Root-secreted Allelochemical in the Noxious Weed Phragmites Australis Deploys a Reactive Oxygen Species Response and Microtubule Assembly Disruption to Execute Rhizotoxicity
- 806 Downloads
Phragmites australis is considered the most invasive plant in marsh and wetland communities in the eastern United States. Although allelopathy has been considered as a possible displacing mechanism in P. australis, there has been minimal success in characterizing the responsible allelochemical. We tested the occurrence of root-derived allelopathy in the invasiveness of P. australis. To this end, root exudates of two P. australis genotypes, BB (native) and P38 (an exotic) were tested for phytotoxicity on different plant species. The treatment of the susceptible plants with P. australis root exudates resulted in acute rhizotoxicity. It is interesting to note that the root exudates of P38 were more effective in causing root death in susceptible plants compared to the native BB exudates. The active ingredient in the P. australis exudates was identified as 3,4,5-trihydroxybenzoic acid (gallic acid). We tested the phytotoxic efficacy of gallic acid on various plant systems, including the model plant Arabidopsis thaliana. Most tested plants succumbed to the gallic acid treatment with the exception of P. australis itself. Mechanistically, gallic acid treatment generated elevated levels of reactive oxygen species (ROS) in the treated plant roots. Furthermore, the triggered ROS mediated the disruption of the root architecture of the susceptible plants by damaging the microtubule assembly. The study also highlights the persistence of the exuded gallic acid in P. australis’s rhizosphere and its inhibitory effects against A. thaliana in the soil. In addition, gallic acid demonstrated an inhibitory effect on Spartina alterniflora, one of the salt marsh species it successfully invades.
KeywordsPhragmites australis Spartina alterniflora Root exudation Allelopathy Gallic acid Reactive oxygen species Microtubule
HPB acknowledges the University of Delaware and EPSCoR for a faculty start-up grant. The authors thank Dr. Jung-Youn Lee and Dr. Gili Ben-Nissan, Delaware Biotechnology Institute for providing the microtubule-specific GFP-fusion line of Arabidopsis. The authors also thank Dr. Kirk Czymmek and the faculty of the Bio-imaging Center, Delaware Biotechnology Institute for the help with the microscopic studies.
- Bais, H. P., Walker, T. S., Kennan, A. J., Stermitz, F. R., and Vivanco, J. M. 2003b. Structure-dependent phytotoxicity of catechins and other flavonoids; flavonoid conversions by cell-free protein extracts of Centaurea maculosa (spotted knapweed) roots. J. Agric. Food Chem. 51:897–901.PubMedCrossRefGoogle Scholar
- Barman, K., and Rai, S. N. 2000. Role of tannins in plant–animal relationship—a review. Ind. J. Dairy Sci. 53:390–410.Google Scholar
- Blossey, B. 2002. Native to North America or introduced or both? Ag Web, Cornell University, Ithaca, NY. http:/www.invasiveplants.net/P. australis/phrag/natint.htm.3p.
- Callaway, R. M., Deluca, T. H., and Belliveaut, W. M. 1999. Biological-control herbivores may increase competitive ability of the noxious weed Centaurea maculosa. Ecology 80:1196–1201.Google Scholar
- D’haeze, W., Rycke, R. D., Mathis, R., Goormachtig, S., Pagnotta, S., Verplancke, C., Capoen, W., and Holsters, M. 2003. Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semi aquatic legume. Proc. Natl. Acad. Sci. U S A 100:11789–11794.PubMedCrossRefGoogle Scholar
- Foreman, J., Demidchik, V., Bothwell, J. H. F., Mylona, P., Miedema, H., Torres, M. A., Linstead, P., Costa, S., Brownlee, C., Jones, J. D. G., Davies, J. M., and Dolan, L. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446.PubMedCrossRefGoogle Scholar
- Hansen, R. M. 1978. Shasta ground sloth food habits, Rampart Cave, Arizona. Paleobiology 4:302–319.Google Scholar
- Harrington, H. D. 1964. Manual of the Plants of Colorado. Sage Books, Denver, CO, pp. 666Google Scholar
- Makoto, P. I., Nahoko, S., Kazutop, I., Hiroyukip, T., and Yukio, P. O. 2000. Role of reactive oxygen species in gallic acid-induced apoptosis. Biol. Pharm. Bull. 23:1153–1157.Google Scholar
- Ohmoto, T. 1969. Triterpenoids and the related compounds from graminaceous plants. Yakugaku Zasshi 89:1682–1687.Google Scholar
- Qin, B., Perry, L. G., Broeckling, C. D., Du, J., Stermitz, F. R., Paschke, M. W., and Vivanco, J. M. 2006. Phytotoxic allelochemicals from roots and root exudates of leafy spurge (Euphorbia esula L). Plant Signaling and Behavior 1:323–327.Google Scholar
- Rafi, M. M., Vastano, B. C., Zhu, N., Ho, C. T., Ghai, G., Rosen, R. T., Gallo, M. A., and Dipaola, R. S. 2002. Novel polyphenol molecule isolated from licorice root (Glycyrrhiza glabra) induces apoptosis, G2/M cell cycle arrest, and Bcl-2 phosphorylation in tumor cell lines. J. Agric. Food Chem. 50:677–684.PubMedCrossRefGoogle Scholar
- Sokal, R. R., and Rolf, F. J. 1995. Biometry: The Principles and Practice of Statistics in Biological Research, 3rd edn. Freeman, New York.Google Scholar
- Staman, K., Blum, U., Louws, F., and Robertson, D. 2001. Can simultaneous inhibition of seedling growth and stimulation of rhizosphere bacterial populations provide evidence for phytotoxin transfer from plant residues in the bulk soil to the rhizosphere of sensitive species? J. Chem. Ecol. 27:807–829.PubMedCrossRefGoogle Scholar
- Weir, T. L., Bais, H. P., Stull, V. J., Callaway, R. M., Thelen, G. C., Ridenour, W. M., Bhamidi, S., Stermitz, F. R., and Vivanco, J. M. 2006. Oxalate contributes to the resistance of Gaillardia grandiflora and Lupinus sericeus to a phytotoxin produced by Centaurea maculosa. Planta 223:785–795.PubMedCrossRefGoogle Scholar