Intercropping different varieties of radish can increase cadmium accumulation in radish
Abstract
Genetic diversity has supplied effective ways to improve crop yields and disease resistance. Therefore, crop uptake of heavy metals may be reduced by collecting germplasm resources. In the present study, cadmium accumulation and nutrients in radish were investigated by intercropping 3 genotypes (red, green, and white radish) in different combinations. Both pot and field experiments showed that cadmium content in radish was increased by intercropping 2 or 3 genotypes, except when white radish was intercropped with green radish. The biomass of red radish was improved by a mixture of all 3 genotypes, green radish biomass was improved by intercropping with the other 2 varieties, and white radish biomass was improved by intercropping with red radish in both pot and field experiments. The pot experiment indicated that the soil exchangeable cadmium concentration of red radish grown with green radish was lower than that of monoculture, whereas red radish intercropped with white radish was between the respective monocultures; the soil exchangeable cadmium concentrations of green radish grown with white radish and with all 3 genotypes grown together were greater than those of the monocultures. Some intercropping modes also improved potassium and phosphorus contents in the edible parts of radish in the pot experiment. Environ Toxicol Chem 2014; 33:1950–1955. © 2014 SETAC
INTRODUCTION
The radish (Raphanus sativus L.) is one of the most important vegetables in the world. Its many varieties can have green, white, or red skins 1. However, seed germination and plant growth are restrained in radishes under cadmium stress 2. Under these conditions, leaf area, chlorophyll and carotenoid contents, and biomass of the radish are decreased, while the activities of antioxidant enzymes increase 3. The stems of radish seedlings have more cell layers in the cambial region when exposed to cadmium because of closure of leaf stomata and cell wall thickening 4. Above 500 mg/kg cadmium in the soil, radish seedlings cannot survive 5.
The levels of cadmium accumulation in different varieties of radish differ significantly. For example, some varieties amass more than the Chinese allowable limit in root vegetables to be protective of human health (0.1 mg/kg fresh wt), while others remain within the permitted range 6. The cadmium content in shoots of radish seedlings is generally greater than in roots 6, 7, but recent studies have found the opposite 3, perhaps because of genotypic differences in the varieties. In addition, as cadmium soil concentration increases, micronutrient absorption is decreased 3. Therefore, increasing the nutrient uptake of radishes is important in remedying cadmium contamination in radish planting areas.
Intercropping is a method of agricultural planting that not only reduces the occurrence of disease and enhances plant productivity by promoting the efficiency of light, water, and fertilizer use 8, 9 but also improves the soil environment, for example, by enhancing soil enzyme activity and nutrient absorption in plants 10-12. In the intercropping system, when the roots of 2 plants contact each other, the phenomenon of “rhizosphere talk” may occur to promote or inhibit plant growth 13. Under heavy metal stress, intercropping influences the accumulation of heavy metals in plants via root secretions such as organic acids, which chelate heavy metals 14, 15 and reduce the biological effectiveness and absorption of the heavy metal in plants 16, 17. Recent studies have reported that hyperaccumulators intercropped with ordinary plants can reduce heavy metal accumulation in the latter and enhance heavy metal uptake in the former at the same time 18-20. Other studies have demonstrated that legumes can increase cadmium accumulation in other intercropped species 21, 22, while growing maize and soybean together reduced the accumulation of zinc and chromium in both crops 23. Thus, the impact of intercropping varies by crop combination and metal and needs to be examined on a case-by-case basis.
There are no reports about the effects of intercropping on radish cadmium accumulation. In the present study, we intercropped 3 radish genotypes (red, green, and white) in both pot and field experiments, and cadmium accumulation and nutrient absorption in each genotype were determined to provide a reference for radish production safety.
MATERIALS AND METHODS
Experimental design
The pot experiment
The pot experiment was conducted at Ya'an campus of Sichuan Agricultural University Farm. The inceptisols soil (purple soil in the Genetic Soil Classification of China) samples came from the farmland of Sichuan Agricultural University Farm. The basic properties of the soil were as follows: pH 7.02, organic matter 41.38 g/kg, total nitrogen 3.05 g/kg, total phosphorus 0.31 g/kg, total potassium 15.22 g/kg, alkali solution nitrogen 165.30 mg/kg, available phosphorus 5.87 mg/kg, and available potassium 187.03 mg/kg. The concentration of total cadmium in soil was 0.101 mg/kg and that of available cadmium was 0.021 mg/kg. The basic soil properties and heavy metal concentrations were determined according to Liu 24.
The soil samples were air-dried and passed through a 5-mm sieve, and then 3.0 kg of the air-dried soil was weighed into individual polyethylene pots (21 cm high, 20 cm in diameter). Cadmium was added to the soils as CdCl2 × 2.5 H2O at 10 mg/kg with a stress concentration according to El-Beltagi et al. 3. The pots were soaked in the cadmium solutions for 4 wk, and then the soil in each pot was mixed thoroughly. Ten seeds of each radish variety were sown directly into the soil for each pot, covered with soil (2 mm), and irrigated in October 2012. When the third euphyllas appeared, all but 3 seedlings were culled in each pot. To ensure that each treatment of 1 variety had the same seedlings for determination, the monoculture of each variety was repeated 3 times (9 pots for 3 varieties); each intercropping of 2 genotypes was replicated 3 times (there were 2 pots as 1 replication: 1 seedling of red radish and 2 seedlings of green radish in 1 pot and 1 seedling of green radish and 2 seedlings of red radish in the other pot). There were 18 pots for red radish with white radish red radish with green radish, and white radish with green radish. Intercropping of all 3 varieties was repeated 3 times (there were 3 pots as 1 replication, 1 seedling of each variety per pot, and 9 pots for 3 replications). The soil moisture content was maintained at 80% of field capacity from soil preparation until harvest. At 60 d after planting (December 2012), all radishes were harvested.
Field experiment
The field experiment was conducted at Ya'an campus of Sichuan Agricultural University Farm. The inceptisols soil (purple soil in the Genetic Soil Classification of China) samples came from the cadmium contamination area of Sichuan Agricultural University Farm. The basic properties of the soil were as follows: pH 6.98, organic matter 35.01 g/kg, total nitrogen 1.19 g/kg, total phosphorus 0.63 g/kg, total potassium 20.64 g/kg, alkali solution nitrogen 80.63 mg/kg, available phosphorus 31.78 mg/kg, and available potassium 115.97 mg/kg. The concentration of total cadmium in soil was 5.39 mg/kg and that of available cadmium was 3.56 mg/kg. Soil properties were determined as above. Each plot was 1.6 m2 (1.6 m × 1 m), and 5 radish seeds were sown directly into each 2-cm-deep hole (made by a cane) and filled with fine soil in November 2012. Each treatment was repeated 3 times (3 plots). There were 21 plots (3 plots for each radish variety monoculture, 9 plots total; 3 plots for each intercropping of 2 varieties, 9 plots total; 3 plots for intercropping of all 3 varieties). Each plot could accomdate 8 rows and 5 columns in a 20 cm × 20 cm grid. In each intercropping of 2 varieties every variety was planted in 4 rows and 5 columns, and 2 varieties were planted in alternate rows. In each intercropping of all 3 varieties, similar to the intercropping of 2 varieties, 3 varieties were planted in alternate rows. When seedlings had 3 euphyllas, they were culled to a density of 25 plants/m2 (in a 20 cm × 20 cm grid), and all radishes were harvested in February 2013 (60 d after planting).
Sample analysis
The roots, tuberous roots, and shoots of radishes in both pot and field experiments were washed with tap water and then with deionized water. Surface water was blotted using absorbent paper, and then the parts were weighed. The fresh roots, tuberous roots, and shoots were processed individually in a blender and kept in clean polyethylene bags for metal analysis. Samples (5.000 g) of pot and field experiments were digested in HNO3/HClO4 (4:1, v/v), then diluted to 50 mL with deionized water. The cadmium concentrations in roots, tuberous roots, and shoots were determined using an iCAP 6300 inductively coupled plasma spectrometer (Thermo Scientific). Samples (5.000 g) of the pot experiment were digested in H2SO4 and H2O2 to determine total phosphorus and total potassium 23. The pot soils were dried naturally and ground into powder of diameter <1 mm to determine pH, exchangeable cadmium, available phosphorus, and available potassium. Soil pH was measured in a 1:2.5 (w/v) suspension of soil and deionized water. The exchangeable cadmium in soil was extracted with 0.005 mol/L DTPA-TEA and analyzed with an iCAP 6300 inductively coupled plasma spectrometer. Soil available phosphorus was extracted by NaHCO3, and available potassium was extracted by NH4OAc for determination 23.
Statistical analyses
Statistical analyses were performed using SPSS 13.0 statistical software (IBM). Data were analyzed by one-way analysis of variance with the least significant difference at the 5% confidence level.
RESULTS
Pot experiment
Cadmium accumulation in radish
The cadmium contents in roots, tuberous roots, leaves, and edible parts of 3 radish genotypes were ranked as follows: white radish > red radish > green radish. The cadmium contents in roots, tuberous roots, leaves, and edible parts of red and green radishes were greater when they were intercropped with 1 or 2 other radish types than when grown in monoculture (p < 0.05; Table 1). The cadmium contents in these parts of white radishes increased when they were intercropped with red radishes (p < 0.05) and decreased when grown with green radishes (p < 0.05) compared with the monoculture. When all 3 varieties were grown together, the cadmium contents in white radishes decreased in roots and tuberous roots (p < 0.05) but increased in leaves and edible parts (p < 0.05) compared with the monoculture.
| Treatments | Cd content in radish (mg/kg fresh wt) | Biomass (g/plant fresh wt) | ||||||
|---|---|---|---|---|---|---|---|---|
| Root | Tuberous root | Leaf | Edible part | Root | Tuberous root | Leaf | Edible part | |
| Red monoculture | 5.02 ± 0.09 b | 0.449 ± 0.003 d | 2.67 ± 0.02 c | 1.36 ± 0.03 d | 1.58 ± 0.02 a | 34.62 ± 1.16 b | 24.03 ± 1.47 b | 58.65 ± 2.63 b |
| Red (inter. green) | 6.71 ± 0.08 a | 0.661 ± 0.009 a | 3.73 ± 0.04 ab | 2.65 ± 0.01 a | 1.60 ± 0.01 a | 16.77 ± 1.13 c | 30.97 ± 1.07 a | 47.74 ± 2.20 c |
| Red (inter. white) | 7.26 ± 0.11 a | 0.566 ± 0.007 b | 4.06 ± 0.04 a | 2.13 ± 0.01 b | 1.40 ± 0.04 b | 31.37 ± 1.63 b | 25.30 ± 0.70 b | 56.67 ± 2.33 b |
| Red (3 inter.) | 5.65 ± 0.06 b | 0.462 ± 0.005 c | 3.49 ± 0.06 b | 1.66 ± 0.06 c | 1.23 ± 0.02 c | 44.95 ± 1.95 a | 29.48 ± 1.88 a | 74.43 ± 3.83 a |
| Green monoculture | 2.67 ± 0.03 c | 0.443 ± 0.005 c | 2.06 ± 0.06 c | 1.32 ± 0.04 d | 1.65 ± 0.03 b | 27.30 ± 1.30 b | 32.77 ± 1.17 c | 60.07 ± 2.47 c |
| Green (inter. red) | 5.90 ± 0.02 a | 0.477 ± 0.002 b | 3.54 ± 0.08 a | 2.14 ± 0.05 b | 1.37 ± 0.04 c | 33.57 ± 1.57 a | 39.87 ± 1.63 b | 73.44 ± 3.20 a |
| Green (inter. white) | 3.92 ± 0.01 b | 0.489 ± 0.006 b | 2.29 ± 0.07 b | 1.60 ± 0.05 c | 1.85 ± 0.02 a | 25.90 ± 1.90 bc | 42.05 ± 0.85 ab | 67.95 ± 2.75 b |
| Green (3 inter.) | 2.68 ± 0.07 c | 0.881 ± 0.012 a | 3.48 ± 0.09 a | 2.58 ± 0.02 a | 1.98 ± 0.03 a | 22.93 ± 1.63 c | 42.97 ± 0.63 a | 65.90 ± 2.26 b |
| White monoculture | 5.83 ± 0.02 a | 0.954 ± 0.007 a | 3.49 ± 0.06 b | 3.13 ± 0.06 c | 1.18 ± 0.01 a | 5.48 ± 0.18 b | 32.83 ± 0.97 a | 38.31 ± 1.15 a |
| White (inter. red) | 6.85 ± 0.03 a | 0.960 ± 0.011 a | 3.87 ± 0.07 a | 3.32 ± 0.04 b | 1.10 ± 0.02 ab | 7.47 ± 0.21 a | 32.20 ± 1.20 a | 39.67 ± 1.41 a |
| White (inter. green) | 4.71 ± 0.06 b | 0.484 ± 0.005 c | 3.17 ± 0.06 c | 2.82 ± 0.02 d | 1.02 ± 0.02 b | 3.47 ± 0.15 c | 23.20 ± 1.22 b | 26.67 ± 1.37 b |
| White (3 inter.) | 4.46 ± 0.03 b | 0.821 ± 0.010 b | 4.02 ± 0.02 a | 3.69 ± 0.03 a | 0.80 ± 0.01 c | 1.95 ± 0.11 d | 16.82 ± 0.18 c | 18.77 ± 0.29 c |
- a Plants were cultured in soil containing 10 mg/kg Cd added to soil for 60 d in a pot experiment. Edible part = tuberous root + leaf. Values are means (± standard error) of 3 replicate pots. Significant differences (indicated by different lowercase letters) within a column are based on one-way analysis of variance with the least significant difference test (p < 0.05).
- inter. = intercropping.
Biomass of radish
The edible part biomass of the 3 radish genotypes was as follows: green radish > red radish > white radish. When 2 or 3 genotypes of radish were grown together, their biomasses were affected (Table 1). Compared with monoculture, the biomasses of green and white radishes were both increased by intercropping with red radishes (p < 0.05), and the biomass of green radishes was increased by intercropping with white radishes (p < 0.05). When all 3 varieties were grown together, only the biomass of red radishes increased (p < 0.05), while that of the others decreased compared with the monoculture.
Potassium and phosphorus contents in radish
When mixed with other radish types, the potassium and phosphorus contents in the edible parts of red radishes increased compared with monoculture, with the exception of potassium content when red radishes were grown with white radishes (Table 2). The potassium content was augmented and the phosphorus content was decreased in the edible parts of green radishes when mixed with other radishes compared with the monoculture. In white radishes, the potassium and phosphorus contents in the edible parts were enhanced by intercropping, except that they decreased when mixed with green radishes compared with the monoculture.
| Treatments | K content in radish (g/kg fresh wt) | P content in radish (g/kg fresh wt) | ||||||
|---|---|---|---|---|---|---|---|---|
| Root | Tuberous root | Leaf | Edible part | Root | Tuberous root | Leaf | Edible part | |
| Red monoculture | 5.35 ± 0.18 a | 2.37 ± 0.12 b | 2.45 ± 0.16 b | 2.40 ± 0.07 b | 0.597 ± 0.012 b | 0.194 ± 0.005 c | 0.227 ± 0.009 b | 0.208 ± 0.011 d |
| Red (inter. green) | 5.27 ± 0.12 a | 2.91 ± 0.07 a | 2.97 ± 0.14 ab | 2.95 ± 0.17 a | 0.578 ± 0.003 b | 0.304 ± 0.011 a | 0.330 ± 0.004 a | 0.321 ± 0.003 a |
| Red (inter. white) | 4.82 ± 0.19 b | 1.81 ± 0.10 c | 3.08 ± 0.19 a | 2.38 ± 0.03 b | 0.533 ± 0.010 c | 0.217 ± 0.003 b | 0.328 ± 0.006 a | 0.267 ± 0.001 b |
| Red (3 inter.) | 4.76 ± 0.18 b | 2.25 ± 0.19 b | 3.21 ± 0.17 a | 2.63 ± 0.11 b | 0.646 ± 0.013 a | 0.213 ± 0.005 b | 0.243 ± 0.007 b | 0.225 ± 0.012 c |
| Green monoculture | 4.70 ± 0.16 a | 2.51 ± 0.11 b | 2.27 ± 0.12 b | 2.38 ± 0.15 b | 0.547 ± 0.003 b | 0.254 ± 0.010 b | 0.278 ± 0.009 b | 0.267 ± 0.010 b |
| Green (inter. red) | 5.14 ± 0.15 a | 2.47 ± 0.09 b | 2.49 ± 0.13 ab | 2.48 ± 0.11 b | 0.597 ± 0.007 a | 0.239 ± 0.012 b | 0.248 ± 0.007 c | 0.244 ± 0.009 c |
| Green (inter. white) | 3.51 ± 0.08 b | 3.07 ± 0.10 a | 2.47 ± 0.09 ab | 2.70 ± 0.12 a | 0.578 ± 0.008 ab | 0.257 ± 0.013 b | 0.244 ± 0.004 c | 0.249 ± 0.007 bc |
| Green (3 inter.) | 2.88 ± 0.03 c | 2.70 ± 0.13 b | 2.80 ± 0.11 a | 2.77 ± 0.05 a | 0.427 ± 0.010 c | 0.296 ± 0.006 a | 0.365 ± 0.006 a | 0.341 ± 0.005 a |
| White monoculture | 5.73 ± 0.20 b | 3.96 ± 0.11 b | 3.74 ± 0.11 a | 3.77 ± 0.14 ab | 0.739 ± 0.011 ab | 0.489 ± 0.009 a | 0.282 ± 0.007 b | 0.312 ± 0.007 b |
| White (inter. red) | 6.81 ± 0.18 a | 4.89 ± 0.18 a | 3.77 ± 0.15 a | 3.98 ± 0.11 a | 0.773 ± 0.014 a | 0.508 ± 0.007 a | 0.327 ± 0.006 a | 0.361 ± 0.009 a |
| White (inter. green) | 6.12 ± 0.22 b | 2.57 ± 0.15 c | 3.66 ± 0.16 a | 3.52 ± 0.17 b | 0.682 ± 0.012 c | 0.283 ± 0.005 b | 0.296 ± 0.010 b | 0.294 ± 0.011 b |
| White (3 inter.) | 5.53 ± 0.16 b | 4.53 ± 0.16 ab | 3.72 ± 0.10 a | 3.80 ± 0.13 ab | 0.713 ± 0.010 bc | 0.486 ± 0.007 a | 0.351 ± 0.009 a | 0.365 ± 0.010 a |
- a Plants were cultured in soil containing 10 mg/kg Cd added to soil for 60 d in a pot experiment. Edible part = tuberous root + leaf. Values are means (±standard error) of 3 replicate pots. Significant differences (indicated by different lowercase letters) within a column are based on one-way analysis of variance with the least significant difference test (p < 0.05).
- inter. = intercropping.
Soil pH
Relative to the monocultures, the soil pH was decreased by intercropping (Table 3), except that it increased when red and white radishes were grown together.
| Treatments | Soil pH | Soil exchangeable cadmium (mg/kg) | Available K (mg/kg) | Available P (mg/kg) |
|---|---|---|---|---|
| Red monoculture | 7.335 ± 0.015 cd | 7.88 ± 0.07 c | 178.43 ± 0.42 ab | 5.74 ± 0.05 a |
| Green monoculture | 7.550 ± 0.03 a | 8.02 ± 0.06 b | 185.16 ± 1.84 a | 5.11 ± 0.02 d |
| White monoculture | 7.363 ± 0.043 c | 8.06 ± 0.05 b | 144.96 ± 0.34 c | 5.50 ± 0.03 b |
| Red intercropped with green | 7.304 ± 0.006 d | 7.76 ± 0.02 c | 123.88 ± 1.42 e | 4.90 ± 0.01 e |
| Red intercropped with white | 7.410 ± 0.010 b | 7.89 ± 0.07 c | 172.52 ± 1.04 b | 5.36 ± 0.04 c |
| Green intercropped with white | 7.295 ± 0.045 d | 8.25 ± 0.03 a | 173.00 ± 2.00 b | 5.16 ± 0.06 d |
| Three intercropped | 7.306 ± 0.014 d | 8.27 ± 0.01 a | 132.16 ± 1.14 d | 5.34 ± 0.09 c |
- a Plants were cultured in soil containing 10 mg/kg Cd added to soil for 60 d in a pot experiment. Values are means (±standard error) of 3 replicate pots. Significant differences (indicated by different lowercase letters) within a column are based on one-way analysis of variance with the least significant difference test (p < 0.05).
Soil exchangeable cadmium
The exchangeable cadmium concentration in the soil when red and green radishes were intercropped was less than in the respective monocultures, and the concentration when red and white radishes were intercropped were between the values of the respective monocultures (Table 3). The exchangeable cadmium concentration in soil when green and white radishes were intercropped and was greater when all 3 varieties were grown together than in the respective monocultures.
Soil available potassium and available phosphorus
Similar to the exchangeable cadmium in the soil, the available potassium in the soil when red and green radishes were intercropped was less than in their monocultures (Table 3). The available potassium was between the respective monoculture values when red and white radishes and when white and green radishes were intercropped. The available potassium in the soil when all 3 radish types were mixed was less than the value in each monoculture. The available soil phosphorus was less than that of the monocultures when red and green radishes and when green and red radishes were intercropped (Table 3). When green and white radishes were grown together, the available soil phosphorus was between those of the green and white radish monocultures. The available phosphorus in soil of the 3 radish types mixed was less than in red radish monoculture and in white radish monoculture but greater than in green radish monoculture.
Field experiment
Cadmium content in the edible parts of radish
In the field experiment, the cadmium contents in the edible parts of the 3 genotype radishes were ranked as follows: white radish > red radish > green radish. The cadmium contents in the edible parts of red and green radishes, but not white radishes, were increased by intercropping compared with the monoculture (Figure 1), which was similar to the pot experiment. The cadmium contents in the edible parts were ranked as follows: for red radish, intercropping with green radish > intercropping with white radish > 3 radishes intercropped > monoculture, and the differences between intercropping treatments and monoculture were significant (p < 0.05); for green radish, 3 radishes intercropped > intercropping with red radish > intercropping with white radish > monoculture, and the differences between intercropping treatments and monoculture were significant (p < 0.05); and for white radish, 3 radishes intercropped > intercropping with red radish > monoculture > intercropping with green radish, and the differences between intercropping treatments and monoculture were significant (p < 0.05).
Yield of edible part in radish
The yield of the 3 radish genotypes was as follows: green radish > red radish > white radish. The field experiment showed that intercropping had different effects on the edible yield of the 3 radish varieties (Figure 2). For red radishes, the edible yield was ranked as follows: 3 radishes intercropped > monoculture > intercropping with white radish > intercropping with green radish, and the differences among treatments were significant (p < 0.05). For green radishes, the order was intercropping with red radish > intercropping with white radish > monoculture > 3 radishes intercropped, and the differences among treatments were significant (p < 0.05). The ranking for white radishes was intercropping with red radish > monoculture > intercropping with green radish > 3 radishes intercropped, and the differences between intercropping treatments and monoculture were significant (p < 0.05) except intercropping with red radishes. Thus, compared with the monoculture, red radishes improved the biomass or yield of both green and white radishes when grown with them, respectively; green radish biomass or yield improved when planted with white radishes; and a mixture of all 3 genotypes increased the biomass or yield of only red radishes.
DISCUSSION
The difference in appearance of radish varieties is mainly attributed to genetic diversity. These radish genotypes have different metabolic pathways that lead to differences in their absorption of elements from the soil 25. Under heavy metal stress, the different genotypes show different levels of resistance, resulting in substantial variations in the uptake of heavy metals 6. In the present experiment, the cadmium uptake in 3 genotypes of radish was ranked as white radish > red radish > green radish and the yield was green radish > red radish > white radish.
When radishes are intercropped with other crops, the 2 species can significantly improve nutrient absorption from the soil and crop yield, reflecting the superiority of intercropping 26. Under heavy metal stress, the root exudates of the 2 plants can change the forms of heavy metal in the rhizosphere and thus increase or decrease heavy metal uptake in plants 14, 15. When the hyperaccumulator Thlaspi carulescens intercropped with the general plant Thlaspi arvense, zinc accumulation in the former was enhanced significantly, while that in the latter significantly dwindled 27. The Zn hyperaccumulator Sedum alfredii intercropped with Zea mays can significantly reduce zinc and copper accumulation in the grains of Z. mays 20. However, the legumes can increase cadmium contamination in neighboring crops 22.
In the pot experiment, the results showed that cadmium content in radishes was increased by intercropping 2 or 3 radish genotypes, except when white and green radishes were grown together; most of these concentrations were above the Chinese allowable limit in root vegetables to be protective of human health 28. The field experiment further ascertained that intercropping different varieties of radish increased cadmium accumulation. However, the soil pH increase or decrease by intercropping was not consistent with the changing of exchangeable cadmium in the soil. This suggests that the increased cadmium uptake in radishes was related to the lower soil pH as a result of organic acids from the roots and to increased exchangeable cadmium concentrations 17 and that there might be other root metabolites in these genotypes to affect cadmium uptake in radishes.
In terms of nutrient uptake, some intercropping modes augmented potassium and phosphorus contents in the edible parts of radishes, and only a few intercropping modes improved the biomass of radishes. In the intercropping system, the green radish was the fastest-growing plant and might get more light resources for growth. Thus, the yield of green radishes was improved by intercropping with the other 2 radish varieties, and the yields of red and white radishes were reduced by intercropping with green radishes. The red radish was the 2nd fastest-growing plant, but only a mixture of all 3 genotypes improved the biomass of red radishes, while the biomass of white radishes was improved by intercropping with red radishes, suggesting that the root metabolites of white radishes could inhibit red radish growth and that those of red radishes could promote radish growth.
Farmland heavy metal contamination, a worldwide problem, is an increasing concern in many developing countries 29. The preferred method of remedying farmland heavy metal contamination is intercropping, which has been successfully applied in agricultural production 20, 30. However, we must find suitable plant species for intercropping to achieve the best results. The present experiments showed that genetic diversity of planted varieties could improve the absorption of cadmium in radishes and that only a few intercropping modes improved the biomass of radishes. Therefore, in cadmium-contaminated soil, planting multiple varieties together should be carefully considered.
Acknowledgment
The authors thank J. Li, J. Huang, H. Lan, H. Liang, and Q. Liu at Sichuan Agricultural University for helping with cadmium measurements.
