Mitigation of rice cadmium (Cd) accumulation by joint application of organic amendments and selenium (Se) in high-Cd-contaminated soils

Chemosphere 241 (2020) 125106

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Mitigation of rice cadmium (Cd) accumulation by joint application of organic amendments and selenium (Se) in high-Cd-contaminated soils Na Liu a, b, c, Zhenmao Jiang a, b, c, Xiong Li d, Hanyi Liu a, b, c, Na Li a, b, c, Shiqiang Wei a, b, c, * a

College of Resources and Environment, Department of Environment Science and Engineering, Southwest University, Chongqing, 400715, China Chongqing Key Laboratory of Agricultural Resources and Environment, Chongqing, 400715, China State Cultivation Base of Eco-agriculture for Southwest Mountainous Land, Southwest University, Chongqing, 400715, China d College of Natural Resources and Environment, Northwest A & F University, Yangling, 712100, Shaanxi, China b c

h i g h l i g h t s

g r a p h i c a l a b s t r a c t


Organic amendments attenuated Cd bioaccumulation and bioavailability in soil rice systems.
Alleviation of Cd phytotoxicity varied with rice cultivars, organic amendment types and doses.
Joint application of organic amendment and Se could further reduce Cd contents in rice grain.
Mitigation of Cd was due to changes of Cd translocation in rice and inhibition of Cd availability.

a r t i c l e i n f o

a b s t r a c t

Article history: Received 21 July 2019 Received in revised form 5 October 2019 Accepted 11 October 2019 Available online 13 October 2019

A pot experiment was conducted to investigate the possible mediatory effect of organic amendments (vermicompost and biochar) and selenium (Se) on Cd bioaccumulation in both rice cultivars (high-Cd accumulation rice: Yuzhenxiang (YZX) and low-Cd accumulation rice: Changliangyou772 (CLY)) in highCd-contaminated soils. The results showed that Cd sensitivity and tolerance were cultivar-dependent, and grain Cd contents for CLY accorded with the Chinese national food safety standards (0.2 mg kg1), whereas grain Cd levels for YZX were 1.4e5.8 times higher than those for CLY. Soil applications of amendments decreased grain Cd levels by 3.5%e36.9% for YZX and 36.1%e74.4% for CLY. Moreover, vermicompost (VC) was more effective in reducing Cd bioaccumulation than biochar (BC). A combination of Se and organic amendments could significantly increase grain Se contents and help further reduce grain Cd levels by 5.8%e20.8%, compared to the single organic amendments. This mitigation progress could be attributed to the changes of Cd translocation and distribution among rice tissues and the inhibition of Cd bioavailability in soil through the alteration in soil properties. Organic amendments, especially high dose (5%), increased soil pH and organic matter contents, and correspondingly decreased soil Cd bioavailability. A sequential extraction analysis suggested that organic amendments and Se facilitated the transformation of soil Cd from the bioavailable form to the immobilized Cd form, and thus decreased grain Cd levels. Hence, co-applications of organic amendments and Se in combination with

Handling Editor: X. Cao Keywords: Cadmium Organic amendment Selenium Rice Bioavailability and bioaccumulation

* Corresponding author. College of Resources and Environment, Department of Environment Science and Engineering, Southwest University, Chongqing, 400715, China. E-mail address: [email protected] (S. Wei). https://doi.org/10.1016/j.chemosphere.2019.125106 0045-6535/© 2019 Elsevier Ltd. All rights reserved.

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N. Liu et al. / Chemosphere 241 (2020) 125106

low-Cd accumulation cultivar could be an effective strategy for both Se needs of humans and safe utilization of Cd polluted soil. © 2019 Elsevier Ltd. All rights reserved.

1. Introduction Cadmium (Cd) is one of the most harmful and widespread contaminants in agricultural soils, and is persistent to degrade and difficult to remove once entered soils (Jiang et al., 2012). Undoubtedly, Cd adversely affects not only the quality of agriculture products but also human health due to its high toxicity and bioavailability (Khan et al., 2018; Lalor, 2008). In China, approximately 2.786  105 ha of agricultural soils were severely contaminated with Cd (Liu et al., 2015), which threaten the crops quality. Rice (Oryza sativa L.) is the most widely consumed cereal crop in Southeast and East Asia, and thus rice yields and qualities are closely connected with economic development and human health (Huang et al., 2017). However, rice is a major dietary Cd source in the human body because it can efficiently accumulate Cd into grains (Qiao et al., 2018). Accordingly, it is of great urgency to develop effective approaches to reduce Cd bioavailability and accumulation in rice, to restrain the threat of Cd to living organisms. Cd accumulation and translocation in rice are considered to be mainly affected by rice varieties (Arao and Ae, 2003; Liu et al., 2007; Wang et al., 2011), Cd bioavailability (Li et al., 2005, 2017), soil pH (Honma et al., 2016; Yu et al., 2016), and organic matters in soil (Filipovi c et al., 2018; Zeng et al., 2011). Based on this, physical, chemical and biological measures have been undertaken to minimize Cd uptake by crops. Recently, screening and breeding low-Cd rice cultivars are becoming an increasingly concerned strategy for reducing grain Cd uptake because of the significant differences in Cd accumulation among cultivars (Wang et al., 2011; Yu et al., 2006). Additionally, inorganic or organic amendments as modifiers of Cd mobility and bioavailability have been studied widely (Jiang et al., 2012). Soil amendments, such as compost, biochar, lime, straw as well as selenium (Se), have performed positive influence on reducing soil Cd availability (Chen et al., 2018). Vermicompost (VC) is a kind of environment-friendly and humus-like products obtained through earthworms digesting organic residues (Benitez et al., 2000). Compared to conventional composts or commercial remediation approaches, VC shows better effects on soil fertility improvement in virtue of its high porosity, rich humified organic substances, high cationic exchange capacity (CEC), good aeration as well as the ability to promote soil microbial growth and activity, subsequently influencing the speciation and bioavailability of heavy metals in soil (Singh and Kalamdhad, 2013). It was reported that the efficient removal of VC on Cd mainly depends on the binding between Cd2þ and humic matters that can form organo‒metal complexes, and then Cd2þ is sequestered by the sorbent (Wu et al., 2012; Zhang et al., 2019). Consequently, VC has been considered as an effective soil amendment or conditioner. In recent years, biochar (BC), a stale organic material generated by pyrolysis process, has been widely considered as soil conditioner to improve soil quality and immobilize metals in soil (Khan et al., 2013; Rizwan et al., 2018), mainly resulting from its high pH, huge surface areas, strong sorption capacity and the large amounts of metal binding sites (O’Connor et al., 2018; Qiao et al., 2018). For instance, Wang et al. (2018) found that BC performed the better immobilization effect on Cd, in which the percentage of acid extractable Cd was at a lower level. However, the addition of

organic amendments may enhance metal bioavailability, for example, dissolved organic carbon (DOC) from organic amendments may increase metals mobility due to the formation of metalDOC complexes in soil, which can be absorbed by plants ( Bolan and Alam Duraisamy, 2003). Hence, the single organic amendments may result in uncertain consequences for Cd bioaccumulation. Joint application of organic amendments and other agents may provide a clue to offset such deficiencies. Se is an essential micronutrient for human health, despite unnecessary for plants (Tran et al., 2018). However, about 72% of the total land area in China have insufficient Se contents (Feng et al., 2013), and thereby crops are generally Se-deficient to not satisfy human dietary requirements that may cause various health disorders (Tan et al., 2002). A moderate Se can engender beneficial impacts on plants, such as improving plant growth (Lin et al., 2012; Xue et al., 2001), enhancing Se concentrations in the edible parts and reducing Cd transportation and uptake by rice strongly affected by Se bioavailability (Huang et al., 2017; Wan et al., 2016, 2018). Organic amendments (e.g., manures, crop residues, compost and biochar) can regulate Se bioavailability in soil and Se accumulation in crops by altering soil physio-chemical and biological properties. Se can be immobilized in soil by these materials as they have a large proportion of highly condensed organic matter, with low solubility  n et al., 2006). However, at high pH level, in soil solution (Madejo the negatively charged functional groups of organic matter from organic materials may enhance the competition with Se anions to be adsorbed on soil particles, thus increasing Se availability (Wang et al., 2017). Additionally, organic matter input will increase soil DOC characterized by strong reactivity, which may facilitate the immobilized Se release (Li et al., 2017). Thus, the presence of organic amendments could possibly enhance Se-induced Cd reduction in rice owing to the variation in soil properties after applying organic amendments. Recently, Wang et al. (2019b) found that MeHg levels in soil and rice in BC combined Se group were less than those in the single Se or BC group, suggesting the synergistic inhibitory role of BC and Se on MeHg bioaccumulation. Similarly, in this study, Se was used for co-application with organic amendments, and we hypothesize that joint application of organic amendments and Se may be helpful for both further reducing Cd accumulation in rice and enhancing grain Se level. Most studies have paid more attention on the effects and protective mechanisms of single organic amendment or Se on Cd bioaccumulation in crops. Nonetheless, the potential impacts and underlying mechanisms of organic amendment combined Se on Cd and Se accumulation in different rice cultivars, and Cd bioavailability in the rhizosphere soil remain largely unknown. Thus, the aims of this study were to investigate: (1) the effects of different types and dosages of organic amendments on Cd forms in the rhizosphere soil and Cd accumulation in rice; (2) the possibility and underlying mechanisms of further alleviating grain Cd uptake and immobilizing Cd in soil by co-application of organic amendments and Se; (3) the traits of Cd accumulation and translocation in different rice varieties. The results are expected to improve the understanding of the interactions among Cd, Se and organic amendments, help control Cd bioaccumulation and offset the Se deficiency of rice grains in high-Cd-contaminated soil.

N. Liu et al. / Chemosphere 241 (2020) 125106

2. Materials and methods 2.1. Experimental materials The tested soil was collected from the surface layer (0e20 cm depth) of a nearby farmland located at the Southwest University in Chongqing, China. The bulk soil samples were air-dried and ground to pass through 0.25-mm sieves for physical-chemical analyses and through 3-mm sieves for pot experiments. The original soil contained 0.22 mg kg1 Cd. Vermicompost (VC) was purchased from an agricultural corporation (Nanjing, China) where the earthworms were used to manage the cow dung. The rice hull biochar (BC) was produced from a commercial producer through pyrolysis of rice hull at 550  C for 6 h in a high performance automatic controlled furnace (Zhenjiang, China). The basic properties of soil, VC and BC were shown in Table S1. Two rice cultivars, namely Changliangyou772 (CLY, low-Cd accumulation rice) and Yuzhenxiang (YZX, high-Cd accumulation rice) screened by Hunan Academy of Agricultural Sciences, were used in this study. The two rice seeds were surface-sterilized in 30% (v/v) H2O2 for 15 min, rinsed with deionized water, and then germinated on a sterile plastic net floating in deionized water at 25  C. After 4 weeks, uniformly grown seedlings were transplanted to soil-filled pots. 2.2. Rice pot experiments Pot experiments were conducted in a nature climate greenhouse located at the Southwest University in Chongqing, China in 2018. All soils were spiked with 5.0 mg Cd kg1 soil as CdCl2$2H2O, which were chosen to reflect a high contaminated level above the ecotoxicity threshold of Cd (China Soil Environmental Quality Standards GB 15618-2018, pH within a range of 6.5e7.5 for a paddy field, 0.6 mg Cd kg1). CO(NH2)2, K2HPO4 and KCl were applied as the basal fertilizer at 150 mg N kg1, 100 mg P2O5 kg1 and 100 mg K2O kg1 soil, respectively. Meanwhile, VC and BC were added at doses of 0% (CK), 1% and 5% (w/w) to each soil batch treatment respectively, which was comparable with those used in previous studies (Rizwan et al., 2018; Shu et al., 2016), and the part of treatments was added 0.8 mg Se (IV, Na2SeO3) kg1 soil to reach a range of environmentally relevant Se concentrations. Therefore, 9 treatments were set for each rice cultivar, abbreviated as CK, VC1, VC5, VC1þSe, VC5þSe, BC1, BC5, BC1þSe and BC5þSe. Detailed information on these treatments is summarized in Table 1. A compartmented rhizo-bag culture system was used. Each pot (height 20 cm; diameter 20 cm) contained 4 kg soil, 1.0 kg of which was placed in a nylon mesh bag (height 10 cm; diameter 8 cm) set in the center of the pot to create a rhizosphere. The mesh was 48 mm, which allowed the movement of water and dissolved Table 1 The design of the pot experiments. Treatment

CK VC1 VC5 VC1þSe VC5þSe BC1 BC5 BC1þSe BC5þSe

YZX or CLY VC dose (%, w/w)

BC dose (%, w/w)

Se (IV) dose (mg$kg1)

Cd dose (mg$kg1)

0 1 5 1 5 0 0 0 0

0 0 0 0 0 1 5 1 5

0 0 0 0.8 0.8 0 0 0.8 0.8

5 5 5 5 5 5 5 5 5

Note: YZX and CLY represent Yuzhenxiang and Changliangyou772, respectively.

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nutrients but not root penetration. Each treatment was treated with 3 replications, resulting in total 54 pots. For all treatments, soils were firstly flooded with 3 cm tap water above the soil layer and equilibrated for 20 days. Then seedlings of both rice cultivars were transplanted into each rhizosphere bag (two plants per pot). Flooding conditions were maintained throughout the rice-growing period using tap water (3 cm above the soil layer). 2.3. Sampling and chemical analysis Rice harvesting was done after 105 days of transplanting in the pots. Grains, leaves, stems and roots were collected and rinsed thoroughly with tap water and then deionized water. A small part of fresh leaves was quickly put into ice boxes, and then brought into the laboratory for chlorophyll analyses, which were determined following 95% ethanol extraction method (Harmut, 1987). Plant samples were oven-dried at 105  C for 30 min and then at 65  C to a constant weight. The dried samples were crushed and passed through 0.25-mm sieves, following by digestion with concentrated HNO3eHClO4 (4:1, v/v) on an electric furnace. The Cd and Se concentrations in the digestion liquid were determined by ICP-MS (NexION 350D, USA). Meanwhile, the rhizosphere soil inside the nylon mesh bags was carefully sampled for each pot. Soil samples were air-dried and ground for the physical-chemical analyses and the sequential extraction of soil Cd. Soil pH was measured using a pH electrode (PB-10) with a soil-water ratio of 1:2.5. Soil organic matters were determined by the method of potassium dichromate oxidationouter heating (Lu, 2000). According to the sequential extraction procedure from the modified European Union Bureau of Reference (BCR) proposed by Arain et al. (2008), Cd forms in soil were divided into four Cd fractions: the acid extractable Cd (F1) extracted by 0.11 M acetic acid; the fraction bound to Fe/Mn oxides (F2) extracted by 0.5 M hydroxylamine hydrochloride (pH 2); the fraction bound to organic matter (F3) extracted by 30% H2O2 (pH 2e3) and 1 M NH4OAc (pH 2); and the residual fraction (F4) digested with HNO3eHCl. Cd concentrations in the extractable solution were determined with atomic absorption spectrophotometer (TAS-990, China). Certified reference materials (CRM) for plants (GBW10044, GSB22) and soil (GBW07428, GSS-14) provided by the National Research Center for CRM (China) were used for quality assurance and quality control of the analysis of Cd and Se. The recovery rates of Cd in the plant and soil samples were 90%e107% and 86%e112%, respectively, and those of Se in plants were 84%e110%. 2.4. Data analysis Chlorophyll contents of fresh leaves were calculated using the following formula:

  ð13:95A 665  6:88A649 Þ*V Chlorophyll a mg$g1 ; FW ¼ 1000*W

(1)

  ð24:96A 649  7:32A665 Þ*V Chlorophyll b mg$g1 ; FW ¼ 1000*W

(2)

  Total chlorophyll mg$g1 ; FW ¼ chlorophyll a þ chlorophyll b ¼

ð18:16A649 þ 6:63A665 Þ*V 1000*W (3)

where A665 and A649 represent the absorbance at 665 and 649 nm, respectively; V represents distilling volume; W represents leaf fresh

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N. Liu et al. / Chemosphere 241 (2020) 125106

weight. Bio-accumulation factors (BAFs) and translocation factors (TFs) of Cd from roots to stems, stems to leaves, and stems to grains were calculated based on the following equations:

software.

TCd ¼ CrootCd  Rootbiomass þ CstemCd  Stembiomass

3.1. Plant biomass and chlorophyll contents

(4)

þ Cleaf Cd  Leafbiomass þ CgrainCd  Grainbiomass Root  Cd ð%Þ ¼

CrootCd  Rootbiomass  100% TCd

(5)

Stem  Cdð%Þ ¼

CstemCd  Stembiomass  100% TCd

(6)

Leaf  Cd ð%Þ ¼

Cleaf Cd  Leafbiomass  100% TCd

(7)

CgrainCd  Grainbiomass  100% TCd

(8)

Grain  Cdð%Þ ¼

BAF ¼

TF ¼

CrootCd CsoilCd

(9)

CbCd CaCd

(10)

where a represents roots or stems; b represents leaves or grains; CaeCd and Cb-Cd represents Cd concentration in a and b, respectively.

2.5. Statistical analyses Statistical analyses were performed using one-way ANOVA analysis of variance and Tukey’s HSD (Honest Significant Difference) to determine the significance of data (SPSS 21.0 software). The variability in the data was expressed as the standard error, and p < 0.05 was considered to be statistically significant. The correlation analyses were based on the Pearson’s correlation coefficients (P < 0.01 and P < 0.05). All figures were performed with Origin 8.6

3. Results

The biomasses of rice grains, leaves, stems and roots in different treatments are presented in Table 2. Compared to the control, soil applications of VC, BC and Se significantly affect the biomasses of rice tissues (except for leaves), especially grain yields were greatly increased by 10.7%e41.7% for YZX and 1.8%e59.6% for CLY. The highest grain yields of both cultivars were observed in BC þ Se groups. Overall, the grain yields of CLY were higher than those of YZX in each treatment. In no-Se treatments, the grain yields generally increased with increasing addition of organic amendments, which might mainly be explained by an efficient utilization of nutrients facilitating plant growth treated with organic amendments. Compared to single organic amendments, low-rate organic amendments (1%) combined Se resulted in a slight increase of grain yields, by contrast, high-rate organic amendments (5%) combined Se exhibited a slight decrease. Thus, rice grain yields were significantly influenced by rice cultivars, organic amendment dosages and application modes (single- or co-application). Similar effects were observed for leaf chlorophyll contents (Table 2). In the control, chlorophyll a, chlorophyll b and total chlorophyll contents of CLY were considerably higher than those of YZX. Once soil addition of organic amendments, leaf chlorophyll contents were raised apparently, and VC5 treatments possessed the highest total chlorophyll contents, an increase by 107.5% for YZX and 19.3% for CLY compared to the control. In comparison with single organic amendments, Se addition did not significantly affect chlorophyll contents (P > 0.05). Chlorophylls are the participant of energy production and transformation through photosynthesis for crop growth, and thus higher chlorophyll levels often resulted in higher crop yields (Alam et al., 2019). Herein, chlorophyll contents were also closely related to grain yields, especially for YZX, there was a significant positive correlation between chlorophyll contents and grain yields (Table S2), suggesting that soil applications of amendments could increase grain yields by promoting photosynthesis.

Table 2 Effects of organic amendments and Se on rice growth in high-Cd polluted soil. Treatments

Grain g$pot

YZX CK VC1 VC5 VC1þSe VC5þSe BC1 BC5 BC1þSe BC5þSe CLY CK VC1 VC5 VC1þSe VC5þSe BC1 BC5 BC1þSe BC5þSe

1

Leaf

Stem

Root

Chlorophyll a 1

DW

mg$g

Chlorophyll b

Total chlorophyll

FW

12.84 ± 0.91d 14.22 ± 0.76cd 17.21 ± 1.12abc 15.10 ± 0.97abcd 16.53 ± 0.54abc 17.47 ± 1.48 ab 15.67 ± 0.93abcd 18.20 ± 1.33a 14.95 ± 1.54bcd

12.87 ± 0.86a 12.04 ± 0.76a 12.32 ± 1.20a 11.72 ± 1.19a 10.95 ± 1.83a 12.10 ± 1.52a 11.20 ± 0.45a 13.17 ± 0.78a 13.84 ± 0.72a

33.69 ± 2.41a 24.93 ± 0.55b 30.59 ± 2.32 ab 28.51 ± 4.13 ab 28.78 ± 3.44 ab 26.48 ± 3.32 ab 30.18 ± 0.66 ab 30.13 ± 0.80 ab 32.32 ± 3.27a

11.90 ± 0.48b 10.44 ± 1.10b 13.14 ± 1.38 ab 12.30 ± 2.53 ab 13.43 ± 2.01 ab 11.18 ± 1.53b 13.24 ± 1.72 ab 14.36 ± 0.59a 16.02 ± 1.00a

7.01 ± 0.83d 11.41 ± 1.49bc 14.40 ± 0.22a 11.89 ± 0.26bc 13.67 ± 1.12 ab 11.61 ± 0.56bc 12.80 ± 1.48abc 13.13 ± 0.04abc 10.68 ± 0.36c

2.58 ± 0.25d 4.39 ± 0.30bc 5.50 ± 0.11a 4.40 ± 0.03bc 5.17 ± 0.41 ab 4.50 ± 0.28bc 4.78 ± 0.63abc 4.45 ± 0.69bc 4.09 ± 0.16c

9.59 ± 1.07d 15.80 ± 1.79bc 19.90 ± 0.33a 16.29 ± 0.29bc 18.84 ± 1.53 ab 16.11 ± 0.84bc 17.58 ± 2.11abc 17.58 ± 0.64abc 14.78 ± 0.52c

13.65 ± 1.03c 13.90 ± 0.99c 20.83 ± 2.32 ab 19.21 ± 0.90 ab 17.08 ± 1.88bc 18.56 ± 2.07 ab 19.06 ± 1.65 ab 19.31 ± 1.16 ab 21.79 ± 0.78a

13.04 ± 1.01a 14.45 ± 1.17a 14.12 ± 2.38a 13.79 ± 0.42a 13.73 ± 0.96a 13.08 ± 0.97a 11.29 ± 1.54a 13.21 ± 1.00a 13.50 ± 1.06a

31.91 ± 3.72a 26.35 ± 2.91 ab 26.71 ± 1.56 ab 26.49 ± 3.03 ab 26.02 ± 1.44 ab 25.86 ± 4.13 ab 23.33 ± 2.36b 24.94 ± 4.40 ab 28.71 ± 1.95a

10.04 ± 0.63 ab 9.37 ± 1.85b 13.39 ± 2.14a 10.99 ± 0.37 ab 11.53 ± 0.60 ab 10.36 ± 1.73 ab 9.82 ± 1.69 ab 12.31 ± 0.46 ab 11.79 ± 1.48 ab

10.20 ± 0.09b 12.76 ± 1.72a 12.65 ± 0.32a 12.23 ± 0.29a 12.25 ± 0.12a 12.16 ± 0.78a 10.72 ± 0.85 ab 12.52 ± 0.49a 11.64 ± 0.42a

4.50 ± 0.30a 4.69 ± 0.64a 4.88 ± 0.24a 4.89 ± 0.29a 4.80 ± 0.00a 4.60 ± 0.36a 4.29 ± 0.21a 4.92 ± 0.14a 4.43 ± 0.16a

14.70 ± 0.39c 17.44 ± 2.36 ab 17.53 ± 0.56a 17.12 ± 0.00 ab 17.05 ± 0.12 ab 16.76 ± 1.14abc 15.01 ± 1.05bc 17.44 ± 0.36 ab 16.07 ± 0.58abc

Notes: Values are the mean ± SD (n ¼ 3); different letters in the same column indicate significant differences (P < 0.05) among different treatment groups for the same cultivar.

N. Liu et al. / Chemosphere 241 (2020) 125106

3.2. Cd and Se accumulation in rice Cd concentrations in roots, stems, leaves and rice grains in different treatments are given in Fig. 1. The Cd levels in rice tissues varied with rice varieties, organic amendment dosages and types, and application modes (single- or co-application). For both cultivars, Cd concentrations in rice tissues were clearly reduced in the order of root > stem > leaf > grain. Cd levels in grains, leaves, stems and roots of YZX were 1.4e5.8, 0.6e2.0, 0.6e2.4 and 0.4e1.3 times higher than those in CLY tissues, respectively. Whether amendments were added or not, grain Cd concentrations for CLY were far below the maximum level recommended by the Chinese food standard (0.2 mg kg1, GB 2762e2017), but not for YZX. Compared to the control, soil applications of amendments decreased grain Cd levels by 3.5%e36.9% for YZX and by 36.1%e74.4% for CLY, respectively. Cd contents in rice tissues under VC treatments were found to be lower than those under the counterparts with BC in most case, and Cd levels in both rice cultivars decreased with increasing organic amendment dosage. In general, co-application of organic amendments and Se further reduced Cd concentrations in rice tissues, in which grain Cd levels further decreased by 5.8%e20.8% compared to the counterparts with single organic amendments, except for VC1þSe versus VC1 for YZX and VC5þSe versus VC5 for CLY (Fig. 1A). For YZX, Cd concentrations in rice tissues under highrate organic amendments combined Se were obviously less than those under low-rate organic amendments combined Se. Noticeably, VC5þSe treatment was the most effective in reducing grain Cd contents, correspondingly a decrease by 26.3% in comparison with VC1þSe treatment (Fig. 1A). However, for CLY, this was not the case, i.e., VC5þSe treatment generally resulted in a slight increase of Cd levels in CLY tissues (except for the leaf), compared with VC1þSe treatment. Effects of rice varieties, organic amendment dosages and types, as well as the interactions between organic amendments and Se on

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Se concentrations in rice tissues were also examined (Fig. 2). Generally, there were no obvious differences in Se contents in rice tissues among treatment groups without additional Se (P > 0.05), in which grain Se levels were in the range 0.038e0.065 mg kg1 for both cultivars that could not meet the Se requirement of Se-rich rice (0.1e0.8 mg kg1, DB13/T 27022018). However, adjustment with Se dramatically increased Se uptake by both cultivars. Organic amendment types and dosages also greatly influenced rice Se uptake, i.e., BC þ Se groups were obviously more effective in enhancing grain Se levels than VC þ Se groups (Fig. 2A). In BC þ Se treatments, Se concentrations in both cultivars generally remarkably increased with increasing BC dosage, probably attributing to higher Se availability in soil amended with high-rate BC with higher soil pH, organic matter, and the decomposition of organicbound Se (Li et al., 2017), while Se contents in YZX obviously decreased with increasing VC dosage, except for roots. Noticeably, grain Se concentrations in BC5þSe treatment (0.96 ± 0.05 mg kg1 for YZX and 0.98 ± 0.08 mg kg1 for CLY, Fig. 2A) exceeded the maximum Se level in Seenriched rice (0.8 mg kg1, DB13/T 27022018), which might lead to the potential Se toxicity. Therefore, the types and dosages of organic amendments might play an important role in regulating rice Se uptake.

3.3. Cd distribution and translocation in rice Rice cultivars, organic amendment types and dosages, as well as Se significantly affected the distribution and uptake of Cd in rice (Fig. 3 and Table S3). Cd was predominantly distributed in roots of YZX (67.5%e80.3%) and CLY (71.9%e83.0%), while only a small part of Cd was transported to grains (2.4%e5.0% for YZX and 1.5%e2.7% for CLY). Meanwhile, the percentages of Cd in grains and stems for CLY were greatly lower than those for YZX. Overall, organic amendments resulted in an increase of the Cd percentages in grains, mainly attributing to the higher grain yields. Noticeably,

Fig. 1. Effects of VC, BC and Se on Cd accumulation in grains (A), leaves (B), stems (C) and roots (D) of both rice cultivars in high-Cd-contaminated soil. Error bars represent SD of three replicates. For the same rice cultivar, different small letters indicate significant differences (P < 0.05) among different treatments. The dotted line represents the Chinese food maximum Cd level standard (0.2 mg kg1).

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N. Liu et al. / Chemosphere 241 (2020) 125106

Fig. 2. Effects of VC, BC and Se on Se uptake in grains (A), leaves (B), stems (C) and roots (D) of each cultivar in high Cd contaminated soil. The error bars indicate SD of three replicates. For the same cultivar, different small letters indicate significant differences (P < 0.05) among different treatments.

Fig. 3. Effects of VC, BC and Se on the percentages of Cd in different parts of both cultivars.

total Cd uptake by the whole plant in VC1 or BC1 group far exceeded that in VC1þSe or BC1þSe group, respectively (Table S3), implying that co-application of moderate organic amendments and Se might further alleviate the Cd amount in rice. The BAFs and TFs of Cd were determined to evaluate the ability of Cd uptake from soil and transport among rice different tissues, respectively. As shown in Table 3, the BAFs and TFs varied greatly among the treatments. Both BAFs and TFs (except for TFs from stems to leaves) for YZX were markedly higher than those for CLY, suggesting that Cd in soil could be accessibly absorbed by roots and then translocated to grains for high-Cd accumulation rice. Despite the Cd TFs from stems to grains and roots to stems under VC treatments had no significant differences from those under BC treatments (P > 0.05), the BAFs under the former were far less than those under the latter, implying that VC was more effective in reducing grain Cd levels mainly by restraining root Cd

accumulation from soil. For YZX, soil applications of amendments (except for BC1) increased TFs from stems to grains by 0.4%e28.7% compared with the control, but decreased the BAFs by 8.2%e53.6%, and thus grain Cd concentrations in groups with amendments still declined (Fig. 1A). For CLY, amendments decreased Cd BAFs and TFs from stems to grains by 7.1%e63.2% and 5.4%e25.3% compared with the control respectively, correspondingly resulting in a great decrease of grain Cd levels. Compared to the counterparts with single organic amendments, low-rate organic amendments combined Se simultaneously reduced BAFs and TFs from stems to grains, suggesting that this might further restrained Cd levels in CLY grains, which was consistent with the results in Fig. 1A. In summary, amendments might either reduce root Cd uptake from soil or influence Cd transportation in rice tissues, which eventually led to a decrease of grain Cd levels.

N. Liu et al. / Chemosphere 241 (2020) 125106

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Table 3 Changes in Cd bio-accumulation factors (BAFs) and translocation factors (TFs) in rice under different treatments. Treatment

YZX TF

CK VC1 VC5 VC1þSe VC5þSe BC1 BC5 BC1þSe BC5þSe

root to stem

0.11 ± 0.01abc 0.12 ± 0.01 ab 0.13 ± 0.01 ab 0.12 ± 0.02 ab 0.10 ± 0.01bc 0.11 ± 0.01abc 0.08 ± 0.01bc 0.15 ± 0.03a 0.08 ± 0.00c

CLY TF

stem to leaf

0.80 ± 0.08a 0.64 ± 0.04bcd 0.75 ± 0.04abc 0.75 ± 0.06abc 0.75 ± 0.05 ab 0.58 ± 0.06de 0.60 ± 0.05de 0.49 ± 0.04e 0.60 ± 0.03cde

TF

stem to grain

0.33 ± 0.03 ab 0.36 ± 0.02 ab 0.42 ± 0.05a 0.41 ± 0.01a 0.41 ± 0.04a 0.28 ± 0.03b 0.40 ± 0.02a 0.33 ± 0.03 ab 0.38 ± 0.05a

BAF

TF

TF

2.21 ± 0.27a 1.52 ± 0.11cd 1.03 ± 0.12e 1.28 ± 0.11de 1.13 ± 0.11de 2.29 ± 0.11a 2.03 ± 0.13 ab 1.41 ± 0.15cde 1.72 ± 0.11bc

0.08 ± 0.00 ab 0.07 ± 0.01 ab 0.06 ± 0.01b 0.10 ± 0.01a 0.08 ± 0.02 ab 0.07 ± 0.01 ab 0.08 ± 0.01 ab 0.10 ± 0.02a 0.07 ± 0.00 ab

root to stem

stem to leaf

0.65 ± 0.08cd 0.86 ± 0.016b 1.21 ± 0.17a 0.81 ± 0.05bc 0.66 ± 0.07cd 0.58 ± 0.04d 0.85 ± 0.03b 0.35 ± 0.05e 0.75 ± 0.14bcd

TF

stem to grain

0.26 ± 0.03a 0.21 ± 0.01abc 0.21 ± 0.03abc 0.19 ± 0.02bc 0.19 ± 0.02c 0.20 ± 0.02bc 0.20 ± 0.01bc 0.19 ± 0.00c 0.25 ± 0.01 ab

BAF 1.56 ± 0.16a 0.94 ± 0.13cd 0.72 ± 0.09de 0.57 ± 0.06e 0.74 ± 0.12de 1.44 ± 0.10 ab 1.19 ± 0.12bc 0.92 ± 0.10cd 1.00 ± 0.11cd

Note: Different letters in the same column indicate significant difference among treatment groups (P < 0.05) (n ¼ 3).

3.4. Cd speciation distribution in the rhizosphere soil To analyze the distribution of Cd speciation in the rhizosphere soil, the percentages and concentrations of four Cd forms were detected by the improved BCR extraction (Fig. 4 and Table S4). The acid extractable Cd normally represented the bioavailable Cd for plants, while oxidizable and residual forms implied the immobilized Cd in soil due to difficulty to release from soil. As shown in Fig. 4, the majority of the total Cd in the rhizosphere soil existed as the acid extractable Cd (F1) for YZX and reducible Cd (F2) for CLY respectively, conversely, oxidizable (F3) and residual fraction (F4) occupied a small part of the total Cd. Compared with the control, soil applications of amendments generally decreased the concentrations and percentages of F1, accompanying by an increase of F3 and F4, indicating that amendments could facilitated in the transformation from the available Cd to the immobilized forms. Meanwhile, F1 contents declined with increasing organic amendments, whereas F3 and F4 levels generally increased (Table S4). Se addition had a positive effect on Cd immobilization that the lower percentage and concentration of F1 in the rhizosphere soil were observed in organic amendments combined Se treatments, while F3 and F4 showed the opposite trend in most case (Fig. 4 and Table S4). To elucidate the relationship between Cd levels in rice and Cd forms in soil, a further multiple liner regression analysis was explored (Table 4). There was a significant correlation between Cd concentrations in rice and Cd fractions in soil. For both cultivars, Cd contents in rice were greatly influenced by F1, F2 and F3, and F1 had a significantly positive contribution to Cd concentrations in rice, whereas F2 and F3 showed greatly negative contributions.

Table 4 Regression equations between Cd concentration in rice tissues and Cd speciation in the rhizosphere soil. Regression equations Grain Leaf Stem Root

Y Y Y Y

¼ ¼ ¼ ¼

0.14 þ 0.42 F1 ‒ 0.35 F2 ‒ 0.02 F3 0.92 þ 0.45 F1 ‒ 0.51 F2 ‒ 0.70 F3 0.70 þ 0.87 F1 ‒ 0.67 F2 ‒ 0.81 F3 5.83 þ 7.79 F1 þ 0.68 F2 ‒ 10.24 F3

F 38.11** 18.94** 19.20** 9.67**

Notes: F1, F2 and F3 indicated the contents of acid extractable, reducible and oxidizable Cd, respectively; ** represented the significance at 0.01 level.

3.5. The pH and organic matter in the rhizosphere soil As shown in Fig. 5, the pH and organic matter in the rhizosphere soil markedly varied over soil application of amendments. Compared with the control, soil applications of amendments generally increased soil pH and organic matter contents, which increased with increasing organic amendments. BC groups exhibited obviously higher pH than the corresponding VC groups, i.e., soil pH in BC5 treatment (8.32) was substantially higher than that in VC5 treatment (8.21) for YZX (Fig. 5A). For CLY, soil pH in BC5þSe treatment was higher than BC5 treatment, which might be because the adsorption of oxyanions containing Se in soil caused the hydroxyl ions release to soil solution, finally resulting in a slight elevation of soil pH in BC5þSe treatment. Nevertheless, there was no significant difference in soil pH between organic amendments combined Se and the corresponding organic amendments alone (P > 0.05). Soil organic matters under VC treatments, especially high-rate VC, were higher than those under BC treatments, probably attributing to the more amount of organic carbon input from VC into soil. Compared with organic amendments alone, co-

Fig. 4. The percentages of Cd speciation in the total Cd in the rhizosphere soil with organic amendments (VC and BC) and Se for both cultivars (a, b). Cd speciation: F1 (acid extractable fraction), F2 (reducible fraction), F3 (oxidizable fraction) and F4 (residual fraction).

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Fig. 5. Effects of organic amendments and Se on the pH (A) and organic matter (B) in the rhizosphere soil. Error bars represent SD of three replicates. For the same rice cultivar, different small letters indicate significant differences (P < 0.05) among different treatments.

applications of organic amendments and Se reduced soil organic matter contents. 4. Discussion 4.1. The traits of Cd accumulation and translocation in different rice varieties The experimental results showed that the low-Cd accumulation rice CLY accumulated much less Cd compared to high-Cd accumulation cultivar YZX, and grain Cd concentrations of the former could match the requirement of Chinese national food safety standards even in high-Cd-contaminated soil (Fig. 1A), indicating that the Cd accumulation in rice grains were largely cultivar-dependent, which were in good accordance with previous studies (Liu et al., 2007; Wang et al., 2011). The discrepancy of Cd accumulation in different rice cultivars may be resulted from their genotype difference. It was reported that low-Cd accumulation cultivar could absorb less Cd by reducing Cd bioavailability in the rhizosphere soil via various mechanisms such as secretion of root organic acid, alteration of root oxidation etc. (Ye et al., 2012), and/or restrain Cd translocation from roots to shoots by selectively binding Cd into root vacuoles (Ueno et al., 2010; Huang et al., 2017). This is supported by the lower available Cd level in the rhizosphere soil, and apparently lower BAFs and TFs (from roots to stems and stems to grains, Table 3) for CLY comparing to YZX. Therefore, the screening and breeding of low-Cd accumulation rice cultivars are special effective in reducing the risk of Cd accumulation in rice in Cd-contaminated soil.

instance, the grain yield of YZX in VC5 treatment was 1.34 times as many as the control, while Cd levels in grains in the control were 1.29 times as many as those in VC5 treatment. Furthermore, organic amendments facilitated the retention or immobilization of high amounts of Cd in roots (Fig. 3), which was considered as a vital process for protecting against Cd spread in plants (Lux et al., 2010). Once absorbed by roots, there might be two major pathways of Cd transport from roots to grains: (1) Cd is taken up and directly transported to the developing grains through the xylem, or (2) Cd is transported to the actively transpiring parts (e.g., culms, rachis, flag leaves and the external parts of panicles), and subsequently rapidly remobilized to grains via phloem (Rodda et al., 2011). Herein, there was a significant positive liner correlation between grain-Cd and leaf-Cd or stem-Cd or root-Cd (Fig. 6), indicating that lower Cd accumulation in roots, stems and leaves was also responsible for lower Cd accumulation in grains under organic amendment groups. Noticeably, we observed that organic amendments efficiently inhibited Cd translocation from stems to grains, and concomitantly increased translocation from stems to leaves for CLY (Table 3), suggesting that amendments used in this study could reduce Cd uptake by grains through the priority Cd accumulation in leaves. Given that heavy metals in soil were not completely available for plant uptake, only those bioavailable forms could be absorbed by plants (Sarwar et al., 2010). Murakami et al. (2008) documented that the exchangeable Cd fraction in soil was the best measure

4.2. Effects of organic amendments on Cd accumulation in rice It was reported that, in Cd-contaminated acidic soil, grain Cd contents in the treatment of single cultivation low-Cd accumulation rice could still not meet the limit standard (Chen et al., 2018; Wang et al., 2019a), and thus it would be necessary to combine with other measures such as soil application of amendments. Here, for both cultivars, organic amendments not only further effectively reduced Cd concentrations in rice tissues but also obviously improved grain yields, indicating that amendments used in our study still played a positive role in mitigating Cd accumulation in rice, of which effects varied with rice cultivars, and types and dosages of these amendments. This mitigation process might be mainly resulted from the variations in rice biomass, Cd phytoavailability, and soil properties. Our study observed that a decrease in grain Cd concentrations was accompanied with an increase in grain yields following additions of organic amendments (Table 2 and Fig. 1A), corresponding to so-called bio-dilution effect, which was in agreement with previous studies (Rizwan et al., 2018). For

Fig. 6. Correlations between grain-Cd concentrations and leaf-Cd, stem-Cd or root-Cd concentrations for all treatments. Cg, Cl, Cs and Cr represent the concentrations of grains, leaves, stems and roots, respectively.

N. Liu et al. / Chemosphere 241 (2020) 125106

among the five Cd forms for predicting Cd uptake by soybeans. Here, the acid extractable Cd had greatly positive contribution to Cd concentrations in rice (Table 4), which was in good agreement with Yanai et al. (2006) study. Nevertheless, reducible and oxidizable Cd showed remarkably negative contributions to Cd contents in rice. After flooding, the reduction condition induces the reactions of 2 Fe3þ to Fe2þ and SO2 (de Livera et al., 2011), then S2 4 to S 2þ 2þ combines with Cd and Fe to form CdS and FeS, which are insoluble in soil solution (Porter et al., 2004), and subsequently reduce rice Cd uptake. This well explained why high-rate organic amendments (higher reducible and oxidizable Cd) were more effective in reducing Cd accumulation in rice than low-rate organic amendments. The discrepancy of the immobilized effects of amendments on Cd was generally attributed to the combination of the complexation of Cd and amendment compositions, and the changes in soil properties, such as pH, CEC, organic matter and so on (Ding et al., 2013; Li et al., 2017; Qiao et al., 2018). It was reported that heavy metals were less mobile and bio-accessible in alkaline soil than in acid soil (Rizwan et al., 2018), attributing to the low solubility of Cd2þ at a higher pH (Qiao et al., 2018). Herein, soil pH under amendment groups increased to alkaline levels, especially highrate organic amendments, which accordingly possessed lower acid extractable Cd. Generally, the soil with high organic matter would have high adsorption capacity, facilitate Cd to form stable complexes with humic substances, and redistribute Cd from available forms to less accessible fractions (Walker et al., 2004), and thus reduce Cd bioavailability and accumulation in rice. Here, the soil treated with VC had obviously higher soil organic matter compared to BC (Fig. 5B), which could probably adsorb more Cd or form more complexes with Cd in VC group. Additionally, the soil in VC group mostly had lower acid extractable Cd, and higher organicbound Cd and residual Cd than BC (Fig. 4). These might explain why Cd levels in rice under VC treatment was lower than those under BC treatment. Indeed, effects of organic matters on Cd bioavailability are complicated and controlled by their structures and characterization, i.e., some low molecular weight organic acids may facilitate  ski et al., 1998), whereas the Cd uptake by plants (Cieslin complexation of Cd and large molecules like humic acid was considered to reduce Cd availability to plants (Voigt et al., 2006). These factors should be investigated in future studies.

4.3. The combined effects of organic amendments and Se on Cd accumulation in rice Even though single organic amendments could reduce Cd accumulation in rice, grain Se levels were way off Se needs of human beings. Soil co-application of organic amendments and Se could address this concern that not only increased grain Se contents (Fig. 2), but also further alleviated the risk of Cd uptake in rice (Fig. 1). The decrease in Cd accumulation in rice under organic amendments combined Se groups was likely to be related to the variation in Se phytoavailability, because Se uptake by rice under organic amendments combined Se groups greatly differed from those of the counterparts without Se addition (Fig. 2). Despite no extracellular competition between Cd and Se anions (SeO2 3 and SeO2 4 ) for uptake by roots (Wan et al., 2016), Se addition could enhance the apoplastic barriers (Casparian bands and suberin lamellae) in the endodermis that may restrain heavy metal uptake and translocation in rice (Wang et al., 2014). Similar with S, the moderate Se may play a crucial role in inducing glutathione (GSH) and phytochelatins (PCs), which are essential for the sequestration and detoxification of Cd (Schiavon et al., 2016). Lin et al. (2012) also suggested that there was possible competition for specific binding

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sites in proteins between Cd and Se. In this study, Se addition promoted the Cd retention in roots, as indicated by the higher percentages of root distribution (i.e., VC5þSe and BC5þSe versus VC5 and BC5 for YZX, Fig. 3). However, Cd levels in CLY tissues (except for leaves) under VC5þSe treatment were slightly higher than those under VC5 treatment (Fig. 1), which was possibly because Se anions could also act as a buffer or reagent, which led to the formation of CdSeO03 and CdSeO04 that could be absorbed more efficiently by plants (Huang et al., 2018). The Se-induced reduction in Cd levels in rice might be also attributed to a decrease of the bioavailable Cd fraction in soil, which was consistent with previous studies (Huang et al., 2018). Interestingly, in organic amendments combined Se groups, acid extractable Cd in the rhizosphere soil decreased with increasing organic amendment dosage, however, the immobilized Cd forms increased (Table S4). The effectiveness of Se in reducing rice Cd accumulation was influenced by the changes in soil properties. Organic amendments could further influence Se-induced Cd reduction in rice through the variation in soil properties. Cd accumulation in whole plant under low-rate organic amendments combined Se treatments was generally lower than those under single counterparts (Table S3), implying the synergistic inhibitory effects of Se and organic amendments on Cd uptake by rice. However, co-application of excessive organic amendments and Se might result in the potential Se toxicity, i.e., in BC5þSe groups, grain Se contents for both cultivars exceeded the maximum Se level in Seenriched rice (0.8 mg kg1, DB13/T 27022018), and therefore more attention should be paid to the doses of amendments. Consequently, the synthetic variations in grain biomass, soil properties, Cd speciation and availability in soil, and Cd transportation and distribution among rice tissues eventually resulted in the mitigation of Cd accumulation in grains. 5. Conclusion In this study, the addition of organic amendments could effectively reduce the Cd uptake by rice that varied greatly with rice cultivars, types and doses of organic amendments, and Se under high-Cd-contaminated soil. The possible reasons for the decreased Cd accumulation are that organic amendments influences soil properties, reduces soil Cd bioavailability, and subsequently affect Cd translocation and distribution in rice tissues. The co-application of moderate organic amendments and Se have synergistic effects, briefly, this could not only enhance the Cd transformation from the bioavailable Cd to less accessible Cd forms, and thereby further alleviate Cd accumulate in rice, but also greatly increase Se uptake by grains to help overcome Se deficiency in humans. Thus, coapplication of moderate organic amendments and Se, combined with planting low-Cd accumulation rice, may be a promising remediation practice to have the ability to offset the deficiencies of single amendments and meet food safety standards. Acknowledgement This work was financially supported by the National Key R & D Program of China (2018YFD0800600), Chongqing Key R & D Program (cstc2017shms-zdyfX0008) and the National Natural Science Foundation of China (No. 41771347). Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.chemosphere.2019.125106.

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