EDTA and citric acid on the growth of sunflower (Helianthus annuus L.) under chromium stress: a meta-analysisABSTRACT:
Human mining contributes to increasing the release of chromium (Cr) into the environment. For the phytoremediation of soil with high Cr content, sunflower is the right choice because the Cr in its seeds can be removed during the production of sunflower seed oil. However, the high content of Cr in the soil will inhibit the growth of sunflower, so the soil remediation agents commonly used with sunflower planting are ethylene diamine tetraacetic acid (EDTA) and citric acid (CA). This study conducted a meta-analysis on the effects of EDTA and CA on the development of sunflower under Cr stress. It will provide a reference for sunflower to improve Cr-contaminated soil or a reference to produce crops in Cr-polluted cultivated areas. A total of 97 articles were found, and 7 studies were used in this meta-analysis from January 1990 to January 2022. The results showed that EDTA treatment had no effect on the leaf weight, shoot weight and root weight. CA treatment had a positive effect on the leaf weight, shoot weight and root weight. EDTA and CA increased the Cr concentration in the root, leaf and shoot. This study recommends the addition of any chelating agent or activator, but the content of toxic metals in the soil must first be measured carefully. Unfortunately, in this study, we did not obtain a reference dose, and future research should focus on this problem.
Key words:
Cr; Ethylene Diamine Tetraacetic Acid; network meta-analysis; phytoremediation; soil
RESUMO:
A mineração humana contribui para aumentar a liberação de cromo (Cr) no ambiente. Para a fitorremediação de solo com alto teor de Cr, o girassol é a escolha certa porque o Cr em suas sementes pode ser removido durante a produção de óleo de semente de girassol. No entanto, o alto teor de Cr no solo inibirá o crescimento do girassol, então os agentes de remediação do solo comumente usados com o plantio de girassol são ácido etilenodiaminotetracético (EDTA) e ácido cítrico (AC). Este estudo conduziu uma meta-análise sobre os efeitos do EDTA e AC no desenvolvimento do girassol sob estresse de Cr. Ele fornecerá uma referência para o girassol para melhorar o solo contaminado com Cr ou uma referência para produzir safras em áreas cultivadas poluídas com Cr. Um total de 97 artigos foram encontrados, e sete estudos foram usados nesta meta-análise de janeiro de 1990 a janeiro de 2022. Os resultados mostraram que o tratamento com EDTA não teve efeito no peso das folhas, peso da parte aérea e peso da raiz. O tratamento com AC teve um efeito positivo no peso das folhas, peso da parte aérea e peso da raiz. EDTA e CA aumentaram a concentração de Cr na raiz, folha e broto. Este estudo recomenda a adição de qualquer agente quelante ou ativador, mas o conteúdo de metais tóxicos no solo deve primeiro ser medido cuidadosamente. Infelizmente, neste estudo, não obtivemos uma dose de referência, e pesquisas futuras devem se concentrar neste problema.
Palavras-chave:
Cr; Ácido Etileno Diamina Tetraacético; meta-análise de rede; fitorremediação; solo
INTRODUCTION
With the development of human industry, toxic metals deposited in the environment are problematic, and toxic metals accumulate daily (LI et al., 2022; SAMAL et al., 2023; LAILA et al., 2023). Chromium (Cr) in soil has the characteristics of difficult elimination, strong toxicity, a wide range of influence and serious pollution. It affects the growth of plants, destroys the soil environment and poses a great threat to the ecological environment and human health (MAHAR et al., 2022; KANG et al., 2022; SAMAL et al., 2023). Bioremediation is the most common treatment for toxic metals (APREJA et al., 2022). The treatment of Cr-contaminated soil is mainly to change the form of Cr ions, reduce the proportion of toxic and harmful hexavalent Cr (VI) and directly remove Cr from the soil (RAMACHANDRAN et al., 2022). Phytoremediation technology can be divided into four types: plant extraction, volatilization, stabilization and rhizofiltration. Plant extraction is the most potential research direction (HOODA, 2007; GAVRILESCU, 2022; LAILA et al., 2023). Hyperaccumulators such as sunflower and phytolacca acinose are searched on this way (ZHOU et al., 2022; ZHONG et al., 2024; BAYAT et al., 2022; SAMAL et al., 2023).
Sunflower is an ideal soil remediation plant (FORTE et al., 2017; SAMAL et al., 2023). Oilseed sunflower plants enrich Cr in soil, and Cr in edible oil can be removed after sunflower seed oil is extracted. The problem of toxic metal contamination of ornamental sunflowers is of no concern (WU et al., 2023). A high content of Cr in soil will inhibit the biological enzyme activity of sunflower, affect chlorophyll a and b, and then affect growth (MALLHI et al., 2020). The growth of root and bud tissues of sunflower was inhibited under Cr stress (MOHAMMADI et al., 2020). Therefore, some additives should be used to reduce the toxicity of Cr to sunflowers. Ethylene diamine tetraacetic acid (EDTA) and citric acid (CA) are the most studied soil remediation agents used in combination with sunflower planting (MOHAMMADI et al., 2021; NAWAZ et al., 2022; WANG et al., 2024; LU et al., 2023).
EDTA is often used as a chelating agent (MOHAMMADI et al., 2021; WANG et al., 2024). Some studies have shown that the use of EDTA in soil can promote the growth of sunflower and improve the leaf weight and stem weight (TURGUT et al., 2005; TURGUT et al., 2004; CICATELLI et al., 2017), and some researchers believe that the addition of EDTA can inhibit the growth of sunflower (ASLAM et al., 2014). CA is a soil washing agent. Some studies have shown that the use of CA in soil can promote the growth of sunflower and improve the leaf weight and stem weight (FARID et al., 2017; FARID et al., 2019; MALLHI et al., 2020). However, researchers of a previous study believed that adding CA can inhibit the growth of sunflower (TURGUT et al., 2004). Therefore, it is necessary to conduct a meta-analysis of the effects of EDTA and CA on the development of sunflower under Cr stress. This study will provide a reference for hyperaccumulators to improve Cr-contaminated soil bioremediation. One possible remediation approach is growing sunflower plants on Cr-contaminated soil that absorb Cr from the soil, which can then be removed during the production of sunflower seed oil.
METHODS
Database search strategy and data extraction
The search included PubMed, ProQuest and ScienceDirect databases. The key terms were (sunflower OR (Helianthus annuus) OR (Helianthus annuus L)) AND chromium AND acid, from January 1990 to January 2023. Two independent authors screened the literature following table 1. The included studies consisted of different treatments with acid; thus, each dataset was extracted according to different treatments separately and analyzed as independent data (MAILLARD et al., 2014). When the data were presented in figures, GetData Graph Digitizer V2.5 was used (ZHOU et al., 2021). Figure 1 shows the retrieval processes of all datasets.
Summary of the study selection procedure. Two authors completed independently and retrieved from January 1990 to January 2023.
Data analysis
Traditional meta-analysis: In the reviewed literature, soil under Cr stress was used to plant sunflower in all groups. The treatment group included CA or EDTA, whereas the control group did not include CA or EDTA. Raw data of the blank control without Cr were not used in the analysis. Standard mean difference (SMD) meta-analyses were performed using Stata 12.0 (Stata Corp, College Station, TX, USA) with a continuous model. CA and EDTA treatment effects on the leaf, shoot and root weight were analyzed. The Cr content in the leaf, shoot and root was also studied. Two independent analyses were conducted for CA and EDTA.
Network meta-analysis: The traditional meta-analysis showed that EDTA and CA increased the Cr concentration in the root, leaf, and shoot. This result motivated us to further study the dataset of EDTA, CA, 5-aminolevulinic acid (ALA), and ethylene diamine disuccinate (EDDS) mentioned in previous studies (TURGUT et al., 2004; CICATELLI et al., 2017; FARID et al., 2019). After data consolidation, network meta-analysis was performed using the coda, rjags and gemtc packages in R software (version 4.1.2). The output network mapping was obtained using Gephi (version 0.9.2).
RESULTS
A total of 97 articles were found, and 7 studies were used in this meta-analysis (MALLHI et al., 2020; FARID et al., 2017; FARID et al., 2019; TURGUT et al., 2004; TURGUT et al., 2005; CICATELLI et al., 2017; ASLAM et al., 2014), as shown in table 2. In total, 41 datasets were extracted; EDTA included 17 datasets, and 23 datasets were about CA. Some studies focused on glutamic acid (FARID et al., 2020), gibberellic acid (SALEEM et al., 2015) and 5-aminolevulinic acid (FARID et al., 2018), but a single study cannot be included in meta-analyses.
Table 3 shows that EDTA treatment had no effect on the leaf weight (SMD = 0.42, 95% CI = -0.70 - 1.55), shoot weight (SMD = 0.36, 95% CI = - 1.02 - 0.3) and root weight (SMD = - 0.51, 95% CI = - 1.07 - 0.05). The value of the invalid line marked in table 3 was 0, and the result was considered to have no significant correlation when the 95% CI included this value. Figure 2 shows that CA treatment had positive effects on the leaf weight, shoot weight and root weight. None of the results touched the invalid line (0). EDTA and CA increased the Cr concentration in the leaf, root and shoot, as shown in table 4 and figure 3. All of the results had a positive correlation. This indicates that EDTA cannot promote the growth of sunflowers, but it can alleviate the toxicity of Cr, ensuring that the growth of sunflower plants is not affected and allowing them to absorb more Cr from the soil. CA had a more comprehensive effect than EDTA.
Forest plot of CA treatment effects on sunflower growth, CI = 95%, CA denotes citric acid, 24 datasets from 4 studies for analysis.
Forest plot of CA treatment effects on sunflower Cr content, CI = 95%, 24 datasets from 4 studies for analysis.
The results showed that CA had a better promotive effect than EDTA on the growth of sunflowers. However, both CA and EDTA increased Cr concentration within the plant. Then EDTA, CA, ALA, and EDDS network meta-analyses were conducted; three two-arm studies were used. It was found that these four substances showed no difference in altering the Cr concentration in sunflower roots (Figure 4).
Different treatment effects on sunflower Cr content in root, A: network mapping of EDTA, CA, ALA and EDDS, round size means datasets number. Line size denote studies number. B: forest plot of EDTA, CA, ALA and EDDS effects on sunflower Cr content, CI = 95%.
DISCUSSION
Sunflower is an important hyperaccumulator, which can be used for the bioremediation of Cr-polluted environments (BAYAT et al., 2022; SAMAL et al., 2023). In soil, Cr exists in different oxidation forms, and the most stable forms are Cr (III) and Cr (VI). The toxicity of Cr (VI) is significantly higher than that of Cr (III) (LI et al., 2024) . There are many methods to classify the forms of toxic metals. The most commonly used method is continuous extraction form analysis. The existing forms of toxic metals in soil are divided into five kinds: exchangeable state, carbonate-bound state, iron oxide-bound state, organic matter-bound state and residual state (TESSIER et al., 1979). Cr translocation and bioaccumulation are gradual processes, and higher concentrations of Cr accumulate in sunflower stems and leaves than in roots (MOHAMMADI et al., 2020). The results showed that EDTA and CA increased the Cr concentration in the root, leaf and shoot.
In the research of the remediation of toxic metal-contaminated soil, scientists are committed to the screening of super enriched plants, the screening of curing agents, the development of more convenient leaching equipment, the development of cheaper and durable electrode materials in the process of electric remediation and the exploration of more efficient strains in the use of microorganisms to remediate soil polluted with toxic metals. Toxic metals destroy the nutritional balance of plants (MALLHI et al., 2020), resulting in poor growth. The target plants for profitable remediation of soil contaminated with toxic metals should have the characteristics of toxic metal tolerance, strong adaptability, wide distribution and high biomass. Sunflower is a suitable plant due to its high biomass and is resistant to salt and alkali stress and has a high enrichment rate (ZEHRA et al., 2020).
The mechanism of Cr affecting sunflower growth is not very clear. Cr inhibits chlorophyll a and b, which in turn affects growth through effects on photosynthesis (MALLHI et al., 2020). Cr inhibits the growth of root and bud tissues of sunflower (MOHAMMADI et al., 2020). Cr increases H2O2 and malondialdehyde (MDA), causes oxidative damage, and leads to morphological and physiological damage (MOHAMMADI et al., 2018). Cr can increase the activity of antioxidant enzymes (ALI et al., 2016). ROS produced by Cr stress can lead to tolerance in plants (HATAMI et al., 2019). Catalase (CAT), ascorbate peroxidase (APX), peroxidase (POX) and superoxide dismutase (SOD) control the intracellular ROS content under Cr stress (TIAN et al., 2018; GHORBANPOUR & HADIAN, 2015).
Currently, there are many kinds of materials commonly used to affect the desorption of Cr in soil, such as surfactants (sodium dodecylbenzene sulfonate, the cationic surfactant cetyltrimethylammonium bromide (CTAB) and tea saponins), chelating agents or activators (CA, diethylenetriaminepentaacetic acid (DTPA) and ethylene glycol tetraacetic acid (EGTA)). Among them, CA, EDTA and surfactants have a good desorption effect on soil Cr. EDTA can activate Cr (VI) and make it more easily absorbed by plants (RAM et al., 2019). EDTA also inhibits plant growth (ALI et al., 2016). This inhibition can be attributed to EDTA toxicity and the formation of a Cr-EDTA chelator complex (BAREEN et al., 2019). In addition, due to the increased migration of toxic metals in soil, the absorption of essential nutrients (such as Zn 2 + and Ca 2 +) is reduced (ALI & CHAUDHURY, 2016; BAREEN et al., 2019). EDTA can change soil pH and promote plants to absorb more Cr (TAHIRA, 2010). The results of this research show that under Cr stress, the addition of EDTA cannot promote plant growth but can promote sunflower to absorb more Cr.
The main reasons why CA promotes the absorption and transfer of Cr by plants are as follows: first, CA acidifies the plant rhizosphere, reduces the soil pH value, increases the mobility of toxic metal ions and increases the accumulation and transfer of toxic metals from roots to aboveground parts (NASCIMENTO et al., 2020). Second, anions released from CA can react with toxic metals, effectively promote the release of metal ions, reduce the attachment of toxic metal ions to soil organic matter, clay and oxides, and enhance the mobility of toxic metals in soil (ZHENG et al., 2020). The results of this research show that under Cr stress, CA can not only significantly correlate with sunflower plant growth but can also promote sunflower to absorb more Cr from the soil, and the positive effect of its application is higher than that of EDTA.
Only one study has examined the simultaneous influence of both CA and EDTA on Cr absorption in sunflower. However, it did not employ both CA and EDTA in a single treatment (TURGUT et al., 2004). In a study on pepper (Capsicum annuum L.), (ALSHEGAIHI et al., 2023) found that EDTA and CA can mitigate Cr damage to plants. Due to this reason, Cr stress enhances plant secretion of organic acids (JAVED et al., 2017). CA and EDTA alter soil pH, leading to a decrease in the quantity of organic acids produced by the plant (ALSHEGAIHI et al., 2023).
Limitations
In several studies, irrigation was conducted with Cr-containing water (MALLHI et al., 2020). The purpose of these studies was to grow crops on cultivated land with excessive amounts of toxic metals. Other studies focused on soil remediation, which may lead to the limitation of our results.
Implications of this research
Some of the studies mentioned in this research were conducted in Pakistan, and the research report pointed out that due to the lack of irrigation water, researchers had to use water with excessive amounts of toxic metals for irrigation (MALLHI et al., 2020). The impact of Cr on human health has been widely reported. Cr alloys as implants for human joint replacements (MILLER et al., 2022) and Cr in food will also cause harm to our body (WANG et al., 2022a). We think this is just the tip of the iceberg. After the in-depth study of Fe-mediated ferroptosis (GARCIA-BERMUDEZ et al., 2021; MAO et al., 2021), some studies proposed Cu-mediated cuproptosis (WANG et al., 2022b). There will be more in-depth research reports on the effects of Cr on animal cells and tissues in the future (Figure 5).
The high content of Cr in the soil will inhibit the growth of sunflower. This meta-analysis ethylene diamine tetraacetic acid (EDTA), acidcitric acid (CA), 5-aminolevulinic acid (ALA) and ethylene diamine disuccinate (EDDS) effect sunflower on growth. The result showed that EDTA cannot promote the growth of sunflowers, but it can alleviate the toxicity of Cr, ensuring that the growth of sunflowers is not affected, and simultaneously absorb more Cr from the soil. Relative to EDTA, CA has a more comprehensive effect, not only promoting the growth of sunflowers but also simultaneously absorbing more Cr. The study recommended the addition of any chelating agent or activator, but the content of toxic metal s in the soil must first be measured carefully.
A low concentration of Cr (VI) can improve photosynthesis and promote plant growth by enhancing the electron transfer activity of PSII (RAM et al., 2019). However, high concentrations of Cr (VI) can hinder water transport, reduce transpiration and inhibit plant growth (MA et al., 2016).
CONCLUSION
The future direction of soil remediation involves the combined use of various methods. One approach to consider is growing sunflower plants on Cr-contaminated soil; the plants can absorb the Cr from the soil, which can later be removed during the production of sunflower seed oil. Through this remediation process, Cr concentrations can be reduced in the soil, allowing other plants can be cultivated in it. Additionally, before adding any chelating agent or activator, the content of toxic metals in the soil must be measured carefully. Unfortunately, in this study, we did not obtain the reference dose, and future research should focus on this problem.
ACKNOWLEDGMENTS
We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript. This research was supported by the China Agriculture Research System of MOF and MARA (CARS-14).
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Edited by
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Editors
Leandro Souza da Silva (0000-0002-1636-6643)Anderson Luis Nunes (0000-0002-4789-0253)
Publication Dates
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Publication in this collection
20 Jan 2025 -
Date of issue
2025
History
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Received
24 Jan 2024 -
Accepted
25 July 2024 -
Reviewed
18 Oct 2024
