Effect of biochar on yield and quality of tomato grown on a metal-contaminated soil

Effect of biochar on yield and quality of tomato grown on a metal-contaminated soil

Scientia Horticulturae 265 (2020) 109210 Contents lists available at ScienceDirect Scientia Horticulturae journal homepage: www.elsevier.com/locate/...

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Scientia Horticulturae 265 (2020) 109210

Contents lists available at ScienceDirect

Scientia Horticulturae journal homepage: www.elsevier.com/locate/scihorti

Effect of biochar on yield and quality of tomato grown on a metalcontaminated soil

T

Yaser A. Almaroaia,b, Mamdouh A. Eissac,* a

Department of Biology, Faculty of Applied Science, Umm Al-Qura University, Makkah, Saudi Arabia Research Laboratories Centre, Faculty of Applied Science, Umm Al-Qura University, Makkah, Saudi Arabia c Departments of Soils and Water, Faculty of Agriculture, Assiut University, Assiut 71526, Egypt b

A R T I C LE I N FO

A B S T R A C T

Keywords: Toxic metals Wastewater Metal uptake Translocation

Metal contamination of soils is a main source of hazard materials in food chain. Biochar is a promising agriculture tool to improve plant yield and enhance quality of vegetable crops. Three rates of biochar (C = 0, BC1 = 5 and BC2 = 10 ton ha−1) were added to a metal-polluted soil before the cultivation of tomato (Solanum lycopersicum cv Super). The non-edible part of tomato accumulated 80 and 84 % of Cu and Zn, while 20 and 16 % was transferred to the fruit. Whereas the non-edible part of tomato kept 99.9 and 99.8 % of Pb and Cd, less than 0.1 and 0.2 % were moved to tomato fruit. Metal concentrations in tomato tissues as affected by biochar application found to decrease in the order: C > BC1 > BC2. BC1 and BC2 significantly increased the tomato fruit yield by 20 and 30 %, respectively, above C treatment. BC2 increased the total acidity, TSS, vitamin C and lycopene in the juice of tomato by 33, 29, 39 and 24 % compared to the control. Biochar increased essential nutrient availability and uptake and minimized those of the toxic element. For improve tomato quality and productivity, it is recommended to apply biochar to metal-contaminated soils.

1. Introduction Sewage wastewater is a main source of soil contamination with toxic metals (Eissa, 2016a). The diluted raw sewage wastewaters may be used in agriculture in many developing countries, although it is considered unlawful (Huibers et al., 2004). Sewage water includes extraordinary concentrations of toxic metals and it will certainly increase their accumulation in soils, plants and groundwater (Kanwar and Sandha, 2000; Ghosh et al., 2012). These metals are non-essential for nutrition of animal or green plants (Kanwar and Sandha, 2000; Ghosh et al., 2012).The increase of metal concentrations in soil will transfer these metals to food crops producing hazardous effects on organisms and environmental ecosystems (Ghosh et al., 2012; Eissa, 2016a). The plants grown on soil contaminated with toxic elements contained higher concentrations of these elements than those grown on clean soil (Ghosh et al., 2012; Eissa, 2016b). Pb and Cd are very toxic to organism and they negatively affect plant, animal and human even at low concentrations (Wolnik et al., 1983; Watanabe, 1997). Zn and Cu are trace elements and essential for plant nutrition; but when they are existing in higher levels they may be toxic for organisms (Marschner, 1995). As a result of the accumulation of hazard materials such as toxic metals, the food quality will declined (Antisari et al., 2015; Eissa, 2016a).



Tomato (Solanum lycopersicum) is a plant from Solanaceae and its fruits contain high concentrations of minerals and vitamins (Sharma, 2010; Bjarnadottir, 2015). Food quality of the plant grown on metalcontaminated soil will affect human health (Antisari et al., 2015; Eissa, 2016a). The investigation of toxic metal uptake and translocation is useful in management of metal-contaminated soil (Eissa and Roshdy, 2018). Studying the movement of toxic metals and determining the final place where metal accumulated are very useful in determination of the safety degree of the edible plant parts (Antisari et al., 2015; Eissa, 2019). Controlling metal availability in soils is a vital action to minimize injurious properties of toxic elements in the environmental ecosystem (Eissa, 2016b; Youssef and Eissa, 2017). Several methods were used to reduce the bioavailability of toxic elements such as precipitation in soil solution and surface complexation with the organic and inorganic soil colloids (Bian et al., 2014). Biochar is one of promising tools and it enhances the soil physiochemical properties e.g., moisture retention and aggregation of soil particles (Curaqueo et al., 2014; Ippolito et al., 2016), besides, it raises the soil organic matter (Curaqueo et al., 2014). Thus, it raises the soil cation exchange capacity (Park et al., 2011). Numerous researchers showed that biochar amendment is able to reduce the bioavailability of toxic metal (Khan et al., 2017) due to high

Corresponding author. E-mail address: [email protected] (M.A. Eissa).

https://doi.org/10.1016/j.scienta.2020.109210 Received 20 August 2019; Received in revised form 9 January 2020; Accepted 17 January 2020 0304-4238/ © 2020 Elsevier B.V. All rights reserved.

Scientia Horticulturae 265 (2020) 109210

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Fernández et al., 2001). Finally; the samples were rinsed by distilled water, oven-dried at 70 °C for 48 h to obtain a stable weight and then ground and then were stored for chemical analysis.

pH and CEC and organic carbon (Park et al., 2011; Mohamed et al., 2016). Biochar is rich in organic carbon and has active functional groups and special structure which enhance its ability to react with toxic metals (Karami et al., 2011; Park et al., 2011; Mohamed et al., 2016). The encouraging results of biochar application to cultivated crops are well known but biochar effect depends on type of soil, crop, biochar raw material and other environmental conditions (Spokas et al., 2012; Eissa, 2019). The current research was undertaken to assess the role of biochar in improving quality and minimized the concentrations of toxic elements in the fruit of tomato grown on a soil contaminated with heavy metals.

2.2. Biochar preparation an analysis The maize stalks (30 cm length) were brought from the farm of Assiut University Experimental Station to prepare the biochar. Maize stalks were pyrolyzed in a muffle furnace, set at a heating rate of 15 °C min–1 for 2.5 h at a peak temperature of 450 °C. Biochar were digested in -H2SO4 and HClO4 (1:1 v/v), then were analyzed for the total N, P, K, Zn, Cu, Cd, Ni, and Pb content. Biochar pH was measured by a digital pH meter in a 1:10 suspension. The EC was estimated in 1:10 extract using the salt bridge method (Burt, 2004).

2. Materials and methods 2.1. Field experiments and sampling Two years of field trials were established to study the effect of biochar at three rates 0, 5, and 10 t ha–1 on the growth and quality of tomato grown on a metal-contaminated soil. The soils in this village have been irrigated with raw sewage water for more than 60 years. The current field trails were carried out at Arab Elmadabegh village, Assiut, Egypt located at 27° 12− 16.67= N latitude and 31° 09- 36.86= E longitude. The plot size of each experimental unit was 5 × 10 m2 and 2 m were used to separate distance between the experimental units. Table 1 shows some physiochemical properties of the studied soil. In the two studied seasons, biochar was added before cultivation and mixed manually with the surface soil (0−30 cm). The data in Table 2 show the chemical properties of the studied biochar. The seedlings of tomato (Solanum lycopersicum cv Super) were cultivated on the first week of April in 2017 and 2018 growing seasons. The tomato plants were cultivated on ridges at 50 × 100 cm with a density of about 20,000 plants ha–1. Tomato was fertilized with 400, 250 and 150 kg ha–1 of urea (46 %N), potassium sulfate (50 %K2O) and superphosphate (15 %P2O5). The rates of fertilization were based on the recommended dose of the Ministry of Agriculture and Land Reclamation (Egypt) recommendations. Tomato plants were irrigated by Nile River water (EC of 1.1 dS m–1). Composite plant samples, each consists of ten plants, were collected after 100 days of cultivation. Each plant sample was divided to roots, shoots and fruits. The plant samples were washed twice with tap water. Solution of HCl (0.1 %) was used to wash the plant samples to remove the surface inorganic wastes (Álvarez-

2.3. Soil and plant analysis A composite soil sample (0−30 cm) was collected before cultivation to evaluate some physio-chemical characteristics of soil. The physiochemical characteristics of the studied soil and plant samples were determined according to Burt (2004). Soil texture was determined by pipette method according to Burt (2004). Soil organic carbon was measured by dichromate oxidation method while the calcimeter method was used in the determination of soil calcium carbonate (Burt, 2004). Salt bridge method was used in measuring the soil salinity in soil paste by EC meter (LOvibond 200 con, Germany) while the soil pH was determined 1:2 soil suspension by pH meter (Hanna Instruments pH 211, Romania) (Burt, 2004). 25 mL of 2 M potassium chloride added to 5 g of dried soil sample then shaked for 1 h on to extract the available N (NH4+NO3) from soil. 25 L of the available N-extract were distilled by kjeldahl method to determine the available N in the soil sample (Gerhrdit s10Vabodest, Germany) (Burt, 2004). Sodium bicarbonate (0.5 M adjusted at pH 8.5) was used in the extraction of available P from soil samples while ammonium acetate (1 M adjusted at pH 7.0) was used in the case of K (Burt, 2004). Stannous chloride method was used in the measuring of P which was determined by spectrophotometer (Unico 2000UV, Germany) at 660 mm (Burt, 2004). Potassium was determined by flame photometer (Jenway 7PFP, England) according to Burt (2004). The availability of Zn, Cu, Pb, Cd and Ni was measured after the extraction of soil samples with a 0.005 M DTPA (diethylen triamine penta acetic acid) solution (pH 7.3) as recommended by Lindsay and Norvell (1969). The total metals were measured after the soil samples were digested according to the procedure given by the US EPA (1996). The metals in the digest extract of soil and plant were determined using the ICP-OES thermo iCAP 6000 series. A composite soil sample (0−30 cm) was collected from each experimental unit to study the effect of biochar on nutrients availability and physio-chemical characteristics of the studied soil. The ground plant samples were digested using concentrated acids of H2SO4 and HClO4. Then the digested extracts were analyzed for N, P, K, Zn, Cu, cD, Ni and Pb with same standard methods which used in soil analysis. The analysis of a reference material was performed during the soil and plant analysis for quality control and assurance. Recovery of Zn, Cu, Pb, Cd and Ni was 103, 102, 97, 98 and 105 %. The following equation was used to calculate the translocation factor (TF):

Table 1 Some physical and chemical characteristics of the soil in the studied site. Soil properties Clay (g⁄kg) Silt (g⁄kg) Sand (g⁄kg) Texture CaCO3 (g⁄kg) pH (1:2) CEC (cmol⁄kg) Total Organic-C (g⁄kg) EC (1:2) (dS⁄m) Available nitrogen (mg kg−1) Available Olsen P (mg kg−1) Available-K (mg kg−1)

−1

Zn (mg kg ) Cu (mg kg−1) Pb (mg kg−1) Cd (mg kg−1) Ni (mg kg−1)

100 200 700 Sandy loam 80 7.77 18 26.0 1.7 20 7.0 290

DTPA-Extractable

Total content

PL*

8.8 6.2 4.5 0.55 1.5

600 335 320 8.5 150

200-300 50-140 300 3 50

Translocation Factor=

Element concentrations in the shoot (mg / kg) Element concentrations in the root (mg / kg)

Chlorophyll (Ch-a and Ch-b) and carotenoid contents were measured based on the method of Lichtenthaler (1987). 200 mg of leaf were extracted with 10 mL ethyl alcohol (95 %). Carotenoid, Chl-a, and Chl-b concentrations were measured by spectrophotometer at 470, 663 and 644 nm, respectively (El-Mahdy et al., 2018).

The permissible limits based on the total concentrations. * Permissible limits according to European Union Standards (EU, 2002) and U.S. Environmental Protection Agency (USEPA, 1996). 2

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Table 2 Some chemical properties of the studied biochar. OC (g/ kg)

pH 1:10

EC (dS/m)

N (g/kg)

P (g/kg)

K (g/kg)

Zn (mg/kg)

Cu (mg/kg)

Cd (mg/kg)

Pb (mg/kg)

530

9.21

5.0

5.2

2.4

20

50

25

nd

nd

OC = organic carbon. nd = not detected.

20 and 30 %, respectively, above the non-amended soil (C). Amendment of the soil with biochar caused remarkable increases in the total acidity, TSS, vitamin C and lycopene. The maximum significant values of the total acidity, TSS, vitamin C and lycopene in the fruit of tomato the maximum significant value were obtained from BC2 while the minimum ones were obtained from C treatment. The moisture content in tomato fruit of the non-treated soil (C) was higher by 20 % compared to that amended with BC2. The highest rate of biochar (10 ton ha−1) significantly increased the total acidity, TSS, vitamin C and lycopene by 33, 29, 39 % and 24 % compared to the control.

2.4. Determination of quality of tomato fruit Ten tomato fruits from each experimental unit were selected randomly, to determine the fruit quality. Samples of tomato fruit were washed with tap water, then by distilled water and then were converted to a juice by a blender. The pH of the tomato juice was measured by a pH meter and the total soluble solid (TSS) values were measured with a digital refractometer according to AOAC (2000). The total acidity (TA) of tomato was measured by 0.01 N NaOH and the obtained result were shown in g citric acid / 100 g of fresh weight of tomato fruit (AOAC, 2000). Lycopene was extracted with hexane and determined using spectrophotometer at at a wavelength of A503 nm (Ravelo-Pérez et al., 2008). Vitamin C in tomato juice was measured by titration method using 2,6-dichlorophenolindophenol solution and ascorbic acid (Patanè et al., 2011).

3.2. Metal concentration in tomato root and shoot as affected by biochar Zinc, copper, lead, cadmium and nickel in tomato plant tissues were measured and Table 4 shows these results. The application of biochar affected significantly (P < 0.05) in Zn, Cu and Pb in the roots and shoots of tomato. Tomato roots stored 33–47, 30–48 and 76–91 % of the total Zn, Cu and Pb absorbed by tomato, while the shoots stored 39–50, 37–51 and 9–18 % (Fig. 1). Zn, Cu and Pb concentration in the root was higher than that stored in the shoot of tomato plants. Biochar application significantly decreased Zn, Cu and Pb in tomato root and shoot. Zn, Cu and Pb concentrations tomato root and shoot as affected by the biochar rates were found to decrease in the order: C > BC1 > BC2. The roots of tomato plants grown on C treatment contained Zn, Pb and Cu concentrations higher by 14, 4 and 11 % compared to BC2. The shoots of tomato plants grown on C treatment contained Zn, Pb and Cu concentrations higher by 17, 25 and 15 % compared to BC2. The roots of the tomato plants grown on the control soil stored 33, 30 and 76 % of the total Zn, Cu and Pb absorbed by the whole plant, while that grown on the soil amended with BC2 stored 47, 48 and 91 %. Concentrations of Cd and Ni in the shoots of tomato were not affected by the biochar application rates. Concentrations of Cd in tomato roots were affected significantly by the application of BC1 or BC2. Tomato roots grown on C treatment contained Cd and Ni concentrations higher by 18 and 26 % compared to that grown on the soil amended with BC2. Tomato root contained higher concentrations of Cd and Ni than shoot. Tomato roots stored about 62–81 and 64–88 % of the total Cd and Ni taken up by tomato plant, but tomato shoot accumulated about 18–24 and 10–13 %. Overall, tomato root contained higher concentrations of lead, cadmium and nickel than the aboveground parts of the studied plant. Metal concentrations in tomato root were found to increase in the order: Ni > Cd > Cu > Zn > Pb but these orders in tomato shoot were increase in the order Ni > Cd > Pb > Cu > Zn. Biochar raised the amount of Zn, Cu, Pb Cd and Ni accumulated in tomato root.

2.5. Statistical analysis The obtained results were statistically analysed by One-way ANOVA and Duncan test (at 0.05 % probability) which were run by SPSS 15.0 package (SPSS, Chicago, IL, USA). 3. Results 3.1. Biochar effects on photosynthetic pigments, yield and quality of tomato Fig. 1 shows the effect of biochar rates on chlorophyll and carotenoids in the leaves of tomato. Biochar application caused significance increases in the concentrations of photosynthetic pigments. Amendment of soil with BC2 (10 ton ha−1) increased the amount of chlorophyll a, b and carotenoids by 51, 9 and 35 % above the control soil. Table 3 shows the effect of biochar on tomato yield and some quality parameters of fruit. Amendment of soil with BC1 (5 ton ha−1) or BC2 (10 ton ha−1) caused significance increases on the yield and quality of tomato. The yield of tomato ranged between 10−13 ton ha−1 and the highest significant value was obtained from the soil amended with BC2 while the lowest one was obtained from the control soil (C). The application of BC1 and BC2 significantly increased the tomato yield by

3.3. Effect of biochar on metal concentrations in tomato fruit Metal concentrations in the edible portion of tomato were measured and the obtained results are shown in Table 4. BC2 decreased Zn, Pb, Cd and Ni in tomato fruit by 10, 44, 50 and 20 % in comparison with C. The fruit of tomato stored 14–16, 14–16, 0.06–0.15, 0.14–0.37 and 1.47–2.37 % of the total Zn, Cu, Pb, Cd and Ni absorbed by the whole plants (Fig. 2). Metal concentrations in tomato fruit were found to increase in the following order: Cd > Ni > Pb > Cu > Zn and these obtained trends were correct for the tested treatments. The non-edible

Fig. 1. Photosynthesis pigments in the leaves of tomato as affected by biochar. Means denoted by the same letter indicate no significant difference according to Duncan’s test at P < 0.05. C, BC1 and BC2= control, biochar at a rate of 5 and 10 ton ha−1. 3

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Table 3 Fruit yield and quality of tomato as affected by biochar.

C BC1 BC2

Fruit yield (ton ha−1)

VC (mg 100 g−1)

Fruit diameter (cm)

Fruit moisture (%)

Total acidity (%)

TSS (°Brix)

Lycopene (mg g−1 FW)

10 ± 1 c 12 ± 1 b 13 ± 1 a

3.5 ± 0.1 a 4.5 ± 0.2 a 4.8 ± 0.1 a

5.0 ± 0.2 a 4.9 ± 0.3 a 5.1 ± 0.2 a

72 ± 4 a 67 ± 3 b 60 ± 3 c

0.30 ± 0.0 c 0.36 ± 0.0 b 0.40 ± 0.0 a

3.5 ± 0.1 c 3.9 ± 0.2 b 4.5 ± 0.2 a

13.3 ± 0.7 c 15.6 ± 0.8 b 16.5 ± 0.8 a

Means denoted by the same letter indicate no significant difference according to Duncan’s test at P < 0.05. C, BC1 and BC2= control, biochar at a rate of 5 and 10 ton ha−1. VC = vitamin C. Table 4 Metal concentrations (mg kg−1) in the roots, shoots and fruits of tomato as affected by biochar. Zn

Cu

Pb

Cd

Ni

100 ± 5 a 90 ± 6 b 88 ± 4 b

70 ± 3 a 65 ± 3 b 63 ± 5 b

120 ± 6 a 120 ± 7 a 115 ± 8 a

17.1 ± 1.0 a 15.1 ± 1.2 b 14.5 ± 1.4 b

15.1 ± 1.1 a 12.2 ± 1.3 b 12.0 ± 1.2 b

Shoots C 90 ± 5 a BC1 80 ± 4 b BC2 77 ± 3 b

60 ± 3 a 50 ± 3 b 52 ± 4 b

15.2 ± 1.3 a 12.2 ± 1.4 b 12.0 ± 1.01 b

3.2 ± 0.4 a 3.5 ± 0.3 a 3.5 ± 0.2 a

1.2 ± 0.0 a 1.5 ± 0.0 a 1.5 ± 0.0 a

Fruits C BC1 BC2

35 ± 2 b 38 ± 2 a 38 ± 2 a

0.27 ± 0.0 a 0.24 ± 0.0 a 0.15 ± 0.0 b

0.10 ± 0.0 a 0.07 ± 0.0 b 0.05 ± 0.0 b

0.50 ± 0.0 a 0.35 ± 0.0 b 0.40 ± 0.0 b

Roots C BC1 BC2

60 ± 3 a 55 ± 3 b 54 ± 2 b

Means denoted by the same letter indicate no significant difference according to Duncan’s test at P < 0.05. C, BC1 and BC2= control, biochar at a rate of 5 and 10 ton ha−1.

part of tomato accumulated 84 and 80 % of Zn and Cu, 16 and 20 % was moved to the fruit. The edible part of tomato stored 0.1 and 0.2 % of Pb and Cd absorbed by the whole plant and 99.9 and 99.8 % of Pb and Cd were accumulated in the non-edible part. Fig. 4 shows the translocation factor (TF) of the studied metals as affected by biochar application. Data of the present research showed that TF of the studied metals ranged from 0.08 to 0.90. Values of TF of the studied metals were found to increase in the following order: Pb = Ni > Cd > Cu > Zn. Maximum TF was obtained in Zn and Cu, but the minimum value was obtained from Ni, Cd and Pb. Biochar significantly minimized TF of Zn, Cu and Pb. BC2 minimized the TF values of Zn, Cu and Pb by 2.5, 3.5 and 2.3 % in comparison with C. Fig. 2. Distribution of metals in the different tissues of tomato. Metal uptake by a plant part = metal concentration (mg g−1) × dry weight (g). % Metal uptake by a plant part = (metal uptake by a plant part / total metal uptake by the whole plant) x 100. C, BC1 and BC2= control, biochar at a rate of 5 and 10 ton ha−1.

3.4. Biochar effects on some chemical properties of the investigated soil and the availability of nutrients and metals Table 5 shows biochar effects on some essential nutrients availability and uptake. The highest rate of biochar significantly increased the availability and uptake of N and K. Amendment of the soil with BC2 (10 ton ha−1) increased the availability of N, P and K 67, 54 and 43 % above the control soil. Amendment of the soil with BC2 increased the uptake of N and K by 67 and 56 % above the control soil. The availability of P in soil was affected significantly by the higher rate of biochar while the P uptake was not affected by any treatment. Fig. 3 shows the availability of metals in the investigated soil. Biochar application has significance effects (P < 0.05) in bioavailability of the investigated elements. The highest significant values of the available Zn, Cu, Pb Cd and Ni were obtained from C while the lowest ones were obtained from BC2. The available Zn, Pb, Cu, Cd and Ni in C treatment were higher by 33, 33, 50, 25 and 20 % compared to that amended with BC2. The application of biochar has significance effects and minimized element bioavailability compared to the control. The data illustrated in Fig. 5 show the soil pH, OC and CEC of the

investigated soil as affected by biochar rates. BC1 and BC2 caused significant (P < 0.05) effects on the studied soil chemical properties. The pH of the studied soil ranged between 7.80–8.40 and the maximum significant value was obtained from BC2 while the lowest one was obtained from C. BC1 and BC2 significantly increased the soil pH by 2.5 and 7.7 % above the control. The soil organic carbon (OC) ranged between 27−33 g kg−1 and the highest significant value was recoded from the soil amended with BC2 while the minimum value was recorded from C. BC1 and BC2 significantly increased the OC by 11 and 22 % above the control. The cation exchange capacity of the studied soil (CEC) ranged between 18–21 cmol kg −1 and the maximum significant value was obtained from BC2 while the lowest one was obtained from C. Biochar significantly improved soil CEC by 11 and 17 % above the control in the case of BC1 and BC2.

4

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Table 5 Availability and uptake of nutrients as affected by biochar application. Available soil nutrients (mg/kg)

C BC1 BC2

Nutrients in plant (g / plant)

NH4+NO3

P

K

N

P

K

15 ± 2b 12 ± 2 b 25 ± 3 a

6.5 ± 0.7 b 7.1 ± 0.9 b 10.0 ± 1.2 a

280 ± 12 c 320 ± 8 b 400 ± 10 a

0.42 ± 0.0 c 0.50 ± 0.0 b 0.70 ± 0.0 a

0.08 ± 0.0 a 0.07 ± 0.0 a 0.08 ± 0.0 a

0.2 ± 0.05 c 0.27 ± 0.0 b 0.39 ± 0.0 a

Fig. 3. Root-shoot translocation factor (TF) of metal as affected by biochar. Means denoted by the same letter indicate no significant difference according to Duncan’s test at P < 0.05. C, BC1 and BC2= control, biochar at a rate of 5 and 10 ton ha−1.

Fig. 5. Some chemical properties of the studied soil as affected by biochar. Means denoted by the same letter indicate no significant difference according to Duncan’s test at P < 0.05. C, BC1 and BC2= control, biochar at a rate of 5 and 10 ton ha−1.

a rate of 10 ton ha−1 raised the titretable acidity, TSS, vitamin C and lycopene by 33, 29, 39 % and 24 % in comparison with the control. The high biochar rate (50 ton ha−1) in the study of Agbna et al. (2017) is too high compared to 10 ton ha−1 used in the current study. But the high rate of Agbna et al. (2017) study may be due to the low soil organic content (1.3 g kg−1) while the current studied soil contained 26 g kg−1. Akhtar et al. (2014) studied the effect of biochar rate (0 and 5 % of the soil weight) in tomato plants grown on a greenhouse and they found that the high rate of biochar increased the TSS, vitamin C and titrateable acidity of tomato juice by 10, 13 and 20 % while that application rate increased the total yield by 23 % over the control. Biochar may increase the fruit yield and tomato quality by increasing leaf photosynthetic and nutrients uptake (Kammann et al., 2011; Wang et al., 2014). Abid et al. (2017) reported that biochar increased the photosynthetic pigments in tomato (Solanum lycopersicum L.) and reduced the Cd and Zn in tomato tissues. The obtained results of the present field trials illustrated that amendment of the soil with 10 ton ha−1 of biochar increased chlorophyll and carotenoids in tomato leaves by 51 and 35 % above the control soil, besides, this rate of biochar significantly enhanced the uptake of N and K by 67 and 56 % over the control. Increasing the organic matter in soil improved the nutrient availability and enhanced physiochemical properties of the soil (Bauer and Black, 1994; Abiven et al., 2009). In the current study as shown in Fig. 5, amendment of the soil with BC1 and BC2 increased the soil organic carbon by 11 and 22 % above the control. The investigation of metal uptake and translocation and exploring the tissues which accumulated high levels of metals helps greatly in the studying of food safety in metal-contaminated soil (Eissa, 2014; Eissa, 2016a). Data obtained from the present field trials clearly showed that tomato shoot and root accumulated 80 and 84 % of Cu and Zn, but 20 and 16 % was moved to the edible portions. While in case of Cd and Pb, tomato shoots and roots accumulated 99.9 and 99.8 %, respectively, and only 0.1 and 0.2 % of the total metal uptake was transported to the edible portions of the root-shoot transfer of Pb and Cd is low and thus they accumulated in high concentrations in the plant root (Wozny,

Fig. 4. Availability of metals in the studied soil as affected by biochar. Means denoted by the same letter indicate no significant difference according to Duncan’s test at P < 0.05. C, BC1 and BC2= control, biochar at a rate of 5 and 10 ton ha−1.

4. Discussion Biochar may improve soil physicochemical properties, consequently increasing the root growth, caused increases in essential nutrients uptake (Hameeda et al., 2019). Biochar application improved soil moisture and increased barley growth (Bruun et al. (2014). In the current field study, the application of 5 and 10 ton ha−1 caused 20 and 30 % increases in the yield of tomato; moreover, the application of biochar enhanced the quality of tomato fruit in comparison with the control. Agbna et al. (2017) studied the response of tomato plants to three rates of biochar (0, 25 and 50 ton ha−1) and he reported that the higher rates of biochar improved tomato growth and fruit quality in comparison with the non-amended soil. These results are in agreement with those obtained by Hameeda et al. (2019) and Akhtar et al. (2014). The application of 50 ton ha−1 of biochar increased the TSS, vitamin C and titrateable acidity of tomato juice by 7, 29 and 23 % while that application rate increased the total yield by 25 % over the control (Agbna et al., 2017). The current study clearly depicted that biochar at 5

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1995; Kadukova et al., 2004; Eissa, 2019; Nzediegwu et al., 2019). Biochar application at higher rate reduced Zn, Pb, Cd and Ni levels in tomato fruit by 10, 44, 50 and 20 % as compared to the control; moreover the application of biochar reduced the bioavailability of Zn, Cu, Pb, Cd and Ni in the studied contaminated soil. Data of the present investigation revealed that biochar is an active method in decreasing the bioavailability of heavy metals. Cd and Pb levels were decreased by 16 and 29 % in wheat grain as a result of the application of 20 ton biochar/ha (Sui et al., 2018). The ability of biochar in reducing metal availability and uptake is well known and this may be by controlling soil pH and metal adsorption (Zhu et al., 2018; Eissa, 2019). Amendment of the soil with biochar (8 ton ha−1) decreased the availability of Cd, Zn, Pb, Cu and Ni by 14, 13, 9, 8, and 3.6 %, in comparison with non-treated soil (Eissa, 2019). Eissa (2019) confirmed that cow manure biochar applied to contaminated soil minimized the root-shoot translocation of Zn, Cu, Pb and Cd by 5, 8, 23 and 6 % in zucchini plants. Eissa (2014) and Li et al. (2016) suggested that the precipitation of metals in plant root zone may reduce the metals root-shoot transfer. Biochar application to soil may increase the soil pH and CEC, so, the metals binding with soil particles will become stronger (Tang et al., 2013). In the current study, the available Zn, Cu, Pb Cd and Ni in the non-amended soil were higher by 33, 50, 33, 25 and 20 % compared to that amended with 10 ton ha−1. Biochar application at a rate of 10 ton ha−1 significantly increased soil pH, soil organic matter and cation exchange capacity by 7.7, 22 and 17 % above the control. Raising the SOM and CEC may reduce the metal bioavailability especially under the high pH conditions (Eissa, 2016a). Biochar has a high ability in reducing the metal bioavailability through increasing the soil pH (Tang et al., 2013). Data of the present study confirmed that pH of the soil amended with the 10 ton ha−1 of biochar was 8.40 while in the case of control it was 7.80. The obtained results in the current study are in agreement with previous studies (Zhu et al., 2018; Eissa, 2019).

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5. Conclusion Guidelines used for metal-contaminated soils must be based on actual field trials to ensure safe food is produced. Two-years field study was conducted to evaluate the quality and safety of tomato grown on a metal-contaminated soil as affected by biochar application. Biochar effect on metal uptake by tomato plant was investigated based on twoyear field trials. Biochar application caused increases in the accumulation of elements in tomato root and shoots and conveyed negligible concentrations to tomato fruit. Biochar enhanced tomato growth and increased the plant productivity; moreover, it reduced the metal concentrations in tomato fruit. Authors' contributions" section Eissa and Almaroi made the field trials design. Eissa wrote the first draft of the manuscript and provided all the data, Almaroi conducted all statistical analyses. All authors reviewed 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. References A. O. A. C, 2000. Association of Official Analytical Chemists: Official Methods of Analysis. Washington, DC, USA. . Abid, M., Danish, S., Zafar-Ul-Hye, M., Shaaban, M., Iqbal, M.M., Rehim, A., Qayyum, M.F., Naqqash, M.N., 2017. Biochar increased photosynthetic and accessory pigmentsin tomato (Solanum lycopersicumL.) plants by reducing cadmium concentration undervarious irrigation waters. Environ. Sci. Pollut. Res. 24, 22111–22118. Abiven, S., Menassero, S., Chenu, S., 2009. The effect of organic inputs over time on soil

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