Biochar application modified growth and physiological parameters of Ocimum ciliatum L. and reduced human risk assessment under cadmium stress
Graphical Abstract
Introduction
Heavy metals contamination is one obstacle factor for plant development. Soil pollution by Cd is a serious problem because of using chemical fertilizers, pesticides, and sewage sludge (Yang et al., 2011). Among the trace elements, Cd enhancement in the soils becomes a serious problem worldwide (Rizwan et al., 2016a), so it is a danger to the health of the environment and humans. Among 20 metals with high toxicity, Cd is graded as the 7th one which is very dangerous for people and plants (Gill et al., 2012).
The average concentration of Cd in the soil was changed from neodymium to about 2.01 mg/kg in different regions of Iran (Amini et al., 2005, Solgi et al., 2012, Fattahi et al., 2019). Cd accumulates in the soils in different geochemical forms such as exchangeable and bounded. Their availabilities to plants are various include bioavailable (exchangeable and bounded to carbonates), potentially bioavailable (reducible and oxidizable fractions), and not available (residual fraction) (Alvarez et al., 2006, Obrador et al., 2007). Chemical forms and availability of Cd to plants are connected to the soil properties such as texture, CEC, pH, other cations concentration, and organic matter (Gallego et al., 2012; Umoren and Udousoro, 2009). Recently, Cd contamination in agricultural soils has become one of the most widespread and severe environmental and agricultural problems in Asian countries (Fan et al., 2010, Gallego et al., 2012, Mori et al., 2016). Enhancement in Cd concentration is being found in agricultural soils due to the chemical fertilizer application, organic manures, sewage irrigation, sludge usage, and atmospheric deposition (Inglezakis et al., 2014, Liang et al., 2017, Dharma-Wardana, 2018). The sources of Cd vary in different places. For instance, the potential risk of Cd accumulation in the farmland soil is more related to irrigation water compared with fertilizer and atmospheric deposition (Shiyu et al., 2020). Sewage sludge application to agricultural farmlands is very common worldwide because they are a low-cost source of plant nutrients and can improve soil properties. Nevertheless, sludge probably contains a high concentration of heavy metals such as Cd which have increased some effects regarding soil pollution. One study has concluded that greater metal mobility after sludge application (Moradi et al., 2005). Moreover, sewage sludge addition raises the inorganic part of the soil that can lead to an increase in the sorption affinity of soils for heavy metals (Moradi et al., 2005). In the arid region of central Iran, farmers extensively use sewage sludge as fertilizer. Due to the lack of controlling reducing pollutant concentrations in sewage sludge and the rate of sludge application on agricultural farmlands, high loads of heavy metals are introduced by sewage sludge application onto extremely farmed and excessively irrigated soils which may provide suitable conditions for heavy metal leaching. The long-term effect of Cd in the farmlands irrigated with Cd-enriched sewage sludge is important (Moradi et al., 2005). Thus, it seems that the most important Cd source in the studied region is irrigation water enriched sewage sludge that is polluted from materials from some factories and sewage. Depending on the sorption properties of the soil, the sludge adsorption capacity contributed by the inorganic fraction, and the sludge loading. Various effects of Cd on plants such as the nutrient absorption and distribution imbalance, growth inhibition, pigment decomposition, chlorosis, and finally death were observed (Yang et al., 2011, Gill et al., 2012). The root uptake and transfer Cd into the stem simply even though it is not necessary for the growth of some plant species. As a result, using Cd in the food chain possibly dangerous for people and other organisms (Rizwan et al., 2016b). The toxic influences of Cd on the health of plants and people were reported before in some researches (Nagajyoti et al., 2010, Rizwan et al., 2016b). In addition, some physiological disorders occur in the response to Cd stress. Cd increases the oxidative stress in plants by raising the ROS production in different plant parts. Moreover, the plant antioxidant defensive system disturbing which causes lipid peroxidation and oxidative stress (Gill and Tuteja, 2010). In addition, for protection against ROS, the plants improve non-enzymatic and enzymatic antioxidants like CAT, GPX, and APX (Vajpaee et al., 2000). Moreover, proline accumulation occurs under heavy metals stress. During stress in the plants, proline interfering in supporting the cell wall strength, inhibiting, and cleansing produced hydroxyls macromolecules degradation (Zarei et al., 2012).
There are various techniques to decrease the detrimental and toxic effects of heavy metals in plants. Organic additives such as BC have been revealed as highly effective and environment-friendly immobilizers to reduce Cd contamination (Hamid et al., 2020). BC is a carbonous pyrolyzed organic material used as a soil amendment in sustainable agriculture management (Lehmann and Joseph, 2015). The health of the soil and productivity of the crops are improved by BC due to its high carbon content (Lehmann et al., 2011, Ye et al., 2017, Ye et al., 2019a, Ye et al., 2019b, Yu et al., 2019, Kwon et al., 2020). It has a great surface area and its usage enhances soil quality, raises soil fertility and pH, improves water holding, and CEC which resulting in higher crop yields (Lehmann et al., 2011). Furthermore, the application of BC in the soils under plants cultivation decreases trace element toxicity and in the soil enhances metal immobilization (Younis et al., 2016, Abbas et al., 2017, Chang et al., 2019, Qiu et al., 2020, Khan et al., 2020a, Albert et al., 2020). Based on the findings of previous studies, BC was effective in promoting plant growth and reducing Cd accumulation (Qi et al., 2020, Albert et al., 2020, Khan et al., 2020b). These influences of BC depend on the chemical and physical traits of BC such as the type of used materials, conditions of pyrolysis, the used method, and its rate, porosity, and specific surface area (Abbas et al., 2018). Furthermore, its application affects plant growth in different ways. It has various positive, detrimental, and neutral effects on the productivity of plants (Jeffery et al., 2011, Kwon et al., 2020). The influences of BC usage on crop growth have been studied before (Jeffery et al., 2011, Lehmann et al., 2011, Yu et al., 2019, Kwon et al., 2020), but the exact mechanistic of BC effects is not known completely. Under heavy element stress, there are several investigations regarding the positive influence of BC on the plants (Rehman and Ahmad, 2016, Zhang et al., 2016, Khan et al., 2020a). Therefore, BC application may provide a possible technology for green, environmental-friendly, and cost-effective remediation of Cd contaminated soil (Qi et al., 2020, Albert et al., 2020, Khan et al., 2020b).
On the other hand, the heavy metal contaminated soils are potential threats to human health because of entering the toxic elements through the edible plants into the food chain and disrupt the health systems of humans. Such health risks can be decreased by suitable management of pollution sources, using remediation methods and plants pattern adjustment. Previously, BC application in contaminated soils decreased heavy metal concentration and alleviate associated health hazards (Khan et al., 2020a, Khan et al., 2020b).
BC indicated different effects on growth, biochemical, and physiological characteristics of the plants under Cd stress as schematic explanations have shown in Fig. 1.
Basil (Ocimum spp.) is one of the largest genera of Lamiaceae family which is native to Africa, Asia, and South America, especially the tropical and subtropical regions. The herbaceous parts of this aromatic plant have several attributes which are applied in food (as a vegetable, culinary), pharmaceuticals, and cosmetic industries (Makari and Kintzios, 2008, Moghaddam et al., 2011). As a traditional medicine, it has been used for curing some illnesses such as abdominal pains, constipation, worms, headaches, and kidney malfunctions (Makari and Kintzios, 2008). Between Iranian accessions of Ocimum spp., genetic diversity was done before. Ocimum ciliatum is one of the Iranian basil species which is grown at vegetable gardens and home in various areas of Iran. (Moghaddam et al., 2011).
Based on the literature, some reports about the effect of BC amendment on different traits of plants under Cd stress are available. But there was no research available on the effect of the BC on the studied traits of O. ciliatum under Cd stress until now. Since O. ciliatum is a valuable plant that is used as a culinary vegetable in Iran, consequently, the authors carried out this study to investigate the influences of BC on morphological, biochemical as well as physiological traits of O. ciliatum. On the other hand, one of the valuable parameters for estimating the human health risks of O. ciliatum that is consumed widely as an ordinary crop in the Iranian daily diet is the THQ. The low concentration of Cd can indicate no risk to human health. According to the literature review, until now there is no study to evaluate the role of BC in health risk reduction. Therefore, the authors evaluated the effect of BC on Cd content and human risk assessment of Cd in O. ciliatum for the first time.
Section snippets
Experimental design and growth conditions
A pot factorial experiment with three replications was done as a complete randomized design (CRD) in the greenhouse of Ferdowsi University of Mashhad, Iran. O. ciliatum L. seeds were prepared from Anbari Company, Mashhad, Iran. The sandy loam soil contained 73.4%, 18.3%, and 8.3% sand, silt, and clay, respectively. Soil pH, EC (dS/cm), CEC (cmol (+) kg−1), and organic matters (%) values were 8.08, 3.09, 8, and 1.14, respectively. Other characteristics of the soil included: organic matter
Growth characteristics
The findings of ANOVA in this study showed that the interaction effect of BC application under Cd stress was significant (P < 0.05) in the case of growth characteristics. Although the growth traits of the plants included plant height, branches number, number of nodes, number of inflorescences, inflorescence length, fresh and dry weight of leaf and stem reduced under Cd stress, BC usage increased these growth characteristics (Table 1). The highest plant height (51.8 cm), branchlet number (17.1),
Discussion
One toxic element for plants is Cd which can reduce the growth, yield, and plant quality (Rizwan et al., 2016a, Xie et al., 2019). The reduction in growth factors connected to Cd concentration in the soil may be as a result of a reduction in cell wall constituents, mitosis inhibition, Golgi apparatus damage, and changes in the metabolism of polysaccharides (Sai Kachout et al., 2010). Cell meiosis and growth of plants reduce by heavy metals because of decreasing the photosynthesis and exchange
Conclusion
The findings of the present experiment showed that growth, biochemical and physiological characteristics of O. ciliatum as well as Cd content of the leaves are influenced by different Cd concentrations. As the authors indicated in the results, O. ciliatum exhibited different reactions to Cd stress and BC usage in the soil, especially at 2% w/w, alleviate negative effects of Cd stress on all of the studied traits of O. ciliatum significantly. In this study, the authors understand that BC can
CRediT authorship contribution statement
Leila Mehdizadeh designed the research, Writing - review & editing. Sara Farsaraei designed the research, and review and editing. Mohammad Moghaddam designed the research, Writing - review & editing. All authors read and approved the final manuscript.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgment
This research was supported by Ferdowsi University of Mashhad (Grant No. 2/43992).
References (96)
- et al.
Biochar application increased the growth and yield and reduced cadmium in drought stressed wheat grown in an aged contaminated soil
Ecotoxicol. Environ. Saf.
(2018) - et al.
Effect of biochar on cadmium bioavailability and uptake in wheat (Triticum aestivum L.) grown in a soil with aged contamination
Ecotoxicol. Environ. Saf.
(2017) - et al.
Heavy metal concentrations in edible muscle of white cheek shark, Carcharhinus dussumieri (elasmobranchii, chondrichthyes) from the Persian Gulf: a food safety issue
Food Chem. Toxicol.
(2016) - et al.
Residual effects of biochar on improving growth, physiology and yield of wheat under salt stress
Agric. Water Manag.
(2015) - et al.
Translocation of cadmium in Ocimum basilicum at low concentration of CdSSe nanoparticles
Appl. Mater. Today
(2017) - et al.
Comparison of EDTA and sequential extraction tests for phytoavailability prediction of manganese and zinc in Agricultural alkaline soils
Geoderma
(2006) - et al.
A spectrophotometric method of measuring the breakdown of hydrogen peroxide by catalase
J. Biol. Chem.
(1952) - et al.
A review of biochars’ potential role in the remediation, revegetation and restoration of contaminated soils
Environ. Pollut.
(2011) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding
Anal. Biochem.
(1976)- et al.
The effect of biochar addition on N2O and CO2 emissions from a sandy loam soil–the role of soil aeration
Soil Biol. Biochem.
(2012)
Excessive sulfur supply reduces cadmium accumulation in brown rice (Oryza sativa L.)
Environ. Pollut.
Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms
Environ. Exp. Bot.
Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium sativum L.)
Plant Sci.
Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants
Plant Physiol. Biochem.
Remediation of heavy metal contaminated soils by biochar: mechanisms, potential risks and applications in China
Environ. Pollut.
Effect of cadmium on the growth and antioxidant enzymes in two varieties of Brassica juncea
Saudi J. Biol. Sci.
Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress
J. Plant Physiol.
A quantitative review of the effects of biochar application to soils on crop productivity using meta-analysis
Agric. Ecosyst. Environ.
Biochar effects on soil biota–a review
Soil Biol. Biochem.
Atmospheric deposition of mercury and cadmium impacts on topsoil in a typical coal mine city, Lianyuan, China
Chemosphere
Salinity and water stress have contrasting effects on the relationship between growth and cell viability during and after stress exposure in durum wheat callus
Plant. Sci.
Effect of bamboo and rice straw biochars on the mobility and redistribution of heavy metals (Cd, Cu, Pb and Zn) in contaminated soil
J. Environ. Manag.
Evaluation of genetic diversity among Iranian accessions of Ocimum spp. using AFLP markers
Biochem. Syst. Ecol.
Modelling field-scale cadmium transport below the root zone of a sewage sludge amended soil in an arid region in central Iran
J. Contam. Hydrol.
Suppression of cadmium uptake in rice using fermented bark as a soil amendment
Chemosphere
Relationships of soil properties with Mn and Zn distribution in acidic soil sand their by a barley crop
Geoderma
Concentrations of cadmium, lead, mercury and arsenic in Chinese market milled rice and associated population health risk
Food Control
Residual effects of biochar on growth, photosynthesis and cadmium uptake in rice (Oryza sativa L.) under Cd stress with different water conditions
J. Environ. Manag.
Cadmium minimization in wheat: a critical review
Ecotoxicol. Environ. Saf.
Growth and some physiological characteristics of Pistacia vera L. cv Ahmad Aghaei in response to cadmium stress and Glomus mosseae symbiosis
South Afr. J. Bot.
A genotype dependent-response to cadmium contamination in soil is displayed by Pinus pinaster in symbiosis with different mycorrhizal fungi
Appl. Soil Ecol.
Potential human health risks from metals (Hg, Cd, and Pb) and polychlorinated biphenyls (PCBs) via seafood consumption: estimation of target hazard quotients (THQs) and toxic equivalents (TEQs)
Food Chem. Toxicol.
Stress enhances the gene expression and enzyme activity of phenylalanine ammonia-lyase and the endogenous content of salicylic acid to induce flowering in pharbitis
J. Plant Physiol.
The spectral determination of chlorophylls a and b as well as total carotenoids, using various solvents with spectrophotometers of different resolution
J. Plant Physiol.
Facile assembled biochar-based nanocomposite with improved graphitization for efficient photocatalytic activity driven by visible light
Appl. Catal. B: Environ.
The effects of activated biochar addition on remediation efficiency of co-composting with contaminated wetland soil
Resour. Conserv. Recycl.
Varying effect of biochar on Cd, Pb and as mobility in a multi-metal contaminated paddy soil
Chemosphere
Biochar amendment improves crop production in problem soils: a review
J. Environ. Manag.
Effects of biochars on the availability of heavy metals to ryegrass in an alkaline contaminated soil
Environ. Pollut.
Effective phytoextraction of cadmium (Cd) with increasing concentration of total phenolics and free proline in Cannabis sativa (L.) plant under various treatments of fertilizers, plant growth regulators and sodium salt
Int. J. Phytoremediat.
Physiological responses of summer savory (Satureja hortensis L.) under salinity stress
Int. J. Agric. Crop Sci.
Influence of biochar and soil properties on soil and plant tissue concentrations of Cd and Pb: a meta-analysis
Sci. Total. Environ.
Variability of available cadmium in relation to soil properties and land use in an arid region in central Iran
Water Air Soil Pollut.
Macro-and micro-elements in some herbal drug raw materials and their water extracts consumed in Poland
Open Chem.
Rapid determination of free proline for water-stress studies
Plant Soil
Swailing affects seed germination of plants of European bio-and agricenosis in a different way
Open Life Sci.
A comparative study on biochar properties and Cd adsorption behavior under effects of ageing processes of leaching, acidification and oxidation
Environ. Pollut.
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