Skip to main content

Advertisement

SpringerLink
Log in

The characterization of two peroxiredoxin genes in Dunaliella viridis provides insights into antioxidative response to salt stress

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Peroxiredoxins (Prxs), a group of antioxidant enzymes, are an important component of the oxidative defense system and have been demonstrated to function as peroxidases, sensors of H2O2-mediated signaling and/or chaperones. In this study, a cDNA library was constructed from a halotolerant alga, Dunaliella viridis, and was used in a functional complementation screen for antioxidative genes in an oxidative sensitive yeast mutant. Two Prx genes, DvPrx1 and DvPrx2, were obtained from this screen. These two genes were classified as type II Prx and 2-Cys Prx based on amino acid sequence and phylogenetic analysis. When over-expressed in yeast cells, both Prx genes were able to confer better oxidative tolerance and decrease the level of reactive oxygen species (ROS). Subcellular localization experiments in tobacco cells revealed that both DvPrx1 and DvPrx2 were localized in the cytosol. The transcription of DvPrx1 and DvPrx2 can be induced by hypersalinity shock, but is not obviously affected by treatment with high levels of oxidant. Our results shed light on the function and regulation of Prx genes from Dunaliella and their potential roles in salt tolerance.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Belles-Boix E, Babiychuk E, Van Montagu M, Inze D, Kushnir S (2000) CEO1, a new protein from Arabidopsis thaliana, protects yeast against oxidative damage. FEBS Lett 482:19–24

    Article  PubMed  CAS  Google Scholar 

  • Biteau B, Labarre J, Toledano MB (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425:980–984

    Article  PubMed  CAS  Google Scholar 

  • Borowitzka LJ, Brown AD (1974) The salt relations of marine and halophilic species of the unicellular green alga, Dunaliella. The role of glycerol as a compatible solute. Arch Microbiol 96:37–52

    Article  CAS  Google Scholar 

  • Bryk R, Griffin P, Nathan C (2000) Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407:211–215

    Article  PubMed  CAS  Google Scholar 

  • Budanov AV, Sablina AA, Feinstein E, Koonin EV, Chumakov PM (2004) Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science 304:596–600

    Article  PubMed  CAS  Google Scholar 

  • Chang TS, Jeong W, Choi SY, Yu S, Kang SW, Rhee SG (2002) Regulation of peroxiredoxin I activity by Cdc2-mediated phosphorylation. J Biol Chem 277:25370–25376

    Article  PubMed  CAS  Google Scholar 

  • Chattopadhyay MK, Tabor CW, Tabor H (2006) Polyamine deficiency leads to accumulation of reactive oxygen species in a spe2Delta mutant of Saccharomyces cerevisiae. Yeast 23:751–761

    Article  PubMed  CAS  Google Scholar 

  • Contreras-Porcia L, Dennett G, Gonzalez A, Vergara E, Medina C, Correa JA, Moenne A (2010) Identification of copper-induced genes in the marine alga Ulva compressa (Chlorophyta). Mar Biotechnol (NY). doi:10.1007/s10126-010-9325-8

  • Dietz KJ (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54:93–107

    Article  PubMed  CAS  Google Scholar 

  • Gomez JM, Hernandez JA, Jimenez A, del Rio LA, Sevilla F (1999) Differential response of antioxidative enzymes of chloroplasts and mitochondria to long-term NaCl stress of pea plants. Free Radic Res 31(Suppl):S11–S18

    Article  PubMed  CAS  Google Scholar 

  • Gorlich D, Mattaj IW (1996) Nucleocytoplasmic transport. Science 271:1513–1518

    Article  PubMed  CAS  Google Scholar 

  • Goyer A, Haslekas C, Miginiac-Maslow M, Klein U, Le Marechal P, Jacquot JP, Decottignies P (2002) Isolation and characterization of a thioredoxin-dependent peroxidase from Chlamydomonas reinhardtii. Eur J Biochem 269:272–282

    Article  PubMed  CAS  Google Scholar 

  • Guan Z, Meng X, Sun Z, Xu Z, Song R (2008) Characterization of duplicated Dunaliella viridis SPT1 genes provides insights into early gene divergence after duplication. Gene 423:36–42

    Article  PubMed  CAS  Google Scholar 

  • Hall A, Karplus PA, Poole LB (2009) Typical 2-Cys peroxiredoxins—structures, mechanisms and functions. FEBS J 276:2469–2477

    Article  PubMed  CAS  Google Scholar 

  • He Y, Meng X, Fan Q, Sun X, Xu Z, Song R (2009) Cloning and characterization of two novel chloroplastic glycerol-3-phosphate dehydrogenases from Dunaliella viridis. Plant Mol Biol 71:193–205

    Article  PubMed  CAS  Google Scholar 

  • Horling F, Lamkemeyer P, Konig J, Finkemeier I, Kandlbinder A, Baier M, Dietz KJ (2003) Divergent light-, ascorbate-, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiol 131:317–325

    Article  PubMed  CAS  Google Scholar 

  • Ito H, Fukuda Y, Murata K, Kimura A (1983) Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153:163–168

    PubMed  CAS  Google Scholar 

  • Jahnke LS, White AL (2003) Long-term hyposaline and hypersaline stresses produce distinct antioxidant responses in the marine alga Dunaliella tertiolecta. J Plant Physiol 160:1193–1202

    Article  PubMed  CAS  Google Scholar 

  • Jeong W, Park SJ, Chang TS, Lee DY, Rhee SG (2006) Molecular mechanism of the reduction of cysteine sulfinic acid of peroxiredoxin to cysteine by mammalian sulfiredoxin. J Biol Chem 281:14400–14407

    Article  PubMed  CAS  Google Scholar 

  • Kim SY, Jang HH, Lee JR, Sung NR, Lee HB, Lee DH, Park D-J, Kang CH, Chung WS, Lim CO, Yun D-J, 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 

  • Kozak M (1986) Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44:283–292

    Article  PubMed  CAS  Google Scholar 

  • Kuge S, Jones N (1994) YAP1 dependent activation of TRX2 is essential for the response of Saccharomyces cerevisiae to oxidative stress by hydroperoxides. EMBO J 13:655–664

    PubMed  CAS  Google Scholar 

  • Lemaire SD, Guillon B, Le Marechal P, Keryer E, Miginiac-Maslow M, Decottignies P (2004) New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 101:7475–7480

    Article  PubMed  CAS  Google Scholar 

  • Li Q, Gao X, Sun Y, Zhang Q, Song R, Xu Z (2006) Isolation and characterization of a sodium-dependent phosphate transporter gene in Dunaliella viridis. Biochem Biophys Res Commun 340:95–104

    Article  PubMed  CAS  Google Scholar 

  • Meng X, Xu Z, Song R (2010) Molecular cloning and characterization of a vacuolar H(+)-pyrophosphatase from Dunaliella viridis. Mol Biol Rep. doi:10.1007/s11033-010-0445-z

  • Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–250

    Article  PubMed  CAS  Google Scholar 

  • Nogoceke E, Gommel DU, Kiess M, Kalisz HM, Flohe L (1997) A unique cascade of oxidoreductases catalyses trypanothione-mediated peroxide metabolism in Crithidia fasciculata. Biol Chem 378:827–836

    Article  PubMed  CAS  Google Scholar 

  • Shalata A, Mittova V, Volokita M, Guy M, Tal M (2001) Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: the root antioxidative system. Physiol Plant 112:487–494

    Article  PubMed  CAS  Google Scholar 

  • Stork T, Michel KP, Pistorius EK, Dietz KJ (2005) Bioinformatic analysis of the genomes of the cyanobacteria Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942 for the presence of peroxiredoxins and their transcript regulation under stress. J Exp Bot 56:3193–3206

    Article  PubMed  CAS  Google Scholar 

  • Sun Y, Yang Z, Gao X, Li Q, Zhang Q, Xu Z (2005) Expression of foreign genes in Dunaliella by electroporation. Mol Biotechnol 30:185–192

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Veal EA, Findlay VJ, Day AM, Bozonet SM, Evans JM, Quinn J, Morgan BA (2004) A 2-Cys peroxiredoxin regulates peroxide-induced oxidation and activation of a stress-activated MAP kinase. Mol Cell 15:129–139

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Shrager J, Jain M, Chang CW, Vallon O, Grossman AR (2004) Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot Cell 3:1331–1348

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. Anu Saloheimo for providing the pAJ401 plasmid, Dr. Michel B. Toledano for the ∆yap1 and Y252 strains, Dr. Yan Zhang for the pB7FWG2 plasmid, Dr. Xiaoyong Deng for confocal microscopy support and Yihan Chen for technical assistance. This work was supported by the National Natural Sciences Foundation of China (30871278, 30970242), the Ministry of Agriculture of China (2008ZX08003-001, 2008ZX08003-005), Shanghai Municipal Science and Technology Commission (09DZ2271800).

Author information

Authors and Affiliations

  1. Shanghai Key Laboratory of Bio-Energy Crops, School of Life Sciences, Shanghai University, 99 Shangda Road, 200444, Shanghai, People’s Republic of China

    Huijuan Yuan, Xiangzong Meng, Qiang Gao, Wufei Qu, Tengjiao Xu, Zhengkai Xu & Rentao Song

Authors
  1. Huijuan Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiangzong Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qiang Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wufei Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tengjiao Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhengkai Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rentao Song
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rentao Song.

Additional information

Communicated by P. Kumar.

Electronic supplementary material

Below is the link to the electronic supplementary material.

299_2011_1060_MOESM1_ESM.tif

Online Recourse 1 The full-length cDNA sequence and the deduced amino acid sequence of DvPrx1 (A) and DvPrx2 (B).The start codon (ATG) and the stop codon (TAA) are showed in bold; mark * also represents TAA in the translated line; the in-frame stop codon upstream DvPrx1 is shaded in grey (TIFF 908 kb)

299_2011_1060_MOESM2_ESM.tif

Online Recourse 2 The phylogenetic tree of peroxiredoxins from different species.CLUSTAL X was used to generate the tree for general classification of DvPrx1 and DvPrx2 (A) or detailed comparison of DvPrx2 (B) with their orthologs. See Online Recourse 3 for species abbreviations and protein accession numbers (TIFF 385 kb)

Online Recourse 3Species abbreviations and Genbank accession numbers of the peptide sequence (TIFF 179 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yuan, H., Meng, X., Gao, Q. et al. The characterization of two peroxiredoxin genes in Dunaliella viridis provides insights into antioxidative response to salt stress. Plant Cell Rep 30, 1503–1512 (2011). https://doi.org/10.1007/s00299-011-1060-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-011-1060-8

Keywords

Search

Navigation