Abstract
Slaked lime has been used to remediate contaminated agricultural soils as an in situ chemical immobilization amendment for a long time. However, the effects of slaked lime on peanut and soil cadmium (Cd) levels remain poorly understood with respect to remediating Cd-contaminated soil. In this study, six rates of slaked lime (e.g., 0, 300, 600, 900, 1200 and 1500 kg ha−1) were applied to evaluate the effects of slaked lime treatments on soil pH and the growth, Cd accumulation and physiology characteristics of peanut, which were in Cd-contaminated soil, and 0 kg ha−1 was taken as the control. The results indicated that slaked lime application significantly increased soil pH and reduced total Cd contents in peanut tissues at all growth stages. As the rates of slaked lime were increased, kernel biomass increased in the maturity stage, which increased peanut yields. The irregular variations in catalase, peroxidase, and superoxide dismutase activities and chlorophyll and malondialdehyde contents that were observed at all growth stages may be due to the interactions among soil pH, Ca nutrients and Cd, etc. In summary, slaked lime is suitable as an in situ chemical immobilization amendment to increase Cd immobilization and peanut yields in Cd-contaminated soil.
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Introduction
Soil pollution by heavy metals is a world-wide issue to human health and food security. Cadmium (Cd) is a poisonous element. The negative effects of Cd in crops produce intricate genetic, biochemical, and physiological shifts, which slow water and nutrient absorption, growth and development, and protein decomposition1. Cd accumulations in farmlands is attributable to manure, sewage sludge, municipal waste, phosphatic fertilizer, mining and metallurgy2,3, and due to its persistent nature, Cd is ranked as the 7th most toxic heavy metal out of 20 metals4. According to the Chinese soil environmental quality limits, the maximum allowed value of Cd in soil is 0.3 mg kg−1 when pH is below 7.55, however, approximately 7.0% of agricultural soils are Cd-polluted6.
Peanuts (Arachis hypogaea L.) generally take about 100–150 days from planting to harvesting, and about 180 days for individual late-ripening varieties. Peanuts will not bloom until about 2 months after sowing, and should be harvested in time once they reached maturity, or they will re-germinate in the soil. Peanuts like light and are afraid of waterlogging, and should be planted in a plot with sufficient light and good drainage. Peanut is a crucial oilseed and economic crop. Its seeds contain vitamins, minerals, and essential proteins7. In recent years, peanut has been a major oil crop in China due its large cultivated area that exceeds 5.0 × 106 ha and yearly pod production that exceeds 1.6 × 107 t8, and peanut plays a crucial part in ensuring the safety of cooking oils9. In some cases, peanuts can also be a complementary food due to their abundant nutritional contents10. According to the National Food Safety Standards (GB2762-2017), the current maximum residual limit permitted of 0.5 mg/kg.
For agricultural soils, the toxicity, bioaccumulation and persistence of Cd in the environment require remediation of polluted soils. Different strategies have been applied ameliorate metal-polluted sites, including excavation, washing, landfills, immobilization/stabilization and phytoremediation11,12,13.
Recently, in-place chemical fixation has gained prominence for remediating polluted farmland due to its rapid implementation, cost-effectiveness and capacity for expansion over large areas14,15. This method is based on adding soil amendments to bond to metal, which thereby decreases heavy metal concentration in the soil that is available by root absorption16. The adsorption/desorption behaviour of Cd in a soil/limestone blend was dominated by the structure and density of sorption sites and subsequently the sorption conditions, which were mostly impacted by soil pH and levels of exchangeable calcium ions (Ca2+)17.
Slaked lime is a conventional and most widely used fixation amendment that enhances soil pH and reduces metal availability14. Application of lime enhances sorption of metals by reducing H+ concentrations and increasing the number of negatively charged ions18. Lime addition increases the concentrations of residual Cd fractions in polluted soil. For example, lime spread at 150 g m−2 remarkably enhanced soil pH, and the formation of carbonate and Fe/Mn oxide-bound Cd reduced Cd concentrations in crop tissues by 20–37.5%19. Furthermore, as a traditional common trace metal passivating agent, the rates of applied lime are also one of the pivotal factors for controlling repair efficiency20.
To the best of our knowledge, studies of how liming alters Cd phytoaccessibility have concentrated on mechanisms such as soil pH, Cd sorption, complexation and precipitation reactions18,21. According to these studies, we assumed that there are dynamic fluctuations between soil Cd fixation and peanut Cd absorption in response to liming applications. Accordingly, liming applications, especially the rates used, can be optimized to minimize Cd absorption by peanut17,22.
In this research, a field experiment was conducted on Cd-polluted farmland to characterize the impacts of liming on soil pH and the behaviour of Cd absorption and translocation in the soil–peanut system over the full growth stage. The main purposes of this research were to determine the uncertainties in whether liming reduces the phytoaccessibility of Cd to peanut and determine the impacts of lime rates on soil pH, biomass and Cd content of peanut, and chlorophyll content, malondialdehyde (MDA) content and antioxidant enzyme activity of leaves.
Materials and methods
Ethics statement
All the samples used in this study were collected with the confirmation and admission of the local authorities. During the sample collection and experimentation, we strictly followed the China’s laws and regulations with respect to the protection of endangered wilding plant resources and abided by the Convention on the Trade in Endangered Species of Wild Fauna and Flora.
Experimental site and description
The field experiment was carried out in Changsha County, Hunan Province, China (28°43′N, 113°06′E) from March to November 2016. This location has a humid subtropical monsoon climate with a yearly average temperature of 12.67 °C and annual precipitation of 1100 mm. Soil Cd concentrations in this area are moderate (0.7 mg kg−1), and the characteristics of the test soil (0–20 cm) in 2016 before peanut planting are shown in Table 1.
Experimental materials
The peanut seeds (‘Zhonghua No. 23’) used in the study were obtained from the Chinese Academy of Agricultural Sciences and were selected because of their higher yields and protein contents and lower Cd uptake. The selection of low Cd-accumulating peanut variety is mainly for economic and food safety reasons. Moreover, the peanut seeds have not been inoculated. Slaked lime (Ca(OH)2 > 95%), an alkaline amendment, was purchased from the Yuanshan Lime Processing Co., Ltd., Shaoguan, Guangdong Province.
Experimental design and treatments
The experiment was carried out under field experimental conditions. The slaked lime treatments used in this experiment were spread over the fields and were labelled C0 (0 kg ha−1), C300 (300 kg ha−1), C600 (600 kg ha−1), C900 (900 kg ha−1), C1200 (1200 kg ha−1), and C1500 (1500 kg ha−1) in triplicates following a randomized completely block design. The area of plot was 24 m2 with 8 m long and 3 m width, twenty rows located in each plot. The row spacing was 0.40 m, the plant spacing was 0.15 m and the number of plants was 400 in each plot. Single-seed precision sowing was conducted on 30 April, and peanut and soil samples were collected on 30 May (seeding stage), 20 June (pod-pin stage), 10 July (pod bearing stage), and 10 August (maturity stage). Chemical fertilizer was applied in the form of bulk-blended fertilizer (N:P:K) = 15:15:15, GB15063-2009, Zhongnong Group Fertilizer Co., Ltd. Beijing, China, which was applied to the peanut soil at a rate of 225 kg ha−1 in the seeding stage. Weeds were eliminated with glyphosate, which was produced by the Green Agricultural Science and Technology Group Co. Ltd.
Soil and peanut sample analyses
A pH meter (PHS-3C, Rex, China) was used to determine soil pH values (soil:1 M KCl solution = 1:5, w/v)23.
Before harvested, three mature leaves of peanut were harvested and packed in ice bags to measure chlorophyll content, MDA content and enzyme activity. After that, the harvested peanuts were split four parts, including roots, shoots, shells and kernels and then rinsed thoroughly in deionized water and oven-dried at 80 °C to a constant weight before biomass measurements. The Cd concentrations of different peanut tissues were measured by placing them in 5 mL of pure HNO3, letting them stand for 12 h, and then using a tubular digestion instrument (XJS36-42W, Laboratory) to conduct the digestion measurements. The total Cd contents in each tissue of the peanut were determined by using inductively coupled plasma mass spectrometry (ICP-MS, Perkin Elmer NexION 300X, USA) under optimization of measurement conditions. Reagent blanks were used in each batch of samples. Each experiment was executed in triplicate.
A method similar to that of Booker and Fiscus24 was used for chlorophyll extraction. Calculated chlorophyll contents were calculated according to Lichtenthaler and Wellburn25.
Catalase (CAT) activity was determined by the method of Beer and Sizer26 as follows. Fresh leaf (0.5 g) was homogenized in a mortar with 4 mL phosphate buffer (pH 7.0). Extract was centrifuged at 4000 rpm for 15 min. CAT activity was measured in the supernatant using 1.9 mL of reagent-grade water, 1.0 mL of H2O2 as substrate and 0.1 mL of extract, and expressed (U g−1 min−1 FW) as changes in optical density (OD) at 240 nm.
For the assessment of peroxidase (POD), samples were homogenized in 50 mM potassium phosphate buffer (pH 7.0), which contained 0.1 mM ethylene diamine tetraacetic acid (EDTA) and 1 mM dithiothreitol (DTT). The POD activity was calculated using method described by Chance and Maehly27 with few adjustments28. For POD assessment, the mixture (3 ml) comprised of 50 mM phosphate buffer (pH 7.0), 20 mM guaiacol, 40 mM H2O2 and 0.1 ml of enzyme extract which was added to start the reaction. The change in absorbance of the solution at 470 nm was read on spectrophotometer.
Activity of superoxide dismutase (SOD) was assayed according to Beauchamp and Fridovich29, with slight modification30. The activity was assayed by measuring its ability to inhibit the photochemical reduction of nitro blue tetrazolium (NBT). The reaction mixture contained 13 mM riboflavin, 13 mM methionine, 63 mM NBT, and 50 mM potassium phosphate buffer (pH 7.8). Absorbance was then measured at 560 nm. One unit of SOD activity was defined as the amount of enzyme, which causes a 50% decrease of the inhibition of NBT reduction.
The MDA content was assayed by the thiobarbituric acid method according to Peever and Higgins31. Briefly, the fresh leaves (0.2 g) were homogenized in 10% trichloroacetic acid (5 mL) and centrifuged at 12,000×g for 10 min. The mixture containing the supernatant (2 mL) and 0.5% thiobarbituric acid (2 mL) was placed in a boiling water bath. After 15 min, the mixture was rapidly cooled and then centrifuged at 12,000×g for 10 min. The absorbance of the supernatant was determined at 450, 532, and 600 nm using a spectrometer. The following formula was used to calculate the MDA content:
The phytoaccumulation ability of peanut was estimated by detecting the bioaccumulation factor (BCF) and translocation factor (TCF) and by using these equationns32:
Data analysis
All values of the determined parameters are the averages of three duplicates. The results are reported as mean values ± SD. Microsoft Excel 2016 and SPSS 19.0 software were used to conduct statistical analysis and data processing, and figures were drawn with Origin 8.5 software. Differences at p < 0.05 were believed to be significant.
Results and discussion
Soil pH, biomass and Cd content of peanut
Soil pH
Figure 1 shows that, in this study, application of slaked lime significantly increased soil pH in nearly all growth stages (p < 0.05). The following general pH trend with increasing application rates of slaked lime during the growth stages was observed: C1500 > C1200 > C900 > C600 > C300 > C0. Among the soil characteristics, soil pH is considered as an important index that impact Cd uptake by crops, since pH can obviously affect the speciation and solubility of Cd in soil liquids15. The use of slaked lime can neutralize excessive H+ concentrations in soil solutions and decrease Cd solubility33, but there were no observable differences among the different growth stages.
Compared with C0, soil pH increased by 3.3, 12.92, 16.88, 25.0, and 28.96% at the seeding stage; 5.86, 20.08, 22.18, 28.45, and 34.1% at the pod-pin stage; 4.74, 7.01, 19.79, 23.92, and 27.84% at the pod bearing stage; and 1.4, 2.2, 14.37, 23.35, and 24.95% at the maturity stage for the C300, C600, C900, C1200 and C1500 treatments, respectively. Slaked lime is an alkaline substance that can increase soil pH by increasing metal precipitation and ion adsorption34, increasing soil adsorption and promoting changes from soluble metals to residuals35. In the present study, the pristine soil pH was between 4.5–5.5, which was considered to be a strong acid soil. Lower soil pH may cause high metal ion availability because of the greater competition between free metal ions and protons for binding on soil surfaces36. Application of slaked lime could induce changes in carbonate or hydroxide precipitation or by enhancing adsorption sites by inducing deprotonation at the soil surface37.
Biomass of peanut
As shown in Table 2, for the root biomass, there were no significant effects from the slaked lime applications in the seeding, pod-pin and pod bearing stages, with the exception of the maturity stage (p < 0.05). Compared with C0, root biomass increased by 22.95% at the maturity stage for the C300 treatment. Under slaked lime applications, there were significant differences in shoot biomass at all growth stages except for the seeding stage (p < 0.05). Compared with C0, shoot biomass increased by 61.64% at the pod-pin stage, 58.4% at the pod-bearing stage for the C1500 treatment, and increased by 4% at the maturity stage for the C300 treatment. Pod biomass describes peanut productivity38. The biomass in shells and kernels showed an increasing trend under higher application rates of slaked lime at the maturity stage. Compared with C0, shell biomass increased by 23.08, 54.03, 57.97, 60.6, and 79.18% and kernel biomass increased by 0.30, 28.39, 44.89, 46.78, and 77.23% for the C300, C600, C900, C1200, and C1500 treatments, respectively.
Cd toxicity directly affects net CO2 assimilation and the transportation of photosynthetic electrons and indirectly reduces chlorophyll concentrations (by indirectly inhibiting chlorophyll biosynthesis) or by preventing the photosynthetic process at different levels of its tissues, the lipid and protein ingredients of thylakoid membranes, and chloroplast fine structure39. It has been widely demonstrated that addition of slaked lime to acidic soils very strongly and directly enhances crop productivity by improving the soil physical–chemical and biological characteristics, which ultimately boost the mobility and availability of essential crop nutrients33.
Soil nutrients that are crucial for plant growth include OM, N, P and K. The nutrient contents in heavy-metal-contaminated soil comprise a pivotal factor that affects seed germination and plant settlement40. Agegnehu et al.41 and Melo et al.42 reported that soil amendments lead to higher plant uptake of C, N, P and K, as well as increased availability of soluble organic carbon (SOC) in soil due to changes in soil pH. Therefore, chlorophyll contents and plant yields were improved.
Slaked lime contains large amounts of the Ca nutrient. Ca is an essential main element for plant growth and accounts for 0.1–5% of dry plant biomass7. It is the second messenger in signal transition and plays a key role in crop cell supersession, signal shift, and nutrient uptake over cell membranes43. Peanut is a calciphilic crop, and peanut yields in acidic soil are often limited by a lack of Ca rather than by a lack of other plant nutrients. In peanut, exogenous application of Ca2+ can improve plant stress resistance by enhancing PSII efficiency, boosting the activities of antioxidant enzymes (e.g., SOD and CAT), and decreasing MDA content under stress14,44.
Cd content of peanut
Cd uptake clearly decreased in nearly all growth stages when the rates of slaked lime application increased (p < 0.05) (Fig. 2). Compared with C0, the Cd contents in roots decreased by 17.07, 22.84, 52.16, 67.79, and 53.85% at the seeding stage; 23.62, 30.32, 58.02, 55.39, and 70.55% at the pod-pin stage; 3.13, 26.65, 61.31, 63.68, and 71.27% at the pod-bearing stage; and 19.39, 29.01, 30.90, 40.23, and 53.79% at the maturity stage for the C300, C600, C900, C1200 and C1500 treatments, respectively (Fig. 2a).
For the Cd contents in shoots, obvious reductions were found with increasing application rates of slaked lime in nearly all growth stages (p < 0.05). Compared with C0, the Cd contents in shoots decreased by 7.36, 15.20, 42.52, 43.47, and 57.96% at the seeding stage; 18.32, 44.67, 52.90, 63.93, and 72.52% at the pod-pin stage; 6.64, 28.05, 41.03, 50.94, and 62.64% at the pod bearing stage; and 13.09, 23.68, 29.11, 30.08, and 30.92% at the maturity stage for the C300, C600, C900, C1200 and C1500 treatments, respectively (Fig. 2b).
Similarly, the Cd contents in shells showed a decreasing trend that was similar to those for roots and shoots in the maturity stage (p < 0.05), and these contents decreased by 5.76, 23.02, 41.73, 42.45, and 43.17% for the C300, C600, C900, C1200 and C1500 treatments compared to C0, respectively (Fig. 2c).
Peanut kernels contain large amounts of protein and oil and are a crucial oil source in the food processing industry, therefore, pollution by heavy metals in peanut kernels is an important concern for food security and international business45. Figure 2d shows that the Cd concentrations in peanut kernels were greater than the maximum approved levels defined by the National Food Safety Standard of Contaminants in Foods (GB2762-2017). However, the Cd contents markedly decreased with increasing rates of slaked lime and decreased by 8.57, 43.81, 43.81, 47.62, and 50.48% in the C300, C600, C900, C1200 and C1500 treatments, respectively, when compared to C0. In addition, the process of absorbing Cd by peanut shells and seeds is almost simultaneous. Therefore, Cd accumulation was similar between peanut shells and kernels. Furthermore, previous study has shown that mechanisms of Cd immobilization affected by slaked lime are principally due to the changes in soil Cd availability and crops root absorption instead of internal translocation in plants12.
Generally, one of the most effective remediation options for eliminating Cd is the improvement of soils and minimization of metal bioavailability. The bioavailability of metals can be minimized via chemical and biological immobilization by using a series of inorganic compounds, which include clay minerals, P compounds, and lime, as well as organic amendments46.
Slaked lime is employed to mitigate soil acidity; simultaneously, it has gained wide acceptance as a popular choice in the scientific community due to its ability to decrease heavy metal toxicity in soils. For many years, liming has been accepted as a conventional treatment to reduce Cd contents in the edible parts of farmland crops46.
The results indicated that peanuts exhibited good adsorption capacity for Cd, and the differences in uptake among the different tissues at various growth stages may be related to the application rates of slaked lime. Soil pH affected Cd transportation from soil to roots and improved metal absorption onto soil particles15. Due to the competition between Ca and Cd for uptake by crop roots, the higher Ca concentrations in lime strongly reduced Cd adsorption by farmland crops. It has been accepted that competition between Ca2+ and Cd2+ is one of the crucial influences for suppressing Cd mobility and therefore remarkably enhanced Ca concentrations and decreased Cd accumulations in crops33. In addition, increasing soil pH usually results in the formation of more negatively charged sorption sites, hydroxyl species of positive metal ions, and sedimentation of Cd2+ as Cd(OH)2 and leads to a reduction in soil Cd availability12. Previous studies have indicated that Cd addition in the soil did not inhibit the formation of external hyphae and mycorrhizal colonization47,48,49, which maybe the reason of Cd translocation excessive, this mechanism will continue to be discussed in future studies.
Effect of Cd absorption by peanut
Cd accumulation in peanut
The effects of slaked lime on Cd accumulation in the tissues of peanuts at various growth stages are presented in Table 3. With the application of slaked lime, at the pod-bearing stage, Cd accumulations in shoots and roots of peanuts were higher in the C300 treatment than in the C0 treatment, however, it has a decreasing trend with the increasing of slaked lime. This result indicated that slaked lime at quantities of 300 kg ha−1 had not reduced the content of Cd markedly in roots and shoots at the pod-bearing stage. Pod bearing is a crucial stage in which peanuts absorb nutrients to increase the number of pods and kernel filling of peanuts50. However, lower slaked lime levels reduced Cd immobilization34.
The lowest Cd accumulations in roots were observed for the C1200 treatment (seeding stage), C1500 treatment (pod-pin stage), C1200 treatment (pod bearing stage) and C1500 treatment (maturity stage). Moreover, the lowest Cd accumulations in shoots were for the C900 treatment (seeding stage), C1500 treatment (pod-pin stage), C1500 treatment (pod bearing stage) and C900 treatment (maturity stage). With respect to the shells and kernels, the lowest Cd accumulations were for the C1500 and C300 treatments in the maturity stage, respectively. These results demonstrate that there were significant differences in the rates of slaked lime application among the growth stages.
Peanut is considered to be a higher metal accumulator among crops and is thereby applicable for the absorption of heavy metals, with its roots usually gathering much higher concentrations51. In contrast, with the addition of slaked lime, the biomass and Cd content (Table 2 and Fig. 2) in shoots were obviously higher than those in roots. This result indicated that higher Cd accumulations in shoots than in roots. This may be due to the high genotypic variations in Cd accumulation between cultivars12.
BCF and TCF value of Cd in peanut
The bioconcentration factor (BCF) is generally defined as the proportion of metal content in crop tissues to that in soil. The translocation factor (TCF) measures the ability of a crop to transport metals from roots to shoots15.
BCFs obviously decreased for different tissues when the rates of slaked lime application increased (p < 0.05) (Table 4). Compared with C0, BCFs for the roots decreased by 22.46, 32.44, 59.00, 74.87, and 64.88% at the seeding stage; 29.72, 40.16, 64.17, 66.73, and 79.33% at the pod-pin stage; 3.16, 33.03, 67.08, 65.16, and 73.84% at the pod bearing stage and 19.82, 42.91, 47.37, 53.82, and 64.72% at the maturity stage for the C300, C600, C900, C1200 and C1500 treatments, respectively. The BCFs for the shoots, compared with C0, decreased by 13.38, 25.53, 50.70, 55.81, and 68.13% at the seeding stage; 24.84, 52.59, 59.52, 73.14, and 80.58% at the pod-pin stage; 6.60, 33.88, 49.76, 53.62, and 65.96% at the pod bearing stage and 13.62, 38.69, 45.98, 45.98, and 47.30% at the maturity stage for the C300, C600, C900, C1200 and C1500 treatments, respectively. In addition, compared with C0, BCFs for the shells and kernels decreased by 29.43, 60.00, 74.72, 79.62, and 83.40% and by 18.75, 45.00, 50.00, 53.75, and 58.75% at the maturity stage for the C300, C600, C900, C1200 and C1500 treatments, respectively.
The accumulation efficiency of metals is characterised by the BCF, and higher BCFs of metals in aboveground sections may lead to hazards for grazers and dissemination of metals in the environment via wind or water15. Therefore, management steps and rational methods for polluted crop treatments, such as liming, should be employed to decrease the hazards that contaminate the food cycle or environment52.
The higher TCFs, the higher Cd content uptake and translocation by plants53. A TCF value above 1 indicates a high capacity for plants to translocate metals54. The results of the TCFs obtained are presented in Table 5. Except for the C1500 treatment in the seeding stage, the TCF values were above 1 for nearly all treatments, which demonstrated the higher tolerance to Cd for peanut in its growth stages. As a conventional common trace metal passivating agent, the efficiency of slaked lime application is related to the application rates55. As shown in Table 5, there were significant differences among the application rates of slaked lime during the growth stages (p < 0.05). Higher Ca content in lime reduces crop uptake of accumulated Cd due to competing Ca and Cd uptake in plant roots56. Previous studies have indicated that the competition between Ca2+ and Cd2+ was one of the crucial reasons for the inhibition of Cd migration, thereby significantly enhancing the Ca content in plants and decreasing the accumulation of Cd in plants33,56,57. Besides, too high soil pH can lead to the dissolution of heavy metals. Within a certain range, the increase of soil pH will enhance the uptake of heavy metals, however, the mobility of heavy metals decreases due to the formation of hydroxyl complexes under strong alkaline conditions, which ultimately leads to metal precipitation33,58,59. This indicated that the optimal amount of slaked lime in this experiment was 900 kg ha−1. De Maria and Rivelli60 reported higher Cd accumulations in roots and older leaves of sunflower at the blossom bud stage, while Cd remigrated at the maturity stage. These results indicated that heavy metal accumulations in the roots in the early growth stages and the transfer to shoots at more mature stages may be a strategy that was utilized by sunflowers to address heavy metal stress. We speculated that peanut, which is an oil crop, may have a similar ability as sunflower.
Effects of slaked lime on the physiological and biochemical characteristics of peanut
Chlorophyll content
Chlorophyll content is an important index for indicating environmental stress in plants and reflects plant tolerance. In addition, chlorophyll content has been considered to be a reliable stress-induced biomarker to assess heavy metal-induced phytotoxicity in a variety of farmland crops61.
Figure 3a shows that the application of slaked lime significantly enhanced chlorophyll contents except for the pod-pin stage (p < 0.05) and that the variations in chlorophyll content were related to the application rates of slaked lime. Compared with C0, the chlorophyll contents increased by 10.53% for the C300 treatment at the seeding stage; 1.3, 3.93, 16.62, and 12.12 and 11.65% for the C300, C600, C900, C1200, and C1500 treatments at the pod-bearing stage, respectively, and by 0.68% for the C1200 treatment at the maturity stage.
Higher chlorophyll contents were observed in the seeding stage than in the pod-pin stage (Fig. 3a). The main reason is that the chlorophyll contents of peanut increased at the initial stage under mild and moderate Cd stress but decreased as the Cd contents of peanut increased45. Subsequently, slaked lime increased soil pH and reduced Cd availability by improving the surface areas and numbers of special sorption sites for Cd and constituted insoluble metal compounds of higher stability in soil, which decreased the impact of Cd stress on the plants62. Also, application of slaked lime improved the quantity of nutrients for peanuts and enhanced the mineral metabolism of plant Fe (a co-factor related to chlorophyll biosynthesis) and Mn transport63. Furthermore, the correlation between chlorophyll contents and application rates of slaked lime may offer reliable information for the reliability of the rate of slaked lime that is determined to be necessary for application to polluted soil to obtain the expected standard of photosynthesis efficiency and CO2 sequestration64.
MDA content
In general, Cd-induced oxidative problems increased MDA content by generating higher reactive oxygen species (ROS) levels; therefore, observation of MDA in crop tissues could be considered as a criterion of oxidative harm. Obviously, slaked lime significantly influenced the MDA content of peanuts except at the seeding stage (p < 0.05) (Fig. 3b). This effect may be due to the enhanced antioxidant defence system in peanut under Cd stress under application of slaked lime65.
On the one hand, compared with C0, the MDA contents decreased by 47.94, 49.15, 46.85, and 48.18% and by 47.04, 26.48, 33.96, and 22.74% for the C600, C900, C1200, C1500 treatments at the pod-pin and pod bearing stages, respectively. Furthermore, the MDA contents decreased by 31.22, 53.96, 60.85, 51.32 and 66.67% for the C300, C600, C900, C1200, C1500 treatments at the maturity stage, respectively, compared to C0.
Slaked lime acts as a soil conditioner that further increases OM, Ca and major nutrient (e.g., N, P and K) concentrations that are essential for plant growth50. OM and nutrition (particularly N and P) may be related to the combination of polyphenols present and increased activity of phenylalanine ammonia-lyase, which would increase phenolic concentrations and lead to stress alleviation for the crop. Phenolics may be related to the alleviation of metal-induced stress, and flavonoids and phenolics play the role of energetic antioxidants that support ROS alleviation50. K aids in the reduction of O2− and decreases the danger of OH− generation under metal stress66. N provides nutrition for peanuts and facilitates the generation of organic acid–metal complexes in peanut tissues, which mitigate Cd poisoning67.
CAT, POD and SOD activity
Antioxidant enzymes, such as CAT, POD and SOD, represent the physiological reactions of crops to reject oxidative stress that is caused by many abiotic stress components34.
Liming substantially influenced antioxidant enzyme activities (p < 0.05) in the leaves of peanut under Cd-polluted soil68. Figure 4a shows that, with applications of slaked lime, CAT activities showed significant differences at various growth stages except for the pod-pin stage (p < 0.05). Compared with C0, CAT activities for the pod bearing stage increased by 82.98, 85.96, 97.13, 106.38 and 153.51% for the C300, C600, C900, C1200 and C1500 treatments, respectively. However, CAT activities decreased by 17.64, 48.78, 34.38, 67.84 and 57.71% and by 12.34, 18.69, 27.99, 32.55, and 37.03% at the seeding and maturity stages for the C300, C600, C900, C1200 and C1500 treatments, respectively, compared to C0.
Compared with C0, notable reductions (p < 0.05) were observed for POD activities in the C300 (22.58%), C600 (21.67%), C1200 (51.35%), and C1500 (17.09%) treatments at the seeding stage; C600 (29.87%), C900 (36.99%), C1200 (32.4%), and C1500 (30.9%) at the pod-pin stage; and C600 (48.47%) and C1200 (38.42%) treatments at the pod bearing stage, respectively. However, compared with the other stages, POD activities significantly decreased (p < 0.05) at the maturity stage, and the highest and lowest values were observed for the C300 and C1500 treatments, respectively (Fig. 4b).
Furthermore, for the SOD activities, we observed no remarkable differences (p < 0.05) among all treatments at the seedling stage (Fig. 4c). Compared with C0, SOD activities increased by 37.37, 98.73 and 129.73% for the C300, C600 and C1200 treatments, respectively, but decreased by 1.06 and 91.09% for the C900 and C1500 treatments at the pod-pin stage, respectively. Moreover, the highest SOD activity was recorded for C0, whereas other treatments with slaked lime application led to 17.11, 54.74, 47.02, 84.07 and 29.62%, and to 9.13, 19.57, 22.29, 47.36, 12.54% reductions in SOD activities at the pod bearing and maturity stages, respectively.
The activities of antioxidant enzymes, such as SOD and CAT, in crops can alleviate oxidative stress and neutralize ROS toxicity caused by metals50. Within crop cells, SOD provides the front line of protection by transforming O2− into H2O2. Next, SOD further detoxifies and/or transforms to H2O and O2 with the involvement of CAT. Moreover, POD is regarded as another antioxidant enzyme that transforms H2O2 into O2 and H2O69.
It was previously mentioned that OM and the main nutrients, such as N and P, are the main components which alter SOD and CAT activities70. Essential nutrients, mainly K, can promote the activity of these enzymes when the crop is under metal stress. K aids in the transportation of water and nutrition via the xylem and may further promote the involvement of many other latent enzymes61. Therefore, with the application of slaked lime, supplementing with K increased H2O2 detoxification due to increased SOD and CAT activity50.
Correlation analysis
Figure 5 shows the correlations between the application rates of slaked lime and peanut biomass, Cd content of peanut, and chlorophyll content, MDA content and antioxidant enzyme activity of leaves. Lime application rates (L ar) were significantly positively correlated with soil pH, and a noteworthy negative correlation was found between the Cd and L ar contents of peanut tissues for all growth stages. This result agreed with previous studies that indicated that liming addition in Cd-contaminated soil increased soil pH71, and with another study that reported that soil pH was negatively correlated with heavy metal availability in crops72.
With the exception of the seeding stage, L ar was significantly negatively correlated with MDA, which may be due to the activation of the antioxidant defence system, while the impact of slaked lime on MDA was not significantly different at the seeding stage (Fig. 3b). Cd is a nonessential, toxic heavy metal that can promote ROS generation by inhibiting the antioxidant defence system and transportation of electrons in photosystem II. Overgeneration of ROS induces production of higher MDA levels73. Significant positive correlations were noted between L ar and SLB and KB at the maturity stage. Previous studies have shown that slaked lime significantly increased soil pH, alleviated the toxicity of Cd to the photosystem, boosted chlorophyll content, and improved yields45.
Moreover, there were obvious differences between L ar and enzyme activities at different growth stages. Figure 5 shows that L ar was significantly negatively correlated with CAT, POD (seeding stage), POD (pod-pin stage), CAT, and SOD (maturity stage) and was significantly positively correlated with CAT (pod bearing stage). These results indicated that there were significant correlations among the L ar, soil pH, Cd contents in peanut tissues, MDA contents and antioxidant enzyme activities (e.g., CAT, POD, and SOD) at different growth stages.
Conclusion
This research points out that slaked lime application clearly improved soil pH, decreased Cd contents in peanut tissues, and enhanced peanut yields in the maturity stage in Cd-contaminated soil. The results show that L ar was significantly positively correlated with soil pH, and negatively correlated with the Cd and MDA contents of peanut tissues for all growth stages, moreover, SLB and KB were enhanced when L ar increased in the maturity stage, while the relationship between L ar and antioxidant enzyme activity and chlorophyll content varied in the different growth stages. The peanut with higher Cd uptake may have a similar trend to the results of this experimental variety, but the specific situation needs to be further analysed in the future. Besides, further field experimental studies are still needed to elucidate the physiological and molecular mechanisms of slaked lime in increasing Cd immobilization and productivity of peanut plants.
References
Zhi, Y., Sun, T., Zhou, Q. & Leng, X. Screening of safe soybean cultivars for cadmium contaminated fields. Sci. Rep. 10, 1–12 (2020).
Khan, M. A., Khan, S., Khan, A. & Alam, M. Soil contamination with cadmium, consequences and remediation using organic amendments. Sci. Total Environ. 601–602, 1591–1605 (2017).
Zhang, Q. et al. Effect of the direct use of biomass in agricultural soil on heavy metals—Activation or immobilization?. Environ. Pollut. 272, 115989 (2021).
Chen, X., He, H. Z., Chen, G. K. & Li, H. S. Effects of biochar and crop straws on the bioavailability of cadmium in contaminated soil. Sci. Rep. 10, 1–12 (2020).
Zhao, F., Ma, Y., Zhu, Y., Tang, Z. & Mcgrath, S. P. Soil contamination in China: Current status and mitigation strategies. Environ. Sci. Technol. 49, 750–759 (2015).
He, Y. et al. A three-season field study on the in-situ remediation of Cd-contaminated paddy soil using lime, two industrial by-products, and a low-Cd-accumulation rice cultivar. Ecotoxicol. Environ. Saf. 136, 135–141 (2017).
Cui, L. et al. Arbuscular mycorrhizal fungi combined with exogenous calcium improves the growth of peanut (Arachis hypogaea L.) seedlings under continuous cropping. J. Integr. Agric. 18, 407–416 (2019).
Yang, B. et al. Survey of aflatoxin B1 and heavy metal contamination in peanut and peanut soil in China during 2017–2018. Food Control 118, 1–8 (2020).
Zhang, J., Geng, Y., Guo, F., Li, X. & Wan, S. B. Research progress on the mechanism of improving peanut yield by single-seed precision sowing. J. Integr. Agric. 19, 1919–1927 (2020).
Du, L. et al. Effects of different stoichiometric ratios on mineralisation of root exudates and its priming effect in paddy soil. Sci. Total Environ. 743, 140808 (2020).
Li, L. et al. Enhancing cadmium extraction potential of Brassica napus: Effect of rhizosphere interactions. J. Environ. Manag. 284, 112056 (2021).
Guo, F., Ding, C., Zhou, Z., Huang, G. & Wang, X. Effects of combined amendments on crop yield and cadmium uptake in two cadmium contaminated soils under rice-wheat rotation. Ecotoxicol. Environ. Saf. 148, 303–310 (2018).
Wang, A. et al. Speciation and environmental risk of heavy metals in biochars produced by pyrolysis of chicken manure and water-washed swine manure. Sci. Rep. 11, 1–14 (2021).
Hamid, Y. et al. Immobilization of cadmium and lead in contaminated paddy field using inorganic and organic additives. Sci. Rep. 8, 1–10 (2018).
Ou, J. et al. In situ immobilisation of toxic metals in soil using Maifan stone and illite/smectite clay. Sci. Rep. 8, 1–9 (2018).
Kong, L., Guo, Z., Peng, C., Xiao, X. & He, Y. Factors influencing the effectiveness of liming on cadmium reduction in rice: A meta-analysis and decision tree analysis. Sci. Total Environ. 779, 146477 (2021).
Yang, Y., Li, Y., Wang, M., Chen, W. & Dai, Y. Limestone dosage response of cadmium phytoavailability minimization in rice: A trade-off relationship between soil pH and amorphous manganese content. J. Hazard. Mater. 403, 123664 (2021).
He, L. L. et al. Meta-analysis of the effects of liming on soil pH and cadmium accumulation in crops. Ecotoxicol. Environ. Saf. 223, 112621 (2021).
Zhu, Q. H. et al. Sepiolite is recommended for the remediation of Cd-contaminated paddy soil. Acta Agric. Scand. Sect. B Soil Plant Sci. 60, 110–116 (2010).
He, H. et al. Effects of alkaline and bioorganic amendments on cadmium, lead, zinc, and nutrient accumulation in brown rice and grain yield in acidic paddy fields contaminated with a mixture of heavy metals. Environ. Sci. Pollut. Res. 23, 23551–23560 (2016).
de Campos, M., Penn, C. J., Gonzalez, J. M. & Alexandre Costa Crusciol, C. Effectiveness of deep lime placement and tillage systems on aluminum fractions and soil chemical attributes in sugarcane cultivation. Geoderma 407, 115545 (2022).
Jiang, Y. et al. Responses of microbial community and soil enzyme to heavy metal passivators in cadmium contaminated paddy soils: An in situ field experiment. Int. Biodeterior. Biodegrad. 164, 105292 (2021).
Verstraeten, G. et al. Tree species effects are amplified by clay content in acidic soils. Soil Biol. Biochem. 121, 43–49 (2018).
Booker, F. L. & Fiscus, E. L. The role of ozone flux and antioxidants in the suppression of ozone injury by elevated CO2 in soybean. J. Exp. Bot. 56, 2139–2151 (2005).
Lichtenthaler, H. K. & Wellburn, A. R. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem. Soc. Trans. 11, 591–592 (1983).
Beers, R. F. & Sizer, I. W. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem. 195, 133–140 (1952).
Chance, B. & Maehly, A. C. [136] Assay of catalases and peroxidases. Methods Enzymol. 2, 764–775 (1955).
Farid, M. et al. Exogenous application of ethylenediamminetetraacetic acid enhanced phytoremediation of cadmium by Brassica napus L. Int. J. Environ. Sci. Technol. 12, 3981–3992 (2015).
Beauchamp, C. & Fridovich, I. Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 44, 276–287 (1971).
Konkolewska, A. et al. Combined use of companion planting and PGPR for the assisted phytoextraction of trace metals (Zn, Pb, Cd). Environ. Sci. Pollut. Res. 27, 13809–13825 (2020).
Peever, T. L. & Higgins, V. J. Electrolyte leakage, lipoxygenase, and lipid peroxidation induced in tomato leaf tissue by specific and nonspecific elicitors from Cladosporium fulvum. Plant Physiol. 90, 867–875 (1989).
Zhan, J., Li, T., Zhang, X., Yu, H. & Zhao, L. Rhizosphere characteristics of phytostabilizer Athyrium wardii (Hook.) involved in Cd and Pb accumulation. Ecotoxicol. Environ. Saf. 148, 892–900 (2018).
Liu, Z. et al. Effects and mechanism of continuous liming on cadmium immobilization and uptake by rice grown on acid paddy soils. J. Soil Sci. Plant Nutr. 20, 2316–2328 (2020).
Huang, S. et al. Application of inorganic passivators reduced Cd contents in brown rice in oilseed rape-rice rotation under Cd contaminated soil. Chemosphere 259, 1–36 (2020).
Wang, S. et al. Speciation and phytoavailability of cadmium in soil treated with cadmium-contaminated rice straw. Environ. Sci. Pollut. Res. 22, 2679–2686 (2015).
Ardestani, M. M. & Van Gestel, C. A. M. Using a toxicokinetics approach to explain the effect of soil pH on cadmium bioavailability to Folsomia candida. Environ. Pollut. 180, 122–130 (2013).
Miura, K. et al. Effect of liming using a partial mixing technique on reductions in the seed cadmium levels for soybeans (Glycine max (L.) Merr.) under field conditions. Soil Sci. Plant Nutr. 62, 201–211 (2016).
Rachaputi, R., Chauhan, Y. S. & Wright, G. C. Chapter 11 Peanut. Crop Physiol. Case Hist. Major Crop. Vadez, 360–382 (2021).
Dobrikova, A. G. & Apostolova, E. L. Damage and protection of the photosynthetic apparatus under cadmium stress. in Cadmium Toxicity and Tolerance in Plants 275–298 (Elsevier, 2019). https://doi.org/10.1016/B978-0-12-814864-8.00011-5
Yu, H., Xiang, Y. & Zou, D. The effect of Eulaliopsis binata on the physi-chemical properties, microbial biomass, and enzymatic activities in Cd–Pb polluted soil. Environ. Sci. Pollut. Res. 23, 19212–19218 (2016).
Agegnehu, G. et al. Biochar and biochar-compost as soil amendments: Effects on peanut yield, soil properties and greenhouse gas emissions in tropical North Queensland, Australia. Agric. Ecosyst. Environ. 213, 72–85 (2015).
Melo, L. C. A. et al. Sorption and desorption of cadmium and zinc in two tropical soils amended with sugarcane-straw-derived biochar. J. Soils Sediments 16, 226–234 (2016).
Ahmad, P. et al. Calcium and potassium supplementation enhanced growth, osmolyte secondary metabolite production, and enzymatic antioxidant machinery in cadmium-exposed chickpea (Cicer arietinum L.). Front. Plant Sci. 7, 1–12 (2016).
Yang, S. et al. Exogenous calcium alleviates photoinhibition of PSII by improving the xanthophyll cycle in peanut (Arachis hypogaea) leaves during heat stress under high irradiance. PLoS One 8, 1–10 (2013).
Gao, F. et al. Effects of cadmium stress on physiological characteristics, pod yield, and kernel quality in peanut. Acta Agron. Sin. 37, 2269–2277 (2012).
Mahar, A., Wang, P., Li, R. & Zhang, Z. Immobilization of lead and cadmium in contaminated soil using amendments: A review. Pedosphere 25, 555–568 (2015).
Jiang, Q. Y. et al. Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd-added soils?. Sci. Rep. 6, 2–10 (2016).
Chen, B. D., Liu, Y., Shen, H., Li, X. L. & Christie, P. Uptake of cadmium from an experimentally contaminated calcareous soil by arbuscular mycorrhizal maize (Zea mays L.). Mycorrhiza 14, 347–354 (2004).
Jiang, Q. Y. et al. Effect of Funneliformis mosseae on the growth, cadmium accumulation and antioxidant activities of Solanum nigrum. Appl. Soil Ecol. 98, 112–120 (2016).
Salam, M. M. A., Mohsin, M., Pulkkinen, P., Pelkonen, P. & Pappinen, A. Effects of soil amendments on the growth response and phytoextraction capability of a willow variety (S. viminalis × S. schwerinii × S. dasyclados) grown in contaminated soils. Ecotoxicol. Environ. Saf. 171, 753–770 (2019).
Yu, R. et al. Comparative proteomics analysis of peanut roots reveals differential mechanisms of cadmium detoxification and translocation between two cultivars differing in cadmium accumulation. BMC Plant Biol. 19, 1–15 (2019).
Yang, Y. et al. Comparison of three types of oil crop rotation systems for effective use and remediation of heavy metal contaminated agricultural soil. Chemosphere 188, 148–156 (2017).
Cai, X. et al. Biomass allocation strategies and Pb-enrichment characteristics of six dwarf bamboos under soil Pb stress. Ecotoxicol. Environ. Saf. 207, 111500 (2021).
Cojocaru, P., Gusiatin, Z. M. & Cretescu, I. Phytoextraction of Cd and Zn as single or mixed pollutants from soil by rape (Brassica napus). Environ. Sci. Pollut. Res. 23, 10693–10701 (2016).
Park, J. H. et al. Role of organic amendments on enhanced bioremediation of heavy metal(loid) contaminated soils. J. Hazard. Mater. 185, 549–574 (2011).
Li, P. et al. Calcium alleviates cadmium-induced inhibition on root growth by maintaining auxin homeostasis in Arabidopsis seedlings. Protoplasma 253, 185–200 (2016).
Wang, Q. et al. Effects of exogenous nitric oxide on cadmium toxicity, element contents and antioxidative system in perennial ryegrass. Plant Growth Regul. 69, 11–20 (2013).
Rees, F., Germain, C., Sterckeman, T. & Morel, J. L. Plant growth and metal uptake by a non-hyperaccumulating species (Lolium perenne) and a Cd-Zn hyperaccumulator (Noccaea caerulescens) in contaminated soils amended with biochar. Plant Soil 395, 57–73 (2015).
Wang, A. S., Angle, J. S., Chaney, R. L., Delorme, T. A. & Reeves, R. D. Soil pH effects on uptake of Cd and Zn by Thlaspi caerulescens. Plant Soil 281, 325–337 (2006).
De Maria, S. & Rivelli, A. R. Trace element accumulation and distribution in sunflower plants at the stages of flower bud and maturity. Ital. J. Agron. 8, 65–72 (2013).
Naciri, R., Lahrir, M., Benadis, C., Chtouki, M. & Oukarroum, A. Interactive effect of potassium and cadmium on growth, root morphology and chlorophyll a fluorescence in tomato plant. Sci. Rep. 11, 5384 (2021).
Kumarpandit, T. et al. Influence of organic manure and lime on cadmium mobility in soil and uptake by spinach (Spinacia oleracea L.). Commun. Soil Sci. Plant Anal. 48, 357–369 (2017).
Bianucci, E. et al. Contribution of phytochelatins to cadmium tolerance in peanut plants. Metallomics 4, 1119–1124 (2012).
Jaskulak, M., Rorat, A., Grobelak, A. & Kacprzak, M. Antioxidative enzymes and expression of rbcL gene as tools to monitor heavy metal-related stress in plants. J. Environ. Manag. 218, 71–78 (2018).
Marques, D. N. et al. Antioxidant defense response in plants to cadmium stress. in Cadmium Tolerance in Plants 423–461 (Elsevier, 2019). https://doi.org/10.1016/B978-0-12-815794-7.00016-3
Ramana Gopavajhula, V. et al. Modeling and analysis of soybean (Glycine max L.) Cu/Zn, Mn and Fe superoxide dismutases. Genet. Mol. Biol. 36, 225–236 (2013).
Novak, J. M. et al. Remediation of an acidic mine spoil: Miscanthus biochar and lime amendment affects metal availability, plant growth, and soil enzyme activity. Chemosphere 205, 709–718 (2018).
Fageria, N. K. & Baligar, V. C. Chapter 7 Ameliorating soil acidity of tropical oxisols by liming for sustainable crop production. Adv. Agron. 99, 345–399 (2008).
You, J. & Chan, Z. Ros regulation during abiotic stress responses in crop plants. Front. Plant Sci. 6, 1–15 (2015).
Mehmood, S. et al. Impact of different amendments on biochemical responses of sesame (Sesamum indicum L.) plants grown in lead-cadmium contaminated soil. Plant Physiol. Biochem. 132, 345–355 (2018).
Zhu, H., Chen, C., Xu, C., Zhu, Q. & Huang, D. Effects of soil acidification and liming on the phytoavailability of cadmium in paddy soils of central subtropical China. Environ. Pollut. 219, 99–106 (2016).
Zeng, F. et al. The influence of pH and organic matter content in paddy soil on heavy metal availability and their uptake by rice plants. Environ. Pollut. 159, 84–91 (2011).
Al Mahmud, J., Hasanuzzaman, M., Nahar, K., Bhuyan, M. H. M. B. & Fujita, M. Insights into citric acid-induced cadmium tolerance and phytoremediation in Brassica juncea L.: Coordinated functions of metal chelation, antioxidant defense and glyoxalase systems. Ecotoxicol. Environ. Saf. 147, 990–1001 (2018).
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The Chinese Ministry of Agriculture Project.
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L.Z.: Data curation, Analyzation and Writing; D.Z.: Conceptualization and Methodology; L.L.: Supervision, Resources and Project administration; Z.X.: Supervision, Writing—review and editing; N.Z.: Resources, Investigation.
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Zhang, L., Zou, D., Zeng, N. et al. Slaked lime improves growth, antioxidant capacity and reduces Cd accumulation of peanut (Arachis hypogaea L.) under Cd stress. Sci Rep 12, 4388 (2022). https://doi.org/10.1038/s41598-022-08339-1
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DOI: https://doi.org/10.1038/s41598-022-08339-1
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