Annals of Applied Biology ISSN 0003-4746
R E S E A R C H A RT I C L E
Varietal differences in mungbean (Vigna radiata) for growth, yield, toxicity symptoms and cadmium accumulation A. Wahid & A. Ghani Department of Botany, University of Agriculture, Faisalabad 38040, Pakistan
Keywords Correlations; mesophyll tissue; nutrients; Pakistan; toxicity; Vigna radiata. Correspondence A. Wahid, Department of Botany, University of Agriculture, Faisalabad 38040, Pakistan. Email:
[email protected] Received: 20 June 2007; revised version accepted: 5 September 2007. doi:10.1111/j.1744-7348.2007.00192.x
Abstract Increased cadmium (Cd) contamination of soils resulting from industrial activities is critical to crop production. The objective of this study was to find varietal differences for foliar chlorosis and necrosis, growth and Cd accumulation in mungbean (Vigna radiata). Despite substantial varietal differences, increased Cd levels reduced the shoot and root dry weight and the number and area of leaves at different growth stages. Applied Cd stress produced the foliar symptoms such as marginal and intervein chlorosis and scattered necrotic spots on younger leaves while accelerating the senescence of older leaves. Slope of regression equation and correlations of shoot Cd content with foliar Cd toxicity revealed that leaf chlorosis was more damaging than necrosis. At maturity, number of pods per plant and seeds per pod were maximally reduced to 37% and 26%, while 100-seed weight, seed yield and harvest index showed 61%, 79% and 54% reduction, respectively, as a result of Cd toxicity. Results suggested that although varietal difference exists, the accumulated Cd is mainly toxic to the mesophyll tissue, most probably by interfering with the uptake of essential nutrients, thereby reducing growth and yield at various stages. Therefore, selection programmes based on foliar toxicity criteria may be beneficial for better utilisation of Cd-polluted soils.
Introduction Heavy metal contamination of soils is an increasing worldwide problem and great environmental threat to biota as these metals accumulate in soils and plants in undesirable amounts (Jamali et al., 2007). Although some heavy metals such as iron, molybdenum, copper, cobalt, zinc and manganese are nutritionally important in trace amounts, their increased levels are potentially hazardous (Keeling et al., 2003). Among the other abundant/toxic metals, cadmium (Cd) is a more devastating soil pollutant because of its excessive discharge as a by-product from different industries (Mengel et al., 2001). Cadmium (Cd) is a non-essential and highly toxic metal ion for growth and development. It is easily taken up and translocated to different plant parts (Benavides et al., 2005; Grata˜o et al., 2005). Reduction in growth and yield with increased levels of Cd in growth media arises because of increased leaf rolling and chlorosis of leaf and
Ann Appl Biol 152 (2008) 59–69 ª 2007 The Authors Journal compilation ª 2007 Association of Applied Biologists
stem (Ghani & Wahid, 2007) and reduced photosynthetic rate (Chugh & Sawhney, 1999). Studies suggest that Cd reduces ATPase activity of plasmalemma fraction in wheat and sunflower roots (Astolfi et al., 2005), changes lipid composition by enhanced production of reactive oxygen species or free radicals (Balakhnina et al., 2005; Gomes-Junior et al., 2006) or decreases activities of antioxidants (Pal et al., 2006). Species and cultivars display marked differences for Cd tolerance in, for example, wheat (Zhang et al., 2002), rice (Wu et al., 2004; He et al., 2006) and pea (Metwally et al., 2005). When Cd enters the food chain, it causes intricate health problems. Being more readily bioavailable, hyperaccumulation of Cd causes leaf chlorosis and inhibits chlorophyll biosynthesis (Baryla et al., 2001; Wang & Zhou, 2006; Lea et al., 2007). Mungbean [Vigna radiata (L.) Wilczek] is an important source of human diet, feed and fodder for animals and green manure (Saleemi, 1998). It demands less
59
Varietal difference for Cd toxicity effects in mungbean
A. Wahid & A. Ghani
nitrogenous fertilisers, maintains soil fertility and fits well in different cropping systems (Nazir, 1994). Identified as a high yielding crop in many Asian countries, mungbean’s sensitivity to potential toxicants such as Cd remains to be comprehensively assessed. Available data show that mungbean is sensitive to Cd stress (Bindhu & Bera, 2001). The symptoms appearing on various plant parts are direct measures of the intensity of prevailing stress. These effects can be greatly helpful in diagnosing stress effects and adopting appropriate strategies to increase stress tolerance and selection of promising materials (Wahid et al., 1999; Ahmad et al., 2005). Despite sporadic reports, varietal differences in mungbean for Cd tolerance need to be comprehensively investigated. It is predicted that hampered growth in mungbean is because of foliar toxicity symptoms produced by Cd accumulation and that the appearance of these effects are genetically related. This study evaluated some elite mungbean varieties for changes in growth, shoot Cd accumulation and yield at various growth stages.
Materials and methods Experimental details This study was conducted during 10 February to 5 June of 2004 and 2005. Seeds were sown in plastic pots (five per pot) containing 10 kg soil. Thinning was carried out 3 days after emergence of seedlings, and two uniform plants were maintained per pot. The experimental design was completely randomised with four replications. Physicochemical characteristics of the soil were as follows: texture, sandy loam; saturation, 27–29%; pH 8; ECe, 2.5 dS m–1; organic matter, 1.05%; total N, 0.50%; other
nutrients (mg kg–1) included total P, 6.6; K+, 160 and Ca2+, 10.3. Plants were irrigated with subsoil water whenever needed to keep soil moisture up to field capacity. Nutrient solution (Hoagland & Arnon, 1950) was fortnightly applied to avoid the nutrient depletion. Treatment selection and application The majority of metal ions including Cd are more bioavailable at acidic than alkaline pH (Mengel et al., 2001). Most studies on plant responses to Cd have been reported from acidic soils, and data on Cd toxicity effects in alkaline soils are scarce. In view of the alkaline nature of soils in Pakistan, industrial set-up and improper management of effluents, an experiment was performed to determine the toxic levels of Cd for mungbean growth. Seven Cd levels (1, 2.5, 5, 10, 15, 20 and 25 mg kg–1 soil using analytical grade CdCl22.5 H2O in distilled water) were applied to 10-day-old mungbean seedlings grown in soil with pH ;8. Of these, CdCl2 up to a level of 2.5 mg had negligible effect, but there was hardly any plant survival beyond 15 mg kg–1 soil level. Therefore, 3, 6, 9 and 12 mg CdCl2 kg–1 soil were applied to mungbean varieties grown at each of the seedling, vegetative and reproductive stages, at 15, 40 and 60 days after emergence, respectively. Visual symptoms, plant growth and yield determinations The plants were grown for 15 days after treatment application at each growth stage. An additional set of plants treated at 60 days was reserved for determination of pod, seed yield and harvest index (HI) attributes at maturity. For comparative effect of Cd stress on mungbean
Table 1 Estimates (approximate values in percentage of total leaf area) of leaf chlorosis and necrosis as function of Cd toxicity at seedling, vegetative and reproductive growth stages at 15, 40 and 60 days after emergence, respectively. The data have been presented for 0 (no Cd applied) and 12 mg kg–1 level of applied CdCl2 Chlorosis (%) Seedling
Necrosis (%) Vegetative
Reproductive
Seedling
Varieties
0
12
0
12
0
12
0
12
Vegetative 0
12
Reproductive 0
12
NM-13-1 NM-19-19 NM-20-21 NM-28 NM-51 NM-54 NM-88 NM-92 NM-98 Chakwal-97
2.4c 2.5c 2.8c 2.2c 2.5c 2.2c 1.9c 2.0c 1.9c 2.1c
22.5a 17.5b 23.4a 25.6a 18.3ab 17.2b 23.7a 20.5a 15.3b 18.5ab
1.9c 2.1c 2.6c 2.2c 2.2c 2.7c 2.6c 2.4c 1.6c 2.7c
21.0ab 15.5b 23.5ab 28.5a 24.0ab 21.2ab 22.4ab 17.1b 14.5b 20.6b
3.2c 3.2c 3.1c 2.5c 3.6c 3.2c 2.6c 2.9c 2.9c 2.1c
27.5a 16.5b 28.0a 29.5a 25.5a 28.2a 27.1a 22.2ab 19.0ab 24.5a
1.12c 1.31c 1.02c 1.31c 1.12c 1.21c 1.25c 1.24c 1.12c 1.23c
12.5a 7.5b 13.5a 15.2a 8.1b 10.3ab 13.4a 10.2ab 5.5b 8.5b
1.49c 1.04c 1.32c 1.25c 1.14c 1.23c 1.45c 1.23c 1.21c 1.36c
11.4ab 8.5ab 13.5a 16.5a 14.0a 9.5ab 10.2ab 6.3b 5.5b 8.5ab
1.18d 1.25d 1.05d 1.12d 1.24d 1.27d 1.41d 1.26d 1.08d 1.05d
19.5a 9.5c 18.1a 21.5a 15.5ab 19.4a 19.4a 19.2a 10.1c 15.5ab
Means sharing same letter differ non-significantly (P 0.05).
60
Ann Appl Biol 152 (2008) 59–69 ª 2007 The Authors Journal compilation ª 2007 Association of Applied Biologists
Varietal difference for Cd toxicity effects in mungbean
A. Wahid & A. Ghani
12
Seedling stage
0
3
6
9
12
8
4
Shoot dry weight (g plant–1) Vegetative stage
0 12
8
4
0
Reproductive stage
12
8
4
Ch ak w al -9 7
N M -9 8
N M -9 2
N M -8 8
N M -5 4
N M -5 1
N M -1 31 N M -1 919 N M -2 021 N M -2 8
0
Varieties Figure 1 Changes in shoot dry weight of mungbean varieties under increasing levels of Cd treatment at three growth stages. Legends in this and subsequent figures indicate CdCl2 levels in mg kg21 soil.
varieties at each harvest, chlorosis and necrosis of leaves were assessed by measuring chlorosed area and necrotic spots with a Vernier caliper and expressed as percentage of total area. Leaf number on each plant was counted and leaf area was determined by leaf area meter (Model LI3000; LICOR Inc., Lincoln, NE, USA). At harvest, the shoot was excised from its attachment with the root, and roots were carefully removed after flooding the soil. The shoot and root were put in paper envelopes and kept in an oven at 70C for a week and their dry mass determined. At maturity, the number of pods on each plant was counted, seeds extracted from pods and 100-seed weight and seed yield per plant were determined. The above ground dry matter was used to determine the HI as follows: HI (%) = [(Seed yield per plant/ plant dry mass) 100].
Ann Appl Biol 152 (2008) 59–69 ª 2007 The Authors Journal compilation ª 2007 Association of Applied Biologists
Shoot Cd content Dried, powdered samples of shoot (0.5 g) were digested in a mixture of concentrated HNO3 and perchloric acid (3:1 ratio) on a heating block for about 1 h by gradually raising the temperature to 250C, then filtered and the volume made up to 50 mL. The Cd content from the unknown samples was determined using an atomic absorption spectrophotometer (Perkin Elmer Model AAnalyst 3000; Perkin Elmer, Norwalk, CT, USA) and compared with a standard curve. Statistical analysis In the absence of any remarkable difference in various symptomatic and quantitative growth attributes for both the years, the data were averaged to perform analysis of 61
Varietal difference for Cd toxicity effects in mungbean
A. Wahid & A. Ghani
Seedling stage
3.5 0
2.8
3
6
9
12
2.1 1.4 0.7
Root dry weight (g plant-1) Vegetative stage
0 3.5 2.8 2.1 1.4 0.7 0.0
Reproductive stage
3.5 2.8 2.1 1.4 0.7
Ch ak w al -9 7
N M -9 8
N M -9 2
N M -8 8
N M -5 4
N M -5 1
N M -2 8
N M -1 31 N M -1 919 N M -2 021
0.0
Varieties Figure 2 Changes in root dry weight of mungbean varieties under increasing levels of Cd treatment at three growth stages.
variance using COSTAT computer package (COHORT software, Monterey, CA, USA) and to determine significant (P 0.05) differences among mungbean varieties, Cd treatments and their interactions. Regression lines and correlation coefficients were drawn between the degrees of leaf chlorosis and necrosis with shoot Cd content at corresponding growth stages.
Results Visual symptoms of Cd toxicity In addition to the scattered chlorosis on the leaf lamina, interveinal and marginal chlorosis on leaves were well evident. Likewise, scattered necrotic spots on the lamina were noted but to a lesser extent than chlorosis. Although these effects were noted at all Cd levels, the data have been 62
shown as estimated areas at 0 and 12 mg kg–1 Cd level only (Table 1). In control leaves, there was negligible natural chlorosis or necrosis. However, at 12 mg kg–1 CdCl2, both these effects were well evident at seedling and vegetative stages, albeit with greater frequency at the reproductive stage in all varieties. Older, but not the younger leaves, exhibited accelerated senescence in the sensitive varieties. NM-98 in seedling and vegetative stages and NM-19-19 in the reproductive stage showed the lowest foliar chlorosis and necrosis, while NM-28 indicated the greatest foliar chlorosis and necrosis in all stages (Table 1). Plant growth attributes and shoot Cd content Shoot dry mass per plant indicated significant (P 0.01) difference among varieties and Cd levels at all growth
Ann Appl Biol 152 (2008) 59–69 ª 2007 The Authors Journal compilation ª 2007 Association of Applied Biologists
Varietal difference for Cd toxicity effects in mungbean
A. Wahid & A. Ghani
65
Seedling stage
0
3
6
9
12
52 39 26 13 0
Leaf area (cm2 plant-1) Vegetative stage
65 52 39 26 13 0
Reproductive stage
65 52 39 26 13
Ch ak w al -9 7
N M -9 8
N M -9 2
N M -8 8
N M -5 4
N M -5 1
N M -2 8
N M -1 31 N M -1 919 N M -2 021
0
Varieties Figure 3 Changes in leaf area per plant of mungbean varieties under increasing levels of Cd treatment at three growth stages.
stages; however, no interaction of these factors was evident at seedling (P 0.05) but a stronger one was seen (P < 0.01) in the vegetative and reproductive stages. Although increased Cd levels concomitantly decreased shoot dry mass in all the varieties, NM-98 at all stages indicated the least reduction, whereas Chakwal-97 at seedling stage and NM-28 at vegetative and reproductive growth stages presented the greatest reduction in this attribute (Fig. 1). For root dry mass per plant, varieties and Cd levels indicated significant (P 0.01) differences, with an interaction (P < 0.01) of these factors at all growth stages. Although increased Cd levels with remarkable varietal difference reduced this interaction, NM-98 and NM-54 at seedling and NM-98 at vegetative and reproductive stages produced greater root dry matter, while NM-28 during the seedling stage and NM-13-1 and NM-28 both at vegetative and reproductive stages indicated the least root dry matter (Fig. 2). Applied Cd
Ann Appl Biol 152 (2008) 59–69 ª 2007 The Authors Journal compilation ª 2007 Association of Applied Biologists
substantially reduced area of green leaves in all the varieties thus showing significant (P 0.01) differences between varieties, Cd levels and an interaction (P < 0.01) between them at all growth stages. Under Cd stress, NM-98 during seedling and reproductive stages and NM-51 at vegetative stage indicated the least reduction in leaf area, whereas NM-13-1 in seedling stage, NM-54 in vegetative stage and NM-28 in reproductive stage manifested the greatest reduction in leaf area (Fig. 3). Mungbean varieties, Cd treatments and their interactions were significant (P 0.01) at all growth stages for shoot Cd content. All varieties indicated lowest shoot Cd content when no Cd was applied. However, there was a concurrent increase in shoot Cd content under increased CdCl2 levels, the greatest being at 12 mg kg–1. A comparison of varieties indicated that NM-98 during seedling and vegetative stages and NM-19-19 at reproductive stage indicated the lowest Cd accumulation in 63
Varietal difference for Cd toxicity effects in mungbean
A. Wahid & A. Ghani
0
80
3
6
9 12
60 40 20 0 100 80
Reproductive stage
_
Leaf Cd - content (µg g 1 dry weight) Vegetative stage
Seedling stage
100
60 40 20 0 100 80 60 40 20
Ch ak w al -9 7
N M -9 8
N M -9 2
N M -8 8
N M -5 4
N M -5 1
N M -2 8
N M -1 31 N M -1 919 N M -2 021
0
Varieties Figure 4 Changes in shoot Cd content of mungbean varieties under increasing levels of Cd treatment at three growth stages.
the shoot, while NM-28 at all stages indicated the highest Cd accumulation in the shoot (Fig. 4). Economic yield attributes Number of pods per plant revealed significant (P 0.01) differences among mungbean varieties and Cd levels, although there was no interaction (P 0.05) of these factors. Applied Cd treatments produced a gradual reduction in all the varieties; nonetheless, NM-98 produced the highest number of pods per plant, while NM-28 the lowest number of pods per plant (Fig. 5). Number of seeds per pod showed no significant (P 0.05) difference among the varieties, although a significant (P 0.01) difference was evident among Cd levels, while no interaction (P 0.05) of varieties and Cd levels was evident. NM-98 under control or Cd stress indicated the greatest seeds number per pod, but this number was the lowest in 64
NM-28 and NM-51 at the highest Cd level (Fig. 5). Data on 100-seed weight, seed yield per plant and HI revealed significant (P 0.01) differences among varieties and Cd levels, with a significant (P 0.01) interaction of these factors. Applied Cd levels reduced this attribute in all varieties, but a least reduction was recorded in NM-98 and a greatest one in NM-54 and NM-88. Likewise, seed yield per plant under Cd treatments was reduced in all varieties, although NM-19-19 displayed greatest and NM-54 lowest values compared with other varieties. Data revealed substantial differences in the varieties for HI under Cd stress; nonetheless, NM-98 excelled above the other varieties by showing greatest HI (Fig. 5). Trend lines and correlations Trend lines set between foliar toxicity symptoms and plant dry weight at three growth stages displayed no
Ann Appl Biol 152 (2008) 59–69 ª 2007 The Authors Journal compilation ª 2007 Association of Applied Biologists
Varietal difference for Cd toxicity effects in mungbean
Seed yield (g plant-1)
100 seed weight (g)
Number of seeds per pod
Number of pods per plant
A. Wahid & A. Ghani
15 0
12
3
6
9
12
9 6 3 0
12 9 6 3 0 8 6 4 2 0 8 6 4 2 0
Harvest index ( )
60 45 30 15
Ch ak w al -9 7
N M -9 8
N M -9 2
N M -8 8
N M -5 4
N M -5 1
N M -2 8
N M -1 31 N M -1 919 N M -2 021
0
Varieties Figure 5 Changes in pod, seed yield and harvest index characteristics of mungbean varieties upon exposure to increasing Cd levels at maturity.
relationships under control (data not shown), but negative ones at the highest level (12 mg kg–1) of CdCl2 applied (Fig. 6). Slope of the regression equations and correlation of shoot Cd content at the highest Cd level were positive and tighter for chlorosis than necrosis at all
Ann Appl Biol 152 (2008) 59–69 ª 2007 The Authors Journal compilation ª 2007 Association of Applied Biologists
stages (Fig. 7). At maturity, no correlations was noted between foliar chlorosis and necrosis at reproductive stage and number of pods per plant and seeds per pod, while these correlations were negative with 100-seed weight, seed yield per plant and HI (Fig. 8). 65
Varietal difference for Cd toxicity effects in mungbean
A. Wahid & A. Ghani
Foliar chlorosis ( )
Foliar necrosis ( )
30
16
Seedling stage
25 12 20 15
8
10 4
y = -8.71x+29.39 r = -0.910**
5 0
y = -6.90x+17.74 r = -0.864**
0 0
1
2
3
0
1
2
3
16
30
Vegetative stage
25 12 20 8
15 10
4
y = -5.53x + 37.16 r = -0.907**
5 0
0 0
2
4
6
8
35
Reproductive stage
y = -4.25x + 22.96 r = -0.876** 0
2
4
6
8
24
28
18
21 12 14 6
y = -4.91x+50.66 r = -0.911**
7 0
y = -3.30x + 34.06 r = -0.805**
0 0
4
8
12
Plant dry matter (g plant-1)
16
0
4
8
12
16
Plant dry matter (g plant-1)
Figure 6 Regressions and relationships of foliar chlorosis and necrosis of mungbean varieties with plant dry weight Cd stress applied at three growth stages. Correlation coefficient significant at **P 0.01.
Discussion Earlier reports showed that mungbean was sensitive to increased Cd levels (Chaoui et al., 1997), and major effects were reductions in shoot and root growth and their dry mass (Rout et al., 1999). Root being the first target of Cd toxicity exhibits considerable changes at histological and molecular levels (Hernandez & Cook, 1997; Suzuki, 2005). Therefore, tolerance at root level is likely to determine the Cd accumulation in the shoot. Despite substantial varietal differences at all the stages, increased Cd accumulation in the shoot was detrimental as evident from more tangible symptoms of Cd toxicity (Table 1),
66
gradual reductions in the dry weight of shoot (Fig. 1) and root (Fig. 2) as well as reducing the available leaf area (Fig. 3). The changes in plant growth attributes as a result of Cd stress were because of enhanced shoot Cd content (Fig. 4). It was noteworthy that greater Cd toxicity at reproductive stage was more crucial to seed yield attributes as a substantial reduction in the HI was evident (Fig. 5). Although Cd-induced foliar chlorosis and necrosis have been reported in certain plant species including radish (Khan & Frankland, 1983) and pea (Hernandez & Cooke, 1997) and leaf chlorosis in oilseed rape (Baryla et al., 2001) and rice (Adhikari et al., 2006), no previous study reports such effects in mungbean. In
Ann Appl Biol 152 (2008) 59–69 ª 2007 The Authors Journal compilation ª 2007 Association of Applied Biologists
Varietal difference for Cd toxicity effects in mungbean
A. Wahid & A. Ghani
Foliar chlorosis ( )
Foliar necrosis ( )
30
16
Seedling stage
25 12 20 8
15 10
y = 0.68x - 22.54 r = 0.895**
5
4
0
0
30
16
y = 0.56x - 24.73 r = 0.803**
Vegetative stage
25 12 20 15
8
10
y = 0.58x - 15.26 r = 0.910**
Reproductive stage
5
4
0
0
35
24
28
y = 0.41x - 15.15 r = 0.780**
18
21 12 14 y = 0.60x - 16.03 r = 0.848**
7
y = 0.53x- 19.21 r = 0.782**
6
0
0 40
50
60
70
Shoot Cd (µg g-1 dry weight)
80
40
50
60
70
80
Shoot Cd (µg g-1 dry weight)
Figure 7 Regressions and relationships of foliar chlorosis and necrosis of mungbean varieties with shoot Cd content at 12 mg CdCl2 kg–1 soil applied at three growth stages. Correlation coefficient significant at **P 0.01.
this species, foliar chlorosis and necrosis were recorded at all stages, but with greater frequency at reproductive stage (Table 1). Such effects may result from the reduced uptake of essential nutrients and toxicity of metal ions accumulated in various plant parts (Zhang et al., 2002; Adhikari et al., 2006). The extent of changes in growth attributes and incidence of visual effects of Cd damage revealed the existence of great varietal differences throughout the mungbean ontogeny for Cd tolerance. Slope of regression equation and correlation coefficient were tighter with chlorosis than with necrosis, although negative with plant dry weight (Fig. 6) and with shoot Cd content (Fig. 7). These visual effects of Cd damage at all stages were largely similar to the deficiency of essential
Ann Appl Biol 152 (2008) 59–69 ª 2007 The Authors Journal compilation ª 2007 Association of Applied Biologists
nutrients including K, Mg, Mn and Fe (Epstein & Bloom, 2005; Ghnaya et al., 2007). This is plausible in view of the fact that all these elements are either structurally or functionally involved in chlorophyll biosynthesis and its activity. Hence, loss and/or reduced biosynthesis of chlorophyll in response to Cd stress are the determinants of growth, biomass and seed yield throughout the mungbean ontogeny. The majority of varieties indicated enhanced sensitivity to Cd stress as a result of greater accumulation of Cd in the shoot at reproductive stage, which had great implications for economic yield attributes. Determinations made on the pod and seed yield contributing factors at maturity revealed a pronounced reduction in 100-seed weight, seed 67
Number of pods per plant
10.0
0.0
0.0
Number of seeds per pod
Varietal difference for Cd toxicity effects in mungbean
10.0
10.0
7.5
7.5
10.0
7.5
7.5 5.0
5.0 y = -0.02x + 7.79 r = -0.129ns
2.5
5.0
5.0
y = -0.02x + 7.79 r = -0.129ns
2.5
100 seed weight (g) Seed yield (g plant -1)
y = -0.01x + 7.33 r = -0.256ns
2.5
0.0
0.0
8.0
Harvest index ( )
y = -0.02x + 7.67 r = -0.276ns
2.5
8.0 y = -0.19x + 8.47 r = -0.858**
6.0
y = -0.17x + 6.71 r = -0.750*
6.0
weight, seed yield and HI with foliar chlorosis and necrosis at maturity (Fig. 8) has specific implications towards final productivity. Taking together the reductions in growth attributes at reproductive stage, seed yield and HI data at maturity and symptomatic data, it was evident that despite sporadic necrosis spots, foliar chlorosis between the veins was critical. This is important because the Cd appeared to mainly damage the mesophyll tissue between the veins. Such effects reduce the production and phloem loading of photosynthates for their partitioning to the seed during filling, leading to reduced seed yield and HI. In crux, despite substantial genetic variability for tolerance, the damaging effects of Cd on growth and yield of mungbean were intricate, which might involve the deficiencies of essential nutrients, leading to reduced mesophyll area for leaf gas exchanges and photoassimilate partitioning to seed during filling. Findings of this study are important with respect to selection and cultivation of relatively Cd-tolerant mungbean varieties in moderately Cd-polluted soils.
4.0
4.0
2.0
2.0
References
0.0
0.0
Adhikari T., Tel-Or E., Libal Y., Shenker M. (2006) Effect of cadmium and iron on rice (Oryza sativa L.) plant in chelatorbuffered nutrient solution. Journal of Plant Nutrition, 29, 1919–1940. Ahmad S., Wahid A., Rasul E., Wahid A. (2005) Comparative morphological and physiological responses of green gram genotypes to salinity applied at different growth stages. Botanical Bulletin of Academia Sinica, 46, 135–142. Astolfi S., Zuchi S., Passera C. (2005) Effect of cadmium on H+-ATPase activity of plasma membrane vesicles isolated from roots of different S-supplied maize (Zea mays L.) plants. Plant Science, 169, 361–368. Balakhnina T., Kosobryukhov A., Ivanov A., Kreslavskii V. (2005) The effect of cadmium on CO2 exchange, variable fluorescence of chlorophyll, and the level of antioxidant enzymes in pea leaves. Russian Journal of Plant Physiology, 52, 15–20. Baryla A., Carrier P., Franck F., Coulomb C., Sahut C., Havaux M. (2001) Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. Planta, 212, 696–709. Benavides M.P., Gallego S.M., Tomaro M.L. (2005) Cadmium toxicity in plants. Brazilian Journal of Plant Physiology, 17, 49–55. Bindhu S.J., Bera A.K. (2001) Impact of cadmium toxicity on leaf area, stomatal frequency, stomatal index and pigment content in mungbean seedlings. Journal of Environmental Biology, 22, 307–309.
4.0
4.0 y = -0.12x + 4.82 r = -0.807**
3.0 2.0
2.0
1.0
1.0
0.0
0.0
40.0
40.0
30.0
30.0
20.0
20.0 y = -0.84x + 46.86 r = -0.838**
10.0
y = -0.11x + 3.82 r = -0.833**
3.0
y = -0.74x + 38.42 r = -0.705*
10.0
0.0
0.0 10
20
30
Chlorosis ( )
40
0
5
10 15 20 25
Necrosis ( )
Figure 8 Regression and relationships of foliar chlorosis and necrosis, some pod, seed yield and harvest index attributes. Correlation coefficient significant at *P 0.05; **P 0.01 and n.s., non-significant.
yield per plant and HI (Fig. 5). Such reductions are assignable to hampered rate of photosynthesis and partitioning of photoassimilates to seed during filling because of Cd (Bindhu & Bera, 2001; Balakhnina et al., 2005; Wahid et al., 2007). Inverse relationships of 100-seed 68
A. Wahid & A. Ghani
Ann Appl Biol 152 (2008) 59–69 ª 2007 The Authors Journal compilation ª 2007 Association of Applied Biologists
A. Wahid & A. Ghani
Chaoui A., Ghorbal M.H., El-Ferjani E. (1997) Effects of cadmium-zinc interactions on hydroponically grown bean (Phaseolus vulgaris L.). Plant Science, 126, 21–28. Chugh L.K., Sawhney S.K. (1999) Photosynthetic activities of Pisum sativum seedlings grown in presence of cadmium. Plant Physiology and Biochemistry, 37, 297–303. Epstein E., Bloom A.J. (2005) Mineral Nutrition of Plants: Principles and Perspectives. 2nd edn. MA, USA: Sinauer Associates Inc. Ghani A., Wahid A. (2007) Varietal difference for cadmiuminduced seedling mortality and foliar-toxicity symptoms in mungbean (Vigna radiata). International Journal of Agriculture and Biology, 9, 555–558. Ghnaya T., Slama I., Messedi D., Grignon C., Ghorbel M.H., Abdelly C. (2007) Effects of Cd2+ on K+, Ca2+ and N uptake in two halophytes Sesuvium portulacastrum and Mesembryanthemum crystallinum: consequences on growth. Chemosphere, 67, 72–79. Gomes-Junior R.A., Moldes C.A., Delite F.S., Pompeu G.B., Grata˜o P.L., Mazzafera P., Lea P.J., Azevedo R.A. (2006) Antioxidant metabolism of coffee cell suspension cultures in response to cadmium. Chemosphere, 65, 1330–1337. Grata˜o P.L., Polle A., Lea P.J., Azevedo R.A. (2005) Making the life of heavy metal-stressed plants a little easier. Functional Plant Biology, 32, 481–494. He J., Zhu C., Ren Y., Yan Y., Jiang D. (2006) Genotypic variation in grain cadmium concentration of lowland rice. Journal of Plant Nutrition and Soil Science, 169, 711–716. Hernandez L.E., Cooke D.T. (1997) Modification of the roots plasma membrane lipid composition of cadmium treated Pisum sativum. Journal of Experimental Botany, 48, 1375–1381. Hoagland D.R., Arnon D.I. (1950) The water-culture method for growing plants without soil. Circular 347. Berkeley, CA, USA: University of. California, The College of Agriculture. Jamali M.K., Kazi T.G., Arain M.B., Afridi H.I., Jalbani N., Memon A.R. (2007) Heavy metal contents of vegetables grown in soil, irrigated with mixtures of wastewater and sewage sludge in Pakistan, using ultrasonic-assisted pseudo-digestion. Journal of Agronomy and Crop Science, 193, 218–228. Keeling S.M., Stewart R.B., Anderson C.W.N., Robinson B.H. (2003) Nickel and cobalt phytoextraction by the hyperaccumulator Berkheya coddii: implications for polymetallic phytomining and phytoremediation. International Journal of Phytoremediation, 5, 235–244. Khan D.H., Frankland B. (1983) Effects of cadmium and lead on radish plant with particular reference to move-
Ann Appl Biol 152 (2008) 59–69 ª 2007 The Authors Journal compilation ª 2007 Association of Applied Biologists
Varietal difference for Cd toxicity effects in mungbean
ment of metals through soil profile and plant. Plant and Soil, 70, 335–345. Lea P.J., Sodek L., Parry M.A.J., Shewry P.R., Halford N.G. (2007) Asparagine in plants. Annals of Applied Biology, 150, 1–26. Mengel K., Kirkby E.A., Kosegarten H., Appel T. (2001) Principles of Plant Nutrition. 5th edn. Heidelberg, Germany: Springer. Metwally A., Safronova V.I., Bellimov A.A., Dietz K.-J. (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. Journal of Experimental Botany, 56, 167–178. Nazir M.S. (1994) Crop Production. Islamabad, Pakistan: National Book Foundation. Pal M., Horvath E., Janda T., Paldi E., Szalai G. (2006) Physiological changes and defence mechanisms induced by cadmium stress in maize. Journal of Plant Nutrition and Soil Science, 169, 239–246. Rout G.R., Samantaray S., Das P. (1999) Differential cadmium tolerance of mungbean and rice genotypes in hydroponic culture. Acta Agriculturae Scandinavica, 49, 234–241. Saleemi M.A. (1998) Environmental Assessment and Management of Irrigation and Drainage Scheme for Sustainable Agriculture Growth. Lahore, Pakistan: Environmental Protection Agency. Suzuki N. (2005) Alleviation by calcium of cadmium-induced root growth inhibition in Arabidopsis seedlings. Plant Biotechnology, 22, 19–25. Wahid A., Masood I., Javed I-ul-H., Rasul E. (1999) Phenotypic flexibility as marker of sodium chloride tolerance in sunflower genotypes. Environmental and Experimental Botany, 42, 85–94. Wahid A., Ghani A., Ali I., Ashraf M.Y. (2007) Effects of cadmium on carbon and nitrogen assimilation in shoots of mungbean [Vigna radiata (L.) Wilczek] seedlings. Journal of Agronomy and Crop Science, 193, 357–365. Wang M.-E., Zhou Q.-X. (2006) Joint stress of chlorimuronethyl and cadmium on wheat Triticum aestivum at biochemical levels. Environmental Pollution, 144, 572–580. Wu F., Wu H., Zhang G., Bachir D.M.L. (2004) Differences in growth and yield in response to cadmium toxicity in cotton genotypes. Journal of Plant Nutrition and Soil Science, 167, 85–90. Zhang G., Fukami M., Sekimoto H. (2002) Influence of cadmium on mineral concentration and yield components in wheat genotypes differing in Cd tolerance at seedling stage. Field Crops Research, 77, 93–98.
69
