in rice (Oryza sativa L.) induced by exogenous salicylic acid. Plant Growth Regul. 57:163–172.CrossRefGoogle Scholar
  12. Fang, C. X., Wang, Q. S., Yu, Y., Li, Q. M., Zhang, H. L., Wu, X. C., Chen, T., and Lin, W. X. 2011. Suppression and overexpression of Lsi1 induce differential gene expression in rice under ultraviolet radiation. Plant Growth Regul. 65:1–10.CrossRefGoogle Scholar
  13. Ferrer, J. L., Austin, M. B., Stewart Jr., C., and Noel, J. P. 2008. Structure and function of enzymes involved in the biosynthesis of phenylpropanoids. Plant Physiol. Biochem. 46:356–370.PubMedCrossRefGoogle Scholar
  14. Gealy, D., Moldenhauer, K., and Duke, S. 2013. Root distribution and potential interactions between allelopathic rice, sprangletop (Leptochloa spp.), and barnyardgrass (Echinochloa crus-galli) based on 13C isotope discrimination analysis. J. Chem. Ecol. 39:186–203.Google Scholar
  15. He, H. Q., Lin, W. X., Liang, Y. Y., Song, B. Q., Ke, Y. Q., Guo, Y. C., and Liang, K. J. 2005. Analyzing the molecular mechanism of crop allelopathy by using differential proteomics. Acta Ecol. Sin. 25:3141–3146 (in Chinese with English abstract).Google Scholar
  16. He, H. B., Wang, H. B., Fang, C. X., Lin, Z. H., Yu, Z. M., and Lin, W. X. 2012a. Separation of allelopathy from resource competition using rice/barnyardgrass mixed-cultures. PLoS One 7:e37201. doi:10.1371/journal.pone.0037201.PubMedCrossRefGoogle Scholar
  17. He, H. B., Wang, H. B., Fang, C. X., Wu, H. W., Guo, X. K., Liu, C. H., Lin, Z. H., and Lin, W. X. 2012b. Barnyard grass stress up regulates the biosynthesis of phenolic compounds in allelopathic rice. J. Plant Physiol.. doi:10.1016/j.jplph.2012.06.018.
  18. Höfgen, R. and Willmitzer, L. 1988. Storage of competent cells for Agrobacterium transformation. Nucleic Acids Res. 16:9877.PubMedCrossRefGoogle Scholar
  19. IRRI (International Rice Research Institute). 1993. Rice Almanac 1993–95. IRRI, P.O. Box: 933, 1099 Manila, PhilippinesGoogle Scholar
  20. Jefferson, R. A. 1989. The GUS reporter system. Nature 342:837Y838.CrossRefGoogle Scholar
  21. Johnson, D. E., Wopereis, M. C. S., Mbodj, D., Diallo, S., Powers, S., and Haefele, S. M. 2004. Timing of weed management and yield losses due to weeds in irrigated rice in the Sahel. Field Crop Res. 85:31–42.CrossRefGoogle Scholar
  22. Kato-Noguchi, H. 2011. Barnyard grass-induced rice allelopathy and momilactone B. J. Plant Physiol. 168:1016–1020.PubMedCrossRefGoogle Scholar
  23. Kato-Noguchi, H. and Peters, R. J. 2013. The role of momilactones in rice allelopathy, J. Chem. Ecol. 39:175–185.Google Scholar
  24. Kato-Notuchi, H., Tamura, K., Sasaki, H., and Suenaga, K. 2012. Identification of two phytotoxins, blumenol A and grasshopper ketone, in the allelopathic Japanese rice variety Awaakamai. J. Plant Physiol. 169:682–685.CrossRefGoogle Scholar
  25. Lehoczky, E., Nelima, M. O., Szabó, R., Szalai, A., and Nagy, P. 2011. Allelopathic effect of Bromus spp. and Lolium spp. shoot extracts on some crops. Commun. Agric. Appl. Biol. Sci. 76:537–554.PubMedGoogle Scholar
  26. Lin, R. Y., Rong, H., Zhou, J. J., Yu, C. P., Ye, C. Y., Chen, L. S., and Lin, W. X. 2007. Impact of allelopathic rice seedlings on rhizospheric microbial populations and their functional diversity. Acta Ecol. Sin. 27:3644–3654.CrossRefGoogle Scholar
  27. Lin, R. Y., Wang, H. B., Guo, X. K., Ye, C. Y., He, H. B., Zhou, Y., and Lin, W. X. 2011. Impact of applied phenolic acids on the microbes, enzymes and available nutrients in paddy soils. Allelopathy J. 28:225–236.Google Scholar
  28. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265–275.PubMedGoogle Scholar
  29. Macdonald, M. J. and D’Cunha, G. B. 2007. A modern view of phenylalanine ammonia lyase. Biochem. Cell Biol. 85:273–282.PubMedCrossRefGoogle Scholar
  30. Macias, F. A., Chinchilla, N., Varela, R. M., and Molinllo, J. M. G. 2006. Bioactive steroids from Oryza sativa L. Steroids 71:603–608.PubMedCrossRefGoogle Scholar
  31. 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. Proceeding of the Workshop on Allelopathy in Rice. International Rice Research Institute, Manila, Philippines.Google Scholar
  32. Peršoh, D., Theuerl, S., Buscot, F., and Rambold, G. 2008. Towards a universally adaptable method for quantitative extraction of high-purity nucleic acids from soil. J. Microbiol. Meth. 75:19–24.CrossRefGoogle Scholar
  33. Seal, A. N., Pratley, J. E., Haig, T., and An, M. 2004. Identification and quantitation of compounds in a series of allelopathic and non-allelopathic rice root exudates. J. Chem. Ecol. 30:1647–1662.PubMedCrossRefGoogle Scholar
  34. Shen, Y., Jin, L., Xiao, P., Lu, Y., and Bao, J. S. 2009. Total phenolics, flavonoids, antioxidant capacity in rice grain and their relations to grain color, size and weight. J. Cereal Sci. 49:106–111.CrossRefGoogle Scholar
  35. Shin, D. H., Kim, K. U., Sohn, D. S., Kang, S. G., Kim, H. Y., Lee, I. J., and Kim, M. Y. 2000. Regulation of gene expression related to allelopathy, pp. 109Y24, in K. U. Kim and D. H. Shin (eds.), Rice Allelopathy. Proceedings of the Workshop in Rice Allelopathy. Kyungpook National University, Korea, Taegu.Google Scholar
  36. Singleton, V. L., Orthofer, R., and Lamuela-Raventós, R. M. 1999. Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods Enzymol. 299:152–178.CrossRefGoogle Scholar
  37. Song, B. Q., Xiong, J., Fang, C. X., Qiu, L., Lin, R. Y., Liang, Y. Y., and Lin, W. X. 2008. Allelopathic enhancement and differential gene expression in rice under low nitrogen treatment. J. Chem. Ecol. 34:688–695.PubMedCrossRefGoogle Scholar
  38. Supartana, P., Shimizu, T., Shioiri, H., Nogawa, M., Nozue, M., and Kojima, M. 2005. Development of simple and efficient in planta transformation method for rice (Oryza sativa L.) using Agrobacterium tumefaciens. J. Biosci. Bioeng. 4:391–397.CrossRefGoogle Scholar
  39. Walker, T. S., Bais, H. P., Grotewold, E., and Vivanco, J. M. 2003. Root exudation and rhizosphere biology. Plant Physiol. 132:44–51.PubMedCrossRefGoogle Scholar
  40. Wang, H. B., Yu, Z. M., He, H. B., Guo, X. K., Huang, J. W., Zhou, Y., Xu, Z. B., and Lin, W. X. 2012. Relationship between allelopathic potential and grain yield of different allelopathic rice accessions. Chin. J. Eco-Agric. 20:75–79 (in Chinese with English abstract).CrossRefGoogle Scholar
  41. Worthington, M. and Reberg-Horton, S. C. 2013. Breeding cereal crops for enhanced weed suppression: optimizing allelopathy and competitive ability. J. Chem. Ecol. 39:2. 39:213–231.Google Scholar
  42. Xu, Z. H., Guo, D. P., Yu, L. Q., Zhao, M., Zhang, X., Li, D., Zheng, K. L., and Ye, Y. L. 2003. Molecular biological study on the action mechanism of rice allelochemicals against weeds. Chin. J. Appl. Ecol. l4:829–833. in Chinese with English abstract.Google Scholar
  43. Xu, M., Galhano, R., Wiemann, P., Bueno, E., Tiernan, M., Wu, W., Chung, I. M., Gershenzon, J., Tudzynski, B., Sesma, A., and Peters, R. J. 2012. Genetic evidence for natural product-mediated plantYplant allelopathy in rice (Oryza sativa). New Phytol. 193:570–575.PubMedCrossRefGoogle Scholar
  44. Yoshida, S., Forno, D. A., and Cock, J. H. 1976. pp. 1–83, Laboratory Manual for Physiological Studies of Rice, 3rd ed. The International Rice Research Institute, Manila, the Philippines.Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Changxun Fang
    • 1
    • 2
  • Yuee Zhuang
    • 3
  • Tiecheng Xu
    • 1
    • 2
  • Yingzhe Li
    • 1
    • 2
  • Yue Li
    • 1
    • 2
  • Wenxiong Lin
    • 1
    • 2
  1. 1.Key Laboratory of Biopesticide and Chemical Biology, Ministry of EducationFuzhouPeople’s Republic of China
  2. 2.Institute of Agroecology/School of Life SciencesFujian Agriculture and Forestry University (FAFU)FuzhouPeople’s Republic of China
  3. 3.Quanzhou Medical CollegeQuanzhouPeople’s Republic of China

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