Toxicity of arsenic on germination and seedling growth of rice

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affected the seed germination and various growth parameters e.g. seedling height, ... reported that As depressed the radicle growth in rice and arsenite is more ...
J. Bangladesh Soc. Agric. Sci. Technol., 4(1&2): 153 - 156, 2007

ISSN 1811-6221

Toxicity of arsenic on germination and seedling growth of rice M.A. Hossain, M.N. Uddin and A.K.M.G. Sarwar Department of Crop Botany, Bangladesh Agricultural University, Mymensingh Abstract The study examined the effect of arsenic (As) on the germination and seedling growth of rice. Eight different concentrations of As viz., 0.0 (control), 0.5, 1.0, 2.0, 4.0, 6.0, 8.0 and 10.0 mg As L-1 were tested on 5 rice varieties viz., BR11, BRRI dhan30, BRRI dhan3l, BRRI dhan34 and BRRI dhan37. Arsenic contaminated water adversely affected the seed germination and various growth parameters e.g. seedling height, number of leaves seedling-1, length of primary leaf, length of coleoptile, number of roots seedling-1, average root length, and total dry matter of 10-day old seedlings. Germination and seedling growth of the rice varieties suffered at different magnitude in response to the added As supplied as solution during germination. Water containing 10 mg As L-1 had full inhibitory effect on the germination of seeds in all studied rice varieties. Whereas 8 mg As L-1 caused germination reduction by 5.5% (93.93% reduction over control) compared to 90.6% in control. The total dry matter yield of 10day old seedlings varied between 1.02 to 11.66 mg seedling-1 in the 0 to 8.0 mg As L-1. Therefore, appropriate precautionary measures should be taken during raising of rice seedling in the arsenic affected areas of Bangladesh. Tolerance to As at the germination and seedling stage might be used as a selection criterion for As tolerant varieties. Keywords: Arsenic, rice, germination, seedling growth Introduction Arsenic is one of the most serious global environmental toxicants. Groundwater contamination by arsenic (As) has been reported from many parts of Bangladesh and the country is currently facing the challenge of high As concentrations in shallow aquifers (Nickson et al., 1998). In some areas of Bangladesh, the ground water As contaminations reach 2 mg As L-1 which is higher than the recommended maximum concentration of As (0.1 mg As L-1) in irrigation water (Tondel et al., 1999). Background levels of As in soils can be between 4 - 8 mg As kg-1 but in the areas irrigated with As contaminated water, the soil level can reach up to 83 mg As kg-1 (Ullah, 1998). Rice (Oryza sativa L.) is the staple food and the main agricultural crop of Bangladesh. In Bangladesh, 70% of the total cropped area and 82% of the irrigated area are used for rice cultivation (BBS 2002). Groundwater is the primary source of irrigation water especially in the dry seasons. The production of rice is dependent involuntarily on As contaminated irrigation water, which explain the importance of As issue in rice. All activities related with rice cultivation such as germination, raising of seedlings, transplanting and growing rice in main field are mostly done by ground water irrigation. Plants can develop the toxicity symptoms while they are exposed to excess As either in soil or in solution culture such as, inhibition of seed germination, reduction in root and shoot growths, decrease in plant height and tiller number, and reduction of grain yield (Abedin et al., 2002; Jahiruddin et al., 2004; Liu et al., 2005; Uddin et al., 2005). However, only a little information about the effect of As on seed germination and seedling growth of rice is available (Tsutsumi, 1983). Tsutsumi (1983) reported that As depressed the radicle growth in rice and arsenite is more toxic than arsenate. Therefore, a laboratory experiment was carried out to evaluate the effects of different concentration of As in irrigation water on the germination and seedling growth of rice. Materials and Methods The laboratory experiment was conducted at the Department of Crop Botany, Bangladesh Agricultural University, Mymensingh. Eight different concentrations of arsenic viz., 0 (control), 0.5, 1.0, 2.0, 4.0, 6.0, 8.0 and 10.0 mg As L-1 were evaluated on seed germination and seedling growth of 5 rice varieties viz., BR11, BRRI dhan30, BRRI dhan3l, BRRI dhan34 and BRRI dhan37. Arsenic was supplied as a solution of Na2HAsO4.7H2O. The highest As treatment (10.0 mg As L-1) of this study was much higher than the reported maximum level of As (2.0 mg As L-1) in irrigation water of Bangladesh. All the seeds of the respective varieties were surface sterilized by soaking them in 1% NaOCl for one minute followed by rinsing with deionized water. Germination of seeds was tested on moist filter paper (Whatman No.1). Two filter papers were placed on each of 15.0 cm diameter Petri dishes. Each Petri dish was then moistened with 10 mL of respective As solution. Fifty sterilized seeds of each variety were laid on filter paper bed in each Petri dish. Each dish was then covered

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by a lid, and incubated at room temperature (28° - 32°C). Each treatment was replicated three times following randomized complete design (CRD). The seeds were allowed to germinate and grow for 10 days. During this period the Petri dishes were moistened by respective solutions of As when needed. Lids of all the dishes were removed during plumule growth. Data were recorded from 10-day old seedlings on germination, seedling height, number of leaves seedling-1, length of primary leaf, length of coleoptile, number of roots seedling-1, average root length, and total dry matter seedling-1. Experimental data were analyzed statistically by using MStat-C computer package following ANOVA technique and the means were separated by Duncan's New Multiple Range Test. Results Seed germination Arsenic contaminated water had a marked effect on germination of the rice seeds (Table 1 and Fig. 1A). The results showed that the % seed germination over control decreased significantly with the increasing As concentration. The germination varied between 5.5 to 90.6% in 0 to 8.0 mg As L-1 treatment. Germination of seeds were totally failed in 10 mg As L-1 solution of all the varieties studied and seeds of BRRI dhan3l and BRRI dhan37 did not germinate even at 8 mg As L-1 solution.. The highest (90.6 %) germination was recorded in control treatment and lowest (5.5%) in 8 mg As L-I solution. Germination decreased by 15.45, 25.39, 35.54, 56.51, 75.5 and 93.93 % over control in 0.5, 1.0, 2.0, 4.0, 6.0 and 8.0 mg As L-1 treatment, respectively. BRRI dhan34 showed the higher and BRRI dhan30 showed the lower % germination in most As treatment (Fig. 1A). Seedling growth parameters The means of different growth parameters viz., seedling height, number of leaf seedlling-1, length of primary leaf, length of coleoptile, number of root seedling-1, root length and total dry matter seedling-1 were significantly influenced by different As treatments (Table 1). The maximum seedling height (8.88 cm) was recorded in control treatment and the minimum (1.08 cm) in 8 mg As L-1 treatment. There were significant varietals differences in seedling height (Fig. 1B). BR11 produced taller seedlings at lower concentrations of As solution (0 to 4 mg As L-1), while BRRI dhan30 produced the taller seedlings at higher concentrations (6 to 8 mg As L-1) and BRRI dhan34 produced shorter seedlings at all concentrations of As. The number of leaves seedling-1 varied from 1.0 to 3.0 in the 0 to 8.0 mg As L-1 treatment, however, no significant differences were experienced up to 1.0 mg As L-1 treatment. The treatment of As between 2.0 to 6.0 mg As L-1 produced statistically similar number of leaves seedling-1. The length of primary leaf varied between 0.28 to 1.33 cm in the As treatment. The length of primary leaf progressively shortened with increasing concentration of As from 2.0 to 8.0 mg As L-1. The length of coleoptile was also affected by As almost in the similar way as primary leaf. The highest number of root seedling-1 (4.6) was recorded in control (0 mg As L-1) which was statistically identical with that of 0.5 mg As L-1. The lowest number of root seedling-1 (0.6) was traced in 8.0 mg As L-1. Up to 4.0 mg As L-1, the variety BRRI dhan31 produced the highest number of root seedling-1 (Fig. 1C). On the contrary, BRRI dhan30 produced the lowest number of roots in all As treatments. The treatment receiving no As produced the highest root length (2.44 cm), while the lowest root length (0.21 cm) was observed in 8.0 mg As L-1. The total dry matter seedling-1 was found to be strongly affected by the concentration of As in water. Total dry matter decreased significantly with increasing As concentration (Table 1). The range of total dry matter seedling-1 due to As contamination varied from 1.02 to 11.66 mg seedling-1. Arsenic contaminated water accounted for the reduction of dry matter seedling-1 by 19.04, 36.88, 44.94, 66.04, 76.67 and 91.25 % in 0.5, 1.0, 2.0, 4.0, 6.0 and 8.0 mg As L-1 treatments, respectively over control. Total dry matter production also varied among the varieties (Fig. 1D). BR11 and BRRI dhan31 produced the highest and the lowest total dry matter contents seedling-1, respectively. Neither BRRI dhan31 nor BRRI dhan37 produced any dry mass in 10 mg As L-1 as germination of these two varieties failed in this treatment. Discussion The germination of rice seed decreased significantly with the higher concentrations of As in water and the adverse effect was different among the varieties. The lower percentage of seed germination corroborates with the result of Liu et al. (2005) who reported reduced germination in wheat seed with increasing concentration of As. Sodium arsenate (Na2HAsO4.7H2O) was found as a potent inhibitor of mungbean seed germination and seedling growth. Germination of mungbean was totally inhibited at or above 50 µM Na2HAsO4.7H2O, while inhibition of seedling elongation started at a lower concentration of 5 µM As(V) and was drastically reduced at 20 µM As(V) (Swarnakar & Mukherji, 2005). In our study we found that water with 10 mg As L-1 had full lethal effect on germination of seeds in all rice varieties and 8 mg As L-1 also showed lethal action on some rice

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Table1. Effect of arsenic (As) contaminated irrigation water on germination and seedling growth of rice Arsenic Germinaadded tion (mg As L-1) ( %) 0.0 90.6a 0.5 76.6b 1.0 67.6c 2.0 58.4d 4.0 39.4e 6.0 22.2f 8.0 5.5g 7.70 LSD(0.05)

Reduction in germiation (%) 0 15.45 25.39 35.54 56.51 75.50 93.93 --

Seedling height (cm) 8.88a 7.86b 6.86c 5.06d 3.80e 2.92f 1.08g 0.70

Leaf number seedling-1 3.0a 3.0a 2.8a 2.4ab 2.0b 1.8b 1.0c 0.77

Length of primary leaf (cm) 1.33a 1.28a 1.21ab 1.06b 0.84c 0.57d 0.28e 0.19

Length of Root Root Total dry Reduction coleoptile number length matter in total dry seedling1(mg) matter (%) (cm) seedling-1 (cm) 0.48a 4.6a 2.44a 11.66a 0 0.44ab 4.1ab 1.47b 9.44b 19.04 0.40b 3.8b 1.03c 7.36c 36.88 0.36b 3.0c 0. 81cd 6.42d 44.94 0.28c 2.0d 0.56de 3.96e 66.04 0.22c 1.1 e 0.26ef 2.72f 76.67 0.11 d 0.6e 0.21f 1.02g 91.25 0.08 0.57 0.31 0.93 --

In a column, the means having common letter(s) do not differ significantly at 5% level by DMRT.

Figure 1. Effect of different concentrations of arsenic on percent seed germination (A), seedling height (B), root numbers seedling-1 (C) and total dry matter seedling-1 (D).

varieties (Fig. 1A). Arsenic acts as a metabolic inhibitor. Once inside the cytoplasm it competes with phosphate, for example replacing phosphate in ATP which leads to disruption of energy flow in cells (Meharg, 1994). Arsenic is also toxic to plants as it reacts with enzymes and tissue proteins. Seed germination is energy (ATP) depending process and during germination many enzymes are critically involved to transform complex seed storage into simpler form and translocate them in growing region of seedlings (Meharg, 1994). So, higher As concentration might be associated with disruption of enzymatic activity and energy synthesis of seeds which eventually accounted for the death of seed tissues and inhibition of seed germination. Rice seeds subjected to higher concentrations of As reduced the seedling height. Reduced shoot growth in rice due to application of arsenate had been reported by Abedin et al. (2002) and Marin et al. (1992). Abedin et al. (2002) reported that plant height ranged between 91.1 and 84.1 cm with lower ranges of arsenate doses (0-1.0 mg As L-1), while with higher arsenate doses (2.0 - 8.0 mg of As L-1) plant height decreased to 79.2 - 63.8 cm. Leaf number plant-1 was less affected by As in water. Similar to germination of seeds, the adverse effect of As on seedling height was different among the varieties (Fig. 1B).

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Rice root development was also affected by the As containing irrigation water. The treatment receiving 0.5 mg As L-1 produced significantly lower root length compared to that of control treatment whereas no significant differences in root number were found in the same concentration. The reduction in root biomass was more pronounced in higher arsenate content (Abedin et al., 2002). Tsutsumi (1983) observed that the radicle growth was almost entirely suppressed by arsenite at 10-4.0 M. It might be due to induction of phytotoxicity by As which resulted in restricted root growth. The adverse effect of As on number of roots plant-1 was also different among the varieties (Fig. 1C). Marin et al. (1992) also reported a differential response in rice root dry matter production between two rice varieties, Lemont and Mercury, when treated with different concentrations of arsenite and arsenate in hydrophonic culture. Considerable reduction in total dry matter in the highest arsenate treatment recorded in this experiment may be primarily as a result of stunted seedling height, reduced root number and root length, and reduced number of leaf seedling-1 (Table 1). Exposure to arsenic, causing a reduction in shoot biomass and/ or growth, was also reported by Tsutsumi (1983) for rice. Therefore, appropriate precautionary measures like use of surface water or As free irrigation water, tolerant varieties etc., should be taken during raising of rice seedling in the arsenic affected areas of Bangladesh. Tolerance to As at germination and seedling stages might be used as a selection criterion for As tolerant varieties. References Abedin, M.J., Cresser, M.S., Nlehar, A.A., Feldmann, J. and Cotter-Howells, J. 2002. Arsenic accumulation and metabolism in rice (Oryza sativa L.). Environ. Sci. Technol., 36:962-968. BBS (Bangladesh Bureau of Statistics) 2002. Statistical Pocket Book of Bangladesh 2000. Statistics Division, Ministry of Planning. Govt. of the People's Republic of Bangladesh. pp. 192-202. Jahiruddin, M., Islam, M.A., Islam, M.R. and Islam, S. 2004. Effects of arsenic contamination on rice crop (Oryza sativa). J. Environtropica, 1(2): 104-110. Liu, X., Zhang, S., Shan, X. and Zhu., Y. 2005. Toxicity of arsenate and arsenite on germination, seedling growth and amylolytic activity of wheat. Chemosphere, 61(2): 293-301. Marin, A.R., Masscheleyn, P.H. and Patrick, W.H.Jr. 1992. The influence of chemical form and concentration of arsenic on rice growth and tissue arsenic concentration. Plant Soil, 139:175-183. Meharg, A.A. 1994. Integrated tolerance mechamisms-constitutive and adaptive plant-responses to elevated metal concentrations in the environment. Plant Cell & Environ., 17: 989-993. Nickson, R., McArthur, J., Burgess, W., Ahmed, K.M., Raven-scroft, P. and Rahman, M. 1998. Arsenic poisoning in Bangladesh groundwater. Nature, 395: 338-338. Swarnakar, A. and Mukherji, S. 2005. Amelioration of arsenic toxicity by phosphate salts in mungbean seedlings. J. Environ. Biol., 26 (3): 551-555. Tondel, M., Rahman, M., Magnuson, A., Chowdhury, I.A., Faruquee, M.H. and Ahmad, S.A. 1999. The relationship of arsenic levels in drinking water and the prevalence rate of skin lesions in Bangladesh. Environ. Health Perspect, 107: 727-729. Tsutsumi, M. 1983. Comparative toxicity of arsenite and arsenate to the rice seedling under various levels of phosphate supply. Soil Sci. Plant Nutr., 29: 63-69. Uddin, M.N., Karim, M.A. and Zaman, M.W. 2005. Arsenic stress on the performance of T. aman rice. Crop Sci., 16(2): 327-332. Ullah, S.M. 1998. Arsenic contamination of groundwater and irrigated soils of Bangladesh. In Abstracts: International Conference on arsenic pollution of groundwater in Bangladesh: causes, effects and remedies. 8-12 February. 1998. Dhaka Community Hospital, Dhaka. Bangladesh. p. 133.