Botanical Studies (2011) 52: 41-46.
Effects of cadmium on growth and photosynthetic activities in pakchoi and mustard
Xin CHEN1, *, J. WANG1, 2, Y. SHI1, M.Q. ZHAO1, 2, and G.Y. CHI1' 2
1Key Laboratory of Terrestrial Ecological Process, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, People's Republic of China
2Graduate School of the Chinese Academy of Sciences, Beijing 100039, People's Republic of China
(Received December 18, 2008; Accepted June 8, 2010)
ABSTRACT. In this study, we determined the effects of different concentrations of soil cadmium (0-24 mg-kg-1) on growth and photosynthetic activities in leaves of pakchoi and mustard using pot experiments un­der greenhouse conditions. Both shoot and root weight decreased progressively with increasing Cd concentra­tion for pakchoi and mustard. Negative linear relationships were observed between total Chlorophyll contents and Cd concentrations in soils in pakchoi (r2=-0.681, P<0.01) and mustard (r2=-0.463, P<0.05). In comparison to the controls (Cd=0 mg-kg-1), significant reductions of chlorophyll-a and chlorophyll-b were both observed at 24 mg Cd kg-1soil. The increase in cadmium concentration also caused a decline in the net rate of photo­synthesis (Pn) and stomatal conductance (Gs). At lower concentrations of Cd (e.g. 6 mg-kg-1), a retarded de­velopment was observed only in mustard. However, a significant decrease of Gs for both plants was observed at concentrations above 12 mg Cd kg-1 soil. From this study, we found the photosynthetic activity of pakchoi more sensitive to Cd stress than that of mustard.
Keywords: Cadmium; Growth; Photosynthetic activities; Pigments.
INTRODUCTION
content (Shakya et al., 2008) and growth (Zhou and Qiu, 2005), affects chloroplast function or CO2 fixation (Krupa and Baszynski, 1995; Seidlecka et al., 1997). Peter Faller et al. (2005) showed that Cd2+ inhibited photoactivation of photosystem II by competitive binding to the essential Ca2+ site. Earlier investigations have demonstrated that the net rate of photosynthesis can be conspicuously decreased with increasing concentrations of Cd (Lakshaman and Su-rinder, 1999). Studies on the dose-response of plants to Cd stress have shown that stomatal conductance varies with different Cd2+ concentrations (Chugh et al., 1999). Further­more, the photosynthetic responses of monocotyledons to a stress factor have been observed as have those of dicoty­ledons (Drazkiewicz and Baszynski, 2005).
Thus, in our study, we chose to investigate pakchoi cabbage, which stood in for monocotyledons, and mus­tard, which represented dicotyledons. Both plants are very common in China, especially in the northeast, and are well known for their tolerance to heavy metals such as Cd (Fang et al., 2004; Xu et al., 2007). Cadmium, a major pollutant due to its great toxicity and high mobility in soil-plant-human (or animal) systems, was examined for its toxicological effects on chlorophyll content and on some photosynthetic parameters (e.g. photosynthetic rate and stomatal conductance) in leaf vegetables that are essential for human health. In addition, growth parameters were also determined. Therefore, the aim of this paper was to characterize the changes in growth parameters and photo-
Heavy metals have been increasingly found in soils due to atmosphere deposition, sludge, sewage irrigation, utilization of metal-containing farmyard manures and fertilizers, and industry and mine residues, resulting in a potential risk for human health when thse metals are transferred from crops to the human diet. They play an important role in the environment not as a result of human activity but also as toxic species above certain concentra­tions (Ngayila et al., 2008; 2009). At high concentrations, a number of heavy metals have been reported to inhibit the growth and decrease the productivity of crops (Liu et al., 2003). Among them, cadmium (Cd) is well known as a highly toxic environmental element due to its great toxic-ity and high mobility from soil to plants and further down the food chain (Vig et al., 2003). It can be incorporated and accumulated by all organisms in large amounts and disturb physiological metabolisms in plants like transpira­tion, photosynthesis, respiration, and nitrogen assimila­tion (Chugh et al., 1999; Zhou et al., 2006; Wang et al., 2008). Additionally, Cd is a divalent heavy metal cation (Cd2+) which is readily taken up and causes phytotoxic-ity. Cd excess in the environment decreases chlorophyll

*Corresponding author: E-mail: chenxin@iae.ac.cn; Tel: +86-24-88087808; Fax: +86-24-83970300.
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Botanical Studies, Vol. 52, 2011
synthetic activity in two types of vegetables representing monocotyledons and dicotyledons and to relate them to defense strategies against Cd toxicity.
Analysis of photosynthetic parameters, the net rate of photosynthesis (Pn) and stomatal conductance (Gs) were carried out on the third (fully expanding) leaves of each entire plant just prior the harvest, using an open gas ex­change system (Li-6400; Li-Cor Inc., NE, USA). All the measurements were made between 9:30 and 11:30 am. These determinations were recorded on five plants in a treatment.
Based on the data obtained from the experiment, the results presented are the mean standard deviation (SD) gained from at least three replicate samples using Micro­soft Office Excel 2003. Statistical analysis by the least sig­nificant difference (LSD) for multiple comparisons, taking P<0.05 as significant, was calculated by SPSS 13.0.
MATERIALS AND METHODS
Some abbreviations used in this article were as follows: TOC means total organic carbon; Pn means the net rate of photosynthesis; Gs means the stomatal conductance; Chl-a means chlorophyll-a contents; Chl-b means chlorophyll-b contents.
The tested soil was collected from an agricultural field in the suburb of Shenyang, Liaoning Province, China. This soil is grey meadow soil, and chemical analysis showed that its soil bulk density, total organic carbon (TOC), total N, total P, and pH were 1.33±0.09 g-cm-3, 1.67±0.13%, 0.91±0.11 g-kg-1, 0.47±0.24 g-kg-1, and 7.63±0.57, respec­tively. Surface soil (0-20 cm) samples, which were ground to pass through a 4-mm nylon sieve, were used in the pot-culture experiment. 5.5 kilograms of soils were mixed with CdCl2-5H2O solutions for a series of soil Cd levels of 3 (T1), 6 (T2), 9 (T3), 12 (T4), 24 (T5) mg-kg-1 dry soil, and treatment without adding Cd was regarded as control (T0). Soluble fertilizers including 150 mg N, 200 mg P and 300 mg K kg-1 dry soil were applied at the same time. Soils were mixed sufficiently and then placed into plastic pots (20 cm><20 cm><20 cm), incubated for two weeks. Each treatment was replicated five times. This experiment was carried out in a greenhouse.
Leaf vegetables used in this investigation were pakchoi (Brassica campestris ssp.) and mustard (Brassica juncea Czernajew), which were cultivated until 4-5 cm height in seedbeds, and then transplanted into each pot. Each pot had three plants. All the plastic pots were buried in the earth ran­domly in the greenhouse situated in the Shenyang Station of Experimental Ecology, Chinese Academy of Sciences (123°41' N and 41°31' E), and watered daily to maintain around 75% of the field water holding capacity during the whole test period. The tested vegetables were harvested af­ter 60 days when they reached their physiological maturity. They were washed thoroughly first with running tap water followed by distilled water and then dried at 105°C for 10 min. and thereafter at 80°C until completely dry.
Pigments were extracted by grinding 0.2 g freshly sam­pled leaves in 80% (v/v) acetone/water at room tempera­ture for 24 h in the dark according to Arnon (1949) and Wellburn (1994) with some modifications. Photosynthetic pigments of all the samples were extracted in triplicate to minimize experimental errors. Chlorophyll and carotenoid contents were measured by using absorbance recorded at 647 nm, 663 nm and 470 nm for maximum absorption of chlorophyll-a, chlorophyll-b and carotenoid, respectively. The extinction coefficients were determined by a UV-Vis spectrophotometer (SPECORD50; Analytik Jena AG; Ger­many). Pigment contents were calculated in mg-g-1 fresh weight by applying the absorption coefficient equations described by Lichtenthaler (1987).
RESULTS
Effect of Cadmium on plant growth
Exposing leaf vegetables to different levels of Cd re­sulted in reductions of growth as shown in Table 1. A retarded development in Cd-treated plants compared to the controls was observed. In the presence of 12 mg Cd kg-1 soil, significant reduction was found in shoot weight for pakchoi (P<0.05), and a marked decrease in root weight was observed at 6 mg Cd kg-1 soil. Compared with the non-treated mustard, shoot weight in mustard was signifi­cantly suppressed at 9 mg Cd kg-1soil, and root weight was noticably decreased at 12 mg Cd kg-1 soil. Furthermore, the Cd tolerance index in root was less than in shoot.
Effect of Cadmium on photosynthetic pigments
The expanding leaves of mustard had higher total chlo­rophyll than those of pakchoi (Figure 1). Chlorophyll-b concentration was significantly lower than that of chlo-rophyll-a in both tested plants (P<0.01). The pigment contents in plants showed an almost linear decrease in response to Cd concentration increases in the soil, which ranged from 0 mg-kg-1 (the control) to 24 mg-kg-1. Nega-
Figure 1. Impacts of Cd on the chlorophyll contents of pakchoi and mustard. Values are average of five replicates.
CHEN et al. ― Effects of Cd on leaf vegetables
43
Table 1. Shoot and root weight in plants exposed to different Cd concentrations.

Plants

Cd concentration

Shoot


Root

(mg.kg-1)

Dry Weight (g-plant-1)

Cd tolerance index (%)

Dry Weight (g-plant-1)

Cd tolerance index (%)

Packchoi

0 (Control)

8.99±0.66a


100.0

0.90±0.10a


100.0
3
8.35±0.29ab
92.9
0.81±0.05ab
89.7
6
8.09±0.24ab
90.0
0.74±0.09bc
82.6
9
7.68±0.84ab
85.4
0.72±0.05bc
80.6
12
6.71±1.68b
74.6
0.64±0.05c
70.8
24
6.66±1.53b
74.0
0.47±0.02c
52.8
Mustard
0 (Control)
7.31±0.09a
100.0
1.20±0.09a
100.0
3
7.12±0.13ab
97.4
1.15±0.08ab
95.9
6
6.98±0.62ab
95.5
0.94±0.06b
78.2
9
6.54±0.40b
89.5
0.79±0.10b
65.7
12
6.41±0.54b
87.7
0.62±0.14c
51.2
24
5.61±0.45c
76.8
0.51±0.03c
42.4

Cadmium tolerance index was calculated as the ratio of shoot or root dry weight at Cd supply to that of control. Means ± SD with different letters are significantly different from each other (P<0.05) according to LSD (n=5).
tive linear relationships were observed between total Chl contents and Cd concentrations in soils in pakchoi (r2=-0.681, P<0.01) and mustard (r2=-0.463, P<0.05). Chlorophyll-a content was conspicuously greater than that of chlorophyll-b in all test plants. Additionally, parallel de­creases in Chl-a and Chl-b due to Cd stress have also been observed. Significant reductions of Chl-a and Chl-b were also observed at 24 mg Cd kg-1 soil. In comparison to the control (Cd=0 mg-kg-1), the Chl-a in pakchoi and mustard decreased by 32.29% and 20.56% at 24 mg Cd kg-1 soil. However, the decreases in the Chl-b in pakchoi and mus-tard were 21.54% and 21.55% with 24 mg Cd kg-1soil in comparison to the control. The highest carotenoid content was measured in the control plants of test vegetables, and these contents decreased with increasing Cd concentration (Figure 2). The content of mustard was higher than that of all Cd treatments.
Figure 2. Impacts of Cd on the carotenoid content of pakchoi and mustard. Values are average of five replicates.
DISCUSSION
Effect of Cadmium on photosynthesis
Parameters of plant growth like biomass have been shown to be very sensitive to heavy metals in higher plants (Arun et al., 2005). Our research has clearly illustrated that cadmium inhibited plant growth. Both shoot and root weight decreased progressively with increasing Cd con­centration for both vegetables, and significantly higher reductions of weight were observed at lower Cd concen­tration in root than in shoot (Table 1). Low concentrations of Cd retard root growth without toxic effects in leaves, and moderately higher concentrations severely inhibit root growth and lead to Cd accumulation in leaves (Prasad, 1995). Cadmium affected root more than shoot, leading to a lower tolerance index for root. The phenomenon can be attributed to the fact that roots are the first organs receiv­ing cadmium ions in soils via apoplastic transport, result­ing in a higher Cd accumulation there (Drazkiewicz et al.,
Exposing plants to different levels of Cd resulted in changes to the photosynthetic parameters, Pn and Gs in leaves, as shown in Figure 3. The effect of Cd on these pa­rameters declined progressively with the increasing concen­tration of applied cadmium. In comparison to control, the Pn of pakchoi at 12 mg Cd kg-1 soil decreased (P<0.05) by 9.33% and reached the bottom at 24 mg Cd kg-1 soil (Figure 3a). Mustard supplied with 6 mg Cd kg-1 soil showed a sig­nificant decline in the rate of photosynthesis, with a decline of 9.02%. Cadmium also exerted a profoundly deleterious effect on stomatal conductance (Gs) (Figure 3b). Compared with theGs of non-treated (control) plants, the Gs of pakchoi was suppressed by 12.26% at the highest Cd concentration (Cd=24 mg-kg-1). However, the mustard Gs was depressed
by 15.95% at 12 mg Cd kg-1 soil.
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Botanical Studies, Vol. 52, 2011
tron transport chain, resulting in reduction of chlorophyll content (Thapar et al., 2008). It was reported that cadmium caused a decline in carotenoid content (Thapar et al., 2008). In this study, the carotenoid content of both vegeta­bles fell as cadmium concentrations increased (Figure 2). In our experiment, the highest net rate of photosynthesis (Pn) was observed in the control plants of test vegetables, and it declined with increasing Cd concentration (Figure 3 a). Compared with the controls, significant decreases of photosynthetic rate and shoot weight for pakchoi were observed after 12 mg Cd kg-1 soil. However, in mustard the net rate of photosynthesis showed sensitivity to lower Cd concentrations than did plant growth. We conclude that mustard is more sensitive to net rate of photosynthesis changes than is pakchoi under Cd stress. Therefore, it is deduced that Pn can be used as a bioindicator of photo­synthesis in plants undergoing metal stress. Cadmium had no significant effects on stomatal conductance from 3 to 9 mg Cd kg-1 soil in tested vegetables, but a significant de­crease of Gs was observed after 12 mg Cd kg-1 soil (Figure 3b). The decrease in stomatal conductance in response to Cd treatment was accompanied by a decline in the net rate of photosynthesis. Similar results have been reported by other researchers (Dunand et al., 2002). According to our results, the physiological responses of tested plants to cadmium exposure were much more conspicuous than was growth. Furthermore, Cd affects the photosynthetic activity of mustard via inhibiting chlorophyll biosynthesis and photosynthetic rate while stomatal conductance was not sensitive to Cd at moderately higher concentrations. In pakchoi, chlorophyll content, the net rate of photosyn­thesis, and stomatal conductance all can be inhibited by cadmium, which results in a significant reduction of shoot weight. Based on the results, we can conclude that the re­sistance of pakchoi to Cd is greater than that of mustard in respect to photosynthetic activity and growth.
From this study, it can be concluded that certain con­centrations of Cd inhibit plant growth, cause chlorophyll loss, and affect photosynthetic activities. The photosyn­thesis of pakchoi seems to be more sensitive to Cd stress probably due to more rapid damage in the cell membrane and to the biosynthesis of the photosynthetic enzymes of this species. Therefore, further investigation on a cellular or molecular level is necessary to understand the mecha­nism behind the differences in Cd reaction between the monocotyledon pakchoi and the dicotyledon mustard.
Figure 3. Impacts of Cd on the net rate of photosynthesis (Pn) and stomatal conductance (Gs) of pakchoi and mustard. Values are average of five replicates.
2003). Heavy metals such as Cd can efficiently inhibit the synthesis of proteins, such as phosphoenolpyruvate car-boxylase (Stiborovd et al., 1986).
In agreement with earlier reports (Papazpglou et al., 2005; Sun et al., 2008), we find that photosynthetic activ­ity is suppressed by heavy metals. This can be attributed to the disruptive action of metals on chlorophyll synthesis (Vajpayee et al., 2000), on photosystem efficiency (Chugh et al., 1997), on the activity of photosynthetic enzymes (Mobin and Nafees, 2007), and on plant water balance (Zhou and Qiu, 2005). It is also attributable to chloroplast damage (Baszynski et al., 1988). The levels of pigment content were affected negatively by the presence of cad­mium. The chlorophyll contents of vegetables decreased with increasing Cd concentrations (Figure 1). Similar re­sults have been obtained in other laboratory studies (Jiang et al., 2007). Continuous metabolization of chlorophyll in plants is adapted to different physiological processes. In the process of chlorophyll synthesis, chlorophyll-a can be synthesized earlier, and transformed to Chlorophyll-b (Guo et al., 2006). Therefore, the similar trend of Chl-a and Chl-b was noted as shown in Figure 1. Chlorophyll-a content exceeded that of chlorophyll-b in all test plants, which has been proven by other researchers (Mobin and Nafees, 2007; Yasemin et al., 2008). In addition, high con­centrations of heavy metals can degrade the activities of photosynthetic enzymes and block the photosynthetic elec-
Acknowledgments. This research was financially sup­ported by the National Key Technology R&D Program of China (No. 2007BAD89B03) and the project of Knowl-edge Innovation of the Chinese Academy of Sciences (No. KSCXZ-YW-N-037).
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鎘脅迫對小白菜、油菜生長和光合活性的影響
陳欣1 王俊1,2 史奕1 趙牧秋1,2 遲光宇1,2
1中國科學院沈陽應用生態研究所陸地生態過程重點實驗室 2中國北京科學院研究生院
本文研究了溫室盆栽條件下,不同濃度鎘對小白菜和油菜生長及光合作用的影響。結果表明:小白
菜和芥菜地上、地下幹重隨 Cd 濃度升高而減少,葉綠素含量與土壤 Cd呈顯著負相關,相關係數分別
-0.681-0.463 Cd濃度達到 24 mg - kg-1時,葉綠素a和葉綠素b含量顯著低於對照處理。Cd 濃度
升高會降低淨光合速率 (Pn) 和氣孔導度(Gs) 。在較低Cd濃度 (6 mg- kg-1) 時,只有芥菜的淨光合效
率受到了顯著抑制,而當
Cd 濃度達到12 mg/kg ,小白菜和芥菜的氣孔導度均顯著低於對照處理。研究
發現,小白菜光合活性對鎘脅迫較芥菜敏感。
關鍵詞:鎘;生長;光合活性。