Agronomic biofortification with selenium improves the yield and nutraceutical quality in tomato under soilless conditions

  • Jazmín M. GAUCIN-DELGADO Instituto Tecnológico Nacional de México- Instituto Tecnológico de Torreón (ITT), Torreón, Coahuila 27170
  • Luis G. HERNÁNDEZ-MONTIEL Centro de Investigación Biológica del Noroeste de México (CIBNOR S.C.), La Paz, B.C.S. 23096
  • Esteban SÁNCHEZ-CHAVEZ Centro de Investigación y Desarrollo de Alimentos AC. Delicias, Chihuahua
  • Hortensia ORTEGA-ORTIZ Centro de Investigación en Química Aplicada (CIQA), Enrique Reyna H. No. 140, San José de los Cerritos, 25294 Saltillo, Coahuila
  • Manuel FORTIS-HERNÁNDEZ Instituto Tecnológico Nacional de México- Instituto Tecnológico de Torreón (ITT), Torreón, Coahuila 27170
  • Juan Jose REYES-PÉREZ Universidad Técnica Estatal de Quevedo, Quevedo EC 120501, Los Ríos
  • Pablo PRECIADO-RANGEL Instituto Tecnológico Nacional de México- Instituto Tecnológico de Torreón (ITT), Torreón, Coahuila 27170
Keywords: biofortification; nutraceutical quality; Solanum lycopersicum L.

Abstract

Selenium (Se) is an essential element for humans. Its consumption comes from food of animal or vegetal origin; whose content varies widely depending on its availability in soil or anthropogenic sources. Biofortification improves food nutritional quality, and its consumption has a positive influence in human health. Thus, the objective of this research was to assess agricultural biofortification with Se in tomato fruit and its effects on yield, nutraceutical quality, and antioxidant capacity.  Five Se doses (0, 2, 4, 6, and 8 mg L-1) in the form of sodium selenite (Na2SeO3) were added in a nutritional solution in a hydroponic system.  The results obtained indicated that agricultural biofortification with Se applied in the nutritional solution improved yield, nutraceutical quality, and Se concentration in tomato fruit. The optimum Se dose that maximized yield and nutraceutical quality, as well as the recommended consumption concentration in tomato fruit in this study was 2 mg L-1 (Na2SeO4) because higher doses decreased yield and bioactive compound biosynthesis. Incorporating Se in the nutritional solution is an alternative to increase phytochemical compound biosynthesis in tomato fruit and yield with the possibility of improving public health with its consumption.

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References

Alves LR, Rossatto DR, Rossi ML, Martinelli AP, Gratão PL (2020). Selenium improves photosynthesis and induces ultrastructural changes but does not alleviate cadmium-stress damages in tomato plants. Protoplasma 257(2):597-605. https://doi.org/10.1007/s00709-019-01469-w

Andrade FR, da Silva GN, Guimarães KC, Barreto HBF, de Souza KRD, Guilherme LRG, … dos Reis AR (2018). Selenium protects rice plants from water deficit stress. Ecotoxicology environmental safety 164:562-570. https://doi.org/10.1016/j.ecoenv.2018.08.022

Andrejiová A, Hegedűsová A, Adamec S, Hegedűs O, Mezeyová IJ (2019). Increasing of selenium content and qualitative parameters in tomato (Lycopersicon esculentum Mill.) after its foliar application. Potravinarstvo Slovak Journal of Food Sciences 13(1):351-358. https://doi.org/10.5219/1097

AOAC (1990). Official methods of analysis. Association of official analytical chemists. https://doi.org/10.1007/BF02670789

Astaneh RK, Bolandnazar S, Nahandi FZ, Oustan S (2018). Effect of selenium application on phenylalanine ammonia-lyase (PAL) activity, phenol leakage and total phenolic content in garlic (Allium sativum L.) under NaCl stress. Information Processing in Agriculture 5(3):339-344. https://doi.org/10.1016/j.inpa.2018.04.004

Babalar M, Mohebbi S Zamani Z, Askari MA (2019). Effect of foliar application with sodium selenate on selenium biofortification and fruit quality maintenance of 'Starking Delicious' apple during storage. Journal of the Science of Food and Agriculture 99(11):5149-5156. https://doi.org/10.1002/jsfa.9761

Bastías JM, Cepero YJ (2016). La vitamina C como un eficaz micronutriente en la fortificación de alimentos. [Vitamin C as an effective micronutrient in the food fortification]. Revista Chilena de Nutrición 43(1):81-86. http://dx.doi.org/10.4067/S0717-75182016000100012

Boldrin PF, de Figueiredo MA,Yang Y, Luo H, Giri S, Hart JJ, … Li L (2016). Selenium promotes sulfur accumulation and plant growth in wheat (Triticum aestivum). Physiologia Plantarum 158(1):80-91. https://doi.org/10.1111/ppl.12465

Brand-Williams W, Cuvelier ME, Berset C (1995). Use of a free radical method to evaluate antioxidant activity. Food Science 28(1):25-30. https://doi.org/10.1016/S0023-6438(95)80008-5

Brisson LF, Tenhaken R, Lamb C (1994). Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. The Plant Cell 6(12):1703-1712, https://doi.org/10.1105/tpc.6.12.1703

Castillo-Godina R, Foroughbakhch-Pournavab R, Benavides-Mendoza A (2016). Effect of selenium on elemental concentration and antioxidant enzymatic activity of tomato plants. Journal of Agricultural Science 18(1):233-244

Chen Z, Young, TE, Ling J, Chang SC, Gallie DR (2003). Increasing vitamin C content of plants through enhanced ascorbate recycling. Proceedings of the National Academy of Science USA 100:3525. https://doi.org/10.1073/pnas.0635176100

Chomchan R, Siripongvutikorn S, Puttarak P (2017). Selenium bio-fortification: an alternative to improve phytochemicals and bioactivities of plant foods. Functional Foods in Health and Disease 7(6):263-279. https://doi.org/10.31989/ffhd.v7i4.323

D’Amato R, Fontanella MC, Falcinelli B, Beone GM, Bravi E, Marconi O, Benincasa P, Businelli D (2018). Selenium biofortification in rice (Oryza sativa L.) sprouting: effects on Se yield and nutritional traits with focus on phenolic acid profile. Journal of Agricultural Food Chemistry 66(16):4082-4090. https://doi.org/10.1021/acs.jafc.8b00127

Da Cruz Ferreira RL, de Mello Prado R, de Souza Junior JP, Gratão PL, Tezotto T, Cruz FJR (2020). Oxidative stress, nutritional disorders, and gas exchange in lettuce plants subjected to two selenium sources. Journal of Soil Science and Plant Nutrition 1:14. https://doi.org/10.1007/s42729-020-00206-0

Dall'Acqua S, Ertani A, Pilon-Smits EAH, Fabrega-Prats M, Schiavon M (2019). Selenium biofortification differentially affects sulfur metabolism and accumulation of phytochemicals in two rocket species (Eruca sativa Mill. and Diplotaxis tenuifolia) grown in hydroponics. Plants (Basel) 8(3):68. https://doi.org/10.3390/plants8030068

Das D, Seal P,Biswas AK (2019). Influence of selenium on growth, antioxidants production and physiological parameters of rice (Oryza sativa L.) seedlings and its possible reversal by coapplication of sulphate. American Journal of Plant Sciences 10(12):2236-2278. http://doi.org/10.4236/ajps.2019.1012158

Del Giudice R, Raiola A, Tenore GC, Frusciante L, Barone A, Monti DM, Rigano MM (2015). Antioxidant bioactive compounds in tomato fruits at different ripening stages and their effects on normal and cancer cells. Journal of Functional Foods 18:83-94. https://doi.org/10.1016/j.jff.2015.06.060

Edelstein M, Berstein D, Shenker M, Azaizeh H, Ben-Hur M (2016). Effects of selenium on growth parameters of tomato and basil under fertigation management. HortScience 51(8):1050-1056. https://doi.org/10.21273/HORTSCI.51.8.1050

Fernández C, Pitre A, LLobregat MJ, Rondón Y (2007). Evaluación del contenido de licopeno en pastas de tomate comerciales. [Determination of the Lycopene Content in Different Commercial Tomato Pastes]. Información Tecnológica 18(3):31-38. http://doi.org/10.4067/S0718-076.42007000300005

Foyer CH, Noctor G (2011). Ascorbate and glutathione: the heart of the redox hub. Plant Physiology 155(1):2-18. https://doi.org/10.1104/pp.110.167569

Garduño-Zepeda A, Márquez-Quiroz C (2018). Aplicación de selenio en cultivos agrícolas. Revisión bibliográfica [Use of selenium in crop production. Review]. ITEA, Información Técnica Económica Agraria: Revista de la Asociación Interprofesional para el Desarrollo Agrario (AIDA) 114:327-343. https://doi.org/10.12706/itea.2018.019

Golubkina N, Folmanis G,Tananaev I, Krivenkov L, Kosheleva O, Soldatenko A (2017). Comparative evaluation of spinach biofortification with selenium nanoparticles and ionic forms of the element. Nanotechnologies in Russia 12(1-9):569-576. https://doi.org/10.1134/S1995078017050032

Golubkina N, Zamana S, Seredin T, Poluboyarinov P, Sokolov S, Baranova H, … Caruso G (2019). Effect of selenium biofortification and beneficial microorganism inoculation on yield, quality and antioxidant properties of shallot bulbs. Plants (Basel) 8(4):102. https://doi.org/10.3390/plants8040102

Gupta M, Gupta S (2017). An overview of selenium uptake, metabolism, and toxicity in plants. Frontiers in Plant Science 7:2074. https://doi.org/10.3389/fpls.2016.02074

Hachmann TL, Rezende R, Matumoto-Pintro PT, Saath R, Anjo FA, Menezes CSL (2019). Yield, antioxidant activity and shelf-life of cauliflower inflorescences under droughtstress and foliar spraying of selenium. Ciência e Agrotecnologia 43:e017819. http://doi.org/10.1590/1413-7054201943017819

Hassan A,Mostafa E (2016). Selenium invoked antioxidant defense system in Azolla caroliniana plant. Phyton-International Journal of Experimental Botany 85:262-269.

Hawrylak-Nowak B, Dresler S, Rubinowska K, Matraszek-Gawron R, Woch W, Hasanuzzaman M (2018). Selenium biofortification enhances the growth and alters the physiological response of lamb's lettuce grown under high temperature stress. Plant Physiology Biochemistry 127:446-456. https://doi.org/10.1016/j.plaphy.2018.04.018

Hibaturrahman SN, Koyama H, Kameo S, Waspodo P, Wardana AA, Surono IS (2020). Effect of cocoyam modified starch (Xanthosoma sagittifolium), beetroot juice, cocoyam modified starch adsorbing beetroot on plasma selenium and glutathione peroxidase of pre-diabetic rat. Earth and Environmental Science 426(1):012184. https://doi.org/10.1088/1755-1315/426/1/012184

Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui HJP (2001). A large family of class III plant peroxidases. Plant Cell Physiology 42(5):462-468. https://doi.org/10.1093/pcp/pce061

Hu T, Liang Y, Zhao G, Wu W, Li H, Guo Y (2019). Selenium biofortification and antioxidant activity in Cordyceps militaris supplied with selenate, selenite, or selenomethionine. Biological Trace Element Research 187(2):553-561. https://doi.org/10.1007/s12011-018-1386-y

Jiang Y,El Mehdawi AF, Tripti LW, Stonehouse G, Fakra SC, Hu Y, … Pilon-Smits EAH (2018). Characterization of selenium accumulation, localization and speciation in buckwheat-implications for biofortification. Frontiers in Plant Science 9:1583. https://doi.org/10.3389/fpls.2018.01583

Jimenez A, Creissen G, Kular B, Firmin J, Robinson S, Verhoeyen M, Mullineaux P (2002). Changes in oxidative processes and components of the antioxidant system during tomato fruit ripening. Planta 214(5):751-758. https://doi.org/10.1007/s004250100667

Kavcic A, Budic B, Vogel-Mikus K (2020). The effects of selenium biofortification on mercury bioavailability and toxicity in the lettuce-slug food chain. Food and Chemical Toxicology 135:110939. https://doi.org/10.1016/j.fct.2019.110939

Lidon FC, Oliveira K, Ribeiro MM, Pelica J, Pataco I, Ramalho JC, … Ribeiro-Barros AI (2018). Selenium biofortification of rice grains and implications on macronutrients quality. Journal of Cereal Science 81:22-29. https://doi.org/10.1016/j.jcs.2018.03.010

Lyons G (2018) Biofortification of cereals with foliar selenium and iodine could reduce hypothyroidism. Frontiers in Plant Science 9:730. https://doi.org/10.3389/fpls.2018.00730

Martínez-Damián MT, Cano-Hernández R, Moreno-Pérez EdC, Sánchez-del Castillo F, Cruz-Álvarez O (2019). Efecto de biorreguladores del crecimiento en precosecha sobre la calidad fisicoquímica de tomate saladette [Effect of preharvest growth bioregulators on physicochemical quality of saladette tomato]. Revista Chapingo. Serie Horticultura 25(1):29-43. http://doi.org/10.5154/r.rchsh.2018.06.013

Mondal K, Sharma NS, Malhotra SP, Dhawan K, Singh R (2004). Antioxidant systems in ripening tomato fruits. Biologia Plantarum 48(1):49-53. https://doi.org/10.1023/B:BIOP.0000024274.43874.5b

Moretti M, Cossignani L, Messina F, Dominici L, Villarini M,Curini M, Marcotullio MCJ (2013). Antigenotoxic effect, composition and antioxidant activity of Dendrobium speciosum. Food Chemistry 140(84):660-665. https://doi.org/10.1016/j.foodchem.2012.10.022

Motesharezadeh B, Ghorbani S, Alikhani HA (2020). The effect of selenium biofortification in alfalfa (Medicago sativa). Journal of Plant Nutrition 43(2):240-250. https://doi.org/10.1080/01904167.2019.1676900

Narváez-Ortiz WA, Martínez-Hernández M, Fuentes-Lara LO, Benavides-Mendoza A, Valenzuela-García JR, González-Fuentes J (2018). Effect of selenium application on mineral macro-and micronutrients and antioxidant status in strawberries. Journal of Applied Botany and Food Quality 91:321-331. https://doi.org/10.5073/JABFQ.2018.091.041

Nedelkov K, Chen X, Martins C, Melgar A, Harper M, Räisänen S, … Hristov A (2020). Alternative selenium supplement for sheep. Animal Feed Science Technology 261:114390. https://doi.org/10.1016/j.anifeedsci.2020.114390

Nepal N, Yactayo‐Chang JP, Medina‐Jiménez K, Acosta‐Gamboa LM, González‐Romero ME, Arteaga‐Vázquez MA, Lorence A (2019). Mechanisms underlying the enhanced biomass and abiotic stress tolerance phenotype of an Arabidopsis MIOX over‐expresser. Plant Direct 3(9):e00165. https://doi.org/10.1002/pld3.165

Oliveira VC, Faquin V, Andrade FR, Carneiro JP, da Silva Júnior EC, de Souza KRD, … Guilherme LRG (2019). Physiological and Physicochemical Responses of Potato to Selenium Biofortification in Tropical Soil. Potato Research 62(3):315-331. https://doi.org/10.1007/s11540-019-9413-8

Oliveira VC, Faquin V, Guimarães KC, Andrade FR, Pereira J, Guilherme LRG (2018). Agronomic biofortification of carrot with selenium. Ciência e Agrotecnologia 42(2):138-147. https://doi.org/10.1590/1413-70542018422031217

Ordóñez-Santos LE, Portilla MAO, Rodríguez DXR (2013). Cinética de degradación térmica de vitamina C en frutos de guayaba (Psidium guajava L.) [Thermal degradation kinetics of vitamin C in guava fruits (Psidium guajava L.)]. Revista Lasallista de Investigación 10(2):44-51. https://doi.org/10.1002/hep.23201

Palencia P, Martinez F, Burducea M, Oliveira JA, Giralde I (2016). Efectos del enriquecimiento con Selenio en SPAD, calidad de la fruta y parámetros de crecimiento de plantas de fresa en un sistema de cultivo sin suelo [Effects of se-enrichment on SPAD, fruit quality and growth parameters of strawberry plants in soilless growing system] Revista Brasileira de Fruticultura 38(1):202-212. https://doi.org/10.1590/0100-2945-294/14

Pannico A, El-Nakhel C, Kyriacou MC, Giordano M, Stazi SR, De Pascale S, Rouphael Y (2019). Combating micronutrient deficiency and enhancing food functional quality through selenium fortification of select lettuce genotypes grown in a closed soilless system. Frontiers in Plant Science 10:1495. https://doi.org/10.3389/fpls.2019.01495

Pérez MB, Lipinski VM, Filippini MF, Chacón-Madrid K, Arruda MAZ, Wuilloud RG (2019). Selenium biofortification on garlic growth and other nutrients accumulation. Horticultura Brasileira 37(3):294-301. https://doi.org/10.1590/s0102-053620190307

Puccinelli M, Malorgio F, Pezzarossa B (2017). Selenium enrichment of horticultural crops. Molecules 22(6):E933. http://doi.org/10.3390/molecules22060933

Pullar, JM, Carr AC, Vissers M (2017). The roles of vitamin C in skin health. Nutrients 9(8):866. https://doi.org/10.3390/nu9080866

Qui-Zapata JA, Peña-Rodríguez LM, Castro-Concha LA, Miranda-Ham MdL (2010). Peroxidación lipídica como marcador de muerte celular en cultivos celulares de cempasúchil (Tagetes erecta L.) [Lipid peroxidation as a marker of cell death in cell cultures of mexican marigold (Tagetes erecta L.)]. Revista Mexicana de Fitopatología 28(2):165-167

Rady MM, Belal HE, Gadallah FM, Semida WM (2020). Selenium application in two methods promotes drought tolerance in Solanum lycopersicum plant by inducing the antioxidant defense system. Scientia Horticulturae 266:109290. https://doi.org/10.1016/j.scienta.2020.109290

Ramadan AMA, Khaled YAH (2020) Effect of bio-fertilizer and foliar spray of selenium of growth, yield and quality of potato plants. Academic Journal of Life Sciences 6(1):1-7. https://doi.org/10.32861/ajls.61.1.7

Ramos S, Faquin V, Guilherme L, Castro E, Ávila F, Carvalho G, … Oliveira CJ (2010). Selenium biofortification and antioxidant activity in lettuce plants fed with selenate and selenite. Plant, Soil Environmental Epidemiology 56(4):584-588. https://doi.org/10.17221/113/2010-PSE

Ryant P, Antošovský J, Adam V, Ducsay L, Škarpa P, Sapáková E (2020). The importance of selenium in fruit nutrition. Fruit Crops, Constraints, F.C.D.a.M.o.N., Ed. Elsevier 241-254. https://doi.org/10.1016/B978-0-12-818732-6.00018-6

Sabatino L, Ntatsi G, Iapichino G, D’Anna F, De Pasquale C (2019). Effect of selenium enrichment and type of application on yield, functional quality and mineral composition of curly endive grown in a hydroponic System. Agronomy 9(4):207. https://doi.org/10.3390/agronomy9040207

Schiavon M, dall’Acqua S, Mietto A, Pilon-Smits EA, Sambo P, Masi A, Malagoli M (2013). Selenium fertilization alters the chemical composition and antioxidant constituents of tomato (Solanum lycopersicon L.). Journal of Agricultural and Food Chemistry 61(144):10542-10554. https://doi.org/10.1021/jf4031822

Silva DF, Cipriano PE, de Souza RR, Júnior MS, Faquin V, de Souza Silva ML, Guilherme LRG (2020). Biofortification with selenium and implications in the absorption of macronutrients in Raphanus sativus L. Journal of Food Composition and Analysis 86:103382 https://doi.org/10.1016/j.jfca.2019.103382

Singleton VL, Orthofer R, Lamuela-Raventós RM (1999). Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. In: Methods in enzymology 299:152-178. https://doi.org/10.1016/S0076-6879(99)99017-1

Skrypnik L, Novikova A, Tokupova E (2019). Improvement of phenolic compounds, essential oil content and antioxidant properties of sweet basil (Ocimum basilicum L.) depending on type and concentration of selenium application. Plants 8(11):458. https://doi.org/10.3390/plants8110458

Stefani S, Halim L Andayani DE, Witjaksono F (2020). Selenium in hyperthyroidism. World Nutrition Journal 3(2):24-37. https://doi.org/10.25220/WNJ.V03.i2.0004

Thavarajah D, Abare A, Mapa I, Coyne CJ, Thavarajah P, Kumar S (2017). selecting lentil accessions for global selenium biofortification. Plants (Basel) 6(3):34. https://doi.org/10.3390/plants6030034

Utoiu E, Oacea A, Gaspar A, Seciu AM, Ștefan LM, Coroiu V, … Oancea F (2017). Selenium biofortification treatment of cauliflower enhances their content in chemopreventive compounds and in vitro antitumoral activity. Scientific Bulletin. Series F. Biotechnologies 21:33-40. https://doi.org/10.1007/s11101-016-9454-4

Vallarino JG, Yeats TH, Maximova E, Rose JK, Fernie AR, Osorio S (2017). Postharvest changes in LIN5-down-regulated plants suggest a role for sugar deficiency in cuticle metabolism during ripening. Phytochemistry 142:11-20. https://doi.org/10.1016/j.phytochem.2017.06.007

Vinceti M, Filippini T, Del Giovane C, Dennert G, Zwahlen M, Brinkman M, … Crespi CM (2018Selenium for preventing cancer. Cochrane Database of Systematic Reviews 1(1). https://doi.org/10.1002/14651858.CD005195.pub4

Wakchaure G, Minhas P, Meena KK, Kumar S, Rane J (2020). Effect of plant growth regulators and deficit irrigation on canopy traits, yield, water productivity and fruit quality of eggplant (Solanum melongena L.) grown in the water scarce environment. Journal of Environmental Management 262:110320. http://doi.org/10.1016/j.jenvman.2020.110320

White P (2016). Selenium accumulation by plants. Annals of Botany 117(2):217-235. https://doi.org/10.1093/aob/mcv180

Zhao W, Xu W, Chai Y, Zhou X, Zhang M, Xie W (2017). Differences in selenium uptake, distribution and expression of selenium metabolism genes in tomatoes. International Journal of Agriculture Biology 19(3):528-534. https://doi.org/10.17957/IJAB/15.0330

Zieba P, Kala K, Wlodarczyk A, Szewczyk A, Kunicki E, Sekara A, Muszynska B (2020). Selenium and zinc biofortification of Pleurotus eryngii mycelium and fruiting bodies as a tool for controlling their biological activity. Molecules 25(4): 899. http://doi.org/10.3390/molecules25040889

Zou C, Du Y, Rashid A, Ram H, Savasli E, Pieterse PJ, … Mahmood K (2019). Simultaneous biofortification of wheat with zinc, iodine, selenium, and iron through foliar treatment of a micronutrient cocktail in six countries. Journal of Agricultural and Food Chemistry 67(29):8096-8106. https://doi.org/10.1021/acs.jafc.9b01829

Published
2020-08-25
How to Cite
GAUCIN-DELGADO, J. M., HERNÁNDEZ-MONTIEL, L. G., SÁNCHEZ-CHAVEZ, E., ORTEGA-ORTIZ, H., FORTIS-HERNÁNDEZ, M., REYES-PÉREZ, J. J., & PRECIADO-RANGEL, P. (2020). Agronomic biofortification with selenium improves the yield and nutraceutical quality in tomato under soilless conditions. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 48(3), 1221-1232. https://doi.org/10.15835/nbha48312000
Section
Research Articles