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Sphaerophysa kotschyana, an endemic species from Central Anatolia: antioxidant system responses under salt stress

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Abstract

Sphaerophysa kotschyana is a Turkish endemic and endangered plant that grows near Salt Lake, in Konya, Turkey. However, little is known about the ability of this plant to generate/remove reactive oxygen species (ROS) or its adaptive biochemical responses to saline environments. After exposure of S. kotschyana to 0, 150, and 300 mM NaCl for 7 and 14 days, we investigated (1) the activities and isozyme compositions of the antioxidant enzymes superoxide dismutase (SOD), catalase (CAT), peroxidase (POX), ascorbate peroxidase (APX), and glutathione reductase (GR); (2) the oxidative stress parameters NADPH oxidase (NOX) activity, lipid peroxidation (MDA), total ascorbate (tAsA) content, and total glutathione content (tGlut); and (3) ROS levels for superoxide anion radical (O ·−2 ), hydrogen peroxide (H2O2), hydroxyl radicals (OH·), and histochemical staining of O ·−2 and H2O2. H2O2 content increased after 14 days of salt stress, which was consistent with the results from histochemical staining and NOX activity measurements. In contrast, oxidative stress induced by 150 mM NaCl was more efficiently prevented, as indicated by low malondialdehyde (MDA) levels and especially at 7 days, by increased levels of SOD, POX, APX, and GR. However, at 300 mM NaCl, decreased levels of protective enzymes such as SOD, CAT, POX, and GR, particularly with long-term stress (14 days), resulted in limited ROS scavenging activity and increased MDA levels. Moreover, at 300 mM NaCl, the high H2O2 content caused oxidative damage rather than inducing protective responses against H2O2. These results suggest that S. kotschyana is potentially tolerant to salt-induced damage only at low salt concentrations.

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References

  • Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93

    Article  PubMed  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  PubMed  CAS  Google Scholar 

  • Ben Amor N, Ben Hamed K, Debez A, Grignon G, Abdelly C (2005) Physiological and antioxidant responses of the perennial halophyte Crithmum maritimum to salinity. Plant Sci 168:889–899

    Article  CAS  Google Scholar 

  • Bergmeyer N (1970) Methoden der enzymatischen analyse, vol 1. Akademie Verlag, Berlin

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of the protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Gruissem W, Buchannan B, Jones R (eds) Biochemistry and molecular biology of plants. ASSP, Rockville, pp 1158–1249

    Google Scholar 

  • Cheeseman JM (2007) Hydrogen peroxide and plant stress: a challenging relationship. Plant Stress 1:4–15

    Google Scholar 

  • Chung SK, Osawa T, Kawakishi S (1997) Hydroxyl radical-scavenging effects of spices and scavengers from brown mustard (Brassica nigra). Biosci Biotechnol Biochem 61:118–123

    Article  CAS  Google Scholar 

  • CITES (2008) Convention on international trade in endangered species of wild fauna and flora. Appendices I, II and III. http://www.cites.org/

  • Duran A, Martin E, Ozturk M, Cetin O, Dinc M, Ozdemir A (2010) Morphological, karyological and ecological features of halophytic endemic Sphaerophysa kotschyana Boiss (Fabaceae) in Turkey. Biodicon 3:163–169

    Google Scholar 

  • Ellouzi H, Hamed KB, Cela J, Munné-Bosch S, Abdelly C (2011) Early effects of salt stress on the physiological and oxidative status of Cakile maritima (halophyte) and Arabidopsis thaliana (glycophyte). Physiol Plant 142:128–143

    Article  PubMed  CAS  Google Scholar 

  • FAO (Food and Agriculture Organization) (2008) Land and plant nutrition management service. http://www.fao.org/ag/ag/agll/spush

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplast: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  Google Scholar 

  • Fryer M, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53:1249–1254

    Article  PubMed  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  PubMed  CAS  Google Scholar 

  • Gossett DR, Millhollon EP, Lucas MC (1994) Changes in antioxidant levels in response to NaCl treatment in salt tolerant and sensitive cultivars of cotton Gossypium hirsutum L. Crop Sci 34:706–714

    Article  CAS  Google Scholar 

  • Grosicka-Maciag E, Kurpios D, Czeczot H, Szumilo M, Skrzycki M, Suchocki P, Rahden-Staron I (2008) Changes in antioxidant defense systems induced by thiram in V79 Chinese hamster fibroblasts. Toxicol in Vitro 22:28–35

    Article  PubMed  CAS  Google Scholar 

  • Hasanuzzaman M, Nahar K, Alam M, Fujita M (2012) Exogenous nitric oxide alleviates high temperature induced oxidative stress in wheat (Triticum aestivum L.) seedlings by modulating the antioxidant defense and glyoxalase system. Aus J. Crop Sci 6:1314–1323

    CAS  Google Scholar 

  • Hasanuzzaman M, Nahar K, Fujita M (2013) Plant response to salt stress and role of exogenous protectants to mitigate salt-induced damages. In: Ahmad P, Azooz MM, Prasad MNV (eds) Ecophysiology and responses of plants under salt stress. Springer, New York, pp 25–87

    Chapter  Google Scholar 

  • Heidari M, Jamshidi P (2011) Effects of salinity and potassium application on antioxidant enzyme activities and physiological parameters in pearl millet. Agric Sci China 10:228–237

    Article  CAS  Google Scholar 

  • Hernandez JA, Almansa MS (2002) Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. Physiol Plant 115:251–257

    Article  PubMed  CAS  Google Scholar 

  • Hernandez JA, Jimenez A, Mullineaux P, Sevilla F (2000) Tolerance of pea (Pisum sativum L.) to long term salt stress is associated with induction of antioxidant defences. Plant Cell Environ 23:853–862

    Article  CAS  Google Scholar 

  • Hernandez M, Fernandez-Garcia N, Diaz-Vivancos P, Olmos E (2010) A different role for hydrogen peroxide and the antioxidative system under short and long salt stress in Brassica oleracea roots. J Exp Bot 61:521–535

    Article  PubMed  CAS  Google Scholar 

  • Herzog V, Fahimi H (1973) Determination of the activity of peroxidase. Anal Biochem 55:554–562

    Article  PubMed  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. Calif AES Bull 347:1–32

    Google Scholar 

  • Hodges M (2003) Oxidative stress and post harvest produce. In: Hodges M (ed) Post harvest oxidative stress in horticultural crops. Food Products Press, New York, pp 1–12

    Google Scholar 

  • Isayenkov SV (2012) Physiological and molecular aspects of salt stress in plants. Cytol Genet 46:302–318

    Article  Google Scholar 

  • Jaleel CA, Gopi R, Sankar B, Manivannan P, Kishorekumar A, Sridharan R, Panneerselvam R (2007) Studies on germination, seedling vigour, lipid peroxidation and proline metabolism in Catharanthus roseus seedlings under salt stress. South Afr J Bot 73:190–195

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Johnson CM, Ulrich A (1959) Analytical methods for use in plant analysis. Calif Aes Bull 766:11

    Google Scholar 

  • Joo JH, Wang SY, Chen JG, Jones AM, Fedoroff NV (2005) Different signaling and cell death roles of heterotrimeric G protein α- and β-subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17:957–970

    Article  PubMed  CAS  Google Scholar 

  • Joseph B, Jini D, Sujatha S (2010) Biological and physiological perspectives of specificity in abiotic salt stress response from various rice plants. Asian J Agric Sci 2:99–105

    Google Scholar 

  • Kholova J, Hash CT, Kakkera A, Kocova M, Vadez V (2010) Constitutive water-conserving mechanisms are correlated with the terminal drought tolerance of pearl millet [Pennisetum glaucum (L.) R.Br.]. J Exp Bot 61:369–377

    Article  PubMed  CAS  Google Scholar 

  • Ksouri R, Megdiche W, Debez A, Falleh H, Grignon C, Abdelly C (2007) Salinity effects on polyphenol content and antioxidant activities in leaves of the halophyte Cakile maritima. Plant Physiol Biochem 45:244–249

    Article  PubMed  CAS  Google Scholar 

  • Ksouri R, Megdiche W, Falleh H, Trabelsi N, Boulaaba M, Smaoui A, Abdelly C (2008) Influence of biological, environmental and technical factors on phenolic content and antioxidant activities of Tunisian halophytes. C. R. Biol 331:865–873

    Google Scholar 

  • Kwak JM, Mori IC, Pei Z, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633

    Article  PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Lee DH, Kim YS, Lee CB (2001) The inductive responses of the antioxidant enzymes by salt stress in the rice (Oryza sativa L.). J Plant Physiol 158:737–745

    Article  CAS  Google Scholar 

  • 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. J Plant Growth Regul 29:171–183

    Article  Google Scholar 

  • Lokhande VH, Nikam TD, Patade VY, Ahire ML, Suprasanna P (2011) Effects of optimal and supra-optimal salinity stress on antioxidative defence, osmolytes and in vitro growth responses in Sesuvium portulacastrum L. Plant Cell Tissue Organ Cult 104:41–49

    Article  CAS  Google Scholar 

  • Madhava Rao KV, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeon pea [Cajanus cajan (L.) Millspaugh] in response to Zn and Ni stresses. Plant Sci 157:113–128

    Article  PubMed  CAS  Google Scholar 

  • Meloni DA, Oliva MA, Martinez CA, Cambrai J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ Exp Bot 49:69–76

    Article  CAS  Google Scholar 

  • Mittler R, Zilinskas BA (1993) Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate dependent reduction of nitroblue tetrazolium. Anal Biochem 212:540–546

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nyomora AMS, Sah RN, Brown PH, Miller RO (1997) Boron determination in biological materials by inductively coupled plasma atomic emission and mass spectrophotometry: effects of sample dissolution methods. Fresenius J Anal Chem 357:1185–1191

    Article  CAS  Google Scholar 

  • Panda SK, Khan MH (2009) Growth, oxidative damage and antioxidant responses in greengram (Vigna radiata L.) under short-term salinity stress and its recovery. J Agron Crop Sci 195:442–454

    Article  CAS  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349

    Article  PubMed  CAS  Google Scholar 

  • Parida AK, Das AB, Mohanty P (2004) Defense potentials to NaCl in a mangrove Bruguiera parviflora: differential changes of isozymes of some antioxidant enzymes. J Plant Physiol 161:531–542

    Article  PubMed  CAS  Google Scholar 

  • Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734

    Article  PubMed  CAS  Google Scholar 

  • Polhill R, Raven P (1981) Advances in legume systematics part I. Royal Botanic Gardens, Kew

    Google Scholar 

  • Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91(phox) NADPH oxidase: modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290

    Google Scholar 

  • Seevers FM, Daly JM, Catedral FF (1971) The role of peroxidase isozymes in resistance to wheat stem rust. Plant Physiol 48:353–360

    Article  PubMed  CAS  Google Scholar 

  • Sekmen AH, Turkan I, Tanyolac ZO, Ozfidan C, Dinc A (2012) Different antioxidant defense responses to salt stress during germination and vegetative stages of endemic halophyte Gypsophila oblanceolata Bark. Environ Exp Bot 77:63–76

    Article  CAS  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    Article  PubMed  CAS  Google Scholar 

  • Tester M, Davenport RJ (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  PubMed  CAS  Google Scholar 

  • Turkan I, Demiral T (2009) Recent developments in understanding salinity tolerance. Environ Exp Bot 67:2–9

    Article  Google Scholar 

  • Uzilday B, Turkan I, Sekmen AH, Ozgur R, Karakaya HC (2012) Comparison of ROS formation and antioxidant enzymes in Cleome gynandra (C4) and Cleome spinosa (C3) under drought stress. Plant Sci 182:59–70

    Article  PubMed  CAS  Google Scholar 

  • Vitória AP, Lea PJ, Azevedo RA (2001) Antioxidant enzymes responses to cadmium in radish tissues. Phytochemistry 57:701–710

    Article  PubMed  Google Scholar 

  • Woodbury W, Spencer AK, Stahman MA (1971) An improved procedure for using ferricyanide for detecting catalase isozymes. Anal Biochem 44:301–305

    Article  PubMed  CAS  Google Scholar 

  • Xu S, Li J, Zhang X, Wei H, Cui L (2006) Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environ Exp Bot 56:274–285

    Article  CAS  Google Scholar 

  • Xue B, Zhang A, Jiang M (2009) Involvement of polyamine oxidase in abscisic acid induced cytosolic antioxidant defense in leaves of maize. J Integr Plant Biol 51:225–234

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Xu S, An L, Chen N (2007) NADPH oxidase-dependent hydrogen peroxide production, induced by salinity stress, may be involved in the regulation of total calcium in roots of wheat. J Plant Physiol 164:1429–1435

    Article  PubMed  CAS  Google Scholar 

  • Yazici I, Turkan I, Sekmen AH, Demiral T (2007) Salinity tolerance of purslane (Portulaca oleracea L.) is achieved by enhanced antioxidative system, lower level of lipid peroxidation and proline accumulation. Environ Exp Bot 61:49–57

    Article  CAS  Google Scholar 

  • Yildiztugay E, Sekmen AH, Turkan I, Kucukoduk M (2011) Elucidation of physiological and biochemical mechanisms of an endemic halophyte Centaurea tuzgoluensis under salt stress. Plant Physiol Biochem 49:816–824

    Article  PubMed  CAS  Google Scholar 

  • Zhou F, Mosher S, Tian M, Sassi G, Parker J, Klessig DF (2008) The Arabidopsis gain-of-function mutant ssi4 requires RAR1 and SGT1b differentially for defense activation and morphological alterations. Mol Plant Microbe Interact 21:40–49

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Financial support for this work was provided by Selcuk University Scientific Research Projects Coordinating Office (Project number: 11401069). We gratefully thank to Dr. Mirza Hasanuzzaman Assist. Prof., department of Agronomy, Sher-e-Bangla Agricultural University, Dhaka, Bangladesh, for his recommendation on performing on analysis of tAsA and tGlut contents and language correction. We also would like to thank to Dr. Mehmet Hamurcu Assist. Prof., for his technical assistance on ICP-OES analyses.

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Authors and Affiliations

  1. Department of Biology, Science Faculty, Selcuk University, Campus, 42031, Konya, Turkey

    Evren Yildiztugay & Mustafa Kucukoduk

  2. Department of Biology, Science Faculty, Necmettin Erbakan University, Meram, 42090, Konya, Turkey

    Ceyda Ozfidan-Konakci

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  1. Evren Yildiztugay
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Correspondence to Evren Yildiztugay.

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Yildiztugay, E., Ozfidan-Konakci, C. & Kucukoduk, M. Sphaerophysa kotschyana, an endemic species from Central Anatolia: antioxidant system responses under salt stress. J Plant Res 126, 729–742 (2013). https://doi.org/10.1007/s10265-013-0573-3

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