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Expression of Yeast YAP1 in Transgenic Arabidopsis Results in Increased Salt Tolerance

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Abstract

Soil salinity is a major abiotic stress that lowers agricultural production around the world. Mainly caused by elevated levels of NaCl, it induces a wide range of responses in plants. In addition to ion toxicity, high salt levels can induce oxidative stress with the formation and accumulation of reactive oxygen species (ROS). We introduced the transcription factor YAP1, originally from yeast (Saccharomyces cerevisiae), into Arabidopsis thaliana (ecotype Columbia). When treated with various NaCl concentrations, transgenic plants showed increased activities of antioxidant enzymes catalase, superoxide dismutase, ascorbate peroxidase, peroxidase, glutathione S-transferase, and glutathione reductase compared with the wild-type Arabidopsis. This demonstrated that an active oxygen scavenging system was enhanced to protect plants from salt stress by equilibrating ROS metabolism. Transgenic Arabidopsis maintained higher photosynthesis levels and lower amounts of H2O2, suggesting that ROS production was reduced. Physiological analysis implied that transgenic Arabidopsis might employ multiple mechanisms to improve its salt tolerance.

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References

  1. Alia Saradhi PP, Mohanty P (1997) Involvement of proline in protecting thylakoid membranes against free radical-induced photodamage. J Photochem Photobiol B: Biol 38:253–257

    Article  Google Scholar 

  2. Allakhverdiev SI, Sakamoto A, Nishiyama Y, Murata N (2000) Inactivation of photosystems I and II in response to osmotic stress in Synechococcus. Contribution of water channels. Plant Physiol 122:1201–1208

    Article  PubMed  CAS  Google Scholar 

  3. Baker NR (1991) A possible role for photosystem II in environmental perturbations of photosynthesis. Physiol Plant 81:563–570

    Article  CAS  Google Scholar 

  4. 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 

  5. Bowler C, van Montagu M, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116

    Article  CAS  Google Scholar 

  6. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principal of protein–dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  7. Cheong MS, Yun DJ (2007) Salt-stress signaling. J Plant Biol 51:159–165

    Google Scholar 

  8. Chinnusamy V, Jagendorf A, Zhu JK (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448

    CAS  Google Scholar 

  9. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  11. Davis DG, Swanson HR (2001) Activity of stress-related enzymes in the perennial weed leafy spurge (Euphorbia esula L.). Environ Exp Bot 46:95–108

    Article  CAS  Google Scholar 

  12. Delaunay A, Isnard AD, Toledano MB (2000) H2O2 sensing through oxidation of the YAP1 transcription factor. EMBO J 19:5157–5166

    Article  PubMed  CAS  Google Scholar 

  13. Delaunay A, Pflieger D, Barrault M, Vinh J, Toledano M (2002) A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111:471–481

    Article  PubMed  CAS  Google Scholar 

  14. Dias MA, Costa MM (1983) Effect of low salt concentrations on nitrate reductase and peroxidase of sugar beet leaves. J Exp Bot 34:537–543

    Article  CAS  Google Scholar 

  15. Gasch AP, Spellman PT, Kao CM, Harel OC, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257

    PubMed  CAS  Google Scholar 

  16. Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865

    Article  PubMed  CAS  Google Scholar 

  17. Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 31:149–190

    Article  CAS  Google Scholar 

  18. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  PubMed  CAS  Google Scholar 

  19. 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 

  20. Hernández JA, Ferrer MA, Jiménez A, Barceló AR, Sevilla F (2001) Antioxidant systems and \({{{\text{O}} \cdot _{\text{2}} - {\text{ }}} \mathord{\left/ {\vphantom {{{\text{O}} \cdot _{\text{2}} - {\text{ }}} {{\text{H}}_{\text{2}} {\text{O}}_{\text{2}} }}} \right. \kern-\nulldelimiterspace} {{\text{H}}_{\text{2}} {\text{O}}_{\text{2}} }}\) production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127:817–831

    Article  PubMed  Google Scholar 

  21. Hirata D, Yano K, Miyakawa T (1994) Stress-induced transcriptional activation mediated by YAP1 and YAP2 genes that encode the Jun family of transcriptional activators in Saccharomyces cerevisiae. Mol Gen Genet 242:250–256

    Article  PubMed  CAS  Google Scholar 

  22. Kato M, Shimizu S (1987) Chlorophyll metabolism in higher plants. VII: chlorophyll degradation in senescing tobacco leaves: phenolic-dependent peroxidative degradation. Can J Bot 65:729–735

    Article  CAS  Google Scholar 

  23. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291

    Article  PubMed  CAS  Google Scholar 

  24. Khan MH, Singha KLB, Panda SK (2002) Changes in antioxidant levels in Oryza sativa L. roots subjected to NaCl-salinity stress. Acta Physiol Plant 24:145–148

    Article  CAS  Google Scholar 

  25. 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 

  26. Kuge S, Jones N, Nomoto A (1997) Regulation of YAP-1 nuclear localization in response to oxidative stress. EMBO J 16:1710–1720

    Article  PubMed  CAS  Google Scholar 

  27. Kuge S, Arita M, Murayama A, Maeta K, Izawa S, Inoue Y, Nomoto A (2001) Regulation of the yeast YAP1p nuclear export signal is mediated by redox signal-induced reversible disulfide bond formation. Mol Cell Biol 21:6139–6150

    Article  PubMed  CAS  Google Scholar 

  28. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  31. Mittova V, Guy M, Tal M, Volokita M (2004) Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J Exp Bot 55:1105–1113

    Article  PubMed  CAS  Google Scholar 

  32. Moye-Rowley WS, Harshman KD, Parker CS (1989) Yeast YAP1 encodes a novel form of the jun family of transcriptional activator proteins. Genes Dev 3:283–292

    Article  PubMed  CAS  Google Scholar 

  33. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  34. 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 

  35. Nelson DE et al (2007) Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proc Natl Acad Sci U S A 104:16450–16455

    Article  PubMed  CAS  Google Scholar 

  36. Patterson BD, Macrae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal Biochem 139:487–492

    Article  PubMed  CAS  Google Scholar 

  37. Qiu NW, Lu QT, Lu CM (2003) Photosynthesis, photosystem II efficiency and the xanthophyll cycle in the salt-adapted halophyte Atriplex centralasiatica. New Phytol 159:479–486

    Article  CAS  Google Scholar 

  38. Rao MV, Paliyath G, Ormrod DP (1996) Ultraviolet-B-and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol 110:125–136

    Article  PubMed  CAS  Google Scholar 

  39. Schnell N, Krems B, Entian KD (1992) The PAR1 (YAP1/SNQ3) gene of Saccharomyces cerevisiae, ac-jun homologue, is involved in oxygen metabolism. Curr Genet 21:269–273

    Article  PubMed  CAS  Google Scholar 

  40. Stephen DW, Rivers SL, Jamieson DJ (1995) The role of the YAP1 and YAP2 genes in the regulation of the adaptive oxidative stress responses of Saccharomyces cerevisiae. Mol Microbiol 16:415–423

    Article  PubMed  CAS  Google Scholar 

  41. Sugiyama K, Izawa S, Inoue Y (2000) The Yap1p-dependent induction of glutathione synthesis in heat shock response of Saccharomyces cerevisiae. J Biol Chem 275:15535–15540

    Article  PubMed  CAS  Google Scholar 

  42. Wu AL, Moye-Rowley WS (1994) GSH1, which encodes gamma-glutamylcysteine synthetase, is a target gene for yAP-1 transcriptional regulation. Mol Cell Biol 14:5832–5839

    PubMed  CAS  Google Scholar 

  43. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This work was supported by the National Key Fundamental Research Program of China (No. 2006CB100104) and the Natural Science Foundation of Shandong Province, China (Grant No. Y2006D30).

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Authors and Affiliations

  1. Key Laboratory of Plant Stress Research, College of Life Science, Shandong Normal University, Jinan, 250014, Shandong Province, People’s Republic of China

    Jiqiang Zhao, Hui Zhang & Yanxiu Zhao

  2. Chemistry and Biology College, Yantai University, Yantai, 264005, Shandong Province, People’s Republic of China

    Jiqiang Zhao, Shanli Guo & Shihua Chen

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  1. Jiqiang Zhao
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Correspondence to Yanxiu Zhao.

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Zhao, J., Guo, S., Chen, S. et al. Expression of Yeast YAP1 in Transgenic Arabidopsis Results in Increased Salt Tolerance. J. Plant Biol. 52, 56–64 (2009). https://doi.org/10.1007/s12374-008-9004-8

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  • DOI: https://doi.org/10.1007/s12374-008-9004-8

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