Influence of abiotic stress during soybean germination followed by recovery on the phenolic compounds of radicles and their antioxidant capacity

Sylwia Swigonska, Ryszard Amarowicz, Angelika Król, Agnieszka Mostek, Anna Badowiec, Stanisław Weidner


Abiotic stress factors are among the major causes of lower crop yields. It is known, that in response to cold and/or osmotic stress, crops activate various defense mechanisms, including morphological, physiological and metabolic adaptations. Secondary metabolism, especially phenolic compounds, seem to be an important factor of stress-induced metabolic re-engineering as their levels are alternated by abiotic stress in plants. Despite the fact, that the nature and function of phenolic compounds was already studied in various plant species, it is important to define tissue-specific changes induced by two most potent abiotic stressors – low temperature and decreased water potential. Moreover, in fields, the appearance of single stress is rather rare. Usually two or more factors are acting in parallel, which may potentially result in different effects. Therefore, the aim of this study was to analyze selected elements of secondary metabolism in roots of germinating soybean seeds under cold stress, osmotic stress and both stresses combined. In addition the effects of constant and persistent stress were compared to those induced by sudden and brief stress appearance, as well as after the post-stress recovery process. In the presented study standard methods for identification and quantification of phenolic acids and isoflavones were used and the antioxidant capacity of the radicle extracts was measured. The phenolic metabolism in plants was greatly intensified in response to cold and osmotic stress and remained at high level during the post-stress recovery. The amount and composition of both phenolic acids and identified isoflavones also changed in stress- and duration-dependent manner. This proves an important role of phenolic compounds in abiotic stress response of germinating soybean seeds and opens up new perspectives for further investigations.


environmental stress; antioxidant capacity; phenolic compounds; phenolic acids; isoflavones

Full Text:



França SC, Roberto PG, Marins MA, Puga RD, Rodrigues A, Pereira JO. Biosynthesis of secondary metabolites in sugarcane. Genet Mol Biol. 2001;24(1–4):243–250.

Oh MM, Carey EE, Rajashekar CB. Environmental stresses induce health-promoting phytochemicals in lettuce. Plant Physiol Biochem. 2009;47(7):578–583.

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(6):1005–1012.

Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. 2012;2012:1–26.

Amarowicz R, Weidner S. Biological activity of grapevine phenolic compounds. In: Roubelakis-Angelakis KA, editor. Grapevine molecular physiology and biotechnology. Dordrecht: Springer Netherlands; 2009. p. 389–405.

Cheynier V, Sarni-Manchado P, Quidean S, editors. Recent advances in polyphenol research. Oxford: Wiley-Blackwell; 2012. (vol 3).

Chalker-Scott L, Fuchigami LH. The role of phenolic compounds in plant stress responses. In: Li PH, editor. Low temperature stress physiology in crops. Boca Raton, FL: CRC Press; 1989. p. 27–40.

Ippolito A, Nigro F, Lima G. Mechanism of resistance to Botrytis cinerea in wound of cured kiwifruits. Acta Hortic. 1997;444:719–724.

Amarowicz R, Raabe B. Antioxidative activity of leguminous seed extracts evaluated by chemiluminescence methods. Z Naturforsch C. 1997;52:709–712.

Amarowicz R, Pegg RB, Rahimi-Moghaddam P, Barl B, Weil JA. Free-radical scavenging capacity and antioxidant activity of selected plant species from the Canadian prairies. Food Chem. 2004;84(4):551–562.

Weidner A, Amarowicz R, Karamać M, Frączek E. Changes in endogenous phenolic acids during development of Secale cereale caryopses and after dehydration treatment of unripe rye grains. Plant Physiol Biochem. 2000;38(7–8):595–602.

Amarowicz R, Karamac M, Weidner S, Abe S, Shahidi F. Antioxidant activity of wheat caryopses and embryos extracts. J Food Lipids. 2002;9(3):201–210.

Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med. 1999;26(9–10):1231–1237.

Amarowicz R, Piskuła M, Honke J, Rudnicka B, Troszyńska A, Kozłowska H. Extraction of phenolic compounds from lentil seeds (Lens culinaris) with various solvents. Pol J Food Nutr Sci. 1995;4(3):53–62.

Amarowicz R, Weidner S. Content of phenolic acids in rye caryopses determined using DAD-HPLC method. Czech J Food Sci. 2001;19(6):201–205.

Uma S, Prasad TG, Kumar MU. Genetic variability in recovery growth and synthesis of stress proteins in response to polyethylene glycol and salt stress in finger millet. Ann Bot. 1995;76(1):43–49.

Raven PH. Biology of plants. 7th ed. New York, NY: W.H. Freeman; 2005.

Kosowska M, Frączek E, Amarowicz R, Karama M, Abe S, Weidner S. Water-deficit-induced changes in cytoskeleton-bound and other polysomal populations in embryonic tissue during triticale caryopsis germination. Acta Physiol Plant. 2004;26(1):67–74.

Wróbel M, Karama M, Amarowicz R, Fr czek E, Weidner S. Metabolism of phenolic compounds in Vitis riparia seeds during stratification and during germination under optimal and low temperature stress conditions. Acta Physiol Plant. 2005;27(3):313–320.

Costa França MG, Pham Thi AT, Pimentel C, Pereyra Rossiello RO, Zuily-Fodil Y, Laffray D. Differences in growth and water relations among Phaseolus vulgaris cultivars in response to induced drought stress. Env Exp Bot. 2000;43(3):227–237.

Caruso A, Morabito D, Delmotte F, Kahlem G, Carpin S. Dehydrin induction during drought and osmotic stress in Populus. Plant Physiol Biochem. 2002;40(12):1033–1042.

Ismail AM, Hall AE. Variation in traits associated with chilling tolerance during emergence in cowpea germplasm. Field Crops Res. 2002;77(2–3):99–113.

Munns R. Comparative physiology of salt and water stress. Plant Cell Env. 2002;25(2):239–250.

Duncan RF, Hershey JW. Protein synthesis and protein phosphorylation during heat stress, recovery, and adaptation. J Cell Biol. 1989;109(4 pt 1):1467–1481.

Weidner S, Kordala E, Brosowska-Arendt W, Karamać M, Kosińska A, Amarowicz R. Phenolic compounds and properties of antioxidants in grapevine roots (Vitis vinifera L.) under low-temperature stress followed by recovery. Acta Soc Bot Pol. 2009;78(4):279–286.

Posmyk MM, Bailly C, Szafrańska K, Janas KM, Corbineau F. Antioxidant enzymes and isoflavonoids in chilled soybean [Glycine max (L.) Merr.] seedlings. J Plant Physiol. 2005;162(4):403–412.

Chung IM, Kim JJ, Lim JD, Yu CY, Kim SH, Hahn SJ. Comparison of resveratrol, SOD activity, phenolic compounds and free amino acids in Rehmannia glutinosa under temperature and water stress. Env Exp Bot. 2006;56(1):44–53.

Solecka D. Role of phenylpropanoid compounds in plant responses to different stress factors. Acta Physiol Plant. 1997;19(3):257–268.

Karamać M, Kosińska A, Pegg RB. Comparison of radical-scavenging activities for selected phenolic acids. Pol J Food Nutr Sci. 2005;14(2):165–169.

Dixon RA, Paiva NL. Stress-induced phenylpropanoid metabolism. Plant Cell. 1995;7(7):1085–1097.

Szwajgier D, Pielecki J, Targoński Z. Antioxidant activities of cinnamic and benzoic acid derivatives. Acta Sci Pol Technol Aliment. 2005;4(2):129–142.

Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MSS, Wang L. The phenylpropanoid pathway and plant defence – a genomics perspective. Mol Plant Pathol. 2002;3(5):371–390.

Janas KM, Cvikrová M, Pałagiewicz A, Szafranska K, Posmyk MM. Constitutive elevated accumulation of phenylpropanoids in soybean roots at low temperature. Plant Sci. 2002;163(2):369–373.

Naczk M, Shahidi F. Phenolics in cereals, fruits and vegetables: occurrence, extraction and analysis. J Pharm Biomed Anal. 2006;41(5):1523–1542.

López-Amorós ML, Hernández T, Estrella I. Effect of germination on legume phenolic compounds and their antioxidant activity. J Food Compos Anal. 2006;19(4):277–283.

Prasad TK. Mechanisms of chilling-induced oxidative stress injury and tolerance in developing maize seedlings: changes in antioxidant system, oxidation of proteins and lipids, and protease activities. Plant J. 1996;10(6):1017–1026.

Graham TL, Graham MY. Signaling in soybean phenylpropanoid responses (dissection of primary, secondary, and conditioning effects of light, wounding, and elicitor treatments). Plant Physiol. 1996;110(4):1123–1133.

Piślewska M, Bednarek P, Stobiecki M, Zielińska M, Wojtaszek P. Cell wall-associated isoflavonoids and β-glucosidase activity in Lupinus albus plants responding to environmental stimuli. Plant Cell Env. 2002;25(1):20–40.

Wu Q. Purification and antioxidant activities of soybean isoflavones [Master thesis]. Baton Rouge, LA: Departament of Food Science, Louisiana State University; 2003.

Lee CH, Yang L, Xu JZ, Yeung SYV, Huang Y, Chen ZY. Relative antioxidant activity of soybean isoflavones and their glycosides. Food Chem. 2005;90(4):735–741.

Yu O, Jung W, Shi J, Croes RA, Fader GM, McGonigle B, et al. Production of the isoflavones genistein and daidzein in non-legume dicot and monocot tissues. Plant Physiol. 2000;124(2):781–794.

Dixon RA, Harrison MJ, Paiva NL. The isoflavonoid phytoalexin pathway: from enzymes to genes to transcription factors. Physiol Plant. 1995;93(2):385–392.

Dixon RA, Summer LW. Legume natural products: understanding and manipulating complex pathways for human and animal health. Plant Physiol. 2003;131(3):878–885.

Winkel-Shirley B. Flavonoid biosynthesis. a colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 2001;126(2):485–493.

Rawel HM, Czajka D, Rohn S, Kroll J. Interactions of different phenolic acids and flavonoids with soy proteins. Int J Biol Macromol. 2002;30(3–4):137–150.