Feasibility of metal (loid) phytoextraction from polluted soils: the need for greater scrutiny污染土壤中金属（类金属）植物提取的可行性：需要更严格的审视

Points of Reference are part of a regular series intended to address emerging or controversial topics of interest to the scientific community.

Alexander Neaman,^a,* Brett Robinson,^b Tatiana M. Minkina,^c Kooichi Vidal,^d Michel Mench,^e Yurii A. Krutyakov,^f,g and Olga A. Shapoval^h

^aInstituto de Ingeniería Agraria y Suelos, Facultad de Ciencias Agrarias y Alimentarias, Universidad Austral de Chile, Valdivia, Chile ^bSchool of Physical and Chemical Sciences, University of Canterbury, Christchurch, New Zealand ^cAcademy of Biology and Biotechnology, Southern Federal University, Rostov‐on‐Don, Russian Federation ^dEscuela de Agronomía, Pontificia Universidad Católica de Valparaíso, Quillota, Chile ^eUniversity of Bordeaux, INRAE, BIOGECO, Pessac, France ^fNational Research Center Kurchatov Institute, Moscow, Russia ^gDepartment of Chemistry, Lomonosov Moscow State University, Moscow, Russia ^{hPryanishnikov} All‐Russian Scientific Research Institute of Agrochemistry, Moscow, Russia

^a智利瓦尔迪维亚，智利南方大学农业与食品科学学院农业工程与土壤研究所（Instituto de Ingeniería Agraria y Suelos, Facultad de Ciencias Agrarias y Alimentarias, Universidad Austral de Chile）；^b新西兰基督城，坎特伯雷大学物理与化学科学学院；^c俄罗斯联邦顿河畔罗斯托夫，南方联邦大学生物学与生物技术学院；^d智利基约塔，瓦尔帕莱索天主教大学农学院（Escuela de Agronomía, Pontificia Universidad Católica de Valparaíso）；^e法国佩萨克，波尔多大学，INRAE，BIOGECO；^f俄罗斯莫斯科，国家研究中心库尔恰托夫研究所；^g俄罗斯莫斯科，莫斯科国立罗蒙诺索夫大学化学系；^h俄罗斯莫斯科，普里亚尼什尼科夫全俄农业化学科学研究所

The goal of phytoextraction is to remove contaminants—for example, metal(loid)s—from polluted soils through root uptake and accumulation in the harvested plant parts. Many articles propound phytoextraction as a low‐cost means of cleaning up such polluted soils. However, if legislation is based on total soil metal(loid) concentrations, phytoextraction is generally infeasible because of unrealistically long time frames required for success in this process (Robinson et al. 2015).

植物提取的目标是通过植物根系吸收并在收获部位中累积，从污染土壤中去除污染物（例如金属及类金属）。许多文章将植物提取宣扬为清理此类污染土壤的一种低成本手段。然而，如果法规以土壤金属（类金属）总量为依据，植物提取通常并不可行，因为该过程取得成效所需的时间长得不切实际（Robinson et al. 2015）。

Nevertheless, articles on phytoextraction continue to appear in scientific journals, although few contain any calculations showing the likely time span and mass balance of the metal(loid)s in the soil–plant system. As of April 2020, there were approximately 4000 and 12 500 articles in the Web of Science database containing the words “phytoextraction” and “phytoremediation,” respectively, in the title, abstract, or keywords. Only 227 of them contained the abbreviations “g” or “kg” and “ha⁻¹” or “hectare” or “ac⁻¹” or “acre” (or “g/ha” or “kg/ha” or “g/ac” or “kg/ac”) in their abstracts, despite these units being the primary measures for assessing metal phytoextraction rate. Likewise, only 87 of them contained the term “mass balance” in their abstracts. It is likely that the bulk of publications on phytoextraction are authored by academic researchers with limited specific industry experience. On the other hand, industry scientists who ask themselves the right questions and find the right answers through their practical work in remediating polluted sites may be less likely to publish the results of their studies. Therefore, the mostly perfunctory allusions to phytoextraction may cause some researchers to overlook any article with words relating to “phyto” technologies in the title.

尽管如此，有关植物提取的文章仍不断见诸科学期刊，但其中鲜有文章给出任何计算，以说明土壤–植物系统中金属（类金属）可能所需的时间跨度及其质量平衡。截至2020年4月，Web of Science数据库中标题、摘要或关键词含有“phytoextraction”（植物提取）和“phytoremediation”（植物修复）的文章分别约有4000篇和12 500篇。其中仅有227篇在摘要中包含缩写“g”或“kg”以及“ha⁻¹”或“hectare”或“ac⁻¹”或“acre”（或“g/ha”“kg/ha”“g/ac”“kg/ac”），尽管这些单位是评估金属植物提取速率的主要度量。同样，其中仅有87篇在摘要中包含“mass balance”（质量平衡）一词。植物提取相关出版物的大部分很可能由缺乏具体行业经验的学术研究人员撰写。另一方面，那些在污染场地修复的实际工作中提出正确问题并找到正确答案的行业科学家，发表其研究成果的可能性或许较低。因此，对植物提取大多流于形式的提及，可能导致部分研究人员忽视任何标题中含有“phyto”（植物）类技术相关词语的文章。

* Address correspondence to alexander.neaman@gmail.com Published online 27 May 2020 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/etc.4787

Table 1 illustrates cleanup time‐scale calculations required to achieve a 50% reduction in total soil metals assuming a constant rate over time. For instance, Sauropus androgynus may be useful in cleaning up Zn from soils within a reasonable time span, that is, within less than one human generation of <25 yr (Xia et al. 2013). However, it would take >1000 yr to clean up Pb using this plant species. Meanwhile, chelate‐enhanced phytoextraction, where chelating agents such as ethylenediaminetetraacetic acid are added to the soil to increase plant‐metal uptake, can reduce cleanup time in some cases. However, such chelate application almost invariably leads to groundwater contamination, unless carried out ex situ or in arid areas (Nowack et al. 2006). Although biodegradable chelating agents (e.g., methylglycinediacetic acid) may reduce metal leaching, they are expensive and still require impractically long times for cleanup (González et al. 2014).

表1列出了在假定速率随时间保持恒定的条件下，使土壤金属总量降低50%所需清理时间尺度的计算结果。例如，Sauropus androgynus可用于在合理的时间跨度内（即不到一代人的时间，<25 yr）清除土壤中的Zn（Xia et al. 2013）。然而，使用该植物清除Pb则需要>1000 yr。与此同时，螯合剂强化植物提取（即向土壤中添加乙二胺四乙酸等螯合剂以提高植物对金属的吸收）在某些情况下可缩短清理时间。然而，除非在异位或干旱地区实施，此类螯合剂的施用几乎无一例外地会导致地下水污染（Nowack et al. 2006）。可生物降解的螯合剂（如甲基甘氨酸二乙酸）虽可减少金属淋溶，但价格昂贵，且清理所需时间仍长得不切实际（González et al. 2014）。

Moreover, this extraction rate decreases as bioavailable soil metal declines, which may double the phytoextraction time. Another factor increasing the phytoextraction time is the spatial variability of contaminants on sites. Furthermore, high metal concentrations in soil are likely to be associated with the formation of precipitates that are not readily bioavailable or easily dissolved, particularly in the long term, which is highly relevant in the context of this article. It is for this reason that Swiss soil protection laws, to give but one example, account for both total and labile (salt‐extractable) soil metals. When the primary goal is to phytoextract only labile metal(loid) fractions, that is, bioavailable contaminant stripping (BCS), phytoextraction may be appropriate owing to a short time span of only a few years (e.g., Herzig et al. 2014).

此外，这一提取速率会随土壤中生物有效态金属的减少而下降，这可能使植物提取时间延长一倍。另一个延长植物提取时间的因素是场地内污染物的空间变异性。再者，土壤中高浓度金属很可能伴随着沉淀物的形成，这些沉淀物不易被生物利用或溶解，尤其是在长期尺度上，而这与本文的讨论高度相关。正因如此，以瑞士土壤保护法为例，其同时考虑土壤金属总量和活性态（盐提取态）金属。当主要目标仅为植物提取活性态金属（类金属）组分，即生物有效态污染物剥离（BCS）时，由于所需时间跨度仅为数年，植物提取可能是适宜的（例如Herzig et al. 2014）。

^aSoil bulk density was assumed to be 1200 kg m−3. ^bAssumed value. ^cFor aboveground biomass.

^a假定土壤容重为1200 kg m−3。^b假定值。^c针对地上部生物量。

Yet studies on the efficiency of phytoextraction at reducing available soil metal(loid)s are scarce. So far, few have reported the phytoextraction rate of bioavailable soil metal(loid)s, and thus, we were unable to include it in Table 1. Mench et al. (2018) reported that the annual shoot Cu removal ranged from 2.6 to 9% of 1 M NH4NO3‐ extractable topsoil Cu. Thus, approximately 5 to 20 yr will be required to halve bioavailable topsoil Cu, which is more feasible than the timeline to halve total topsoil Cu (Table 1). Determining the role of phytoextraction for BCS is complicated by other rhizosphere processes that affect bioavailability, such as changes in pH and organic carbon. A key aspect of BCS is to determine the factors affecting the replenishment of the labile pool of the targeted metal(loid)s. Metal phytotoxicity and uptake might depend on both bioavailable and total soil metal pools that are capable of supplying metal to the soil solution at the same time as plant roots take up ions (e.g., Lillo et al. 2020).

然而，关于植物提取降低土壤有效态金属（类金属）效率的研究十分匮乏。迄今为止，报道土壤生物有效态金属（类金属）植物提取速率的研究很少，因此我们未能将其纳入表1。Mench et al. (2018) 报道，地上部每年移除的Cu占表土1 M NH4NO3可提取态Cu的2.6%至9%。据此，使表土生物有效态Cu减半约需5至20 yr，这比使表土Cu总量减半的时间更为可行（表1）。由于存在影响生物有效性的其他根际过程（如pH和有机碳的变化），确定植物提取在BCS中的作用较为复杂。BCS的一个关键方面在于确定影响目标金属（类金属）活性库补给的因素。金属的植物毒性及吸收可能同时取决于土壤中生物有效态金属库和总金属库，二者均能在植物根系吸收离子的同时向土壤溶液供给金属（例如Lillo et al. 2020）。

For applying the BCS concept in practice, there must be support from legislation in countries where laws governing mandatory threshold values are still based solely on total soil metal(loid)s, rather than bioavailable pools. Globally, the risk‐ intolerant contaminated land management approach based on total metals (which often necessitates exhaustive remediation) is being gradually replaced by the concept of risk‐based sustainable land management (Reinikainen et al. 2016). Currently, the most advanced soil remediation frameworks are considering site‐specific risk‐based assessment of pollutant linkages and future land use, rather than promoting legislation based only on mandatory threshold values. For instance, site‐specific assessment using leafy and root vegetables can be carried out. If metal(loid) concentrations in edible parts of vegetables are below the threshold values, there might be no need to remediate this soil. However, vegetable consumption rate and other exposure pathways (e.g., incidental soil ingestion) also should be considered in human health risk assessment (e.g., Lizardi et al. 2020).

要在实践中应用BCS概念，在那些强制性阈值法规仍仅以土壤金属（类金属）总量而非生物有效态库为依据的国家，必须获得立法层面的支持。在全球范围内，基于金属总量、对风险零容忍的污染土地管理方法（通常需要彻底修复）正逐渐被基于风险的可持续土地管理理念所取代（Reinikainen et al. 2016）。目前，最先进的土壤修复框架考虑的是针对污染物暴露链接与未来土地利用的场地特异性风险评估，而非推行仅以强制性阈值为依据的立法。例如，可利用叶菜类和根菜类蔬菜开展场地特异性评估。若蔬菜可食部分中的金属（类金属）浓度低于阈值，则可能无需修复该土壤。然而，在人体健康风险评估中还应考虑蔬菜消费量及其他暴露途径（如无意摄入土壤）（例如Lizardi et al. 2020）。

Practical phytoextraction research has been incorporated into the concept of phytomanagement, which includes growing nonfood crops on contaminated soils to source biomasses for various bioeconomy sectors, such as bioenergy, biofuels, timber, fiber, ecomaterials, green chemistry, and essential oils (Mench et al. 2018). Likewise, phytomanagement can change the composition and structure of microbial communities, thus restoring soil ecological functions (Burges et al. 2020).

实际的植物提取研究已被纳入植物管理的概念之中，其内容包括在污染土壤上种植非食用作物，为生物能源、生物燃料、木材、纤维、生态材料、绿色化学和精油等各类生物经济部门提供生物质来源（Mench et al. 2018）。同样，植物管理可改变微生物群落的组成与结构，从而恢复土壤生态功能（Burges et al. 2020）。

The current challenge is how to bridge plant biomass production for the purposes of financial returns with the remediation of contaminated soils in a feasible time span. There is a need to integrate metal(loid) phytoextraction into the concepts of BCS and phytomanagement. Furthermore, it should be noted that contaminated soil can hinder plant biomass production. Therefore, finding plants with both economic value and capacity to tolerate high metal exposure is important.

当前面临的挑战是如何将以获取经济回报为目的的植物生物质生产与在可行时间跨度内修复污染土壤相结合。有必要将金属（类金属）植物提取纳入BCS和植物管理的概念之中。此外，应当注意的是，污染土壤可能会阻碍植物生物质的生产。因此，寻找既具有经济价值、又能耐受高金属暴露的植物十分重要。

In summary, we encourage authors, reviewers, and editors to be more stringent with phytoextraction articles, demanding that they include information on metal(loid) phytoextraction rates to reach an acceptable level of residual risks in a site‐ specific risk‐based assessment of pollutant linkages according to future land use.

综上所述，我们鼓励作者、审稿人和编辑对植物提取类文章采取更为严格的标准，要求其提供金属（类金属）植物提取速率的相关信息，以便在依据未来土地利用、针对污染物暴露链接开展的场地特异性风险评估中，使残余风险达到可接受水平。

Acknowledgment—Article writing was partially funded by the Ministry of Science and Higher Education of the Russian Federation as part of the state assignment in the field of scientific activity No. 0852‐2020‐0029. The research team also acknowledges A. Tchourakov for commenting on, editing, and proofreading the article.

致谢——本文的撰写部分得到俄罗斯联邦科学与高等教育部科学活动领域国家任务（编号0852‐2020‐0029）的资助。研究团队亦感谢A. Tchourakov对本文提出意见并进行编辑和校对。

Data Availability Statement—For further information, please contact the corresponding author (alexander.neaman@ gmail.com).

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