Differential growth and metal accumulation response of castor bean genotypes on a lead contaminated soil

doi:10.21203/rs.3.rs-3344644/v1

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Differential growth and metal accumulation response of castor bean genotypes on a lead contaminated soil

https://doi.org/10.21203/rs.3.rs-3344644/v1

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In Pakistan, probably thousands of hectares are contaminated with heavy metals. As castor plant is hyper-accumulator of heavy metals, its cultivation in the area of lead (Pb) contamination can show great potential in terms of remediation of soils. Present study aimed to evaluate the phytoremediation potential of different castor genotypes, NIAB Gold, NIAB Spineless, NIAB-2020, DS-30 and C-3 grown in pots filled with 5 kg soil, spiked with various concentrations of Pb (0, 100, 200, 400, and 800 mg kg^− 1). Results showed that plant biomass and photosynthetic pigments reduced significantly with increasing Pb concentrations. Activities of superoxide dismutase and peroxidase were decreased significantly whereas catalase and ascorbate peroxidase were increased with increasing Pb levels in all genotypes. At 800 mg Pb kg^− 1 soil, the highest catalase and ascorbate peroxidase activities of 12.23 and 64.43 mM/g FW, respectively, were recorded in DS-30 followed by NIAB-2020. The highest total soluble proteins (8.44 mg g^− 1) were recorded in DS-30 followed by NIAB-2020 under Pb contamination at 800 mg kg^− 1 soil. Lead uptake increased significantly with increasing levels of Pb and highest uptake in roots were recorded in NIAB-2020 (302 mg kg^− 1) followed by DS-30 (299 mg kg^− 1) under Pb contamination at 800 mg kg^− 1. All genotypes showed metal translocation factor less than 1 under all Pb levels. In conclusion, NIAB-2020 and DS-30 possessed good potential with better Pb accumulation, osmolytes production and antioxidant activities compared to other castor bean genotypes.

Castor bean

phytoremediation

lead uptake

antioxidants

water relation

In the 21st century, pollution control is a major challenge due to the massive increase in pollutants produced by human activities. Among all, heavy metals and organic pollutants are known as two major factors behind soil pollution (LlnDh and LeMenkOVA, 2022). Lead is widely utilized for the manufacture of storage batteries, paints, alloy formation and casting etc (Khan et al., 2018). The presence of Pb in the soil is hazardous to human health due to its long-lasting residual and chance of entry in the food chain (Mühlbachová, 2011).

Different strategies are proposed for the remediation of heavy metal contaminated soils however, phytoremediation is considered cost-effective, environmental friendly, and easy to adopt technology with good public perception (Priya et al., 2023). Phytoremediation, use of plants for environmental cleanup, is a promising remediation strategy. This technique is a safe and effective way to remove a variety of contaminants, with fewer negative side effects than traditional remediation strategies (Zulkernain et al., 2023).

Castor bean, Ricinus communis L., has good potential to grow well on heavy metal contaminated soils and accumulate these metals including Pb in aerial parts. Additionally, castor possesses enormous adaptive potential in diverse habitats including resistance against drought, salinity, and climate warming, hence, suitable for marginal lands. Moreover, castor is an important non-edible industrial oil crop with various non-food and industrial applications as being used in soap, cosmetics, pharmaceutical, paints and lubricants. Therefore, phytoremediation of Pb contaminated soils using castor crop may be an environmental friendly and safe option that could give economic benefits from contaminated soils as well (Song et al., 2021).

Various studies have reported the potential of castor bean for the phytoremediation of heavy metal contaminated soils in Brazil (Andreazza et al., 2013), China (Yang et al., 2017) and India (Boda et al., 2017). Heavy metal pollution is becoming an adverse problem in many cities of Pakistan including Karachi (Karim et al., 2015), Faisalabad (Farid et al., 2015), Lahore (Khan et al., 2013), Kasur (Afzal et al., 2014), Sialkot (Malik et al., 2010), and Peshawar (Jan et al., 2010). In a survey study, Afzal and coworkers (2014) determined the level of heavy metal contamination in groundwater and soil near the industrial area of Kasur. The survey results revealed that soil and groundwater in the study area are highly contaminated with all tested heavy metals specially chromium. Similarly, in case of soil, highest Pb concentration (1753 mg kg^− 1) was detected under mining activities from Kohistan region, Gilgit Baltistan province (Muhammad et al., 2011).

These findings indicate an alarming situation of heavy metals contamination of agricultural soils in the vicinities of industrial cities of Pakistan and demands urgent remedy for the removal of heavy metals from soils. Various lab and greenhouse studies reported the potential of different grasses (Ullah et al., 2019), vegetables (Akhtar et al., 2018) and oilseed crops (Qureshi et al., 2020) for the phytoremediation of heavy metal contaminated soil. However, no mechanism based study is available regarding phytoremediation of Pb-contaminated soils using castor bean. Therefore, present study was designed to evaluate the growth, physiology and Pb uptake efficacy of castor genotypes for phytoremediation of Pb contaminated soils.

Experimental structure and treatment plan

A pot experiment was conducted to evaluate the growth, physiological and phytoremediation response of different castor genotypes on Pb contaminated soil under wire house conditions at the Nuclear Institute for Agriculture and Biology (NIAB) Faisalabad, Pakistan with coordinates 31.4504 N and 73.1350 E. Seeds of five castor genotypes (NIAB Gold, NIAB Spineless, NIAB-2020, DS-30 and C-3) were collected from Plant Breeding and Genetics Division (PBGD), NIAB. Plastic pots (20 × 22.5 cm) were filled with thoroughly mixed, air-dried and precisely sieved soil (5 kg) using 2 mm mesh. The well prepared soil was spiked with different concentrations of Pb (0, 100, 200, 400, and 800 mg kg^− 1 soil) prior to 3 months of sowing to equilibrate the metal in the soil. For this, above stated Pb concentrations were firstly calculated and then applied in solution form using lead nitrate of Sigma Aldrich (purity ≥ 99.0%). Soil without any treatment of Pb was considered as control. After the accomplishment of the required time period, pre-soaked seeds were sown in each pot with three replications following completely randomized design (CRD) with factorial settings. Plants were grown under natural environment with average temperatures of 30–35°C (night-day). The basal dose of fertilizer (NPK) was calculated and applied to each pot. Addition of nitrogen in soil through lead nitrate was adjusted while calculating the fertilizer dose (Ahmad, 2010).

Physicochemical analysis of the experimental soil

Soil was collected in bulk from the experimental site of NIAB and categorized for different physicochemical analysis (Table 1). Bouyoucos hydrometer protocol was followed for the determination of soil texture (Lotfy and Mostafa, 2014). Saturated paste was prepared to determine the pH of the soil using pH meter (ST-5000-OHAUS-USA) whereas soil extract was used to determine EC using EC meter (a-AB33EC, OHAUS, USA). Total nitrogen and available phosphorous were analyzed following Kjeldahl (Bremner, 1960) and Olsen (1954) method, respectively. Organic matter was determined as described by Walkley and Black (1934). Total Pb in soil was determined by the method as described by Ullah et al. (2020).

Table 1

Physiochemical analysis of the experimental soil
Sand (%)	Silt (%)	Clay (%)	Texture	pH	EC (dS m^− 1)	Total N (%)	Available P (mg kg^− 1)	O.M (%)	Total Pb (mg kg^− 1)
58	34.7	4.5	Sandy loam	7.65	2.05	0.081	5.9	0.99	N.D
O.M = Organic matter, N.D = Not detected

Gas exchange parameters

Stomatal conductance, transpiration and photosynthetic rate of the plants were measured through Decagon (2011) method in the morning hours using a porometer (Lincor.Inc steady state porometer).

Estimation of relative water content and electrolyte leakage

Relative water content (RWC) of the castor bean genotypes were determined using the method as described by Teulat et al. (2003) whereas electrolyte leakage of castor genotypes were determined by the method as described by Yang et al. (1996).

Plant growth parameters

Plants were harvested after 2 months and data regarding plant height and shoot fresh weight were recorded. Roots were washed thoroughly with tap water using plastic mesh to remove the soil particles and then with deionized water to determine root fresh weight. Shoot and root samples were oven dried at 70^°C for 72 hours to record dry weight.

Determination of photosynthetic activity

Arnon (1949) protocol was opted to determine photosynthetic pigments in fresh leaves of castor genotypes.

Determination of antioxidants enzymes

After five weeks of germination, fresh samples (0.2 g) of castor leaves were ground and homogenized in 0.05 M phosphate buffer solution (pH 7.8). The homogenized mixture was filtered and centrifuged at 12,000 rpm for 10 minutes at 4^°C.

Superoxide dismutase activity was measured by following Giannopolitis and Ries (1977) protocol at 560 nm. Pütter (1974) procedure was opted to determine peroxidase activity. The increase in absorbance due to the oxidation of guaiacol was measured spectrophotometrically at 470 nm. Catalase activity was determined by monitoring the reduction in the absorbance at 240 nm using the procedure as described by Aebi (1984). Ascorbate peroxidase (APX) activity was determined by the method as described by Nakano and Asada (1981).

Determination of total soluble proteins, total soluble sugars and total phenolic contents

Total soluble protein (TSP) was determined as described by Bradford (1976). Total soluble sugars (TSS) were analyzed spectrophotometrically according to Riazi et al. (1985) procedure. Micro-colorimetric method was followed for the determination of total phenolic contents (TPC) (Ainsworth and Gillespie, 2007).

Lead concentration in shoot and root

The heavy metal analysis was performed following the protocol of Ullah et al. (2020) with some modifications. Ground and oven-dried shoot and root samples were digested with nitric acid and perchloric acid (8:2 v/v) on a hot plate until the sample become colorless. After cooling, the digested samples were diluted to 50 mL with distilled water and filtered through Whatman No. 42 filter paper. The metal analysis was carried out using atomic absorption spectroscopy (Analytikjena, contrAA 800D, Germany).

Statistical analysis

The data obtained were analyzed using two-way analysis of variance (ANOVA) (Steel et al., 1997) and the means were compared by applying the least significance difference test at p ≤ 0.05. Data represent the mean of three replicates. The statistical analysis was conducted using the statistical software Statistix 8.1. Mean data of all parameters in the study were subjected to perform Principal Component Analysis (PCA) using XL-STAT software version 2014.

Effect of Pb contamination on plant growth attributes

The analysis of variance showed a significant influence of Pb treatments on the growth attributes of different castor bean genotypes. Plant height was significantly decreased (p ≤ 0.05) with the increasing concentrations of Pb in the soil. At 800 mg Pb kg^− 1 soil, NIAB-2020 showed better performance against Pb with an average height of 29.3 cm followed by DS-30 (28.0 cm) as compared to other genotypes. Shoot fresh biomass, root dry weight and shoot dry biomass were decreased due the presence of Pb. At 800 mg Pb kg^− 1 soil, the highest shoot fresh biomass up to 9.23 g plant^− 1 was observed in DS-30 followed by NIAB-2020 and C-3 i.e. 8.15 and 7.39 g plant^− 1 whereas maximum shoot dry weight and root dry weight i.e. 1.31 and 0.26 g plant^− 1 were recorded in NIAB-2020, respectively followed by DS-30 (Table 2).

Table 2

Effect of different levels of lead contamination of soil on the agronomic parameters of different castor genotypes
Pb (mg kg^− 1) soil	Genotypes	HT (cm)	FBM (g plant^− 1)	DBM (g plant^− 1)	RDW (g plant^− 1)
0	NIAB-G	39.33 c	27.77 b	2.23 c	0.50 d
	NIAB-SPN	39.66 c	31.11 a	2.44 b	0.57 c
	NIAB- 2020	46.66 b	32.31 a	2.69 a	0.69 a
	DS-30	52.33 a	32.34 a	2.67 a	0.66 b
	C-3	45.66 b	27.93 b	2.47 b	0.57 c
100	NIAB-G	38.00 cde	24.92 cd	1.93 e	0.42 f
	NIAB-SPN	38.33 cd	24.95 cd	2.09 d	0.48 e
	NIAB- 2020	39.33 c	27.19 bc	2.21 cd	0.49 e
	DS-30	38.66 cd	26.92 bc	2.19 cd	0.49 e
	C-3	38.33 cd	26.06 bc	2.14 cd	0.43 f
200	NIAB-G	31.66 fg	21.20 ef	1.78 f	0.37 j
	NIAB-SPN	33.33 f	21.60 e	1.53 g	0.39 i
	NIAB- 2020	37.00 de	22.66 de	1.92 e	0.41 g
	DS-30	36.00 e	22.31 e	1.93 e	0.41 gh
	C-3	33.66 f	21.30 e	1.52 g	0.40 hi
400	NIAB-G	30.00 ghi	15.93 g	1.31 hij	0.30 m
	NIAB-SPN	31.00 gh	16.04 g	1.35 hi	0.32 l
	NIAB- 2020	31.00 gh	20.58 ef	1.50 g	0.33 l
	DS-30	31.00 gh	20.94 ef	1.51 g	0.35 k
	C-3	30.33 gh	18.37 f	1.43 gh	0.32 l
800	NIAB-G	23.66 k	6.31 i	1.09 k	0.13 p
	NIAB-SPN	22.00 k	6.52 i	1.19 jk	0.19 o
	NIAB- 2020	29.33 hi	8.15 hi	1.31 hij	0.26 n
	DS-30	28.00 ij	9.23 h	1.29 ij	0.20 o
	C-3	26.00 j	7.39 hi	1.25 ij	0.19 o
LSD		2.25	2.44	0.12	0.02
Data represent the mean of three replicates. Means within the same column having different letters are significantly different at p ≤ 0.05 according to LSD. (Pb = lead); (NIAB-G = NIAB GOLD, NIAB-SPN = NIAB SPINELESS) and (Ht = Plant Height, FBM = Shoot fresh Biomass, DBM = Dry Biomass, RDW = Root dry weight).

Effect of Pb contamination of soil on physiological parameters

Table 3 illustrates the effect of Pb on the physiological parameters of different castor genotypes. The RWC of all genotypes were slightly affected with the increasing concentrations of Pb (p ≤ 0.05). Comparing the varieties against each level of Pb, RWC showed a faint decreasing trend from 0 to 200 mg kg^− 1. At 800 mg Pb kg^− 1 soil, NIAB-2020 showed maximum retention of water in leaves (90%) followed by DS-30 (82%), NIAB Gold (80%), NIAB spineless (78%) and C-3 (70%) due to the production of osmolytes. Electrolyte leakage is the key response of plant against any abiotic stress. Electrolyte leakage was increased significantly with the increasing concentration of Pb in the soil (p ≤ 0.05). At 800 mg Pb kg^− 1 soil, maximum electrolyte leakage was observed in NIAB spineless and NIAB Gold as compared to other genotypes.

Table 3

Effect of different levels of lead contamination of soil on the physiological parameters of different castor genotypes
Pb (mg kg^− 1) soil	Genotypes	RWC (%)	EL (%)	SC (mmol m^− 2 s^− 1)	TR (mmol m^− 2 s^− 1)	PR (umol m^− 2 s^− 1)
0	NIAB-G	99.00 a-d	9.16 qr	11.36 c	2.55 ab	383.53 cd
	NIAB-SPN	99.40 abc	8.42 rs	12.40 b	2.52 abc	427.16 bc
	NIAB- 2020	100.00 a	6.67 s	12.87 b	2.63 a	454.50 ab
	DS-30	100.00 a	7.23 s	15.76 a	2.58 ab	485.89 a
	C-3	99.80 ab	10.81 pq	12.20 b	2.52 abc	346.52 de
100	NIAB-G	95.62 a-f	12.80 mno	10.64 cd	2.44 b-e	287.41 fgh
	NIAB-SPN	96.02 a-f	13.85 lmn	10.91 cd	2.45 b-e	304.20 efg
	NIAB- 2020	98.80 a-d	11.49 op	11.26 c	2.50 abc	332.52 e
	DS-30	97.93 a-e	12.47 nop	11.26 c	2.49 a-d	325.09 ef
	C-3	96.90 a-f	14.49 klm	10.99 cd	2.46 a-e	314.71 ef
200	NIAB-G	93.37 a-f	15.36 kl	9.38 fg	2.31 efg	242.76 hi
	NIAB-SPN	93.82 a-f	16.19 jk	9.39 fg	2.32 d-g	245.29 hi
	NIAB- 2020	94.25 a-f	14.75 kl	10.38 de	2.42 b-e	251.62 hi
	DS-30	95.01 a-f	14.49 klm	9.78 ef	2.42 b-e	268.39 ghi
	C-3	93.82 a-f	17.19 ij	9.62 efg	2.37 c-f	230.30 ij
400	NIAB-G	91.04 f	37.68 f	7.00 jk	2.06 hij	193.41 jkl
	NIAB-SPN	91.87 ef	24.54 g	7.68 ij	2.11 hi	183.64 klm
	NIAB- 2020	93.06 b-f	17.36 ij	8.85 gh	2.14 ghi	223.93 ijk
	DS-30	92.82 c-f	18.25 i	8.09 hi	2.20 fgh	194.73 jkl
	C-3	92.58 def	20.24 h	7.92 i	2.05 h-k	177.87 lm
800	NIAB-G	80.40 g	109.92 b	5.51 m	1.92 jkl	140.63 mn
	NIAB-SPN	78.69 g	223.59 a	6.09 lm	1.88 kl	157.45 lmn
	NIAB- 2020	90.79 f	81.85 e	6.65 kl	2.00 ijk	165.68 lm
	DS-30	82.26 g	102.36 d	6.80 kl	1.97 i-l	173.37 lm
	C-3	70.59 h	106.26 c	5.44 m	1.81 l	119.66 n
LSD		6.76	1.81	0.81	0.18	44.91
Data represent the mean of three replicates. Means within the same column having different letters are significantly different at p ≤ 0.05 according to LSD. (Pb = lead); (NIAB-G = NIAB GOLD, NIAB-SPN = NIAB SPINELESS) and (RWC = Relative Water content, EL = Electrolyte Leakage, SC = Stomatal Conductance, TR = Transpiration rate, PR = Photosynthesis rate).

Observing the gas exchange parameters, stomatal conductance, transpiration and photosynthetic rate were significantly reduced with the increasing concentrations of Pb (p ≤ 0.05). A gradual decrease in stomatal conductance due to 100 to 800 mg kg^− 1 Pb in soil disturbed the transpiration rate and photosynthesis in castor genotypes. At 800 mg kg^− 1, significant reduction in photosynthetic activity was observed in C-3 and NIAB Gold i.e. 119.6 and 140.63 mmol m^− 2 s^− 1 respectively, while highest photosynthetic activity was recorded in DS-30 and NIAB-2020.

Effects of Pb on leaf pigment contents

The effect of Pb on the pigment content of the castor genotypes resulted in significant decreasing trend (p ≤ 0.05) with increasing metal stress. Interestingly, NIAB-2020 exhibited highest total chlorophyll and carotenoid content up to 8.61 and 3.59 mg g^− 1 respectively, as compared to other genotypes at 800 mg kg^− 1 (Table 4).

Table 4

Effect of different levels of lead contamination of soil on the photosynthetic pigments of different castor genotypes
Pb (mg kg^− 1) soil	Genotypes	Chl a mg g^− 1	Chl b mg g^− 1	Total Chl mg g^− 1	Carotenoids mg g^− 1
0	NIAB-G	5.42 ab	4.65 ab	10.0 abc	4.15 b
	NIAB-SPN	5.40 ab	4.64 ab	10.0 abc	4.15 b
	NIAB- 2020	5.47 a	4.72 a	10.1 a	4.20 a
	DS-30	5.47 a	4.65 ab	10.1 ab	4.16 ab
	C-3	5.40 ab	4.63 ab	10.0 abc	4.14 b
100	NIAB-G	5.13 def	4.58 b	9.72 d	4.04 c
	NIAB-SPN	5.13 def	4.59 ab	9.71 d	4.04 c
	NIAB- 2020	5.23 bcd	4.62 ab	9.85 cd	4.05 c
	DS-30	5.35 abc	4.59 ab	9.94 bc	4.05 c
	C-3	5.19 cde	4.27 c	9.46 e	4.04 c
200	NIAB-G	4.98 f-j	4.24 c	9.23 fgh	4.01 c
	NIAB-SPN	5.02 e-i	4.23 c	9.24 fgh	4.02 c
	NIAB- 2020	5.11 d-g	4.26 c	9.37 ef	4.04 c
	DS-30	5.07 d-h	4.25 c	9.32 efg	4.03 c
	C-3	4.97 f-k	4.23 c	9.20 fgh	3.96 d
400	NIAB-G	4.89 h-l	4.16 c	9.05 h	3.71 f
	NIAB-SPN	4.86 i-l	3.88 d	8.74 i	3.90 e
	NIAB- 2020	4.92 g-k	4.19 c	9.11 gh	3.95 de
	DS-30	4.97 f-k	4.21 c	9.18 fgh	3.92 de
	C-3	4.87 i-l	3.82 de	8.69 ij	3.68 f
800	NIAB-G	4.66 m-p	3.76 def	8.42 klm	3.50 h
	NIAB-SPN	4.72 l-o	3.76 def	8.47 jkl	3.58 g
	NIAB- 2020	4.84 i-m	3.77 def	8.61 ijk	3.59 g
	DS-30	4.82 j-m	3.76 def	8.58 ijk	3.59 g
	C-3	4.78 k-n	3.75 def	8.54 i-l	3.58 g
LSD		0.19	0.13	0.21	0.05
Data represent the mean of three replicates. Means within the same column having different letters are significantly different at p ≤ 0.05 according to LSD. (Pb = lead); (NIAB-G = NIAB GOLD, NIAB-SPN = NIAB SPINELESS) and (Chl a = Chlorophyll a, Chl b = Chlorophyll b, Total Chl = Total Chlorophyll).

Effect of Pb on the biochemical profile of castor bean

Results revealed that in all genotypes, SOD and POD showed negative correlation whereas an increasing trend of CAT and APX were recorded with increasing concentrations of Pb (p ≤ 0.05) as shown in Table 5. Interestingly, at 800 mg kg^− 1, highest CAT and APX activities were recorded in DS-30 (12.23 and 64.43 mM/g FW) followed by NIAB-2020 (12.13 and 64.31 mM/g FW), respectively (Table 5).

Table 5

Effect of different levels of lead contamination of soil on the enzymatic antioxidants of different castor genotypes
Pb (mg kg^− 1) soil	Genotypes	SOD (U/g FW)	POD (mM/g FW)	CAT (mM/g FW)	APX (mM/g FW)
0	NIAB-G	2196.7 cde	8.19 bc	3.86 i	30.73
	NIAB-SPN	2300.7 c	8.29 bc	1.86 j	31.53 j
	NIAB- 2020	3284.0 a	12.07 a	4.63 hi	38.10 i
	DS-30	2979.5 b	11.75 a	4.70 hi	38.50 i
	C-3	2251.1 cd	8.39 b	4.20 i	29.29 k
100	NIAB-G	1993.3 ef	6.41 ef	5.10 ghi	40.77 h
	NIAB-SPN	2045.8 de	5.97 fg	5.60 gh	40.53 h
	NIAB- 2020	2142.2 cde	7.32 d	5.70 gh	53.37 f
	DS-30	2078.3 cde	7.46 cd	5.83 fgh	53.40 f
	C-3	2032.5 de	7.01 de	5.10 ghi	42.26 g
200	NIAB-G	1583.8 g-j	5.39 ghi	7.03 ef	57.24 e
	NIAB-SPN	1780.4 fgh	5.66 fgh	8.20 de	59.12 d
	NIAB- 2020	1801.4 fg	5.82 fg	8.40 d	59.38 cd
	DS-30	1794.7 fg	5.78 fg	8.30 de	59.13 cd
	C-3	1663.0 ghi	5.30 g-j	6.30 fg	53.58 f
400	NIAB-G	1454.9 i-l	4.51 jk	8.80 cd	59.75 bcd
	NIAB-SPN	1548.4 ijk	4.58 ijk	8.40 d	59.64 bcd
	NIAB- 2020	1568.5 h-k	5.27 g-j	9.20 bcd	60.73 b
	DS-30	1582.8 g-j	5.14 g-j	9.30 bcd	60.70 b
	C-3	1520.8 ijk	4.90 hij	9.13 bcd	60.26 bc
800	NIAB-G	1059.6 n	3.03 m	9.80 bc	63.45 a
	NIAB-SPN	1278.3 lmn	2.17 n	9.96 bc	64.02 a
	NIAB- 2020	1388.1 j-m	3.92 kl	12.13 a	64.31 a
	DS-30	1357.5 klm	3.56 lm	12.23 a	64.43 a
	C-3	1182.8 mn	3.24 lm	10.33 b	63.45 a
LSD		224.4	0.83	1.29	1.13
Data represent the mean of three replicates. Means within the same column having different letters are significantly different at p ≤ 0.05 according to LSD. (Pb = lead); (NIAB-G = NIAB GOLD, NIAB-SPN = NIAB SPINELESS) and (SOD = Superoxide dismutase, POD = Peroxidase, CAT = Catalase, APX = Ascorbate Peroxidase).

A vigorous increase in TSS and TPC from 200 to 800 mg kg^− 1 were observed in all castor genotypes. At 800 mg kg^− 1, NIAB-2020, DS-30 and NIAB Spineless showed an equal production of soluble sugars of 18.6 mg g^− 1. With reference to phenolic contents, NIAB-2020 produced two times more phenolic contents up to 0.49 mg g^− 1 as compared to other genotypes. Total soluble proteins showed negative relation to Pb concentrations. At 800 mg kg^− 1, DS-30 produced 8.44 mg g^− 1 total soluble proteins followed by NIAB-2020, NIAB spineless, NIAB Gold and C-3 (Table 6).

Table 6

Effect of different levels of lead contamination on the non-enzymatic antioxidants of different castor genotypes
Pb (mg kg^− 1)	Genotypes	TSP (mg/g)	TSS (mg/g)	TPC (mg/g)
0	NIAB-G	11.33 b	13.99 e	0.14 k
	NIAB-SPN	11.60 ab	13.99 e	0.14 k
	NIAB- 2020	11.90 ab	14.01 e	0.15 k
	DS-30	12.10 a	14.09 de	0.15 k
	C-3	11.60 ab	14.01 e	0.14 k
100	NIAB-G	10.00 c	14.09 de	0.15 k
	NIAB-SPN	10.03 c	14.12 de	0.19 j
	NIAB- 2020	11.23 b	14.20 d	0.21 hi
	DS-30	11.25 b	14.20 d	0.20 ij
	C-3	11.23 b	14.12 de	0.19 j
200	NIAB-G	9.02 efg	18.42 c	0.21 ghi
	NIAB-SPN	9.04 efg	18.42 c	0.22 gh
	NIAB- 2020	9.94 cd	18.44 bc	0.23 g
	DS-30	9.66 cde	18.44 bc	0.23 g
	C-3	9.26 def	18.42 c	0.21 ghi
400	NIAB-G	8.48 ghi	18.44 bc	0.28 f
	NIAB-SPN	8.71 fgh	18.54 abc	0.30 ef
	NIAB- 2020	8.90 fgh	18.54 abc	0.31 de
	DS-30	9.01 efg	18.59 ab	0.31 de
	C-3	8.90 fgh	18.54 abc	0.31 de
800	NIAB-G	7.59 j	18.59 ab	0.32 d
	NIAB-SPN	7.83 ij	18.69 a	0.34 c
	NIAB- 2020	8.21 hij	18.69 a	0.49 a
	DS-30	8.44 ghi	18.69 a	0.38 b
	C-3	6.77 k	18.59 ab	0.34 c
LSD		0.68	0.15	0.02
Data represent the mean of three replicates. Means within the same column having different letters are significantly different at p ≤ 0.05 according to LSD. (Pb = lead); (NIAB-G = NIAB GOLD, NIAB-SPN = NIAB SPINELESS) and (TSS = Total Soluble sugars, TSP = Total Soluble Proteins, TPC = Total Phenolic contents).

Lead uptake in castor genotypes

Results have shown a significant increase in the concentration of Pb in plant tissues of all castor genotypes (p ≤ 0.05). Elemental analysis have shown higher concentration of Pb in roots as compared to shoots. At 800 mg kg^− 1, highest concentration of Pb in the roots were recorded in NIAB-2020 (302.0 mg kg^− 1) followed by DS-30 (299.3 mg kg^− 1). The highest translocation factor of 0.99 was observed in NIAB-2020. The bioconcentration factor of roots (BCFroot) increased with the increasing concentration of Pb as compared to bioconcentration factor of shoots (BCFshoot). At 800 mg kg^− 1, NIAB-2020 showed the maximum value of 3.59 followed by DS-30 (3.29) (Table 7).

Table 7

Determination of different levels of lead in the shoot and root of different castor genotypes
Pb (mg kg^− 1)	Genotypes	Shoot (mg kg^− 1)	Root (mg kg^− 1)	TF	BCFshoots	BCFroots
0	NIAB-G	N/D	N/D	N/D	N/D	N/D
	NIAB-SPN	N/D	N/D	N/D	N/D	N/D
	NIAB- 2020	N/D	N/D	N/D	N/D	N/D
	DS-30	N/D	N/D	N/D	N/D	N/D
	C-3	N/D	N/D	N/D	N/D	N/D
100	NIAB-G	28.67 o	43.67 o	0.63 m	0.93 o	1.38 l
	NIAB-SPN	29.83 o	50.33 n	0.64 lm	0.94 o	1.71 k
	NIAB- 2020	33.67 n	51.50 n	0.65 klm	1.20 mn	1.81 k
	DS-30	37.00 m	50.50 n	0.66 kl	1.30 m	1.80 k
	C-3	32.00 n	43.67 o	0.64 klm	1.09 n	1.41 l
200	NIAB-G	81.00 j	90.33 m	0.68 i	1.86 k	2.45 j
	NIAB-SPN	78.33 k	99.67 kl	0.68 ij	1.75 kl	2.64 hi
	NIAB- 2020	83.67 i	103.00 j	0.71 gh	2.07 ij	2.70 gh
	DS-30	82.00 ij	100.67 k	0.69 hi	2.05 j	2.66 h
	C-3	71.00 l	98.00 l	0.66 jk	1.70 l	2.52 ij
400	NIAB-G	122.67 h	190.00 hi	0.72 g	2.12 ij	2.87 ef
	NIAB-SPN	123.00 h	189.00 i	0.78 f	2.18 hi	2.82 fg
	NIAB- 2020	135.00 f	196.00 g	0.81 e	2.39 fg	2.92 ef
	DS-30	139.00 e	199.00 f	0.86 d	2.50 ef	2.96 de
	C-3	125.67 g	191.67 h	0.81e	2.29 gh	2.88 ef
800	NIAB-G	252.00 d	288.00 e	0.86 d	2.58 de	2.98 de
	NIAB-SPN	253.00 d	290.00 d	0.89 c	2.68 cd	3.05 cd
	NIAB- 2020	299.23 a	302.00 a	0.99 a	2.92 a	3.59 a
	DS-30	289.17 b	299.33 b	0.96 b	2.89 ab	3.29 b
	C-3	272.80 c	293.00 c	0.94 b	2.78 bc	3.16 c
LSD		2.06	1.71	0.02	0.12	0.12
Data represent the mean of three replicates. Means within the same column having different letters are significantly different at p ≤ 0.05 according to LSD. (Pb = lead); (NIAB-G = NIAB GOLD, NIAB-SPN = NIAB SPINELESS) and (N/D = Not Detected, TF = Translocation factor, BCF = Bio concentration factor).

Principal component analysis

Principal component analysis was performed to analyze the visual comparison of castor genotypes, and to collect information about the inter-relationship between variables at different levels of Pb as shown in Fig. 1. Morpho-physiological parameters, pigment content, antioxidant activities, osmolytes, and Pb uptake were investigated using PCA. Biplot showed that among 8 principal components, 4 have Eigenvalues > 1, while remaining components have not been discussed due to Eigenvalues < 1.

At 0 mg kg^− 1, EL showed strong association with NIAB Gold, NIAB Spineless and C-3 whereas RWW, TF, TSS, CAT, DBM, RWC, FBM, Pb in root and shoot, chlorophyll a, total chlorophyll and bioconcentration factor in roots were linked to DS-30. Ascorbate peroxidase, SC, PR, SOD, TPC, and chlorophyll b co-occurred with NIAB-2020 (Fig. 1-a). It have been observed that with the increase in Pb contamination in soil, major agronomic, physiological and biochemical parameters were strongly connected to DS-30 and NIAB-2020 as compared to NIAB Gold, NIAB Spineless and C-3. At 100 and 200 mg kg^− 1, CAT, TPC, RWC, TSS, APX, TSP, SOD and POD along with other parameters aids in the survival of DS-30 and NIAB-2020 under Pb stress (Fig. 1-b, c). Similar responses were observed at 400 and 800 mg kg^− 1 in DS-30 and NIAB-2020 (Fig. 1-d, e).

Lead exposure have a variety of negative effects on plant growth including physiological disruptions, decreased biomass production, membrane and structural damage and reduced pigment contents. The extent of these effects depends on the type of plant and the concentration of Pb in soil. Our present study have shown that plant height, shoot fresh weight, shoot dry weight and root dry weight in all castor genotypes were decreased due to Pb contamination in soil. Physiological parameters including RWC, EL, SC, TR and PR were also decreased. Photosynthetic pigments including chlorophyll a, b and carotenoids were reduced due to Pb stress.

Plant height was decreased with the increasing concentrations of Pb. Similar trend was reported in Brachiaria mutica (Ullah et al., 2021). This suggests that lead interfered more strongly with the plant's metabolic processes over time. It has been observed that shoot fresh and dry biomass declined in Parthenium hysterophorus (Javaid et al., 2023) due to Pb contamination. Comparable outcomes in terms of shoot fresh and dry biomass in the present study under higher level of Pb contamination were recorded in castor bean. Likewise, a declining trend was observed in root dry weight with increasing levels of Pb contamination. Similar effects of Pb contamination on root dry weight have also been reported in Solanum lycopersicum (Ma et al., 2022) and Sesamum indicum (Naveed et al., 2023).

Relative water content (RWC) is an important parameter in water relation studies. Upon exposure to Pb stress, relative water content was decreased with the increasing Pb concentrations. Previous studies on Helianthus annuus also showed the similar results (Al-Jobori and Kadhim, 2019). In castor bean, electrolyte leakage was increased with the increasing Pb concentrations in soil. Our findings are consistent with the previous studies which reported that exposure to Ni and Pb can increase electrolyte leakage in Coronopus didymus (Sidhu et al., 2016). Observing the gas exchange attributes, stomatal conductance, transpiration and photosynthetic rate were declined with the increasing concentrations of Pb in soil as reported in Corchorus capsularis (Saleem et al., 2020). Exposure to lead (Pb) can have a significant impact on the amount and type of pigments synthesis in plants. Different studies on tomato (Ma et al., 2022) supported the results recorded in castor bean under Pb contamination. The concentrations of chlorophyll and carotenoids were reduced as Pb disrupted the structure and function of enzymes involved in chlorophyll synthesis and directly interact with the components of photosystem II (PSII).

Superoxide dismutase is especially important in providing first-line resistance to the toxic impact of ROS (Zhou et al., 2022). In general, antioxidant activity is promoted under lower levels of heavy metal stress, but it decreases at higher levels of stress. In this study, SOD and POD was decreased with the increasing concentrations of Pb. The decline in SOD and POD in our study may be assigned to Pb stress that damaged the antioxidant enzymatic systems. Similarly, decreasing trend of SOD and POD has been observed in Brachiaria mutica. Conversely, CAT and APX were increased upon exposure to Pb stress. For example, in E. argyi, a concentration-dependent increase in CAT activity was observed in response to Pb toxicity. This suggests that CAT activity may be one of the mechanisms by which castor bean plants detoxify Pb. The increase in CAT activity can be explained by an increase in its substrate (H₂O₂) and could be an adaptive mechanism of the plant to balance H₂O₂ level (Khan et al., 2018).

The production of total soluble proteins in castor bean has been decreased under Pb stress. Previously, under Pb stress Brassica rapa have shown a decline in concentration of TSP (Ahmad et al., 2023). Results showed that TPC have been increased under Pb stress. Similar increase in phenol content has been reported in winter wheat plants under Pb contamination (Jańczak-Pieniążek et al., 2022). Studies have shown that the concentration of soluble sugars in plants increased markebly when exposed to stress. This is a possible mechanism that plants use to mitigate the negative effects of Pb stress. Our findings have shown an abrupt increase in the concentration of total soluble sugars from 200–800 mg kg^− 1. In a previous study, Phaseolus vulgaris showed significant increase in reducing sugars under Pb contamination (Aldoobie et al., 2013).

Castor bean has been well known for its hyperaccumulating efficiency to uptake various heavy metals from soil. Results have shown that accumulation of Pb was higher in roots of castor as compared to shoots. The plant's extensive root system aids in binding and immobilizing lead ions, thereby reducing their movement in the soil profile (Wani et al., 2023). The accumulation of lead is known to increase in a concentration-dependent manner, but its translocation from root to shoot is low in plants such as Zea mays (Yang et al., 2016), Cannabis sativa (Ćaćić et al., 2019), Helianthus annuus (Ullah et al., 2011), Brachiaria mutica (Khan et al., 2018), and Sesbania grandiflora (Malar et al., 2014). Hence, phytoremediation using castor bean could be a promising technology for the removal of heavy metals from contaminated soil. This can help to certify the security of agricultural products, such as fruits and vegetables which are an important part of the human food.

The current study has revealed that Pb toxicity negatively affects the agronomic and physiological parameters, pigment content as well as some osmolytes in castor genotypes due to ROS production and reduced antioxidant capacities. Hyper-Accumulation of Pb was higher in castor roots as compared to shoots. NIAB-2020 and DS-30 showed the better performance as compared to NIAB Gold, NIAB Spineless and C-3. Thus, castor bean has demonstrated its efficiency in multiple phytoremediation mechanisms, making it a versatile tool for remediating lead-contaminated soils.

Acknowledgments

Authors are extremely obliged to NIAB-C, PIEAS, for providing the permission and analytical facilities to carry out the PhD study and complete the research.

Ethics approval and consent to participate

All authors have read, understood, and have complied as applicable with the statement on "Ethical responsibilities of Authors" as found in the Instructions for Authors and are aware that with minor exceptions, no changes can be made to authorship once the paper is submitted. Moreover, all authors consent to participate.

Availability of data and material

The authors confirm that the data supporting the findings of this study are available within the article.

Competing interests

Authors declare no competing interest.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or Not for profit sectors

Authors contributions

Sahar Naveed: literature review, conceptualization, methodology, modeling, result analysis, conclusion, and writing the original manuscript. Sajid Mahmood: conceptualization, supervision/guidance, and reviewed original manuscript. Wajid Ishaque: technical support and helped in concluding the manuscript.

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Differential growth and metal accumulation response of castor bean genotypes on a lead contaminated soil

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Abstract

Figures

Introduction

Materials and methods

Experimental structure and treatment plan

Physicochemical analysis of the experimental soil

Gas exchange parameters

Estimation of relative water content and electrolyte leakage

Plant growth parameters

Determination of photosynthetic activity

Determination of antioxidants enzymes

Determination of total soluble proteins, total soluble sugars and total phenolic contents

Lead concentration in shoot and root

Statistical analysis

Results and Discussion

Effect of Pb contamination on plant growth attributes

Effect of Pb contamination of soil on physiological parameters

Effects of Pb on leaf pigment contents

Effect of Pb on the biochemical profile of castor bean

Lead uptake in castor genotypes

Principal component analysis

Conclusion

Declarations

References

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