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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Environ. Sci.</journal-id>
<journal-title>Frontiers in Environmental Science</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Environ. Sci.</abbrev-journal-title>
<issn pub-type="epub">2296-665X</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="publisher-id">1253144</article-id>
<article-id pub-id-type="doi">10.3389/fenvs.2023.1253144</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Environmental Science</subject>
<subj-group>
<subject>Review</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Biochar; an effective factor in improving phytoremediation of metal(iod)s in polluted sites</article-title>
<alt-title alt-title-type="left-running-head">Boorboori and Lack&#xf3;ov&#xe1;</alt-title>
<alt-title alt-title-type="right-running-head">
<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fenvs.2023.1253144">10.3389/fenvs.2023.1253144</ext-link>
</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Boorboori</surname>
<given-names>Mohammad Reza</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="corresp" rid="c001">&#x2a;</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1978191/overview"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Lack&#xf3;ov&#xe1;</surname>
<given-names>Lenka</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="corresp" rid="c001">&#x2a;</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2543581/overview"/>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>College of Environment and Surveying and Mapping Engineering</institution>, <institution>Suzhou University</institution>, <addr-line>Suzhou</addr-line>, <addr-line>Anhui</addr-line>, <country>China</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Faculty of Horticulture and Landscape Engineering</institution>, <institution>Institute of Landscape Engineering</institution>, <institution>Slovak University of Agriculture in Nitra</institution>, <addr-line>Nitra</addr-line>, <country>Slovakia</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>
<bold>Edited by:</bold> <ext-link ext-link-type="uri" xlink:href="https://loop.frontiersin.org/people/1599128/overview">Paula P&#xe9;rez-Rodr&#xed;guez</ext-link>, University of Vigo, Spain</p>
</fn>
<fn fn-type="edited-by">
<p>
<bold>Reviewed by:</bold> <ext-link ext-link-type="uri" xlink:href="https://loop.frontiersin.org/people/454996/overview">Milan Skalicky</ext-link>, Czech University of Life Sciences Prague, Czechia</p>
<p>
<ext-link ext-link-type="uri" xlink:href="https://loop.frontiersin.org/people/2427529/overview">Luis Lopez</ext-link>, Universidad Mayor de San Andres, Bolivia</p>
</fn>
<corresp id="c001">&#x2a;Correspondence: Mohammad Reza Boorboori, <email>boorboori@ahszu.edu.cn</email>; Lenka Lack&#xf3;ov&#xe1;, <email>lenka.lackoova@uniag.sk</email>
</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>19</day>
<month>10</month>
<year>2023</year>
</pub-date>
<pub-date pub-type="collection">
<year>2023</year>
</pub-date>
<volume>11</volume>
<elocation-id>1253144</elocation-id>
<history>
<date date-type="received">
<day>05</day>
<month>07</month>
<year>2023</year>
</date>
<date date-type="accepted">
<day>11</day>
<month>10</month>
<year>2023</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2023 Boorboori and Lack&#xf3;ov&#xe1;.</copyright-statement>
<copyright-year>2023</copyright-year>
<copyright-holder>Boorboori and Lack&#xf3;ov&#xe1;</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p>
</license>
</permissions>
<abstract>
<p>Phytoremediation is one of the cheapest and most widely used technologies for stabilizing and extracting pollutants from contaminated sites. Recently, a variety of solutions, such as the use of different elements, compost, nanoparticles, microorganisms, etc., have been explored for improving and accelerating the phytoremediation process. Biochar has also gained attention for its affordability, abundance, ability to improve soil structure and plant morpho-physiology and biochemistry, lack of environmental hazards, etc. As a first step, this study aimed to provide an overview of biochar&#x2019;s properties, and operation by identifying the method of production and examining the differences between different types of biochar. Following that, by examining various factors that pollute the environment, the influence of different types of biochar on phytoremediation efficiency was explored. Also, in this study, an attempt has been made to examine the effect of the combination of biochar with other factors in improving the phytoremediation of pollutants, as well as the use of the residues of phytoremediation for the production of biochar, so that future research can be planned based on the results obtained.</p>
</abstract>
<kwd-group>
<kwd>pollutants</kwd>
<kwd>biochar</kwd>
<kwd>phytoremediation</kwd>
<kwd>environment</kwd>
<kwd>stabilization</kwd>
<kwd>extraction</kwd>
</kwd-group>
<custom-meta-wrap>
<custom-meta>
<meta-name>section-at-acceptance</meta-name>
<meta-value>Soil Processes</meta-value>
</custom-meta>
</custom-meta-wrap>
</article-meta>
</front>
<body>
<sec id="s1">
<title>1 Introduction</title>
<p>Biochar is a stable carbon-rich product that is made by decomposing animal or plant residues under anaerobic (or low oxygen) and heat conditions (<xref ref-type="bibr" rid="B114">Lehmann and Joseph, 2015</xref>; <xref ref-type="bibr" rid="B149">Nguyen et al., 2017</xref>; <xref ref-type="bibr" rid="B181">Tomczyk et al., 2020</xref>). This porous material, which contains more than 60% carbon, along with oil and gas, is one of the products of biomass decomposition by heat (<xref ref-type="bibr" rid="B109">Lebrun et al., 2021a</xref>), and based on research, thousands-year-old biochar particles have been found in the soil of Amazon&#x2019;s tropical and humid regions (<xref ref-type="bibr" rid="B148">Narayanan and Ma, 2022</xref>). Since it has a special properties, this cheap material has a very high application and efficiency in improving different soil ecosystems (<xref ref-type="bibr" rid="B69">Ghosh and Maiti, 2021</xref>). In general, Biochar is obtained from the decomposition of various biomass such as urban waste, industrial waste, agricultural waste (sugarcane, sugar beet, corn, weeds, etc.), poultry litter, animal manure, forestry waste (waste of trees, wood, bamboo, etc.) and sludge (<xref ref-type="bibr" rid="B100">Khiari et al., 2019</xref>; <xref ref-type="bibr" rid="B102">Kiran and Prasad, 2019</xref>; <xref ref-type="bibr" rid="B145">Marou&#x161;ek et al., 2019</xref>; <xref ref-type="bibr" rid="B8">Albalasmeh et al., 2020</xref>; <xref ref-type="bibr" rid="B176">Simiele et al., 2020</xref>) (<xref ref-type="fig" rid="F1">Figure 1</xref>).</p>
<fig id="F1" position="float">
<label>FIGURE 1</label>
<caption>
<p>Possible ways to prepare biochar.</p>
</caption>
<graphic xlink:href="fenvs-11-1253144-g001.tif"/>
</fig>
<p>To prepare Biochar, biomass is heated to between 400&#xb0;C and 700&#xb0;C under limited oxygen conditions (decomposition by pyrolysis method) (<xref ref-type="bibr" rid="B199">Yavari et al., 2015</xref>; <xref ref-type="bibr" rid="B176">Simiele et al., 2020</xref>), and biochar&#x2019;s physicochemical properties are directly related to its raw material and pyrolysis conditions (<xref ref-type="bibr" rid="B19">Benavente et al., 2018</xref>; <xref ref-type="bibr" rid="B8">Albalasmeh et al., 2020</xref>) (<xref ref-type="table" rid="T1">Table 1</xref>), and to the extent that biochar derived from animal manure has more nutrients than biochar derived from plants (<xref ref-type="bibr" rid="B148">Narayanan and Ma, 2022</xref>). Researchers also found that changing the temperature of pyrolysis from 400&#xb0;C to 500&#xb0;C increases the content (mg/kg) of magnesium (Mg), potassium (K), phosphate (P), Carbon (C), nitrogen (N), oxygen (O), hydrogen (H), and calcium (Ca) in the biochar produced, and this increase in temperature also increases the mineralization of raw materials (<xref ref-type="bibr" rid="B141">Ma et al., 2015</xref>; <xref ref-type="bibr" rid="B30">Brassard et al., 2017</xref>; <xref ref-type="bibr" rid="B62">Ferjani et al., 2019</xref>). Additionally, the cost of raw materials, labor costs, and production technologies affect the cost of biochar production, and the average cost varies from one hundred to five thousand US dollars per ton in different countries (<xref ref-type="bibr" rid="B145">Marou&#x161;ek et al., 2019</xref>) (<xref ref-type="fig" rid="F2">Figure 2</xref>).</p>
<table-wrap id="T1" position="float">
<label>TABLE 1</label>
<caption>
<p>Characteristics of biochars produced from different raw materials.</p>
</caption>
<table>
<thead valign="top">
<tr>
<th align="center">Biochar type</th>
<th align="center">N (%)</th>
<th align="center">C (%)</th>
<th align="center">H (%)</th>
<th align="center">O (%)</th>
<th align="center">pH</th>
<th align="center">Ash content (%)</th>
<th align="center">EC (dS/m)</th>
<th align="center">Moisture content (%)</th>
</tr>
</thead>
<tbody valign="top">
<tr>
<td align="center">Bamboo</td>
<td align="center">0.57</td>
<td align="center">76.69</td>
<td align="center">1.59</td>
<td align="center">21.15</td>
<td align="center">10.80</td>
<td align="center">5.51</td>
<td align="center">1.54</td>
<td align="center">-</td>
</tr>
<tr>
<td align="center">Wood apple fruit shell</td>
<td align="center">0.12</td>
<td align="center">81.18</td>
<td align="center">2.12</td>
<td align="center">16.58</td>
<td align="center">-</td>
<td align="center">3.41</td>
<td align="center">-</td>
<td align="center">4.17</td>
</tr>
<tr>
<td align="center">Maize residue</td>
<td align="center">0.93</td>
<td align="center">42.94</td>
<td align="center">-</td>
<td align="center">-</td>
<td align="center">8.54</td>
<td align="center">36.7</td>
<td align="center">3.34</td>
<td align="center">-</td>
</tr>
<tr>
<td align="center">Rice husk</td>
<td align="center">0.51</td>
<td align="center">47.13</td>
<td align="center">-</td>
<td align="center">-</td>
<td align="center">8.75</td>
<td align="center">31</td>
<td align="center">-</td>
<td align="center">-</td>
</tr>
<tr>
<td align="center">Loblolly pine chips</td>
<td align="center">0.65</td>
<td align="center">72.6</td>
<td align="center">0.77</td>
<td align="center">21.3</td>
<td align="center">-</td>
<td align="center">4.7</td>
<td align="center">-</td>
<td align="center">-</td>
</tr>
<tr>
<td align="center">Sewage sludge</td>
<td align="center">4.9</td>
<td align="center">33.1</td>
<td align="center">4.1</td>
<td align="center">-</td>
<td align="center">6.7</td>
<td align="center">46.9</td>
<td align="center">0.91</td>
<td align="center">-</td>
</tr>
<tr>
<td align="center">Red spruce pellets</td>
<td align="center">0.21</td>
<td align="center">84.0</td>
<td align="center">1.5</td>
<td align="center">-</td>
<td align="center">9.1</td>
<td align="center">4.7</td>
<td align="center">0.39</td>
<td align="center">2.6</td>
</tr>
<tr>
<td align="center">Grapevine pruning residues</td>
<td align="center">0.53</td>
<td align="center">75.5</td>
<td align="center">1.3</td>
<td align="center">-</td>
<td align="center">9.9</td>
<td align="center">9.9</td>
<td align="center">2.23</td>
<td align="center">4.5</td>
</tr>
<tr>
<td align="center">Hydrochar from urban pruning residues</td>
<td align="center">1.7</td>
<td align="center">61.5</td>
<td align="center">6.2</td>
<td align="center">-</td>
<td align="center">6.6</td>
<td align="center">12.5</td>
<td align="center">1.02</td>
<td align="center">7.0</td>
</tr>
<tr>
<td align="center">Paper mill waste</td>
<td align="center">0.07</td>
<td align="center">19.2</td>
<td align="center">0.50</td>
<td align="center">9.40</td>
<td align="center">9.48</td>
<td align="center">57.5</td>
<td align="center">0.30</td>
<td align="center">-</td>
</tr>
<tr>
<td align="center">Bio-oil</td>
<td align="center">5.6</td>
<td align="center">27.7</td>
<td align="center">1.2</td>
<td align="center">5.9</td>
<td align="center">-</td>
<td align="center">60.3</td>
<td align="center">-</td>
<td align="center">-</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
<p>The results are taken from the following references <xref ref-type="bibr" rid="B187">Wei et al. (2015)</xref>, <xref ref-type="bibr" rid="B101">Kim et al. (2016)</xref>, <xref ref-type="bibr" rid="B107">Kupryianchyk et al. (2016)</xref>, <xref ref-type="bibr" rid="B206">Zhang et al. (2016)</xref>, <xref ref-type="bibr" rid="B116">Li et al. (2019a)</xref>, <xref ref-type="bibr" rid="B169">Regkouzas and Diamadopoulos (2019)</xref>, <xref ref-type="bibr" rid="B180">Taskin et al. (2019)</xref>, <xref ref-type="bibr" rid="B105">Kumar et al. (2021)</xref>, and <xref ref-type="bibr" rid="B129">Liu et al. (2021)</xref>.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<fig id="F2" position="float">
<label>FIGURE 2</label>
<caption>
<p>An analysis of the soil components affected by biochar. The results are taken from <xref ref-type="bibr" rid="B42">Chukwuka et al. (2020)</xref>.</p>
</caption>
<graphic xlink:href="fenvs-11-1253144-g002.tif"/>
</fig>
<p>Biochar can be widely used in agriculture and the environment due to its unique characteristics, which include its ability to improve soil fertility and adsorption of various pollutants (<xref ref-type="bibr" rid="B192">Xie et al., 2015</xref>; <xref ref-type="bibr" rid="B201">Zanganeh et al., 2022</xref>). The special characteristics of biochar include high porosity, high cation exchange capacity (CEC), alkaline pH, low density, abundant functional groups (aromatic and heterocyclic carbons such as C&#x3d;N, COOH, OH), high water holding capacity, high specific surface area and adsorption capacity (<xref ref-type="bibr" rid="B47">Czeka&#x142;a et al., 2016</xref>; <xref ref-type="bibr" rid="B52">Du et al., 2019a</xref>; <xref ref-type="bibr" rid="B176">Simiele et al., 2020</xref>; <xref ref-type="bibr" rid="B182">Tu et al., 2020</xref>; <xref ref-type="bibr" rid="B118">Li et al., 2021a</xref>; <xref ref-type="bibr" rid="B77">Gonzaga et al., 2022</xref>). According to Ahmad et al., biochar is an alkaline material with pH 8-11, a specific surface area of 10&#x2013;1,400&#xa0;m<sup>2</sup>&#xb7;g<sup>&#x2212;1</sup>, a porosity of 0&#x2013;1.32&#xa0;cm<sup>3</sup>&#xb7;g<sup>&#x2212;1</sup>, and CEC of 25&#x2013;485&#xa0;cmol (&#xfe;) kg<sup>&#x2212;1</sup> (<xref ref-type="bibr" rid="B6">Ahmad et al., 2014</xref>). Furthermore, while biochar has a very low mineralization rate, its particle size affects its interactions with soil, changing its porosity and ions adsorption and exchange capacity (<xref ref-type="bibr" rid="B188">Williams et al., 2019</xref>; <xref ref-type="bibr" rid="B118">Li et al., 2021a</xref>).</p>
<p>Biochar is a low-cost and environmentally friendly amendment that can cause long-term positive effects in soil ecosystems by improving biogeochemical processes and physicochemical properties (<xref ref-type="bibr" rid="B79">Gul et al., 2015</xref>; <xref ref-type="bibr" rid="B204">Zhang et al., 2018</xref>). Biochar&#x2019;s higher content of polycyclic aromatic hydrocarbons (PAHs) than other organic carbons makes it more compatible with soils and contributes to climate change mitigation through improving soil ventilation, carbon sequestration, and reduction of greenhouse gases such as Nitrous oxide (N<sub>2</sub>O) (<xref ref-type="bibr" rid="B170">Rizwan et al., 2016</xref>; <xref ref-type="bibr" rid="B103">Kolton et al., 2017</xref>; <xref ref-type="bibr" rid="B122">Lian and Xing, 2017</xref>; <xref ref-type="bibr" rid="B102">Kiran and Prasad, 2019</xref>). Biochar increases soil fertility by improving water and nutrient availability and increasing the content of organic matter (<xref ref-type="bibr" rid="B112">Lebrun et al., 2018</xref>; <xref ref-type="bibr" rid="B109">Lebrun et al., 2021a</xref>; <xref ref-type="bibr" rid="B10">Ali et al., 2021</xref>), and by softening soil, it improves water retention capacity, reduces nutrient leaching, and improves nutrient cycling in soil (<xref ref-type="bibr" rid="B204">Zhang et al., 2018</xref>; <xref ref-type="bibr" rid="B118">Li et al., 2021a</xref>; <xref ref-type="bibr" rid="B68">Gholizadeh and Hu, 2021</xref>). Additionally, biochar in soil regulates pH, CEC, EC, and ash content as well as increasing catalase, urease, and dehydrogenase activity, and increasing microbial activities, especially indigenous microbes (<xref ref-type="bibr" rid="B87">Hossain et al., 2010</xref>; <xref ref-type="bibr" rid="B24">Binti Ab Aziz et al., 2015</xref>; <xref ref-type="bibr" rid="B39">Chen et al., 2017</xref>; <xref ref-type="bibr" rid="B202">Zhang et al., 2019b</xref>; <xref ref-type="bibr" rid="B76">Gong et al., 2021</xref>) (<xref ref-type="fig" rid="F2">Figure 2</xref>).</p>
<p>Furthermore, biochar increases plant growth, biomass, and yield by improving soil conditions, improving water quality, providing nutrients, increasing root colonization by microbes, and improving the propagation and surface of roots (<xref ref-type="bibr" rid="B157">Paz-Ferreiro et al., 2014</xref>; <xref ref-type="bibr" rid="B50">Doan et al., 2015</xref>; <xref ref-type="bibr" rid="B168">Rees et al., 2016</xref>; <xref ref-type="bibr" rid="B86">Herman and Resigia, 2018</xref>; <xref ref-type="bibr" rid="B203">Zhang et al., 2019a</xref>; <xref ref-type="bibr" rid="B212">Zhou et al., 2020</xref>). Nonetheless, dissolved organic matter in biochar (aqueous biochar extract) contains a considerable amount of organic compounds, including organic acids with low molecular weight, humic organic molecules, and complex sugars, which have significant effects on plant growth (<xref ref-type="bibr" rid="B134">Lou et al., 2016</xref>; <xref ref-type="bibr" rid="B23">Bian et al., 2018</xref>). Enriching biochar with elements such as silicon, iron, selenium, calcium, etc., in addition to increasing biochar availability in soil, can improve the positive properties of biochar (<xref ref-type="bibr" rid="B160">Rajkovich et al., 2012</xref>; <xref ref-type="bibr" rid="B176">Simiele et al., 2020</xref>), further, other methods for modifying biochar have been considered, including ultraviolet (UV) radiation, which increases the specific surface area of biochar and can introduce oxygen-containing functional groups (<xref ref-type="bibr" rid="B158">Peng et al., 2019</xref>). Several studies have been conducted in recent years on the pyrolysis of lignocellulosic wastes to produce biochar, and if this technology becomes common, it can be seen as a promising method for reducing greenhouse gas emissions and other environmental pollution in addition to producing added value (<xref ref-type="bibr" rid="B131">Liu et al., 2015b</xref>; <xref ref-type="bibr" rid="B52">Du et al., 2019a</xref>; <xref ref-type="bibr" rid="B53">Du et al., 2019b</xref>). In this study, various pollutants in the soil ecosystem were investigated, as well as how phytoremediation reduces these pollutants, and how biochar affect in the process of phytoremediation.</p>
</sec>
<sec id="s2">
<title>2 Soil pollution problem</title>
<p>In general, HMs consist of elements with a high atomic mass and weight, and a specific density exceeding 5&#xa0;g/cm<sup>3</sup>, and are classified into two groups, essentials, and non-essentials (<xref ref-type="bibr" rid="B31">Buha et al., 2014</xref>; <xref ref-type="bibr" rid="B59">Farooq et al., 2016</xref>). Essential elements (micronutrients) are necessary in very small amounts for plants and animals, such as copper (Cu), iron (Fe), manganese (Mn), cobalt (Co), zinc (Zn), and chromium (Cr), which in high concentrations can cause soil pollution and harm to organisms (<xref ref-type="bibr" rid="B147">Naja and Volesky, 2017</xref>; <xref ref-type="bibr" rid="B13">Awad et al., 2021</xref>; <xref ref-type="bibr" rid="B161">Rathika et al., 2021</xref>); However, non-essential elements [including cadmium (Cd), mercury, (Hg) arsenic (As), and lead (Pb)] are very dangerous and can lead to severe soil contamination (<xref ref-type="bibr" rid="B91">Huang et al., 2012</xref>; <xref ref-type="bibr" rid="B161">Rathika et al., 2021</xref>; <xref ref-type="bibr" rid="B82">Haider et al., 2022</xref>; <xref ref-type="bibr" rid="B26">Boorboori, 2023</xref>). In contrast to organic pollutants, HMs are resistant to degradation and remain in soil and sediment for a long time, for instance, it has been reported that HMs contamination can persist in soil for more than 5,000&#xa0;years (<xref ref-type="bibr" rid="B135">Lu et al., 2015</xref>; <xref ref-type="bibr" rid="B75">Gong et al., 2018b</xref>; <xref ref-type="bibr" rid="B119">Li et al., 2021b</xref>), as a result, long-term persistence in polluted sites facilitates their entry into the food cycle and ultimately causes severe environmental damage (<xref ref-type="bibr" rid="B195">Xu et al., 2018b</xref>; <xref ref-type="bibr" rid="B209">Zhao et al., 2019</xref>; <xref ref-type="bibr" rid="B201">Zanganeh et al., 2022</xref>) (<xref ref-type="table" rid="T2">Table 2</xref>).</p>
<table-wrap id="T2" position="float">
<label>TABLE 2</label>
<caption>
<p>Amount of heavy metals intake through food consumption (&#x3bc;g/day).</p>
</caption>
<table>
<thead valign="top">
<tr>
<th align="center">Heavy metals</th>
<th align="center">Fish</th>
<th align="center">Meat</th>
<th align="center">Fruit</th>
<th align="center">Vegetable</th>
<th align="center">Cereals</th>
<th align="center">Total intake</th>
</tr>
</thead>
<tbody valign="top">
<tr>
<td align="center">Cd</td>
<td align="center">0.58</td>
<td align="center">1.54</td>
<td align="center">0.41</td>
<td align="center">19.63</td>
<td align="center">7.32</td>
<td align="center">29.48</td>
</tr>
<tr>
<td align="center">As</td>
<td align="center">7.84</td>
<td align="center">5.54</td>
<td align="center">2.35</td>
<td align="center">8.23</td>
<td align="center">10.07</td>
<td align="center">34.02</td>
</tr>
<tr>
<td align="center">Pb</td>
<td align="center">9.91</td>
<td align="center">17.54</td>
<td align="center">3.86</td>
<td align="center">41.24</td>
<td align="center">22.60</td>
<td align="center">95.15</td>
</tr>
<tr>
<td align="center">Hg</td>
<td align="center">4.68</td>
<td align="center">1.86</td>
<td align="center">0.58</td>
<td align="center">1.23</td>
<td align="center">7.27</td>
<td align="center">15.63</td>
</tr>
<tr>
<td align="center">Cr</td>
<td align="center">38.50</td>
<td align="center">60.14</td>
<td align="center">5.36</td>
<td align="center">54.85</td>
<td align="center">46.67</td>
<td align="center">205.52</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
<p>The results are taken from <xref ref-type="bibr" rid="B123">Liang et al. (2019)</xref>.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</sec>
<sec id="s3">
<title>3 Phytoremediation of metal(iod)s</title>
<p>Considering the growing trend of combined pollution in soil, it seems necessary to find strategies for cleaning contaminated soil (<xref ref-type="bibr" rid="B210">Zhen et al., 2019</xref>; <xref ref-type="bibr" rid="B207">Zhang et al., 2021</xref>; <xref ref-type="bibr" rid="B63">Fern&#xe1;ndez-Bra&#xf1;a et al., 2023</xref>). There have been several physical and chemical methods also are available for the remediation of soils contaminated with HMs, including encapsulation, soil washing, freezing, electrokinetic remediation, membrane filtration, reverse osmosis (RO), 3 electrodialytic remediation (EDR), landfilling, nanomaterials, immobilization, and surface capping (<xref ref-type="bibr" rid="B16">Barati et al., 2018</xref>; <xref ref-type="bibr" rid="B128">Liu et al., 2018</xref>; <xref ref-type="bibr" rid="B102">Kiran and Prasad, 2019</xref>; <xref ref-type="bibr" rid="B174">Shah and Daverey, 2020</xref>). However, all the aforementioned techniques have several limitations, including high economic costs, creating secondary pollution for the environment, inapplicability in wide areas, high energy consumption, and extensive chemical needs (<xref ref-type="bibr" rid="B156">Paz-Alberto and Sigua, 2013</xref>; <xref ref-type="bibr" rid="B70">Gkorezis et al., 2016</xref>; <xref ref-type="bibr" rid="B126">Lin et al., 2019</xref>; <xref ref-type="bibr" rid="B200">Yrj&#xe4;l&#xe4; and Lopez-Echartea, 2021</xref>), therefore, finding cheaper and more effective methods can be a remedial to reduce pollution in soils contaminated with HMs.</p>
<p>During the past few decades, plants have been used to decompose, convert, stabilize, or remove pollutants in sediments, underground and surface water, soil, and the atmosphere (<xref ref-type="bibr" rid="B164">Reddy and Chirakkara, 2013</xref>; <xref ref-type="bibr" rid="B163">Ratnasari et al., 2020</xref>), and this green biological technique based on hyperaccumulators or non-hyperaccumulators plant species and their associated microorganisms is called phytoremediation (<xref ref-type="bibr" rid="B140">Ma et al., 2016</xref>; <xref ref-type="bibr" rid="B93">Jha et al., 2017</xref>; <xref ref-type="bibr" rid="B161">Rathika et al., 2021</xref>; <xref ref-type="bibr" rid="B27">Boorboori and Zhang, 2022a</xref>). The low cost of phytoremediation (about 25&#x2013;100 US dollars per ton of soil) makes it a cost-effective technology that, in addition to being environmentally friendly, is highly effective and simple to use (<xref ref-type="bibr" rid="B185">Wang et al., 2017a</xref>; <xref ref-type="bibr" rid="B66">Gao et al., 2018</xref>; <xref ref-type="bibr" rid="B133">Logeshwaran et al., 2018</xref>). As a result of its general acceptance, no disruption to soil fertility and biodiversity, prevention of soil erosion, carbon sequestration, extensive application, and use in sites with multiple types of pollutants, this method has become increasingly subject for potted and field studies (<xref ref-type="bibr" rid="B112">Lebrun et al., 2018</xref>; <xref ref-type="bibr" rid="B35">C&#xe1;rdenas-Aguiar et al., 2020</xref>; <xref ref-type="bibr" rid="B201">Zanganeh et al., 2022</xref>).</p>
<p>Phytoremediation which can be used alone or in conjunction with other soil remediation methods improves soils contaminated with organic and inorganic compounds by various routes such as extraction, evaporation, transpiration, stabilization, Rhizofiltration, and transformation (<xref ref-type="bibr" rid="B65">Forj&#xe1;n et al., 2018</xref>; <xref ref-type="bibr" rid="B56">Fancello et al., 2019</xref>; <xref ref-type="bibr" rid="B174">Shah and Daverey, 2020</xref>) (<xref ref-type="table" rid="T3">Table 3</xref>). Plant extraction and plant stabilization are the most important phytoremediation processes (<xref ref-type="bibr" rid="B143">Mahar et al., 2016</xref>), in the plant extraction method, environmental pollution is absorbed into the roots and transferred to the plant&#x2019;s aerial organs, which are then harvested and removed (<xref ref-type="bibr" rid="B109">Lebrun et al., 2021a</xref>). Although plant extraction offers many advantages, including safety and high efficiency, it faces a problem in disposing of contaminated biomass, which incurs additional costs (<xref ref-type="bibr" rid="B25">Boominathan et al., 2004</xref>; <xref ref-type="bibr" rid="B109">Lebrun et al., 2021a</xref>).</p>
<table-wrap id="T3" position="float">
<label>TABLE 3</label>
<caption>
<p>The name of hyperaccumulator plants for remediating soils contaminated with heavy metals.</p>
</caption>
<table>
<thead valign="top">
<tr>
<th align="center">Heavy metals</th>
<th align="center">Kinds of plant</th>
<th align="center">Uptake of heavy metals (mg/kg)</th>
</tr>
</thead>
<tbody valign="top">
<tr>
<td rowspan="7" align="center">Cd</td>
<td align="center">
<italic>Pteris vittata</italic> L.</td>
<td align="center">20.67</td>
</tr>
<tr>
<td align="left">
<italic>Thlaspi caerulescens</italic> J.Presl and C.Presl synonym of <italic>Noccaea caerulescens</italic> (J.Presl and C.Presl) F.K.Mey.</td>
<td align="center">263</td>
</tr>
<tr>
<td align="center">
<italic>Rorippa globosa</italic> (Turcz. ex Fisch. and C.A.Mey.)</td>
<td align="center">&#x3e;100</td>
</tr>
<tr>
<td align="center">
<italic>Deschampsia cespitosa</italic> L. P.Beauv.</td>
<td align="center">236.2</td>
</tr>
<tr>
<td align="center">
<italic>Prosopis laevigata</italic>
</td>
<td align="center">8,176</td>
</tr>
<tr>
<td align="center">
<italic>Phytolacca americana</italic> L.</td>
<td align="center">10,700</td>
</tr>
<tr>
<td align="center">
<italic>D. cespitosa</italic> L. P. Beauv.</td>
<td align="center">966.5&#x2013;3,614</td>
</tr>
<tr>
<td rowspan="5" align="center">As</td>
<td align="center">
<italic>Corrigiola telephiifolia</italic> Pourr.</td>
<td align="center">2,110</td>
</tr>
<tr>
<td align="center">
<italic>Pteris biaurita</italic> L.</td>
<td align="center">2,000</td>
</tr>
<tr>
<td align="center">
<italic>Pteris ryukyuensis</italic> Tagawa</td>
<td align="center">3,647</td>
</tr>
<tr>
<td align="center">
<italic>Pteris quadriaurita</italic> Retz.</td>
<td align="center">2,900</td>
</tr>
<tr>
<td align="center">
<italic>P. vittata</italic> L.</td>
<td align="center">8,331</td>
</tr>
<tr>
<td rowspan="11" align="center">Hg</td>
<td align="center">
<italic>P. vittata</italic> L.</td>
<td align="center">91.975</td>
</tr>
<tr>
<td align="center">
<italic>Haumaniastrum katangense</italic>
</td>
<td align="center">8,356</td>
</tr>
<tr>
<td align="center">
<italic>Aeollanthus biformifolius</italic>
</td>
<td align="center">13,700</td>
</tr>
<tr>
<td align="center">
<italic>Eleocharis acicularis</italic>
</td>
<td align="center">20,200</td>
</tr>
<tr>
<td align="center">
<italic>Cicer arietinum</italic> L.</td>
<td align="center">0.2</td>
</tr>
<tr>
<td align="center">
<italic>Poa pratensis</italic> L.</td>
<td align="center">2.74</td>
</tr>
<tr>
<td align="center">
<italic>Festuca rubra</italic> L.</td>
<td align="center">3.17</td>
</tr>
<tr>
<td align="center">
<italic>Silene vulgaris</italic>
</td>
<td align="center">4.25</td>
</tr>
<tr>
<td align="center">
<italic>Rumex induratus s</italic> Boiss. and Reut.</td>
<td align="center">6.45</td>
</tr>
<tr>
<td align="center">
<italic>Marrubium vulgare</italic> L. (Moench) Garcke</td>
<td align="center">13.8</td>
</tr>
<tr>
<td align="center">
<italic>Achillea millefolium</italic> L.</td>
<td align="center">18.275</td>
</tr>
<tr>
<td rowspan="3" align="center">Pb</td>
<td align="center">
<italic>Euphorbia cheiradenia</italic> Boiss. and Hohen</td>
<td align="center">1,138</td>
</tr>
<tr>
<td align="center">
<italic>D. cespitosa</italic> P.Beauv.</td>
<td align="center">966.5</td>
</tr>
<tr>
<td align="center">
<italic>Medicago sativa</italic> L.</td>
<td align="center">43,300</td>
</tr>
<tr>
<td rowspan="4" align="center">Ni</td>
<td align="center">
<italic>Isatis pinnatiloba</italic> P.H.Davis</td>
<td align="center">1,441</td>
</tr>
<tr>
<td align="center">
<italic>Alyssum serpyllifolium</italic> Desf.</td>
<td align="center">10,000</td>
</tr>
<tr>
<td align="center">
<italic>Alyssum heldreichii Hausskn</italic>
</td>
<td align="center">11,800</td>
</tr>
<tr>
<td align="left">
<italic>Alyssum bertolonii</italic> Desv. synonym of Odontarrhena bertolonii (Desv.) Jord. and Fourr.</td>
<td align="center">10,900</td>
</tr>
<tr>
<td align="center">Cr</td>
<td align="center">
<italic>P. vittata</italic> L.</td>
<td align="center">20,675</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
<p>The results are taken from <xref ref-type="bibr" rid="B95">Kanwar et al. (2020)</xref>.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<p>As the process of extracting plants from highly polluted lands takes tens of years, and because falling leaves and branches also are responsible for returning pollution to the ground, plant stabilization may be a suitable alternative in the contaminated environment (<xref ref-type="bibr" rid="B138">Lucchini et al., 2014</xref>; <xref ref-type="bibr" rid="B108">Laghlimi et al., 2015</xref>). In this method, which aims to reduce the mobility and bioavailability of pollutants, resistant plants with extensive root systems can be used along with soil amendment compounds, provided that the plants used do not transfer the pollutants from the roots to the aerial organs, but stabilize it on the surface and inside the roots through the complexation with root secretions (<xref ref-type="bibr" rid="B106">Kumpiene et al., 2008</xref>; <xref ref-type="bibr" rid="B2">Acosta et al., 2018</xref>; <xref ref-type="bibr" rid="B109">Lebrun et al., 2021a</xref>). Since HMs do not decompose, plant stabilization is more effective for them and prevents them from transferring to the surrounding environments, and the efficiency of this method depends on several factors, including the hydrological regime, pollution type, soil geochemistry, etc., (<xref ref-type="bibr" rid="B37">Chehregani et al., 2009</xref>; <xref ref-type="bibr" rid="B65">Forj&#xe1;n et al., 2018</xref>; <xref ref-type="bibr" rid="B102">Kiran and Prasad, 2019</xref>). Despite all the benefits of phytoremediation, it also has weaknesses, including a long remediation period, non-implementation at high pollution sites, production of contaminated biomass, secondary pollution, slow growth of plants, limited plant resistance to unfavorable physical and chemical conditions found in polluted soils, and plants&#x2019; limited capacity to accumulate pollution (<xref ref-type="bibr" rid="B197">Yang et al., 2017b</xref>; <xref ref-type="bibr" rid="B35">C&#xe1;rdenas-Aguiar et al., 2020</xref>; <xref ref-type="bibr" rid="B78">Gu et al., 2020</xref>; <xref ref-type="bibr" rid="B144">Manori et al., 2021</xref>).</p>
</sec>
<sec id="s4">
<title>4 Phytoremediation efficiency, plant type, and other factors</title>
<p>In the phytoremediation process, plants are used to remove and stabilization of soil pollution without negatively affecting the structure, quality, and biological activities of the soil, so it is necessary to select plants that are not only tolerant of pollution but also fast-growing and provide maximum root surface (<xref ref-type="bibr" rid="B43">Claus et al., 2007</xref>; <xref ref-type="bibr" rid="B16">Barati et al., 2018</xref>; <xref ref-type="bibr" rid="B119">Li et al., 2021b</xref>). Also, phytoremediation can be used as a first step to creating wildlife habitats, which will only be possible if native plant species are used that are well adapted to the local climate and soil (<xref ref-type="bibr" rid="B172">Roohi et al., 2020</xref>), because native plants will have better growth, survival, and reproduction under environmental stress than non-native plants (<xref ref-type="bibr" rid="B16">Barati et al., 2018</xref>) (<xref ref-type="table" rid="T3">Table 3</xref>). There has been a high degree of focus in recent years on woody plant species in phytoremediation because these plant species, in addition to concentrating soil pollution in their tissues, can be used for various types of pollution as well as be economically viable due to their efficiency in various industries (<xref ref-type="bibr" rid="B154">Pandey et al., 2009</xref>; <xref ref-type="bibr" rid="B56">Fancello et al., 2019</xref>). Plants belonging to the <italic>Salicaceae</italic> family (Salix and Picea) are among the most important woody species used in phytoremediation (<xref ref-type="bibr" rid="B55">Evlard et al., 2014</xref>), which are suitable for growing in abandoned agricultural lands and polluted marginal lands because of their rapid growth, extensive root system, high biomass production rate, ability to support microbial communities, high transpiration rate, capability to absorb nutrients, tolerance to a wide range of organic and inorganic pollutants, high antioxidant activities, and easy reproduction (<xref ref-type="bibr" rid="B189">Wu et al., 2010</xref>; <xref ref-type="bibr" rid="B45">Cloutier-Hurteau et al., 2014</xref>; <xref ref-type="bibr" rid="B173">Salam et al., 2019</xref>; <xref ref-type="bibr" rid="B113">Lebrun et al., 2021b</xref>; <xref ref-type="bibr" rid="B119">Li et al., 2021b</xref>).</p>
<p>Among other woody plants, <italic>Populus x euramericana</italic> clones could potentially be used for the phytoremediation of polluted lands due to their high growth, biomass, and ability to extract various types of HMs (<xref ref-type="bibr" rid="B29">Borghi et al., 2007</xref>; <xref ref-type="bibr" rid="B165">Redovnikovi&#x107; et al., 2017</xref>; <xref ref-type="bibr" rid="B176">Simiele et al., 2020</xref>). In contrast, herbaceous species with extensive fibrous roots also are very beneficial for remediating polluted soils (<xref ref-type="bibr" rid="B11">APHA, 2003</xref>), especially those species known as hyperaccumulators, which are capable of absorbing large amounts of HMs and transferring them to their aerial organs, such as <italic>Sedum alfredii</italic> and <italic>Thlaspi caerulescens</italic> (<xref ref-type="bibr" rid="B113">Lebrun et al., 2021b</xref>). <italic>Symphytum officinale</italic> also is a perennial herbaceous plant that, due to its high biomass, rapid growth, and high accumulation of HMs, can be widely spread across large areas and improve phytoremediation (<xref ref-type="bibr" rid="B184">Wang et al., 2017b</xref>; <xref ref-type="bibr" rid="B190">Xiao et al., 2018</xref>). However, one of the most ideal plants for polluted environments is <italic>Solanum nigrum</italic>, which is relatively easy to adapt to different conditions and highly tolerant (<xref ref-type="bibr" rid="B124">Liang et al., 2017</xref>). This plant has a strong antioxidant system and the ability to produce macrophage proteins and various organic acids in different organs involved in the transport and accumulation of HMs, which makes it capable of extracting several types of HMs (such as Cr, As, Pb, Cd, and Ni) as well as carbon tetrachloride, polycyclic aromatic hydrocarbons, etc., (<xref ref-type="bibr" rid="B124">Liang et al., 2017</xref>; <xref ref-type="bibr" rid="B183">Ur Rehman et al., 2017</xref>). Among other herbaceous plants with a high ability to heavy metals accumulate and phytoremediation are <italic>Beta vulgaris</italic> var. cicla and <italic>Potentilla griffithii</italic> Hook. f. var. velutina Card (<xref ref-type="bibr" rid="B9">Ali et al., 2013</xref>; <xref ref-type="bibr" rid="B78">Gu et al., 2020</xref>).</p>
<p>The use of economic crops such as rice, cotton, sunflower, etc., which have high environmental compatibility and biomass production potential, has attracted the attention of researchers for the phytoremediation of contaminated land on a large scale (<xref ref-type="bibr" rid="B22">Bhardwaj et al., 2014</xref>; <xref ref-type="bibr" rid="B113">Lebrun et al., 2021b</xref>; <xref ref-type="bibr" rid="B81">Gusmini et al., 2021</xref>). Alfalfa (<italic>Medicago sativa</italic> L.) is another crop that can be used to remediate contaminated soils, as it has high yields, deep roots, and drought tolerance that distinguish it from other plants used in the phytoremediation process (<xref ref-type="bibr" rid="B4">Agegnehu et al., 2016</xref>). Another crop suitable for phytoremediation is corn, which, in addition to its economic importance, can provide a biological indicator of pollution (<xref ref-type="bibr" rid="B98">Khan et al., 2018</xref>). With its fibrous root system, global availability, ability to grow in diverse climates, and fast germination rate, corn has special advantages over other crops for phytoremediation (<xref ref-type="bibr" rid="B98">Khan et al., 2018</xref>; <xref ref-type="bibr" rid="B113">Lebrun et al., 2021b</xref>). In addition, there has been a recent focus on using a periodic system of oil crops to improve polluted soils, which has economic benefits as well as the effect on crop production (<xref ref-type="bibr" rid="B197">Yang et al., 2017b</xref>; <xref ref-type="bibr" rid="B75">Gong et al., 2018b</xref>).</p>
<p>On the other hand, in the stabilization process, certain plants are used in polluted soils that are not capable of transferring pollutants to their aerial organs, but in addition to reducing the bioavailability and mobility of pollutants in soil, they prevent them from entering underground water and the food chain (<xref ref-type="bibr" rid="B56">Fancello et al., 2019</xref>; <xref ref-type="bibr" rid="B172">Roohi et al., 2020</xref>). Therefore, plants should be selected that are capable of stabilizing pollutants on the epidermis of their roots or rhizosphere, Among the most important of these plants are <italic>Euphorbia Pithyulentum</italic>, <italic>Spartina anglica</italic>, <italic>Solanum lycopersicum</italic>, <italic>Juncus acutus</italic>, <italic>Lycopersicon esculentum</italic>, <italic>Phragmites australis</italic>, <italic>Vallisneria americana</italic>, and <italic>Bromus tomentellus</italic> (<xref ref-type="bibr" rid="B56">Fancello et al., 2019</xref>; <xref ref-type="bibr" rid="B210">Zhen et al., 2019</xref>; <xref ref-type="bibr" rid="B172">Roohi et al., 2020</xref>). In addition, plants of <italic>Salicaceae</italic> family are also potent stabilizers due to their extensive root systems, abundant biomass, high transpiration rates, ability to grow in polluted environments, high water-use efficiency, and high contaminant accumulation at the roots (<xref ref-type="bibr" rid="B55">Evlard et al., 2014</xref>; <xref ref-type="bibr" rid="B165">Redovnikovi&#x107; et al., 2017</xref>; <xref ref-type="bibr" rid="B112">Lebrun et al., 2018</xref>).</p>
<p>In addition to the selection of suitable plants, phytoremediation&#x2019;s efficiency is highly influenced by the chemical and physical properties of soil, including the quantity and nature of organic matter and nutrients, mineralogy, texture, structure, and pH (<xref ref-type="bibr" rid="B97">Kayser et al., 2000</xref>; <xref ref-type="bibr" rid="B209">Zhao et al., 2019</xref>). Therefore, modifying polluted environments with mineral and organic modifiers improves phytoremediation efficiency (<xref ref-type="bibr" rid="B40">Cheng et al., 2020</xref>). Several studies have demonstrated that a wide range of microbial communities, including bacteria, algae, and fungi, enhance the effectiveness of phytoremediation by influencing the soil&#x2019;s physical and chemical properties (<xref ref-type="bibr" rid="B104">Koul and Taak, 2018</xref>; <xref ref-type="bibr" rid="B46">Cui et al., 2020</xref>). A microbial community produces different types of enzymes to regulate degradation pathways through various oxidation reactions that result in the production of CO<sub>2</sub> and H<sub>2</sub>O (<xref ref-type="bibr" rid="B10">Ali et al., 2021</xref>). Additionally, microbial communities can improve the morpho-physiological structures of plants through ACC-deaminase activity, phosphorus dissolution, siderophores production, and ethylene stress reduction, thereby increasing phytoremediation efficiency (<xref ref-type="bibr" rid="B130">Liu et al., 2015a</xref>; <xref ref-type="bibr" rid="B60">Fatima et al., 2018</xref>; <xref ref-type="bibr" rid="B3">Afzal et al., 2020</xref>). The microbes also play a major role in changing HMs&#x2019; chemical behavior in the rhizosphere, and in addition to influencing plant growth during phytoremediation, that effect at improving HMs extraction, bioavailability, and accumulation in plants as well (<xref ref-type="bibr" rid="B117">Li et al., 2019b</xref>; <xref ref-type="bibr" rid="B56">Fancello et al., 2019</xref>; <xref ref-type="bibr" rid="B58">Farias et al., 2020</xref>).</p>
<p>The use of organic and inorganic modifiers in phytoremediation has gained popularity in recent years (<xref ref-type="bibr" rid="B109">Lebrun et al., 2021a</xref>; <xref ref-type="bibr" rid="B144">Manori et al., 2021</xref>). Several studies have shown that the addition of these soil modifiers through increasing the stabilization of HMs in the soil, reducing the toxicity of HMs in plants, increasing the cation exchange capacity (CEC) of the soil, improving soil structure, enhancing soil ventilation, increasing nutrient availability and content, and improving soil water holding capacity, increases the efficiency of phytoremediation in polluted environments (<xref ref-type="bibr" rid="B17">Bashir et al., 2018</xref>; <xref ref-type="bibr" rid="B172">Roohi et al., 2020</xref>; <xref ref-type="bibr" rid="B109">Lebrun et al., 2021a</xref>). Furthermore, these organic and inorganic modifiers increase phytoremediation efficiency by stimulating microorganisms&#x2019; activities, increasing plant growth and biomass production (<xref ref-type="bibr" rid="B44">Clemente et al., 2012</xref>; <xref ref-type="bibr" rid="B16">Barati et al., 2018</xref>; <xref ref-type="bibr" rid="B172">Roohi et al., 2020</xref>; <xref ref-type="bibr" rid="B28">Boorboori and Zhang, 2022b</xref>). The following are some of the most important modifiers used in recent years: poultry droppings, cow dung, biochar, rice husk, compost, technocell, steel slag, carbon materials (CMs), and nanomaterials (NMs) (<xref ref-type="bibr" rid="B177">Singh and Lee, 2016</xref>; <xref ref-type="bibr" rid="B65">Forj&#xe1;n et al., 2018</xref>; <xref ref-type="bibr" rid="B109">Lebrun et al., 2021a</xref>; <xref ref-type="bibr" rid="B48">Deebika et al., 2021</xref>), and in the following, biochar&#x2019;s role in phytoremediation of HMs will be discussed in more detail.</p>
</sec>
<sec id="s5">
<title>5 Biochar and phytoremediation</title>
<p>Since contaminated soil is not an ideal environment for plant growth, phytoremediation is greatly reduced in efficiency (<xref ref-type="bibr" rid="B61">Fellet et al., 2014</xref>). Therefore, the use of modifiers like Biochar can, in addition to improving soil structure, promote the growth of plants used for phytoremediation (<xref ref-type="bibr" rid="B176">Simiele et al., 2020</xref>; <xref ref-type="bibr" rid="B119">Li et al., 2021b</xref>). Moreover, biochar has attracted researchers&#x2019; attention due to its cost-effectiveness and ability to clean environments contaminated with organic and inorganic pollutants (<xref ref-type="bibr" rid="B33">Byrne et al., 2018</xref>; <xref ref-type="bibr" rid="B49">Ding et al., 2020</xref>). Phytoremediation can be improved with biochar due to its long-term stability compared to other organic amendments as well as its effective role in improving the soil&#x2019;s physical, chemical, and biological properties (<xref ref-type="bibr" rid="B34">C&#xe1;rdenas-Aguiar et al., 2019</xref>; <xref ref-type="bibr" rid="B163">Ratnasari et al., 2020</xref>). By improving soil pH, carbon content, soil aeration, soil fertility, water retention capacity, microbial diversity, and plant growth, biochar is highly effective at cleaning environments contaminated with HMs (<xref ref-type="bibr" rid="B65">Forj&#xe1;n et al., 2018</xref>; <xref ref-type="bibr" rid="B73">Gong et al., 2019</xref>; <xref ref-type="bibr" rid="B48">Deebika et al., 2021</xref>). Furthermore, Its high specific surface area, porous structure (macropores and micropores), cation exchange capacity, and active functional groups make biochar an effective tool for stabilizing soil pollution and reducing HMs bioavailability for organisms (<xref ref-type="bibr" rid="B178">Song et al., 2016</xref>; <xref ref-type="bibr" rid="B196">Yang et al., 2017a</xref>; <xref ref-type="bibr" rid="B203">Zhang et al., 2019a</xref>). It is important to note that all the benefits mentioned above depend on the particle size, intrinsic properties, application method, and the amount of biochar applied to the soil (<xref ref-type="bibr" rid="B118">Li et al., 2021a</xref>), and in the following, it will be discussed the details how biochar can improve the phytoremediation process of HMs (<xref ref-type="fig" rid="F3">Figure 3</xref>).</p>
<fig id="F3" position="float">
<label>FIGURE 3</label>
<caption>
<p>The effect of adding biochar on soil and plants in the phytoremediation process. BCF, Bioconcentration factor; TF, Transfer factor; HMs, Heavy metals.</p>
</caption>
<graphic xlink:href="fenvs-11-1253144-g003.tif"/>
</fig>
<p>Studies have shown that adding biochar to the culture medium can significantly increase the growth of plants, and this growth may be heterogeneous across different organs of the plant, but it generally results in a 10% increase in overall growth (<xref ref-type="bibr" rid="B157">Paz-Ferreiro et al., 2014</xref>; <xref ref-type="bibr" rid="B32">Burachevskaya et al., 2021</xref>). Biochar causes morphological changes in plant roots, as well as affects a plant&#x2019;s ability to absorb pollutants (<xref ref-type="bibr" rid="B168">Rees et al., 2016</xref>; <xref ref-type="bibr" rid="B78">Gu et al., 2020</xref>); however, the extent of reduction in pollutant absorption depends on the species of plants and the speciation characteristics of environmental pollutants (<xref ref-type="bibr" rid="B78">Gu et al., 2020</xref>). On the other hand, the cell walls of roots contain molecules such as pectin, proteins, and dissolved phosphates that stabilize pollutants in the root space and prevent their transfer to aerial organs, and biochar increases the efficiency of these physiological structures in plants&#x2019; roots (<xref ref-type="bibr" rid="B111">Lebrun et al., 2017</xref>; <xref ref-type="bibr" rid="B78">Gu et al., 2020</xref>). Previous studies confirm that amended soils by biochar increase plant tolerance to environmental pollution by improving parameters such as chlorophyll pigment content, intercellular CO<sub>2</sub> concentration, transpiration rate, photosynthetic rate, and stomatal conductance, as well as reducing the efficiency of HMs transport in plants (<xref ref-type="bibr" rid="B58">Farias et al., 2020</xref>; <xref ref-type="bibr" rid="B119">Li et al., 2021b</xref>; <xref ref-type="bibr" rid="B139">Lyu et al., 2021</xref>) (<xref ref-type="fig" rid="F3">Figure 3</xref>).</p>
<p>According to a study conducted on <italic>Brassica juncea</italic> in a copper-contaminated environment, by increasing the rate of Holm oak biochar (BH), plant growth increased and Cu absorption decreased (<xref ref-type="bibr" rid="B171">Rodr&#xed;guez-Vila et al., 2014</xref>). Furthermore, a study conducted on <italic>Bidens pilosa</italic> grown in Cd-contaminated soil found that pine needle biochar had a positive effect on root growth, and at the same time decreased chlorophyll concentrations and increased proline concentrations, which revealed an increase in Cd toxicity in plant tissues (<xref ref-type="bibr" rid="B144">Manori et al., 2021</xref>); therefore it can be concluded that pine needle biochar can be used as a soil amendment to increase plant HMs extraction. In a study conducted by <xref ref-type="bibr" rid="B119">Li et al. (2021b)</xref> on <italic>Salix psammophila</italic> grown in Cu, Zn, and Cd-contaminated environments, it was shown that bamboo biochar, in addition to a slight increase in plant biomass, improved Bioconcentration Factor (BCF) and Translocation Factor (TF), which indicate that bamboo biochar improves the efficiency of HMs extraction and phytoremediation. Additionally, the study on <italic>Boehmeria nivea</italic> demonstrated that tea waste biochar reduced Cd toxicity and increased its accumulation and displacement in seedlings by changing the intracellular distribution of Cd, reducing oxidative stress, and improving plant growth (<xref ref-type="bibr" rid="B73">Gong et al., 2019</xref>) (<xref ref-type="table" rid="T4">Table 4</xref>).</p>
<table-wrap id="T4" position="float">
<label>TABLE 4</label>
<caption>
<p>Incorporating biochar into phytoremediation of polluted soils that contain metal(iod)s.</p>
</caption>
<table>
<thead valign="top">
<tr>
<th align="center">Biochar feedstock and dose</th>
<th align="center">Plant</th>
<th align="center">Metal(iod)s</th>
<th align="center">Effects on phytoremediation</th>
<th align="center">References</th>
</tr>
</thead>
<tbody valign="top">
<tr>
<td align="center">Wood: 2.5%&#x2013;5%</td>
<td align="center">
<italic>Lycopersicon esculentum</italic>
</td>
<td align="center">Cr, Mn, and Ni</td>
<td align="center">Reduce exchangeable Cr, Ni, and Mn. Enhanced plant growth</td>
<td align="center">
<xref ref-type="bibr" rid="B15">Bandara et al. (2017)</xref>
</td>
</tr>
<tr>
<td align="center">Sewage sludge: 5% and 10%</td>
<td align="center">
<italic>Oryza sativa</italic>
</td>
<td align="center">As, Zn, Cd, Ni, Cr, Co, Pb, and Cu</td>
<td align="center">Reduced pore water Pb, As, Ni, Cr, and Co owing to elevated soil pH. Mobilize Cd, Cu, and Zn</td>
<td align="center">
<xref ref-type="bibr" rid="B99">Khan et al. (2013)</xref>
</td>
</tr>
<tr>
<td align="center">Pruning residues and manure: 1.5%&#x2013;3%</td>
<td align="center">
<italic>Anthyllis vulneraria</italic>
</td>
<td align="center">Ni, Cd, Ti, Zn, Cr, Pb, Cu, and Fe</td>
<td align="center">Reduced water-extractable Zn, Cu, Cd, and Cr.Increased pH</td>
<td align="center">
<xref ref-type="bibr" rid="B61">Fellet et al. (2014)</xref>
</td>
</tr>
<tr>
<td align="center">Poultry manure and green waste</td>
<td align="center">
<italic>Brassica juncea</italic>
</td>
<td align="center">Cd, Pb, and Cu</td>
<td align="center">Increased (353%) plant shoot dry biomass. Decreased Pb, Cd, and Cu accumulation in plants</td>
<td align="center">
<xref ref-type="bibr" rid="B155">Park et al. (2011)</xref>
</td>
</tr>
<tr>
<td align="center">Hardwoods: 20%</td>
<td align="center">
<italic>Miscanthus</italic>&#xd7;<italic>giganteus</italic>
</td>
<td align="center">As</td>
<td align="center">Improved pore water with As</td>
<td align="center">
<xref ref-type="bibr" rid="B179">Sun et al. (2018)</xref>
</td>
</tr>
<tr>
<td align="center">Miscanthus: 5% and 10%</td>
<td align="center">
<italic>Brassica napus</italic>
</td>
<td align="center">Cd, Zn, and Pb</td>
<td align="center">Reduced metals bioavailability in shoot biomass</td>
<td align="center">
<xref ref-type="bibr" rid="B15">Bandara et al. (2017)</xref>
</td>
</tr>
<tr>
<td align="center">Oka, Ash, and Birch: 20%v/v</td>
<td align="center">
<italic>Lolium perenne</italic> L.</td>
<td align="center">Pb and Cu</td>
<td align="center">Reduced pore water-mediated Pb and Cu doses in shoots</td>
<td align="center">
<xref ref-type="bibr" rid="B179">Sun et al. (2018)</xref>
</td>
</tr>
<tr>
<td align="center">Hardwood</td>
<td align="center">
<italic>Solanum lycopersicum</italic>
</td>
<td align="center">As, Cd, Zn, and Cu</td>
<td align="center">Raised pore water with Cu and As. Immobilize Zn and Cd owing to elevated DOC and pH</td>
<td align="center">
<xref ref-type="bibr" rid="B18">Beesley and Marmiroli (2011)</xref>
</td>
</tr>
</tbody>
</table>
</table-wrap>
<p>An investigation of the potential of <italic>Ipomoea reptans Poir</italic> for phytoremediation of Cd-contaminated soils revealed that adding corn biochar in addition to increasing Cd absorption by seedlings, increased the dry and fresh weight of shoots, the dry and fresh weight of roots, chlorophyll content, the leaf area, the number of leaves and plant height (<xref ref-type="bibr" rid="B163">Ratnasari et al., 2020</xref>). In the study conducted on coconut husk and orange bagasse biochars, it was demonstrated that their use for <italic>B. juncea</italic> under Cu stress with low concentration, increased root and shoot mass, photosynthetic activity, chlorophyll content, Cu absorption from the soil, and Cu concentration in the aerial parts of plants (<xref ref-type="bibr" rid="B77">Gonzaga et al., 2022</xref>), which showed that these biochars increased effectiveness of <italic>B. juncea</italic> in phytoremediation. <xref ref-type="bibr" rid="B202">Zhang et al. (2019b)</xref> found that adding rice straw biochar to alfalfa (<italic>M. sativa</italic> L.) culture medium improved the plant&#x2019;s ability to extract Cd from contaminated soils as well as produce the seedlings&#x2019; biomass. Another study that was conducted on <italic>B. vulgaris</italic> grown in a Cd-contaminated environment found that cornstalk biochar, in addition to producing more root biomass, increased Cd extraction from the soil environment, as well as Cd absorption into the roots&#x2019; cell walls (<xref ref-type="bibr" rid="B78">Gu et al., 2020</xref>), therefore, cornstalk biochar, in addition to helping the phytoremediation process, can also enhance <italic>B. vulgaris</italic>&#x2019; resistance to pollutions. Similar results have been reported using straw biochar in improving Cd absorption and root morphology of <italic>Sedum plumbizincicola</italic> in acidic soils (<xref ref-type="bibr" rid="B121">Li et al., 2018</xref>) (<xref ref-type="fig" rid="F3">Figure 3</xref>; <xref ref-type="table" rid="T4">Table 4</xref>).</p>
<p>As well as influencing the morpho-physiological structure of plants involved in phytoremediation, biochar also helps stabilize pollutants and reduce their bioavailability in the soil through its effects on soil structures (<xref ref-type="bibr" rid="B69">Ghosh and Maiti, 2021</xref>; <xref ref-type="bibr" rid="B77">Gonzaga et al., 2022</xref>). Since HMs are both cationic and anionic, they interact with the anionic and cationic ions on biochar and directly absorb on the biochar surface, therefore reducing their bioavailability in soil (<xref ref-type="bibr" rid="B167">Rees et al., 2014</xref>; <xref ref-type="bibr" rid="B64">Fija&#x142;kowska et al., 2021</xref>). Biochar Also contains functional groups on its surface that can form complexes with soil pollutants and stabilize them (<xref ref-type="bibr" rid="B10">Ali et al., 2021</xref>; <xref ref-type="bibr" rid="B80">Gupta et al., 2021</xref>). According to <xref ref-type="bibr" rid="B80">Gupta et al. (2021)</xref>, when biochar is combined with the soil surface, the biochar particles with cation charged can absorb anionic HMs, such as arsenate and arsenite, while negatively charged particles of biochar stabilize soil positive components, including Pb and Cd (<xref ref-type="fig" rid="F3">Figure 3</xref>).</p>
<p>
<xref ref-type="bibr" rid="B171">Rodr&#xed;guez-Vila et al. (2014)</xref> found that Holm oak biochar reduced the bioavailability of Cu in contaminated mine soils, and at the same time, <xref ref-type="bibr" rid="B159">Puga et al. (2015)</xref> showed that sugar cane biochar reduced Zn, Pb, and Cd bioavailability in contaminated mineral soils. A study conducted on soils contaminated with Pb and Cd showed that bamboo biochar could stabilize and reduce the bioavailability of these HMs, possibly due to the absorption of HMs on the surface of biochar (<xref ref-type="bibr" rid="B193">Xu et al., 2016</xref>). A greenhouse experiment showed that the addition of pig manure biochar reduced Pb leaching by 71% in soils with low organic carbon (<xref ref-type="bibr" rid="B102">Kiran and Prasad, 2019</xref>), while <xref ref-type="bibr" rid="B61">Fellet et al. (2014)</xref> demonstrated in their studies that garden pruning residues biochar reduces Pb, Cd, and Zn bioavailability in the soil. Moreover, biochar can convert Cr (VI) into less mobile Cr (III) by continuously transferring electrons, which connect with oxygen-containing functional groups on its surface (<xref ref-type="bibr" rid="B51">Dong et al., 2017</xref>). A study conducted on soils contaminated with Cd, Pb, Mn, Cu, and Fe showed that date palm waste biochar can significantly reduce the concentration of extractable HMs in the soil (<xref ref-type="bibr" rid="B7">Al-Wabel et al., 2015</xref>). Various studies have also shown that miscanthus, poplar wood, and rice straw biochars can significantly stabilize HMs in polluted soils, reducing their bioavailability to living organisms (<xref ref-type="bibr" rid="B88">Houben et al., 2013</xref>; <xref ref-type="bibr" rid="B94">Jones et al., 2016</xref>; <xref ref-type="bibr" rid="B38">Chen et al., 2018</xref>). According to <xref ref-type="bibr" rid="B148">Narayanan and Ma (2022)</xref> study, the type of biochar used plays an important role in the amount of Ni and Cd stabilization.</p>
<p>In addition to being capable of stabilizing HMs, biochar can also cause the absorption of soil nutrients, reducing the competition between HMs and nutrients in the soil, which, in addition to the accumulation of soil nutrients, increases the absorption of HMs in plants used in the phytoremediation and extraction process (<xref ref-type="bibr" rid="B166">Rees et al., 2015</xref>; <xref ref-type="bibr" rid="B119">Li et al., 2021b</xref>). Studies have shown that adding biochar to the environment causes a deficiency of nitrogen, phosphorus, and calcium in plants, and in addition, biochar with different functional groups (carboxylic, lactonic, and organic nitrogen) and inorganic impurities (metal oxides and Ash) increases the capacity of soil to absorb carbon materials (<xref ref-type="bibr" rid="B5">Agrafioti et al., 2014</xref>; <xref ref-type="bibr" rid="B168">Rees et al., 2016</xref>; <xref ref-type="bibr" rid="B172">Roohi et al., 2020</xref>). Aside from competing for absorption sites on biochar, nutrients and HMs also compete for transporters and entry channels into plants (<xref ref-type="bibr" rid="B57">Farhangi-Abriz and Torabian, 2017</xref>). As a result of adding bamboo biochar to soil, <xref ref-type="bibr" rid="B119">Li et al. (2021b)</xref> found that the soil content of potassium and organic matter increased, and it decreased the accumulation of Zn, Cd, and Cu in the soil, while biochar increased the accumulation of these HMs in <italic>S. psammophila</italic>, which was used in the experiment (<xref ref-type="fig" rid="F3">Figure 3</xref>).</p>
<p>The addition of biochar to soil changes soil pH, water holding capacity, and dissolved organic content (DOC) (<xref ref-type="bibr" rid="B1">Abdelaal et al., 2021</xref>; <xref ref-type="bibr" rid="B148">Narayanan and Ma, 2022</xref>). In general, biochar creates a liming effect and increases the pH of the soil, which is due to the increase of ash content in the soil (<xref ref-type="bibr" rid="B176">Simiele et al., 2020</xref>), and since pH and DOC have a significant effect on HMs removal and absorption in soil (<xref ref-type="bibr" rid="B186">Wang et al., 2020</xref>), thus, adding biochar to the soil increases the mobility of anionic HMs like Selenium (Se), As, Cu, Cr, and Antimony (Sb), among which Cu mobility heavily depends on DOC content of biochar (<xref ref-type="bibr" rid="B179">Sun et al., 2018</xref>; <xref ref-type="bibr" rid="B80">Gupta et al., 2021</xref>; <xref ref-type="bibr" rid="B148">Narayanan and Ma, 2022</xref>). Furthermore, some studies have shown that increasing the pH of soil through biochar addition reduces the bioavailability of some heavy metals (such as Pb, Zn, and Cd), and reduces their concentration in soil pore water (<xref ref-type="bibr" rid="B166">Rees et al., 2015</xref>; <xref ref-type="bibr" rid="B111">Lebrun et al., 2017</xref>; <xref ref-type="bibr" rid="B146">Mehmood et al., 2018</xref>; <xref ref-type="bibr" rid="B207">Zhang et al., 2021</xref>) (<xref ref-type="fig" rid="F3">Figures 3</xref>, <xref ref-type="fig" rid="F4">4</xref>).</p>
<fig id="F4" position="float">
<label>FIGURE 4</label>
<caption>
<p>The sorption of Cd, Pb, and As by biochars in soil. The results are taken from <xref ref-type="bibr" rid="B175">Shaheen et al. (2023)</xref>.</p>
</caption>
<graphic xlink:href="fenvs-11-1253144-g004.tif"/>
</fig>
<p>Biochar treatment efficiency in the phytoremediation process is also influenced by several factors, such as pyrolysis temperature, heating rate, raw materials, aging, and particle size (<xref ref-type="bibr" rid="B137">Lu et al., 2014</xref>; <xref ref-type="bibr" rid="B67">Gasco et al., 2016</xref>; <xref ref-type="bibr" rid="B162">Rathnayake et al., 2021</xref>) (<xref ref-type="fig" rid="F5">Figure 5</xref>). Although the addition of biochar improves the absorption and stabilization of various pollutants, in general, the temperature of the pyrolysis for the preparation of biochar plays an effective role in improving phytoremediation in addition to soil type, plant type, and target pollutant (<xref ref-type="bibr" rid="B35">C&#xe1;rdenas-Aguiar et al., 2020</xref>). Biochar obtained from biomass at high temperatures is more stable in the environment and can be used for carbon sequestration (<xref ref-type="bibr" rid="B67">Gasco et al., 2016</xref>), while biochar made at low temperatures and from raw materials high in nutrients (such as sewage sludge or manure waste) is good for soil improvement (CEC and water retention capacity) and can be used to replace commercial fertilizers in soils contaminated with HMs (<xref ref-type="bibr" rid="B35">C&#xe1;rdenas-Aguiar et al., 2020</xref>). Due to the risk of the re-release of pollutants stabilized by biochar over time (<xref ref-type="bibr" rid="B78">Gu et al., 2020</xref>), researchers have been exploring whether the aging of biochar increases the release of pollutants. Based on the limited research that has been done on biochar aging, it has been shown that during the aging process, a wide range of functional groups, including carboxylic, hydroxyl, and phenolic, are formed on the surface of biochar (<xref ref-type="bibr" rid="B148">Narayanan and Ma, 2022</xref>), and the aging process does not affect the ability of biochar to stabilize HMs, especially those with a positive charge (<xref ref-type="bibr" rid="B69">Ghosh and Maiti, 2021</xref>; <xref ref-type="bibr" rid="B148">Narayanan and Ma, 2022</xref>), In studies, aged biochar produced at high pyrolysis temperatures more effectively stabilized pollutants in contaminated soils than aged biochar produced at lower pyrolysis temperatures (<xref ref-type="bibr" rid="B162">Rathnayake et al., 2021</xref>), however, this process needs more studies.</p>
<fig id="F5" position="float">
<label>FIGURE 5</label>
<caption>
<p>The effects of an increase in pyrolysis temperature, soil exposure time, and lignin content of the feedstock on the properties of biochar. The results are taken from <xref ref-type="bibr" rid="B21">Beusch (2021)</xref>.</p>
</caption>
<graphic xlink:href="fenvs-11-1253144-g005.tif"/>
</fig>
<p>On the other hand, studies conducted on the effect of biochar particle size on phytoremediation efficiency have indicated that biochar particle size plays a role in plants&#x2019; response to polluted culture environments (<xref ref-type="bibr" rid="B113">Lebrun et al., 2021b</xref>). Biochar particle size, which is divided into large (&#x3e;4&#xa0;mm) and small (&#x3c;20&#xa0;&#xb5;m) particles, is not expected to play a significant role in nutrient uptake, but it can alter biochar surface properties that affect contaminant stabilization (<xref ref-type="bibr" rid="B109">Lebrun et al., 2021a</xref>; <xref ref-type="bibr" rid="B113">Lebrun et al., 2021b</xref>). There have been limited studies on the effect of biochar particle size on the absorption and stabilization of HMs (<xref ref-type="bibr" rid="B205">Zhang et al., 2017</xref>; <xref ref-type="bibr" rid="B118">Li et al., 2021a</xref>; <xref ref-type="bibr" rid="B113">Lebrun et al., 2021b</xref>). In their study of <italic>S. psammophila</italic> treated with different particle sizes of bamboo biochar (P1&#x3c;0.15&#xa0;mm, 0.15&#xa0;mm &#x3c; P2 &#x3c; 0.25&#xa0;mm and 0.25&#xa0;mm &#x3c; P3 &#x3c; 0.50&#xa0;mm), <xref ref-type="bibr" rid="B118">Li et al. (2021a)</xref> found that treatment P2 had the greatest effect on Cd and Zn accumulation as well as plant growth. Furthermore, <xref ref-type="bibr" rid="B205">Zhang et al. (2017)</xref> showed that small particles of corn biochar increased Cd transfer from roots to shoots of <italic>Brassica chinensis</italic> L. Studies have also shown that treating rice and <italic>S. plumbizincicola</italic> with small particle size biochar reduces Zn concentrations in their aerial organs (<xref ref-type="bibr" rid="B211">Zheng et al., 2012</xref>; <xref ref-type="bibr" rid="B137">Lu et al., 2014</xref>).</p>
<p>The researchers found that biochar increases the activity and population of microbes (fungi and bacteria) in HMs-contaminated environments, whether there are plants present or not (<xref ref-type="bibr" rid="B96">Karppinen et al., 2017</xref>; <xref ref-type="bibr" rid="B204">Zhang et al., 2018</xref>; <xref ref-type="bibr" rid="B73">Gong et al., 2019</xref>). Additionally, biochar reduces the bioavailability of pollutants in soils by improving the physical and chemical properties of contaminated soils and creating conducive conditions for soil microorganisms, thus increasing the efficiency of phytoremediation in contaminated environments (<xref ref-type="bibr" rid="B127">Liu et al., 2017a</xref>; <xref ref-type="bibr" rid="B102">Kiran and Prasad, 2019</xref>; <xref ref-type="bibr" rid="B12">Arif et al., 2020</xref>). According to a study conducted on the effect of wheat straw biochar on cadmium remediation by <italic>M. sativa</italic> L, the addition of biochar improved soil enzyme productions (chitinase and protease), and fungal community growth (<xref ref-type="bibr" rid="B204">Zhang et al., 2018</xref>). In <xref ref-type="bibr" rid="B73">Gong et al. (2019)</xref>&#x2019;s study on the effect of biochar derived from tea waste in reducing the toxicity caused by Cd in polluted sediments, it was shown that biochar improved the activity of microbes producing catalase, phosphatase, and urease and decreased the Cd toxicity to ramie and microbes. <xref ref-type="bibr" rid="B142">Mackie et al. (2015)</xref> also found in their study in copper-contaminated vineyards that biochar increases the activity and abundance of microbes and their ecosystem services. In another study, it was found that biochar derived from sugarcane bagasse, in addition to increasing the population of Actinomycetales and bacteria, increased the activity of soil enzymes in soils contaminated with Pb, Cu, and Cd (<xref ref-type="bibr" rid="B150">Nie et al., 2018</xref>) (<xref ref-type="fig" rid="F3">Figure 3</xref>).</p>
</sec>
<sec id="s6">
<title>6 Phytoremediation with biochar in combination with other factors</title>
<p>Using biochar simultaneously with other compounds and amendment materials, in addition to overlapping their defects, enhances phytoremediation and pollution stabilization and removal (<xref ref-type="bibr" rid="B65">Forj&#xe1;n et al., 2018</xref>; <xref ref-type="bibr" rid="B76">Gong et al., 2021</xref>), therefore, researchers have been focusing on how biochar can be combined with nanoparticles, compost, lime, sulfur, metal oxides, etc., to improve phytoremediation in recent decades (<xref ref-type="bibr" rid="B194">Xu et al., 2018a</xref>; <xref ref-type="bibr" rid="B49">Ding et al., 2020</xref>; <xref ref-type="bibr" rid="B172">Roohi et al., 2020</xref>; <xref ref-type="bibr" rid="B71">Gogoi et al., 2021</xref>; <xref ref-type="bibr" rid="B148">Narayanan and Ma, 2022</xref>). In a study conducted on <italic>B. juncea</italic> for lead extraction, it was found that the simultaneous application of Neem tree wood logs biochar and EDTA significantly increased the biomass and total chlorophyll content of plants and increased lead absorption by the seedlings compared to the application of each treatment separately (<xref ref-type="bibr" rid="B161">Rathika et al., 2021</xref>). Several studies have shown that the combination of iron sulfate and biochar can be an effective strategy for increasing the stabilization and reducing the bioavailability of As in polluted environments through absorption or surface precipitation mechanisms (<xref ref-type="bibr" rid="B85">Hartley and Lepp, 2008</xref>; <xref ref-type="bibr" rid="B110">Lebrun et al., 2020</xref>; <xref ref-type="bibr" rid="B176">Simiele et al., 2020</xref>), and besides improving soil fertility, this combination can also boost plant growth and survival (<xref ref-type="bibr" rid="B84">Hartley et al., 2009</xref>; <xref ref-type="bibr" rid="B176">Simiele et al., 2020</xref>).</p>
<p>A study conducted by <xref ref-type="bibr" rid="B117">Li et al. (2019b)</xref> on <italic>S. nigrum</italic> L. treated with biochar and attapulgite showed that the simultaneous application of these treatments improved the fresh weight and length of the seedlings, while also increasing the absorption of Zn, Mn, Hg, Cu, Cd, and Pb in the plant roots, which demonstrates the positive effect of this compound in improving the stabilization of HMs. Furthermore, adding lime and sulfur to biochar can reduce HM bioavailability and improve plant growth in the process of phytoremediation (<xref ref-type="bibr" rid="B194">Xu et al., 2018a</xref>; <xref ref-type="bibr" rid="B148">Narayanan and Ma, 2022</xref>). Studies have also been conducted on the effectiveness of compost and biochar combination in phytoremediation of soil contaminated with HMs (<xref ref-type="bibr" rid="B172">Roohi et al., 2020</xref>; <xref ref-type="bibr" rid="B48">Deebika et al., 2021</xref>), some of which are listed below. In a study that was conducted to evaluate the potential of <italic>B. tomentellus</italic> for phytoremediation of soils contaminated with Cr and Zn with the help of biochar treatment and urban waste compost, it was shown that by combining these treatments, HMs absorption by seedlings significantly increased (<xref ref-type="bibr" rid="B172">Roohi et al., 2020</xref>). In addition, <xref ref-type="bibr" rid="B65">Forj&#xe1;n et al. (2018)</xref> showed that <italic>B. juncea</italic> L. &#x2b; compost &#x2b; biochar is the best combination for reducing Zn, Pb, Ni, and Cu concentrations in polluted soils. In another study, <xref ref-type="bibr" rid="B132">Liu et al. (2017b)</xref> found that the combination of compost and biochar reduces the bioavailability of HMs such as Cd, Cr, Zn, As, Cu, Ni, and Pb due to the higher levels of extractable minerals (such as nitrogen, phosphorus, calcium, magnesium, and potassium).</p>
<p>In a study that was conducted to evaluate the effectiveness of rice husk ash and Prosopis biochar in phytoremediation of Pb by <italic>Ricinus communis</italic>, it was demonstrated that the simultaneous use of these treatments improves soil pH, seedling tolerance to Pb, antioxidant activity, and nutrient uptake, while it reduced the availability of Pb in the soil, and a detailed analysis of the infrared spectra confirmed that oxygenated (ester and ether), amide and phosphate functional groups absorbed Pb and reduced its toxicity for plants (<xref ref-type="bibr" rid="B102">Kiran and Prasad, 2019</xref>). Similarly, a study conducted with rice straw and bamboo biochar found that the combination of these treatments reduced the extractable concentration of Zn, Pb, Cu, and Cd in contaminated soils (<xref ref-type="bibr" rid="B136">Lu et al., 2017</xref>). A positive effect on plant growth factors was observed following the addition of the above-mentioned treatments to the cultivation environment due to the improvement of physical and biological properties and the enhancement of soil nutrients (<xref ref-type="bibr" rid="B92">Isitekhale et al., 2013</xref>; <xref ref-type="bibr" rid="B16">Barati et al., 2018</xref>).</p>
<p>It has also been shown that the simultaneous treatment of microbes and biochar can improve the phytoremediation of HMs and increase the resistance of plants to these pollutants (<xref ref-type="bibr" rid="B58">Farias et al., 2020</xref>). Alternatively, heavy metal toxicity could affect the microorganisms that are added to soil environments to improve phytoremediation, and their efficiency may decrease (<xref ref-type="bibr" rid="B54">Dzionek et al., 2016</xref>; <xref ref-type="bibr" rid="B198">Yao et al., 2017</xref>). Thus, cell stabilization is an effective way of increasing microorganism resistance to pollution and restoring native soil microflora, and biochar, as a good carrier material for cell stabilization, can increase microorganisms&#x2019; resistance to pollutants&#x2019; toxicity (<xref ref-type="bibr" rid="B54">Dzionek et al., 2016</xref>; <xref ref-type="bibr" rid="B41">Chuaphasuk and Prapagdee, 2019</xref>), and It is clear that, in this case, a more in-depth research is required. In an experiment conducted on Plant extraction of Cd by <italic>Chlorophytum laxum R.Br</italic>, it was shown that bacteria (<italic>Arthrobacter sp</italic>. and <italic>Micrococcus sp</italic>.) stabilized with biochar increased the accumulation of Cd in the roots and shoots of seedlings and the extraction of Cd from contaminated soils (<xref ref-type="bibr" rid="B41">Chuaphasuk and Prapagdee, 2019</xref>). Another study conducted on <italic>Portulaca oleracea</italic> L. under Zn, Al, Cr (III), Cr (VI), and Fe stress demonstrated that by using biochar combined with <italic>Oscillatoria sp</italic>, in addition to increasing root and shoot lengths, organic carbon, nitrogen content, chlorophyll content, and stabilizing HMs in the soil, the accumulation of HMs in plant organs decreased (<xref ref-type="bibr" rid="B201">Zanganeh et al., 2022</xref>). In a study on the role of <italic>Jacaranda mimosifolia</italic> in the phytoremediation of Zn, Mn, and Cu under the treatment of biochar and spore suspension of five fungal isolates (<italic>Metarhizium anisopliae</italic>, <italic>Trichoderma asperella</italic>, <italic>Beauveria bassiana</italic>, <italic>Purpureocillium lilacinum</italic>, and <italic>Pochonia chlamydosporia</italic>), it was found that the extraction rate of HMs and their concentration in plant tissues increased noticeably, reducing the risk of HMs leaching in the soil (<xref ref-type="bibr" rid="B58">Farias et al., 2020</xref>) (<xref ref-type="fig" rid="F6">Figure 6</xref>).</p>
<fig id="F6" position="float">
<label>FIGURE 6</label>
<caption>
<p>Mechanisms of immobilization of metal(iod)s (HMs) by soil microorganisms in biocharamended soil; EPS (Extracellular polymeric substances). The results are taken from <xref ref-type="bibr" rid="B14">Bandara et al. (2020)</xref>.</p>
</caption>
<graphic xlink:href="fenvs-11-1253144-g006.tif"/>
</fig>
</sec>
<sec id="s7">
<title>7 Pyrolysis of phytoremediation residues</title>
<p>As phytoremediation plays an increasingly important role in cleaning polluted environments, disposing of plants used in this process has become an urgent issue (<xref ref-type="bibr" rid="B75">Gong et al., 2018b</xref>; <xref ref-type="bibr" rid="B212">Zhou et al., 2020</xref>). If contaminated biomass is returned directly to the soil after phytoremediation, it can cause secondary pollution in the soil and underground water, which can have irreparable effects on the ecosystem, animals, and humans (<xref ref-type="bibr" rid="B89">Huang et al., 2015</xref>; <xref ref-type="bibr" rid="B152">&#xd6;zkan et al., 2016</xref>; <xref ref-type="bibr" rid="B74">Gong et al., 2017</xref>). Therefore, in recent years, several solutions have been proposed for recycling plants grown in polluted environments, including making furniture, burning, and composting, though each mentioned method has obvious disadvantages (<xref ref-type="bibr" rid="B36">Chalot et al., 2012</xref>; <xref ref-type="bibr" rid="B115">Li et al., 2020a</xref>; <xref ref-type="bibr" rid="B69">Ghosh and Maiti, 2021</xref>). For example, only wooden plants can be used to make household furniture, while herbaceous plants resulting from the phytoremediation process are not useful (<xref ref-type="bibr" rid="B69">Ghosh and Maiti, 2021</xref>); On the other hand, burning or composting contaminated biomass can release pollutants into the air, water, and soil (<xref ref-type="bibr" rid="B207">Zhang et al., 2021</xref>).</p>
<p>One of the best ways to utilize phytoremediation residues and produce biochar is through pyrolysis, which offers many advantages such as reducing contaminated biomass volume and mass, stabilizing (reducing bioavailability) and decomposing organic and inorganic pollutants, producing valuable pyrolytic products (such as coal, biofuel, etc.), and improving soil quality (carbon sequestration, stabilization of metals in polluted soil and increasing soil fertility) (<xref ref-type="bibr" rid="B125">Lievens et al., 2008</xref>; <xref ref-type="bibr" rid="B191">Xiao et al., 2015</xref>; <xref ref-type="bibr" rid="B20">Bert et al., 2017</xref>; <xref ref-type="bibr" rid="B151">Niu et al., 2017</xref>; <xref ref-type="bibr" rid="B53">Du et al., 2019b</xref>; <xref ref-type="bibr" rid="B153">Palansooriya et al., 2020</xref>; <xref ref-type="bibr" rid="B208">Zhang et al., 2020</xref>). A key factor in producing biochar from phytoremediation residues is the pyrolysis temperature, which determines the distribution of heavy metals in biochar (<xref ref-type="bibr" rid="B90">Huang et al., 2018</xref>). For instance, Cd evaporates at a temperature above 600&#xb0;C, while Hg completely evaporates at 350&#xb0;C (<xref ref-type="bibr" rid="B72">Gong et al., 2018a</xref>). Compared to high pyrolysis temperatures, low pyrolysis temperatures increase the accumulation of heavy metals and humic substances in biochar, while reducing the amount of low molecular weight acids (<xref ref-type="bibr" rid="B23">Bian et al., 2018</xref>). On the other hand, HMs species present in phytoremediation plants can influence the properties of biochar, for instance, Fe can enhance the graphicization of biochar, while Zn can increase the porosity of biochar (<xref ref-type="bibr" rid="B49">Ding et al., 2020</xref>).</p>
<p>In their studies on <italic>S. officinale</italic> L. used in phytoremediation, <xref ref-type="bibr" rid="B53">Du et al. (2019b)</xref> found that pyrolysis temperatures above 550&#xb0;C stabilize HMs and greatly reduce their leaching into biochar, and improve biochar environmental safety. In another study by <xref ref-type="bibr" rid="B208">Zhang et al. (2020)</xref> on pyrolysis of <italic>Lolium perenne</italic> L., <italic>Pennisetum sinese</italic>, and <italic>Brassica napus</italic> L. residues obtained from phytoremediation, they found that a temperature higher than 600&#xb0;C makes the Cd toxicity in biochar acceptable to the environment and its leaching rate in biochar is reduced to an acceptable level. A study on <italic>Silphium perfoliatum</italic> L. obtained from a phytoremediation process and containing HMs found that pyrolysis at 750&#xb0;C reduces the long-term leaching of HMs, increases oxidation resistance, and prevents the release of HMs attached to organic materials (<xref ref-type="bibr" rid="B52">Du et al., 2019a</xref>). The study by <xref ref-type="bibr" rid="B212">Zhou et al. (2020)</xref> found that biochar obtained from <italic>Helianthus annuus</italic> L. containing Cd, Zn, Pb, and Cu can be used as a fertilizer to improve soil quality. Researchers found that converting cobalt-containing Siberian iris into biochar through one-step pyrolysis improved mercury phytoremediation of polluted soils and waters (<xref ref-type="bibr" rid="B120">Li et al., 2020b</xref>). The results of another study conducted on ramie after the phytoremediation process showed that pyrolysis can enhance the stabilization of Pb, Cu, Zn, Cd, and Cr in plant residues and increase the possibility of reusing phytoremediation residues (<xref ref-type="bibr" rid="B75">Gong et al., 2018b</xref>). Moreover, <xref ref-type="bibr" rid="B207">Zhang et al. (2021)</xref> found that biochar produced from cadmium-contaminated <italic>L. perenne</italic> L. and <italic>B. napus</italic> L. residues at high pyrolysis temperatures, due to the increase in Cd stabilization in biochar, had a greatly decreased risk of environmental contamination. However, to demonstrate the effectiveness of phytoremediation residues as biochar, more studies are necessary about environmental toxicity, washability, stability, environmental hazards, and its chemical forms (<xref ref-type="bibr" rid="B83">Han et al., 2018</xref>; <xref ref-type="bibr" rid="B52">Du et al., 2019a</xref>).</p>
</sec>
<sec sec-type="conclusion" id="s8">
<title>8 Conclusion</title>
<p>The results of the present study demonstrated that using biochar in the phytoremediation process can improve the extraction and stabilization of HMs pollution, as well as increase plant resistance under stress conditions. On the other hand, owing to the variety of pollutions, plants suitable for phytoremediation, biochars, and other factors that enhance the phytoremediation process, the positive effects of different types of biochar on reducing all pollution in the environment cannot be mentioned with absolute certainty. Therefore, in future studies, a complex investigation of the interplay between different factors (biochar, plants, pollutants, etc.) is required to improve the efficiency of phytoremediation. It is also suggested that future studies should focus on field experiments so that by obtaining more practical information, an effective step can be taken toward reducing pollution and creating a healthier environment for future generations.</p>
</sec>
</body>
<back>
<sec id="s9">
<title>Author contributions</title>
<p>MB and LL wrote and edited the manuscript. All authors contributed to the article and approved the submitted version.</p>
</sec>
<sec id="s10">
<title>Funding</title>
<p>This paper was funded by the project: VEGA 1/0186/23 Windbreaks in the agricultural landscape&#x2014;ecological, environmental, and economic value of multifunctional structures acting as soil degradation measures.</p>
</sec>
<sec sec-type="COI-statement" id="s11">
<title>Conflict of interest</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
</sec>
<sec sec-type="disclaimer" id="s12">
<title>Publisher&#x2019;s note</title>
<p>All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.</p>
</sec>
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