Journal of Hazardous Materials 441 (2023) 129904

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Journal of Hazardous Materials

journal homepage: www.elsevier.com/locate/jhazmat

Modeling phytoremediation of heavy metal contaminated soils through

machine learning
Liang Shi a, b, 1, Jie Li c, d, 1, Kumuduni Niroshika Palansooriya a, e, Yahua Chen b, Deyi Hou f,
Erik Meers g, Daniel C.W. Tsang h, Xiaonan Wang i, *, Yong Sik Ok a, *
a
Korea Biochar Research Center, APRU Sustainable Waste Management Program & Division of Environmental Science and Ecological Engineering, Korea University,
Seoul 02841, South Korea
b
College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China
c
Department of Chemical and Biomolecular Engineering, National University of Singapore, Singapore 117585, Singapore
d
CAS Key Laboratory of Urban Pollutant Conversion, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China
e
State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Hangzhou 311300, China
f
School of Environment, Tsinghua University, Beijing 100084, China
g
Department of Green Chemistry & Technology, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, Belgiu
h
Department of Civil and Environmental Engineering, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong, China
i
Department of Chemical Engineering, Tsinghua University, Beijing 100084, China

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Machine learning was used to predict

factors that affect phytoremediation.
• Metal ion radius was the most important
factor affects HM accumulation in
shoots.
• Plant family was the most important
factor that affect BCF and MER.
• Crassulaceae family had the highest
potential as hyperaccumulators.

A R T I C L E I N F O A B S T R A C T

Editor: Lingxin CHEN As an important subtopic within phytoremediation, hyperaccumulators have garnered significant attention due
to their ability of super-enriching heavy metals. Identifying the factors that affecting phytoextraction efficiency
has important application value in guiding the efficient remediation of heavy metal contaminated soil. However,
Keywords:
it is challenging to identify the critical factors that affect the phytoextraction of heavy metals in
Heavy metal
Hyperaccumulator
soil–hyperaccumulator ecosystems because the current projections on phytoremediation extrapolations are
Machine learning rudimentary at best using simple linear models. Here, machine learning (ML) approaches were used to predict

* Corresponding authors.
E-mail addresses: wangxiaonan@tsinghua.edu.cn (X. Wang), yongsikok@korea.ac.kr (Y.S. Ok).
1
These authors contributed equally to this work

https://doi.org/10.1016/j.jhazmat.2022.129904
Received 12 May 2022; Received in revised form 24 August 2022; Accepted 1 September 2022
Available online 5 September 2022
0304-3894/© 2022 Published by Elsevier B.V.
L. Shi et al. Journal of Hazardous Materials 441 (2023) 129904

Phytoextraction the important factors that affecting phytoextraction efficiency of hyperaccumulators. ML analysis was based on
Soil remediation 173 data points with consideration of soil properties, experimental conditions, plant families, low-molecular-
weight organic acids from plants, plant genes, and heavy metal properties. Heavy metal properties, especially
the metal ion radius, were the most important factors that affect heavy metal accumulation in shoots, and the
plant family was the most important factor that affect the bioconcentration factor, metal extraction ratio, and
remediation time. Furthermore, the Crassulaceae family had the highest potential as hyperaccumulators for
phytoremediation, which was related to the expression of genes encoding heavy metal transporting ATPase
(HMA), Metallothioneins (MTL), and natural resistance associated macrophage protein (NRAMP), and also the
secretion of malate and threonine. New insights into the effects of plant characteristics, experimental conditions,
soil characteristics, and heavy metal properties on phytoextraction efficiency from ML model interpretation
could guide the efficient phytoremediation by identifying the best hyperaccumulators and resolving its efficient
remediation mechanisms.

1. Introduction 2019a). For example, Sheoran et al (Sheoran et al., 2016). discovered

Heavy metals and metalloids are harmful pollutants owing to their
toxicity, ubiquity, non-biodegradability, and bioavailability for crop
uptake. Hence, they pose significant threats to worldwide food safety
and security (Hou et al., 2020). The enrichment of heavy metals will
reduce biodiversity and productivity, thereby altering the structure and
function of ecosystems (Montoya-Mayor et al., 2013; Niemeyer et al.,
2012). Some heavy metals are toxic and carcinogenic to humans. For
example, Hg, Pb, and As can affect the growth and function of the central
nervous system. Hg, Pb, and Cd can affect the kidney and liver. Ni, Cd,
and Cu can affect the skin, bone, and teeth (Bertin et al., 2017). For
example, the National Soil Pollution Survey Report jointly issued by the
Chinese Ministry of Environmental Protection and the Chinese Ministry
of Land and Resources shows that the point exceeding rates of Cd, Ni, As,
Cu, and Zn in Chinese soil are 7.0%, 4.8%, 2.7%, 2.1% and 0.9%,
respectively, threatening farmland production and food quality and
safety. Therefore, toxic heavy metals in ecosystems are detrimental to
the environment and human health, and we focus on these five kinds of
heavy metals here.
Phytoremediation is an environmentally friendly method compared
with physical, chemical, and other biological methods (Jin et al., 2021;
Wang et al., 2021). Plants with accumulation or super-accumulation
ability can transfer or immobilize heavy metals in soil to reduce their
damage to ecosystems (Wood et al., 2016). Phytoextraction is promising
for the in situ remediation of large area of contaminated land because it
directly employs plants with large biomass, rapid growth, heavy metal
tolerance, and high accumulation ability to repair heavy
metal-contaminated soil (Robinson et al., 2002). Plants with the
following heavy metal hold capacity are identified as hyper­
accumulators: plants with leaves or aboveground segments whose Cd
content exceeds 100 mg kg− 1; Co, Cr, Cu, Ni, and Pb contents exceed
1000 mg kg− 1; Zn content exceeds 3000 mg kg− 1; and Mn content
exceeds 10,000 mg kg− 1 (Li et al., 2018a). Additionally, the ratio of
heavy metal content in an aboveground hyperaccumulator to that un­
derground is always greater than 1 (Wood et al., 2016). More than 450
species of plants belonging to at least 34 families have been identified as
hyperaccumulators (Verbruggen et al., 2009). For example, Pteris cre­
tica, Pteris fauriei, Pteris oshimensis, and Pteris vittata are As hyper­
accumulators. Sedum alfredii, Sedum plumbizincicola, Arabis paniculata,
and Centella asiatica are Cd hyperaccumulators. Arabis paniculata,
Isachne globosa, Pogonatherum crinitum, are Pb hyperaccumulators. Ce­
losia argentea, Phytolacca americana, Polygonum lapathifolium, Polygonum
pubescens, and Schima superba are Mn hyperaccumulators. Arabis pan­
iculata, Corydalis davidii, Picris divaricata, S. alfredii, S. plumbizincicola,
and Viola baoshanensis are Zn hyperaccumulators (Li et al., 2018a).
Phytoremediation is a complicated process in which the trans­
formation and accumulation of heavy metals from soil to plants are
affected by the species, uptake mechanisms and physiological charac­
teristics of plants, soil physicochemical properties and agronomic
practices, physical and chemical properties of the heavy metals, and
environmental and experimental factors (Hu et al., 2020; Wang et al.,
that the success of phytoextraction depended on the plant biomass and
metal bioavailability, and that the phytoavailability of metals was
affected by the pH, redox potential, cation exchange capacity, type and
texture of soil, root exudates, and rhizosphere processes of plants. Liang
et al (Liang et al., 2009). compared the remediation efficiency of Cd/Zn
hyper- and non-hyperaccumulator plants and discovered that although
some hyperaccumulators had high bioconcentration factor (BCF), phy­
toextraction efficiency remained limited because of the small biomass.
However, these studies only considered a few or a single aspect of
quantitative variables, such as plant or soil variables; and they could not
be applied to quantitatively analyze the effect of qualitative variables
such as plant species, genotypes, and organic acids, which affected
phytoextraction efficiency. Few studies simultaneously considered
various factors (such as plants, soil, metals, experiment, and environ­
ment) and quantitatively evaluated the effects of each potential factor
and the spatial characteristics of bioaccumulation with respect to
different heavy metals and plants (Hanandeh et al., 2021; Li et al.,
2021a; Cipullo et al., 2019). Furthermore, it is difficult to construct a
comprehensive model that can predict the bioaccumulation factors of
heavy metals in soil–hyperaccumulator systems. The methods used in
previous studies could not identify the importance of different variables
in the modeling process, which is vital for decision-makers in identifying
the essential factors for heavy metal pollution control and phytor­
emediation in soils.
ML, a subcategory of artificial intelligence, can adapt and learn from
large, complex, and multidimensional data to develop predictive
models. Different ML algorithms, such as artificial neural networks
(ANNs), random forests, and gradient boosted machines, have been
widely used to model the heavy metal adsorption in water systems. For
example, Cd accumulation in farmland soils, availability and toxicity of
heavy metals in soils by compost or biochar, and heavy metal accumu­
lation derived from soil–crop systems (Hu et al., 2020; Hanandeh et al.,
2021; Li et al., 2021a; Cipullo et al., 2019). However, the use of ML to
identify the factors that affect the accumulation of heavy metals in
hyperaccumulators has not been established and is worth investigating
to elucidate the hidden and intertwined relations.
Hence, plant family, environmental conditions, soil properties, and
metal properties are considered as input data in this study to predict the
factors that affecting phytoextraction by ML approach. This study pro­
vides new insights into the phytoremediation of heavy metal contami­
nation in soil–hyperaccumulator ecosystems and guarantees the safety
of agricultural products (Fig. 1).
2. Methodology
2.1. Dataset preparation
We performed a systematic literature search and review to obtain a
comprehensive dataset for the ML model. Keywords associated with the
phytoremediation of heavy metals in soils were used to obtain relevant
literature from Google Scholar (https://scholar.google.com) and Web of

2
L. Shi et al.
Fig. 1. Schematic diagram of Machine Learning applied in this work. Driven by
the ML model, 173 available input and output data were used to evaluate the
heavy metal enrichment effect of hyperaccumulators.
Science (https://www.webofscience.com). We used ‘Hyper­
accumulator’, ‘Heavy metal’ and ‘pH’ as key words to search paper on
‘Web of Science’. In addition, we used ‘Hyperaccumulator’, ‘Heavy
metal’, ‘pH’, ‘Cation exchange capacity’, ‘Organic carbon’, ‘Tempera­
ture’, ‘Organic acid’, ‘Gene’, ‘Time’, ‘Pot’, ‘Field’, ‘Soil weight’, ‘Ni’,
‘Cd’, ‘Zn’, ‘As’, ‘Cu’ as key words to search paper on ‘Google Scholar’.
Data pertaining to soil, heavy metals, plants, and experiments were
extracted as inputs, and the shoot heavy metal concentration (HMshoot,
µg/g), shoot yield (yield, mg/plant), BCFs, metal extraction ratio (MER,
%), and remediation time (RT, per kg soil [yr]) were identified as out­
puts to compile the original datasets (Fig. 1).
The properties of the soil, including pH, cation exchange capacity
(CEC, cmol/kg), and organic carbon (OC, g/kg) were considered for the
properties of different heavy metals, and the electronegativity of heavy
metals (HM_x), ion radius of heavy metals (HM_r, nm), and total heavy
metal concentration (μg/g) were identified from only 20 papers by
searching across major databases. Information regarding the different
plants obtained from the literature was categorized based on the family
level. The experimental conditions, including the temperature differ­
ence during planting, planting time, soil mass used for pot experiments,
and pot depth, were considered for modeling. A dataset contained 173
data points were obtained with five heavy metals (As, Cd, Cu, Ni, and
Zn), seven different family levels of plants, and seven types of soils
related. All of the data come from 20 papers which provide all the
necessary information, including experimental conditions, hyper­
accumulator information, heavy metal properties and soil properties in
common.
To interpret the phytoremediation mechanism, eight types of low
molecular weight organic acids (LMWOAs) generated from plants and
21 types of gene expression in plants were considered as other outputs
here to develop individual classification models that could aid in un­
derstanding the mechanism (Fig. 1). Since organic acids have the
function of chelating heavy metals, they may change the available
content of heavy metals in the soil. Under the regulatory action of heavy
metal-related transport genes, the accumulation of heavy metals by
plants increase. Therefore, we also targeted the two aspects (LMWOAs
and gene expression) to investigate their impacts on the phytor­
emediation efficiency of hyperaccumulator.
2.2. Data pre-processing and ML model development
For the preliminary datasets, the unit for each variable was uniform
before the model development. We performed the data statistics on the
compiled datasets and found that 2.9% and 4.6% of the temperature
difference and soil weight data were missing. The missing values were
filled in using the K-Nearest Neighbor method to complete the dataset
for model training. After this data filling, we obtained three datasets for
phytoremediation properties, plant acid generation and plant genes
expression, respectively. Each dataset contained 173 pieces of data­
points without missing values. Moreover, one-hot encoding was per­
formed to transfer the categorical features (heavy metal type, plant
family, LMWOA, and plant genes) into a one-hot numeric array (Pant
3
Journal of Hazardous Materials 441 (2023) 129904
et al., 2021). To ease downstream model training and testing, the entire
dataset was partitioned into two, i.e., 80% for hyperparameter tuning
based on 5-fold cross-validation (CV) and ML model training, and the
remaining 20% data as test set for validating the generalization ability of
the trained models.
Based on our previous work, extreme gradient boosting (XGBoost),
an effective ML algorithm for modeling the application of carbon related
material (Yuan et al., 2021), was employed to develop multilabel pre­
diction model where the model could predict the five above-mentioned
outcomes (i.e., HMshoot, yield, BCFs, MER, and RT) at the same time. It
was owing to the success of tree-based ensemble algorithms develop­
ment and good tradeoff between bias and variance to avoid overfitting
for the regression predictive model. Based on the gradient boosting
models demonstrated in our previous study (Li et al., 2021a), XGBoost
used more accurate approximations to identify the best tree model, i.e.,
by computing second partial derivatives (second-order gradients) of the
loss function to obtain more information for the gradient direction (Chen
and Guestrin, 2016). Moreover, regularization terms as penalty were
integrated to avoid the bias and improve model generalization. In
XGBoost, four important hyperparameters, including the n_estimators,
learning_rate, subsample ratio, and max_depth, were adjusted to adapt
to our dataset. For tree-based models, it is unnecessarily to do the data
normalization because they are irrelevant to the absolute values to split
the trees (Li et al., 2021b). Therefore, the original input values were
directly used for the model development of XGBoost.
To identify the types of LMWOA generated and the effect of plant
genes on the mechanism of heavy metal phytoremediation, the ANN
algorithm with ‘sigmoid’ as the activation function in the output layer
was applied to develop classification models. The reason to select ANN
model for classification is that ANN has been proven to be able to handle
the gene expression profiling and it is also quite popular in the phytor­
emediation domain. The detailed description of the ANN algorithm is
described in our previous paper (Li et al., 2021b). Here, two hidden layer
ANNs were developed and the number of neurons in each hidden layer
was optimized by searching optimal numbers from 2 to 128. Moreover,
the activation function in the hidden layer was ‘relu’, and ‘adam’ was
selected as the optimizer with learning rate oof 0.001 during model
training. To train the ANN classification model, in addition to the inputs
considered in the previous regression model, the heavy metal type was
considered by creating a binary column for each heavy metal. Subse­
quently, all inputs in the entire dataset were normalized before training
and test data splitting to improve the convergence process during model
training by removing the mean and scaling to the unit variance (Li et al.,
2021c).
2.3. ML model performance evaluation and model-based feature analysis
Once the ML models were developed, the remaining 20% of the data
points were introduced to evaluate the prediction performance. For the
regression model, the determination coefficient (R2) and root mean
squared error (RMSE) were applied to obtain the prediction accuracy
(Yuan et al., 2021) with an R2 value closer to one indicating a better
prediction; whereas, a smaller RMSE represented a higher accuracy.
Accuracy was denoted by the accuracy score and F1 score were for the
classification models (Anon, 2022a).
∑
N
y n − yn )2
(̂
R 2
(y, ̂y ) = 1 − n=1
(1)
∑N
(yn − y)2
n=1
√̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅
√N
√∑
2
√ (̂
√n=1 y n − yn )
RMSE (y, ̂y ) = (2)
N
L. Shi et al.
1 ∑
N− 1
accuracy score (y, ̂
y) = I(̂
y i = yi ), (3)
N N
where y, y, and ̂ y are the true value, average of the true value, and
predicted value among the total number of data points (N) for each
prediction target, respectively. I(̂y i = yi ) represents the indicator func­
tion, as follows:
{ }
1 if ̂y i = yi ,
I(̂
y i = yi ) = (4)
0 if ̂y i ∕
= yi .
F1 score = 2 ×
Pr × Re
(5)
Pr + Re
TP
Pr = (6)
TP + FP
TP
Re = (7)
TP + FN
where, Pr and Re are the precision and recall of the classification model.
TP, FN, and FP are the numbers of true positives, false negatives, and
false positives, respectively. The “micro” was selected during F1 score
calculate to calculate metrics globally by counting the total true posi­
tives, false negatives and false positives.
Feature analysis, including feature importance and feature correla­
tion, was interpreted based on the developed models with the best
prediction performance. For the regression model, the feature impor­
tance was automatically achieved from the Gini importance by devel­
oping a tree-based XGBoost model (Rosa, 2022). This model provided a
score to indicate the value of each feature during the construction of
trees within the model. The importance was calculated based on the
improvement in the performance measured by the Gini index during the
selection of the split point to develop the trees. The final feature
importance was averaged from all constructed trees in the model. It
should be noted that although the Gini importance tends to bias towards
numerical values, such feature importance could be acceptable since it
has been cross validated by another feature analysis method (Pal­
ansooriya et al., 2022). For the feature correlation, XGBoost was inte­
grated with the partial dependence plot (PDP) Python tool (PDPbox) to
visualize the marginal effect of a specified input variable with different
values on the model outcome (Anon, 2022b). In the ANN classification
models, feature importance was identified using the SHAP method,
which proved to be useful for explaining black box models. SHAP
method determines the importance of features based on SHAP value
which is a concept in cooperative game theory. More details regarding
the SHAP method are available in our previous paper (Li et al., 2020).
3. Results and discussion
3.1. Statistical analysis of data acquired
Table S1 lists the basic descriptive statistics of the heavy metal
concentrations in the soil samples. The average, minimum and
maximum concentrations of heavy metals in soil were in the following
order: Ni (1014 mg kg-1; min: 553 mg kg-1 - max: 1780 mg kg-1) > Zn
(631 mg kg-1; min: 109 mg kg-1 - max: 3170 mg kg-1) > Cu (294 mg kg-
1
; min: 196 mg kg-1 - max: 801 mg kg-1) > As (131 mg kg-1; min:
126 mg kg-1 - max: 135 mg kg-1) > Cd (7.1 mg kg-1, min: 0.34 mg kg-1 -
max: 48 mg kg-1). The concentrations of all heavy metals in the soil were
higher than the typical background concentrations and ecological soil
screening levels. The coefficient of variation (CV) represented the degree
of variability in heavy metal concentrations. The high CV of heavy
metals in soils from the survey region indicated that the accumulation of
heavy metals in these soils was likely due to anthropogenic activities
(Manta et al., 2002).
Table S2 presents the basic statistical characteristics of the heavy
4
Journal of Hazardous Materials 441 (2023) 129904
metal concentrations in the hyperaccumulator. The average, minimum
and maximum concentrations of heavy metals in the hyperaccumulators
were in the following order: Ni (8586 mg kg-1; min: 1303 - max: 23387)
> Zn (3430 mg kg-1; min: 79.7 - max: 15469) > As (3109 mg kg-1; min:
1080 - max: 5138) > Cd (96.8 mg kg-1; min: 0.45 - max: 1310) > Cu
(15.6 mg kg-1; min: 5.7 - max: 35.6). The CVs of Ni, Zn, As, Cd, and Cu
concentrations were 72.07%, 114.63%, 92.29%, 190.48%, and 62.32%,
respectively. The CVs of all heavy metal concentrations in the hyper­
accumulators indicated high or exceptionally high variabilities (Ridge­
way, 2020). The maximum concentrations of Ni, Zn, As, Cd, and Cu in
the hyperaccumulators here were significantly higher than the defined
heavy metal concentrations in typical hyperaccumulators.
Figure S3 shows the BCFs of the heavy metals in the different
hyperaccumulators. The mean BCFs for each heavy metal based on
average values from different hyperaccumulators were as follows: As
(24.39) > Cd (21.96) > Ni (7.71) > Zn (7.21) > Cu (0.05). Crassulaceae
exhibited the highest BCFs for Cd (37.33) and Zn (9.50), Brassicaceae,
Cu (0.06), Ni (7.71), and Pteridaceae, for As (24.39).
3.2. Development of regression predictive model
Based on our preliminary regression model development trials, it was
difficult to adapt the outputs, including the five identified targets
(HMshoot [µg/g], yield [mg/plant], BCF, MER [%], and RT per kg soil
[y]), to the ML models. After performing a data distribution analysis, it
was discovered that the data did not present a normal distribution owing
to the dispersed data points (see Figure S1). To solve this issue and
improve the model performance, a logarithmic transformation was
employed to redistribute the data, (see Figure S2).
Apart from the data preprocessing, several critical hyperparameters
in XGBoost were adjusted using the training dataset based on five-fold
cross-validation to obtain a predictive model with good prediction
performance. The average RMSE for all targets from validation was used
to determine the optimal hyperparameters. Based on the hyper-
parameter tuning results of XGBoost (see Figure S4), the average
RMSE decreased as the number of trees (n_estimators) increased from 10
to 30; then, decreased until the learning rate increased to 0.1. Moreover,
based on an optimal n_estimator of 30 and a learning rate of 0.1, the
subsample rate and maximum depth (max_depth) of the trees were
further optimized. The results indicated that a smaller average RMSE
was achieved with a subsample rate of 0.7 and a maximum depth of 5
(see Figure S4). Based on the optimal hyperparameters, two XGBoost
models were trained with the output data before and after logarithmic
transformation (Sigmund et al., 2020). It was discovered that the pre­
diction performance improved after the original output data were
logarithmically transferred, particularly for the testing performance.
The XGBoost model performed better with the transformed data closer
to a normal distribution, since the value ranges of the transformed data
were more compact and balanceable, which was more acceptable for
regression model (Table 1, Figures S1 and S2).
The original experimental data versus the predicted data of heavy
metal concentrations in terms of the shoot concentration (HMshoot),
shoot yield (yield), BCF, MER, and RT are shown as scatter plots (see
Fig. 2). The line y = x indicated that the predicted values were equal to
the measured value, and the closer the dots were to the y = x line, the
better the prediction efficiency. Almost all the predicted and training
points were concentrated on the y = x line; however, the predicted
points indicated a less dense distribution than the training data points
because of the slightly deteriorated accuracy in the prediction perfor­
mance. The R2 values of the XGBoost model for the HMshoot, yield, BCF,
MER, and RT in the test dataset were 0.93, 0.79, 0.89, 0.92, and 0.91,
respectively, which were higher than the average 5-fold CV R2. How­
ever, these values were still located in the ranges of the standard devi­
ation plus the average 5-fold CV R2 (See Figure S5). This result indicated
that our developed model did not have serious overfitting issues.
L. Shi et al. Journal of Hazardous Materials 441 (2023) 129904

Table 1 importance of the pot depth and total heavy metal concentrations was
Training and testing performance of developed XGBoost models based on orig­ less than 25% of the metal ion radius. This showed that the heavy metal
inal and log-transferred output data. concentration in the shoots was primarily determined by the metal ion
Items Output parameters Training Testing radius. Based on the correlation analysis of the top four features (see
R2 RMSE R2 RMSE
Fig. 4a), the metal ion radius and pot depth were negatively associated
Original HMshoot (µg/g) 0.97 629 0.77 1371 with the HMshoot, and they exhibited a linear relationship with a high
Yield (mg/plant) 0.98 346 -0.15 1804 slope in the metal ion radius range of 0.07–0.10 nm and pot depth range
BCF 0.97 2.99 0.59 13.19 of 20–100 cm. In addition, the total heavy metal concentrations in soil
MER (%) 0.97 0.80 0.52 2.11
and soil mass (0.6–1 kg) contributed positively to the HMshoot (see
RT per kg soil (yr) 0.91 8420 0.71 9460
Log transferred HMshoot (µg/g) 0.96 0.57 0.93 0.66 Fig. 4a). The results showed that the high HMshoot was primarily due to
Yield (mg/plant) 0.93 0.55 0.79 0.77 the small metal ion radius, shallow pot depth, high total heavy metal
BCF 0.95 0.44 0.89 0.69 concentrations in soil, and soil mass (0.60–1 kg). Gu et al (Gu and Lan,
MER (%) 0.95 0.60 0.92 0.77 2021). discovered that the adsorption capacity of Neochloris oleoa­
RT per kg soil (yr) 0.96 0.59 0.91 0.83
bundans biomass to two-valence metal ions investigated in their study
Note: HMshoot: heavy metal concentration in shoots (µg/g); yield: shoot yield was proportional to the electronegativity and inversely proportional to
(mg/plant); BCF: bioconcentration factor; MER: metal extraction ratio (%); RT the radius of the metal ions; however, the exact reason has not been
per kg soil (yr): remediation time (1 year, 1 kg contaminated soil). clarified.
Fig. 3b shows that the experimental condition type constituted 48%
3.3. Model-based interpretation to yield prediction; whereas, the metal property type constituted only
4%. Soil mass was the most important feature for yield, followed by OC
Further, a feature analysis of each input to each output was per­ in soil, Brassicaceae, and planting time. Based on the correlation anal­
formed to understand the phytoremediation process (see Fig. 3). The ysis of the top-four experimental condition features (see Fig. 4b), the soil
input variables were categorized into four types to determine the mass was positively associated with the yield in the ranges of 0.6–1.5 kg
importance of each feature type: plant family, experimental conditions, and negatively related in the ranges of 4–6 kg. The soil OC was nega­
soil properties, and metal properties. Fig. 3a shows the metal property tively associated with the yield when the concentration was 24.6 kg to
contributed 71% to the HMshoot in terms of importance; whereas the soil 81.7 g/kg. The planting time was positively associated with the yield
property contributed only 4%. The ionic radius of metal was the most from 0.83 to 2.84 months. Meanwhile, the yield increased and reached a
important feature for the HMshoot, followed by the pot depth and total maximum when the temperature difference was 4 ◦ C; this increase was
heavy metal concentration in the soil (see Fig. 3a). Although the three associated with an improvement in soil enzyme activity. The yield of
features mentioned were the top three notable features, they indicated buckwheat (Polygonaceae family) increased owing to improvements in
significant differences on the importance for the HMshoot. The the accumulated temperature, temperature and water use efficiency,

Fig. 2. Multi-task predicted data vs original experimental data of (a) heavy metal concentration in shoot (HMshoot), (b) shoot yield (Yield), (c) BCF, (d) MER and (e)
RT based on optimized ML models XGBoost with training and testing datasets. 173 available input and output data were used to develop the predictive model.

5
L. Shi et al. Journal of Hazardous Materials 441 (2023) 129904

Fig. 3. Prediction plots (training and testing) based on feature importance of XGBoost for (a) heavy metal concentration in shoot (HMshoot), (b) shoot yield (Yield),
(c) BCF, (d) MER, and (e) RT. Plant family: Amaranthaceae, Asteraceae, Brassicaceae, Crassulaceae, Fabaceae, Pteridaceae, and Solanaceae; Experimental conditions:
T difference (◦ C), planting time (months), Pot depth (cm), soil mass (kg); Soil properties: soil pH, soil CEC (cmol/kg), and soil OC (g/kg); Metal properties: HM_x,
HM_r (nm), and total heavy metal concentration (µg/g). Note: HM_r (nm): Ion radius of heavy metals; Total HM conc (μg/g): Total heavy metal concentration in soil
before planting; Soil mass (kg): Fresh weight of soil used in each treatment; HM_X: Electronegativity of heavy metals; T difference (℃): Temperature difference; Soil
CEC (cmol/kg): Soil cation exchange capacity; Soil OC (g/kg): Soil organic carbon.

and soil organic carbon. Qu et al (Qu and Feng, 2020). discovered that
buckwheat yield increased owing to improvements in the OC in the soil,
accumulated temperature, temperature and water use efficiency. In
addition, the increase in OC in the soil was associated with an
improvement in soil enzyme activity.
For the BCF (see Fig. 3c), the plant family was the most important
feature type, accounting for 41%, whereas Crassulaceae, soil mass, and
pot depth were the top three vital features. Employment of appropriate
plants is the key to the success of phytoremediation. Crassulaceae has
high BCF and MER may be due to high biomass, high growth rate and
strong ability of absorbing and accumulating heavy metals compare
with other hyperaccumulators (Shen et al., 2022). The soil mass
(0.6–1 kg) was positively associated with the BCF. However, the pot
depth, HM_x, and temperature difference were the three negative fea­
tures associated with BCF (see Fig. 4c). Although we can not find the
relationship between soil mass and BCF in reference, we speculate that
within a certain mass range, as the soil mass increases, the total heavy
metal content in the culture system gradually increases, and the
enrichment capacity of plants is gradually enhanced within the
threshold, and when the threshold of plants can absorb heavy metals is
reached, the BCF will remain unchanged. For pot depth, Tőzsér et al
(Tőzsér et al., 2017). found that increasing element concentrations to­
ward deeper layers, which could explain the relative low BCF in
deep-soil experiments. For HM_x, the low accumulation efficiency of
heavy metals with plants might be related to the high electronegativity
(Fan et al., 2016). In addition, a higher temperature difference may
increase the growth rate of plants, thereby diluting the content of heavy
metals in plants, resulting in a decrease in BCF (Venzhik et al., 2015).
Fig. 3d shows that the plant family type constituted 58% in terms of
importance to the MER, whereas Crassulaceae, pot depth, and Pter­
idaceae were the most notable features for MER. Pot depth was nega­
tively correlated with the MER (Fig. 4d), this might be also due to the
higher heavy metal concentration in the deeper soil layer (Tőzsér et al.,
2017). However, more in-depth research may be needed to explain why
the contribution of ‘Plant family’ feature on BCF and MER significant
higher than ‘Experimental condition’, ‘Soil property’ and ‘Metal prop­
erty’. For RT, the plant family was the most important feature type,
accounting for 51%, followed by the experimental conditions, metal
properties, and soil properties (see Fig. 3e). These important feature
results for the inputs were similar to those of the MER. The pot depth,
temperature difference, total heavy metal concentration, and HM_x were
all positively associated with RT (see Fig. 4e).
3.4. LMWOA and gene identification for in-depth interpretation
Figure S5 and Figure S6 shows the results of accuracy based on five-
fold cross-validation for hyperparameter tuning for the ANN model
based on 80% of the data points from the dataset. The accuracy of
organic acid (a) and genes (b) increased with the number of neurons in
the first hidden layer from 2 to 16. In addition, as the number of neurons
increased in the second hidden layer, the accuracy increased. However,
no further improvement for organic acid identification was observed as

6
L. Shi et al. Journal of Hazardous Materials 441 (2023) 129904

Fig. 4. Correlation of top-four continuous input features with log-based (a) heavy metal concentration in shoot (HMshoot), (b) shoot yield (yield), (c) bioconcentration
factor (BCF), (d) metal extraction factors (MER), and (e) RT. Note: HM_r (nm): Ion radius of heavy metals; Total HM conc (μg/g): Total heavy metal concentration in
soil before planting; Soil mass (kg): Fresh weight of soil used in each treatment; Soil OC (g/kg): Soil organic carbon; T difference (℃): Temperature difference; HM_X:
Electronegativity of heavy metals.

the number of neurons increased continuously in the first hidden layer
from 16 to 128 with the number of neurons in the second hidden layer
over 64. Therefore, the final optimized hyper-parameters of ANN for
organic acid identification were 16 and 46 for the first and second
hidden lawyers, respectively. Similarly, the optimized number of neu­
rons in the first and second layers of ANN determined for gene
identification were 32 and 128. Once determined the optimal hyper­
parameters of ANN, it was retrained by the all the training data for
LMWOAs and gene identification. As shown in Fig. 5, the accuracy and
F1 score of the classification model for test data of LMWOAs exhibited a
lower accuracy than the training data, though not significantly, with a
test accuracy and F1 score of approximately 0.8 and 0.85 for identifying

7
L. Shi et al.
Fig. 5. Test performance including prediction accuracy and F1 score based on
optimal hyperparameters with testing data points for LMWOA and genes
identification. 173 available input and output data were used to develop the
predictive model.
LMWOAs. For the genes, the training and test data matched well, and the
test accuracy and F1 score exceeded 0.9.
The LMWOAs secreted by plants could change the available heavy
metal concentration in soil through chelation; thereby, affecting the
absorption of heavy metals by plants (Meier et al., 2012). This is a
principle we also adopt to engineer for increasing the uptake efficiency.
For example, LMWOAs and some chelators have always been added to
the soil to increase metal uptake by phytoremediation hyper­
accumulators or crops (Duquène et al., 2009; Wang et al., 2022). The
heavy metal transporter genes in the roots, stems, and leaves of hyper­
accumulators can transport metal elements from roots to stems or leaves
to enhance phytoremediation efficiency, or transport metal elements to
vacuoles and cell walls to participate in detoxification (Liu et al., 2017a;
Ye et al., 2020). For plant features, Brassicaceae exhibited the highest
shoot yield compared with other hyperaccumulators, which might be
due to the high secretion of various LMWOAs (Fig. 6a), which could
chelate heavy metals in soil and reduce their toxicity to plants; thereby,
promoting plant growth (Yang et al., 2019). In addition, some gene
expression occurred in Brassicaceae, which was beneficial to plant
growth. For example, the HMA4 gene in Brassica juncea was involved in
Cd2+ binding in the cytosol under low heavy metal concentrations
(Wang et al., 2019b). (Li et al., 2018b). reported that Nramp1;4,
Nramp3;5, Nramp3;10, Nramp4;4, HMA3, and HMA4 were vital for the
Fig. 6. Feature importance analysis with respect to (a) LMWOA and (b) genes of plants based on the explanation of ANN model using SHAP values. Note: Soil mass
(kg): Fresh weight of soil used in each treatment; Soil CEC (cmol/kg): Cation exchange capacity; T difference (℃): Temperature difference; Total HM conc (μg/g):
Total heavy metal concentration in soil before planting; HM_X: Electronegativity of heavy metals; HM_r (nm): Ion radius of heavy metals; Soil OC (g/kg): Soil organic
carbon; Plant family: Amaranthaceae, Asteraceae, Brassicaceae, Crassulaceae, Fabaceae, and Solanaceae.
8
Journal of Hazardous Materials 441 (2023) 129904
uptake and accumulation of Cd in the roots of B. juncea. However,
compared with Brassicaceae and other plants, Crassulaceae played the
most important role in BCF, MER, and RT (see Fig. 3c-e), which might be
due to the high secretion of malate and threonine (see Fig. 6a), and also
the high expression of HMA, MTL, and NRAMP (see Fig. 6b). This
indicated that these three genes had a significant impact on BCF, MER,
and RT. As reported in the literature, the elevated expression of
tonoplast-localized HMA3 in the shoots of S. plumbizincicola was vital to
Cd detoxification, which contributed to the maintenance of the normal
growth of young leaves of S. plumbizincicola in Cd-contaminated soils
(Liu et al., 2017b). Peng et al (Peng et al., 2017). discovered a positive
correlation between transcript levels of MTL in roots and Cd accumu­
lation in leaves of S. plumbizincicola, and that elevated transcript levels
and heterotypic variation in protein sequences of SpMTL might
contribute to Cd hyperaccumulation and hypertolerance in
S. plumbizincicola. In addition, the lower biomass of Crassulaceae
resulted in the longest RT compared with other hyperaccumulators.
Except for the plant features, HM_r, soil mass, and pot depth were the
most important features of the HMshoot, yield, BCF, MER, and RT (see
Fig. 3). However, in addition to the plant features, soil pH, pot depth,
and soil mass were the most important factors contributing to the eight
types of LMWOA secretion. In addition, pot depth was the most
important factor contributing to the expression of the 21 genes. The pot
depth primarily contributed to malate, citrate, and fumarate secretion,
as well as the expression of the HMA gene. The encoded protein of the
HMA (HM ATP synthase) family gene loaded Cd from the symplasm to
the xylem, affecting the migration rate of Cd from the root to the
aboveground segment as well as the accumulation of Cd in the above­
ground segment (Uraguchi and Fujiwara, 2012; Wu et al., 2021). The
HMA1 gene in the root of high-Cd-accumulation pepper X55 under Cd
10 level was 52 times more upregulated compared with that under the
Cd 0 level (Hu et al., 2021). This showed that the expression of HMA1
was regulated by exogenous Cd, and that the expression of HMA in
plants planted in deeper soil might be lower than that of plants growing
in shallower soil, owing to the lower heavy metal concentrations in
deeper soil layers. However, the direct relationship between plant
organic acid secretion and pot depth has not been reported; hence,
further confirmation is required. For example, experiments and genetic
analysis could be conducted to detailly investigate the mechanism
behind pot depth affecting gene expressions.
Here, the XGBoost and ANN models were applied to model the
complicated process of hyperaccumulator remediation for heavy metal-
L. Shi et al.
containing soils. The developed ML models predicted the heavy metal
concentration in shoots, yield, BCFs, MER, and RT of different heavy
metals, as well as identified the acid generation and gene expression for
a deep interpretation of soil–hyperaccumulator ecosystems. It was used
to quantify the importance of variables and identify potential control
factors affecting phytoremediation efficiency in soil-hyperaccumulator
systems, as well as to provide the suitable hyperaccumulators for spe­
cific heavy metal-contained soil to accelerate the remediation process.
However, some limitations of this study could be improved in the future.
First of all, extreme gradient boosting (XGBoost) should be compared
with other ML algorithms to evaluate their suitability for phytor­
emediation models. Secondly, there is a need to increase the amount of
data to improve the model’s accuracy. For example, factors that might
affect the phytoremediation efficiency were not comprehensively
considered because of the lack of data, such as geographical location of
soil, climate factors, soil texture, etc. Moreover, the model-guided
phytoremediation experimental work could be another direction for
the continuation of the present work based on the suitable plant, and
also experimental and soil conditions.
4. Conclusions
In summary, the ‘plant family’ was the most important feature for
phytoremediation, followed by experimental conditions, soil properties,
and heavy metal properties. In addition, the plant family dominated the
BCF, MER, and RT. The Crassulaceae family had the highest potential of
hyperaccumulators for phytoremediation, which was related to the
expression of HMA, MTL, and NRAMP genes. The metal ion radius was
the most important factor affecting heavy metal concentration in shoots.
In addition to the comprehensive interpretation of phytoremediation,
the developed ML model can adapt to other phytoremediation systems
to evaluate the soil remediation performance by predicting final heavy
metal distributions in plants and the plant growth. Moreover, the ML
model can be utilized to design new phytoremediation experiments and
guide the field phytoremediation for a specific and heavy metal-
contaminated soil.
CRediT authorship contribution statement
L.S. and J.L. contributed equally to this work. L.S.: data collection,
writing (review and editing) and visualization; J.L.: modeling, writing
(review and editing), and visualization; K.N.P.: review and editing; X.N.
W.: conceptualization, writing (review and editing), and supervision;
and Y.S.O.: conceptualization, writing (review and editing), and
supervision.
Statement of environmental implication
Machine learning can guide the phytoremediation of heavy metal-
contaminated soils to improve remediation efficiency.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Data availability
Data will be made available on request.
Acknowledgements
This work was carried out with the support of the Cooperative
Research Program for Agriculture Science and Technology Development
(Project No. PJ01475801) from Rural Development Administration, the
9
Journal of Hazardous Materials 441 (2023) 129904
Republic of Korea. This work was also supported by the International
Postdoctoral Exchange Program Fellowship (PC2020041). This work
was also supported by the National Research Foundation of Korea (NRF)
grant funded by the Korea government (MSIT) (No.
2021R1A2C2011734). This research was supported by Basic Science
Research Program through the National Research Foundation of Korea
(NRF) funded by the Ministry of Education (NRF-
2021R1A6A1A10045235).
Appendix A. Supporting information
Supplementary data associated with this article can be found in the
online version at doi:10.1016/j.jhazmat.2022.129904.
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