Gamma-Aminobutyric Acid Enhances Cadmium Phytoextraction by Coreopsis grandiflora by Remodeling the Rhizospheric Environment

Abstract

Gamma-aminobutyric acid (GABA) significantly affects plant responses to heavy metals in hydroponics or culture media, but its corresponding effects in plant-soil systems remain unknown. In this study, different GABA dosages (0-8 g kg^-1) were added to the rhizosphere of Coreopsis grandiflora grown in Cd-contaminated soils. Cd accumulation in the shoots of C. grandiflora was enhanced by 38.9-159.5% by GABA in a dose-dependent approach because of accelerated Cd absorption and transport. The increase in exchangeable Cd transformed from Fe-Mn oxide and carbonate-bound Cd, which may be mainly driven by decreased soil pH rather than GABA itself, could be a determining factor responsible for this phenomenon. The N, P, and K availability was affected by multiple factors under GABA treatment, which may regulate Cd accommodation and accumulation in C. grandiflora. The rhizospheric environment dynamics remodeled the bacterial community composition, resulting in a decline in overall bacterial diversity and richness. However, several important plant growth-promoting rhizobacteria, especially Pseudomonas and Sphingomonas, were recruited under GABA treatment to assist Cd phytoextraction in C. grandiflora. This study reveals that GABA as a soil amendment remodels the rhizospheric environment (e.g., soil pH and rhizobacteria) to enhance Cd phytoextraction in plant-soil systems.

Keywords: gamma-aminobutyric acid; heavy metal; phytoextraction; plant growth-promoting rhizobacteria; soil amendment.

Figure 1

Growth and Cd accumulation characteristics of C. grandiflora in Cd-contaminated soils supplemented with 0 (T1), 1 (T2), 2 (T3), 4 (T4), and 8 (T5) g kg⁻¹ gamma-aminobutyric acid (GABA). (A) Plant morphological features at harvest. (B) Plant biomasses (ANOVA for shoot: F = 1.109, P = 0.404, degree of freedom = 4; ANOVA for root: F = 3.140, p = 0.065, degree of freedom = 4). (C) Cd concentrations in plants (ANOVA for shoot: F = 9.143, p = 0.002, degree of freedom = 4; ANOVA for root: F = 19.554, p = 0.000, degree of freedom = 4). (D) Cd contents accumulated in plants in a single pot (ANOVA for shoot: F = 9.707, p = 0.002, degree of freedom = 4; ANOVA for root: F = 5.131, p = 0.016, degree of freedom = 4). (E) Cd bioconcentration factors (ANOVA for shoot: F = 9.049, p = 0.002, degree of freedom = 4; ANOVA for root: F = 19.675, p = 0.000, degree of freedom = 4). (F) Cd translocation factors (ANOVA: F = 4.468, p = 0.025, degree of freedom = 4). Data represent means ± standard deviations (B–F: n = 3); the same-colored bars labelled with different letters (a, b, c, and d) indicate significant differences (p < 0.05, Duncan’s test, one-way ANOVA) between groups. DW: dry weight.

Figure 1

Growth and Cd accumulation characteristics of C. grandiflora in Cd-contaminated soils supplemented with 0 (T1), 1 (T2), 2 (T3), 4 (T4), and 8 (T5) g kg⁻¹ gamma-aminobutyric acid (GABA). (A) Plant morphological features at harvest. (B) Plant biomasses (ANOVA for shoot: F = 1.109, P = 0.404, degree of freedom = 4; ANOVA for root: F = 3.140, p = 0.065, degree of freedom = 4). (C) Cd concentrations in plants (ANOVA for shoot: F = 9.143, p = 0.002, degree of freedom = 4; ANOVA for root: F = 19.554, p = 0.000, degree of freedom = 4). (D) Cd contents accumulated in plants in a single pot (ANOVA for shoot: F = 9.707, p = 0.002, degree of freedom = 4; ANOVA for root: F = 5.131, p = 0.016, degree of freedom = 4). (E) Cd bioconcentration factors (ANOVA for shoot: F = 9.049, p = 0.002, degree of freedom = 4; ANOVA for root: F = 19.675, p = 0.000, degree of freedom = 4). (F) Cd translocation factors (ANOVA: F = 4.468, p = 0.025, degree of freedom = 4). Data represent means ± standard deviations (B–F: n = 3); the same-colored bars labelled with different letters (a, b, c, and d) indicate significant differences (p < 0.05, Duncan’s test, one-way ANOVA) between groups. DW: dry weight.

Figure 2

Correlation network between soil physicochemical indices and alpha diversity indices. The color block size in the correlation heatmap indicates the absolute value of the correlation coefficient. *, **, and *** represent 0.01 < p < 0.05, 0.001 < p < 0.01, and p < 0.001, respectively. Orange and blue network lines indicate significantly positive and negative correlations (p < 0.05), respectively.

Figure 3

The rhizosphere bacterial community composition of C. grandiflora grown in Cd-contaminated soils supplemented with 0 (T1), 2 (T3), and 8 (T5) g kg⁻¹ GABA. The unweighted pair group method with arithmetic mean clustering tree (A) and principal component analysis (B) of samples at the operational taxonomic unit (OTU) level. (C) Venn diagram of OTUs among different soils. (D) Venn diagram of bacterial phyla among different soils. (E) Venn diagram of bacterial genera among different soils. (F) Stacked diagram showing the relative abundance of the top ten bacterial phyla in different soils.

Figure 4

Linear discriminant analysis (LDA) and effect size analysis (LDA scores > 3) showing the indicator bacteria in rhizosphere soils of C. grandiflora supplemented with 0 (T1), 2 (T3) and 8 (T5) g kg⁻¹ GABA. (A) Cladogram showing dominant bacteria between T1 and T3 soils. Identifiers labelled on the cladogram correspond to those in Supplementary Table S6. (B) Cladogram showing dominant bacteria between T1 and T5 soils. Identifiers labelled on the cladogram correspond to those in Supplementary Table S7. (C) Numbers of dominant bacteria at different taxonomic levels between T1 and T3 soils. (D) Numbers of dominant bacteria at different taxonomic levels between T1 and T5 soils. (E) Venn diagram of the differential bacterial phyla between T3 and T5 soils compared to the T1 soil. (F) Venn diagram of the differential bacterial genera between T3 and T5 soils compared to the T1 soil.

Figure 5

Dynamic heatmap and stacked graph showing the enriched bacterial genera (A) and correlation analysis between relative abundance of bacterial taxa and soil exchangeable Cd concentration (B) in C. grandiflora rhizosphere soils supplemented with 2 (T3) and 8 (T5) g kg⁻¹ GABA compared with the control soil (T1). The relative abundances of bacterial genera in the graph are normalized at the row level of the heatmap. The plus (+) sign indicates the rhizobacteria enriched in the T3 and/or T5 soils. Bacterial genera in red font indicate plant growth-promoting rhizobacteria, and bacterial genera marked with purple, green, and orange circles indicate rhizobacteria involved in Cd mobilization/immobilization, K solubilization, and P solubilization, respectively.