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Overexpression of a peroxiredoxin gene from Tamarix hispida, ThPrx1, confers tolerance to oxidative stress in yeast and Arabidopsis

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Abstract

Peroxiredoxins (Prxs) are ubiquitous thiol-specific antioxidant enzymes that are critically involved in cell defense and protect cells from oxidative damage. In this study, a putative Type II Prx (ThPrx1) was identified and characterized from Tamarix hispida. The expression of ThPrx1 is highly induced in response to hydrogen peroxide (H2O2) and methyl viologen (MV) stresses. When expressed ectopically, ThPrx1 showed enhanced tolerance against oxidative stress in yeast and Arabidopsis. In addition, transgenic Arabidopsis plants overexpressing ThPrx1 displayed improved seedling survival rates and increased root growth and fresh weight gain under H2O2 and MV treatments. Moreover, transgenic Arabidopsis plants showed decreased accumulation of H2O2, superoxide (O2•−) and malondialdehyde (MDA), increased superoxide dismutase (SOD) activity compared to wild-type (WT) plants under oxidative stress. Moreover, transgenic plants maintained higher photosynthesis efficiency and lower electrolyte leakage rates than that of WT plants under stress conditions. These results clearly indicated that ThPrx1 plays an important role in cellular redox homeostasis under stress conditions, leading to the maintenance of membrane integrity and increased tolerance to oxidative stress.

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References

  • Baier M, Dietz KJ (1999) Protective function of chloroplast 2-cysteine peroxiredoxin in photosynthesis. Evidence from transgenic Arabidopsis. Plant Physiol 119:1407–1414

    Article  CAS  PubMed  Google Scholar 

  • Barranco-Medina S, Krell T, Finkemeier I, Sevilla F, Lázaro JJ, Dietz KJ (2007) Biochemical and molecular characterization of the mitochondrial peroxiredoxin PsPrxII F from Pisum sativum. Plant Physiol Bioch 45:729–739

    Article  CAS  Google Scholar 

  • Ben-Amor M, Flores B, Latché A, Bouzayen M, Pech JC, Fomojaro F (1999) Inhibition of ethylene biosynthesis by antisense ACC oxidase RNA prevents chilling injury in Charentais cantaloupe melons. Plant Cell Environ 22:1579–1586

    Article  CAS  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • Chen HH, Chu P, Zhou YL, Ding Y, Li Y, Liu J, Jiang LW, Huang SZ (2016) Ectopic expression of NnPER1, a Nelumbo nucifera 1- cysteine peroxiredoxin antioxidant, enhances seed longevity and stress tolerance in Arabidopsis. Plant J 88:608–619

    CAS  PubMed  Google Scholar 

  • Cheng F, Yin LL, Zhou J, Xia XJ, Shi K, Yu JQ, Zhou YH, Foyer CH (2016) Interactions between 2-Cys peroxiredoxins and ascorbate in autophagosome formation during the heat stress response in Solanum lycopersicum. J Exp Bot 67:1919–1933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Duan J, Cai W (2012) OsLEA3-2, an abiotic stress induced gene of rice plays a key role in salt and drought tolerance. PLoS One 7:e45117

    Article  Google Scholar 

  • Finkemeier I, Goodman M, Lamkemeyer P, Kandlbinder A, Sweetlove LJ, Dietz KJ (2005) The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. J Biol Chem 280:12168–12180

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Sign 11:861–905

    Article  CAS  Google Scholar 

  • Gama F, Keech O, Eymery F, Finkemeier I, Gelhaye E, Gardeström P, Dietz KJ, Rey P, Jacquot JP, Rouhie N (2007) The mitochondrial type II peroxiredoxin from poplar. Physiol Plantarum 129:196–206

    Article  CAS  Google Scholar 

  • Gao C, Wang Y, Liu G, Yang C, Jiang J, Li H (2008) Expression profiling of salinity-alkali stress responses by large-scale expressed sequence tag analysis in Tamarix hispida. Plant Mol Biol 66:245–258

    Article  CAS  PubMed  Google Scholar 

  • Horling F, König J, Dietz KJ (2002) Type II peroxiredoxin C, a member of the peroxiredoxin family of Arabidopsis thaliana: its expression and activity in comparison with other peroxiredoxins. Plant Physiol Bioch 40:491–499

    Article  CAS  Google Scholar 

  • Kiba A, Nishihara M, Tsukatani N, Nakatsuka T, Kato Y, Yamamura S (2005) A peroxiredoxin Q homolog from gentians is involved in both resistance against fungal disease and oxidative stress. Plant Cell Physiol 46:1007–1015

    Article  CAS  PubMed  Google Scholar 

  • Kim C, Meskauskiene R, Apel K, Laloi C (2008) No single way to understand singlet oxygen signalling in plants. EMBO Rep 9:435–439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim IS, Kim YS, Yoon HS (2013) Expression of salt-induced 2-Cys peroxiredoxin from Oryza sativa increases stress tolerance and fermentation capacity in genetically engineered yeast Saccharomyces cerevisiae. Appl Microbiol Biot 97:3519–3533

    Article  CAS  Google Scholar 

  • Kim KH, Alam I, Lee KW, Sharmin SA, Kwak SS, Lee SY, Lee BH (2010) Enhanced tolerance of transgenic tall fescue plants overexpressing 2-Cys peroxiredoxin against methyl viologen and heat stresses. Biotechnol Lett 32:571–576

    Article  CAS  PubMed  Google Scholar 

  • Kim MD, Kim YH, Kwon SY, Jang BY, Lee SY, Yun DJ, Cho JH, Kwak SS, Lee HS (2011a) Overexpression of 2-cysteine peroxiredoxin enhances tolerance to methyl viologen-mediated oxidative stress and high temperature in potato plants. Plant Physiol Bioch 49:891–897

    Article  CAS  Google Scholar 

  • Kim SY, Jang HH, Lee JR, Sung NR, Lee HB, Lee DH, Park DJ, Kang CH, Chung WS, Lim CO, Yun DJ, Kim WY, Lee KO, Lee SY (2009) Oligomerization and chaperone activity of a plant 2-Cys peroxiredoxin in response to oxidative stress. Plant Sci 177:227–232

    Article  CAS  Google Scholar 

  • Kim SY, Jung YJ, Shin MR, Park JH, Nawkar GM, Maibam P, Lee ES, Kim KS, Paeng SK, Kim WY, Lee KO, Yun DJ, Kang CH, Lee SY (2012) Molecular and functional properties of three different peroxiredoxin isotypes in Chinese cabbage. Mol Cells 33:27–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim SY, Paeng SK, Nawkar GM, Maibam P, Lee ES, Kim KS, Lee DH, Park DJ, Kang SB, Kim MR, Lee JH, Kim YH, Kim WY, Kang CH (2011b) The 1-Cys peroxiredoxin, a regulator of seed dormancy, functions as a molecular chaperone under oxidative stress conditions. Plant Sci 181:119–124

    Article  CAS  PubMed  Google Scholar 

  • Kong W, Shiota S, Shi Y, Nakayama H, Nakayama K (2000) A novel peroxiredoxin of the plant Sedum lineare is a homologue of Escherichia coli bacterioferritin co-migratory protein (Bcp). Biochem J 351:107–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Moore K, Roberts LJ (1998) Measurement of lipid peroxidation. Free Radical Res 28:659–671

    Article  CAS  Google Scholar 

  • Pulido P, Cazalis R, Cejudo FJ (2009) An antioxidant redox system in the nucleus of wheat seed cells suffering oxidative stress. Plant J 57:132–145

    Article  CAS  PubMed  Google Scholar 

  • Rhee SG (2006) H2O2, a necessary evil for cell signaling. Science 312:1882–1883

    Article  PubMed  Google Scholar 

  • Rouhier N, Jacquot JP (2002) Plant peroxiredoxins: alternative hydroperoxide scavenging enzymes. Photosynth Res 74:259–268

    Article  CAS  PubMed  Google Scholar 

  • Saad RB, Zouari N, Ramdhan WB, Azaza J, Meynard D, Guiderdoni E, Hassairi A (2010) Improved drought and salt stress tolerance in transgenic tobacco overexpressing a novel A20/AN1 zincfinger “AlSAP” gene isolated from the halophyte grass Aeluropus littoralis. Plant Mol Biol 72:171–190

    Article  PubMed  Google Scholar 

  • Sergiev I, Alexieva V, Karanov E (1997) Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Compt Rend Acad Bulg Sci 51:121–124

    Google Scholar 

  • Sun L, Ren H, Liu R, Li B, Wu T, Sun F, Liu H, Wang X, Dong H (2010) An h-type thioredoxin functions in tobacco defense responses to two species of viruses and an abiotic oxidative stress. Mol Plant Microbe In 23:1470–1485

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Roy NV, Paepe AD, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: research0034. 1

    Article  PubMed  PubMed Central  Google Scholar 

  • Vidigal P, Martin-Hernandez AM, Guiu-Aragonés C, Amâncio S, Carvalho L (2015) Selective silencing of 2Cys and type-IIB peroxiredoxins discloses their roles in cell redox state and stress signaling. J Integr Plant Biol 57:591–601

    Article  CAS  PubMed  Google Scholar 

  • Wang FZ, Wang QB, Kwon SY, Kwak SS, Su WA (2005) Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. J Plant Physiol 162:465–472

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Qin L, Liu W, Zhang D, Wang Y (2014) A novel ethyleneresponsive factor from Tamarix hispida, ThERF1, is a GCCbox- and DRE-motif binding protein that negatively modulates abiotic stress tolerance in Arabidopsis. Physiol Plantarum 152:84–97

    Article  CAS  Google Scholar 

  • Wang L, Xu C, Wang C, Wang Y (2012) Characterization of a eukaryotic translation initiation factor 5A homolog from Tamarix androssowii involved in plant abiotic stress tolerance. BMC Plant Biol 12:118

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang YC, Gao CQ, Liang YN, Wang C, Yang CP, Liu GF (2010) A novel bZIP gene from Tamarix hispida mediates physiological responses to salt stress in tobacco plants. J Plant Physiol 167:222–230

    Article  CAS  PubMed  Google Scholar 

  • Xue T, Li X, Zhu W, Wu C, Yang G, Zheng C (2009) Cotton metallothionein GhMT3a, a reactive oxygen species scavenger, increased tolerance against abiotic stress in transgenic tobacco and yeast. J Exp Bot 60:339–349

    Article  CAS  PubMed  Google Scholar 

  • Yuan H, Meng X, Gao Q, Qu W, Xu T, Xu Z, Song R (2011) The characterization of two peroxiredoxin genes in Dunaliella viridis provides insights into antioxidative response to salt stress. Plant Cell Rep 30:1503–1512

    Article  CAS  PubMed  Google Scholar 

  • Zhang CJ, Zhao BC, Ge WN, Zhang YF, Song Y, Sun DY, Guo Y (2011) An apoplastic H-type thioredoxin is involved in the stress response through regulation of the apoplastic reactive oxygen species in rice. Plant Physiol 157:1884–1899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Yucheng Wang or Mengzhu Lu.

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Wang, L., Li, Z., Wang, C. et al. Overexpression of a peroxiredoxin gene from Tamarix hispida, ThPrx1, confers tolerance to oxidative stress in yeast and Arabidopsis. J. Plant Biol. 60, 548–557 (2017). https://doi.org/10.1007/s12374-017-0187-8

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  • DOI: https://doi.org/10.1007/s12374-017-0187-8

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