Victor Hugo Cruz1
Henzo Henrique Simionatto2Emanuella Roberto Ribeiro3
Yanca Araujo Frias1Thalia Silva Valério1
Paulo Renato Matos Lopes1*- 1College of Agricultural and Technological Sciences, São Paulo State University (UNESP), Dracena, SP, Brazil
- 2Institute of Science and Technology, São Paulo State University (UNESP), Sorocaba, SP, Brazil
- 3Institute of Biosciences, Languages and Exact Sciences, São Paulo State University (UNESP), São José do Rio Preto, Brazil
The widespread and indiscriminate use of pesticides in modern agriculture has caused severe environmental contamination, significantly affecting terrestrial and aquatic ecosystems and non-target organisms. To meet this challenge, it is necessary to improve bioremediation techniques such as phytoremediation, bioaugmentation, biostimulation, and vermiremediation. The key findings highlight the synergistic potential of combining these approaches to accelerate pesticide degradation and improve remediation outcomes. Plant families such as Fabaceae and Poaceae have demonstrated significant ability for phytoremediation, with species such as Canavalia ensiformis and Zea mays excelling in the remediation of herbicides and insecticides. Microbial genera such as Bacillus, Pseudomonas, and Streptomyces play a key role as essential contributors to the degradation process, particularly when associated with plants. The integration of organic additives, such as vinasse, further improves the interactions between plants, microbes, and soil fauna, increasing the efficiency of remediation. In addition, the role of vermiremediation using earthworms such as Eisenia foetida to improve soil aeration and microbial activity has received attention. Therefore, approaches combining phytoremediation with bioaugmentation, biostimulation, and vermiremediation could offer a scalable and sustainable pathway to accelerate pollutant degradation, restore soil health, and promote agricultural sustainability. Future research should focus on the optimization of these techniques, the exploration of genetic advances to enhance microbial and plant remediation capabilities, and the assessment of their feasibility at a global scale. These efforts are vital for mitigating the environmental impacts of pesticides and for promoting a more resilient agricultural system.
Introduction
Environmental pesticide contamination is one of the most challenging issues in modern agriculture, resulting in negative impacts on the aquatic and terrestrial ecosystems (Mendes et al., 2021). The continuous and indiscriminate use of pesticides for the control of plant pests and diseases can result in long-term harmful effects. These compounds can persist in the environment, affecting non-target organisms (Wan et al., 2025). In view of these impacts, there is a growing need for effective and sustainable remediation solutions to minimize environmental damage and ensure ecotoxicological and food security.
A sustainable alternative is phytoremediation, a remediation technique based on the use of plants to stabilize (Teófilo et al., 2020), metabolize (Aguiar et al., 2020), and accumulate (Akpinar et al., 2021) pesticides present in the soil. This technique stands out due to its low cost, its ease of application in large areas, and its potential for environmental recovery without the invasive effects of chemical or mechanical techniques. In addition, phytoremediation contributes to the maintenance of local biodiversity and can be integrated into agricultural production systems while preserving productive land use (Conciani et al., 2023).
However, phytoremediation has certain significant limitations. The time required for plants to be able to remediate the soil to safe levels can be prolonged, especially in areas with elevated levels of contamination (Solá et al., 2021). In addition to the time requirement, phytoremediation also faces other relevant limitations. The efficiency of contaminant removal is often dependent on pollutant specificity as not all compounds are equally bioavailable or degradable by plants (Aryal, 2024; Susarla et al., 2002). Furthermore, exposure to high contaminant concentrations can induce plant stress, reducing the growth and remediation capacity (Frias et al., 2023). Climatic factors such as temperature, rainfall, and soil moisture also play a decisive role as they can limit plant development and microbial interactions, thereby affecting the remediation outcomes (Oishy et al., 2025). These limitations imply the need to integrate other complementary techniques that can increase the speed and effectiveness of the remediation process under adverse conditions.
Strategies such as bioaugmentation, biostimulation, and vermiremediation have emerged as complementary approaches to enhancing the efficiency of phytoremediation in soils contaminated by pesticides. Bioaugmentation involves the introduction of specialized microorganisms capable of degrading specific contaminants (Giaccio et al., 2023). These microorganisms, when added to the soil, accelerate the process of decomposition of pesticides, allowing plants to reduce the toxic load of the environment in less time (Tripathi et al., 2021).
Biostimulation, in turn, aims to promote the growth and activity of native microorganisms through the addition of nutrients or compounds that stimulate the degradation of contaminants (Ferreira et al., 2021). This method does not add new organisms to the soil, but by providing stimulating substances, it favors the fauna and flora, improving the degradation ability of pesticides (Xu et al., 2019; Raimondo et al., 2020; Ataikiru and Ajuzieogu, 2023).
Another relevant complementary method is vermiremediation (Lacalle et al., 2020), which uses organisms such as earthworms to improve the soil structure and increase the natural microbiota. Earthworms create tunnels that improve soil oxygenation and contribute to the degradation of pesticides as they transport microorganisms in their daily activities, helping in the decomposition of contaminants and providing a constructive collaboration with plants in remediation.
The combination of these techniques—bioaugmentation, biostimulation, and vermiremediation—with phytoremediation can enhance the efficiency of remediation processes, representing a multifunctional and integrated approach. Each of these strategies complements phytoremediation, adding benefits such as faster contaminant degradation and an increased effectiveness in areas that are difficult to access or have elevated levels of contamination (Mielke et al., 2020; Lacalle et al., 2020).
The present systematic review aimed to compile and analyze the data on the efficiency and applicability of the combination of phytoremediation, bioaugmentation, biostimulation, and vermiremediation. By reviewing the body of available studies, this paper aimed to determine the conditions under which each combination is most effective and the potential challenges and limitations of these strategies. This will advance the understanding of the best practices for pesticide remediation in various scenarios and crops, contributing to the development of sustainable and low-cost solutions for agriculture and environmental preservation.
Despite the progress in understanding individual phytoremediation strategies, a major knowledge gap remains with regard to comparative analyses of their integration with complementary biological approaches. This review specifically addresses this gap by systematically evaluating and contrasting the different combinations of phytoremediation, bioaugmentation, biostimulation, and vermiremediation, providing insights into their relative efficiencies and practical applicability.
Methodology
The method for data extraction and the creation of the database followed the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) protocol (Tricco et al., 2018). A systematic literature search was conducted in the Scopus database (2014–2024) to discover studies on pesticide-contaminated soil remediation, focusing on phytoremediation combined with other biological methods. All articles were retrieved via CAPES Institutional Access. The search strategy, detailed below, was structured to discover studies on the remediation of soils contaminated with various pesticides, focusing on phytoremediation associated with other biological remediation methods:
“soil” AND (“pesticid*” OR “herbicid*” OR “fungicid*” OR “insecticid*” OR “acaricid*” OR “nematicid*”) AND (“phytorem*” OR “phytovolati*” OR “phytodegrad*” OR “phytostabili*” OR “rhizostabili*” OR “phytoextract” OR “phytofiltrat*” OR “rhizodegrad*”) AND (“enrich*” OR “stimulat*” OR “augment*” OR “microbial bior*” OR “bacter*” OR “fung*” OR “mycoremed*” OR “inocul*” OR “microorg*” OR “worm*” OR “vermiremed*”) AND NOT (“rhizofiltrat*” OR “electr*” OR “water*” OR “aquatic*” OR “wetland*” OR “hydrop*” OR “mulch*” OR “alg*” OR “phycoremed*” OR “metal*” OR “PAH” OR “antibiotic” OR “add” OR “*char*” OR “*sor*” OR “organic amend*” OR “add” OR “attenuat*” OR “surfact*” OR “parasiticid*”)
The search strategy employed multiple operators, each defined and explained below:
a. Wildcard operator (*): This allows finding variations in the terms used in agriculture and other contexts.
b. AND: This serves to combine two or more terms and narrow the search as it requires that all terms connected by the AND appear in the results. This means that each returned article must have all the terms linked by AND.
c. AND NOT: This excludes articles that deal with unwanted areas. These terms help refine the search and drop studies not aligned with the research focus.
d. OR: This expands the search as it allows any of the terms connected by the OR to appear in the results. It is useful when there are synonyms or related terms because the OR shows that the presence of at least one of the terms is enough.
Following the database search (Figure 1), 42 potentially relevant articles were identified. After screening of the title and abstract and application of the predefined eligibility criteria, 22 articles that did not address bioremediation of pesticide-contaminated soils or failed to meet methodological requirements were excluded. Consequently, 20 articles proceeded to full-text assessment and were retained. In parallel, a snowballing screening (reference tracking) was applied to the initially included studies, which resulted in 372 additional records. After duplicate removal and screening based on PEAK (Population, Exposure, Assessment, Knowledge) adequacy, data completeness, and minimal risk of bias, 303 articles were excluded, leaving 69 eligible studies. Therefore, a total of 89 studies were included in this systematic review, comprising 20 from the database search and 69 retrieved through snowballing.
Figure 1. Flowchart of the article selection process for the systematic review on the associations between the biological remediators of pesticides in agricultural soils. Based on the PRISMA protocol, which illustrates the stages of identification, screening, eligibility, and inclusion of studies, indicating the numbers of articles retrieved, excluded, and included in the final analysis.
It should be emphasized that all Supplementary Materials included in this study provide an expanded and detailed view of the database compiled for systematic review. Each Supplementary Table addresses a specific analytical dimension of pesticide bioremediation, ensuring data transparency and reproducibility. Supplementary Table S1 presents a global overview of the soil textures and references in studies on biological approaches for pesticide remediation. It compiles information from multiple countries and soil types (e.g., clayey, loamy, and sandy), linking these environmental characteristics to the experimental studies evaluated. This table enables comparative assessment of the influence of soil on the remediation outcomes. Supplementary Table S2 summarizes the environmental persistence, toxicological hazards, and regulatory status of key pesticides. It includes data on the soil half-life, acute and chronic mammalian toxicity, and regulatory information gathered from international organizations. This table provides the toxicological foundation supporting the discussion of pesticide risks and their management. Supplementary Table S3 compiles the phytoremediation efficiency data for a wide range of plant species and pesticide types. It details the removal percentages, the phytoremediation mechanisms (e.g., rhizodegradation, phytostabilization, and phytoaccumulation), and the associated references, providing a consolidated view of plant performance across studies. Supplementary Table S4 details the synergistic plant–microbe systems for enhanced pesticide bioremediation. It lists combinations of plant species and microbial taxa (e.g., bacteria, fungi, and lichens) that have demonstrated cooperative effects in contaminant removal. This table emphasizes the role of microbial symbioses—such as those involving Bacillus, Pseudomonas, Streptomyces, and Sphingobium—in boosting the degradation rates and ecological resilience. Supplementary Table S5 addresses enhanced phytoremediation through soil amendments and plant growth regulators. It includes data on the use of organic amendments (e.g., vinasse, compost, and other conditioners) and hormonal stimulants that promote pesticide degradation and plant vitality. This dataset supports the discussion on biostimulation and soil fertility improvement as complementary remediation strategies. Supplementary Table S6 compiles studies on integrated plant–microbe–earthworm systems, representing a multifunctional remediation approach that combines phytoremediation, bioaugmentation, and vermiremediation. It reports the removal percentages, the involved species, and the types of bioremediation mechanisms observed, showcasing the synergistic role of earthworms (Eisenia foetida) in improving soil aeration and microbial activity.
Together, these six supplementary materials constitute a comprehensive repository that links the cited literature to the datasets analyzed in this systematic review. They collectively illustrate the diversity of the bioremediation strategies investigated—ranging from plant-based to integrated multi-organism systems—and provide a valuable reference framework for future studies aiming to optimize sustainable pesticide remediation in agricultural soils.
Regulatory frameworks and guideline documents from international agencies have established standardized procedures for pesticide risk assessment, environmental monitoring, and ecotoxicological testing (FAO, OECD, EPA, ECHA, EFSA, WHO). In parallel, a broad range of experimental and modeling approaches has been applied to evaluate pesticide behavior, soil–plant interactions, and ecological impacts, including multivariate statistical methods, neural network–based analyses, and bioassays (Bai et al., 2015; Belouchrani et al., 2016; Dubey et al., 2014; Dash and Osborne, 2020; Qin et al., 2014; Gotelli et al., 2023). Previous studies have further demonstrated the relevance of integrated ecotoxicological assessments in contaminated soils and agroecosystems, emphasizing plant responses, residue dynamics, and remediation strategies (Alvarez et al., 2022; Barroso et al., 2022; Cabral et al., 2017; Campos et al., 2017; Erinle et al., 2016; Fiore et al., 2016, 2019; Lin et al., 2018; Madariaga-Navarrete et al., 2017; Marihal et al., 2014; Mierzejewska et al., 2022; Nurzhanova et al., 2021; Pino et al., 2016; Prado et al., 2014; Rainbird et al., 2018; Ramborger et al., 2017; Rissato et al., 2015; San Miguel et al., 2014; Sauvêtre and Schröder, 2015; Singh et al., 2019; Urbaniak et al., 2016, 2019; Wyrwicka et al., 2014, 2019). All studies used to construct the supplementary datasets (Tables S1–S6), including those contributing exclusively to data compilation and comparative analyses, are cited collectively here (Alvarez et al., 2022; Bai et al., 2015; Barroso et al., 2022; Belouchrani et al., 2016; Cabral et al., 2017; Campos et al., 2017; Dash and Osborne, 2020; Dubey et al., 2014; ECHA; EFSA; EPA; FAO; Ferreira et al., 2019; Fiore et al., 2016, 2019; Gotelli et al., 2023; Houjayfa et al., 2020; Lin et al., 2018; Madariaga-Navarrete et al., 2017; Marihal et al., 2014; Mierzejewska et al., 2022; Mitton et al., 2016a, b; Nurzhanova et al., 2021; OECD; Passos et al., 2019; Pino et al., 2016; Prado et al., 2014; Qin et al., 2014; Rainbird et al., 2018; Ramborger et al., 2017; Rani et al., 2021; Rissato et al., 2015; San Miguel et al., 2014; Santos et al., 2024; Sauvêtre and Schröder, 2015; Singh et al., 2019; Singh and Singh, 2014; Somtrakoon et al., 2024; Urbaniak et al., 2016, 2019; WHO; Wyrwicka et al., 2014, 2019).
Results and discussion
Phytoremediation
The families Fabaceae (legumes) and Poaceae (grasses) stand out, with 17 and 16 studies found, respectively (Figure 2A). Together, they make up more than 50% of the families surveyed, showing enormous potential for phytoremediation. Legumes are known for their ability to fix atmospheric nitrogen, enriching the soil and promoting the growth of other plants (Teófilo et al., 2020). This characteristic, combined with their interactions with microorganisms, makes them promising candidates for pesticide degradation. Grasses, in turn, stand out for their robustness, fast growth, and extensive root system (Nascimento et al., 2015). These characteristics ease soil stabilization, as well as water and nutrient absorption, and promote pesticide degradation (Sánchez et al., 2017).
Figure 2. Main plant groups used in the phytoremediation of pesticides in agricultural soils. Distribution of botanical families and plant species most frequently reported in pesticide phytoremediation studies. (A) Most frequently reported botanical families. (B) Most investigated plant species.
Beyond the Fabaceae and Poaceae families, Asteraceae and Brassicaceae also stand out, with five studies, followed by Cucurbitaceae (four studies) and Anacardiaceae (three studies) (Figure 2A). Although fewer in number, these families also contribute significantly to phytoremediation. Brassicaceae, for example, is known for its ability to hyperaccumulate or degrade organic compounds, such as pesticides (Azab et al., 2016). On the other hand, the Asteraceae, with its adaptable root system, is efficient in absorbing contaminants, in particular in heterogeneous soils (Santos et al., 2018).Furthermore, the presence of such diverse botanical families, such as Cucurbitaceae and Anacardiaceae, indicates the wide range of physiological and biochemical strategies employed by plants in phytoremediation.
However, the less studied families, including Bignoniaceae, Burseraceae, Clusiaceae, and Euphorbiaceae, represent a promising field of research. These families may harbor species with unique characteristics that make them highly efficient in the phytoremediation of distinct types of contaminants. More in-depth investigations into the physiology, genetics, and ecology of these plants may be key to unlocking their potential and to developing new strategies for the recovery of degraded areas.
On plant species, Canavalia ensiformis appears to be the most promising for the phytoremediation of soils contaminated by pesticides, being the subject of seven studies (Figure 2A). Several studies have shown that this species is capable of remediating soils contaminated with sulfentrazone (Belo et al., 2016; Ferraço et al., 2019; Madalão et al., 2017; Melo et al., 2017; Madalão et al., 2016), tebuthiuron (Mendes et al., 2021), diuron (Teófilo et al., 2020), hexazinone (Teófilo et al., 2020), and sulfometuron-methyl (Teófilo et al., 2020). According to these authors, the adaptation of the vascular and physiological system of C. ensiformis directly contributes to the absorption, translocation, and degradation of these pesticides. Moreover, this plant harbors rhizosphere microorganisms capable of fixing atmospheric nitrogen and adding carbon to the soil, which is essential to increasing pesticide removal, thus contributing to the sustainability of agricultural systems (Teófilo et al., 2020).
Other species with significant potential in phytoremediation are Raphanus sativus, Urochloa brizantha, and Zea mays, each with four studies in its history (Figure 2B). Chlorosis has been observed in studies, and R. sativus stands out for its ability to bioaccumulate chlorimuron-ethyl, sulfometuron-methyl, and atrazine (Galon et al., 2017). On the other hand, U. brizantha, a forage species, has been shown to be effective in the phytoremediation of soils contaminated with picloram (Franco et al., 2016, 2015) and can certainly reduce the risk of environmental contamination (Souza et al., 2017). In a pasture area, Passos et al. (2018) noted that the half-life of picloram in the presence of U. brizantha was reduced after 100 days of cultivation. Z. mays, in turn, is a commercial species used in phytoremediation studies due to its high biomass and pesticide removal ability. Based on the results of some studies, Z. mays is a suitable candidate for the phytoremediation of soils contaminated with endosulfan and its metabolite (endosulfan sulfate) (Somtrakoon et al., 2014), lindane and chlordecone (Blondel et al., 2017), atrazine (Sánchez et al., 2017), and picloram (Souza et al., 2017). According to these authors, the presence of these pesticides did not inhibit plant growth or development, indicating high plant tolerance. Furthermore, the plant rhizosphere has been shown to stimulate the rhizodegradation of pesticides through distinct mechanisms such as co-metabolism, increased bioavailability, and improved soil aeration (Blondel et al., 2017).
The diversity of plant species with potential for phytoremediation is remarkable, with emphasis on Caesalpinia ferrea, Inga marginata, Crotalaria spectabilis, Cucumis sativus, Cucurbita moschata, Solanum lycopersicum, Glycine max, and Panicum maximum, each with three studies in its history (Figure 2B).
The presence of commercial species in the majority of phytoremediation studies shows enormous potential for the integration of this technology in agricultural systems. These species, in addition to their productivity and economic value, have proven their ability to decontaminate soils, promoting environmental sustainability and the economic viability of agricultural production. The use of forage, for example, allows the recovery of degraded areas and the production of forage simultaneously (Galon et al., 2017).
The class of pesticides most often addressed in phytoremediation studies is herbicides, which appear in 27 studies (Figure 3A). Herbicides predominate due to their frequent annual application in agriculture, more so than other pesticide classes, which is driven by the need for continuous weed control (Conciani et al., 2023). Therefore, agricultural soils often have prominent levels of herbicide contamination, which makes them a priority in research aimed at environmental remediation (Aguiar et al., 2020). The focus on herbicides shows that their environmental impact is a central concern, particularly due to their high persistence and frequent application in agricultural practices.
Figure 3. Classes and active ingredients of the pesticides evaluated in phytoremediation studies. Profile of the most studied classes of pesticides and active ingredients in phytoremediation strategies. (A) Distribution of pesticide classes. (B) Most investigated active ingredients.
A notable gap was identified with regard to the remediation of fungicides and nematicides. Their low representation in the analyzed literature underscores a significant area for future research, as the environmental persistence and toxicity of these compounds also pose a substantial risk to soil health.
Insecticides, although appearing in smaller quantities, with 11 studies, are also relevant in the context of phytoremediation (Figure 3A). The application of pesticides in agriculture—including organophosphates and carbamates—leads to frequent soil contamination (Mitton et al., 2018). Multifunctional formulations appear in six studies (Figure 3A), highlighting their use in single treatments targeting fungi, insects, and weeds (Clostre et al., 2014; Létondor et al., 2015; Blondel et al., 2014). The smaller number of studies on these pesticides indicates that their use in phytoremediation experiments is more specific or less frequent compared with herbicides and insecticides. Although herbicides are more studied, it is critical that the remediation of multifunction insecticides and pesticides also receive more attention in research. This is because these pesticides can have significant adverse effects on human health and biodiversity, highlighting the need to scale-up research in this area.
The frequent mention of picloram and atrazine in the reviewed studies (n = 7) (Figure 3B) underscores their importance in phytoremediation research. Given their extensive use and environmental persistence, these herbicides are among the most relevant targets of soil remediation strategies.
2,4-Dichlorophenoxyacetic acid (2,4-D), often six, is also a widely used herbicide known for its historical use and the environmental risks associated with its application (Figure 3B). Its presence in multiple studies reinforces the concern with the impacts it can have on the environment and the search for remediation solutions.
Sulfentrazone and lindane, with frequency five, represent a focus on compounds that are more persistent and toxic to soil organisms (Figure 3B). Lindane is an organochlorine of great environmental concern due to its toxicity and persistence (Blondel et al., 2017). On the other hand, sulfentrazone, a more modern herbicide, has also been the subject of recent studies for its mobility in the soil and its impacts on non-target organisms (Ferraço et al., 2019).
Chlordecone (four studies), dichloro-diphenyl-trichloroethane (DDT; three studies), and endosulfan, dieldrin, endosulfan sulfate, sulfometuron-methyl, and tebuthiuron (all with two studies each) complete the list. These pesticides, for the most part, are persistent in the environment and, in some cases, are prohibited or restricted, such as DDT (Mitton et al., 2018, 2014; Mitton et al., 2016a, b) and chlordecone (Clostre et al., 2014; Létondor et al., 2015; Blondel et al., 2014). Their long-lasting effects on the soil and biota call for further studies in search of more effective remediation methods.
Table 1 and Figures 4, 5 display the interactions between the various plant families and pesticides used in phytoremediation studies. Table 1 shows three plant families used in phytoremediation studies of chlordecone-contaminated soils (multiple functions).
Table 1. Plant families used in phytoremediation studies in multifunction pesticide-contaminated soils.
Figure 4. Studies on pesticides in integrated phytoremediation and bioaugmentation systems. Classes of pesticides and active ingredients most frequently found in studies involving phytoremediation and bioaugmentation. (A) Most frequently investigated pesticide classes. (B) Most studied active ingredients.
Figure 5. Sankey diagram of the interactions between various plant families and the insecticides used in phytoremediation and bioaugmentation studies. This illustrates, for example, the association between Cucurbitaceae and Pseudomonas in the remediation of dichloro-diphenyl-trichloroethane (DDT) and between Poaceae and Streptomyces for lindane.
The Brassicaceae family, present in three studies, stands out as the most used in comparison with other plant families (Table 1). Brassicaceae species have been shown to effectively absorb and accumulate pesticides, justifying their prominent role in phytoremediation studies (Létondor et al., 2015). The Poaceae family, represented in two studies (Table 1), also presents considerable potential for phytoremediation. Although not traditionally associated with the accumulation of persistent organic compounds in the same way as Brassicaceae, their use in phytoremediation is valued for their efficiency in stabilizing contaminated soil, particularly in agricultural settings where pesticides, such as chlordecone, pose a major challenge (Blondel et al., 2014).
In contrast, the Cucurbitaceae family, represented in only one study (Table 1), appears as a less explored possibility in the field of chlordecone phytoremediation. Plants in this family, such as pumpkins and cucumbers, are known for their ability to hyperaccumulate different pesticides (Clostre et al., 2014; Somtrakoon et al., 2014; Mitton et al., 2018; Colin et al., 2024). However, the lower presence of Cucurbitaceae in the literature on chlordecone phytoremediation may reflect a research gap or the limited efficiency of these plants in the uptake of persistent organic compounds. Nevertheless, this underutilization shows an opportunity for future studies as the plants in this family may have untapped potential to remediate organic pollutants, provided that their characteristics receive in-depth investigation.
Figure 6 shows Fabaceae represented by the thickest arrows connecting to multiple herbicides, including sulfentrazone, 2,4-D, and atrazine, indicating its predominant use in phytoremediation studies. On the other hand, other families, such as Poaceae and Brassicaceae, are shown by thinner arrows, indicating that they are less explored in phytoremediation studies, at least in relation to these specific herbicides. The Poaceae family has certain relevant connections, but its application in phytoremediation appears less than that of Fabaceae.
Figure 6. Sankey diagram of the interactions between the various plant families and herbicides used in phytoremediation studies. This shows the strong association of Fabaceae with herbicides such as sulfentrazone, atrazine, and 2,4-dichlorophenoxyacetic acid (2,4-D) and the role of other families such as Poaceae and Brassicaceae in the remediation of multiple herbicides.
The crossed arrows indicate that multiple plant families can remediate the same herbicide, highlighting functional redundancy. For example, Fabaceae and Poaceae both remediate atrazine and 2,4-D—herbicides commonly applied in grain agriculture. Researchers are therefore examining diverse species with varying physiological and biochemical profiles to determine the most efficient phytoremediation strategies.
The use of thicker and longer arrows for certain pesticides, such as sulfentrazone and 2,4-D, represents that these herbicides are widely studied in conjunction with various plant families, which may reflect their high persistence in the soil and the impact they cause on the environment, requiring more research to determine effective decontamination solutions. In contrast, tebuthiuron and picloram show connections with fewer plant families, suggesting that they have received less research focus or have presented fewer challenges in phytoremediation.
As shown in Figure 7, plant families such as Poaceae, Fabaceae, Asteraceae, and Cucurbitaceae exhibit marked differences in their morphological and physiological traits, which directly influence their ability to remove soil contaminants. For example, the Asteraceae family, which includes a wide range of herbaceous plants, also plays a relevant role in pesticide absorption. Due to their high biomass production and their ability to accumulate toxic compounds, species such as Eremanthus crotonoides and Helianthus annuus can be extremely effective for phytoremediation (Santos et al., 2018; Aguiar et al., 2020; Mitton et al., 2014; Mitton et al., 2016a, b; Melo et al., 2017). A clear example of this is the potential of H. annuus in the removal of DDT, a pesticide notoriously persistent in the environment (Mitton et al., 2014). The Sankey diagram can show that certain plants of this family possess greater ability to absorb and degrade this pesticide, suggesting that Asteraceae could be an important component in soil remediation strategies where DDT is a significant problem.
Figure 7. Sankey diagram of the interactions between the various plant families and insecticides used in phytoremediation studies. This highlights the role of Poaceae in the remediation of endosulfan and lindane and of Asteraceae and Cucurbitaceae in the absorption of dichloro-diphenyl-trichloroethane (DDT) and chlordecone.
Analysis of the insecticides represented in the diagram also revealed additional challenges in the phytoremediation process. Compounds such as endosulfan and its derivative, endosulfan sulfate, are known for their high toxicity and persistence in the soil, which makes them particularly difficult to eliminate (Somtrakoon et al., 2014). However, as illustrated in the Sankey diagram, the Poaceae family has a considerable uptake flux of these compounds, while Z. mays (Somtrakoon et al., 2014), Digitaria longiflora, and Vetiveria zizanioides (Singh and Singh, 2014) can reduce the concentration of endosulfan and its derivative from agricultural soils and be accumulated in parts of the plant, such as the leaves, stems, and roots.
Phytoremediation and bioaugmentation
As displayed in Figure 8A, the Poaceae family, with seven studies, is the most representative, followed by the Asteraceae and Cucurbitaceae families, with six studies each. The Fabaceae family has four studies. Although less represented, the Salicaceae family, with two studies, includes the species Salix fragilis.
Figure 8. Main plant groups used in integrated phytoremediation and bioaugmentation systems for the decontamination of soils with pesticides. Botanical families and plant species most used in combined phytoremediation and bioaugmentation systems. (A) Most frequently reported botanical families. (B) Most commonly used plant species.
In Figure 8B, the species Cucurbita pepo, presents six studies. This species has significant potential for the absorption and accumulation of persistent organic pesticides in its vegetative and reproductive parts, as well as in the roots, stems, leaves, petioles, and fruits (Akpinar et al., 2021; Eevers et al., 2018; Akpinar et al., 2022; Eevers et al., 2016). Although this trait supports environmental pesticide removal, it presents a critical challenge for agriculture, given the international distribution and widespread consumption of the fruit, which may compromise public health. However, the use of edible species for phytoremediation requires caution since the bioaccumulation of pesticides in fruits, seeds, or leaves may compromise food safety. This represents a potential route of human exposure if the harvested biomass is consumed, highlighting the importance of restricting such plants to remediation purposes only and ensuring proper post-treatment management (Singh and Singh, 2017). H. annuus has five studies and Z. mays has four. Both H. annuus and Z. mays highlight that it is a workable possibility for the remediation of agricultural soil. Finally, there is C. ensiformis, which has two studies. Although less represented, this species is important for its ability to fix nitrogen, which can improve the soil quality and promote microbial activity, aiding in the degradation of organic contaminants (Melo et al., 2019; Mielke et al., 2020).
Moreover, our analysis of Figure 9A revealed the use of 19 bacterial strains, three lichens, and two fungal species in the included studies.
Figure 9. Main microorganisms used in integrated phytoremediation and bioaugmentation systems for the decontamination of pesticide-contaminated soils. Taxonomic profile and microbial groups most used in integrated phytoremediation and bioaugmentation approaches. (A) Most frequently reported groups of microorganisms. (B) Most investigated microbial genera.
The underutilization of lichens in phytoremediation arises from their symbiotic composition, which requires coordinated interactions between fungi and photosynthetic partners, and the limited research on their remediation capacity (Akpinar et al., 2021). Lichens are known to be an ecological indicator in the identification and monitoring of environmental pollution (Akpinar et al., 2021). In addition, lichen hyphae can absorb and accumulate pollutants not only from the surface (e.g., soil or rock) but also from the atmosphere (Akpinar et al., 2022), which makes them promising for future investigations into their applicability in pesticide-contaminated soils.
As for fungi, their low frequency of use is remarkable. This may be related to the difficulty of supporting fungal cultures or the smaller number of studies focused on this group (Lopes et al., 2022). Therefore, these data suggest an underexplored potential for both fungi and lichens.
Furthermore, analysis of the microbial genera involved in phytoremediation and bioaugmentation for soil decontamination with pesticides highlights the relevance of each group (Figure 9B).
For example, Bacillus, covered by six studies, are endophytic rhizobacteria (which live within plant tissues) that promote plant growth and development. They act in atmospheric nitrogen fixation, phosphorus solubilization, and the synthesis of auxin, cytokinin, and 1-aminocyclopropane-1-carboxylate deaminase (an enzyme that reduces plant stress), among other functions (Rani et al., 2019a). Studies have proven that Bacillus can serve as a bioenhancer in contaminated soils and enhance the degradation of pesticide compounds (Rani et al., 2019b).
Another microbial genus is Peltigera, a lichen with three studies, which reflects the use of symbionts in the decontamination process. Although less studied than the bacterial genera, lichens can accumulate pesticides, as discussed earlier, which makes them useful in bioaccumulation and as a complement to the degradation of persistent organic compounds. In turn, there are Pseudomonas, also with three studies. Similarly to Bacillus, the genus Pseudomonas comprises a group of endophytic bacteria that not only increase plant growth and development but also aid in the remediation of recalcitrant pesticides such as sulfentrazone (Melo et al., 2019, 2018) and dichlorodiphenyldichloroethylene (DDE) (Eevers et al., 2016). Next is the genus Streptomyces, with three studies, which comprises a group of saprophytic actinobacteria abundant in the soil. Its presence contributes both to the control of plant pathogens and the degradation of toxic compounds such as glyphosate (Giaccio et al. (2023) and lindane (Álvarez et al., 2015; Solá et al., 2021).
Finally, there are two studies on endophytic bacteria, i.e., Paenibacillus, Sphingobium, and Sphingomonas. Therefore, the use of distinct types of microorganisms, such as endophytic bacteria, lichens, and other microbial genera, reflects a complementary approach in which natural plant or soil symbionts work in conjunction with microorganisms capable of directly degrading pollutants. The diversity of the microbial genera observed, including the predominance of bacteria such as Bacillus and Pseudomonas, indicates the need for different metabolic functions for the degradation of various classes of pesticides. This constructive collaboration between different organisms, which combines bioaccumulation, as in the case of lichens of the genus Peltigera, and bioaugmentation with highly adaptable and efficient microorganisms, can significantly increase the effectiveness of phytoremediation. Thus, the interaction between these organisms maximizes the use of the available ecological and functional diversity, enhancing strategies ranging from the direct degradation of pollutants to the selective accumulation of toxic compounds.
As shown in Figure 4A, insecticides are the subject of 14 studies on phytoremediation and bioaugmentation compared with seven for herbicides.
This higher prevalence indicates that insecticides, such as organochlorines (e.g., DDT, endosulfan, and lindane) and organophosphates (e.g., monostrophes), are considered significant environmental threats due to their recalcitrance and tendency to bioaccumulate in the food chain, causing serious harm to animal and human health, which justifies the emphasis on finding effective biological solutions.
Herbicides, although less frequent, still constitute a considerable part of the studies. This is due to their extensive use in agriculture, especially in monocultures, the large-scale application of which can result in elevated levels of contamination of the terrestrial and aquatic ecosystems.
In this context, DDT, which is featured in five studies, stands out as a pesticide of significant concern due to its environmental persistence and its toxic effects on aquatic and terrestrial organisms—characteristics previously addressed in this review. There is also endosulfan, with four studies, another important target due to its acute toxicity and potential for bioaccumulation, which are factors mentioned above. Lindane and sulfentrazone, both with three studies, also raise additional concerns. Finally, there is atrazine herbicide, with only two studies.
Figure 5 highlights the prominent role of the Cucurbitaceae family in phytoremediation, which is attributed to its adaptability to soils contaminated with DDT and its metabolite DDE. The application of microbial genera such as Peltigera (lichen), Pseudomonas, and Sphingomonas can enhance the degradation of these toxic compounds. This is reflected in the work by Akpinar et al. (2021), which used the combination of C. pepo and Peltigera canina for the removal of DDT from the soil.
The use of Poaceae species in conjunction with Streptomyces and Sphingobium has been proposed as an effective approach for lindane remediation in agricultural soils. Experimental evidence from Álvarez et al. (2015) and Solá et al. (2021) confirms the efficacy of this strategy, particularly with Z. mays and Streptomyces.
For endosulfan remediation, bacterial genera such as Bacillus and Paenibacillus have been used in association with Asteraceae species, which enhances degradation. In this sense, Rani et al. (2019a) gathered H. annuus plants and Bacillus or Paenibacillus to decontaminate soils with this insecticide.
Furthermore, the symbiotic association of H. annuus with Pseudomonas spp. can be employed for the bioremediation of sulfentrazone (Table 2). Melo et al. (2018) provided proof of the bioremediation of sulfentrazone using Pseudomonas. The Fabaceae family could also be suitable for similar applications. An example of this is the work by Melo et al. (2019), in which the combination of C. ensiformis and Pseudomonas sp. was used to effectively remove sulfentrazone.
Table 2. Quantities of pesticide studies on the association between plant families and microbial genera.
Despite these results, it is important to recognize that the effectiveness of pesticide phytoremediation is dependent not only on the plant–microbe interactions but also on environmental factors such as soil composition and moisture (Tripathi et al., 2021). Moreover, the diversity of plants and microorganisms can increase the efficiency of pesticide removal (Yan et al., 2018).
Phytoremediation and biostimulation
Figure 10 shows the Fabaceae and Poaceae family to have five studies. C. ensiformis and Mucuna pruriens (Fabaceae) are the most studied species in phytoremediation, with two studies each. Notably, only C. ensiformis has been discussed previously. It is noteworthy that, of these two species, C. ensiformis is the only one mentioned in earlier topics.
Figure 10. Main families and species of plants used in the association of phytoremediation and biostimulation for soil decontamination with pesticides. This includes the most common botanical families and plant species, such as Canavalia ensiformis and Mucuna pruriens from the Fabaceae family, in studies evaluating the remediation of herbicides using biostimulants.
Table 3 shows that, for the effective remediation of the herbicide tebuthiuron, the studies focused on a specific relationship between the plant, i.e., M. pruriens, and the biostimulator organic material, i.e., vinasse. However, it is important to address certain points of caution that may not be explicit in the table but are important in the interpretation of the data. Although Table 3 shows only one association between M. pruriens, vinasse, and tebuthiuron, two separate studies were included. One highlighted the efficiency of herbicide removal (Ferreira et al., 2021), while the other addressed ecotoxicological and morphometric effects (Frias et al., 2023), which justifies the relevance of considering both in the context of this review.
Table 3. Quantities of pesticide studies on the association between plant families and organic matter.
M. pruriens is a leguminous plant widely used for green manure that, in addition to the ability to fix nitrogen, has phytoremediation potential and contributes to microbial biostimulation in the soil (Cruz et al., 2024; Ferreira et al., 2021; Frias et al., 2023).
Vinasse is a by-product of the sugar and alcohol industry and is rich in organic matter and macro- and micronutrients (Ogura et al., 2022). According to the authors, in addition to providing a sustainable solution for the disposal of industrial waste, the addition of vinasse can also improve the physical (e.g., aeration and moisture retention), chemical (i.e., increased availability of nutrients for plants), and biological (i.e., stimulation of microbial activity) attributes of the soil. Consequently, this positive effect can enhance the efficiency of pesticide removal from the edaphic ecosystem (Ferreira et al., 2021).
However, caution should be exercised in the management of vinasse, as repeated or excessive doses can cause problems such as salinization and the accumulation of organic and inorganic compounds that, over time, can alter the chemical characteristics of the soil, negatively impacting pesticide remediation (Trevisan et al., 2016).
As a result, future research should not only evaluate the effectiveness of vinasse in pesticide degradation but also investigate the interaction between different biostimulant materials and their synergies with plants and microorganisms and determine more effective methods for the recovery of soils contaminated with pesticides.
The predominance of the herbicide tebuthiuron in these studies highlights that this compound is a significant focus of research in the area due to its wide application in agriculture (Frias et al., 2023). This suggests a growing concern about its persistence in the soil and its adverse effects.
Phytoremediation, bioaugmentation, and vermiremediation
Table 4 presents two studies that highlight an integrated approach to the bioremediation of soils contaminated with lindane, which involves the combined action of plants, microorganisms, and annelids. This integration reflects a significant advancement in remediation strategies, which have evolved from isolated techniques to multifunctional systems that consider the ecological complexity of the contaminated agricultural environments.
Table 4. Integration between the main methods of biological remediation of pesticides.
The selection of Brassica napus as the phytoremediation species in both studies appears to be particularly strategic. In addition to its well-known ability for the rhizodegradation of persistent organic compounds, this plant also shows high biomass yield and oil production. These traits not only favor the uptake and degradation of contaminants but also enhance the economic feasibility of the remediation system. This opens possibilities for the application of phytomanagement strategies that combine environmental recovery with the production of marketable goods, aligning with the principles of bioeconomy (Burges et al., 2018).
The microbial part, in turn, further enhances the degradation potential of the contaminant. As previously discussed, the genus Streptomyces has been widely reported for its robust enzymatic activity and production of bioactive compounds, making it a key candidate for bioaugmentation strategies targeting organochlorine pesticide degradation, such as lindane. Amycolaptosis, although studied less to date, has shown promising results. Its inclusion in remediation studies highlights the need to broaden the diversity of microorganisms explored, as relying solely on traditional genera may limit the effectiveness of biotechnological systems under varying environmental conditions. Thus, the investigation of novel strains with unique resistance and metabolic capabilities could enhance the performance of the microbial consortia applied in field settings (Lacalle et al., 2020).
The incorporation of E. foetida as a vermiremediation agent complements the overall remediation process. In addition to promoting aeration and the mineralization of organic matter, earthworms ease the transport and distribution of microorganisms and nutrients through their movement and excreta. Studies have shown that their presence can significantly increase the microbial density and diversity, thereby enhancing contaminant degradation and improving the soil structure and fertility (ChaChina et al., 2016).
Another important aspect of this integrated approach is its adaptability to diverse edaphoclimatic conditions and contamination scenarios, which enhances its practical applicability in agricultural systems. However, the efficiency of this system is dependent on multiple factors, such as the compatibility among the biological agents used, the physicochemical characteristics of the soil, and the degree of contamination. Therefore, future research should prioritize multifactorial experiments under real field conditions to confirm the effectiveness of these synergistic interactions on a larger scale.
Furthermore, studies assessing the long-term effects of such integrated approaches on soil health, native microbiota dynamics, and secondary residue accumulation remain limited. Investigations addressing ecotoxicological aspects, functional resilience, and post-remediation ecological recovery are essential to combine this technology as a sustainable and safe alternative for modern agriculture.
Challenges and future perspectives
Phytoremediation is a well-established and promising strategy for the mitigation of pesticide contamination in agricultural soils. However, its isolated use presents limitations regarding efficiency, treatment duration, and performance in highly contaminated environments. To overcome these challenges, integrating phytoremediation with complementary biological approaches, such as bioaugmentation, biostimulation, and vermiremediation, is a promising path, although still underexplored in several combinations.
Future studies should prioritize field-scale validation under real edaphoclimatic conditions while also evaluating the compatibility and persistence of biological agents. Special attention should be given to the long-term ecological impacts of remediation strategies on soil fertility, microbial communities, and biodiversity. The genetic improvement of plants and microorganisms also represents an important opportunity to enhance remediation efficiency and multifunctionality.
Furthermore, future efforts should be directed toward filling the identified research gaps, particularly concerning the biological remediation of fungicides and nematicides, which are underrepresented in the current body of literature.
Finally, strengthening the socioeconomic and regulatory framework is critical to enable large-scale adoption. Policies that support biological alternatives over chemical remediation, coupled with the circular use of agricultural by-products such as vinasse, can align remediation technologies with the principles of sustainability and the bioeconomy.
Figure 11 provides a cohesive visualization of these concepts. At the core, integrated biological remediation (phytoremediation combined with bioaugmentation, biostimulation, and vermiremediation) generates direct benefits such as pesticide degradation, soil health recovery, and increased microbial diversity. These improvements lead to indirect agroecological outcomes, including higher crop productivity, biodiversity support, and reduced ecotoxicological risks. Ultimately, these cascading effects contribute to global-scale impacts, such as enhanced climate resilience, carbon sequestration, and mitigation of global warming. This framework bridges local remediation actions with broader sustainability and climate goals, reinforcing the multifunctional role of integrated strategies in resilient agricultural systems.
Figure 11. Conceptual framework illustrating the pathway from integrated biological remediation approaches (phytoremediation, bioaugmentation, biostimulation, and vermiremediation) to local benefits, agroecological outcomes, and global climate impacts.
Conclusion
This review confirms that integrated biological approaches provide a scalable, sustainable, and effective pathway for pesticide remediation in agricultural soils. By combining plants, microorganisms, and soil fauna, remediation becomes faster, more efficient, and directly linked to the recovery of soil health and ecosystem resilience.
Importantly, this review addresses a critical knowledge gap by providing a comparative perspective on the integration of phytoremediation with bioaugmentation, biostimulation, and vermiremediation, thereby clarifying their relative efficiencies and applicability.
The main takeaway for agronomy is that these multifunctional systems go beyond contaminant removal: they also improve soil fertility, biodiversity, and crop sustainability, making them a cornerstone for sustainable agricultural practices. Future research should build on this evidence to translate laboratory and greenhouse successes into practical, field-ready solutions that reconcile environmental protection with productive land use.
Data availability statement
The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.
Author contributions
VHC: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing – original draft, Writing – review & editing. HHS: Writing – review & editing. ERR: Writing – review & editing. YAF: Writing – review & editing. TSV: Writing – review & editing. PRML: Conceptualization, Funding acquisition, Methodology, Project administration, Resources, Supervision, Writing – review & editing.
Funding
The author(s) declared that financial support was received for this work and/or its publication. This work was supported by the Coordination for Improvement of Higher Education Personnel (CAPES-Brazil, Financing Code: 001); the São Paulo Research Foundation (FAPESP-Brazil, 2021/01884-6); the National Council for Scientific and Technological De-velopment (CNPq-Brazil, 313530/2021-1 and 302567/2025-9); the Agrisus Foundation (Brazil, PA 3740/24); and the Pro-Rectoris of Graduate Studies and of Research of São Paulo State University (PROPG and PROPe/UNESP-Brazil).
Acknowledgments
The authors would like to acknowledge the thank the Brazilian funding agencies (CAPES, FAPESP, CNPq, Fundação Agrisus, PROPG/UNESP, and PROPe/UNESP).
Conflict of interest
The author(s) declared that this work was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fagro.2025.1686748/full#supplementary-material
Supplementary Table 1 | Global overview of soil textures and references in studies on biological pesticide remediation approaches.
Supplementary Table 2 | Environmental persistence, toxicological hazards, and regulatory status of key pesticides. Information on pesticide properties was collected from leading international organizations: Food and Agriculture Organization of the United Nations (FAO), Organisation for Economic Co-operation and Development (OECD), U.S. Environmental Protection Agency (EPA), European Chemicals Agency (ECHA), World Health Organization (WHO), and European Food Safety Authority (EFSA).
Supplementary Table 3 | Phytoremediation efficiency of various plant species for pesticide removal from soil.
Supplementary Table 4 | Synergistic plant-microbe systems for enhanced pesticide bioremediation.
Supplementary Table 5 | Enhanced phytoremediation: the role of soil amendments and plant growth regulators in pesticide removal.
Supplementary Table 6 | Integrated plant-microbe-earthworm system for pesticide remediation.
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Keywords: bioaugmentation, biostimulation, persistent organic pollutants, phytoremediation, vermiremediation
Citation: Cruz VH, Simionatto HH, Ribeiro ER, Frias YA, Valério TS and Lopes PRM (2026) Multifunctional biological approaches for enhanced pesticide removal in agroecosystems: a path toward soil remediation. Front. Agron. 7:1686748. doi: 10.3389/fagro.2025.1686748
Received: 15 August 2025; Accepted: 08 December 2025; Revised: 17 October 2025;
Published: 23 January 2026.
Edited by:
I. Lopes, University of Aveiro, PortugalReviewed by:
Annamalai Muthusamy, Manipal Academy of Higher Education, IndiaManivannan Paramasivan, Bharathidasan University, India
Copyright © 2026 Cruz, Simionatto, Ribeiro, Frias, Valério and Lopes. 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.
*Correspondence: Paulo Renato Matos Lopes, cHJtLmxvcGVzQHVuZXNwLmJy