Accumulation and distribution of heavy metal cadmium in sweet sorghum

Nong Lam University, Ho Chi Minh City 57 Accumulation and distribution of heavy metal cadmium in sweet sorghum Tra T. T. Dinh Department of Environment and Biology, Quang Binh University, Quang Binh, Vietnam ARTICLE INFO Research Paper Received: October 01, 2019 Revised: November 29, 2019 Accepted: December 09, 2019 Keywords Accumulation Cadmium Distribution Hard dough stage Sweet sorghum Corresponding author Dinh Thi Thanh Tra Email: dinhthanhtra83@gmail.com ABSTRACT Many species of plants have been studied, as well as applied for cleansing the environment. Previous research has concluded that sorghum plants are highly tolerant to metal pollution and capable of reaching high biomass values in the presence of metals. However, the distribution of heavy metals in plant’s parts has not been adequately studied. In this study, two varieties of sweet sorghum (Keller and E- Tian) were grown with 5 levels (0, 5, 10, 25 and 50 ppm) of cadmium (Cd) in order to investigate the accumulation of Cd in plant parts at the hard dough stage. The results clearly showed the absence of Cd in the seeds of the above plants. There was the presence of Cd at the second and fifth leaf when the level of Cd reached 25 - 50 ppm. There was a great correlation coefficient between Cd and the position of the internodes, namely 0.86, 0.96, 0.99, 0.98 with KE, and 0.86, 0.92, 0.94, 0.94 with ET at 5, 10, 25 and 50 ppm Cd (P < 0.01), respectively. The greater the internodes, the lower the accumulation of Cd. The aforementioned plants recorded the high accumulation of Cd in their roots, peaking at 23.27 µg/g (dried weight, dw) in Keller and 21.69 µg/g in E-Tian. Based on these results, it is concluded that the distribution of Cd in the studied sweet sorghum can be arranged in the following order: > stem > old leaves > young leaves. Cited as: Dinh, T. T. T. (2020). Accumulation and distribution of heavy metal cadmium in sweet sorghum. The Journal of Agriculture and Development 19(3), 57-64. 1. Introduction Heavy metal contamination in soil has become a public concern due to industrial development and human activities, such as mining and smelt- ing of metalliferous ores, electroplating, fertilizer and pesticide application, and fuel production (Garbisu & Alkorta, 2003). Excessive heavy met- als, for example, cadmium (Cd), copper (Cu), lead (Pb), chromium (Cr), zinc (Zn), and nickel (Ni), in agricultural areas seriously threaten food safety and public health (Ja¨rup, 2003). Cadmium (Cd) has been placed at seventh rank among the top toxins, although Cd is a non-essential element for crop plants, it is easily taken up by plants growing on Cd-supplemented or Cd- contaminated soils, entering the food chain and causing damage to plant and human health (Ra- hat et al., 2012). Elimination or remediation of heavy metal contamination in soil is urgently needed to prevent humans and animals from tox- icity. Sorghum (Sorghum bicolor L.) is a pro-poor multipurpose crop providing food, feed, fiber, and fuel across a range of agro-ecosystems (Zheng et al., 2011). Sweet sorghum consists of natural vari- ant cultivars of sorghum with abundant sucrose storage in culm and great biomass and is thereby considered an ideal feedstock for biofuel produc- tion (Kokyo et al., 2015). Sweet sorghum will be a competitive candidate species for soil remediation due to its great biomass and strong resistance to adverse environmental conditions. To preliminarily evaluate its potential for phy- toremediation, several morphological and physi- ological characteristics of sorghum were investi- www.jad.hcmuaf.edu.vn The Journal of Agriculture and Development 19(3) 58 Nong Lam University, Ho Chi Minh City gated under heavy metal stresses (Cd, Pb, Zn, Cu) in previous studies (Zhuang et al., 2009; Liu et al., 2011; Soudek et al., 2013). There were several pieces of research which focus on the improvement ability of absorption heavy metal from the contaminated soil (Zhuang et al., 2009; Soudek et al., 2014; Ziarati et al., 2015). The aim of this study was to determine the absorption and distribution of Cd in sweet sorghum plant organs and its distribution in different organs of sweet sorghum. 2. Materials and Methods 2.1. Plant material and experimental design The elite line of sweet sorghum Keller (KE) and E-Tian (ET) were chosen as plant materials. Keller (GRIN access code PI 653617) is an elite sweet sorghum line developed by DM Broadhead at US Sugar Crops Field Station at Meridan, Mis- sissippi in 1982. E-Tian (literally meaning Rus- sian Sweet in Chinese) was introduced into China in the early 1970s and known for having high Brix content in its stem (Zheng et al., 2011). Soil was amended with CdCl2 at final concen- trations of 0, 5, 10, 25, 50 mg/kg. The group not treated with CdCl2 was the control group. The soil was fertilized with base fertilizers (urea, diammonium phosphate, and potassium sulfate), following the technical process for high-yield land application. Seeds were soaked in warm water at 28oC, then placed on a moist filter paper tray in a warm place for germination. After 3 days, the seedlings were subsequently transplanted into plastic pots (diameter: 30 cm; height 25 cm) with peat soil (2 kg soil for 2 seedlings per pot) and cultivated under glasshouse conditions (28 - 32oC with 14 - 16 h light/22 – 26oC with 8 - 10 h dark). The same care conditions and procedures were used for all experimental and control plants. Each ex- periment formula and control formula consisted of 12 plants with 3 replications. Leaves and in- ternodes were numbered from the top to the bot- tom of the plant. The plant materials (root, in- ternodes, leaves, and seed) were harvested when the oldest plants were in the hard dough stage. 2.2. Cd concentration assay The plant samples were dried in a ventilated oven at 105oC for 30 min and 70oC for 48 h and subsequently ground into powders. 0.1 g of the ground sample was soaked in a mixture of HNO3 and HClO4 (3:1; v/v) according to Sun et al. (2008). Cd concentration was determined using a flame atomic absorption spectrometry Hitachi Z5000 (Tokyo, Japan). 2.3. Data analysis The data were calculated using Statistix (ver- sion 10.0). Significant differences were deter- mined by the least significant differences (LSD) at a 5% level of probability. 3. Results 3.1. Cd concentrations in leaves and seeds of sorghum In the control treatment, the concentrations of Cd were not found in any organs of the plant such as the leaf, stem, root, or seed (Figure 1, 2, & 4; Table 1). For the treated plant, there was a significant difference in Cd accumulation in leaf among different Cd treatment levels. In the KE plant, Cd was absent in the second leaf at the lower concentration (5 and 10 ppm), and present when concentration was higher (25 and 50 ppm). The fifth leaf was observed with a presence of Cd at 5 ppm treatment. The highest Cd accumula- tion was recorded by treated 50 ppm Cd (0.9633 µg/g DW). The results displayed the absence of Cd in the seed of a plant in both cultivars, even though Cd concentration was increased from 5 ppm to 50 ppm (Figure 1; Table 1). This result indicated that the transport of Cd from the root to the shoots and then to the seed was strongly inhib- ited. It also suggests that sweet sorghum can be used in safety for providing food, feed, and phy- toremediation. ET plants had a similar trend with KE plant for the accumulation of Cd in organs. By the lower Cd concentration treatments (5 and 10 ppm), Cd was completely absent in leaves and seeds. By the higher Cd treatments (25 and 50 ppm), the presence of Cd in the second leaf and fifth leaf was observed. The fifth leaf had a higher Cd concentration than the second leaf. The higher the concentration Cd treatment, the higher the concentration Cd accumulated in the leaf. There was no presence of Cd in the seed even though Cd concentration was increased from 5 to The Journal of Agriculture and Development 19(3) www.jad.hcmuaf.edu.vn Nong Lam University, Ho Chi Minh City 59 Figure 1. Cadmium concentration in leaves and seeds of a) sweet sorghum KE and b) ET. (DW: dried weight). 50 ppm, similar to the KE seed (Figure 1b, Table 1). 3.2. Cd concentrations in stems of sweet sorghum Compared to the control, more Cd was sig- nificantly enriched in the stem of both sweet sorghum cultivars under excessive Cd condition (Figure 2). The accumulation and distribution of Cd in the internodes of sorghum stem were very different. There was a significant difference in Cd concentration between internodes in stem and be- tween Cd treatment levels. This displayed the dif- ference in the ability of absorption and accumula- tion Cd of sweet sorghum. The Cd concentration in the stem displayed more fold higher than Cd in leaf in both cultivars. For the control plants, Cd was completely ab- sent in the internodes of the stems of both cul- tivars. In KE treated Cd plants, under the lower 5 ppm Cd, Cd was not detected in the intern- odes 1st, 2nd, and 3rd. Cd was detected from the 4th internodes to the 10th internodes. The lower internode had higher Cd concentration (ranged Figure 2. Cd concentration in internodes of sweet sorghum. The internodes were numbered according to the proximity to panicles. (DW: dry weight). from 0.92 µg/g DW to 7.81 µg/g DW at the 4th to 10th internode respectively) (Figure 2a). At the 10 ppm of Cd treatment, Cd was absent in the 1st, 2nd internode, and was detected from the 3rd to the 10th internodes. The highest Cd con- centration was observed at the bottom internode of the stem (10th internode, Cd reached up 10.96 µg/g DW). Cd was recorded at the 2nd internode with 25 ppm Cd, Cd concentration in internodes was increased along the stem. The highest Cd at the 10th internode was 14.51 µg/g DW by 50 ppm Cd. By the highest 50 ppm Cd treatment, Cd was present at the 1st internode (Figure 2a; Table 1) and ranged from 1.65 to 18.13 µg/g DW at 1st to 10th internode respectively. The similar trend was observed in ET, there was a significant difference in accumulation and distribution of Cd in stem among Cd treatment levels. At the lowest Cd treated plant (5 ppm), Cd in 1st and 2nd internode could not be detected. An increase in Cd was recorded from 3rd to the 8th internode (0.598 to 3.617 µg/g DW). At the Cd 10 ppm, Cd was absent in the 1st internode and present from 2nd to 8th internode (0.432 to 5.563 µg/g DW). At 25 and 50 ppm Cd, Cd accu- www.jad.hcmuaf.edu.vn The Journal of Agriculture and Development 19(3) 60 Nong Lam University, Ho Chi Minh City T able 1. C d concentration in organs ofsw eet sorghum at the hard dough stage (µg/g D W ) SS C d Leaf2 Leaf5 Totalleaf Seed I1 I2 I3 I4 I5 I6 I7 I8 I9 I10 R oot K E 0 N D N D N D N D N D N D N D N D N D N D N D N D N D N D N D 5 N D 0.23 ± 0.07 b 0.47 ± 0.07 b N D N D N D N D 0.92 ± 0.29 d 1.29 ±0.18 c 1.77 ± 0.29 d 2.27 ± 0.34 d 3.98 ± 0.76 d 5.63 ± 0.92 d 7.81 ± 0.86 d 2.85 ±0.6 d 10 N D 0.31 ± 0.08 b 0.63 ± 0.07 ab N D N D N D 1.23 ±0.37 c 1.86 ±0.35 c 2.83 ± 0.69 b 4.56 ±0.28 c 7.16 ±0.49 c 9.19 ±0.59 c 10.11 ±0.69 c 10.96 ±0.86 c 6.83 ±0.2 c 25 0.69 ± 0.18 a 0.28 ± 0.06 b 0.58 ± 0.01 ab N D N D 0.68 ±0.2 b 2.48 ± 0.67 b 4.01 ± 0.71 b 6.15 ± 1.40 a 7.86 ± 0.53 b 9.80 ± 0.46 b 11.17 ± 0.59 b 13.22 ± 0.37 b 14.51 ± 0.55 b 13.93 ± 1.19 b 50 0.77 ± 0.15 a 0.96 ± 0.11 a 0.67 ± 0.15 a N D 1.65 ±0.24 2.24 ± 0.65 a 3.88 ± 0.96 a 5.54 ± 0.67 a 7.25 ± 1.11 a 10.97 ± 0.54 a 14.14 ± 0.72 a 14.76 ± 0.75 a 16.26 ± 1.06 a 18.13 ± 0.96 a 23.27 ± 0.13 a ET 0 N D N D N D N D N D N D N D N D N D N D N D N D N A N A N D 5 N D N D N D N D N D N D 0.59 ±0.19 c 0.94 ±0.30 c 1.10 ±0.21 c 1.29 ±0.12 c 2.08 ± 0.28 bc 3.62 ±0.78 c N A N A 3.52 ± 0.29 d 10 N D 0.41 ±0.07 c 0.28 ± 0.02 b N D N D 0.43 ± 0.08 b 1.40 ±0.36 c 1.56 ±0.35 c 1.91 ±0.13 c 2.89 ±0.80 c 3.44 ± 0.27 b 5.56 ± 1.46 b N A N A 7.97 ±0.49 c 25 0.33 ± 0.05 a 0.55 ± 0.14 b 0.71 ± 0.19 a N D 1.29 ± 0.16 b 3.47 ± 0.30 a 6.36 ± 1.44 a 7.64 ± 0.92 a 10.69 ± 1.33 a 10.67 ± 1.30 a 12.19 ± 0.18 a 12.56 ± 0.19 a N A N A 14.46 ± 0.42 b 50 0.51 ± 0.14 a 0,.82 ± 0.06 a 0.77 ± 0.15 a N D 2.64 ± 0.81 a 3.54 ± 0.96 a 4.28 ± 0.75 b 5.52 ± 1.26 b 6.36 ± 1.56 b 7.80 ± 1.97 b 11.00 ± 3.45 a 12.65 ± 0.56 a N A N A 21.69 ± 0.59 a a-dD ata w ith different letters in the sam e colum n of 1 cultivar m eans significant difference at 0.05 level. SS: sw eet sorghum ; I: internode; N D : not detected; N A : not applicable. The Journal of Agriculture and Development 19(3) www.jad.hcmuaf.edu.vn Nong Lam University, Ho Chi Minh City 61 mulation was strongly increased along the stem. Cd accumulation in the 8th internodes was nearly 6-fold higher than that in the 1st internodes (Fig- ure 2b; Table 1). Comparisons with the seedling stage showed Cd accumulation in the stem at the hard dough stage was observed 4 fold higher. This result indicates that the accumulation of Cd was increased more during the longtime of growth. Under Cd exposure, the enriched Cd inhibited differential distribution within the stem of both KE and ET cultivars, which positively correlates with the position of internodes numbered accord- ing to the proximity to panicles. Increases in Cd concentration along the stem from the top in- ternode to the lower internodes could be easily observed. There was a strong positive correla- tion between Cd concentration and internode po- sitions along the stem. The correlation coefficient of KE plant (0.86, 0.96, 0.99, 0.98 for KE and 0.86, 0.92, 0.94, 0.94 for ET by the treated 5, 10, 25 and 50 ppm Cd treatment respectively, P < 0.01). Cd preferen- tially accumulated in the lower internodes, while accumulating less in the upper ones (Figure 3). This indicates that the transport process of Cd from the root up to the tops was strongly inhib- ited. Hence, Cd concentration in the top intern- odes was very low, as in the leaf, and completely absent in the seed. Under Cd exposure, the enriched Cd inhibited differential distribution within the stem of both KE and ET cultivars, which positively correlates with the position of internodes numbered accord- ing to the proximity to panicles. Increases in Cd concentration along the stem from the top in- ternode to the lower internodes could be easily observed. There was a strong positive correla- tion between Cd concentration and internode po- sitions along the stem. The correlation coefficient of KE plant (0.86, 0.96, 0.99, 0.98 for KE and 0.86, 0.92, 0.94, 0.94 for ET by the treated 5, 10, 25 and 50 ppm Cd treatment respectively, P < 0.01). Cd preferen- tially accumulated in the lower internodes, while accumulating less in the upper ones (Figure 3). This indicates that the transport process of Cd from the root up to the tops was strongly inhib- ited. Hence, Cd concentration in the top intern- odes was very low, as in the leaf, and completely absent in the seed. Figure 3. Positive correlation between Cd concen- tration and internode position along the stem. The internodes were numbered according to the proxim- ity to panicles. R indicates the Pearson correlation coefficient. 3.3. Cd concentration in the root of sweet sorghum KE and ET plants could accumulate a high concentration of Cd in the root. There was a significant difference among Cd exposed levels, which displayed differences in absorption and ac- cumulation capacities of Cd in the plant (Figure 4). Figure 4. Cd absorption and accumulation in the root of sweet sorghum (DW: dry weight). www.jad.hcmuaf.edu.vn The Journal of Agriculture and Development 19(3) 62 Nong Lam University, Ho Chi Minh City 4. Discussion The partitioning of Cd to different plant or- gans plays important role in the toxicity of Cd to plants. At the seedling and the hard dough stage, the distribution of Cd was different among organs of sweet sorghum. Results were consistent with previous studies, which showed was Cd in order root > stem > leaf (Barros et al., 2009; Soudek et al., 2013; Ziarati et al., 2015). Tuerxun et al. (2013) found that the Cd concentration in leaves, root, and stem of two sweet sorghum va- rieties increased as to the increased of added Cd content and to the elongation of exposure time. For both varieties of sweet sorghum, roots con- tained the highest Cd content, followed by stem and leaf (Tuerxun et al., 2013). However, Izadi- yar & Yargholi (2010) studied on Cadmium ab- sorption and accumulation in sorghum found that the maximum concentration can be observed in Sorghum root and the minimum concentration in sorghum stem. Cadmium concentration in differ- ent parts of the tested plant species is the follow- ing order of ranking: root > leaf > stem (Izadi- yar & Yargholi, 2010). Probably, the response of sweet sorghum to Cd toxicity is not the same as other sorghums. The results also displayed that the old leaf (the fifth leaf) can accumulate higher Cd than the young leaf (the second leaf) (Figure 1). Maria et al. (2013) indicated that roots and old leaves are the main metal sinks suggesting a defense or tolerance mechanism of the plants to avoid toxic levels in physiologically most active apical tissues (Maria et al., 2013). Moreover, the posi- tion of the fifth leaf was lower than the second leaf along the stem. Combined with the results about distribution Cd in the internodes of the stem (Figure 2), it could be concluded that the process of Cd transport in stem decided the dis- tribution of Cd in aerial parts such as leaf, stem, and seed. Several studies determined the accumu- lation of Cd in the grain of sorghum (Zhuang et al., 2009; Angelova et al., 2011). Angelova et al (2011) studied heavy metals accumulated in dif- ferent sorghums, included grain sorghum, tech- nical sorghum, sugar sorghum, and Sudan grass grown on the soils contaminated with heavy met- als (Pb, Cu, Zn, Cd). Their results showed that heavy metal content in the grains of Sudan grass, technical, and sugar sorghum were in the normal range (below the maximum permissible concen- trations) and did not reach the phytotoxic levels (Angelova et al., 2011). In our result, although Cd treatment was increased from 5 ppm to 50 ppm, there was completely absent of Cd in seed in both cultivars of sweet sorghum (Figure 1; Table 1). Hence, in the present research, the accumulation of Cd was in the following order: roots > stems > old leaf > young leaf > seed. The accumulation of Cd in the stem of sweet sorghum was stud- ied, but all previous studies have no attention to the distribution of Cd in each internode along the stem. This is also one of the new observations of our study. The absorption and accumulation of Cd in the root of both sweet sorghum cultivars in this re- search were consistent with previous studies, root was the highest Cd accumulated part in the plant (Kokyo et al., 2015; Muratova et al., 2015; Nawab et al., 2015). Cadmium was accumulated primar- ily in the roots of sorghum plants and then trans- ferred to the shoots. Sweet sorghum accumulated high Cd in roots and stems, while the shoots had a very low concentration of Cd. Because of the detoxification mechanism in the plant, the plant can uptake and accumulate Cd without being harmed (Cheng, 2003; Etim, 2012; Laghlimi et al., 2015). The inhibition of transport of Cd from roots to shoots may reflect a self-defense mechanism. Studies of Pinto et al. (2006) showed that con- tamination levels of Cd resulted in a correspond- ing increase in concentrations of phytochelatin, produced by Sorghum. Phytochelatins are an im- portant class of cysteine-rich poly peptides, the production of which was increased in response to excessive absorption of metal ions, such as Hg and Cd by plants (Pinto et al., 2006). Soudek et al. (2013) found that in the time dependence experi- ment the cadmium concentration in roots become generally greater than in shoots. The roots seem to have a barrier to prevent the transport of cad- mium to shoots (Soudek et al., 2013). Many species, including sweet sorghum, accu- mulate toxic metals mainly in the roots (Maria et al., 2013; Soudek et al., 2014; Ziarati et al., 2015). For sweet sorghum, increases in the con- centrations of Cd in the soil lead to a higher accu- mulation of this metal in the root. Previous stud- ies demonstrated that sorghum plants were highly tolerant to metal pollution and able to reach high biomass, even in the presence of heavy metals (Marchiol et al., 2007; Epelde et al., 2009; Liu et al., 2011). These results once again confirmed The Journal of Agriculture and Development 19(3) www.jad.hcmuaf.edu.vn Nong Lam University, Ho Chi Minh City 63 the ability to clean up contaminated heavy metal Cd soil of sweet sorghum (Figure 4). The amount of Cd accumulated in the plant is limited by several factors including 1) Cd bioavailability within the rhizosphere; 2) rates of Cd transport into roots via either the apoplastic or symplastic pathways; 3) the proportion of Cd fixed within roots as a Cd- phytochelatin complex and accumulated in the vacuole; and 4) rates of xylem loading and translocation of Cd (Rahat et al., 2012). 5. Conclusions An overall increase of Cd concentration was found in all tissues of the plants (roots, stem, young, mature, and old leaves) by increasing the Cd contamination in the soil. Regardless of treat- ments, Cd concentration in roots always exceeded those in the aboveground dry matter because of a low translocation from roots to shoots. There were significant differences between the heavy metal contents in root, stem and leaf. The Cd was accumulated in the order that root > stem > old leaves > young leaves. The results clearly showed that the absence of Cd in the seeds of the above plants. This study detected that sorghum also had con- siderable accumulation ability to Cd in root and stem. The absence of Cd in seed and inhibition of translocation Cd from root to the shoots may represent the avoid effect on the food chain, which should be suitable for bioremediation. Furthermore, Cd is accumulated preferentially in the lower internodes while scarcely accumu- lated in the upper internodes of both sweet sorghum lines KE and ET. These results sug- gested that excessive Cd accumulation is avoided in leaves, inflorescence, and seeds essential for photosynthate fixation and reproduction. There- fore, Cd accumulation in lower internodes bene- fits the resistance of sweet sorghum to Cd toxicity. In conclusion, sweet sorghum should be a com- petitive candidate species for soil remediation due to its great biomass and strong resistance to ad- verse environmental conditions. Conflicts of interest The authors declare no conflicts of interest. 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