Skip to main content

Plant Glutathione Peroxidases: Antioxidant Enzymes in Plant Stress Responses and Tolerance

  • Chapter
  • First Online:
Glutathione in Plant Growth, Development, and Stress Tolerance

Abstract

In contrast to other eukaryotic organisms, plants are unable to run away from unfavourable conditions; they must cope with different abiotic and biotic stress factors. Under abiotic and biotic stresses, the production of reactive oxygen and reactive nitrogen species (ROS and RNS) can damage the biological membranes, proteins and nucleic acids. However, plants have developed complex defence systems including different non-enzymatic and enzymatic antioxidants as shields to prevent the toxic effects of an increased amount of ROS and RNS. Glutathione peroxidases (GPXs) are important antioxidant enzymes in animals, but plants contain GPX-like (GPXLs) enzymes. In contrast to animal GPXs, plant GPXLs contain cysteine in their active site instead of selenocysteine, and most of them prefer thioredoxin as the electron donor rather than glutathione. In the last 25 years, many researches proved that plant GPXLs also are essential elements of plant stress responses and are important ROS scavengers. Overexpression of GPXLs in different plant species led to increased tolerance against drought, salt, osmotic, heavy metal and particularly oxidative stresses; however, in some cases, it caused decreased tolerance against biotic stresses. In this chapter, we focus on the importance of plant GPXLs in stress responses, highlighting the significance of distinct genes as possible candidates for genetic engineering to improve the yield of agricultural plants under unfavourable environment.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Agrawal GK, Rakwal R, Jwa N-S (2002) Cloning and characterization of a jasmonate inducible rice (Oryza sativa L.) peroxidase gene, OsPOX, against global signaling molecules and certain inhibitors of kinase-signaling cascade(s). Plant Sci 162:49–58

    Google Scholar 

  • Anderson JV, Davis DG (2004) Abiotic stress alters transcript profiles and activity of glutathione S-transferase, glutathione peroxidase, and glutathione reductase in Euphorbia esula. Physiol Plant 120:421–433

    Article  CAS  PubMed  Google Scholar 

  • Ashraf M, Harris P (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16

    Article  CAS  Google Scholar 

  • Avsian-Kretchmer O, Eshdat Y, Gueta-Dahan Y, Ben-Hayyim G (1999) Regulation of stress-induced phospholipid hydroperoxide glutathione peroxidase expression in citrus. Planta 209:469–477

    Article  CAS  PubMed  Google Scholar 

  • Beeor-Tzahar T, Ben-Hayyim G, Holland D, Faltin Z, Eshdat Y (1995) A stress-associated citrus protein is a distinct plant phospholipid hydroperoxide glutathione peroxidase. FEBS Lett 366:151–155

    Article  CAS  PubMed  Google Scholar 

  • Bela K, Horvath E, Galle A, Szabados L, Tari I, Csiszar J (2015) Plant glutathione peroxidases: emerging role of the antioxidant enzymes in plant development and stress responses. J Plant Physiol 176:192–201

    Article  CAS  PubMed  Google Scholar 

  • Ben-Hayyim G, Faltin Z, Gepstein S, Camoin L, Strosberg AD, Eshdat Y (1993) Isolation and characterization of salt-associated protein in citrus. Plant Sci 88:129–140

    Article  CAS  Google Scholar 

  • Brigelius-Flohe R, Maiorino M (2013) Glutathione peroxidases. Biochim Biophys Acta 1830:3289–3303

    Article  CAS  PubMed  Google Scholar 

  • Carillo P, Annunziata MG, Pontecorvo G, Fuggi A, Woodrow P (2011) Salinity stress and salt tolerance. In: Abiotic stress in plants – mechanisms and adaptations. InTech, Rijeka, pp 21–38

    Google Scholar 

  • Chang CC, Ślesak I, Jordá L, Sotnikov A, Melzer M, Miszalski Z, Mullineaux PM, Parker JE, Karpińska B, Karpiński S (2009) Arabidopsis chloroplastic glutathione peroxidases play a role in cross talk between photooxidative stress and immune responses. Plant Physiol 150:670–683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Vaghchhipawala Z, Li W, Asard H, Dickman MB (2004) Tomato phospholipid hydroperoxide glutathione peroxidase inhibits cell death induced by Bax and oxidative stresses in yeast and plants. Plant Physiol 135:1630–1641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Zimei L, Cui J, Jiangang D, Xia X, Liu D, Yu J (2011) Alleviation of chilling-induced oxidative damage by salicylic acid pretreatment and related gene expression in eggplant seedlings. Plant Growth Regul 65:101–108

    Article  CAS  Google Scholar 

  • Churin Y, Schilling S, Börner T (1999) A gene family encoding glutathione peroxidase homologues in Hordeum vulgare (barley). FEBS Lett 459:33–38

    Article  CAS  PubMed  Google Scholar 

  • Criqui MC, Jamet E, Parmentier Y, Marbach J, Durr A, Fleck J (1992) Isolation and characterization of a plant cDNA showing homology to animal glutathione peroxidases. Plant Mol Biol 18:623–627

    Article  CAS  PubMed  Google Scholar 

  • De Gara L, de Pinto MC, Tommasi F (2003) The antioxidant systems vis-à-vis reactive oxygen species during plant–pathogen interaction. Plant Physiol Biochem 41:863–870

    Article  Google Scholar 

  • Depège N, Varenne M, Boyer N (2000) Induction of oxidative stress and GPX-like protein activation in tomato plants after mechanical stimulation. Physiol Plant 110:209–214

    Article  Google Scholar 

  • Diao Y, Xu H, Li G, Yu A, Yu X, Hu W, Zheng X, Li S, Wang Y, Hu Z (2014) Cloning a glutathione peroxidase gene from Nelumbo nucifera and enhanced salt tolerance by overexpressing in rice. Mol Biol Rep 41:4919–4927

    Article  CAS  PubMed  Google Scholar 

  • Dukhovskis P, Juknys R, Brazaityte A, Zukauskaite I (2003) Plant response to integrated impact of natural and anthropogenic stress factors. Russ J Plant Physiol 50:147–154

    Article  CAS  Google Scholar 

  • FAO (2015) The impact of disasters on agriculture and food security. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • FAO (2016) Agriculture, forestry and fishery statistics, Statistical books. Food and Agriculture Organization of the United Nations, Luxembourg: Belgium

    Google Scholar 

  • FAO (2017) The impact of disasters on agriculture: addressing the information gap. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • Farooq M, Wahid A, Kobayashi N, Fujita D, Basra S (2009) Plant drought stress: effects, mechanisms and management. In: Sustainable agriculture. Springer, Dordrecht, pp 153–188

    Chapter  Google Scholar 

  • Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide-and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant 100:241–254

    Article  CAS  Google Scholar 

  • Fu J-Y (2014) Cloning of a new glutathione peroxidase gene from tea plant (Camellia sinensis) and expression analysis under biotic and abiotic stresses. Bot Stud 55:1–6

    Article  Google Scholar 

  • Gaber A (2011) Arabidopsis glutathione peroxidase 8 is a key enzyme in response to environmental stresses. Arab J Biotechnol 14:213–224

    Google Scholar 

  • Gaber A, Ogata T, Maruta T, Yoshimura K, Tamoi M, Shigeoka S (2012) The involvement of Arabidopsis glutathione peroxidase 8 in the suppression of oxidative damage in the nucleus and cytosol. Plant Cell Physiol 53:1596–1606

    Article  CAS  PubMed  Google Scholar 

  • Gao F, Chen J, Ma T, Li H, Wang N, Li Z, Zhang Z, Zhou Y (2014) The glutathione peroxidase gene family in Thellungiella salsuginea: genome-wide identification, classification, and gene and protein expression analysis under stress conditions. Int J Mol Sci 15:3319–3335

    Article  PubMed  PubMed Central  Google Scholar 

  • Heagle AS (1989) Ozone and crop yield. Annu Rev Phytopathol 27:397–423

    Article  CAS  Google Scholar 

  • Herbette S, Lenne C, Leblanc N, Julien JL, Drevet JR, Roeckel-Drevet P (2002) Two GPX-like proteins from Lycopersicon esculentum and Helianthus annuus are antioxidant enzymes with phospholipid hydroperoxide glutathione peroxidase and thioredoxin peroxidase activities. Eur J Biochem 269:2414–2420

    Article  CAS  PubMed  Google Scholar 

  • Herbette S, Menn AL, Rousselle P, Ameglio T, Faltin Z, Branlard G, Eshdat Y, Julien JL, Drevet JR, Roeckel-Drevet P (2005) Modification of photosynthetic regulation in tomato overexpressing glutathione peroxidase. Biochim Biophys Acta 1724:108–118

    Article  CAS  PubMed  Google Scholar 

  • Herbette S, Roeckel-Drevet P, Drevet JR (2007) Seleno-independent glutathione peroxidases. FEBS J 274:2163–2180

    Article  CAS  PubMed  Google Scholar 

  • Herbette S, Labrouhe DTD, Drevet JR, Roeckel-Drevet P (2011) Transgenic tomatoes showing higher glutathione peroxidase antioxidant activity are more resistant to an abiotic stress but more susceptible to biotic stresses. Plant Sci 180:548–553

    Article  CAS  PubMed  Google Scholar 

  • Holland D, Ben-Hayyim G, Faltin Z, Camoin L, Strosberg AD, Eshdat Y (1993) Molecular characterization of salt-stress-associated protein in citrus: protein and cDNA sequence homology to mammalian glutathione peroxidases. Plant Mol Biol 21:923–927

    Article  CAS  PubMed  Google Scholar 

  • Holland D, Faltin Z, Perl A, Ben-Hayyim G, Eshdat Y (1994) A novel plant glutathione peroxidase-like protein provides tolerance to oxygen radicals generated by paraquat in Escherichia coli. FEBS Lett 337:52–55

    Article  CAS  PubMed  Google Scholar 

  • Imai H, Nakagawa Y (2003) Biological significance of phospholipid hydroperoxide glutathione peroxidase (PHGPx, GPx4) in mammalian cells. Free Radic Biol Med 34:145–169

    Article  CAS  PubMed  Google Scholar 

  • Iqbal A, Yabuta Y, Takeda T, Nakano Y, Shigeoka S (2006) Hydroperoxide reduction by thioredoxin-specific glutathione peroxidase isoenzymes of Arabidopsis thaliana. FEBS J 273:5589–5597

    Article  CAS  PubMed  Google Scholar 

  • Islam T, Manna M, Kaul T, Pandey S, Reddy CS, Reddy M (2015) Genome-wide dissection of Arabidopsis and rice for the identification and expression analysis of glutathione peroxidases reveals their stress-specific and overlapping response patterns. Plant Mol Biol Report 33:1413–1427

    Article  CAS  Google Scholar 

  • Jamil A, Riaz S, Ashraf M, Foolad M (2011) Gene expression profiling of plants under salt stress. Crit Rev Plant Sci 30:435–458

    Article  Google Scholar 

  • Jung BG, Lee KO, Lee SS, Chi YH, Jang HH, Kang SS, Lee K, Lim D, Yoon SC, Yun DJ, Inoue Y, Cho MJ, Lee SY (2002) A Chinese cabbage cDNA with high sequence identity to phospholipid hydroperoxide glutathione peroxidases encodes a novel isoform of thioredoxin-dependent peroxidase. J Biol Chem 277:12572–12578

    Article  CAS  PubMed  Google Scholar 

  • Kang S-G, Jeong HK, Suh HS (2004) Characterization of a new member of the glutathione peroxidase gene family in Oryza sativa. Mol Cells 17:23–28

    CAS  PubMed  Google Scholar 

  • Kim YJ, Jang MG, Noh HY, Lee HJ, Sukweenadhi J, Kim JH, Kim SY, Kwon WS, Yang DC (2014) Molecular characterization of two glutathione peroxidase genes of Panax ginseng and their expression analysis against environmental stresses. Gene 535:33–41

    Article  CAS  PubMed  Google Scholar 

  • Li WJ, Feng H, Fan JH, Zhang RQ, Zhao NM, Liu JY (2000) Molecular cloning and expression of a phospholipid hydroperoxide glutathione peroxidase homolog in Oryza sativa. Biochim Biophys Acta 1493:225–230

    Article  CAS  PubMed  Google Scholar 

  • Li G, Peng X, Wei L, Kang G (2013) Salicylic acid increases the contents of glutathione and ascorbate and temporally regulates the related gene expression in salt-stressed wheat seedlings. Gene 529:321–325

    Article  CAS  PubMed  Google Scholar 

  • Lima-Melo Y, Carvalho FE, Martins MO, Passaia G, Sousa RH, Neto MC, Margis-Pinheiro M, Silveira JA (2016) Mitochondrial GPX1 silencing triggers differential photosynthesis impairment in response to salinity in rice plants. J Integr Plant Biol 58:737–748

    Article  CAS  PubMed  Google Scholar 

  • Luis A, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335

    Article  Google Scholar 

  • Margis R, Dunand C, Teixeira FK, Margis-Pinheiro M (2008) Glutathione peroxidase family – an evolutionary overview. FEBS J 275:3959–3970

    Article  CAS  PubMed  Google Scholar 

  • Matamoros MA, Saiz A, Penuelas M, Bustos-Sanmamed P, Mulet JM, Barja MV, Rouhier N, Moore M, James EK, Dietz KJ, Becana M (2015) Function of glutathione peroxidases in legume root nodules. J Exp Bot 66:2979–2990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miao Y, Lv D, Wang P, Wang XC, Chen J, Miao C, Song CP (2006) An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell 18:2749–2766

    Google Scholar 

  • Miao Y, Guo J, Liu E, Li K, Dai J, Wang P, Chen J, Song C (2007) Osmotically stress-regulated the expression of glutathione peroxidase 3 in Arabidopsis. Chin Sci Bull 52:127–130

    Article  CAS  Google Scholar 

  • Milla MAR, Maurer A, Huete AR, Gustafson JP (2003) Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. Plant J 36:602–615

    Article  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot JP, Rouhier N (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol 142:1364–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49:249–279

    Article  CAS  Google Scholar 

  • Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484

    Article  CAS  PubMed  Google Scholar 

  • Passaia G, Fonini LS, Caverzan A, Jardim-Messeder D, Christoff AP, Gaeta ML, de Araujo Mariath JE, Margis R, Margis-Pinheiro M (2013) The mitochondrial glutathione peroxidase GPX3 is essential for H2O2 homeostasis and root and shoot development in rice. Plant Sci 208:93–101

    Article  CAS  PubMed  Google Scholar 

  • Pimentel D, Greiner A (1997) Environmental and socio-economic costs of pesticide use. In: Techniques for reducing pesticide use: economic and environmental benefits. Wiley, New York

    Google Scholar 

  • Ramos J, Matamoros MA, Naya L, James EK, Rouhier N, Sato S, Tabata S, Becana M (2009) The glutathione peroxidase gene family of Lotus japonicus: characterization of genomic clones, expression analyses and immunolocalization in legumes. New Phytol 181:103–114

    Article  CAS  PubMed  Google Scholar 

  • Reig P, Shiao T, Gassert F (2013) Aqueduct water risk framework. Working paper. Washington, DC: World Resources Institute. Available online at http://www.wri.org/publication/aqueduct-water-risk-framework

  • Roeckel-Drevet P, Gagne G, Labrouhe D, Tourvieille D, Dufaure JP, Nicolas P, Drevet J (1998) Molecular characterization, organ distribution and stress-mediated induction of two glutathione peroxidase-encoding mRNAs in sunflower (Helianthus annuus). Physiol Plant 103:385–394

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Sugimoto M, Sakamoto W (1997) Putative phospholipid hydroperoxide glutathione peroxidase gene from Arabidopsis thaliana induced by oxidative stress. Genes Genet Syst 72:311–316

    Article  CAS  PubMed  Google Scholar 

  • Sytykiewicz H (2016) Transcriptional reprogramming of genes related to ascorbate and glutathione biosynthesis, turnover and translocation in aphid-challenged maize seedlings. Biochem Syst Ecol 69:236–251

    Article  CAS  Google Scholar 

  • Tawara T, Fukushima T, Hojo N, Isobe A, Shiwaku K, Setogawa T, Yamane Y (1996) Effects of paraquat on mitochondrial electron transport system and catecholamine contents in rat brain. Arch Toxicol 70:585–589

    Article  CAS  PubMed  Google Scholar 

  • Upham BL, Hatzios KK (1987) Counteraction of paraquat toxicity at the chloroplast level. Z Naturforsch C 42:824–828

    Article  CAS  Google Scholar 

  • Wang X, Fang G, Yang J, Li Y (2017) A thioredoxin-dependent glutathione peroxidase (OsGPX5) is required for rice normal development and salt stress tolerance. Plant Mol Biol Report 35:333–342

    Article  CAS  Google Scholar 

  • Willekens H, Van Camp W, Van Montagu M, Inze D, Langebartels C, Sandermann H Jr (1994) Ozone, sulfur dioxide, and ultraviolet B have similar effects on mRNA accumulation of antioxidant genes in Nicotiana plumbaginifolia L. Plant Physiol 106:1007–1014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322:681–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang XD, Li WJ, Liu JY (2005) Isolation and characterization of a novel PHGPx gene in Raphanus sativus. Biochim Biophys Acta 1728:199–205

    Article  CAS  PubMed  Google Scholar 

  • Yang SL, Yu PL, Chung KR (2015) The glutathione peroxidase-mediated reactive oxygen species resistance, fungicide sensitivity and cell wall construction in the citrus fungal pathogen Alternaria alternata. Environ Microbiol 18:923–935

    Article  Google Scholar 

  • Ye B, Gressel J (2000) Transient, oxidant-induced antioxidant transcript and enzyme levels correlate with greater oxidant-resistance in paraquat-resistant Conyza bonariensis. Planta 211:50–61

    Article  CAS  PubMed  Google Scholar 

  • Zhai CZ, Zhao L, Yin LJ, Chen M, Wang QY, Li LC, Xu ZS, Ma YZ (2013) Two wheat glutathione peroxidase genes whose products are located in chloroplasts improve salt and H2O2 tolerances in Arabidopsis. PLoS One 8:e73989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors are grateful for the support of the Hungarian National Scientific Research Foundation [grant number OTKA K 105956]. Riyazuddin is funded through the Stipendium Hungaricum Scholarship Programme in Hungary. S.A.K.B. thanks the Higher Education Commission (HEC) of Pakistan and the University of Agriculture Peshawar for the scholarship (grant number 360/SIBGE). K.B. received visiting scholarships from the Campus Mundi Programme that is co-financed by the European Union and the Hungarian government.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Krisztina Bela .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Bela, K., Bangash, S.A.K., Riyazuddin, Csiszár, J. (2017). Plant Glutathione Peroxidases: Antioxidant Enzymes in Plant Stress Responses and Tolerance. In: Hossain, M., Mostofa, M., Diaz-Vivancos, P., Burritt, D., Fujita, M., Tran, LS. (eds) Glutathione in Plant Growth, Development, and Stress Tolerance. Springer, Cham. https://doi.org/10.1007/978-3-319-66682-2_5

Download citation

Publish with us

Policies and ethics