Elsevier

Geoderma

Volume 369, 15 June 2020, 114315
Geoderma

Selenium biofortification of crops on a Malawi Alfisol under conservation agriculture

https://doi.org/10.1016/j.geoderma.2020.114315Get rights and content

Highlights

  • Selenium at 20 g ha−1 raises dietary levels above the recommended dietary allowance.

  • Selenium fixation into humus-bound forms eliminates residual availability.

  • Conservation agriculture treatments have little effect on selenium uptake by maize.

  • Legumes (e.g. groundnuts) accumulate greater concentrations of selenium than maize.

Abstract

Biofortification with selenium (Se) may rely on rapid uptake by crops, following application, to offset progressive fixation into unavailable organic forms of Se in soil. A biofortification study was conducted on an Alfisol within a long-term conservation agriculture (CA) field trial at Chitedze Research Station, Malawi. The aim was to assess the dynamics of selenium bioavailability to a staple cereal (Zea mays) and a range of legumes (cowpeas, groundnuts, pigeon peas and velvet beans) under CA management, as well as residual Se effects in the year following biofortification. Isotopically labelled selenate (>99% enriched 77SeVI) was applied to each plot, in solution, at a rate of 20 g ha−1, at maize flowering (75 days after planting), in February 2017. Samples of grain and stover from maize and legumes, and topsoil, were collected at harvest in May 2017 and May 2018. Plant and soil samples were analyzed by ICP-MS for selenium isotopes (77Se and 78Se). The concentration of 77Se in the grain of maize and single-cropped legumes exceeded 200 µg kg−1 in all the treatments. This would contribute approximately 56–64 µg day−1 to the Malawi diet, as refined maize flour. The fertilizer derived Se concentration ratio of maize grain-to-stover Se were >1 in 2017 but <1 in 2018; which followed the same trend as the native soil-derived Se in the residual year. In legumes the grain-to-stover concentration ratio was consistently <1 in both years, except for the velvet beans. Differences in CA management had minimal influence on 77Se concentration in plant grain but the low yield in the single conventional treatment reduced 77Se uptake. Residual 77Se in the soil (35% of the applied) measured at harvest in 2017 was still present at harvest in the residual year (2018) but was completely unavailable to any of the crops. Almost none of the remaining 77Se was present in soluble or phosphate-extractable forms and virtually all was present in the ‘organic’ (TMAH-extractable) fraction. Thus, annual Se applications to maize would be necessary to maintain concentrations which could improve dietary supply and reduce current Se deficiency in Malawi.

Introduction

Selenium (Se) is a trace element with an essential nutritional role in human and animal health. Selenium deficiency in humans has been linked to thyroid gland dysfunction, irreversible brain damage, peripheral vascular diseases, chronic and degenerative osteoarthropathy (Kashin–Beck disease), impaired immune response to viral infections, male infertility, pre-eclampsia in women, heart diseases and higher risks for several types of cancers (Cardoso et al., 2015, Fairweather-tait et al., 2011, Riaz and Mehmood, 2012). According to the Institute of Medicine of the USA National Academy, the Se recommended dietary allowance (RDA) for Se is 55 µg day−1 for adults while the tolerable upper intake for adults is 400 µg day−1 (Bendich, 2001).

Dietary Se intake can be strongly related to the availability of Se in soil (Fairweather-Tait et al., 2011; Rayman, 2008), especially where populations depend on local food production in Se-deficient regions. The bioavailability of selenium in soil depends on supply factors, such as parent material and atmospheric inputs, and on soil factors that affect the strength of Se sorption such as pH and the concentration of soil organic matter and hydrous oxides of Fe, Al and Mn (Fordyce et al., 2000, Lopes et al., 2017, Rayman, 2008). It is recognized that selenite ions (HSeO3, SeO32−) are adsorbed strongly on hydrous oxides at low pH (3.5–6.5). However, most Se in soils is usually organically bound in humus and there is evidence that different forms of humus can give rise to differences in Se bioavailability (Qin et al., 2012). It has also been shown that soil microbial processes have some involvement in the control of inorganic Se availability (Tolu et al., 2014). In highly weathered, acidic, oxide-rich tropical soils, as found in Malawi, low bioavailable Se presents a serious restriction to dietary Se supply with estimates of 70% of the population eating insufficient Se with an average daily intake range of 27–45 μg capita−1 day−1 (Chilimba et al., 2011, Hurst et al., 2013, Joy et al., 2015a, Joy et al., 2015b) which is in close agreement with national plasma Se data for adult women (Phiri et al., 2019).

Dietary intake of Se can be increased through agronomic ‘biofortification’ of crops (Chilimba et al., 2012a, Mathers et al., 2017) with application as Se-containing fertilizers applied to soil or as foliar sprays (Lopes et al., 2017). In particular, the success of agronomic biofortification of staple cereal crops is well recognized (Broadley et al., 2010, Chilimba et al., 2012a, Chilimba et al., 2014). The use of selenium-enriched fertilizers was the public-health solution successfully adopted in 1984 by Finland, that resulted in an increase in Se intake from 38 µg d−1, before fortification, to 80 µg d−1 in 2000, assuming a daily energy intake of 10 MJ (Broadley et al., 2006, Eurola and Hietaniemi, 2000, Hartikainen, 2005).

The use of enriched Se isotopes as tracers in field experimentation permits discrimination between soil-derived and fertilizer-derived Se in crops and, potentially, allows the examination of residual effects of Se application in soil and crops. The approach has been made possible by advances in ICP-MS technology, the commercial availability of several enriched stable Se isotopes and the fact that comparatively small Se additions are required on a field plot scale (c. 1 mg m−2) for realistic biofortification results. To date, there have been relatively few studies that have utilized this approach in field experiments. Chilimba et al. (2012b) studied uptake of 74Se in maize in Malawi; Mathers et al. (2017) used 77Se to audit the fate of Se applied to wheat in U.K. soils. More recently, Ligowe et al. (2020) used enriched 77Se to characterize uptake and residual availability to green vegetables grown in an Oxisol, Alfisol and Vertisol from Malawi (Ligowe et al., 2020).

Conservation agriculture (CA) that focuses on minimum soil disturbance, the retention of crop residues and crop diversification, is one of the cropping systems which has been heavily promoted in recent years in southern Africa (Thierfelder and Wall, 2010, Thierfelder et al., 2017, Kassam et al., 2009). In addition to providing a coping strategy for climate change (Branca et al., 2011, Lipper et al., 2014, Steward et al., 2019), conservation agriculture is widely reported to improve soil health and crop yield through partly increased soil organic matter (Ligowe et al., 2017, Ngwira et al., 2012, Powlson et al., 2016).

The aim of this study was to examine the viability of Se biofortification in an Alfisol, managed under CA, and representing typical agronomic circumstances in Malawi and, more broadly, in sub-Saharan countries. We used application of 77Se-enriched selenate (77SeFert) to sub-plots of maize and selected legumes (cowpea, ground nuts, pigeon peas and velvet beans) within an established CA rotational and intercropped trial. The objectives were (i) to assess Se availability, uptake and translocation within crops and (ii) to quantify residual effects of Se application in the following season.

Section snippets

Study location

The study was carried out within a long-term CA trial situated at Chitedze Research Station (CRS), Malawi. The CRS is located on the Lilongwe-Kasungu plains (13.973 S, 33.654 E) at 1145 m above sea level. The soils are Ferruginous Latosols, classed as Alfisols under the USDA Soil Taxonomy (USDA, 1975) which are deep and free-draining with a well-developed structure. In the first year of the trial establishment (2007), baseline topsoil (0–10 cm) analysis showed the following average values for

Maize

In the year of 77SeFert biofortification (2017) the concentrations of 77SeFert in maize grain had a restricted range across all CA treatments (217 ± 27 µg kg−1), including the conventionally cultivated maize plots, and showed no difference between treatments (Table 3, Table 4). The results confirm the potential of fertilizer to increase Se in staple grain as has been demonstrated in previous studies (Broadley et al., 2010, Broadley et al., 2006, Chilimba et al., 2012a, Mathers et al., 2017).

In

Conclusions

A single application of 77Se to crops grown either under CA or conventional cropping systems, at the grain filling stage, provides a viable approach to Se biofortification. Application of 20 g ha−1 Se produced sufficient grain Se enrichment in maize and legumes to provide the recommended dietary Se requirement. The additional organic inputs to the soil through CA cropping systems has no apparent influence on the rapid fixation of applied 77Se. The transformation of applied selenate was almost

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

Funding and support for this study were provided by the Royal Society - Department for International Development (RS-DFID) Africa Capacity Building Initiative Grant AQ140000 “Strengthening African Capacity in Soil Geochemistry to inform Agricultural and HealthPolicies”, The Malawi Government (Ministry of Agriculture and Food Security – Department of Agricultural Research), Lilongwe University of Agriculture and Natural Resources, the University of Nottingham and the British Geological Survey.

References (51)

  • P.R. Steward et al.

    Conservation agriculture enhances resistance of maize to climate stress in a Malawian medium-term trial

    Agric. Ecosyst. Environ.

    (2019)
  • J. Tolu et al.

    Distribution and speciation of ambient selenium in contrasted soils, from mineral to organic rich

    Sci. Total Environ.

    (2014)
  • C. Thierfelder et al.

    Effects of conservation agriculture techniques on infiltration and soil water content in Zambia and Zimbabwe

    Soil Tillage Res.

    (2009)
  • J. Abadassi

    Cowpea (Vigna unguiculata (L.) Walp.) agronomic traits needed in tropical zone

    Int. J. Pure Appl. Biosci.

    (2015)
  • A. Bendich

    Dietary reference intakes for vitamin C, vitamin E, selenium, and carotenoids

    J. Nutr. Philadelphia

    (2001)
  • G. Branca et al.

    Climate-smart Agriculture: A Synthesis of Empirical Evidence of Food Security and Mitigation Benefits from Improved Cropland Management. Mitigation of Climate Change in Agriculture Series 3

    (2011)
  • M.R. Broadley et al.

    Selenium biofortification of high-yielding winter wheat (Triticum aestivum L.) by liquid or granular Se fertilisation

    Plant Soil

    (2010)
  • M.R. Broadley et al.

    Biofortification of UK food crops with selenium

    Proc. Nutr. Soc.

    (2006)
  • B.R. Cardoso et al.

    Selenium, selenoproteins and neurodegenerative diseases

    Metallomics

    (2015)
  • A.D.C. Chilimba et al.

    Maize grain and soil surveys reveal suboptimal dietary selenium intake is widespread in Malawi

    Sci. Rep.

    (2011)
  • A.D.C. Chilimba et al.

    Agronomic bio-fortification of maize, soyabean and groundnuts with selenium in intercropping and sole cropping systems

    Afr. J. Agric. Res.

    (2014)
  • M. Eurola et al.

    Report of the Selenium Monitoring Programme 1997–1999. Publications of Agricultural Research Centre of Finland Series B 24

    (2000)
  • F. Eick et al.

    Food intake of selenium and sulphur amino acids in tuberculosis patients and healthy adults in Malawi

    Int. J. Tuberculosis Lung Dis.

    (2009)
  • S.J. Fairweather-tait

    Selenium in human health and disease

    Antioxid. Redox Signal.

    (2011)
  • U.C. Gupta et al.

    Selenium content of barley as influenced by selenite-enriched and selenite enriched fertilizers

    Commun. Soil Sci. Plant Anal.

    (1993)
  • Cited by (21)

    • The importance of selenium in food enrichment processes. A comprehensive review

      2023, Journal of Trace Elements in Medicine and Biology
    • Effect of Enterobacter sp. EG16 on Selenium biofortification and speciation in pak choi (Brassica rapa ssp. chinensis)

      2023, Scientia Horticulturae
      Citation Excerpt :

      While the mutual effects of different concentrations of PGPR and Se on Se biofortification have rarely been explored(Izydorczyk et al., 2021; Patel et al., 2018). Further, the beneficial or toxic effects of Se are dose-dependent (D'Amato et al., 2020; Lessa et al., 2020; Lidon et al., 2018; Ligowe et al., 2020; Lindblom et al., 2018; Puccinelli et al., 2017; Ramos et al., 2020; Silva et al., 2019; Versini et al., 2016). For example, although biomass production was not significantly affected, the root biomass was reduced when the Se concentration reached to 12 mg L−1 grown in hydroponics(Puccinelli et al., 2017).

    • Geochemistry of selenium, barium, and iodine in representative soils of the Brazilian Amazon rainforest

      2022, Science of the Total Environment
      Citation Excerpt :

      The digestion programs are detailed in Table S4. Soluble (SeSol) and adsorbed (SeAd) Se were sequentially extracted with 0.01 mol L−1 KNO3 being used for the soluble fraction, and 0.016 mol L−1 KH2PO4 for the adsorbed fraction (Ligowe et al., 2020). The analytical determinations of SeTot, SeSol, SeAd, and BaTot were performed using Inductively Coupled Plasma-Mass Spectrometry (ICP-MS, X-Series II, Thermo Fisher Scientific).

    • Global soil distribution, dietary access routes, bioconversion mechanisms and the human health significance of selenium: A review

      2021, Food Bioscience
      Citation Excerpt :

      In general, Se deficiency diseases are dependent on the poor expression of selenoproteins and in their respective bioactivities (Benstoem et al., 2015; Fairweather-Tait et al., 2011). This is often attributed to the low Se bioavailability globally (Deng et al., 2017; Dinh et al., 2018; Ligowe et al., 2020; Ullah et al., 2019). Selenosis is a toxicological consequence of Se over-consumption (MacFarquhar et al., 2010) occurring mainly in high Se environments (Dinh et al., 2018).

    • Selenium speciation and bioaccessibility in Se-fertilised crops of dietary importance in Malawi

      2021, Journal of Food Composition and Analysis
      Citation Excerpt :

      The CA trial consists of ten agronomic management treatments including a control representing conventional cultivation methods, arranged in a randomised block design with four replicates per treatment. The grains were harvested from a sub-plot of the ten management treatments (Table 1) where an isotopically enriched potassium selenate solution (>99% enriched 77Se, purchased from Isoflex, San Francisco, USA) had been applied to soil at a rate of 20 g ha−1 75 days after planting, or at the maize tasselling stage (Ligowe et al., 2020c). Grains were carefully cleaned and dried to constant weight in an oven at 40 °C after which they were milled using a centrifugal mill (Model SM100, Retsch).

    View all citing articles on Scopus
    View full text