Assessment of antioxidant system and enzyme/nonenzyme regulation related to ascorbate-glutathione cycle in ferulic acid-treated Triticum aestivum L. roots under boron toxicity
Assessment of antioxidant system and enzyme/nonenzyme regulation related to ascorbate-glutathione cycle in ferulic acid-treated Triticum aestivum L. roots under boron toxicity
Ferulic acid (FA; 3-methoxy-4-hydroxycinnamic acid) can eliminate stress-induced damage because of its ability to induceantioxidant activity under stress. The aim of this study was to identify the effects of FA on water status, antioxidant system, and lipidperoxidation in wheat (Triticum aestivum L.) roots exposed to boron (B) stress. Plants were grown in hydroponic culture containingthe combination or alone form of 25–75 μM FA and 4–8 mM B. Stress significantly decreased growth (RGR), water content (RWC),proline content (Pro), and osmotic potential (YP). However, FA alleviated the decrease in RGR, RWC, and Pro content. Compared tothe control groups, stress decreased the activities of superoxide dismutase (SOD), peroxidase (POX), catalase, and ascorbate peroxidase(APX), but an increase was only observed in glutathione reductase (GR) activity. Hydrogen peroxide (H2O2) content accumulated withB stress. Besides, a notable decrease was observed in the scavenging activity of hydroxyl radical (OH•); thus, wheat roots had high lipidperoxidation (thiobarbituric acid reactive substance content). In response to stress, FA triggered the activities of SOD, POX, and APX.Moreover, when FA was made present in stressed wheat roots, we observed the enhanced activities of dehydroascorbate reductase,and monodehydroascorbate reductase and dehydroascorbate contents which are related to ascorbate-glutathione cycle, so FA couldmaintain ascorbate (AsA) regeneration. However, when wheat roots were treated with stress, FA did not induce the regeneration ofglutathione because of decline in GR activity. Due to successful elimination of H2O2 content, the exogenous application of FA alleviatedB-induced lipid peroxidation in wheat. Consequently, FA eliminated the damage induced by B stress via the increased POX and theenzymes related to Asada-Halliwell pathway (AsA-GSH cycle) in wheat roots.
___
- Abu El-Soud W, Hegab MM, AbdElgawad H, Zinta G, Asard H (2013).
Ability of ellagic acid to alleviate osmotic stress on chickpea
seedlings. Plant Physiology and Biochemistry 71: 173-183.
- Acosta-Estrada BA, Gutierrez-Uribe JA, Serna-Saldivar SO (2014).
Bound phenolics in foods, a review. Food Chemistry 152: 46-55.
- Amarowicz R, Pegg RB, Rahimi-Moghaddam P, Barl B, Weil JA
(2004). Free-radical scavenging capacity and antioxidant
activity of selected plant species from the Canadian prairies.
Food Chemistry 84: 551-562.
- Ayvaz M, Guven A, Blokhina O, Fagerstedt KV (2016). Boron stress,
oxidative damage and antioxidant protection in potato cultivars
(Solanum tuberosum L.). A Acta Agriculturae Scandinavica
Section B-Soil and Plant Science 66: 302-316.
- Balasundram N, Sundram K, Samman S (2006). Phenolic compounds
in plants and agri-industrial by-products: Antioxidant activity,
occurrence, and potential uses. Food Chemistry 99: 191-203.
- Beauchamp C, Fridovich I (1971). Superoxide dismutase: improved
assays and an assay applicable to acrylamide gels. Analytical
Biochemistry 44: 276-287.
- Bergmeyer HU (1970). Methoden der enzymatischen Analyse. 2.
Verlag Chemie (in German).
- Bhardwaj RD, Kaur L, Srivastava P (2017). Comparative evaluation of
different phenolic acids as priming agents for mitigating drought
stress in wheat seedlings. Proceedings of the National Academy
of Sciences, India Section B: Biological Sciences 87: 1133-1142.
- Bradford MM (1976). A rapid and sensitive method for the
quantitation of microgram quantities of protein utilizing the
principle of protein-dye binding. Analytical Biochemistry 72:
248-254.
- Cervilla LM, Blasco B, Rios JJ, Romero L, Ruiz JM (2007). Oxidative
stress and antioxidants in tomato (Solanum lycopersicum) plants
subjected to boron toxicity. Annals of Botany 100: 747-756.
- Chung SK, Osawa T, Kawakishi S (1997). Hydroxyl Radical-scavenging
Effects of Spices and Scavengers from Brown Mustard (Brassica
nigra). Bioscience, Biotechnology, and Biochemistry 61: 118-
123.
- Dalton DA, Russell SA, Hanus FJ, Pascoe GA, Evans HJ (1986).
Enzymatic-reactions of ascorbate and glutathione that prevent
peroxide damage in soybean root-nodules. Proceedings of the
National Academy of Sciences of the United States of America
83: 3811-3815.
- Dutilleul C, Driscoll S, Cornic G, De Paepe R, Foyer CH et al. (2003).
Functional mitochondrial complex I is required by tobacco leaves
for optimal photosynthetic performance in photorespiratory
conditions and during transients. Plant Physiology 131: 264-
275.
- Emebiri L, Michael P, Moody D (2009). Enhanced tolerance to boron
toxicity in two-rowed barley by marker-assisted introgression of
favourable alleles derived from Sahara 3771. Plant and Soil 314:
77-85.
- Foyer CH, Halliwell B (1976). The presence of glutathione and
glutathione reductase in chloroplasts: a proposed role in ascorbic
acid metabolism. Planta 133: 21-25.
- Hatcher DW, Kruger JE (1997). Simple phenolic acids in flours prepared
from Canadian wheat: Relationship to ash content, color, and
polyphenol oxidase activity. Cereal Chemistry 74: 337-343.
- Herzog V, Fahimi H (1973). Determination of the activity of peroxidase.
Analytical Biochemistry 55: e62.
- Jiang M, Zhang J (2002). Involvement of plasma-membrane NADPH
oxidase in abscisic acid- and water stress-induced antioxidant
defense in leaves of maize seedlings. Planta 215: 1022-1030.
- Karabal E, Yucel M, Oktem HA (2003). Antioxidant responses of
tolerant and sensitive barley cultivars to boron toxicity. Plant
Science 164: 925-933.
- Kaya C, Ashraf M (2015). Exogenous application of nitric oxide
promotes growth and oxidative defense system in highly boron
stressed tomato plants bearing fruit. Scientia Horticulturae 185:
43-47.
- Kayihan DS, Kayihan C, Ciftci YO (2016). Excess boron responsive
regulations of antioxidative mechanism at physio-biochemical
and molecular levels in Arabidopsis thaliana. Plant Physiology
and Biochemistry 109: 337-345.
- Laemmli UK (1970). Cleavage of structural proteins during the
assembly of the head of bacteriophage T4. Nature 227: 680-685.
- Lattanzio V, Lattanzio VM, Cardinali A (2006). Role of phenolics in
the resistance mechanisms of plants against fungal pathogens
and insects. Phytochemistry: Advances in research 661: 23-67.
- Li DM, Nie YX, Zhang J, Yin JS, Li Q et al. (2013). Ferulic acid
pretreatment enhances dehydration-stress tolerance of cucumber
seedlings. Biologia Plantarum 57: 711-717.
- Liu ZJ, Guo YK, Bai JG (2010). Exogenous hydrogen peroxide changes
antioxidant enzyme activity and protects ultrastructure in leaves
of two Cucumber ecotypes under osmotic stress. Journal of Plant
Growth Regulation 29: 171-183.
- Mathew S, Abraham TE (2004). Ferulic acid: An antioxidant found
naturally in plant cell walls and feruloyl esterases involved in its
release and their applications. Critical Reviews in Biotechnology
24: 59-83.
- Michalak A (2006). Phenolic compounds and their antioxidant activity
in plants growing under heavy metal stress. Polish Journal of
Environmental Studies 15: 523-530.
- Mittler R, Zilinskas BA (1993). Detection of ascorbate peroxidaseactivity in native gels by inhibition of the ascorbate-dependent
reduction of nitroblue tetrazolium. Analytical Biochemistry 212:
540-546.
- Miyake C, Asada K (1992). Thylakoid-bound ascorbate peroxidase
in spinach-chloroplasts and photoreduction of its primary
oxidation-product monodehydroascorbate radicals in thylakoids.
Plant Cell and Physiology 33: 541-553.
- Nable RO, Banuelos GS, Paull JG (1997). Boron toxicity. Plant and Soil
193: 181-198.
- Nakano Y, Asada K (1981). Hydrogen peroxide is scavenged by
ascorbate-specific peroxidase in spinach chloroplasts. Plant
Cell and Physiology 22: 867-880.
- Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J et al. (2012).
Glutathione in plants: an integrated overview. Plant Cell and
Environment 35: 454-484.
- Nyomora AMS, Sah RN, Brown PH (1997). Boron determination
in biological materials by inductively coupled plasma atomic
emission and mass spectrometry: effects of sample dissolution
methods. Fresenius’ Journal of Analytical Chemistry 357:
1185-1191.
- Ouyang B, Yang T, Li HX, Zhang L, Zhang YY et al. (2007).
Identification of early salt stress response genes in tomato
root by suppression subtractive hybridization and microarray
analysis. Journal of Experimental Botany 58: 507-520.
- Ozfidan-Konakci C, Yildiztugay E, Kucukoduk M (2015). Protective
roles of exogenously applied gallic acid in Oryza sativa
subjected to salt and osmotic stresses: effects on the total
antioxidant capacity. Plant Growth Regulation 75: 219-234.
- Papadakis IE, Dimassi KN, Bosabalidis AM, Therios IN, Patakas
A et al. (2004). Effects of B excess on some physiological and
anatomical parameters of Navelina orange plants grafted on
two rootstocks. Environmental and Experimental Botany 51:
247-257.
- Paradiso A, Berardino R, de Pinto MC, Sanita di Toppi L, Storelli MM
et al. (2008). Increase in ascorbate-glutathione metabolism as
local and precocious systemic responses induced by cadmium
in durum wheat plants. Plant and Cell Physiology 49: 362-374.
- Pizzeghello D, Francioso O, Ertani A, Muscolo A, Nardi S (2013).
Isopentenyladenosine and cytokinin-like activity of different
humic substances. Journal of Geochemical Exploration 129:
70-75.
- Rao KM, Sresty T (2000). Antioxidative parameters in the seedlings
of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to
Zn and Ni stresses. Plant Science 157: 113-128.
- Reid R (2010). Can we really increase yields by making crop plants
tolerant to boron toxicity? Plant Science 178: 9-11.
- Rezaee F, Ghanati F, Behmanesh M (2013). Antioxidant activity
and expression of catalase gene of (Eustoma grandiflorum L)
in response to boron and aluminum. South African Journal of
Botany 84: 13-18.
- Rukkumani R, Aruna K, Varma PS, Menon VP (2004).
Hepatoprotective role of ferulic acid: A dose-dependent study.
Journal of Medicinal Food 7: 456-461.
- Sagi M, Fluhr R (2001). Superoxide production by plant homologues
of the gp91phox NADPH oxidase. Modulation of activity
by calcium and by tobacco mosaic virus infection. Plant
Physiology 126: 1281-1290.
- Sarafi E, Siomos A, Tsouvaltzis P, Therios I (2018). Boron toxicity
effects on the concentration of pigments, carbohydrates
and nutrient elements in six non-grafted pepper cultivars
(Capsicum annuum L.) Indian Journal of Plant Physiology
23(3): 474-485.
- Seevers P, Daly J, Catedral F (1971). The role of peroxidase isozymes
in resistance to wheat stem rust disease. Plant Physiology 48:
353-360.
- Shah ZH, Rehman HM, Akhtar T, Daur I, Nawaz MA et al. (2017).
Redox and Ionic Homeostasis Regulations against Oxidative,
Salinity and Drought Stress in Wheat (A Systems Biology
Approach). Frontiers in Genetics 8.
- Singh S, Kumar V, Upadhyay N, Singh J, Singla S et al. (2017a). Efficient
biodegradation of acephate by Pseudomonas pseudoalcaligenes
PS-5 in the presence and absence of heavy metal ions [Cu(II)
and Fe(III)], and humic acid. 3 Biotech 7:262.
- Singh S, Tripathi DK, Singh S, Sharma S, Dubey NK et al. (2017b).
Toxicity of aluminium on various levels of plant cells and
organism: A review. Environmental and Experimental Botany
137: 177-193.
- Sun B, Yan HZ, Zhang F, Wang QM (2012). Effects of plant hormones
on main health-promoting compounds and antioxidant capacity
of Chinese kale. Food Research International 48: 359-366.
- Sun WN, Van Montagu M, Verbruggen N (2002). Small heat shock
proteins and stress tolerance in plants. Biochimica et Biophysica
Acta - Gene Structure and Expression 1577: 1-9.
- Tariq M., Mott CJB (2007). Effect of Boron on the behaviour of
nutrients in soil-plant systems—A review. Asian Journal of Plant
Science and Research, 6: 195-202.
- Uluisik I, Karakaya HC, Koc A (2018). The importance of boron in
biological systems. Journal of Trace Elements in Medicine and
Biology 45: 156-162.
- Velez-Ramirez AI, van Ieperen W, Vreugdenhil D, Millenaar FF
(2011). Plants under continuous light. Trends in Plant Science
16: 310-318.
- Verstraeten SV, Keen CL, Schmitz HH, Fraga CG, Oteiza PI (2003).
Flavan-3-ols and procyanidins protect liposomes against lipid
oxidation and disruption of the bilayer structure. Free Radical
Biology & Medicine 34: 84-92.
- Yildiztugay E, Ozfidan-Konakci C, Karahan H, Kucukoduk M, Turkan
I (2019). Ferulic acid confers tolerance against excess boron by
regulating ROS levels and inducing antioxidant system in wheat
leaves (Triticum aestivum). Environmental and Experimental
Botany 161: 193-202.
- Wan YY, Chen SY, Huang YW, Li X, Zhang Y et al. (2014). Caffeic
acid pretreatment enhances dehydration tolerance in cucumber
seedlings by increasing antioxidant enzyme activity and proline
and soluble sugar contents. Scientia Horticulturae 173: 54-64.
- Wang JZ, Tao ST, Qi KJ, Wu J, Wu HQ et al. (2011). Changes in
photosynthetic properties and antioxidative system of pear
leaves to boron toxicity. African Journal of Biotechnology 10:
19693-19700.
- Wang Y, Li Y, Ma C, Qiu D (2016). Gas exchange, photosystem II
photochemistry, and the antioxidant system of longan plant
(Dimocarpus longan Lour.) leaves in response to lead (Pb) stress.
Plant Omics 9: 240.
- Woodbury W, Spencer A, Stahmann M (1971). An improved
procedure using ferricyanide for detecting catalase isozymes.
Analytical Biochemistry 44: 301-305.