Ying Jing,Xiomin Feng,Ydong Yng,Xingxue Qi,Yongfeng Ren,Youhui Go,Weidong Liu,Yuego Hu,*,Zhohi Zeng

aCollege of Agronomy and Biotechnology,China Agricultural University,Beijing 100193,China

bInstitute of Crop Sciences,Chinese Academy of Agricultural Sciences/Key Laboratory of Crop Physiology and Ecology,Ministry of Agriculture,Beijing 100081,China

Keywords:

A B S T R A C T Selenium(Se)deficiency commonly occurs in soils of northeastern China and leads to insufficient Se intake by humans.A two-year field study of Se biofortification of common buckwheat supplied with 40 g Se ha?1as selenite(Se(IV)),selenate(Se(VI)),or a combination(1/2 Se(IV+VI))was performed to investigate Se accumulation and translocation in plants and determine the effects of different forms of Se on the grain yield,biomass production,and Se use efficiency of plants and seeds.Se application increased seed Se concentrations to 47.1—265.1 μg kg?1.Seed Se concentrations following Se(VI)or 1/2 Se(IV+VI)treatment exceeded 100 μg kg?1,an amount suitable for crop Se biofortification.Se concentration in shoots and roots decreased with plant development,and Se translocation from root to shoot in Se(IV)-treated plants was lower than that in plants treated with 1/2 Se(IV+VI)and Se(VI).Both grain yield and biomass production increased under 1/2 Se(IV+VI)treatment,with grain yields reaching 1663.8 and 1558.5 kg ha?1in 2015 and 2016,respectively,reflecting increases of 11.0%and 10.3%over those without Se application.The Se use efficiency of seeds and plants under Se(VI)treatment was significantly higher than those under 1/2 Se(IV+VI)and Se(IV)treatments.Thus,application of selenate could result in higher Se accumulation in buckwheat seeds than application of the other Se sources,but the combined application of selenate and selenite might be an alternative approach for improving buckwheat grain yield by Se biofortification in northeastern China.

1.Introduction

Although selenium(Se)is a microelement that has been recognized as essential for humans in recent decades,diseases such as chronic bone and cartilage disease(Kashin-Beck disease)and chronic heart disease(Keshan disease)associated with insufficient Se intake still commonly occur in northeastern China[1].Se-deficient soil covers approximately two thirds of total farmland in China,resulting in Se deficiency in the human population in those areas[2].Se deficiency has been observed in approximately 72%of counties with an average daily intake of Se of only 26—32 μg by adults[3],an amount markedly lower than the daily Se intake of 50—200 μg recommended by the World Health Organization(WHO)[4].Recently,Se deficiency was predicted to become more severe with global climate change[5],and Se deposition and volatilization would make this situation even more of a concern in China than in any period before[1].

Se biofortification in the edible parts of crops has been suggested as an effective approach to reducing Se deficiency in the food chain[6,7].To increase Se content in edible parts of crops,agronomic Se biofortification strategies using inorganic Se fertilizers have been successfully implemented in several European countries[8—10].Selenate and selenite,two predominant forms of soil Se,have been applied for crop Se biofortification in various crops including wheat[11],rice[2],maize[12],and vegetable plants[10].Generally,selenate is the dominant form of Se in alkaline and well-oxidized soils,whereas Se is present predominantly as selenite in acidic to neutral soils or under reduced soil conditions[13].Plant uptake of selenate and selenite can occur via different pathways.Selenate uptake can be mediated by sulfate transporters,owing to the chemical similarity between selenate and sulfate[14],whereas uptake of selenite may involve phosphate or silicon transporters[15].It is well documented that selenate or selenite can be supplied as a Se source to crops for Se accumulation under controlled conditions[2,3,10],but a comparison of different forms of Se species for Se biofortification has rarely been investigated under field conditions in northeastern China.

Buckwheat has received increasing attention as a potential functional food and its consumption has become increasingly popular in some developed countries and regions,such as the United States,Canada,and Europe[16,17].China is one of the main world producers of buckwheat[18].Buckwheat has been cultivated for thousands of years in China and Europe,where Se deficiency was common[5,19].Our previous study demonstrated that buckwheat could be a potential crop for Se biofortification in areas where it is the principal crop[20].As a step toward resolving the occurrence of Se deficiency in humans,it is important to determine the effectiveness of Se biofortification in crops under field conditions to improve Se availability in the food chain in China.

Although numerous studies have focused on whether Se concentration increases in the edible parts of crops supplemented with Se[2,10—12],Se use efficiency,Se translocation,and the dynamics of Se accumulation in crops supplied with different forms of Se are still poorly understood under field conditions,particularly in Se-deficient areas.In this study,we compared Se accumulation and distribution in common buckwheat supplied with selenate or selenite and determined the effects of Se application on grain yield and biomass production of common buckwheat,as well as the Se use efficiency of seeds and plants.A further aim was to investigate the dynamic changes in plant tissue Se and Se translocation from root to shoot within plants over their growth period.

2.Materials and methods

2.1.Experimental site description

The field study was performed in 2015 and 2016 at the Chifeng Academy of Agricultural and Animal Husbandry Sciences Research Farm,Chifeng,China(42°17′N,118°52′E).This area is located in the Se-deficiency belt in China,and the region is classified as having a semi-arid continental monsoon climate with an annual precipitation of 250—400 mm.The weather data during the two-year experimental period are presented in Fig.1.The soil of the experimental field was a sandy loam with basic properties described in Table 1.

2.2.Experimental design and crop management

The experiment was laid out in a one-way randomized block design with four replications.The area of each plot was 30 m2and each pair of plots was separated by an empty unplanted row.In both years,buckwheat(cultivar CTQ 1)was sown in the middle of June with 0.45 m of row space.Se treatment was applied at 40 g ha?1as selenite(Se(IV)),selenate(Se(VI)),or 1/2 selenite plus 1/2 selenate(1/2 Se(IV+VI)),with a control lacking Se treatment.Sterile millet seeds were sprayed with a nutrient Se solution,air dried,and sown together with buckwheat.To avoid continuous cropping of buckwheat,two different plots were used at the same experimental site in both years.Each plot received an amount of 300 kg ha?1compound fertilizer(N 20%,P2O514%,and K2O 6%)prior to planting each year,an amount sufficient for the entire lifecycle of buckwheat.Crop management was the same in both years and followed conventional practices.No additional water or fertilizer was added during the growth period,pesticides were applied as needed to control insect populations,and weeds were removed manually.

2.3.Sample collection and preparation

When frost killed the buckwheat plants and most(at least 75%)of seeds were mature,the plants were harvested.Grain yield and yield composition were measured as in our previous study[20].Grain yield was calculated from two 1 m2areas in each plot.Ten randomly selected plants were collected from each plot to determine grain yield per plant and 1000-kernel weight.To measure dry matter production,buckwheat plants within 50 cm of row were sampled randomly from each plot from 30 to 75 days after sowing,at 15-day intervals.Root samples were collected from surface soil(0—30 cm)and the roots in the soil were sieved out using a 2 mm screen,removing other plant material and stones.After careful washing of the plant material with deionized water,the roots and shoots were separated and their dry mass was determined after oven drying at 75°C to constant weight.The dried plant samples were finely ground in a stainless steel Wiley mill(Thomas Scientific,Swedesboro,NJ,USA)for further Se analysis.

2.4.Determination of Se concentration

The dried plant samples were digested following Jiang et al.[18]with modifications:an 0.5-g plant sample was digested with 5 mL of a HNO3and HClO4mixture(v/v,4:1)in a 100 mL digestion tube overnight in a fume hood at room temperature.The mixture was then heated at 60 °C for 2 h followed by 170 °C for 6 h until white smoke appeared.After the samples were cooled to room temperature,5 mL of 6 mol L?1HCl was added and the samples were heated at 60 °C for2 h followed by 170 °C for 2 h for reduction of selenate to selenite.Approximately 2 mL of residual digested solution was diluted with deionized water to a volume of 25 mL.Hydride generation—atomic fluorescence spectrophotometry was used for Se concentration analysis of the digested solution following Liu et al.[21].

2.5.Statistical analysis

The Se translocation factor(TF)from root to shoot was calculated as the ratio of the concentration of shoot Se to that of root Se[22].For the calculation of Se use efficiency of plants and seeds per unit mass of Se application,the total amount of Se accumulation in plants or seeds with Se supplementation was subtracted from that without Se application,and the remainder was then divided by the mass of Se applied.One-way ANOVA with comparisons using Duncan's multiple test was performed to compare the mean values among different treatments at a 5%significance level.

3.Results

3.1.Dry matter,grain yield and yield components

In both study years,shoot DW showed a significant decrease under selenium application treatments 30 days after sowing(DAS30)compared to treatment without selenium supplementation(Table 2).However,higher shoot DW accumulation was observed in the 1/2 Se(IV+VI)treatment during the growth stages of DAS60 and DAS75 in 2015 and DAS75 in 2016,respectively.The highest amount of plant DW accumulation was obtained under the 1/2 Se(IV+VI)treatment,with 8.1 kg ha?1and 11.2 kg ha?1in 2015 and 2016,respectively.The trend of root DW accumulation was generally similar to that of shoot DW over time among different treatments,but no significant difference was found between Se-supplemented and control plants during the growth period in either 2015 or 2016.

The seed number per plant and grain yield per plant under the 1/2 Se(IV+VI)treatment were 13%and 15%higher than that under the CK treatment in 2015 and 2016,respectively(Table 3),whereas no significant effect of Se supplementation on 1000-grain weight was observed in either year(Table 3).Thus,the highest grain yields,1663.8 kg ha?1in 2015 and 1558.5 kg ha?1in 2016,were measured in plants grown under 1/2 Se(IV+VI)treatment.Grain yield was significantly increased under Se application by 11.0%(in 2015)and 10.3%(in 2016),compared to that in the untreated control.The yield under Se(IV)or Se(VI)treatments tended to be greater than that in the untreated control in both study years,but not significantly.

3.2.Dynamic Se accumulation and translocation in shoot and root

Shoot and root Se concentrations in buckwheat were significantly increased by Se application,and Se content in both tissues decreased gradually over the growth period in both experimental years(Fig.2).Compared to those under the CK treatment,all the Se-supplemented treatments showedsignificantly higher Se contents in shoot tissue during the growth periods in both years(Fig.2-a,b).However,the shoot Se concentration under both Se(VI)and1/2Se(IV+VI)treatments was two-to fourfold higher than that under Se(IV)treatment.Se accumulation in roots was significantly increased under all Se treatments(Fig.2-c,d).Se(IV)-treated plants showed a significantly higher root Se concentration than plants in the other three treatments regardless of the concentration measured at growth stage DAS30.Plants at growth stages DAS60 and DAS75 in 2015 and DAS75 in 2016 showed lower root Se accumulation under Se(VI)treatment than under the other two Se application treatments(Se(IV)and 1/2 Se(IV+VI)).

Table 3–Effects of Se application on seed and grain yield per plant,1000-grain weight,and grain yield of common buckwheat in 2015 and 2016.

The Se translocation factor(TF)was used to describe Se translocation from plant root to shoot.The TF values in both study years are shown in Fig.3.The TF values measured for plants grown under the Se(VI)and 1/2 Se(IV+VI)treatments over the entire plant growth period were 3-to 19-fold higher,respectively,than those grown under the Se(IV)treatments in 2015 and 2016.TF values of plants grown under the Se(VI)and 1/2 Se(IV+VI)treatments increased as the plants matured.The opposite trend was shown for the Se(IV)treatment,in which plants tended to accumulate more Se in root tissues,resulting in lower TF.

3.3.Se biofortification in seeds and Se use efficiency of plants and seeds

Se concentration in seeds of common buckwheat was significantly increased by Se application in both experimental years,and there was significant variation in seed Se content among Se treatments(Fig.4).The highest seed Se content was observed in plants supplied with selenate,with respective concentrations of 265.1 and 247.6 μg Se kg?1in the two years,followed by plants treated with 1/2 Se(IV+VI)and Se(IV),with seed Se concentrations of 123.8 and 47.1 μg kg?1in 2015 and 134.8 and 64.4 μg kg?1in 2016.Plants without Se supplementation showed the lowest seed Se concentration.

Fig.2–Shoot(a and b)and root(c and d)selenium(Se)accumulation in common buckwheat plants supplied without Se and with 40 g ha?1Se as selenite,selenate,or a combination of selenite and selenate over the growing period in 2015 and 2016.CK,without Se application;Se(IV),selenite;Se(VI),selenate;1/2 Se(IV+VI),combination of selenite and selenate.DAS,days after sowing.Values shown are mean±SE(n=3).Different letters indicate significant differences(P＜0.05)among treatments.

Plants with selenate supplementation(Se(VI))generally showed higher Se use efficiency than those with selenite(Se(IV))or the combination of selenite and selenate(1/2 Se(IV+VI))in both years,with the exception of plants at growth stage DAS30 in 2015 and at DAS30 and DAS45 in 2016(Table 4).Values of approximately 30—60(Se(IV)),70—200(Se(VI))and 60—140 mg g?1(1/2 Se(IV+VI))were measured between treatments over both growing periods.For Se use efficiency in seeds,a similar trend was observed for the different Se application strategies.Seed Se use efficiencies under selenate applications of 10.4 and 8.9 mg g?1observed in 2015 and 2016,respectively,were 5.7-and 3.8-fold higher than that under selenite application and 1.9-and 1.7-fold higher than that under the combined treatment.

4.Discussion

Agronomic biofortification strategies are often based on soil amendment with chemical Se fertilizers to increase Se accumulation in edible parts of crops[6,23].We investigated selenite,selenite,and their combination as a Se source for Se biofortification in common buckwheat under field conditions in northeastern China.We found that 40 g ha?1Se applied as selenite resulted in seeds with Se concentrations of 47—65 μg kg?1,whereas the same amount of Se applied as selenate or supplied in combination resulted in seeds with a Se concentration of approximately 125—265 μg kg?1,an amount adequate for crop Se biofortification.Under the same Se application conditions,there was a high root and low seed Se content when the plants were supplied with selenite as a Se source for biofortification.Thus,a low Se use efficiency in seeds was observed.These results are readily explained by combination of selenite with soil fractions(e.g.iron oxides or hydroxides),leading to low availability[9].However,it is possible that Se metabolism in plant roots also proceeds at a low rate,given that the translocation of selenate to the shoot is favored over that of selenite.The latter form is more toxic to cells in consequence of oxidative stress,leading plants to retain selenite in their roots and avoid its translocation to the shoot[15].Thus,applying selenite to soil as an Se source is an option for tuber crop Se biofortification or for cultivation of Serich rice in paddy fields or of other Se-rich grain products under leaching soil conditions[2,24],whereas the selenate form of Se fertilizer is preferable for soil amendment of most grains.

Fig.3 – Se translocation factor(TF)of common buckwheat plants grown without Se and with 40 g ha?1Se as selenite,selenite,or a combination of selenite and selenate in 2015 and 2016.Se(IV),selenite;Se(VI),selenate;1/2 Se(IV+VI),combination of selenite and selenate.Values shown are mean±SE(n=3).Different letters indicate significant differences among the treatments(P＜0.05).

Fig.4–Se accumulation in seeds of common buckwheat grown in 2015 and 2016 without Se and with 40 g ha?1of Se as selenite,selenite,or a combination of selenite and selenate.CK,without Se application;Se(IV),selenite;Se(VI),selenate;1/2 Se(IV+VI),combination of selenite and selenate.Values shown are mean±SE(n=3).Different letters indicate significant differences among the treatments(P＜0.05).

With Se supplementation,a general trend of Se accumulation in shoots and roots was revealed:Se concentration in tissues decreased over the growing period in both study years.Owing to the dilution of Se content with the accumulation of plant biomass and the volatilization of organic Se compounds,plant Se concentration decreases continuously throughout the growth period[25—27].This trend of crop Se accumulation was also observed by Zhang et al.[2]in rice supplied with selenite for Se biofortification.We also found in both years that Se use efficiency in plants increased during early stages and then decreased as plants matured.This finding suggests that changing Se availability of Se fertilizer applied in the wake of plant growth may influence plant Se uptake in plants,a suggestion that merits further investigation.

Although the essentiality of Se has not been established in plants,the optimal dosage of Se considered beneficial for plant growth has been reviewed[15].The window within which Se levels are beneficial vs.toxic to plants is narrow and variable,creating difficulties in determining the physiological role of Se in plants[28].We found that biomass accumulation in buckwheat shoots was inhibited by Se application at the early growth stage(DAS30),but was enhanced by the combination of selenate and selenite application when the crop reached maturity(DAS75),corresponding with the Se concentration in the plants during the growth stage.One explanation could be that appropriate Se levels in plants contribute to increasing the photosynthetic rate[29]and counteracting senescence-associated oxidative stress[30—32],whereas excessive Se may aggravate this stress and causedamage to the photosynthesis system[33].The physiological role of Se on photosynthesis and antioxidant mentioned above might account for the dynamic change in biomass production and the increase in grain yield under the combined application of selenate and selenite,a finding with important agronomic implications for buckwheat production.

Table 4–Se use efficiency in seeds and plants of common buckwheat during the growing period in 2015 and 2016.

With respect to Se translocation in common buckwheat,a marked increase in TF during the growth period was observed in plants treated with selenate,followed by treatment with the combination of selenite and selenate,whereas plants supplemented with only selenite showed an inverse trend in TF values over the growing season.Plants absorb and translocate selenate via sulfur transporters,and selenate is further metabolized in leaves[34];these factors may account for the high TF values of plants with selenate supplementation.There could also be a difference in translocation efficiency between selenate and selenite owing to the type of transporters involved[15].Li et al.[35]also reported selenate was translocated to shoots immediately after absorption but that selenite tended to be converted into other organic forms of Se and be stored in the root,explaining the low TF values of selenite-treated plants observed in our study.However,TF values in Se(VI)-treated plants were more than twice those of plants treated with 1/2 Se(IV+VI),suggesting that selenite supplementation might inhibit the translocation of total Se from root to shoot when selenite and selenate interact.Also,a reduction in Se use efficiency was observed in both study years when the plants matured(i.e.,DAS75)(Table 4).These results were comparable with those of a previous study[27],suggesting that most Se applied was retained in the soil environment or volatilized to the atmosphere.The decrease in Se use efficiency may also have been due to an initially high Se uptake rate,which depleted Se in the soil,limiting its availability during the growth period.

5.Conclusions

Our results showed that 40 g Se ha?1applied as selenate yielded average Se concentrations of 256 μg kg?1in seeds of common buckwheat grown under experimental soil conditions in northeastern China,followed by Se concentrations in seeds treated with other two Se application strategies,whereas treatment without Se yielded low seed Se concentrations.In addition to seed Se accumulation,a decreasing trend of Se accumulation in shoots and roots over the entire growth period was observed for all forms of Se.Se applied as selenite reduced translocation of Se from root to shoot,owing partly to the tendency for Se accumulation in the root tissues.With respect to grain yield and biomass production,the 40 g ha?1Se application showed a slight inhibitory effect on seedling growth.There were no significant effects on biomass production as plants matured(DAS45 and DAS60),but biomass accumulation and grain yield increased under combined treatment with selenate and selenite.These results could provide useful information for crop Se biofortification in regions with similar soil and climatic conditions around the world.

Acknowledgments

Funding of this work was provided by the China Agriculture Research System(CARS-08-B-1)to Y.G.Hu,as well as by Special Fund for Agro-scientific Research in the Public Interest(201503121-11)to Z.H.Zeng.The authors thank the China Scholarship Council for providing a graduate research fellowship to Y.Jiang as a joint Ph.D.student at Colorado State University for one year(201606350049).

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