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Capacity to control oxidative stress-induced caspase-like activity determines the level of tolerance to salt stress in two contrasting maize genotypes

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Abstract

The response of two maize (Zea mays L.) genotypes, named GR (salt-tolerant) and SK (salt-sensitive), to salt stress (150 mM NaCl) was investigated under controlled environmental growth conditions. Genotype SK experienced more oxidative damage than the GR genotype when subjected to salt stress, which corresponded to higher O2 − production rate and H2O2 content in the SK genotype than the GR genotype. Induction of caspase-like activity in response to salt stress was stronger in the SK genotype than in the GR genotype. On the other hand, induction of antioxidant enzyme activity to scavenge O2 − and H2O2 in response to salt stress was weaker in the SK genotype than in the GR genotype. Consequently, the higher level of oxidative damage in the SK genotype in response to salt stress was manifested as more extensive cell death and biomass reduction in the SK genotype than it was in the GR genotype. Our results suggest that a direct relationship exists between salt stress-induced oxidative damage and cell death-inducing caspase-like activity, with tolerance to the salt stress being controlled by the efficiency of the plant antioxidant enzymes in limiting salt stress-induced oxidative damage and thus limiting cell death-inducing caspase-like activity.

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Abbreviations

Ac-DEVD-pNA:

N-Acetyl-Asp-Glu-Val-Asp-p-Nitroanilide

ANOVA:

Analysis of variance

APX:

Ascorbate peroxidase

EDTA:

Ethylenediaminetetraacetic acid

DW:

Dry weight

GSH:

Glutathione

GPX:

Glutathione peroxidase

MDA:

Malondialdehyde

MES:

2-(N-Morpholino)ethanesulfonic acid

NADPH:

Nicotinamide adenine dinucleotide phosphate

PMSF:

Phenylmethylsulfonyl fluoride

ROS:

Reactive oxygen species

SDS:

Sodium dodecyl sulphate

SOD:

Superoxide dismutase

TCA:

Trichloroacetic acid

WST-1:

2-(4-Iodophenyl)-3-(4-nitrophenyl)-5-(2,4-disulfophenyl)-2H-tetrazolium

XTT:

2,3-Bis(2-methoxy-4-nitro-5-sulfophenyl)-2H-tetrazolium-5-carbox-anilide

References

  • Able A, Guest D, Sutherland M (1998) Use of a new tetrazoliumbased assay to study the production of superoxide radicals by tobacco cell cultures challenged with avirulent zoospores of Phytophthora parasitica var nicotanae. Plant Physiol 117:491–499

    Article  PubMed  CAS  Google Scholar 

  • Andronis EA, Roubelakis-Angelakis KA (2010) Short-term salinity stress in tobacco plants leads to the onset of animal-like PCD hallmarks in planta in contrast to long-term stress. Planta 231:437–448

    Article  PubMed  CAS  Google Scholar 

  • Asada K (1984) Chloroplasts: formation of active oxygen and its scavenging. Method Enzymol 105:422–429

    Article  CAS  Google Scholar 

  • Badawi GH, Yamauchi Y, Shimada E, Sasaki R, Kawano N, Tanaka K (2004) Enhanced tolerance to salt stress and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts. Plant Sci 166:919–928

    Article  Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 6:559–566

    Article  Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Method Enzymol 52:302–310

    Article  CAS  Google Scholar 

  • Chen HJ, Su CT, Lin CH, Huang GJ, Lin YH (2010) Expression of sweet potato cysteine protease SPCP2 altered developmental characteristics and stress responses in transgenic Arabidopsis plants. J Plant Physiol 167:838–847

    Article  PubMed  CAS  Google Scholar 

  • De Azevedo Neto AD, Prisco JT, Enéas-Filho J, de Abreu CEB, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56:87–94

    Article  Google Scholar 

  • De Pinto MC, Locato V, De Gara L (2012) Redox regulation in plant programmed cell death. Plant Cell Environ 35:234–244

    Article  PubMed  Google Scholar 

  • Ekmekçi Y, Tanyolaç D, Ayhan B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities of two maize cultivars. J Plant Physiol 165:600–611

    Article  PubMed  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 

  • El-Shabrawi H, Kumar B, Kaul T, Reddy MK, Singla-Pareek SL, Sopory SK (2010) Redox homeostasis, antioxidant defense, and methylglyoxal detoxification as markers for salt tolerance in Pokkali rice. Protoplasma 245:85–96

    Article  PubMed  CAS  Google Scholar 

  • Forsthoefel NR, Cushman MAF, Ostrem JA, Cushman JC (1998) Induction of a cysteine protease cDNA from Mesembryanthemum crystallinum leaves by environmental stress and plant growth regulators. Plant Sci 136:195–206

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    Article  PubMed  CAS  Google Scholar 

  • Gémes K, Poór P, Horváth E, Kolbert Z, Szopkó D, Szepesi Á, Tari I (2011) Cross-talk between salicylic acid and NaCl-generated reactive oxygen species and nitric oxide in tomato during acclimation to high salinity. Physiol Plantarum 142:179–192

    Article  Google Scholar 

  • Gossett DR, Millhollon EP, Lucas MC (1994) Antioxidant response to NaCl stress in salt-tolerant and salt-sensitive cultivars of cotton. Crop Sci 34:706–714

    Article  CAS  Google Scholar 

  • Groten K, Dutilleul C, van Heerden PDR, Vanackera H, Bernard S, Finkemeier I, Dietz KJ, Foyer CH (2006) Redox regulation of peroxiredoxin and proteinases by ascorbate and thiols during pea root nodule senescence. FEBS Lett 580:1269–1276

    Article  PubMed  CAS  Google Scholar 

  • He R, Drury GE, Rotari VI, Gordon A, Willer M, Farzaneh T, Woltering EJ, Gallois P (2008) Metacaspase-8 modulates programmed cell death induced by ultraviolet light and H2O2 in Arabidopsis. J Biol Chem 283:774–783

    Article  PubMed  CAS  Google Scholar 

  • Hernández JA, Jiménez A, Mullineaux P, Sevilia 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  Google Scholar 

  • Katsuhara M (1997) Apoptosis-like cell death in barley roots under salt stress. Plant Cell Physiol 38:1091–1093

    Article  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 

  • Li JY, Jiang AL, Zhang W (2007) Salt stress-induced programmed cell death in rice root tip cells. J Integr Plant Biol 49:481–486

    Article  CAS  Google Scholar 

  • Maia JM, Costa de Macedo CE, Voigt EL, Freitas JBS, Silveira JAG (2010) Antioxidant enzymatic protection in leaves of two contrasting cowpea cultivars under salinity. Biol Plant 54:159–163

    Article  CAS  Google Scholar 

  • Mallik S, Nayak M, Sahu BB, Panigrahi AK, Shaw BP (2011) Response of antioxidant enzymes to high NaCl concentration in different salt-tolerant plants. Biol Plant 55:191–195

    Article  CAS  Google Scholar 

  • Mandhania S, Madan S, Sawhney V (2006) Antioxidant defense mechanism under salt stress in wheat seedlings. Biol Plant 50:227–231

    Article  CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  PubMed  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 17:405–410

    Article  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  PubMed  CAS  Google Scholar 

  • Naito Y, Fujie M, Usami S, Murooka Y, Yamada T (2000) The involvement of a cysteine proteinase in the nodule development in Chinese milk vetch infected with Mesorhizobium huakuii subsp. rengei. Plant Physiol 124:1087–1095

    Article  PubMed  CAS  Google Scholar 

  • Noreen Z, Ashraf M, Akram NA (2010) Salt-induced regulation of some key antioxidant enzymes and physio-biochemical phenomena in five diverse cultivars of turnip (Brassica rapa L.). J Agron Crop Sci 196:273–285

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sairam RK, Srivastava GC, Agarwal S, Meena RC (2005) Differences in antioxidant activity in response to salinity stress tolerant and susceptible wheat genotypes. Biol Plant 49:85–89

    Article  CAS  Google Scholar 

  • Sanevas N, Sunohara Y, Matsumoto H (2007) Characterization of reactive oxygen species-involved oxidative damage in Hapalosiphon species crude extract-treated wheat and onion roots. Weed Biol Manag 7:172–177

    Article  CAS  Google Scholar 

  • Seckin B, Turkan I, Sekmen AH, Ozfidan C (2010) The role of antioxidant defense systems at differential salt tolerance of Hordeum marinum Huds. (sea barley grass) and Hordeum vulgare L. (cultivated barley). Environ Exp Bot 69:76–85

    Article  CAS  Google Scholar 

  • Shalata A, Tal M (2002) The effect of salt stress on lipid peroxidation and antioxidants in the leaf of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii. Physiol Plant 104:169–174

    Article  Google Scholar 

  • Solomon M, Belenghi B, Delledonne M, Menachem E, Levine A (1999) The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11:431–443

    PubMed  CAS  Google Scholar 

  • Tseng MJ, Liu CW, Yiu JC (2007) Enhanced tolerance to sulfur dioxide and salt stress of transgenic Chinese cabbage plants expressing both superoxide dismutase and catalase in chloroplasts. Plant Physiol Biochem 45:822–833

    Article  PubMed  CAS  Google Scholar 

  • Vaidyanathan H, Sivakumur P, Chakrabarty R, Thomas G (2003) Scavenging of reactive oxygen species in NaCl-stressed rice (Oryza sativa L.)—differential responses in salt-tolerant and sensitive varieties. Plant Sci 165:1411–1418

    Article  CAS  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • Vincent JL, Brewin NJ (2000) Immunolocalization of cysteine protease in vacuoles, vesicles, and symbiosomes of pea nodule cells. Plant Physiol 123:521–530

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Li X, Liu Y, Zhao X (2010) Salt stress induces programmed cell death in Thellungiella halophila suspension-cultured cells. J Plant Physiol 167:1145–1151

    Article  PubMed  CAS  Google Scholar 

  • Wu L, Zhang Z, Zhang H, Wang XC, Huang R (2008) Transcriptional modulation of ethylene response factor protein JERF3 in the oxidative stress response enhances tolerance of tobacco seedlings to salt, drought, and freezing. Plant Physiol 148:1953–1963

    Article  PubMed  CAS  Google Scholar 

  • Zhang XX, Liu SK, Takano T (2008) Two cysteine proteinase inhibitors from Arabidopsis thaliana, AtCYSa and AtCYSb, increasing the salt, drought, oxidation and cold tolerance. Plant Mol Biol 68:131–143

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the University of the Western Cape, Stellenbosch University, the National Research Foundation (South Africa) and the National Office for Research and Technology (Hungary).

Conflict of interest

All authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Biotechnology, University of the Western Cape, Private Bag X17, Bellville, 7535, South Africa

    Marshall Keyster, Ashwil Klein, Alex Jacobs & Ndiko Ludidi

  2. Institute for Plant Biotechnology, Stellenbosch University, Private Bag X1, Matieland, South Africa

    Marshall Keyster, Morné Du Plessis & Abidemi Kappo

  3. Agricultural Institute, Hungarian Academy of Sciences, Center for Agricultural Research, P.O. Box 19, Martonvásár, 2462, Hungary

    Gábor Kocsy & Gábor Galiba

Authors
  1. Marshall Keyster
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  2. Ashwil Klein
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  3. Morné Du Plessis
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  4. Alex Jacobs
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  5. Abidemi Kappo
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  6. Gábor Kocsy
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  7. Gábor Galiba
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  8. Ndiko Ludidi
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Correspondence to Ndiko Ludidi.

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Communicated by P. Sowinski.

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Keyster, M., Klein, A., Du Plessis, M. et al. Capacity to control oxidative stress-induced caspase-like activity determines the level of tolerance to salt stress in two contrasting maize genotypes. Acta Physiol Plant 35, 31–40 (2013). https://doi.org/10.1007/s11738-012-1045-4

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  • DOI: https://doi.org/10.1007/s11738-012-1045-4

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