Higher iron pearl millet (Pennisetum glaucum L.) provides more absorbable iron that is limited by increased polyphenolic content

Elad Tako, Spenser M Reed, Jessica Budiman, Jonathan J Hart, Raymond P Glahn, Elad Tako, Spenser M Reed, Jessica Budiman, Jonathan J Hart, Raymond P Glahn

Abstract

Background: Our objective was to compare the capacity of iron (Fe) biofortified and standard pearl millet (Pennisetum glaucum L.) to deliver Fe for hemoglobin (Hb)-synthesis. Pearl millet (PM) is common in West-Africa and India, and is well adapted to growing areas characterized by drought, low-soil fertility, and high-temperature. Because of its tolerance to difficult growing conditions, it can be grown in areas where other cereal crops, such as maize, would not survive. It accounts for approximately 50% of the total world-production of millet. Given the widespread use of PM in areas of the world affected by Fe-deficiency, it is important to establish whether biofortified-PM can improve Fe-nutriture.

Methods: Two isolines of PM, a low-Fe-control ("DG-9444", Low-Fe) and biofortified ("ICTP-8203 Fe",High-Fe) in Fe (26 μg and 85 μg-Fe/g, respectively) were used. PM-based diets were formulated to meet the nutrient requirements for the broiler (Gallus-gallus) except for Fe (Fe concentrations were 22.1±0.52 and 78.6±0.51 μg-Fe/g for the Low-Fe and High-Fe diets, respectively). For 6-weeks, Hb, feed-consumption and body-weight were measured (n = 12).

Results: Improved Fe-status was observed in the High-Fe group, as suggested by total-Hb-Fe values (15.5±0.8 and 26.7±1.4 mg, Low-Fe and High-Fe respectively, P<0.05). DMT-1, DcytB, and ferroportin mRNA-expression was higher (P<0.05) and liver-ferritin was lower (P>0.05) in the Low-Fe group versus High-Fe group. In-vitro comparisons indicated that the High-Fe PM should provide more absorbable-Fe; however, the cell-ferritin values of the in-vitro bioassay were very low. Such low in-vitro values, and as previously demonstrated, indicate the presence of high-levels of polyphenolic-compounds or/and phytic-acid that inhibit Fe-absorption. LC/MS-analysis yielded 15 unique parent aglycone polyphenolic-compounds elevated in the High-Fe line, corresponding to m/z = 431.09.

Conclusions: The High-Fe diet appeared to deliver more absorbable-Fe as evidenced by the increased Hb and Hb-Fe status. Results suggest that some PM varieties with higher Fe contents also contain elevated polyphenolic concentrations, which inhibit Fe-bioavailability. Our observations are important as these polyphenols-compounds represent potential targets which can perhaps be manipulated during the breeding process to yield improved dietary Fe-bioavailability. Therefore, the polyphenolic and phytate profiles of PM must be carefully evaluated in order to further improve the nutritional benefit of this crop.

Figures

Figure 1
Figure 1
Iron status parameters of chicken fed the tested diets from days 0- 421. (A) Hb (g/L), (B) Total body Hb-Fe content (mg), and (C) % HME. 1Values are mean daily feed intakes for the 7 days preceding the day designated in the column heading (n=12).
Figure 2
Figure 2
Duodenal mRNA expression of DMT-1, DcytB, and ferroportin on day 42.1Changes in mRNA expression are shown relative to expression of 18S rRNA in arbitrary units (AU, n = 12, P < 0.05).

References

    1. WHO . Iron deficiency anemia assessment, prevention and control. A guide for program managers. Geneva: WHO/NDH; 2001. pp. 15–21.
    1. Nestel P, Bouis HE, Meenakshi JV, Pfeiffer W. Biofortification of staple food crops. J Nutr. 2006;136:1064–7.
    1. Bouis HE. Plant breeding: a new tool for fighting micronutrient malnutrition. J Nutr. 2002;132:S491–4.
    1. Murgia I, Arosio P, Tarantino D, Soave C. Biofortification for combating ‘hidden hunger’ for iron. Trends Plant Sci. 2012;17(1):47–55. doi: 10.1016/j.tplants.2011.10.003.
    1. Fanzo J, Reman R, Pronyk PM, Negin J, Wariero J, Mutuo P, et al. In: A 3-year cohort study to assess the impact of an integrated food- and livelihood-based model on undernutrition in rural western Kenya. Combating micronutrient deficiencies: food based approaches. Thompson B, Amoroso L, et al., editors. Rome: FAO; 2011. p. 76.
    1. Bhargava A, Bouis HE, Scrimshaw NS. Dietary intakes and socioeconomic factors are associated with the hemoglobin concentration of Bangladeshi women. J Nutr. 2001;131:758–64.
    1. Lozoff B, Jimenez E, Wolf AW. Long-term developmental outcome of infants with iron deficiency. N Engl J Med. 1991;325(10):687–94. doi: 10.1056/NEJM199109053251004.
    1. Rao P, Birthal PS, Reddy BVS, Belum VS, Rai KN, Ramesh S. Diagnostics of sorghum and pearl millet grains-based nutrition in India. Int Sor Mil News. 2006;47:93–6.
    1. Govindaraj M, Rai KN, Shanmugasundaram P, Dwivedi SL, Sahrawat KL, Muthaiah AR, et al. Combining Ability and Heterosis for Grain Iron and Zinc Densities in Pearl Millet. Crop Sci. 2013;53(2):507–17. doi: 10.2135/cropsci2012.08.0477.
    1. Agte VV, Khot S, Girigosavi ST, Paknikar KM, Chiplonkar SA. Comparative performance of pearl millet- and sorghum- based diets vs. wheat- and rice-based diets for trace metal bioavailability. J Trace Elem Med Biol. 1999;13(4):215–9. doi: 10.1016/S0946-672X(99)80038-8.
    1. Kodkany BS, Bellad RM, Mahantshetti NS, Westcott JE, Krebs NF, Kemp JF, et al. Biofortification of pearl millet with iron and zinc in a randomized controlled trial increases absorption of these minerals above physiologic requirements in young children. J Nutr. 2013;143(9):1489–93. doi: 10.3945/jn.113.176677.
    1. Pucher A, Hogh-Jensen H, Gondah J, Hash CT, Haussmann BIG. Micronutrient Density and Stability in West African Pearl Millet– Potential for Biofortification. Crop Sci. 2014;54:1709–20. doi: 10.2135/cropsci2013.11.0744.
    1. Board on Science and Technology for International Development; Office of International Affairs, National Research Council . Pearl Millet: Subsistence Types. Lost Crops of Africa. Washington DC: National Academies Press; 1996. pp. 1–108.
    1. Vadez V, Hash T, Bidinger FR, Kholova J. Phenotyping pearl millet for adaptation to drought. Front Physiol. 2012;3(386):1–12.
    1. Ejeta G, Hassen MM, Mertz ET. In vitro digestibility and amino acid composition of pearl millet (Pennisetum typhoides) and other cereals. Proc Natl Acad Sci U S A. 1987;84:6016–9. doi: 10.1073/pnas.84.17.6016.
    1. Dykes L, Rooney LW. Sorghum and millet phenols and antioxidants. J Cereal Sci. 2006;44:236–51. doi: 10.1016/j.jcs.2006.06.007.
    1. Rai KN, Yadav OP, Rajpurohit BS, Patil HT, Govindaraj M, Khairwal IS, et al. Breeding pearl millet cultivars for high iron density with zinc density as an associated trait. J SAT Agric Res. 2013;11:1–7.
    1. Cercamondi CI, Egli IM, Mitchikpe E, Tossou F, Zeder C, Hounhouigan JD, et al. Total iron absorption by young women from iron-biofortified pearl millet composite meals is double that from regular millet meals but less than that from post-harvest iron-fortified millet meals. J Nutr. 2013;143(9):1376–82. doi: 10.3945/jn.113.176826.
    1. Tako E, Beebe SE, Reed S, Hart JJ, Glahn RP. Polyphenolic compounds appear to limit the nutritional benefit of biofortified higher iron black bean (Phaseolus vulgaris L.) Nutr J. 2014;13:28. doi: 10.1186/1475-2891-13-28.
    1. Tako E, Glahn RP. White Beans Provide More Bioavailable Iron than Red Beans: Studies in Poultry (Gallus gallus) and an in vitro Digestion/Caco-2 Model. Int J Vitam Nutr Res. 2011;81(1):1–14.
    1. Tako E, Rutzke MA, Glahn RP. Using the domestic chicken (Gallus gallus) as an in vivo model for iron bioavailability. Poult Sci. 2010;89(3):514–21. doi: 10.3382/ps.2009-00326.
    1. Tako E, Glahn RP, Laparra JM, Welch RM, Lei X, Kelly JD, et al. Iron and zinc bioavailabilities to pigs from red and white beans (Phaseolus vulgaris L.) are similar. J Agric Food Chem. 2009;57:3134–40. doi: 10.1021/jf803647m.
    1. Tako E, Laparra M, Glahn RP, Welch RM, Lei X, Beebe S, et al. Biofortified black beans in a maize and bean diet provide more bioavailable iron to piglets than standard black beans. J Nutr. 2009;139:305–9. doi: 10.3945/jn.108.098657.
    1. Tako E, Blair MW, Glahn RP. Biofortified red mottled beans (Phaseolus vulgaris L.) in a maize and bean diet provide more bioavailable iron than standard red mottled beans: Studies in poultry (Gallus gallus) and an in vitro digestion/Caco-2 model. Nutr J. 2011;10:113. doi: 10.1186/1475-2891-10-113.
    1. Tako E, Hoekenga OA, Kochian LV, Glahn RP. High bioavailablilty iron maize (Zea mays L.) developed through molecular breeding provides more absorbable iron in vitro (Caco-2 model) and in vivo (Gallus gallus) Nutr J. 2013;12:3. doi: 10.1186/1475-2891-12-3.
    1. Tako E, Glahn RP, Knez M, Stangoulis JCR. The effect of wheat prebiotics on the gut bacterial population and iron status of iron deficient broiler chickens. Nutr J. 2014;13:58. doi: 10.1186/1475-2891-13-58.
    1. Hart JJ, Glahn RP. Identification of bean polyphenols that inhibit and enhance iron uptake by Caco-2 cells [abstract] FASEB J. 2013;27:634.13.
    1. Mira L, Fernandez MT, Santos M, Rocha R, Florencio MH, Jennings KR. Interactions of flavonoids with iron and copper ions: a mechanism for their antioxidant activity. Free Radic Res. 2002;36(11):1199–208. doi: 10.1080/1071576021000016463.
    1. Benheral PS, Arumughan C. Studies on modulation of DNA integrity in Fenton’s system by phtytochemicals. Mutat Res. 2008;648(1–2):1–8. doi: 10.1016/j.mrfmmm.2008.09.001.
    1. Mladěnka P, Macáková K, Filipský T, Zatloukalová L, Jahodář L, Bovicelli P, et al. In vitro analysis of iron chelating activity of flavonoids. J Inorg Biochem. 2011;105(5):693–701. doi: 10.1016/j.jinorgbio.2011.02.003.
    1. Perez CA, Wei Y, Guo M. Iron-binding and anti-Fenton properties of baicalein and baicalin. J Inorg Biochem. 2009;103(3):326–32. doi: 10.1016/j.jinorgbio.2008.11.003.
    1. Park SS, Bae I, Lee YJ. Flavonoids-induced accumulation of hypoxia-inducible factor (HIF)-1alpha/2alpha is mediated through chelation of iron. J Cell Biochem. 2008;103(6):1989–98. doi: 10.1002/jcb.21588.
    1. Persichini T, Maio N, di Patti MC, Rizzo G, Colasanti M, Musci G. Genistein up-regulates the iron efflux system in glial cells. Neurosci Lett. 2010;470(2):145–9. doi: 10.1016/j.neulet.2009.12.074.
    1. Wang LS, Sun XD, Cao Y, Wang L, Li FJ, Wang YF. Antioxidant and pro-oxidant properties of acylated pelargonidin derivatives extracted from red radish (Raphanus sativus var. niger, Brassicaceae) Food Chem Toxicol. 2010;48(10):2712–8. doi: 10.1016/j.fct.2010.06.045.
    1. Haussmann BIG, Rattunde FH, Weltzien-Rattunde E, Traore PCS, Vom Brocke K, Parzies HK. Breeding Strategies for Adaptation of Pearl Millet and Sorghum to Climate Variability and Change in West Africa. J Agron Crop Sci. 2012;198:327–39. doi: 10.1111/j.1439-037X.2012.00526.x.
    1. Haas JD, Finkelstein JD, Udipi SA, Ghugre P, Mehta S. Iron Biofortified Pearl Millet Improves Iron Status in Indian School Children: Results of a Feeding Trial [abstract] FASEB J. 2014;27:355.2.
    1. Brune M, Rossander L, Hallberg L. Iron-absorption and phenolic-compounds - importance of different phenolic structures. Eur J Clin Nutr. 1989;43:547–58.
    1. Hurrell RF, Reddy M, Cook JD. Inhibition of non-haem iron absorption in man by polyphenolic-containing beverages. Br J Nutr. 1999;81:289–95.
    1. Hallberg L, Rossander L. Effect of different drinks on the absorption of non-heme iron from composite meals. Hum Nutr Appl Nutr. 1982;36:116–23.
    1. Ramachandra G, Virupaksha TK, Shadaksharaswamy M. Relationship between tannin levels and in vitro protein digestability in finger millet (Eleusine coracana Gaertn) J Agric Food Chem. 1997;25:1101–4. doi: 10.1021/jf60213a046.
    1. Reichert RD. The pH-sensitive pigments in pearl millet. Cereal Chem. 1979;56:291–4.
    1. Chethan S, Sreerama YN, Malleshi NG. Mode of inhibition of finger millet malt amylases by the millet phenolics. Food Chem. 2008;111:187–91. doi: 10.1016/j.foodchem.2008.03.063.
    1. Devi PB, Vijayabharathi R, Sathyabama S, Malleshi NG, Priyadarisini VB. Health benefits of finger millet (Eleusine coracana L.) polyphenols and dietary fiber: a review. J Food Sci Technol. 2014;51(6):1021–40. doi: 10.1007/s13197-011-0584-9.
    1. Salunkhe DK, Jadhav SJ, Kadam SS, Chavan JK. Chemical, biochemical, and biological significance of polyphenols in cereals and legumes. Crit Rev Food Sci Nutr. 1982;17(3):277–305. doi: 10.1080/10408398209527350.
    1. Scalbert A, Johnson IT, Saltmarsh M. Polyphenols: antioxidants and beyond. Am J Clin Nutr. 2005;81:2155–75.

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