Leaf Functional Traits of Invasive Grasses Conferring High-Cadmium Adaptation Over Natives

Abstract

Heavy metal (HM) contamination resulting from industrialization and urbanization during the Anthropocene along with plant invasion can severely threaten the growth and adaptation of local flora. Invasive alien plant species generally exhibit a growth pattern consistent with their functional traits in non-contaminated environments in the introduced range. However, it remains unclear whether invasive alien plants have an advantage over native plants in contaminated environments and whether this growth pattern is dependent on the adaptation of their leaf functional traits. Here, we selected two congeneric pairs of invasive alien and native grasses that naturally co-exist in China and are commonly found growing in contaminated soil. To evaluate the effect of cadmium (Cd) on the structural and physiological leaf traits, we grew all four species in soil contaminated without or with 80 mg/kg Cd. Invasive plants contained significantly higher concentrations of Cd in all three organs (leaf, stem, and root). They displayed a higher transfer factor and bioconcentration factor (BCF) of shoot and root than natives, indicating that invasive species are potential Cd hyperaccumulators. Invasive plants accumulated polyphenol oxidase (PPO) to higher levels than natives and showed similar patterns of leaf structural and physiological traits in response to changes in Cd bioconcentration. The quantifiable leaf structural traits of invasive plants were significantly greater (except for stomatal density and number of dead leaves) than native plants. Leaf physiological traits, chlorophyll content, and flavonoid content were also significantly higher in invasive plants than in natives under Cd stress conditions after 4 weeks, although nitrogen balance index (NBI) showed no significant difference between the two species. Chlorophyll fluorescence parameters decreased, except for the quantum yield of photosystem II (ΦPSII) and the proportion of open photosystem II (qP), which increased under Cd stress conditions in both species. However, invasive plants exhibited higher fluorescence parameters than natives under Cd stress, and the decrement observed in invasive plants under Cd stress was greater than that in natives. High Cd adaptation of invasive grasses over natives suggests that invasive plants possess optimal leaf structural and physiological traits, which enable them to adapt to stressful conditions and capture resources more quickly than natives. This study further emphasizes the potential invasion of alien plants in contaminated soil environments within the introduced range. To a certain extent, some non-invasive alien plants might adapt to metalliferous environments and serve as hyperaccumulator candidates in phytoremediation projects in contaminated environments.

Keywords: bioconcentration factor; cadmium; leaf functional traits; physiological response; phytoremediation.

Figure 1

Experimental design. Notes, CK, control, Cd, cadmium stress. Experimental layout. R1-4 mean replicates.

Figure 2

Number of leaves (A), number of dead leaves (B) and plant height (C) of invasive and native plants during cadmium (Cd) stress. Control: uncontaminated soil + native and invasive: Treatment Cd contaminated soil (80 mg/kg) +native and invasive. Error bars depict the SE of the mean of four independent replicates.

Figure 3

Stomatal density (A), stomatal length (B), stomatal width (C), and stomatal area (D) of the invasive and native plants in response to cadmium (Cd). Values are means ± standard error (SE).

Figure 4

Leaf area (A) and leaf length (B) of the invasive and native plants in response to cadmium (Cd). Values are means ± standard error (SE).

Figure 5

Morphology of the abaxial leaf (A–D) and structure of the guard cells on abaxial surface (E–H) of the invasive (Paspalum dilatatum) and native plant (Pennisetum alopecuroides) in control and Cd stress treatments. Images were taken by light microscope for stomatal density with 50-μm scale and for guard cells with 20-μm scale.

Figure 6

Effect of cadmium (Cd) on chlorophyll content (A), flavonoids content (B) and NBI (C) of leaves in invasive and native plants during stress conditions. Control: uncontaminated soil + native and invasive plants: Treatment Cd contaminated soil (80 mg/kg) +native and invasive. Error bars depict the SE of the mean of four independent replicates.

Figure 7

Changes in chlorophyll fluorescence parameters in young-mature (i.e., just after reaching their final size) leaves of invasive and native plants during long term stress and acclimation in response to cadmium (Cd) treatment (A) F_t, ground fluorescence in the light-adapted state (B) F₀, ground fluorescence in the dark-adapted (C) F_v′/F_m′, maximum chlorophyll fluorescence in the light-adapted (D) F_v/F_m maximum chlorophyll fluorescence in the dark-adapted state. Values are means ± standard error (SE). Notes, 0, control 80, Cd concentration mg/kg.

Figure 8

Changes in chlorophyll fluorescence parameters in young-mature (i.e., just after reaching their final size) leaves of invasive and native plants during stress and long-term acclimation in response to cadmium (Cd) treatments (A) ΦPSII quantum yield of photosystem II (B) ΦPSII qP proportion of open photosystem II (C) ΦPSII F_v/F_m maximum quantum yield of photosystem II. Values are means ± standard error (SE).

Figure 9

Correlation matrix of chlorophyll fluorescence parameters in young-mature leaves of invasive and native plant species, the labels were similar in Table 1. The colored gradient legends represent coefficients of correlation r values from +1.0 (green) to −1.0 (red). The significant correlation at a level (p^*** <0.001), (p^** <0.001), (P^* <0.05). All coefficients were computed by the Pearson correlation for possible pairs of variables in the matrix.

Figure 10

Cd (Cadmium) concentrations in leaf (A), stem (B), and root (C) of the two group of invasive and native species under Cd 80 mg/kg level. Values are means ± standard error (SE).

Figure 11

Shoot BCF (bioconcentration factor) (A), Root BCF (bioconcentration factor) (B), and transfer factor (C), the two group of invasive and native species under Cd 80 mg/kg level. Values are means ± standard error (SE).

Figure 12

Polyphenol oxidase in leaf (A) and in root (B) in the two group of invasive and native species under Cd 80 mg/kg level. Values are means ± standard error (SE).