Systematic evaluation of plant metals/metalloids accumulation efficiency: a global synthesis of bioaccumulation and translocation factors

Abstract

Phytoremediation, which involves the use of plants to accumulate and translocate metals and metalloids, represents a promising strategy for environmental remediation. The efficiency of phytoremediation is influenced by many factors such as metal/metalloid types, soil properties, and plant traits. It remains unclear how these factors modulate the efficiency of phytoremediation. We synthesized 547 data pairs from 82 studies to comprehensively evaluate the ability of hyperaccumulating plants to accumulate and translocate metals/metalloids under varying environmental conditions. The results show that cadmium (Cd), the most frequently investigated heavy metal, has the highest average bioaccumulation factor (BF) (10.0 ± 1.3) but a relatively low average translocation factor (TF) (1.8 ± 0.1). Aboveground biomass (AGB) of Cd hyperaccumulators is negatively correlated with BF but positively correlated with TF. Cd hyperaccumulating plants exhibit the highest accumulation capacity (maximal BF = 191), with roots outperforming aerial parts. The lower TF is mainly due to the lower AGB of Cd hyperaccumulating plants. In contrast, nickel (Ni) hyperaccumulators exhibit the highest TF, particularly in leaves and stems, indicating that Ni primarily accumulates in the aboveground parts. As soil pH increases, the BF of Cd and Zinc (Zn) decrease, whereas the BF of lead (Pb) increases, likely due to their distinct chemical behaviors under different pH conditions. Threshold concentrations were also identified for several for metals/metalloids (e.g., Cd: 214.8 mg kg^-1; Pb: 31352.3 mg kg^-1), beyond which BF falls below 1.0, indicating diminished accumulation efficiency due to toxicity constraints. In sum, these findings provide insights for optimizing phytoremediation strategies, aiding in plant selection and remediation condition optimization for improved efficiency and sustainability.

Keywords: bioaccumulation; hyperaccumulator; metals/metalloids; phytoremediation; soils; translocation.

Figure 1

Bioaccumulation (A) and translocation (B) factors for different metals/metalloids. The numbers in the brackets are the observation numbers included in this study. The black circle points and error bars represent the average values and standard errors.

Figure 2

Comparisons of bioaccumulation (A) and translocation (B) factors between historically and newly contaminated observations. Different colors represents significant difference between historically and newly contaminated observations. Scatter plots show the distribution of bioaccumulation and translocation factors, respectively. ***, **, * represent p<0.001, p<0.01 and p<0.05, respectively.

Figure 3

Comparison of bioaccumulation (A) and translocation (B) factors between field and laboratory studies of different metals/metalloids. Different colors letters represent significant differences between field studies and laboratory studies. Scatter plots show the distribution of bioaccumulation and translocation factors, respectively. ***, **, * represent p<0.001, p<0.01 and p<0.05, respectively.

Figure 4

Relationships between bioaccumulation factor and soil pH. Subplots represent relationships between BF of Cd (A), Pb (B), Zn (C) and soil pH. Power and linear regression model were used to correlate the relationships between BF and soil pH. p value shows the significance of the regression.

Figure 5

Relationship between bioaccumulation factor and total metals/metalloids content (A) in soil. The dash lines mark the total metals/metalloids content in soil when BF is equal to 1.0. Adj. R ², F value and p value show the regression results for Cd, As, Pb, Cu and Zn (B), respectively.

Figure 6

Relationship between available metals/metalloids content in soil and bioaccumulation factor. Based on the database, only the relationships for Cd (A) and Zn (B) are developed by a linear model. p <0.001 represents significance of the regression. The available contents of Cd and Zn when BF=1.0 are marked on the figures.

Figure 7

Spearman’s ranking correlation between bioaccumulation factor and translocation factor and climate, experiment duration, soil properties and plant characteristics for Cd. Color band shows the correlation coefficient. Asterisks show the significance of the correlation. ***, **, * represent p <0.001, p <0.01 and p <0.05, respectively.

Figure 8

BFs of Cd in the stems (A), leaves (B), and roots (C) of 12 plant species and relationship between BF_leaves and BF_stem (D).

Figure 9

Classification map of hyperaccumulator plants. The hyperaccumulators of different heavy metal types were classified according to family, genus and species, and different colors were used to indicate the range of BF and TF value of each plant. Green means greater than 1, red means less than 1, and yellow means both greater than 1 and less than 1.