Native plant and microbial contributions to a negative plant-plant interaction

Abstract

A number of hypotheses have been suggested to explain why invasive exotic plants dramatically increase their abundance upon transport to a new range. The novel weapons hypothesis argues that phytotoxins secreted by roots of an exotic plant are more effective against naïve resident competitors in the range being invaded. The common reed Phragmites australis has a diverse population structure including invasive populations that are noxious weeds in North America. P. australis exudes the common phenolic gallic acid, which restricts the growth of native plants. However, the pathway for free gallic acid production in soils colonized by P. australis requires further elucidation. Here, we show that exotic, invasive P. australis contain elevated levels of polymeric gallotannin relative to native, noninvasive P. australis. We hypothesized that polymeric gallotannin can be attacked by tannase, an enzymatic activity produced by native plant and microbial community members, to release gallic acid in the rhizosphere and exacerbate the noxiousness of P. australis. Native plants and microbes were found to produce high levels of tannase while invasive P. australis produced very little tannase. These results suggest that both invasive and native species participate in signaling events that initiate the execution of allelopathy potentially linking native plant and microbial biochemistry to the invasive traits of an exotic species.

Figure 1.

Specific tannase activity in the root and rhizospheric samples of native plants S. alterniflora and S. patens. Tannase activity is expressed as enzyme units per milligram protein (per gram of FW). One enzyme unit is defined as the release of 1 μmol of gallic acid per minute. Different letters on the bars indicate a statistically significant difference between taxa.

Figure 2.

Neighbor-joining phylogram obtained with 16S rRNA gene sequences of bacterial isolates from exotic (E1–E4) and native (N2–N4) P. australis rhizosphere samples. Numbers at nodes represent bootstrap support.

Figure 3.

Tannase activity in bacterial isolates from exotic (Pseudomonas sp. strain E4) and native (Pseudomonas sp. strain N4) P. australis rhizospheric samples. Specific enzymatic activity is represented as the mean amount of free gallic acid released (μm, ±sd, n = 16) from gallotannin (5 mg L⁻¹) per 10⁵ cells. Same letters on the bars indicate no statistical difference in between treatments.

Figure 4.

Growth curves for Pseudomonas spp. isolated from exotic (strain E4) and native (strain N4). After growth in rich medium, strains were subcultured in minimal medium with either gallotannin (5 mg L⁻¹), gallic acid (5 mg L⁻¹), or no added carbon.

Figure 5.

Degradation of gallotannin by Pseudomonas spp. isolated from exotic (strain E4) and native (strain N4) P. australis stands. Total gallotannin concentration was measured in the medium during growth (Fig. 4) of each strain on gallotannin as the sole carbon source.

Figure 6.

Separation of native and exotic P. australis populations into coherent groups by benzoate-degrading microbial community size and gallotannin content. Data points are the means for four populations each of native and exotic P. australis. The error bars are the sd for MPN and gallotannin contents.