Influence of stress conditions on the quality of obtained sprouts – modification of their chemical composition
Main Article Content
Keywords
abiotic stress, antioxidants, sprouts biofortification, sprouts nutritional value
Abstract
Sprouts are generally accepted as a pro-healthy food. They are consumed as a source of valuable macronutrients, antioxidants, microelements, and vitamins. Changing growth conditions of sprouts enables modification of their nutritional quality, as well as their safety. Thus, in order to achieve the most desirable composition of the produced sprouts, the conditions for their production are optimized. The aim of this review is to present methods currently used to modify the nutritional quality of plant sprouts. Most scientific works focus on stress conditions inducing the synthesis of secondary metabolites, mainly antioxidants. An increase in their content is achieved after application of physical (e.g., light illumination, temperature) or chemical factors (e.g., salinity stress, phytohormones, metal ions, etc). Though the application of these modifications on a larger scale is problematic. These problems include difficulties in predicting the effect of the stressor and an increased price of the obtained sprouts. However, since it is possible to enrich sprouts with valuable health-promoting substances, these methods are still considered very promising.
References
Andini S, Dekker P, Gruppen H, Araya-Cloutier C, Vincken J-P. Modulation of glucosinolate composition in brassicaceae seeds by germination and fungal elicitation. J Agric Food Chem. 2019;67(46):12770–9. 10.1021/acs.jafc.9b05771
Arscott S, Goldman I. Biomass effects and selenium accumulation in sprouts of three vegetable species grown in selenium-enriched conditions. Hortscience. 2012;47(4):497–502. 10.21273/HORTSCI.47.4.497
Aurisano N, Bertani A, Reggiani R. Anaerobic accumulation of 4-aminobutyrate in rice seedlings; causes and significance. Phytochemistry. 1995;38:1147–50. 10.1016/0031-9422(94)00774-N
Bau H-M, Villaume C, Nicolas J-P, Mejean L. Effect of germination on chemical composition, biochemical constituents and antinutritional factors of soya bean (Glycine max) seeds. J Sci Food Agric. 1997;73:1–9. 10.1002/(SICI)1097-0010(199701)73:1<1::AID-JSFA694>3.0.CO;2-B
Benincasa P, Falcinelli B, Lutts S, Stagnari F, Galieni A. Sprouted grains: a comprehensive review. Nutrients. 2019 ;11:421. 10.3390/nu11020421
Boschin G, Resta D. Alkaloids derived from lysine: quinolizidine (a focus on lupin alkaloids). In: Ramawat K, Mérillon JM, editors. Natural products. Berlin, Heidelberg: Springer; 2013. p. 381–403. 10.1007/978-3-642-22144-6_11
Carpici EB, Celik N, Bayram G. Effects of salt stress on germination of some maize (Zea mays L.) cultivars. Afr J Biotechnol. 2009;8(19):4918–22. 10.4314/ajb.v8i19.65187
Chen Y, Chang SKC. Macronutrients, phytochemicals, and antioxidant activity of soybean sprout germinated with or without light exposure. J Food Sci. 2015;80(6):S1391–S1398. 10.1111/1750-3841.12868
Commission Implementing Regulation (EU) No 208/2013 of 11 March 2013 on traceability requirements for sprouts and seeds intended for the production of sprouts; https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2013:068:0016:0018:EN:PDF
Dell’Aquila A, Spada P. Regulation of protein synthesis in germinating wheat embryos under polyethylene glycol and salt stress. Seed Sci Res. 1992;2:75–80. 10.1017/S0960258500001161
Ding J, Yang T, Feng H, Dong M, Slavin M, Xiong S, et al. Enhancing contents of aminobutyric acid (GABA) and other micronutrients in dehulled rice during germination under normoxic and hypoxic conditions. J Agric Food Chem. 2016;64:1094–102. 10.1021/acs.jafc.5b04859
Domash VI, Sharpio TP, Zabreiko SA, Sosnovskaya TF. Proteolytic enzymes and trypsin inhibitors of higher plants under stress conditions. Russ J Bioorg Chem. 2008;34(3):318–22. 10.1134/s1068162008030114
Duenas M, Sarmento T, Aguilera Y, Benitez V, Molla E, Esteban RM, et al. Impact of cooking and germination on phenolic composition and dietary fibre fractions in dark beans (Phaseolus vulgaris L.) and lentils (Lens culinaris L.). LWT-Food Sci Technol. 2016;66:72–8. 10.1016/j.lwt.2015.10.025
Erba D, Angelino D, Marti A, Manini F, Faoro F, Morreale F, et al. Effect of sprouting on nutritional quality of pulses. Int J Food Sci Nutr. 2018;1:11. 10.1080/09637486.2018.1478393
Falcinelli B, Benincasa P, Calzuola I, Gigliarelli L, Lutts S, Marsili V. Phenolic content and antioxidant activity in raw and denatured aqueous extracts from sprouts and wheatgrass of einkorn and emmer obtained under salinity. Molecules. 2017;22:2132. 10.3390/molecules22122132
Fan X, Thayer DW, Sokorai KJB. Changes in growth and antioxidant status of alfalfa sprouts during sprouting as affected by gamma irradiation of seeds. J Food Prot. 2004;67(3):561–6. 10.4315/0362-028X-67.3.561
Gawlik-Dziki U, Świeca M, Dziki D, Sugier D. Improvement of nutraceutical value of broccoli sprouts by natural elicitors. Acta Scientiarum Polonorum-Hortorum Cultus. 2013;12(1):129–40. http://www.hortorumcultus.actapol.net/volume12/issue1/12_1_129.pdf
Gull A, Lone AA, Wani NUI. Biotic and abiotic stresses in plants. Abiotic and biotic stress in plants (A.B. de Oliveira), IntechOpen. 2019. 10.5772/intechopen.85832
Guo Y, Chen H, Song Y, Gu Z. Effects of soaking and aeration treatment on γ-aminobutyric acid accumulation in germinated soybean (Glycine max L.). Eur Food Res Technol. 2011;232:787–95. 10.1007/s00217-011-1444-6
Guo Y, Yang R, Chen H, Song Y, Gu Z. Accumulation of-aminobutyric acid in germinated soybean (Glycine max L.) in relation to glutamate decarboxylase and diamine oxidase activity induced by additives under hypoxia. Eur Food Res Technol. 2012;234:679–87. 10.1007/s00217-012-1678-y
Guo Y, Zhu Y, Chen C, Chen X. Effects of aeration treatment on γ-aminobutyric acid accumulation in germinated tartary buckwheat (Fagopyrum tataricum). J Chem. 2016;2016;1–9. 10.1155/2016/4576758
Islam, M.J., Hassan, M.K., Sarker, S.R., Rahman, A.B., Fakir, M.S.A. 2017. Light and temperature effects on sprout yield and its proximate composition and vitamin C content in lignosus and mung beans. Journal of Bangladesh Agricultural University 15(2): 248-254. 10.3329/jbau.v15i2.35070
Jamil M, Lee DB, Jung KY, Ashraf M, Lee SC, Rha ES. Effect of salt (NaCl) stress on germination and early seedling growth of four vegetable species. J Cent Eur Agric. 2006;7:273–82. https://jcea.agr.hr/en/issues/article/358
Kestwal RM, Lin JCh, Bagal-Kestwal D, Chiang BH. Glucosinolates fortification of cruciferous sprouts by sulphur supplementation during cultivation to enhance anti-cancer activity. Food Chem. 2011;126(3):1164–71. 10.1016/j.foodchem.2010.11.152
Khattak AB, Zeb A, Bibi N, Khalil SA, Khattak MS. Influence of germination techniques on phytic acid and polyphenols content of chickpea (Cicer arietinum L.) sprouts. Food Chem. 2007;104:1074–9. 10.1016/j.foodchem.2007.01.022
Khattak AB, Zeb A, Khan M, Bibi N, Ihsanullah I, Khattak MS. Influence of germination techniques on sprout yield, biosynthesis of ascorbic acid and cooking ability, in chickpea (Cicer arietinum L.). Food Chem. 2006;103(1):115–20. 10.1016/j.foodchem.2006.08.003
Kim I-D, Dhungana SK, Kim J-K, Ahn H, Kim H-R, Shin D-H. Enhancement of yield and nutritional value of soybean sprouts by persimmon fruit powder. Afr J Biotechnol. 2016;15(44):2490–6. 10.5897/AJB2016.15690
Koga R, Meng T, Nakamura E, Miura C, Irino N, Devkota HP, et al. The effect of photo-irradiation on the growth and ingredient composition of young green barley (Hordeum vulgare). Agric Sci. 2013;4:185–94. 10.4236/as.2013.44027
Kyriacou MC, Rouphael Y, Di Gioia F, Kyratzis A, Serio F, Renna M, et al. Micro-scale vegetable production and the rise of microgreens. Trends Food Sci Technol. 2016;57:103–15. 10.1016/j.tifs.2016.09.005
Le TN, Chiu Ch-H, Hsieh P-Ch. Bioactive compounds and bioactivities of Brassica oleracea L. var. Italica sprouts and microgreens: an updated overview from a nutraceutical perspective. Plants. 2020;9:946. 10.3390/plants9080946
Lee Y-S, Kim Y-H, Kim S-B. Changes in the respiration, growth, and vitamin C content of soybean sprouts in response to chitosan of different molecular weights. HortScience. 2005;40(5):1333–5. https://pdfs.semanticscholar.org/2146/47bbf5fff6d62052e52a8950131bc6d0d5e4.pdf
Li H, Li X, Zhang D, Liu H, Guan K. Effects of drought stress on the seed germination and early seedling growth of the endemic desert plant Eremosparton songoricum (Fabaceae). EXCLI. J. 2013;2:89–101.
Lim JH, Park KJ, Kim BK, Jeong JW, Kim HJ. Effect of salinity stress on phenolic compounds and carotenoids in buckwheat (Fagopyrum esculentum M.) sprout. Food Chem. 2012;135:1065–70. 10.1016/j.foodchem.2012.05.068
Liu H, Chen Y, Hu T, Zhang S, Zhang Y, Zhao T, et al. The influence of light-emitting diodes on the phenolic compounds and antioxidant activities in pea sprouts. J Funct Foods. 2016;25:459–65. 10.1016/j.jff.2016.06.028
Masood T, Shah HU, Zeb A. Effect of sprouting time on proximate composition and ascorbic acid level of mung bean (Vigna radiate L.) and chickpea (Cicer arietinum L.) seeds. J Animal Plant Sci. 2014;24:850–9. https://www.researchgate.net/profile/Tariq-Masood-5/publication/286030391_Effect_of_sprouting_time_on_proximate_composition_and_ascorbic_acid_level_of_mung_bean_Vigna_radiate_L_and_chickpea_Cicer_arietinum_L_seeds/links/5e152eef4585159aa4bce73f/Effect-of-sprouting-time-on-proximate-composition-and-ascorbic-acid-level-of-mung-bean-Vigna-radiate-L-and-chickpea-Cicer-arietinum-L-seeds.pdf
Mastropasqua L, Dipierro N, Paciolla C. Effects of darkness and light spectra on nutrients and pigments in radish, soybean, mung bean and pumpkin sprouts. Antioxidants. 2020;9(6):558. 10.3390/antiox9060558
Mendoza-Sánchez M, Guevara-González RG, Castaño-Tostado E, Mercado-Silva EM, Acosta-Gallegos JA, Rocha-Guzmán NE, et al. Effect of chemical stress on germination of cv Dalia bean (Phaseolus vularis L.) as an alternative to increase antioxidant and nutraceutical compounds in sprouts. Food Chem. 2016;212:128–37. 10.1016/j.foodchem.2016.05.110
Meng T, Nakamura E, Irino N, Joshi KR, Devkota HP, Yahara S, et al. Effects of irradiation with light of different photon densities on the growth of young green barley plants. Agric Sci. 2015;6:208–16. 10.4236/as.2015.6202
Moreira-Rodríguez M, Nair V, Benavides J, Cisneros-Zevallos L, Jacobo-Velázquez DA. UVA, UVB light, and methyl jasmonate, alone or combined, redirect the biosynthesis of glucosinolates, phenolics, carotenoids, and chlorophylls in broccoli sprouts. Int J Molec Sci. 2017;18:2330. 10.3390/ijms18112330
Nam TG, Kim D-O, Eom SH. Effects of light sources on major flavonoids and antioxidant activity in common buckwheat sprouts. Food Sci Biotechnol. 2017. 10.1007/s10068-017-0204-1
Nissar N, Wani SM, Hameed OB, Wani TA, Ahmad M. Influence of paddy (Oryza sativa) sprouting on antioxidant activity, nutritional and anti-nutritional properties. J Food Meas Charact. 2017;11(4):1844–50. 10.1007/s11694-017-9566-6
Oh M-M, Rajashekar CB. Antioxidant content of edible sprouts: effects of environmental shocks. J Sci Food Agric. 2009;89(13):2221–7. 10.1002/jsfa.3711
Pérez-Balibrea S, Moreno DA, García-Viguera C. Improving the phytochemical composition of broccoli sprouts by elicitation. Food Chem. 2011;129(1):35–44. 10.1016/j.foodchem.2011.03.049
Promila K, Kumar S. Vigna radiata seed germination under salinity. Biologia Plantarum. 2000;43(3):423–4. 10.1023/A:1026719100256
Przybysz A, Wrochna M, Małecka-Przybysz M, Gawrońska H, Gawroński SW. Vegetable sprouts enriched with iron: effects on yield, ROS generation and antioxidative system. Scientia Horticulturae. 2016;203:110–17. 10.1016/j.scienta.2016.03.017
Przybysz A, Wrochna M, Małecka-Przybysz M, Gawrońska H, Gawroński SW. The effects of Mg enrichment of vegetable sprouts on Mg concentration, yield and ROS generation. J Sci Food Agric. 2015;96(10):3469–76. 10.1002/jsfa.7530
Qian H, Liu T, Deng M, Miao H, Cai C, Shen W, et al. Effects of light quality on main health-promoting compounds and antioxidant capacity of Chinese kale sprouts. Food Chem. 2016;196:1232–8. 10.1016/j.foodchem.2015.10.055
Qiang L, Qing Z, Xirong Z, Changwei T, Yide H. Application of chitosan and chitosan derivatives into processing of mung bean sprout. J Anhui Agric Univ. 2005;32(3):402–5.
Ramakrishna R, Sarkar D, Shetty K. Metabolic stimulation of phenolic biosynthesis and antioxidant enzyme response in dark germinated barley (Hordeum vulgare L.) sprouts using bioprocessed elicitors. Food Sci Biotechnol. 2019;28:1093–106. 10.1007/s10068-018-0535-6
Randhir R, Lin Y-T, Shetty K. Stimulation of phenolics, antioxidant and antimicrobial activities in dark germinated mung bean sprouts in response to peptide and phytochemical elicitors. Process Biochem. 2004a;39:637–46. 10.1016/S0032-9592(03)00197-3
Randhir R, Lin Y-T, Shetty K. Phenolics, their antioxidant and antimicrobial activity in dark germinated fenugreek sprouts in response to peptide and phytochemical elicitors. Asia Pacific J Clin Nutr. 2004b;13(3):295–307.
Samuolienė G, Urbonavičiūtė A, Brazaitytė A, Šabajevienė G, Sakalauskaitė J, Duchovskis P. The impact of LED illumination on antioxidant properties of sprouted seeds. Cent Eur J Biol. 2011;6(1):68–74. 10.2478/s11535-010-0094-1
Scott, S.J. and Jones, R.A., 1985. Quantifying seed germination responses to low temperatures: variation among Lycopersicon spp. Environmental and Experimental Botany 25: 129–137. 10.1016/0098-8472(85)90018-8
Seo J-M, Arasu MV, Kim Y-B, Park SU, Kim S-J. Phenylalanine and LED lights enhance phenolic compound production in Tartary buckwheat sprouts. Food Chem. 2015;177:204–13. 10.1016/j.foodchem.2014.12.094
Shetty P, Atallah MT, Shetty K. Effects of UV treatment on the proline linked pentose phosphate pathway for phenolics and L-DOPA synthesis in dark germinated Vicia faba. Process Biochem. 2002;37:1285–95. 10.1016/S0032-9592(02)00013-4
Sim U, Sung J, Lee H, Heo H, Sang Jeong H, Lee J. Effect of calcium chloride and sucrose on the composition of bioactive compounds and antioxidant activities in buckwheat sprouts. Food Chem. 2019;126075. 10.1016/j.foodchem.2019.126075
Stagnari F, Gallieni A, D’Egidio S, Falcinelli B, Pagnani G, Pace R, et al. Effects of sprouting and salt stress on polyphenol composition and antiradical activity of einkorn, emmer and durum wheat. Italian J Agronomy. 2017;12(848):293-301. 10.4081/ija.2017.848
Sugihara S, Kondo M, Chihara Y, Yuji M, Hattori H, Yoshida M. Preparation of selenium-enriched sprouts and identification of their selenium species by high-performance liquid chromatography-inductively coupled plasma mass spectrometry. Biosci Biotechnol Biochem. 2004;68(1):193–9. 10.1271/bbb.68.193
Świeca M. Production of ready-to-eat lentil sprouts with improved antioxidant capacity: optimization of elicitation conditions with hydrogen peroxide. Food Chem. 2015;180:219-226. 2015. 10.1016/j.foodchem.2015.02.031
Świeca M, Baraniak B. Nutritional and antioxidant potential of lentil sprouts affected by elicitation with temperature stress. J Agric Food Chem. 2014;62(14):3306–13. 10.1021/jf403923x
Świeca M, Sęczyk Ł, Gawlik-Dziki U. Elicitation and precursor feeding as tools for the improvement of the phenolic content and antioxidant activity of lentil sprouts. Food Chem. 2014;161:288–95. 10.1016/j.foodchem.2014.04.012
Tan L, Chen S, Wang T, Dai S. Proteomic insights into seed germination in response to environmental factors. Proteomics. 2013;13(12–13):1850–70. 10.1002/pmic.201200394
Tsurunaga T, Takahashi T, Katsube T, Kudo A, Kuramitsu O, Ishiwata M, et al. Effects of UV-B irradiation on the levels of anthocyanin, rutin and radical scavenging activity of buckwheat sprouts. Food Chem. 2013;141(1):552–6. 10.1016/j.foodchem.2013.03.032
Tuan PA, Thwe AA, Kim YB, Kim JK, Kim SJ, Lee S, et al. Effects of white, blue, and red light-emitting diodes on carotenoid biosynthetic gene expression levels and carotenoid accumulation in sprouts of tartary buckwheat (Fagopyrum tataricum Gaertn.). J Agric Food Chem. 2013;61:12356–61. 10.1021/jf4039937
Viacava GE, Roura SI. Principal component and hierarchical cluster analysis to select natural elicitors for enhancing phytochemical content and antioxidant activity of lettuce sprouts. Scientia Horticulturae. 2015;193:13–21. 10.1016/j.scienta.2015.06.041
Wang P, Li X, Tian L, Gu Z, Yang R. Low salinity promotes the growth of broccoli sprouts by regulating hormonal homeostasis and photosynthesis. Hortic Environ Biotechnol. 2019;60:19–30. 10.1007/s13580-018-0095-y
Wei J, Miao H, Wang Q. Effect of glucose on glucosinolates, antioxidants and metabolic enzymes in Brassica sprouts. Scientia Horticulturae. 2011;129(4):535–40. 10.1016/j.scienta.2011.04.026
Xu MJ, Dong JF, Zhu MY. Effect of germination conditions on ascorbic acid level and yield of soybean sprout. J Sci Food Agric. 2005;85:943–7. 10.1002/jsfa.2050
Yang R, Guo Q, Gu Z. GABA shunt and polyamine degradation pathway on-aminobutyric acid accumulation in germinating fava bean (Vicia faba L.) under hypoxia. Food Chem. 2013;136 152–9. 10.1016/j.foodchem.2012.08.008.
Ye J, Wen B. Seed germination in relation to the invasiveness in spiny amaranth and edible amaranth in Xishuangbanna, SW China. PLoS ONE. 2017;12(4):e0175948. 10.1371/journal.pone.0175948
Youn YS, Park JK, Jang HD, Rhee YW. Sequential hydration with anaerobic and heat treatment increases GABA (g-aminobutyric acid) content in wheat. Food Chem. 2011;129:1631–5. 10.1371/10.1016/j.foodchem.2011.06.020
Zielińska-Dawidziak M. Plant ferritin—a source of iron to prevent its deficiency. Nutrients. 2015;7(2):1184–201. 10.3390/nu7021184
Zielińska-Dawidziak M, Dwiecki K, Lewko K. Modification of soybean and lupine sprouting conditions: influence on yield, ROS generation, and antioxidative systems. Eur Food Res Technol. 2018;244:1945–52. 10.1007/s00217-018-3106-4
Zielińska-Dawidziak M, Hertig I, Piasecka-Kwiatkowska D, Staniek H, Nowak KW, Twardowski T. Study on iron availability from prepared soybean sprouts using an iron-deficient rat model. Food Chem. 2012;135(4):2622–7. 10.1016/j.foodchem.2012.06.113
Zielińska-Dawidziak M, Hertig I, Staniek H, Piasecka-Kwiatkowska D, Nowak KW. Effect of iron status in rats on the absorption of metal ions from plant ferritin. Plant Foods Hum Nutr. 2014a;69(2):101–7. 10.1007/s11130-014-0413-1
Zielińska-Dawidziak M, Piasecka-Kwiatkowska D, Król E, Staniek E, Krejpcio Z. The Safety of Food Supplemented in Iron with Sprouted in Abiotic Stress Legumes Seeds-Heavy Metal Pollution. International Conference on Food Security and Nutrition IPCBEE 2014b;67:23-27. 10.7763/IPCBEE
Zielińska-Dawidziak M, Siger A. Effect of elevated accumulation of iron in ferritin on the antioxidants content in soybean sprouts. Eur Food Res Technol. 2012;234:1005–12. 10.1007/s00217-012-1706-y
Zielińska-Dawidziak M, Staniek H, Król E, Piasecka-Kwiatkowska D, Twardowski T. Legume seeds and cereal grains’ capacity to accumulate iron while sprouting in order to obtain food fortificant. Acta Scientarum Polonorum Technologia Alimentaria. 2016;15(3):333–8. 10.17306/J.AFS.2016.3.32
Zieliński H, Kozłowska H. The content of tocopherols in Cruciferae sprouts. Polish J Food Nutr Sci. 2003;12(4):25–31.