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Environmental Earth Sciences

, Volume 71, Issue 1, pp 277–286 | Cite as

Variation of cadmium uptake, translocation among rice lines and detecting for potential cadmium-safe cultivars

  • Zhang Hongjiang
  • Zhang Xizhou
  • Li Tingxuan
  • Huang Fu
Original Article

Abstract

Cadmium (Cd) pollution highly threats to rice consumption for humans. This study aims to investigate the variation of Cd uptake and translocation among rice lines and to screen cadmium-safe cultivars (CSCs). Total of 146 rice lines were grown in artificially Cd pollution hydroponics within 30 day followed by a pot culture in which 17 rice lines were planted and treated with different Cd levels until maturity. The results showed that Cd tolerance and Cd accumulation significantly (p < 0.05) varied among 146 rice lines in the hydroponics experiment as well as among the 17 rice lines in the followed pot culture. Cd contents of brown rice significantly correlated with Cd accumulations in plant and their translocation from vegetative organs to edible parts, implying that extremely attention should paid to Cd translocation and its influence factors for CSCs selection. IRBN95-90 and D26B of maintainer lines and Lu5278-I332, Lu17-T21712, Lu17-I2R60 of restorer lines were detected to be potential CSCs under 2 and 10 mg kg−1 Cd level, which confirmed the feasibility of selection of CSCs from rice lines. Therefore, the study confirmed the variations of Cd uptake and translocation among rice lines and a combinatorial and recursive selection process is feasible and affordable to screen CSCs to reduce Cd risk for rice consumption.

Keywords

Cadmium-safe cultivar (CSC) Rice line Genetic variation Cadmium (Cd) 

Introduction

Pollution with heavy metals has become a critical problem worldwide as a result of mining, disposal of industrial waste, application of fertilizers and metal contaminated sewages (Gupat and Gupta 1998; Liang et al. 2005; Sun et al. 2008). As a non-essential trace element, cadmium (Cd) is fully considered as one of the most hazardous heavy metals due to its toxicity (Arasimowicz-Jelonek et al. 2011; Järup and Åkesson 2009; Zhou et al. 2007; Zhou 2003). Throughout the world, the background content of soil Cd is in the range of 0.01–2 mg kg−1 with a median of 0.35 mg kg−1 (Zhao et al. 2009), unfortunately, more than 2.2 × 107 kg Cd was dumped into soil and water per year (Liu et al. 2009a), leading health risks to humans and animals through the soil biology chain. Therefore, reducing Cd pollution has been an urgent issue for environmental and agro-scientists (Liu et al. 2010).

Over the past period of time, soil remediation, such as topsoil replacement and extraneous matter addition was applied to remove Cd from soil or limit its activity (Chehregani et al. 2009), yet, popularization and application was limited by its high costs and the induced secondary damage (Bidar et al. 2007; Zhou and Song 2004). Recently, more concerns have been reversed to phyto remediation and more than 400 hyper accumulators, which accumulate heavy metal ions in their shoots or roots, have been gradually reported to be suitable for growing in different metalliferous soils (Brooks et al. 1998). It is disappointing that low biomass and unsuitability of applications have questioned their importance (Liu et al. 2008; Qadir et al. 2004), therefore, only paying attention to soil bodies is insufficient to ensure Cd-safe food production. Based on the theory that Cd tolerance and accumulation varied among species and among cultivars within species, attention should be paid to the selection of pollution-safe plant species and the technology to restrict Cd transportation from Cd-polluted soil to plants for food safety (Kurz et al. 1999; Wang et al. 2007; Yu et al. 2006).

Stable crops have been main diets of human beings for thousands of years. In the last decades, reports have confirmed the existence of potential low-Cd cultivars in conventional crops, such as rice (Oryza sativa L.) (Kurz et al. 1999; Xu et al. 2009), wheat (Triticum sestivum L.) (Li et al. 2003) and maize (Zea mays L.) (Zhang et al. 2000). As one of the important stable crops, the paddy rice is wildly cultivated and consumed all over the world, especially in East Asia. In some regions of Asia, the paddy rice has been reported to be heavily exposed to Cd (Sun et al. 2010). Recently, rice cultivars with low Cd content in brown rice were identified (Yu et al. 2006; Li et al. 2012), which confirmed the possibility of seeking for low-Cd cultivars. To reduce the risk of Cd contamination for rice consumption, the health risk of heavy metal and method of cultivating Cd-safety crop were measured and maximum allowable Cd content (0.2 mg kg−1) in paddy rice was emerged according to NFHSC (National Food Hygienic Standard of China 2010). Although several low-Cd cultivars or cadmium-safe cultivars (CSCs) of rice have been reported (He et al. 2006; Yu et al. 2006; Xu et al. 2009), there is few reports about the selection of CSCs from rice lines. As basic materials for rice breeding, rice lines transmit genetic information to their hybridized rice cultivars and selection of CSCs of rice lines can be a basic, but efficacious mode to minimize Cd risk for rice consumption.

In this study, the 146 rice lines, including 33 maintainer lines and 113 restorer lines, were tested to identify characteristic of Cd accumulation and tolerance of rice lines and to screen CSCs as referring to NFHSC limit (Cd content ≤0.2 mg kg−1). Furthermore, whether differences in Cd accumulation between maintainer line and restorer line exist and relationship between Cd accumulation in plant and Cd content in brown rice were also to be concerned.

Materials and methods

Experimental design

Experiments were carried out in the experimental areas of Sichuan agricultural university at Ya’an, Sichuan province, China (29°54′E, 103°01′N). Two differential and recursive trials (here after referred to as exp. 1 and exp. 2) were conducted in 2009 (exp. 1) and 2010 (exp. 2) for acquiring CSCs from quantities of Chinese rice lines. In the exp. 1, the artificially Cd pollution hydroponics was conducted to select potential CSCs from a large amount of rice lines. In this experiment, the rice lines treated with 0 and 1 mg L−1 Cd were cultivated 30 days, then growth traits, Cd contents of all the rice line seedlings were detected. Thereafter, the pot culture (exp. 2) was designed in the next year to test the variations of Cd uptake and translocation; more importantly, whether CSCs exist or not was tested as well. In this experiment, the tested rice lines were treated Cd within 0, 2 and 10 mg kg−1, respectively, and the samples of root, stem, leaf, grain and brown rice were collected at the maturity stage. Both of the experiments were conducted in the greenhouse within natural illumination and temperature.

Rice lines preparation and hydroponics culture (exp. 1)

The 146 rice lines (provided by College of agriculture, Sichuan agricultural university) were used as experimental materials to test the variation of Cd tolerance and accumulation among cultivars and to acquire low-Cd rice lines at seedling stage. All seeds were surface-sterilized by submerged in H2O2 (10 %) for 30 min and in 0.1 % NaClO for 10 h, then, rinsed thoroughly with deionized water and germinated in an incubator at 30 °C for 24 h. The germinated seeds were sown broadcast and cultivated in trays filled with quartz sands. During the seedling period, rice plants were paced in the artificial climate box, in which the intensity of illumination, illumination time, temperature and humidity were set to 30,000 lx, 14 h, 28/20 °C and 75 %. When the third leaf emerged, the seedlings of uniform size were transferred to 40 L (80 × 50 × 10 cm) hydroponics containers, which were assorted with plastic plates with 30 smoothly round holes (three holes for each cultivars and two plants were cultivated into one hole). The composition of the basic nutrient solution was the same as the International Rice Research Institute recommended formula (Wang and Gong 2006). After the plants had been cultivated in complete nutrient solution for 1 week, Cd treatments with three replications were arranged consisting (1) 0 (CK, control) and (2) 1 mg L−1 Cd (prepared by dissolving analytical grade CdCl2∙2.5H20). The nutrient solution was continuously renewed every 4 days and pH in the solution was adjusted to 5–5.5 daily using HCl or NaOH. After 30 days of Cd treatments, samples were harvested. The roots were dipped in 0.1 μmol L−1 EDTA for 30 min to remove the heavy metal ions absorbed at the surface of roots, then, all samples were rinsed four times with distilled water, oven-dried at 75 °C for 48 h, finally, all samples were weighed and ground to sieve through a 100 mesh nylon sieve.

Soil culture and Cd treatment (exp. 2)

This experiment was conducted to study Cd accumulation and to determine whether potential CSCs existed among 17 rice lines with low or high Cd accumulation selected from exp. 1. The soil was air-dried, sieved through a 6 mm sieve and 10 kg of the soils were placed into each pot. The pots (30 cm in diameter and 40 cm in height) were mixed thoroughly with three levels of Cd in solution: 0 (CK), 2 and 10 mg kg−1, respectively. All pots were ranged in a completely randomized design and submerged in water (2–3 cm above the soil surface) for a month, in the following, the physicochemical properties of the soil were analyzed (Table 1) and five healthy uniform size seedlings of the tested Chinese rice lines (cultivated according to exp. 1) were transplanted into soil culture pots with three replicates for each treatment on May 31, 2010. Pots received N, P and K fertilizers three times i.e., 2.17 g urea and 4 g potassium hydrogen phosphate when the day Cd added and 1 g urea were applied when the 30th day and the 90th day emerged after transplantation. During the rice growing seasons, about 2–3 cm water was maintained above the soil surface. The samples of root, stem, leaf and grain were harvested at maturity during the period of September 28–October 2, 2010. The grain of each treatment was air-dried, weight and then divided into two equal parts. The chaff of one part was removed with sheller machine (JLGJ-45, Zhengzhou, China) according to the standard of “The Testing Methods of Rice Qualities” issued by China Ministry of Agriculture (NY147-88), hereafter brown rice samples were oven-dried and ground through 100 mesh nylon sieve as well as samples of root, stem, leave and grain.
Table 1

Basic physicochemical property of soil used in exp. 2

 

Soil pH

Org C (g kg−1)

CEC (cmol kg−1)

Total N (g kg−1)

Available P (mg kg−1)

Available K (mg kg−1)

Total Cd (mg kg−1)

CK

6.62

14.0 ± 0.93

11.8 ± 1.39

1.31 ± 0.17

8.63 ± 0.57

69.7 ± 2.72

0.31 ± 0.03

Cd2

      

1.98 ± 0.17

Cd10

      

8.99 ± 0.31

Chemical analysis

Plant samples were digested in a 5:1 (v/v) mixture of HNO3–HClO4 and Cd contents of samples in exp. 1 were determined with FAAS (wavelength 228.8 nm, slit 0.7 nm, AAnalyst 800, Perkin Elmer, USA) and Cd contents of root, stem, leaf, grain and brown rice in exp. 2 were determined with GAAS (wavelength 228.8 nm, slit 0.7 nm, AAnalyst 800, Perkin Elmer, USA) (Zou et al. 2011). Analytical procedure control was synchronously performed fourteen times by measuring the reference materials GBW08503b with Cd content of 0.15 mg kg−1 purchased from the National Center for Certificate Reference Materials, China. The relative standard deviations were 1.56 % in exp. 1 and 0.134 % in exp. 2 and the average recoveries were 106.59 % in exp. 1 and 97.33 % in exp. 2, respectively.

Soil pH, organic matter content, total N, available P, available K in exp. 2 were measured following the method of Bao (2007), total Cd of soil after treatment was determined by GAAS (wavelength 228.8 nm, slit 0.7 nm, AAnalyst 800, Perkin Elmer, USA) following a 5:1:1 (v:v:v) mixture of HNO3–HClO4–HF digestion (Zou et al. 2011).

Statistical analysis

To explore the relative response of rice lines to different Cd level, the formula of “Growth Traits Response to Stress (GRS)” was applied and calculated as follow.
$${\text{GRS (\% ) }} = \, (G_{\text{Cd}} - \, G_{\text{CK}} ) \, / \, G_{\text{CK}} \times { 1}00$$
where G Cd and G CK are the growth traits i.e., root lengths, root-shoot ratios, plant heights and grain yields under Cd exposures and controls, respectively.
To figure out the translocation of Cd, the indicators of “distribution ratio of Cd to aboveground” and “distribution ratio of Cd from aboveground to grain” were calculated. We calculated the distribution of Cd to aboveground and the distribution of Cd from aboveground to grain as follows:
$${\text{Distribution ratio of Cd to aboveground\,(\%) }} = \frac{\text{Cd accumulation aboveground}}{\text{Cd accumulation in total}} \times 100$$
$${\text{Distribution ratio of Cd from aboveground to grain\,(\%) }} = \frac{\text{Cd accumulation in grain}}{\text{Cd accumulation aboveground }} \times 100$$
where Cd accumulation aboveground is the sum of Cd accumulations of stem, leaf and grain, and Cd accumulation in total is the sum of Cd accumulations of root, stem, leaf and grain.

Data were analyzed with statistical software of SPSS 17.0, Origin 8.0 and Excel 2007 for windows. An one-way ANOVA was performed for the various of cultivars, where cultivar and its linked cultivar type (maintainer or restorer line) was considered as a random factor, followed by presenting the results at the 0.05 confidence interval.

Results

Cd tolerance and accumulation of 146 rice lines

Growth response to stress (GRS) can be used to evaluate the tolerance of plant when exposed to heavy metals. GRSs of root shoot ratio, plant height and root length (GRS-SRSs, GRS-PHs, GRS-RLs) were in great variation among 146 rice lines as well as GRSs of dry weight (GRS-DWs), however, such situation was not detected between maintainer line and restorer line, i.e., the response characteristic of all tested growth traits of restorer lines were in consistent with those of maintainer lines (Table 2). This suggested that the tolerance of rice lines to Cd stress should be cultivar dependent.
Table 2

Growth responses to Cd stress (GRS %) of 146 rice lines in exp.1

Traits

GRS-RSR

GRS-PH

GRS-RL

GRS-DW

ML

RL

ML

RL

ML

RL

ML

RL

Minimum

12.8

8.4

−43.4

−52.4

−38.8

−48.4

−61.7

−67.1

Maximum

85.9

98.1

−15.1

−17.7

57.3

71

27.7

35.6

Average

46.4

47.5

−29.5

−38.7

4.6

4.1

−24.6

−39.5

Standard deviation

26.7

4

10.1

9.9

29.5

29.7

26.6

24.4

Coefficient of variation

57.4

49.2

34.2

25.5

640.2

610.2

108.5

61.7

F value

2.28**

3.04**

2.32**

2.69**

8.40**

7.84**

2.28**

1.78**

GRS-RSR, GRS-PH, GRS-RL and GRS-DW symbolize the responses of growth traits i.e., RSR root-shoot ratio, PH plant height, RL root length and DW plant dry weight to Cd stress

ML and RL indicate rice maintainer lines (n = 33) and restorer lines (n = 113), respectively.* and ** means significant difference at 0.05 and 0.01 level by using LSD test, respectively

Under 1 mg L−1 of Cd exposure, Cd contents in plant of 146 rice lines were in the range of 44.43–124.02 mg kg−1 and averaged 71.07 mg kg−1, Cd accumulation ranged from 12.02 to 59.86 μg plant−1 and averaged 26.82 μg plant−1. Even though restorer line and maintainer line are in different function for rice breeding, the ability of Cd absorption was somewhat in the same level (Fig. 1). That is to say, it is possible for selecting potential rice CSCs from the tested materials.
Fig. 1

Cd content (a) and Cd accumulation (b) in plants of 146 rice lines exposed to 1 mg L−1 Cd

Based on the concept of CSCs, 14 rice lines (including six maintainer lines and eight restorer lines) were selected as potential CSCs using cluster analysis (by taking the growth responses to Cd stress of all tested traits (GRS-SRSs, GRS-PHs, GRS-RLs and GRS-DWs) and Cd contents in plant as standard factors). Especially, three of high Cd accumulation rice materials were observed, whose Cd contents were almost twofold higher than average Cd contents of those 14 rice lines.

Cd distribution in plants of the 17 tested rice lines

Cd content and Cd accumulation in different organs i.e., roots, stems, leaves and grains of the 17 rice lines are in Table 3. On one hand, significant (p < 0.0.5) difference of Cd content and accumulation in each organ was detected among the 17 rice lines under either level of Cd exposure. Especially, the grain Cd contents ranged from 0.03 to 0.49 mg kg−1 under Cd treatments 2 mg kg−1 (Cd2) and from 0.11 to 1.00 mg kg−1 under Cd treatments 10 mg kg−1 (Cd10), while Cd accumulation were 0.26–4.36 μg plant−1 for Cd2 and 0.81–5.53 μg plant−1 for Cd10, respectively. On the other hand, with regard to Cd content and distribution ratio among different organs, large variation were observed both in Cd2 and Cd10, overall, the average ratios of Cd content in root:stem:leaf:grain were 95.2:6:3.6:1 under Cd2 and 180.3:8.2:3.0:1 under Cd10 with the average Cd distribution in root:stem:leaf:grain 42:6.5:3.2:1 for Cd2 and 44:5.8:2:1 for Cd10. However, Cd contents and accumulations in root, stem, leaf and grain of restorer lines were similar with those of maintainer lines.
Table 3

Variations among 17 rice lines on Cd content (mg kg−1) and quantity accumulation (μg plant−1) in different organs of rice plants exposed to Cd at maturity in exp. 2

Cd content

In root

In stem

In leaf

In grain

Cd2

Cd10

Cd2

Cd10

Cd2

Cd10

Cd2

Cd10

Minimum

6.16

107.66

0.63

2.38

0.32

0.80

0.06

0.11

Maximum

30.41

640.58

1.72

9.34

1.25

2.46

0.49

1.00

Average

16.97

246.93

1.07

3.67

0.64

1.32

0.18

0.45

Standard deviation

6.49

152.89

0.35

1.72

0.29

0.44

0.12

0.30

Coefficient of variation

38.27

61.92

33.15

46.78

45.55

32.99

66.57

66.82

F value

239.5**

262.4**

235.5**

162.5**

129.4**

48.9**

41.4**

284.2**

Cd accumulation

In root

In stem

In leaf

In grain

Cd2

Cd10

Cd2

Cd10

Cd2

Cd10

Cd2

Cd10

Minimum

13.50

63.47

1.27

6.07

0.50

2.30

0.26

0.81

Maximum

42.47

188.93

13.91

49.11

6.85

14.23

4.36

7.57

Average

25.90

127.50

4.61

18.11

2.20

5.68

1.38

3.12

Standard deviation

8.70

40.87

3.22

11.61

1.56

3.21

1.02

2.01

Coefficient of variation

33.58

32.05

69.77

64.09

71.02

56.42

73.72

64.39

F value

15.0**

9.5**

63.0**

35.6**

91.7**

57.7**

29.9**

34.7**

** Means significant difference at 0.05 and 0.01 level by using LSD test, respectively

Yields and Cd accumulations of brown rice

Either under Cd stress or not, brown rice yields were highly variable among the tested 17 Chinese rice lines (Table 4), which seemed to imply that the effects of Cd on yield were both genetic and Cd level dependent. Yield response to Cd stress (YRS) was calculated to evaluate Cd tolerance of brown rice yield and variations in YRS were highly significant among cultivars in spite of those between types both under Cd2 and Cd10 (Table 4). Meanwhile, average YRSs in maintainer line and restorer line were similarly below 0 either under Cd2 or Cd10. That is to say, Cd decreased brown rice yields differently among cultivars, but similarly between types.
Table 4

The brown rice yields (g plant−1) and yield response to Cd stress (YRS,  %) of 17 rice cultivars in exp.2

Type

Cultivars

Brown rice yield

YRS

CK

Cd2

Cd10

Cd2

Cd10

ML

DiguB

17.4bc

17.0bc

16.3ab

−2.46

−3.84

Zhong9B

13.7def

15.3cd

15.1 cd

11.16

−1.03

IRBN95-90

20.8a

20.2a

19.3a

−2.72

−4.80

Wujin4B

9.9 g

11.8e

11.3ef

19.78

−4.48

D26B

12.6ef

12.4de

12.8de

−1.67

3.70

Xiang2B

13.2ef

11.8e

11.4ef

−10.48

−3.67

Mian5B

19.4ab

17.8ab

13.8 cd

−8.37

−22.64

KangfengB

20.1ab

18.3ab

16.2abc

−9.06

−11.09

RL

Lu5278-I332

12.4f

12.9de

14.0 cd

4.20

8.26

Lu17-T2171

12.4f

12.1e

10.2f

−2.66

−15.88

Lu17-T21712

16.9bc

16.5bc

18.8ab

−2.04

13.63

Lu17-IR199

16.7bc

17.3ab

17.6ab

3.70

1.69

Luhui602

16.6bc

16.1bc

15.6bc

−3.03

−3.14

Lu5274-I332

19.6ab

17.6ab

12.9de

−10.11

−26.74

Lu17-I2R60

15.3 cd

13.8de

11.2ef

−9.83

−18.89

Luhui17

15.2de

13.8de

12.6de

−9.20

−8.55

R527-M63

14.2def

14.5 cd

15.5bc

1.99

7.35

The same letters of each column indicate no significant difference at 0.05 level by using LSD test. YRS2 and YRS10 symbolize the brown rice yield response to 2 and 10 mg kg−1 Cd stress, respectively

Brown rice Cd contents were significant different (p < 0.01) among the tested 17 Chinese rice lines under Cd treatments (Cd2 and Cd10). Cd contents were 0.028–0.486 mg kg−1 (average of 0.164 mg kg−1) for Cd2 and 0.073–0.962 mg kg−1 (average of 0.427 mg kg−1) for Cd10 (Fig. 2). Cd contents in brown rice of the eleven Chinese rice lines (including five maintainer lines and six restorer lines) were below the safe limits according to the NFHSC standard in a low Cd contaminated soil, remarkably, some of the tested Chinese rice lines (IRBN95-90, D26B of maintainer lines and Lu5278-I332, Lu17-T21712 and Lu17-I2R60 of restorer lines) produced safe brown rice for rice consumption even when soil Cd contamination approached 10 mg kg−1 (Fig. 2). In addition, brown rice Cd content was detected to be little difference between maintainer and restorer lines. The results indicated that variation of Cd content in brown rice was cultivar and Cd contamination level dependent, while not submit to rice line types.
Fig. 2

Cd content of brown rice in 17 Chinese rice lines under Cd exposure of 2 mg kg−1 (a) and 10 mg kg−1(b), NFHSC shorted for National Food Hygienic Standard of China (GB/T 4789-2010)

Relationship between brown rice Cd content and plant Cd accumulation and distribution

Cd contents in brown rice showed positive and significant correlation with Cd total accumulation in rice plant in exp. 1 (p < 0.01), Cd total accumulation in whole plants (p < 0.01) and Cd distribution ratios to aboveground parts in exp. 2 (p < 0.01) (Figs. 3 and 4). Meanwhile, Cd accumulation in plant in exp. 1 and in exp. 2 were in a positive and significant relationship (p < 0.01) (Fig. 3), which symbolized that the results in exp. 2 were excellently consistent with those in exp. 1. In contrast, the brown rice Cd content correlated significantly, but negatively with Cd distribution proportion of grain in shoot (p < 0.05) (Fig. 5). These demonstrated whether Cd level in edible part exceed safety standard not only subject to Cd accumulation ability but also to Cd transport capacity of plant.
Fig. 3

Relationship among brown rice Cd contents (mg kg−1), Cd accumulation (μg plant−1) in plants in exp. 1 and Cd accumulation in plants in exp. 2 under Cd exposure of 2 mg kg−1 (a) and 10 mg kg−1 (b) (n = 17). Cd accumulation in plant in exp. 1, Cd accumulation in plant in exp. 1 and Cd content in brown rice, were marked as x, y and z, respectively. The r(z, x), r(z, y) and r(x, y) represent the correlation coefficients

Fig. 4

Relationship between brown rice Cd contents (mg kg−1) and distribution of Cd to aboveground (%) under Cd exposure of 2 mg kg−1 (a) and 10 mg kg−1 (b) (n = 17)

Fig. 5

Relationship between brown rice Cd contents (mg kg−1) and distribution of Cd from aboveground to grain (%) under Cd exposure of 2 mg kg−1 (a) and 10 mg kg−1 (b) (n = 17)

Discussion

Cd is one of the most toxic metallic pollutants, and it enters bodies of plant and animal through the soil–plant–animal system. Cd affects photosynthesis and antioxidant enzymes, resulting in growth inhibition and reduction in food production. Liu et al. (2007a) found that plant dry matters and grain yields of six rice cultivars were in great variation under 100 mg kg−1 soil Cd stress. Yu et al. (2006) also figured out that brown rice yields of 43 rice cultivars varied significantly (threefold in most) either under low Cd level or high Cd level. The results in the present hydroponics experiment showed that biomasses of rice lines exposed to 1 mg L−1 Cd were reduced. When respecting the Cd toxicity, significant variation was found among the 146 rice lines (Table 2), which, to a certain extent, suggested that variation of Cd tolerance was due to genotype. Meanwhile, when respecting the yields among rice lines, significant difference was detected both under CK and Cd treatments, when compared with CK, yields of brown rice were averagely and slightly reduced under Cd treatments (Table 4), such phenomenon has been previously observed in paddy rice (Yu et al. 2006; Wu et al. 1999). This phenomenon indicated that the influence of Cd on rice lines was existed but differing in cultivars.

It is publicized that Cd accumulation varied greatly among species and cultivars within a species (Kurz et al. 1999; Liu et al. 2007b). In Japan, Arao and Ae (2003) figured out that large difference in Cd content was explored among 49 cultivars of rice grown in containers. Although in China, paddy rice has been reported to be greatly variable in Cd uptake and transport as well as Cd tolerance among cultivars and between types (i.g., normal type and hybrid) (Yu et al. 2006; Xu et al. 2009; Liu et al. 2003a, b, 2005; Wu et al. 1999). In the present study, visible variation was observed among 146 rice lines both in Cd tolerance and Cd accumulation (Fig. 1), while Cd contents in root, stem and leaf of the 17 rice lines in exp. 2 were significant different, which was consistent with the results of exp. 1 (Table 2). However, Cd accumulation between maintainer line and restorer line was not significant different, that is to say, although the usage of maintainer line and restorer line is different, their genetic characteristics of anti-cadmium in relatively independent and consistent. This phenomenon confirmed the repeatability of Cd accumulation of rice plant and suggested that selection of CSCs from either maintainer lines or restorer lines could be feasible.

Partial distribution of Cd in plants has been reported to be derived by the translocation of Cd from shoot to grain (Arao and Ishikawa 2006). Former reporter accounted that Cd content of edible part was governed by the translocation of Cd from vegetative to generative parts of plant (Morghan 1993) and Cd content in brown rice were significantly correlated with Cd accumulation in rice plant and Cd distribution ratio to aboveground parts (Liu et al. 2007b). Presently, brown rice Cd content correlated significantly (p < 0.01) with total Cd accumulation in plant, Cd distribution ration aboveground and Cd distribution ratio from aboveground to grain (Figs. 3, 4 and 5). It demonstrated that Cd content in generative parts were somehow (maybe genetic) governed by Cd absorption ability and its translocation. Therefore, we should not only focus on Cd accumulation at vegetative stage, but also on Cd translocation for evaluating crop response to Cd and selecting CSCs.

With regard to CSCs selection, NFHSC, in which the maximum permissible Cd content is 0.2 mg kg−1, was frequently applied to be the standard for measuring the safety of rice consumption. Under this standard, paddy rice cultivars produced safe grain or brown rice were selected from the tested rice cultivars in the soil culture experiments, where pots were exposed to Cd at a low level under waterlogging condition (Xu et al. 2009; Yu et al. 2006). On the contrary, no CSC was found under a high level of Cd exposure. Therefore, Yu et al. (2006) pointed that CSCs-selection was highly attached to the level of soil Cd. In this study, eleven rice lines were safe for human feeding under the low level soil Cd treatment (2 mg kg−1), when soil Cd approached to 10 mg kg−1, there were still five rice lines whose Cd content were below 0.2 mg kg−1 in brown rice (Fig. 2). Therefore, two conclusions can be summed up based on our experiments. First, CSCs selection was somewhat both genetic regulated and pollution level dependent. On one hand, although Cd level differed fivefold, five rice lines could be identified as potential CSCs both under low soil Cd level and the higher soil Cd level, which confirmed the genotype advantage to minimize Cd accumulation. On the other hand, Brown rice Cd content of 6 cultivars, which produced safe brown rice for food consumption under Cd treatment Cd2, exceeded 0.2 mg kg−1 under Cd treatment Cd10. Second, slightly variation of Cd content between maintainer line and restorer line was observed in edible parts. The variation of Cd content in rice plant was repeatable and extremely consistent between the recursive two experiment (exp. 1 and 2), which symbolized the consistency of Cd uptake and transportation between rice line types.

Cd accumulation in plant is convinced to be governed by genes and environment influence (Nwugo and Huerta 2008). Increasing Cd content in environment enhances security risks of human feeding. Khan et al. (2008) reported that Cd contents of food crops grown in soil irrigated with wastewater were much higher those in the uncontaminated soil. Feng et al. (2011) studied on the relationship between crop (paddy rice) Cd content and traffic-related contamination in Eastern China and significant correlation was found. He also pointed that heavy metal contents in rice plants were different caused by the distance from rice planted to the road edge. The results in our study showed that Cd contents differed in Cd levels. When Cd was 2 mg kg−1 soil, almost 65 % of the tested rice lines produced safe brown rice for human feeding (Cd contents were below 0.2 mg kg−1), when Cd added to fivefold of the low Cd level, Cd contents of all of the rice lines increased (Fig. 2). Meanwhile, Cd uptake and translocation were also genetic governed and its affection may be higher than environment influence. Liu et al. (2009b) reported that a dose of 0.25 and 0.5 mg L−1 directly leaded to expression of DNA MMR genes in the Arabidopsis seedling, suggesting its function of genetic control. Similarly, QTLs analysis directed by Chen et al. (2009) suggested that Cd contents in brown rice were connected with 2 QTLs, which are both located on the eleventh chromosome. He also pointed out that Cd content in brown rice was a relative independent, but genetic governed trait. Therefore, breeding CSCs can be a widespread approach to reduce Cd risk for food consumption. Yu et al. (2006) pointed that pollution-safe rice cultivars could be found from a large amount of rice cultivars. Liu et al. (2007b) figure out that brown rice Cd content was not only subject to Cd uptake but also translocation. In our study, the Cd ions in brown rice content came from root absorption and the translocation from other parts, which was similar with theirs. Thus, the selection of CSCs of rice lines could be an effective method to breeding cadmium-safe rice cultivars.

Concept of cultivar selection provides an option for farmer to minimize Cd risk in the human food chain. As basic materials for rice breeding, rice lines carrying the low-Cd trait must be embedded the acceptable characteristics for yield, quality, farming-suitability and pest and disease resistance. Therefore, constraints in breeding and developing applicable and acceptable CSCs for breeders are still on the horizon. Consequently, as long as the Cd risk exists, selection and application of CSCs is in large and serious demand (i.g., stabilities of low-Cd traits after hybridization and qualities and yields of CSCs) and environmental effects (i.g., management practices, role of radial oxygen loss (ROL) in the regulation of anti-cadmium) are eager to be exposed in further studies.

Conclusion

The present work demonstrates that Cd uptake and translocation are significant variation among rice lines. With the conception of CSCs, Cd uptake as well as Cd translocation should be concerned. Under the controlled condition, IRBN95-90, D26B (maintainer line) and Lu5278-I332, Lu17-T21712 and Lu17-I2R60 (restorer line) were verified as potential CSCs. It exhibited that Cd accumulation is consistent between maintainer line and restorer line and a combinatorial and recursive selection process is feasible and affordable to screen CSCs. Furthermore, to reduce Cd risk, the application of CSCs and appropriate farming management are both important because of its genetic and environment dependent.

Notes

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (No. 30230250), Keystone Program from the Office of Education in Sichuan Province (No. 2006A008) and the State Key Laboratory of Soil and Sustainable Agriculture (No. 055124).

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Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Zhang Hongjiang
    • 1
  • Zhang Xizhou
    • 1
  • Li Tingxuan
    • 1
  • Huang Fu
    • 2
  1. 1.College of Resource and Environmental ScienceSichuan Agricultural UniversitySichuanPeople’s Republic of China
  2. 2.Rice Research InstituteSichuan Agricultural UniversitySichuanPeople’s Republic of China

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