Cadmium uptake, translocation, and redistribution affect Cd accumulation in grain of common wheat (Triticum aestivum L.) cultivars

To study the cadmium (Cd) accumulation in wheat grain, we evaluated the grain Cd concentrations of 46 common wheat cultivars grown at two sites in Sichuan, China and selected ve different grain Cd accumulators (a high-Cd accumulator ZM18, four low-Cd accumulators YM51, YM53, SM969 and CM104) to explore the physiological processes of Cd accumulation in the grain of wheat grown under varying degrees of Cd stress. Our results showed that the Cd concentration in grain differed among genotypes. Under low-Cd stress, the grain Cd concentration was correlated with the Cd translocation factor (TF) of roots to grain and all the Cd redistribution factors (RFs). Compared with the ZM18, the cultivars YM53 and SM969 accumulated less Cd in the grain due to low Cd redistribution from lower stems and older leaves to grain. The low-Cd accumulators YM51 and CM104 were due to low Cd transport from roots to grain, and low Cd redistribution from glumes, ag leaves, lower stems, and older leaves to grain. Under high-Cd stress, the ZM18, YM53, and SM969 accumulated signicantly more Cd in the grain, root and other tissues than did YM51 and CM104. Correlation analyses showed that the grain Cd concentration of wheat under high Cd stress was positively correlated with the Cd concentration in each tissue and the TFs of roots to grains, rachis, internode 1 and ag leaves.


Background
Cadmium (Cd) is a toxic heavy metal that is not biodegradable and is harmful to all living organisms. Many arable soils in the world are contaminated by Cd, which is released from industrial and agricultural processes Cereal crops grown in Cd-contaminated soils accumulate high concentrations of Cd in the grain. The direct or indirect consumption of these Cdpolluted products poses potential risks to human health (Grant et al., 2008). Thus, reduction of Cd accumulation in grain is an important goal of crop genetic improvement programs.
Wheat is a major staple food for more than half of the world's population. However, increasing areas of arable soils of wheat-growing regions, such as the Yangtze River Basin and the Huang-Huai-Hai Plain in China, have become contaminated by Cd (Liao et al., 2008). Many wheat cultivars grown in Cd-contaminated soils accumulate Cd in grain to more than the recommended limit of 0.2 µg/g, as proposed by the Codes Alimentarius Commission (2005). Therefore, wheat is the main contributor to the average daily dietary intake of Cd in many countries and regions, such as Japan, America, Sweden, and Iran (Greger and Löfstedt, 2004;Stolt et al., 2006;Kubo et al., 2008;Jafarnejadi et al., 2011;Liang et al., 2017). There is an urgent need to limit Cd accumulation in grain. Wheat grain accumulates Cd by three main physiological processes: Cd uptake by roots; Cd transport from roots to shoots; and then Cd redistribution from shoots to grain (Clemens et al., 2002;Arduini et al., 2014;Li et al., 2017). The accumulation of Cd in wheat grain is controlled by genetic factors, and is also affected by environmental conditions (Greger and Löfstedt, 2004;Stolt et al., 2006;Kubo et al., 2008;Jafarnejadi et al., 2011;Liang et al., 2017). To reduce the Cd concentration in wheat grain, therefore, it is necessary to know the differences in Cd accumulation in grain among local wheat varieties and determine the physiological processes that underlie the differences.
In cereals, Cd absorbed by the roots can be directly transported to grain; this process is dependent on the Cd concentration in soil and the retention of Cd in roots. In a previous study on wheat in the United states, the Cd concentration in common wheat grain was not correlated with the retention of Cd in roots of plants grown in soil with low Cd contents (Greger and Landberg, 2008;Kubo et al., 2011;Liang et al., 2017), but was positively correlated with root morphological parameters of plants grown in soil with a high Cd contents (about 2.5 mg/kg) (Liang et al., 2017). In other studies, the grain Cd concentration of common wheat was found to be positively correlated with Cd translocation from roots to shoots (Greger and Löfstedt, 2004). A major dominant gene (Cdu1) limiting Cd translocation from roots to shoots in tetraploid wheat could explain only 20% of the phenotypic variation in grain Cd concentration in common wheat (Wiebe et al., 2010;Pozniak et al., 2012;Harris and Taylor, 2013;Liu et al., 2019). The Cd concentration in grain was found to be positively correlated with the Cd concentration in shoot (Liang et al., 2017). Together, these ndings imply that Cd redistribution from shoots to grain and Cd accumulation Cd in shoots are responsible for grain Cd accumulation (Stolt et al., 2006;Kubo et al., 2011Kubo et al., , 2016Liang et al., 2017). However, it is unknown which shoot part ( ag leaf, older-leaf, internode 1, lower-stem, rachis and glume) contributes the most Cd to grain, or retains Cd to limit its redistribution to grain, in common wheat. Kubo et al. (2016) reported that differences in Cd sequestration between roots and shoot parts could explain differences in grain Cd concentrations; however, their results were obtained glasshouse experiments in pots containing low Cd (0.40 mg/kg). To date, no experiments under open-air condition of eld have been conducted to determine how Cd uptake and accumulation in roots and shoots affect grain Cd accumulation under low-Cd stress during the wheat growing season. Moreover, common wheat cultivars from different ecotypes show different characteristics of Cd accumulation. Thus, it is important to evaluate a range of cultivars to reveal the physiological mechanisms of grain Cd accumulation, and improve the selection of wheat germplasm with low Cd accumulation. In Sichuan, one of the most seriously Cd-contaminated provinces of China, the Cd concentration of arable soil ranges from 0.06 to 4.76 mg/kg (Liu et al., 2016). Under high-Cd stress, it is unknown how Cd is taken up and retention in roots, translocated from roots to shoots, and redistribution from shoots to grain. To answer these questions, we (1) selected several low-Cd accumulators and a high-Cd accumulator after evaluating the grain Cd concentrations of 46 common wheat cultivars; (2) explored the physiological mechanisms of grain Cd accumulation during the wheat growing season in pot experiments with low-Cd stress (0.40 mg/kg) and high-Cd stress (4.00 mg/kg) under the open-air conditions, by determining the Cd concentrations in roots and shoot parts, calculating the Cd translocation factor (TFs) from roots to shoot parts, and calculating the Cd redistribution factor (RFs) from shoot parts to grain.

Plant Materials
Forty-six Chinese common wheat cultivars (36 of them collected from the Southwest wheat region, and 10 of them collected from Huang-Huai-Hai Plain wheat region) were provided by Prof. Jun Li, from Crop Research Institute, Sichuan Academy of Agricultural Sciences. In this study, all cultivars used to investigate the differences of their grain Cd accumulation were planted at two sites, Wenjiang and Shifang, which have high Cd contents in arable soils, in Sichuan, China (Liu et al., 2010;Qian et al., 2014). Five cultivars were selected for analyses, which include three low-Cd accumulators, one high-Cd accumulator, and one variable-Cd accumulator. For these cultivars, we investigated the Cd concentrations in the roots and shoots at the seedling and the mature stages for plants grown in pots under low-Cd and high-Cd stresses in the wheat growing season under open-air environment. The three low-Cd accumulators were Yunmai 51 (YM51) and Yunmai 53 (YM53) from Yunnan and Shumai 969 (SM969) from Sichuan. The high-Cd accumulator was Zhoumai 18 (ZM18) from Henan. The variable-Cd accumulator was Chuanmai 104 (CM104, from Sichuan), its grain Cd concentrations differed signi cantly between the Wenjiang and Shifang sites.

Field experiment
To investigate the differences in grain Cd concentrations, the 46 cultivars were grown at the Wenjiang experimental eld at Sichuan Agricultural University, and the Shifang upland elds of Chengdu Institute of Biology, Chinese Academy of Science, Sichuan, China, in the 2015-2016 wheat growing season (from 26 October, 2015 to 1 June, 2016). Each cultivar was planted in 10 rows (each row 2 m long, with 20 plants per line). At maturity, 15 spikes were stochastically collected from each row to measure the grain Cd concentration.

Pot experiment
To reveal the physiological mechanisms of grain Cd accumulation in open-air grown wheat plants under low-Cd (Cd concentration, 0.4 mg/kg soil) stress and high-Cd (Cd concentration, 4 mg/kg soil) stresses, the ve selected wheat cultivars were grown in pots at the Wenjiang experimental eld (the elements concentration of soil were showed in STable 1) in the 2016-2017 wheat growing season at Sichuan Agricultural University as described above. Seeds of the wheat cultivars were sterilized with 5‰ NaClO for 10 min, washed three times with distilled water, and then allowed to imbibe in deionized water for 24 h. They were then left to germinate at 20 ℃ for 6 days. Six seedlings were grown in each pot lled with 6.5 kg soil, which had been mixed with CdCl 2 solution to give a nal Cd concentration of 4 mg/kg. There were 10 pots of each cultivar. At the seedling stage, three seedlings per pot were randomly harvested and divided into roots and shoots. At maturity, all plants were collected and divided into eight parts as described above, then dried at 80 ℃ before determining the Cd concentration.
The Cd concentrations in roots and shoots represented the Cd accumulation of the roots and shoot parts, respectively; the ratio of shoot Cd concentration to root Cd concentration (translocation factor, TF) represented the Cd translocated from roots to shoots; the ratio of grain Cd concentration to each shoot part Cd concentration (redistribution factor, RF) represented the Cd translocation from different shoot parts to grain (Yan et al., 2010, Shi et al., 2015.

Statistical analyses
Data means ± standard deviation was obtained from three independent biological replicates. One-way analyses of variance (ANOVA) were carried out with SPSS software (version 20.0 for windows; IBM Japan Ltd., Tokyo, Japan). The normal distribution and the homogeneity of variance test of all raw observations were determined using Shapiro-Wilk test and one-way ANOVA test, respectively. When all data passed the normal distribution and the homogeneity of variance test, the differences of data among the treatments were then further analyzed using Duncan's test (P ≤ 0.05). Pearson Correlation was used to analyze the correlations among the treatments (P ≤ 0.05 and P ≤ 0.01). All diagrams were constructed using SigmaPlot (version 12.0, Systat Software Inc. San Jose, CA).

Differences in grain Cd concentrations among wheat cultivars
The Cd concentrations in seeds were determined for 46 wheat cultivars collected from Wenjiang and Shifang in the 2015-2016 wheat growing season. Their grain Cd concentrations ranged from 0.09 to 0.34 µg/g (average, 0.18 ± 0.06 µg/g) in Wenjiang and from 0.08 to 0.38 µg/g (average, 0.13 ± 0.05 µg/g) in Shifang. Of the 46 cultivars, 15 accumulated more than 0.20 µg/g Cd in the grain in Wenjiang, but only three accumulated Cd to this level in Shifang (Fig. 1). Twelve cultivars showed similar grain Cd concentrations between Wenjiang and Shifang, and 31 cultivars had signi cantly higher grain Cd concentrations in Wenjiang than in Shifang; only three cultivars had higher grain Cd concentrations in Shifang than in Wenjiang (Fig. 1). There was a signi cant correlation (r 2 = 0.457, n = 46) between grain Cd concentrations in Wenjiang and Shifang (Fig. 1).
Cd concentrations in different tissues, and TFs and RFs in wheat under low-Cd stress To understand the physiological mechanisms of grain Cd accumulation under low-Cd stress, we investigated the Cd concentrations in various tissues, and calculated the TFs and/or the RFs at the seedling and maturity stages of wheat cultivars under open-air condition. At the seedling stage, the Cd concentrations in the roots and shoots were similar between SM969 and ZM18, but were signi cantly higher than the other cultivars. Although the Cd concentrations in roots were similar among YM51, YM53 and CM104, the Cd concentrations in shoots differed among cultivars (YM51 > YM53 > CM104) (Table 1). However, their TFs were similar ( Table 1). Correlation analyses showed that the Cd concentration in grain was not correlated with the Cd concentrations in roots and shoots or with the TF at the seedling stage (STable 2). At the mature stage, ZM18 accumulated the highest Cd concentration in the grain among all ve cultivars ( Fig. 2A). Thus, ZM18 served as the high-Cd accumulator in this study to understand the physiological mechanisms of grain Cd accumulation. The Cd concentrations in roots and lower stems did not differ signi cantly among the ve cultivars ( Fig. 2B and 2C). The Cd concentrations in older leaves were similar among YM53, SM969, and ZM18, and were noticeably lower than those in YM51 and CM104 (Fig. 2D). In ag leaves, the Cd concentration was only higher in CM104 than in ZM18 (Fig. 2E). In internode 1, the Cd concentration was signi cantly lower in YM51 than in ZM18 (Fig. 2F). The Cd concentrations in the rachis were signi cantly lower in YM51 and SM969 than in ZM18; and were also lower in YM53 and CM104 than in ZM18, but those differences were not signi cant (Fig. 2G). For glumes, although the Cd concentrations were lower in YM51, YM53, SM969, and CM104 than in ZM18, the difference was only signi cant for SM969 (Fig. 2H). Correlation analyses indicated that the Cd concentration in grain was signi cantly positively correlated with the Cd concentrations in the glumes and rachis (Table 4). To evaluate Cd translocation from roots to shoot parts, the TFs were calculated (Table 2). There was no signi cant difference among the ve cultivars in the TFs of roots to total shoots, roots to lower stems, roots to internode 1, roots to rachis, and roots to glumes. The TFs of roots to older leaves and roots to ag leaves were higher in CM104 than in ZM18. The TFs of roots to older leaves and roots to ag leaves were similar in YM51, YM53, SM969, and ZM18. For roots to grain, the TFs were signi cantly lower in YM51 and CM104 than in ZM18. The Cd concentration in grain was signi cantly positively correlated with the TFs of roots to grain. The Cd concentration in grain was negatively correlated with the TFs of roots to ag leaves, roots to older leaves, and roots to lower stems, but the correlation coe cients were not signi cant (Table 4). To analyze Cd redistribution from shoot parts to grain, we calculated RF values ( Table 3). The RFs from lower stems and older leaves to grain were signi cantly lower in YM51, YM53, SM969, and CM104 than in ZM18. For glumes to grain and ag leaves to grain, the RFs were signi cantly lower in YM51 and CM104 than in ZM18; but were not signi cantly lower in YM53 and SM969 than in ZM18. The RFs from internode 1 to grain and rachis 1 to grain did not differ signi cantly among the ve cultivars. Correlation analyses showed that the Cd concentration in grain was signi cantly positively correlated with the RFs of all shoot parts to grain. Among them, the highest correlation coe cient was for glumes to grain, and the lowest correlation coe cient was for rachis to grain (Table 4).

Cd concentrations in tissues, and TFs and RFs in wheat plants under high-Cd stress in the pot experiment
Compared with low-Cd stress, high-Cd stress caused various changes in Cd accumulation, translocation, and redistribution. The Cd concentrations in the roots and shoots of YM53 were the highest at the seedling stage. The Cd concentrations in roots were signi cantly lower in ZM18 and CM104 than in YM51 and SM969. The Cd concentration in shoots was signi cantly lower in CM104 than in YM51, YM53, and ZM18 ( Table 1). The TFs of YM51, YM53, SM969, and CM104 were similar, but were much lower than the TF of ZM18 (Table 1).
At the mature stage, the highest Cd concentrations in grain were in YM53, SM969, and ZM18, and were much higher than those in YM51 and CM104 (Fig. 3A). Thus, ZM18 was selected as the high-Cd accumulator to analyze responses to high-Cd stress. Similar results were observed in the roots and rachis ( Fig. 3B and 3C). For lower stems and older leaves, the Cd concentration in ZM18 was signi cantly lower than that in SM969, but much higher than that in YM51, YM53, and CM104 ( Fig. 3D and 3E). Similar results were detected for ag leaves and internode 1, except in YM53, which had Cd concentrations similar to those in ZM18 ( Fig. 3F and  3G). The Cd concentration in glumes was similar in YM53 and ZM18, and higher in those two cultivars than in YM51, SM969, and CM104 (Fig. 3H). Correlation analyses indicated that the Cd concentration in grain was signi cantly positively correlated with the Cd concentration in each tissue (Table 4).
There was no difference in the TFs of roots to total shoots, roots to lower stems, roots to internode 1, roots to ag leaves, roots to glumes, and roots to grain among the ve cultivars ( Table 2). For roots to rachis, the TFs of YM51, YM53, SM969, and CM104 were signi cantly lower than that of ZM18. The TFs of roots to older leaves were signi cantly lower in YM51 and YM53 than in ZM18. The Cd concentration in grain was signi cantly positively correlated with the TFs of roots to internode 1, roots to ag leaves, roots to rachis, and roots to grain ( Table 4).
The RF of rachis to grain did not differ signi cantly among the ve cultivars ( Table 3). The RF of glumes to grain was signi cantly higher in SM969 than in ZM18; and vice versa for the RFs of internode 1 to grain and ag leaves to grain. The RFs of glumes to grain, internode 1 to grain, and ag leaves to grain were similar among YM51, YM53, CM104, and ZM18. For lower stems to grain and older leaves to grain, the RFs of ZM18 were signi cantly lower than those of YM53 and YM51 (except the RF of lower stems to grain in YM51), but higher than those of SM969 and CM104. The grain Cd concentration was not correlated with any of the RFs (Table 4).

Discussion
Cd concentration in grain differs among different genotypes of common wheat In this study, we found that the grain Cd concentrations varied among the 46 wheat cultivars grown in Wenjiang and Shifang, and the Cd concentrations were positively correlated between the two sites ( Fig. 1). Similar results have also been reported for Japanese wheat cultivars (Kubo et al., 2008) and American winter wheat cultivars (Guttieri et al., 2015). These results indicate that the Cd concentration in grain differs among genotypes, and is controlled by genetic factors. Twelve cultivars accumulated similar grain Cd concentrations in Wenjiang and Shifang; of them, 10 cultivars accumulated Cd in the grain to concentrations of less than 0.15 µg/g (Fig. 1). Thus, low-Cd accumulating lines suitable for cultivation in multiple environments could be bred by genetic improvement. Of the 46 cultivars, 31 had signi cantly higher grain Cd concentrations in Wenjiang than in Shifang, which might because of the higher Cd concentration in soil of Wenjiang than Shifang (STable 3). These result indicates that the grain Cd accumulation is also affected by environmental conditions (Kubo et (Table 1), the grain Cd concentration was not correlated with the Cd concentrations in roots and shoots, or with the TF from root to shoot (STable 2). These different ndings may result from the different genetic background of wheat.
A study on durum wheat found that genetic variation in Cd translocation from roots to shoots accounted for 80-90% of phenotypic variation in grain Cd accumulation, and that this is controlled by a single locus (Cdu1) In this study, the grain Cd concentration was not signi cantly correlated with the TFs of roots to glumes, roots to older leaves, roots to ag leaves, roots to lower stems, roots to internode 1, or roots to rachis (Table 4). Thus, grain Cd accumulation in these cultivars did not result from Cd translocation from roots to shoot parts (Shi et al., 2015). However, the grain Cd concentration was correlated with the Cd concentrations in the glumes and rachis (Table 4), the TF of roots to grain (Table 4), and all the RFs (Table 4) at the mature stage under low-Cd stress. These results clearly indicate that in these cultivars of common wheat, grain Cd accumulation resulted from the direct Cd transport from roots to grain and the redistribution of Cd from shoot parts to grain.
The Cd concentrations in roots were similar among the ve cultivars (Fig. 2B), and there was no signi cant correlation between root Cd concentration and grain Cd concentration (Table 4). Thus, in these cultivars, the Cd in grain resulted from direct Cd transport from roots to grain and was not affected by Cd accumulation in the roots, which supports the results of Kubo et al. (2011) and Liang et al. (2017). Although the TF of roots to grain in ZM18 was signi cantly higher than those in YM51 and CM104, it was not signi cantly different from those in YM53 and SM969 (Table 2). Thus, compared with the high-Cd accumulator ZM18, the low level of direct Cd transport from roots to grain contributed to the low grain Cd concentrations in YM51 and CM104; however for YM53, SM969, the direct Cd transport from roots to grain had a small effect on grain Cd concentration, but not a large effect as reported by Kubo et al. (2016).
In rice, half of the Cd in grain is derived from Cd redistribution from shoots to grain (Rodda et al., 2011), and there are differences in Cd redistribution between high-and low-Cd accumulating genotypes (Liu et al., 2007).
In previous of ve wheat cultivars, the Cd remobilized from leaves and stems to grain contributed to Cd accumulation in the grain (Harris and Taylor, 2001;Greger and Löfstedt, 2004;Chan and Hale, 2004;Kubo et al., 2016). Our results indicated that differences in Cd redistribution from all shoot parts to grain resulted in differences in grain Cd concentrations among cultivars. ZM18, a high-Cd accumulating cultivar, had the highest RFs of all shoot parts to grain (except for rachis to grain) ( Table 3), indicating that the high grain Cd concentration resulted from high Cd redistribution from shoots to grain. Compared with ZM18, YM53 and SM969 had lower RFs for lower stems to grain and older leaves to grain (Table 3). These results indicate that Cd was retained in the lower stems and older leaves in YM53 and SM969, ultimately resulting in their low grain Cd concentrations. The ve cultivars showed differences in the contribution of Cd remobilized from stems to grain (Shi et al., 2019). However, the Cd concentrations in older leaves and lower stems were similar among YM53, SM969, and ZM18 ( Fig. 2C and 2D), suggesting that these three cultivars had similar capacities for Cd sequestration in these parts. For YM51 and CM104, the RFs of glumes to grain, ag leaves to grain, lower stems to grain and older leaves to grain were signi cantly lower than those of ZM18 ( Table 3), suggesting that the low grain Cd concentrations in these cultivars were resulted from retention of Cd in the glumes, ag leaves, lower stems, and older leaves. Thus, Cd retention by these four tissues could explain the differences in grain Cd concentrations between ZM18, YM51, and CM104. The highest Cd concentration in older leaves was detected in YM51 and CM104 (Fig. 2D); while the highest Cd concentration in ag leaves was detected in CM104 (Fig. 2E). Cd concentration in each tissue, and Cd translocation from roots to above-ground parts determine grain Cd accumulation under high-Cd stress The uptake and translocation of Cd by plants are dependent on the Cd concentration in soil. Under high-Cd stress, ZM18, YM53, and SM969 accumulated signi cantly higher Cd concentration in grain than that of YM51 and CM104 (Fig. 3A). The Cd concentrations in all tissues except for older leaves were higher in YM53, SM969, and ZM18 than in YM51 and CM104 (Fig. 3). These results indicate that high-Cd stress changed the accumulation and the partitioning of Cd in the ve cultivars.
In a previous study, which the wheat plants treated with 13.70 mg/kg Cd (a much higher dose than that used in our study, the wheat grain Cd concentration was found to be positively correlated with the root Cd concentration, and Cd redistribution from shoots to grain (Shi et al., 2015). In our study, correlation analyses indicated that the grain Cd concentration was positively correlated with the Cd concentration in each tissue (Table 4), and with the TFs of roots to grain, ag leaves, internode 1 and rachis (Table 4), but not with the RFs (Table 4). Thus, the Cd concentration in each tissue, and the Cd translocation from roots to grain, roots to ag leaves, roots to internode 1, and roots to rachis determined the grain Cd accumulation under high-Cd stress.
In rice and soybean, the Cd concentration in grain/seeds was found to be negatively correlated with the Cd concentration in roots, but positively correlated with the Cd concentration in shoots, and Cd retention in roots limited Cd translocation to shoots (Ueno et al., 2010;Wang et al., 2018). The Cd concentrations in roots and shoot parts are mainly determined by the Cd uptake and retention in roots, and the ability of Cd translocation from roots to the shoots. In our study, we found that the TFs did not differ signi cantly among these ve cultivars (except for the TFs of roots to older leaves and roots to rachis) ( Table 2), indicating that the abilities of roots to retain Cd and to translocate Cd to the shoots were similar among the ve cultivars. Thus, the higher Cd concentrations in all tissues (except for grain) of YM53, SM969 and ZM18 indicated that the Cd uptake abilities of YM53, SM969, and ZM18 were signi cantly higher than those of YM51 and CM104, resulting in their different grain Cd concentrations.
In cereals, the rachis serves as a switch for Cd transport from internode 1 to grain (Shi et al., 2015). The ag leaf connects with internode 1 and the rachis via the uppermost node. The Cd loaded from the xylem to the nodes can be transferred to the phloem. The accumulation of Cd in leaves and grain is dependent on phloem transport (Chen et al., 2007;Kobayashi et al., 2013;Kubo et al., 2016). In this study, the Cd translocation from roots to grain, roots to ag leaves, roots to internode 1, and roots to rachis determined the grain Cd accumulation, but could not explain differences in grain Cd concentrations among cultivars under high-Cd stress because their TFs were similar ( Table 2). In addition, Cd redistribution from these tissues to grain was not correlated with the grain Cd concentration (Table 4). Thus, in these ve wheat cultivars, the Cd taken up by roots was synchronously transported to new shoots, and the amount taken up was determined by the Cduptake ability of the roots.

Conclusions
The results of this study were showed as Fig. 4.
(1) Under low-Cd stress, the grains Cd accumulation in common wheat was strongly affected by the direct transport of Cd from roots to grains, and the redistribution of Cd from shoots to grains. In the ve cultivars, compared with the high-Cd accumulator ZM18, the four low-Cd accumulators possessed at least two pathways to decrease the grains Cd concentration (Fig. 4A). The rst way was to reduce the directly transport of Cd from roots to grains, and the redistribution of Cd from lower stems, older leaves, ag leaves and rachis to grains. The second way was to decrease the Cd redistribution from lower stems and older leaves to grains (Fig. 4A). Therefore, it seemed that the redistribution of Cd from lower stems and older leaves to grains had larger effect on varietal differences in grain Cd accumulation among these cultivars than the direct transport of Cd from roots to grains and the redistribution of Cd from ag leaves and rachis to grains.
(2) High-Cd stress changed the pathway of Cd accumulation in grains when compared with low Cd stress. Although the grain Cd accumulation in common wheat under high-Cd stress was affected by the Cd accumulation in each tissue and the Cd translocation from roots to new shoot tissues (including grains, rachis, internode 1 and ag leaves), it seemed that the different Cd accumulation in grains of these ve cultivars practically came from the variant ability of Cd uptake. Thus, the higher Cd uptake by roots in YM53, SM969 and ZM18 led to the higher Cd accumulation in grains than YM51 and CM104 (Fig. 4B).
(3) For the ve wheat cultivars, it is interesting that although the low/high Cd stress in soil changed the pathway of grains Cd accumulation, YM51 and CM104 showed the similar pathway in low-Cd stress, and the