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Journal of soil science and plant nutrition

versión On-line ISSN 0718-9516

J. Soil Sci. Plant Nutr. vol.12 no.4 Temuco dic. 2012  Epub 21-Ene-2012 

Journal of Soil Science and Plant Nutrition, 2012, 12 (4), 775- 784


Influence of phosphorus on the arsenic uptake by tomato (Solanum lycopersicum L) irrigated with arsenic solutions at four different concentrations


M. Pigna1, A.G. Caporale1, V. Cozzolino1, C. Fernández López2, M.L. Mora3, A. Sommella1 and A. Violante1*

1Dipartimento di Scienze del Suolo, della Pianta, dell'Ambiente e delle Produzioni Animali, Università degli Studi di Napoli Federico II, Portici, Italy.*Corresponding author: 2Cátedra de Edafología. Facultad de Ciencias Agrarias. Universidad Nacional del Nordeste. Sargento Cabral 2131. Corrientes. Argentina. 3Departamento de Ciencias Químicas y Recursos Naturales, and Scientific and Technological Bioresource Nucleus (BIOREN-UFRO), Universidad de La Frontera, Temuco, Chile.



We have studied the uptake and distribution of arsenic (As) and phosphorus (P) in roots, shoots and berries of tomato plants, grown on uncontaminated soil, irrigated with As-contaminated solutions at four concentrations (0, 0.5, 2 and 4 mg L-1), in presence or absence of P fertilization.

The biomass of tomato plants decreased with increasing As concentration in irrigation water, especially tomato berries. In addition, the reduction of biomasses was significantly greater in plants non-fertilized with P. The beneficial effect generated with the P addition indicated that this nutrient played an important role in alleviating As toxicity in tomato plants. The higher the As concentration in irrigation water the higher the As concentration in plant tissues; most of the As absorbed by plants was accumulated in their roots. Phosphorus application has allowed to reduce As translocation toward tomato berries, enhancing plant P status. These observations may be useful for certain areas of the World, in which As-contaminated waters are used for agricultural purposes.

Keywords: tomato, arsenic, uptake, phosphorus fertilization, contamination.

1. Introduction

Arsenic (As) is a carcinogenic metalloid ubiquitous in the environment, because of natural processes as well as anthropogenic activities, such as mining, smelting, pesticide application, which have contributed to increase the As concentration in soils and groundwaters of many areas around the World (Smith et al., 1998; Naidu et al., 2006; Lu et al., 2010). The As concentrations found in natural water bodies range from less than 0.5 mg L-1 to more than 5000 mg L-1 (Mandal and Suzuki, 2002). High As concentrations in ground-waters have been found in Argentina, Chile, Mexico, China, Hungary, West Bengal (India), Bangladesh and Vietnam (Smith et al., 1998). The latest estimates suggested that 30-35 and 6 million people in Bangladesh and West Bengal, respectively, are exposed to high level (more than 50 mg L-1) of As in their drinking waters (Chakrabarti et al, 2002; Mandal and Suzuky, 2002). In some areas of Italy hazardous As concentrations in groundwaters, higher than the recommended threshold (10 mg L-1) set by the World Health Organization (WHO, 2004), have been found. For example, more than 50 mg L-1 has been identified in many groundwaters of Lazio (an Italian region), where 91 towns and villages (among Rome, Viterbo and Latina provinces) with more than 250.000 people are at serious risk.

It is becoming evident that ingestion of drinking water is not the only elevated source ofAs to the human diet. Long-term use of As-contaminated waters for irrigation has resulted in elevated As level in agricultural soils (Meharg and Rahman, 2003; Roychowdhury et al., 2005; Williams et al, 2005). To evaluate the possible health risk to humans consuming crops irrigated with As-contaminated waters, information is needed regarding the soil-to-plant transportation of As and to minimize the accumulation of As in plants consumed directly by humans, farm animals or wildlife (Meharg and Hartley-Whitaker, 2002; Pigna et al, 2010). Apart from the health risk, the presence of As in irrigation water or in soil at an elevated level could hamper normal growth of plants with toxicity symptoms such as biomass reduction (Carbonell-Barrachina et al, 1997) and yield losses (Jiang and Singh, 1994).

It is well known that chemical behaviour of arsenate (AsO4) is similar to that of phosphate (PO4). Arsenate can act as a PO4 analogue with respect to transport across root plasma membrane, with PO4 competing much more effectively for transport sites (Meharg, 1994). The effect of PO4 on the sorption/ desorption processes of As in soil environments has received great attention, being PO4 commonly added as crop fertilizer. Many authors showed that AsO4 may be only partially removed from soil colloids by PO4, even if large amounts of PO4 are applied (Smith et al., 1998; Frankenberger, 2002; Violante and Pigna, 2002). Plant uptake of As has been shown to increase upon P application in pot experiments (Jiang and Singh, 1994) and at field scale (Small and McCants, 1962). Peryea (1998) reported increased As solubility and phytoavailability on P-fertilizer application to soils. On the contrary, application of PO4 was reported to decrease bioavailability of As in soils by Hanada et al. (1975). However, further investigations on the influence of P application to As-contaminated systems, in which food plants are grown, are still necessary (Pigna et al., 2010).

In Italy, tomato is one of the most cultivated food plant (more than 70,000 ha for year). The production amounted to 4,900,000 tons of tomatoes for processing (43.7 % in Northern Italy, 7 % in the Centre and 49.3 % in the Southern Italy). From 2006 to 2010, Italy has produced on average 6.5 milion tons of tomatoes (fresh tomato + tomato to processing), equal to 38% of the entire UE productions (Agroalimentare News, 2011). Arsenic toxic species may be accumulated in tomato tissues and, consequently, could enter in human food chain through the ingestion of its berries. Therefore, we carried out greenhouse experiments to evaluate the influence of P fertilization on the: i) growth of tomato plants (Solanum lycopersicum L., cv. Piennolo), cultivated on As-uncontaminated soil irrigated with solutions containing arsenite (AsO3) at four different concentrations and ii) As uptake by plants and its partitioning among different tissues (roots, shoots and tomato berries).


2. Materials and Methods

2.1 Soil preparation and characterization

The As-uncontaminated soil used in the experiments was collected from the sub-surface layer (0-30 cm) of a natural grassland in Portici, Italy; its physical and chemical properties are reported in Table 1. After air-drying, the soil samples for cultivation and chemical analyses were passed through 5 and 2 mm mesh sieves, respectively. Soil fractions were separated by pipette and sieving following pre-treatment with H2O2 to oxidize organic matter. Soil pH was measured by potentiometry in distilled water (1:2.5 soil: water ratio). Organic C content of soil was determined by wet digestion with a modified Walkley-Black procedure. For determination of CEC the soil was extracted with 1 M NH4OAc at pH 7.0. Total soil N was determined using a NCS auto-analizer (NA 1500 Series 2). Available P concentration was determined by colorimetric method using 0.5 M NaHCO3 as the extractant (Olsen method) (Jackson, 1974). The As concentration in digested soil was determined by Inductively Coupled Plasma Atomic Emission Spectroscopy (ICP - AES, Varian, Liberty 150).

2.2 Experimental conditions

Experiments were conducted from April 2011 to July 2011 in an unheated greenhouse. Tomato plants (Solanum lycopersicum L., cv. Piennolo) were grown in pots filled with 12 kg of the uncontaminated soil; they were planted at a density of 3 seeds per pot, sown directly in the pots and irrigated with water during the first 2 weeks. After this period the seedlings were thinned to 1 per pot and irrigated with water containing sodium arsenite (Na2HAsO3) at four different concentrations: 0 (As control treatment), 0.5, 2, and 4 mg As L-1. The range of As concentrations was chosen to encompass the concentrations occurring in underground waters of the As-affected areas of World.
Arsenic-contaminated waters were added as required to maintain 60 % water holding capacity. All the pots were fertilized every 2 weeks with 80 mL of nutrient solution containing 30 mM of NH4NO3 and 25 mM of K2SO4. Furthermore, in half of the pots 6 mM of
K 2HPO4 was included in the nutrient solution in order
to evaluate the influence of P on As uptake by tomato plants and then, the experimental design also provided 2 levels of P application, without P (P-) and with P (P+). The design was completely randomized and re-arranged every day, and each treatment was replicated 4 times to give a total of 32 pots. Irrigation was stopped 1 week before harvest.

Aboveground biomass was removed by cutting the base of the plant 3-4 cm above the soil surface (to avoid basal tissue contaminated by applied As solution), which was then separated into shoots (stems plus leaves) and berries sub-samples. The fresh tissues of the bean plants were weighed, washed with tap water, rinsed twice with deionized water in order to remove soil residues and then dried to a constant weight in the oven for two days at 70 °C.

Roots, shoots and tomato berries were analyzed for total concentration of As and P. All samples were ground using a PM 200 ball mill (Retsch) and digested in a microwave (Milestone, Digestor/Dring Ethos 900). A sample of about 0.5 g was accurately weighed into a PTFE pressure vessel and 7 mL of HNO3 (65%), 0.5 mL of HF (50%), and 2 mL of H2O2 were added. All glassware and plasticware were previously acid-washed in 3M HCl, and rinsed in deionized water. Total concentrations of As and P in root, shoots and tomato berries were determined by Inductively Coupled Plasma (ICP - AES, Varian, Liberty 150). Arsenic and P detection limits provided by this method were 8 and 12 μg L-1, respectively. All analysis were carried out in triplicate. In each analytical batch at least, one reagent blank and one internationally certified reference material was included to assess precision and accuracy of the chemical analysis. Certified reference material (Oriental tobacco leaves CTA-OTL-1) was used. Repeated analyses of certified reference material gave 0.588 ± 0.013 mg kg-1 for As (certified value 0.539 ± 0.060 mg kg-1) and 3006 ± 85 mg kg-1 for P (certified value 2892 ± 134 mg kg-1).

2.3 Statistical analysis

Data analyses were performed with Kaleidagraph 3.6. Treatment effects were determined by analysis of variance. Where necessary, data were transformed logarithmically to stabilize the variance. Differences were considered as statistically significant at p < 0.05 (Tukey's test).


3. Results and Discussion

3.1 Plant growth and As toxicity

Plant biomass decreased markedly with increasing As concentration in irrigation water (Table 2). Plants non-fertilized with P (P-) and irrigated with solutions containing 0.5, 2 and 4 mg As L-1 showed a decrease in their biomass of 17 %, 42 %, and 58 %, respectively, compared to their own As control treatment. This reduction was less severe (13%, 30%, and 42%, respectively) in the plants fertilized with P (P+) (Table 2). Similar results were also obtained on rice (Abedin et al., 2002) and wheat (Liu et al, 2005; Pigna et al, 2009).

The most negative effect due to the higher As exposure interested the roots dry weight. Specifically, P- plants irrigated with the 0.5, 2 and 4 mg As L-1 solutions showed a reduction of roots biomass of 29 %, 65 %, 74 %, respectively, as referred to control treatment; these percentages, in P+ plants, were significantly lower (4.1 %, 18 %, 34 %, respectively). Hence, these data indicated that the addition of P to the system has significantly increased root biomass, regardless As treatment.

Quaghebeur and Rengel (2003) found that by increasing AsO4 concentration in nutrient solution there was a decrease in the roots and shoots dry weight of Holcus lanatus, accentuated when plants were non-fertilized with P. Similar results were also obtained by Pigna et al., (2009) studying the influence of phosphatic fertilizer on wheat plants irrigated with AsO4-contaminated solutions.

The dry weight of shoots (stem plus leaves biomass) was markedly influenced by the interaction between As and P treatments; the shoots biomass decreased with increasing concentration of As in irrigation water, especially in P- plants. Also the tomato berries yield (mass of tomatoes per pot) decreased significantly with higher As exposure. P- plants non-irrigated with As produced 12.60 g of tomato berries; the same, when irrigated with the most As-contaminated solution (4 mg L-1) realized only 5.30 g pot-1 (Table 2), with a percentage drop of dry weight of 58 %. This reduction of yield was less severe in plants fertilized with P (from 17.40 to 8.40 g pot-1, percentage drop of dry weight of 51 %).

The presence of AsO3 in the irrigation solutions inhibited tomato plant growth and, consequently, their yield, especially in the absence of P fertilization. The higher production of biomass of the plants fertilized with P indicated the beneficial role of P in preventing the toxicity of As promoting the growth of plants. According to Zhao et al. (2009) PO4 and AsO4 are taken up by plant roots through a common carrier, but the PO4/AsO4 plasma membrane carrier shows a much higher affinity for PO4 than AsO4. Arsenate/ PO4 uptake can be suppressed or minimized when the plants show a sufficient P status, as it seems to be occurred in our P+ plants (as discussed below). The suppression of the high-affinity uptake system could be due to a feed back regulation of the AsO4/PO4 transporters (Meharg and Macnair, 1992).

Many authors assessed that non-resistant plants can be made more resistant to AsO4 by raising their P status, as the P is taken more effectively compared to AsO4 (Meharg and Macnair, 1992; Lee et al., 2003).

Also in AsO4 resistant plants with high P status a reduced sensitivity has been observed, which is not due to a difference in AsO4 influx, but is presumably a result of higher cytoplasmatic P status, decreasing AsO4 toxicity within the cell (Meharg, 1994). The effect of P nutrition on As toxicity could be summarized as follow: 1) high plant P status leads to a down-regulation of the AsO4/PO4 plasma-lemma transporters, and 2) high cellular PO4 levels result in greater competition with AsO4 for biochemical processes where AsO4 substitutes for PO4 (Meharg, 2005).

3.2 Arsenic concentration and content in tomato plants

Arsenic concentration in tomato roots, shoots and berries increased with increasing As concentration in irrigation water (Table 3). This trend is particularly evident in the roots of the P+ plants. In fact, by increasing As level from 0.5 to 4.0 mg L-1 in irrigation water, the As concentration in the roots increased from 0.68 to 3.85 and from 1.12 to 4.80 mg kg-1, respectively, in P- and P+ plants (Table 3). Similar results were also found by Tao et al. (2006) and Pigna et al. (2009), who studied the effect of P addition on the As accumulation in wheat plants.

The higher concentration of As in the roots of P+ plants probably occurred because the application of the fertilizer containing P could have inhibited the AsO4/ AsO3 sorption on the surface of the soil colloids (Violante and Pigna, 2002; Violante et al, 2005) and consequently, promoted the As uptake by plants because of the higher concentration of As in soil solution.

Similarly, As content μg pot-1) also increased with increasing As concentration in irrigation water and P application (Table 3). Although the P+ plants showed a higher As content than P- plants, in all their tissues, the alleviation of As toxicity would be attributed to the greater dilution of the As in the greater biomass produced by these plants. This aspect is particularly evident in Figure 1, which shows ratios between the As content in tomato berries and their biomass as a function of As treatment. Regardless As level in the irrigation water, P application has determined a reduction of these ratios, confirming that a greater dilution of the As in the berries biomass occurred in the plants fertilized with P. In addition, a more evident reduction of this ratio between the P- and P+ plants (Figure 1) has been determined in the treatments with higher As levels (2.0 and 4.0 mg L-1) versus the lowest one (0.5 mg L-1).

Figure 1. Arsenic content/biomass ratio in tomato berries exposed to four As concentrations in irrigation water (0, 0.5, 2.0 and 4.0 mg L-1).

The better P nutritional status of P+ plants has also allowed to limit the traslocation of As from roots to aboveground plant tissues. The higher the As concentration in irrigated water, the higher the As content in tomato berries; however, this content has never reached hazardous values, indicating a little accumulation of As in the tomato berries; in addition, P application has further limited the As accumulation in tomato berries, highlighting the crucial role of P in reducing the translocation of As toward tomato berries (Table 3).

The ratios between the As concentration in shoots and roots decreased with increasing As concentration in irrigation water and in P+ plants (Table 3). These results demonstrate that the As concentration in the roots increased more rapidly than that in the shoots; most of the As absorbed by tomato plants, in fact, was accumulated in roots, whereas only a small amount of the toxic element was translocated to the tomato berries; in addition, P application contributed to enhance this positive trend. In a similar experiment on tomato plants, Carbonell-Barrachina et al. (1997) found that the 83.2 % of all the absorbed As remained in the roots, the 16.8 % in the shoots and only 7.3% was accumulated in the leaves. A recent study (Bliek et al., 2008) reported that AsO4 tolerance in plants is dependent on the P nutritional status of the plant. This behaviour is promoted by the activity of AsO4 reductase, involved in the reduction of AsO4 to AsO3 and subsequent vacuolar sequestration of As(III)-phytochelatin complex.

3.3 Phosphorus concentration and content in tomato plants

The concentration (g kg-1) and content (mg pot-1) of P in roots, shoots and tomato berries are reported in Table 4. Phosphorus concentration in roots of the tomato plants significantly increased with P application and by increasing level of As in irrigation water. The concentration of P increased from 1.16 g kg-1 (As control treatment) to 2.30 g kg-1 (highest As level) and from 1.65 to 3.40 g kg-1, respectively, in P- and P+ plants (Table 4).

The content of P in P- plants roots decreased from 2.55 mg pot-1 (As control treatment) to 1.33 mg pot-1 (highest As level) because of the lower biomass produced by the plants irrigated with higher As levels; vice versa it increased in the roots of the P+ plants, from 3.96 to 5.44 mg pot-1 (Table 4). Similar results were obtained by Meharg (1994) who ascertained that PO4 is more efficiently taken up and accumulated in plant tissues than AsO4. These findings may explain how tolerant plants can survive at high levels of AsO4 in soil solution and, indeed, how plants grown on As-contaminated sites are able to obtain enough P to sustain their growth (Meharg, 1994).

The P concentration and content in tomato shoots decreased markedly with increasing concentration of As in the irrigation solutions, especially in the plants non-fertilized with P. For example, the concentration of P in the shoots of P- plants irrigated with solution containing 4 mg As L-1 was 64 % lower than that of their own As control. Similarly, the content of the As in these plants decreased from 30.24 to 4.80 mg pot-1 (Table 4). The same trend was also found in P+ plants, but it was lesser pronounced (percentage drop in P concentration of 23 % and reduction from 52.16 to 27.20 mg pot-1 of P content).

The concentration of P (g kg-1) in tomato berries slightly decreased by higher As exposure, both in P-and P+ plants, while its content (mg pot-1), being related to the biomass, produced more severe decreases in P- plants (Table 4).


4. Conclusion

The results of this study confirm the important role of P fertilization in minimizing the negative effects due to the As toxicity. The addition of this important nutrient has also determined a limited translocation of the toxic element from roots to aboveground plant tissues. Hazardous levels ofAs were not found in tomato berries, which are the edible part of the plant, especially in plant fertilized with P. This aspect has practical importance for the As-contaminated agricultural systems, in which adequate production techniques are required to avoid stunted growth of the food plants, severe yield losses and low food quality.



This study was supported by the Italian Research Program of National Interest (PRIN 2008).



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