BACKGROUND: Selenium (Se) and zinc (Zn) are essential antioxidant enzyme cofactors. Foliar Se/Zn application is a highly effective method of plant biofortification. However, little is known about the effect of such applications on the concentration of trace elements and phytochemicals with pro-oxidant or antioxidant activity in pea (Pisum sativum L.). METHODS: A 2-year pot experiment (2014/2015) was conducted to examine the response of two pea varieties (Ambassador and Premium) to foliar-administered sodium selenate (0/50/100 g Se/ha) and zinc oxide (0/375/750 g Zn/ha) at the flowering stage. Concentrations of selected trace elements (Fe, Cu, and Mn), total phenolic content (TPC), total flavonoid content (TFC), and total antioxidant activity (ABTS, FRAP) of seeds were determined. RESULTS AND CONCLUSIONS: Se/Zn treatments did not improve the concentration of trace elements, while they generally enhanced TPC. Among examined treatments, the highest TPC was found in Ambassador (from 2014) treated with 100 g Se/ha and 750 g Zn/ha (2,926 and 3,221 mg/100 g DW, respectively) vs. the control (1,737 mg/100 g DW). In addition, 50 g of Se/ha increased TFC vs. the control (261 vs. 151 mg/100 g DW) in Premium (from 2014), 750 g of Zn/ha increased ABTS vs. the control (25.2 vs. 59.5 mg/100 g DW) in Ambassador (from 2015), and 50 g of Se/ha increased FRAP vs. the control (26.6 vs. 18.0 mmol/100 g DW) in Ambassador (from 2015). In linear multivariable regression models, Zn, Mn, Cu, and TPC best explained ABTS (R = 0.577), while Se, Cu, and TPC best explained the FRAP findings (R = 0.696). This study highlights the potential of foliar biofortification with trace elements for producing pea/pea products rich in bioactive plant metabolites beneficial for human health.

Department of Plant Protection Crop Research Institute Prague Czechia

Institute of Horticulture Faculty of Horticulture and Landscape Engineering Slovak University of Agriculture in Nitra Nitra Slovakia

Laboratory of Analytical Chemistry and Applied Ecochemistry Department of Green Chemistry and Technology Faculty of Bioscience Engineering Ghent University Ghent Belgium

Nutrition and Health Research Group Department of Precision Health Luxembourg Institute of Health Strassen Luxembourg

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Singh B, Singh JP, Kaur A, Singh N. Phenolic composition and antioxidant potential of grain legume seeds: a review. Food Res Int. (2017) 101:1–16. 10.1016/j.foodres.2017.09.026 PubMed DOI

Lecour S, Lamont KT. Natural polyphenols and cardioprotection. Mini-Rev Med Chem. (2011) 11:1191–9. 10.2174/13895575111091191 PubMed DOI

Ouchemoukh S, Amessis-Ouchemoukh N, Gómez-Romero M, Aboud F, Giuseppe A, Fernández-Gutiérrez A, et al. . Characterisation of phenolic compounds in Algerian honeys by RP-HPLC coupled to electrospray time-of-flight mass spectrometry. LWT Food Sci Technol. (2017) 85:460–9. 10.1016/j.lwt.2016.11.084 DOI

Bravo L. Polyphenols: chemistry, dietary sources, metabolism, and nutritional significance. Nutr Rev. (1998) 56:317–33. PubMed

Alasalvar C, Grigor JM, Zhang D, Quantick PC, Shahidi F. Comparison of volatiles, phenolics, sugars, antioxidant vitamins, and sensory quality of different colored carrot varieties. J Agric Food Chem. (2001) 49:1410–6. 10.1021/jf000595h PubMed DOI

Naumovski N. Bioactive composition of plants and plant foods. In:Scarlett CJ, Vuong QV, editors. Plant Bioactive Compounds for Pancreatic Cancer Prevention and Treatment. New York, NY: Nova Science Publishers; (2015). p. 81–115.

Vagiri M, Johansson E, Rumpunen K. Phenolic compounds in black currant leaves: an interaction between the plant and foliar diseases? J Plant Interact. (2017) 12:193–9. 10.1080/17429145.2017.1316524 DOI

Naczk M, Shahidi F. Phenolics in cereals, fruits and vegetables: occurrence, extraction and analysis. J Pharm Biomed Anal. (2006) 41:1523–42. 10.1016/j.jpba.2006.04.002 PubMed DOI

Ksouri R, Megdiche W, Falleh H, Trabelsi N, Boulaaba M, Smaoui A, et al. . Influence of biological, environmental and technical factors on phenolic content and antioxidant activities of Tunisian halophytes. Comptes Rendus Biol. (2008) 331:865–73. 10.1016/j.crvi.2008.07.024 PubMed DOI

Zargoosh Z, Ghavam M, Bacchetta G, Tavili A. Effects of ecological factors on the antioxidant potential and total phenol content of Scrophularia striata Boiss. Sci Rep. (2019) 9:16021. 10.1038/s41598-019-52605-8 PubMed DOI PMC

Bhuyan DJ, Basu A. Phenolic compounds: potential health benefits and toxicity. In:Vuong QV, editor. Utilisation of Bioactive Compounds from Agricultural and Food Waste. Boca Raton: CRC Press; (2017). p. 27–59. 10.1201/9781315151540-3 DOI

Cory H, Passarelli S, Szeto J, Tamez M, Mattei J. The role of polyphenols in human health and food systems: a mini-review. Front Nutr. (2018) 5:87. 10.3389/fnut.2018.00087 PubMed DOI PMC

Shahidi F, Yeo JD. Bioactivities of phenolics by focusing on suppression of chronic diseases: a review. Int J Mol Sci. (2018) 19:1573. 10.3390/ijms19061573 PubMed DOI PMC

Ozcan T, Akpinar-Bayizit A, Yilmaz-Ersan L, Delikanli B. Phenolics in human health. Int J Chem Eng Appl. (2014) 5:393–396. 10.7763/IJCEA.2014.V5.416 DOI

Zhao D, Shi D, Sun J, Li H, Zhao M, Sun B. Quantification and cytoprotection by vanillin, 4-methylguaiacol and 4-ethylguaiacol against AAPH-induced abnormal oxidative stress in HepG2 cells. RSC Adv. (2018) 8:35474–84. 10.1039/C8RA06505E PubMed DOI PMC

Chen J, He F, Liu S, Zhou T, Baloch S, Jiang C, et al. . Cytoprotective Effect of ligustrum robustum polyphenol extract against hydrogen peroxide-induced oxidative stress via Nrf2 signaling pathway in Caco-2 cells. Evid Based Compl Altern Med. (2019) 2019:6458. 10.1155/2019/5026458 PubMed DOI PMC

Rayman MP. Selenium and human health. Lancet. (2012) 379:1256–68. 10.1016/S0140-6736(11)61452-9 PubMed DOI

Zoidis E, Seremelis I, Kontopoulos N, Danezis GP. Selenium-dependent antioxidant enzymes: actions and properties of selenoproteins. Antioxidants. (2018) 7:66. 10.3390/antiox7050066 PubMed DOI PMC

Barchielli G, Capperucci A, Tanini D. The role of selenium in pathologies: an updated review. Antioxidants. (2022) 11:251. 10.3390/antiox11020251 PubMed DOI PMC

Kambe T, Tsuji T, Hashimoto A, Itsumura N. The physiological, biochemical, and molecular roles of zinc transporters in zinc homeostasis and metabolism. Physiol Rev. (2015) 95:749–84. 10.1152/physrev.00035.2014 PubMed DOI

Marreiro DDN, Cruz KJC, Morais JBS, Beserra JB, Severo JS, de Oliveira ARS. Zinc and oxidative stress: current mechanisms. Antioxidants. (2017) 6:24. 10.3390/antiox6020024 PubMed DOI PMC

Kaur K, Gupta R, Saraf SA, Saraf SK. Zinc: The metal of life. Compr Rev Food Sci Food Saf. (2014) 13:358–76. 10.1111/1541-4337.12067 PubMed DOI

Lee SR. Critical role of zinc as either an antioxidant or a prooxidant in cellular systems. Oxid Med Cell Longev. (2018) 2018:6285. 10.1155/2018/9156285 PubMed DOI PMC

Vallee BL. Zinc: biochemistry, physiology, toxicology and clinical pathology. Biofactors. (1988) 1:31–6. PubMed

Alexander J, Tinkov A, Strand TA, Alehagen U, Skalny A, Aaseth J. Early nutritional interventions with zinc, selenium and vitamin D for raising anti-viral resistance against progressive COVID-19. Nutrients. (2020) 12:2358. 10.3390/nu12082358 PubMed DOI PMC

Du Laing G, Petrovic M, Lachat C, De Boevre M, Klingenberg GJ, Sun Q, et al. . Course and survival of COVID-19 patients with comorbidities in relation to the trace element status at hospital admission. Nutrients. (2021) 13:3304. 10.3390/nu13103304 PubMed DOI PMC

Powers SE, Thavarajah D. Checking agriculture's pulse: field pea (P. sativum L.), sustainability, and phosphorus use efficiency. Front Plant Sci. (2019) 10:1489. 10.3389/fpls.2019.01489 PubMed DOI PMC

Ferreira H, Pinto E, Vasconcelos MW. Legumes as a cornerstone of the transition toward more sustainable agri-food systems and diets in Europe. Front Sustain Food Syst. (2021) 5:694121. 10.3389/fsufs.2021.694121 DOI

Sahruzaini NA, Rejab NA, Harikrishna JA, Khairul Ikram NK, Ismail I, Kugan HM, et al. . Pulse crop genetics for a sustainable future: where we are now and where we should be heading. Front Plant Sci. (2020) 11:531. 10.3389/fpls.2020.00531 PubMed DOI PMC

Ge J, Sun CX, Corke H, Gul K, Gan RY, Fang Y. The health benefits, functional properties, modifications, and applications of pea (P. sativum L.) protein: current status, challenges, and perspectives. Compr Rev Food Sci Food Saf. (2020) 19:1835–76. 10.1111/1541-4337.12573 PubMed DOI

Dahl WJ, Foster LM, Tyler RT. Review of the health benefits of peas (P. sativum L.). Br J Nutr. (2012) 108:S3–S10. 10.1017/S0007114512000852 PubMed DOI

Hegedusová A, Mezeyová I, Timoracká M, Šlosár M, Musilová J, Juríková T. Total polyphenol content and antioxidant capacity changes in dependence on chosen garden pea varieties. Potravinarstvo. (2015) 9:1–8. 10.5219/412 DOI

Fahim JR, Attia EZ, Kamel MS. The phenolic profile of pea (P. sativum): a phytochemical and pharmacological overview. Phytochem Rev. (2019) 18:173–98. 10.1007/s11101-018-9586-9 DOI

Kumari T, Deka SC. Potential health benefits of garden pea seeds and pods: a review. Legum Sci. (2021) 3:e82. 10.1002/leg3.82 DOI

Stanisavljević NS, Ilić MD, Matić IZ, Jovanović ŽS, Cupić T, Dabić D, et al. . Identification of phenolic compounds from seed coats of differently colored european varieties of pea (P. sativum L.) and characterization of their antioxidant and in vitro anticancer activities. Nutr Cancer. (2016) 68:988–1000. 10.1080/01635581.2016.1190019 PubMed DOI

El-Feky AM, Elbatanony MM, Mounier MM. Anti-cancer potential of the lipoidal and flavonoidal compounds from P. sativum and Vicia faba peels. Egy J Basic Appl Sci. (2018) 5:258–64. 10.1016/j.ejbas.2018.11.001 DOI

Delaqua D, Carnier R, Berton RS, Corbi FCA, Coscione AR. Increase of selenium concentration in wheat grains through foliar application of sodium selenate. J Food Compos Anal. (2021) 99:103886. 10.1016/j.jfca.2021.103886 DOI

Sattar A, Wang X, Ul-Allah S, Sher A, Ijaz M, Irfan M, et al. . Foliar application of zinc improves morpho-physiological and antioxidant defense mechanisms, and agronomic grain biofortification of wheat (Triticum aestivum L.) under water stress. Saudi J Biol Sci. (2021) 29:1699–706. 10.1016/j.sjbs.2021.10.061 PubMed DOI PMC

Malka M, Du Laing G, Li J, Bohn T. Separate foliar sodium selenate and zinc oxide application enhances Se but not Zn accumulation in pea (P. sativum L.) seeds. Front Plant Sci. (2022) 13:968324. 10.3389/fpls.2022.968324 PubMed DOI PMC

Poblaciones MJ, Rodrigo S, Santamaría O. Evaluation of the potential of peas (P. sativum L.) to be used in selenium biofortification programs under mediterranean conditions. Biol Trace Elem Res. (2013) 151:132–7. 10.1007/s12011-012-9539-x PubMed DOI

Bouayed J, Hoffmann L, Bohn T. Total phenolics, flavonoids, anthocyanins and antioxidant activity following simulated gastro-intestinal digestion and dialysis of apple varieties: bioaccessibility and potential uptake. Food Chem. (2011) 128:14–21. 10.1016/j.foodchem.2011.02.052 PubMed DOI

Kaulmann A, Jonville MC, Schneider YJ, Hoffmann L, Bohn T. Carotenoids, polyphenols and micronutrient profiles of Brassica oleraceae and plum varieties and their contribution to measures of total antioxidant capacity. Food Chem. (2014) 155:240–50. 10.1016/j.foodchem.2014.01.070 PubMed DOI

Troszyńska A, Ciska E. Phenolic Compounds of seed coats of white and coloured varieties of pea (P. sativum L.) and their total antioxidant activity. Czech J Food Sci. (2002) 20:15–22. 10.17221/3504-CJFS DOI

Dueñas M, Estrella I, Hernández T. Occurrence of phenolic compounds in the seed coat and the cotyledon of peas (P. sativum L.). Eur Food Res Technol. (2004) 219:116–23. 10.1007/s00217-004-0938-x DOI

Xu BJ, Yuan SH, Chang SKC. Comparative analyses of phenolic composition, antioxidant capacity, and color of cool season legumes and other selected food legumes. J Food Sci. (2007) 72:S167–77. 10.1111/j.1750-3841.2006.00261.x PubMed DOI

Campos-Vega R, Loarca-Piña G, Oomah BD. Minor components of pulses and their potential impact on human health. Food Res Int. (2010) 43:461–82. 10.1016/j.foodres.2009.09.004 DOI

Malka M, Du Laing G, Bohn T. Separate effects of foliar applied selenate and zinc oxide on the accumulation of macrominerals, macronutrients and bioactive compounds in two pea (P. sativum L.) seed varieties. Plants. (2022) 11:2009. 10.3390/plants11152009 PubMed DOI PMC

Poblaciones MJ, Rengel Z. The effect of processing on P. sativum L. biofortified with sodium selenate. J Plant Nutr Soil Sci. (2018) 181:932–7. 10.1002/jpln.201800251 DOI

Poblaciones MJ, Rengel Z. Combined foliar selenium and zinc biofortification in field pea (P. sativum): accumulation and bioavailability in raw and cooked grains. Crop Pasture Sci. (2017) 68:265–71. 10.1071/CP17082 DOI

Ros GH, van Rotterdam AMD, Bussink DW, Bindraban PS. Selenium fertilization strategies for bio-fortification of food: an agro-ecosystem approach. Plant Soil. (2016) 404:99–112. 10.1007/s11104-016-2830-4 DOI

Hasanuzzaman M, Bhuyan MB, Raza A, Hawrylak-Nowak B, Matraszek-Gawron R, Al Mahmud J, et al. . Selenium in plants: boon or bane? Environ Exp Bot. (2020) 178:104170. 10.1016/j.envexpbot.2020.104170 DOI

Hacisalihoglu G. Zinc (Zn): the last nutrient in the alphabet and shedding light on Zn efficiency for the future of crop production under suboptimal Zn. Plants. (2020) 9:1471. 10.3390/plants9111471 PubMed DOI PMC

Cartes P, Gianfreda L, Mora ML. Uptake of selenium and its antioxidant activity in ryegrass when applied as selenate and selenite forms. Plant Soil. (2005) 276:359–67. 10.1007/s11104-005-5691-9 DOI

Hartikainen H, Xue T, Piironen V. Selenium as an anti-oxidant and pro-oxidant in ryegrass. Plant Soil. (2000) 225:193–200. 10.1023/A:1026512921026 DOI

Mora ML, Pinilla L, Rosas A, Cartes P. Selenium uptake and its influence on the antioxidative system of white clover as affected by lime and phosphorus fertilization. Plant Soil. (2008) 303:139–49. 10.1007/s11104-007-9494-z DOI

Feng R, Wei C, Tu S, Wu F. Effects of Se on the uptake of essential elements in Pteris vittata L. Plant Soil. (2009) 325:123–32. 10.1007/s11104-009-9961-9 DOI

Ranieri A, Castagna A, Baldan B, Soldatini GF. Iron deficiency differently affects peroxidase isoforms in sunflower. J Exp Bot. (2001) 52:25–35. 10.1093/jexbot/52.354.25 PubMed DOI

Kayan N, Gulmezoglu N, Kaya MD. The optimum foliar zinc source and level for improving Zn content in seed of chickpea. Legum Res. (2015) 38:826–31. 10.18805/lr.v38i6.6731 DOI

Poblaciones MJ, Rengel Z. Soil and foliar zinc biofortification in field pea (P. sativum L.): grain accumulation and bioavailability in raw and cooked grains. Food Chem. (2016) 212:427–33. 10.1016/j.foodchem.2016.05.189 PubMed DOI

Fan X, Zhou X, Chen H, Tang M, Xie X. Cross-talks between macro- and micronutrient uptake and signaling in plants. Front Plant Sci. (2021) 12:663477. 10.3389/fpls.2021.663477 PubMed DOI PMC

Wang Q, Chen M, Hao Q, Zeng H, He Y. Research and progress on the mechanism of iron transfer and accumulation in rice grains. Plants. (2021) 10:2610. 10.3390/plants10122610 PubMed DOI PMC

Sinclair SA, Krämer U. The zinc homeostasis network of land plants. Biochim Biophys Acta. (2012) 1823:1553–67. 10.1016/j.bbamcr.2012.05.016 PubMed DOI

Connolly EL, Fett JP, Guerinot ML. Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell. (2002) 14:1347–57. 10.1105/tpc.001263 PubMed DOI PMC

Bindraban PS, Dimkpa C, Nagarajan L, Roy A, Rabbinge R. Revisiting fertilisers and fertilisation strategies for improved nutrient uptake by plants. Biol Fertil Soils. (2015) 51:897–911. 10.1007/s00374-015-1039-7 DOI

Ghasemi S, Khoshgoftarmanesh AH, Afyuni M, Hadadzadeh H. The effectiveness of foliar applications of synthesized zinc-amino acid chelates in comparison with zinc sulfate to increase yield and grain nutritional quality of wheat. Eur J Agron. (2013) 45:68–74. 10.1016/j.eja.2012.10.012 DOI

Cakmak I, Pfeiffer WH, McClafferty B. Biofortification of durum wheat with zinc and iron. Cereal Chem. (2010) 87:10–20. 10.1094/CCHEM-87-1-0010 DOI

Cakmak I, Torun A, Millet E, Feldman M, Fahima T, Korol A, et al. . Triticum dicoccoides: an important genetic resource for increasing zinc and iron concentration in modern cultivated wheat. Soil Sci Plant Nutr. (2004) 50:1047–54. 10.1080/00380768.2004.10408573 DOI

Hegedusová A, Mezeyová I, Hegedus O, Andrejiová A, Juríková T, Golian M, et al. . Increasing of selenium content and qualitative parameters in garden pea (P. sativum L.) after its foliar application. Acta Sci Pol Hortorum Cultus. (2017) 16:3–17. 10.24326/asphc.2017.6.1 DOI

Sabatino L, Ntatsi G, Iapichino G, D'Anna F, De Pasquale C. Effect of selenium enrichment and type of application on yield, functional quality and mineral composition of curly endive grown in a hydroponic system. Agronomy. (2019) 9:207. 10.3390/agronomy9040207 DOI

Saeedi M, Soltani F, Babalar M, Izadpanah F, Wiesner-Reinhold M, Baldermann S. Selenium fortification alters the growth, antioxidant characteristics and secondary metabolite profiles of cauliflower (Brassica oleracea var. botrytis) cultivars in hydroponic culture. Plants. (2021) 10:1537. 10.3390/plants10081537 PubMed DOI PMC

Golubkina N, Kekina H, Caruso G. Yield, quality and antioxidant properties of Indian mustard (Brassica juncea L.) in response to foliar biofortification with selenium and iodine. Plants. (2018) 7:80. 10.3390/plants7040080 PubMed DOI PMC

Zhu Z, Zhang Y, Liu J, Chen Y, Zhang X. Exploring the effects of selenium treatment on the nutritional quality of tomato fruit. Food Chem. (2018) 252:9–15. 10.1016/j.foodchem.2018.01.064 PubMed DOI

D'Amato R, Fontanella MC, Falcinelli B, Beone GM, Bravi E, Marconi O, et al. . Selenium biofortification in rice (Oryza sativa L.) sprouting: effects on se yield and nutritional traits with focus on phenolic acid profile. J Agric Food Chem. (2018) 66:4082–90. 10.1021/acs.jafc.8b00127 PubMed DOI

Groth S, Budke C, Neugart S, Ackermann S, Kappenstein FS, Daum D, et al. . Influence of a selenium biofortification on antioxidant properties and phenolic compounds of apples (Malus domestica). Antioxidants. (2020) 9:187. 10.3390/antiox9020187 PubMed DOI PMC

Majdoub N, El-Guendouz S, Rezgui M, Carlier J, Costa C, Kaab LBB, et al. . Growth, photosynthetic pigments, phenolic content and biological activities of Foeniculum vulgare Mill, Anethum graveolens L and Pimpinella anisum L (Apiaceae) in response to zinc. Ind Crops Prod. (2017) 109:627–36. 10.1016/j.indcrop.2017.09.012 DOI

Song CZ, Liu MY, Meng JF, Chi M, Xi ZM, Zhang ZW. Promoting effect of foliage sprayed zinc sulfate on accumulation of sugar and phenolics in berries of Vitis vinifera cv. Merlot growing on zinc deficient soil. Molecules. (2015) 20:2536–54. 10.3390/molecules20022536 PubMed DOI PMC

He F, Mu L, Yan GL, Liang NN, Pan QH, Wang J, et al. . Biosynthesis of anthocyanins and their regulation in colored grapes. Molecules. (2010) 15:9057–91. 10.3390/molecules15129057 PubMed DOI PMC

Wang H, Fan W, Li H, Yang J, Huang J, Zhang P. Functional characterization of dihydroflavonol-4-reductase in anthocyanin biosynthesis of purple sweet potato underlies the direct evidence of anthocyanins function against abiotic stresses. PLoS ONE. (2013) 8:e78484. 10.1371/journal.pone.0078484 PubMed DOI PMC

Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P. Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol. (2006) 140:637–46. 10.1104/pp.105.072579 PubMed DOI PMC

Rajput VD, Harish S, Singh RK, Verma KK, Sharma L, Quiroz-Figueroa FR, et al. . Recent developments in enzymatic antioxidant defence mechanism in plants with special reference to abiotic stress. Biology. (2021) 10:267. 10.3390/biology10040267 PubMed DOI PMC

Bouayed J, Hoffmann L, BohnT. Antioxidative mechanisms of whole-apple antioxidants employing different varieties from Luxembourg. J Med Food. (2011) 14:1631–7. 10.1089/jmf.2010.0260 PubMed DOI

Sun B, Tian YX, Jiang M, Yuan Q, Chen Q, Zhang Y, et al. . Variation in the main health-promoting compounds and antioxidant activity of whole and individual edible parts of baby mustard (Brassica juncea var. gemmifera). RSC Adv. (2018) 8:33845–54. 10.1039/C8RA05504A PubMed DOI PMC