Arsenic Influence on Genetic Variation in Grain Trace-Element

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Environ. Sci. Technol. 2010, 44, 8284–8288

Arsenic Influence on Genetic Variation in Grain Trace-Element Nutrient Content in Bengal Delta Grown Rice G A R E T H J . N O R T O N , * ,† TAPASH DASGUPTA,‡ M. RAFIQUL ISLAM,§ SHOFIQUL ISLAM,§ CLAIRE M. DEACON,† FANG-JIE ZHAO,| JACQUELINE L. STROUD,| STEVE P. MCGRATH,| JOERG FELDMANN,⊥ ADAM H. PRICE,† AND ANDREW A. MEHARG† Institute of Biological and Environmental Sciences, University of Aberdeen, Cruickshank Building, St Machar Drive, Aberdeen, AB24 3UU, U.K., Institute of Agriculture Science, Calcutta University, 35 B.C. Road, Kolkata 700 019 West Bengal, India, Department of Soil Science, Bangladesh Agricultural University, Mymensingh-2202, Bangladesh, Soil Science Department, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, U.K., and College of Physical Sciences, University of Aberdeen, Meston Walk, Aberdeen, AB24 3UE, U.K.

Received May 3, 2010. Revised manuscript received August 23, 2010. Accepted September 6, 2010.

It has previously been shown that across different arsenic (As) soil environments, a decrease in grain selenium (Se), zinc (Zn), and nickel (Ni) concentrations is associated with an increase in grain As. In this study we aim to determine if there is a genetic element for this observation or if it is driven by the soil As environment. To determine the genetic and environmental effect on grain element composition, multielement analysis using ICP-MS was performed on rice grain from a range of rice cultivars grown in 4 different field sites (2 in Bangladesh and 2 in West Bengal). At all four sites a negative correlation was observed between grain As and grain Ni, while at three of the four sites a negative correlation was observed between grain As and grain Se and grain copper (Cu). For manganese, Ni, Cu, and Se there was also a significant genetic interaction with grain arsenic indicating some cultivars are more strongly affected by arsenic than others.

Introduction Rice is the major food staple for people living in the Bengal delta. In diets that are largely reliant on rice, a large proportion of caloric intake (1) and dietary minerals is obtained from grain. A number of major minerals are often lacking in the human diet, including Fe, Zn, I, Se, Cu, Ca, and Mg (2). Iron and Zn deficiencies are two of the major micronutrient deficiencies in the world, affecting an estimated 2 billion * Corresponding author e-mail: [email protected]; tel: +44(0)1224272700. † Institute of Biological and Environmental Sciences, University of Aberdeen. ‡ Calcutta University. § Bangladesh Agricultural University. | Rothamsted Research. ⊥ College of Physical Sciences, University of Aberdeen. 8284

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people worldwide for each element (3-5). It has been proposed that even a small increase in the Fe nutritional value of rice grain, in regions where rice is the staple, would be highly significant (6). It is also estimated that 0.5-1 billion people may be Se deficient (7), and that populations which consume largely rice-based foods may therefore have Se deficient diets (8). Human mineral deficiency can be tackled by improving the nutrient density of dietary staples, such as rice (6, 9-11). There are two main approaches to crop biofortification (fortification with desirable minerals/nutrients): agronomic and genetic (2). The latter strategy in particular involves plants that are bred or genetically modified to have increased accumulation of minerals within their edible parts (2). If this strategy is to be used effectively, without genetic modification of crops, an understanding of the full extent of genetic diversity of mineral accumulation within the edible portion of the plants is needed. A number of studies have evaluated the genetic variation of some nutrients within rice. For example, Gregorio et al. (12) examined the concentration of Fe and Zn in brown rice in a wide range of cultivars; more recently Jiang et al. (13) measured 8 minerals in milled rice of 274 rice cultivars. In that study they identified cultivars that could be used in breeding programs. However, as more detail is becoming apparent about the grain ionome (which is the mineral nutrient and trace element composition of an organism) it is important to understand the interactions of the environment on grain element concentration, and the potential interactions among multiple elements. It has recently been demonstrated that different concentrations of soil arsenic, which led to increased grain As concentration, have an interaction with nutritionally important minerals within the grain in rice (8). The current study reports the mineral content of rice grain grown using field sites situated within the Bengal delta. It has been established that this region has high levels of As in the groundwater (14), and that this water has been used to irrigate crops (15). This has led to increased concentrations of As within agricultural soils in the region (16), and consequently elevated concentrations of As within the edible parts of crops (15). In these sites that are irrigated with As contaminated water it is likely that the main stressor to plant growth, transport processes, and metabolism is the As itself, unlike mine impacted sites where the metal/metalloid stressors can be many and interacting. These sites therefore offer an opportunity to study the impact of As on plant nutrient content. Rice is of a particular concern due to the anaerobic soil management which makes the soil As more bioavailable (17), and results in rice accumulating higher concentrations of As compared to aerobically grown cereals (18). In this study the genetic variation in 10 elements (both of nutritional value and/or toxicological relevance) are assessed in the grain of a diverse set of cultivars at 4 field sites in the Bengal delta. The environmental influence on the accumulation of these elemental concentrations was also assessed at the 4 sites by examining a subset of cultivars which were present at all 4 field sites. Finally, an interaction between grain As and other elements was established, revealing that cultivars with high concentrations of As have decreased concentrations of Ni, Cu, and Se within the grain.

Methods Field Sites. Four field trials were conducted: two in Bangladesh and the other two in West Bengal, India. At all field sites the rice plants germinated in December 2007 and were 10.1021/es101487x

 2010 American Chemical Society

Published on Web 09/29/2010

TABLE 1. Genetic Variation in Element Concentrations in Grain among Cultivars at Each Field Site (Values Reported Are the Partition of Variance for the Cultivar Difference (%) and the F-Value Generated from the ANOVA in Brackets)a element As Fe Zn Cu Ni Mn Mo Se P Co a

Faridpur 62.2% 80.6% 69.2% 65.3% 60.6% 80.5% 64.4% 12.3% 45.3% 76.2%

(5.57)*** (12.57)*** (7.25)*** (6.24)*** (5.28)*** (12.44)*** (10.86)*** (2.2)*** (3.30)*** (9.88)***

Sonargaon

Nonaghata

70.6% (7.95)*** 66.1% (6.64)*** 69.4% (7.55)*** 55.9% (4.66)*** 64.8% (6.32)*** 36.5% (2.66)*** 65.2% (6.41)*** 34% (2.49)*** NS 81.0% (13.31)***

72.5% 69.4% 77.9% 39.4% 87.9% 86.8% 78.2% 64.5% 14.0% 84.7%

(8.84)*** (7.74)*** (11.49)*** (2.94)*** (22.7)*** (20.58)*** (11.68)*** (5.75)*** (1.49)* (17.51)***

De Ganga 75.3% 74.2% 80.5% 82.4% 71.9% 83.0% 66.4% 70.6% 58.6% 79.8%

(10.19)*** (9.65)*** (13.47)*** (15.14)*** (8.71)*** (15.74)*** (6.96)*** (8.23)*** (5.27)*** (12.88)***

NS ) not significant. * P < 0.05; ** P < 0.01; *** P < 0.001.

harvested in May 2008. Local faming practice and fertilizer regimes were used at the field sites. The two field sites in Bangladesh were located in Faridpur and Sonargaon. The field site in Faridpur was under continually flooded conditions, with irrigation every 3 days. The field site in Sonargaon was irrigated every 2 days, which resulted in alternative wet-dry cycles. The field sites were fertilized with 70 kg N/ha (split over 3 equal applications), 20 kg P/ha, 50 kg K/ha, 15 kg S/ha, and 2 kg Zn/ha (19). Both sites had a history of dry season (boro) irrigation with As contaminated water extracted from tubewells. The Faridpur field site, which was a silty loam soil (pH 8.0), had an average soil As content of 29.6 ( 7.2 mg kg-1, and a tubewell water As concentration of 198 ( 31 µg L-1. The Sonargaon field site, which was a silty clay loam (pH 7.1), had an average soil As content of 10.3 ( 2.2 mg kg-1, and a tubewell water As content of 331 ( 13 µg L-1. The two field sites in West Bengal were located in Nonaghata and De Ganga. Both field sites were maintained under continually flooded conditions, with irrigation every day. The field sites were fertilized with 70 kg N/ha, 35 kg P/ha, and 35 kg K/ha (20). Both sites had a history of dry season irrigation with As contaminated water extracted from tubewells. The Nonaghata field site (pH 6.4) had low level arsenic in the soil and tubewell water (6.3 ( 1.3 mg kg-1 and 14.9 ( 4.1 µg L-1 respectively), while the De Ganga site (pH 7.2) had higher concentrations of As in the soil and tubewell water (17.9 ( 4.0 mg kg-1 and 131 ( 8.8 µg L-1, respectively). A set of 76 cultivars was grown at the Bangladeshi field sites consisting of Bangladesh Rice Research Institute improved cultivars, diverse cultivars previously used to generate permanent rice mapping populations, and local landraces. At the 2 Indian field sites a total of 89 cultivars were grown, consisting of Indian improved cultivars, Indian landraces, and diverse cultivars previously used to generate permanent rice mapping populations. Plants were sown in a randomized complete block design with 3 replicates. In each replicate each cultivar was planted in a single row of 2 m with 10 hills, each hill (1 seedling) 20 cm apart, and each row 20 cm apart. To separate the test cultivars 2 hills of a check cultivar were planted at each end of the 10-hill test rows. Between every row of test cultivars one row of the check cultivar was planted. From the 4 fields used in this study a total of 18 cultivars were common at all sites. A list of the common cultivars grown at the field sites can be found in Table S1 (Supporting Information). Sample Preparation and Analysis. Trace element grade reagents were used for all digests, and for quality control replicates of certified reference material (Rice flour [NIST 1568a]) were used; spikes and blanks were included. Rice grain samples were dehusked and 0.2 g weighed into 50-mL polyethylene centrifuge tubes. Samples were digested as described in Norton et al. (21). Multielement analysis was

performed by ICP-MS (Agilent Technologies 7500). All standards and blanks contained 10 µg L-1 In as the internal standard and were made in 2% nitric acid. Analysis was performed as described in Sun et al. (22). The recoveries of the certified reference material were P 106 ( 10%, Mn 95 ( 6%, Fe 64 ( 6%, Cu 94 ( 7%, Zn 80 ( 5%, As 95 ( 6%, Se 88 ( 7%, and molybdenum (Mo) 97 ( 6%. The certified reference material is not certified for Co or Ni; the spike recovery for these elements was 103 ( 6% and 106 ( 11%, respectively. Statistical Analysis. Analysis of variance (ANOVA), general linear model (GLM), and correlations were performed using Minitab 15 Statistical Software. For statistical differences between grain concentrations for the cultivars at individual field sites one-way ANOVA was conducted; using the mean sum of squares the partition of variance was estimated. For the 18 cultivars in common across all the field sites, GLM was used with cultivar and field site as the variables to determine the significance of cultivar differences, site differences, and the interaction of cultivars at sites on grain As; using the mean sum of squares the partition of variance was estimated for cultivar differences, site differences, and the interaction of cultivars at sites on grain As. To determine an interaction between grain elements and grain As for the 18 cultivars in common across all the 4 field sites a GLM analysis was performed as described above with As used as a covariable. Correlations between grain As and other elements were conducted on the mean concentrations of the cultivars at each site; only correlations which are significant (P < 0.05) are reported in the text.

Results The results of statistical analysis of the data are presented in Tables 1 to 3, and the mean values of grain elements for each site are presented in Tables S2-S5 (Supporting Information). It has already been demonstrated that for the cultivars at these field sites there is genetic variation for As accumulation in rice grain, and that there is a large environmental effect on the accumulation of grain As (20). The findings of this study indicate that for all elements analyzed there is genetic variation (Table 1). There were also site effects and cultivar by site interactions for all the analyzed elements (Table 2). For Co, Cu, Fe, Mn, and Zn the genetic variation is greater than the environmental effect, whereas for P, As, Ni, Se, and Mo the site effect is larger than the genotypic difference for the accumulation of the elements in the grain. The cultivar by environment interactions for the elements indicate that there is a complex process for the accumulation of these elements within the grain. The mean grain Fe concentration at each site was remarkably similar, ranging from 10.2 to 10.5 mg/kg. Grain Fe was strongly affected by cultivar at all sites, with consistent VOL. 44, NO. 21, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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TABLE 2. Analysis of Multi-Elements for the 18 Cultivars in Common Across All Four Field Sites (Values Reported Are the Partition of Variance for the Cultivar, Site and Cultivar by Site Interaction and the F-Value Generated from the ANOVA in Brackets. Interaction with As is Presented As the F-Value for the Elements with a Significant Interaction with As)a

a

element

cultivar

site

cultivar × site

interaction with As

As Fe Zn Cu Ni Mn Mo Se P Co

13.0% (17.3)*** 45.6% (18.2)*** 34.7% (19.3)*** 45.9% (26.3)*** 17.5% (14.3)*** 54.3% (23.7)*** 10.4% (14.6)*** 6.8% (8.3)*** 9.9% (5.9)*** 29.4% (24.1)***

45.2% (128.0)*** 11.1% (20.0)*** 17.0% (44.5)*** 15.2% (36.4)*** 34.2% (108.7)*** 1.5% (5.3)** 74.1% (450.8)*** 68.2% (308.0)*** 56.2% (114.7)*** 24.1% (59.3)***

25.7% (5.6)*** 12.5% (2.2)* 27.0% (4.7)*** 18.9% (3.8)*** 33.6% (7.7)*** 16.0% (2.7)*** 7.1% (3.5)*** 14.1% (4.8)*** 9.9% (2.2)*** 28.4% (5.4)***

N/A NS NS 5.4* 89.2*** 45.2*** NS 15.2*** NS NS

NS ) not significant. * P < 0.05; ** P < 0.01; *** P < 0.001.

TABLE 3. Correlations (r) among Multi-Elements and As in the Grain at the Four Field Sitesa element

Faridpur

Sonargaon

Nonaghata

De Ganga

Fe Zn Cu Ni Mn Mo Se P Co

0.385** 0.373** -0.434*** -0.677*** NS NS NS -0.503*** 0.446***

0.232* 0.372** NS -0.691*** 0.283* -0.292** -0.354** NS 0.594***

-0.419*** -0.39*** -0.295** -0.638*** 0.485*** NS -0.426*** NS 0.285**

-0.44*** -0.271* -0.63*** -0.715*** NS NS -0.643*** NS NS

a NS ) not significant. * P < 0.05; ** P < 0.01; ***P < 0.001.

1.8- and 2.0-fold range at all sites (Tables S2-S5). At all four sites there was a correlation between Fe concentration in the grain and As concentration in the grain (Table 3). Interestingly at the Bangladeshi sites there were positive correlations between grain As and Fe grain concentrations whereas at the Indian field sites there were negative correlations between grain As and grain Fe. These conflicting correlations may indicate that the environmental conditions and/or field management practices have an effect on the relationships between elements within the grain. No interaction in grain As and Fe was detected for the cultivars in common at all the field sites. Like Fe, the sites had very similar mean grain Zn concentrations (18.9-22.2 mg kg-1) and the fold ranges across cultivars were quite small (2.1, 2.1, 2.1, and 2.6). At all four sites there was a correlation between Zn concentration in the grain and As concentration. Similar to Fe, at the Bangladeshi sites there were positive correlations between grain As and Zn grain concentration whereas at the Indian field sites there were negative correlations. Using a single cultivar grown across multiple Bangladeshi field sites Williams et al. (8) identified a negative correlation between grain As and Zn. However, it seems that this is an environmental effect rather than a genetic effect, because in both this study and in the experiment reported by Williams et al. (8) no interaction was detected in grain As and Zn in the cultivars grown. The mean grain Cu concentration was similar at all four sites, ranging from 3.73 to 4.95 mg kg-1 and there was an approximately 2-fold or 4-fold variation across cultivars within sites in Bangladesh and India, respectively. The genetic variation in Cu in the cultivars in common across the four field sites was larger than the environmental effect (Table 2). For all the cultivars grown at three of the four field sites (not Sonargaon) there were negative correlations between grain 8286

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As and grain Cu, while at the Sonargaon field site there was no correlation between grain As and grain Cu. This is further backed up by the cultivars in common across the four field sites for which an interaction between grain As and grain Cu was detected (Table 2). The mean grain Ni concentration varied from 0.17 mg kg-1 at Faridpur to 0.73 mg kg-1 at Nonaghata. At all sites there were differences between the cultivars for Ni (Table 1). The fold-ranges for the cultivars were large, with the largest range being at the De Ganga field site (>35 fold-range). At all sites there were also large negative correlations between grain As and Ni concentration (Table 3), and this interaction is confirmed by the analysis of the cultivars in common at all four field sites (Table 2). For these cultivars there is a very large interaction between As and Ni in the grainsthe more As the less Ni. This interaction has been observed in a potbased experiment (8). The mean grain Mn concentration was remarkably similar across sites, varying from 18.8 to 19.9 mg kg-1. At all sites there were significant genotypic differences for the concentration of grain Mn; the 2-way ANOVA indicated that the genotypic differences were greater than the site effect. For the cultivars in common across all field sites there was an interaction between grain As and Mn concentrations (Table 2). At the Sonargaon and Nonaghata sites a positive correlation was observed between grain As and Mn concentrations, indicating that increased Mn concentration was associated with increased As concentrations in the grain. The mean grain Mo concentration varied from 1.00 mg kg-1 at De Ganga and Faridpur to 2.08 mg kg-1 at Sonargaon with about a 3-fold range across cultivars at all sites. There was a genotypic difference at all field sites in the Mo concentration in the grain and for the cultivars in common across the four field sites there was also a large site effect and small cultivar by site interaction. There was only a small negative correlation between grain As and Mo at the Sonargaon sites for the individual field sites (Table 3). The mean grain Se concentration varied from 0.04 mg kg-1 at Faridpur to 0.20 mg kg-1 at Sonargaon. There were significant genotypic differences in grain Se concentration although at the Bangladeshi field sites the genotypic effect was relatively small (Table 1). For the cultivars in common across all field sites there was a weak genotypic difference and a large site effect, indicating that the environmental effect has a much larger influence on grain Se (Table 2). At both the Indian field sites and the Sonargaon field site there was a negative correlation with As and in the cultivars in common there was a significant effect of grain As on grain Se (Table 3). For the cultivars in common across the four field sites there was an interaction between grain As concentration and grain Se concentration (Table 2). This is in agreement

with Williams et al. (8) that over a wide range of environments a negative relationship between grain As and Se is observed. The mean grain P concentration varied from 253 mg kg-1 at Faridpur to 385 mg kg-1 at De Ganga. There was genotypic variation at three of the four field sites (not Sonargaon) and in the cultivars in common there was also variation due to cultivar, site effects, and cultivar by site interactions (Tables 1 and 2). There was only a negative correlation between grain P and As concentrations at the Faridpur field site, and no interaction between grain As and P concentration in the cultivars in common across all the field sites, suggesting only weak interactions between As and P. The mean grain Co concentration was very similar at the four sites, ranging from 0.012 to 0.019 mg kg-1. There were genotypic differences between the cultivars at all the sites with fold ranges from 4.4 to 13.3. For the cultivars in common there was also genotypic variation, site effects, and cultivar by site interactions. At three of the field sites (not De Ganga) there were positive correlations between grain Co and As concentrations (Table 3), however, for the 18 cultivars in common across all the sites there was no interaction between grain As and Co concentration (Table 2).

Discussion There are two ways in which the nutritional value of grain can be increased: by crop breeding or by land management. The analysis presented above gives some indication of the likely scope of these approaches for rice grown in the Bengal delta. If the environmental (site) effect presented in Table 2 is large, it indicates land management might have a good potential, although the site effect might also be driven by underlying soil properties that are intractable via management. If the genetic effect is large, then there is scope for crop breeding. For the beneficial elements Mn, Fe, Co, Ni, Cu, and Zn there appears to be some good scope for breeding, however for Ni the site effect is bigger than the cultivar effect. Of the beneficial elements, Se and Mo do not appear to have good opportunities for breeding improvement. The identification of Se of having a low breeding potential is in agreement with a study in wheat, in which it was concluded that there were genotypic differences between wheat cultivars but that these differences are likely to be small compared to the background soil variations (23, 24). The use of inorganic Se fertilizers for the biofortification of crop Se has been successfully used in both New Zealand and Finland (25-27). Furthermore, it has been shown that the foliar application of Se to rice plants increases grain Se by approximately 200% (28). Therefore the deficiency of Se in the human diet could be rectified by Se fertilization. However, whether this is a financially viable solution for the Bengal Delta needs to be explored. For As there is a genetic effect, though the site effects and the cultivar by site interaction are larger. The strong genetic variation in unpolished grain Fe concentration, and the consistent range of Fe grain concentration, confirm that Fe is highly regulated at the genetic level, with respect to accumulation within rice grains. Homeostasis of Fe in plants is tight because Fe, while abundant in the environment, is not very available to the plant, and Fe is a potent stimulator of potentially damaging redox reactions and therefore its cellular uptake is tightly regulated (29). Even though the variations between cultivars are small in grain Fe concentration (but of a consistent range with other studies (for review see 2) if this natural variation could be exploited to breed cultivars with increased grain Fe it could have an impact on a large number of people worldwide (6, 17, 30, 31). Studies have mapped the genetic loci affecting rice Fe (21, 32, 33), and the integration of these loci into breeding programs may increase total grain Fe. The findings from the present studies confirm a number of findings by Williams et al. (8) where a significant decline

in essential nutrients was associated with increasing As within rice grain. In a pot-based experiment using 20 cultivars (18 of which were improved Bangladeshi cultivars) Williams et al. (8) identified significant As by cultivar interactions for grain Ni and Mn concentrations. The data from this study looking at 18 cultivars across 4 field sites confirms both these interactions between grain As and grain Mn and Ni, as well as identifying interactions between grain arsenic with Cu and Se. Recent studies have begun to genetically map the grain ionome in rice (21, 32, 33). The results from this study highlight some important issues regarding the mapping of the ionome. Cultivars in this study that significantly accumulated higher levels of grain As also had decreased levels of some other elements. Whether this decrease in other elements is caused by an increase in grain As concentration or the other way around is unclear at present, however, the effect on the nutrient content of the grain is same. Where grain As affects other elements, the determination of the grain ionome would be compromised, making the physiological or genetic dissection of trace element accumulation into rice grain particularly problematic. For example, if Ni concentrations were being investigated in rice grain to determine genetic loci responsible for increased Ni content, the results could be confounded by the presence of As in the grain.

Acknowledgments This work was funded by BBSRC-DFID grant BBF0041841. We thank the International Rice Research Institute for providing the seeds of the parents of the mapping population, and the Bangladeshi Rice Research Institute for providing the seeds of BRRI varieties and landraces of boro rice. The plant material was imported into the UK under import licence IMP/SOIL/18/2009 issued by Science and Advice for Scottish Agriculture.

Supporting Information Available Information on the average, minimum, and maximum concentrations for all the elements analyzed at each field site. This information is available free of charge via the Internet at http://pubs.acs.org.

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