Root-secreted Allelochemical in the Noxious Weed Phragmites Australis Deploys a Reactive Oxygen Species Response and Microtubule Assembly Disruption to Execute Rhizotoxicity

Abstract

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.

Phytotoxicity induced by Phragmites australis: an assessment of phenotypic and physiological parameters involved in germination process and growth of receptor plant

“…This experiment showed a substantial reduction of root length, biomass, and several ecophysiological parameters. These results are consistent with several studies which found that P. australis lowered the root biomass of endemic Eriocaulon carsonii due to belowground competition (Davies et al 2010) and showed negative effects on the germination and establishment of Arabidopsis thaliana in vivo conditions while conversely showing a positive effect under AC treatment (Rudrappa et al 2007). Our previous study found that P. australis rhizosphere and infested soil contained total phenolics with a concentration of 1.17 and 1.26 mg g (1 , respectively, that might be enough for an inhibitory effect on the associated plant species (Uddin et al 2012).…”

“…The presence of gallic acid in root exudates of P. australis was previously reported by Rudrappa et al (2007), but no relative abundance among organs was studied in details. The present study confirmed the rank of abundance among different organs.…”

“…Some chemicals produced by the decomposition of belowground organs of P. australis may be responsible for the die back of P. australis itself (Armstrong & Armstrong 1999), and photodegradation of secreted phytotoxins by P. australis executes severe phytotoxicity to other plant species ). Previous studies have shown that water extracts of P. australis organs have strong phytotoxic effects on germination and growth of other plant species (Rudrappa et al 2007; Uddin et al 2012). Identified phenolics such as gallic acid in P. asutralis root exudates showed inhibitory effects on the germination and growth of various seeds (Rudrappa et al 2007;Uddin et al 2012), but the physiological and biochemical effects of the extracts have been lacking.…”

“…Previous studies have shown that water extracts of P. australis organs have strong phytotoxic effects on germination and growth of other plant species (Rudrappa et al 2007; Uddin et al 2012). Identified phenolics such as gallic acid in P. asutralis root exudates showed inhibitory effects on the germination and growth of various seeds (Rudrappa et al 2007;Uddin et al 2012), but the physiological and biochemical effects of the extracts have been lacking. Generally, phytotoxic activity in nature depends on the release of a mixture of phytotoxins and joint effects of them rather than an individual chemical (Reigosa et al 1999;Inderjit & Duke 2003).…”

“…Undisturbed reserve mobilization is an important requirement for germination during the catabolic process just after liquid imbibition (Kupidłowska et al 2006). Rudrappa et al (2007) found that the root-secreted allelochemicals from P. australis deployed a reactive oxygen species (ROS) that is responsible for stress conditions on the affected plant. However, most of the studies focused on the individual organ that makes them difficult and assessment of phytotoxicity of that relative to other organs.…”