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Molecular Biotechnology

, 41:115 | Cite as

Allene Oxide Cyclase from Camptotheca acuminata Improves Tolerance Against Low Temperature and Salt Stress in Tobacco and Bacteria

  • Yan Pi
  • Keji Jiang
  • Ying Cao
  • Qian Wang
  • Zhuoshi Huang
  • Le Li
  • Lingchuan Hu
  • Wei Li
  • Xiaofen Sun
  • Kexuan Tang
Research

Abstract

Allene oxide cyclase (AOC, E 5.3.99.6) is an essential enzyme in jasmonate (JA) biosynthetic pathway. An AOC gene (defined as CaAOC, Database Accession No. AY863428) had been isolated from Camptotheca acuminata in previous work. Real-time quantitative PCR analysis indicated that mRNA expression of CaAOC was induced by salt stress (120 mM NaCl) and low temperature (4°C). In order to further investigate the role of AOC gene in the processes, CaAOC was introduced into tobacco via Agrobacterium tumefaciens, and the transgenic lines were subjected to the examination of tolerance against salt stress and low temperature. Under salt stress, the chlorophyll content in transgenic tobacco was higher than that of in the wild plants. The electrolyte leakage test revealed that transgenic tobacco plants were more resistant to low temperature over control. Furthermore, 5′-truncated CaAOC was inserted into pET30 and then expressed in Escherichia coli strain BL21DE3 (pLysS). Interestingly, the transformants could grow on 2YT agar containing 400 mM NaCl. Although these mechanisms are not clear yet, this study suggested that CaAOC could not only be a potential target gene in the engineering of plants and bacteria for improved endurance against salt stress, but also be quite useful in enhancing plant tolerance to cold.

Keywords

Allene oxide cyclase Camptotheca acuminata Escherichia coli Low temperature Nicotiana tabacum Salt stress 

Abbreviations

AOC

Allene oxide cyclase

JA

Jasmonate

OPDA

12-Oxo-phytodienoic acid

RT-QPCR

Real-time quantitative PCR

Notes

Acknowledgment

This work was funded by National Basic Research Program of China (973 Program, 2007CB108805), China National ‘863’ High-Tech Program, China Ministry of Education, and Shanghai Science and Technology Committee.

References

  1. 1.
    Creelman, R. A., & Mullet, J. E. (1997). Biosynthesis and action of jasmonates in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 48, 355–381. doi: 10.1146/annurev.arplant.48.1.355.CrossRefGoogle Scholar
  2. 2.
    Parchmann, S., Gundlach, H., & Mueller, M. J. (1997). Induction of 12-oxo-phytodienoic acid in wounded plants and elicited plant cell cultures. Plant Physiology, 115, 1057–1064. doi: 10.1104/pp.115.3.1057.CrossRefGoogle Scholar
  3. 3.
    Farmer, E. E., & Ryan, C. A. (1990). Interplant communication—airborne methyl jasmonate induces synthesis of proteinase-inhibitors in plant-leaves. Proceedings of the National Academy of Sciences of the United States of America, 87, 7713–7716. doi: 10.1073/pnas.87.19.7713.CrossRefGoogle Scholar
  4. 4.
    Thomma, B., Eggermont, K., Penninckx, I., et al. (1998). Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proceedings of the National Academy of Sciences of the United States of America, 95, 15107–15111. doi: 10.1073/pnas.95.25.15107.CrossRefGoogle Scholar
  5. 5.
    Bohlmann, H., Vignutelli, A., Hilpert, B., et al. (1998). Wounding and chemicals induce expression of the Arabidopsis thaliana gene Thi2.1, encoding a fungal defense thionin, via the octadecanoid pathway. FEBS Letters, 437, 281–286. doi: 10.1016/S0014-5793(98)01251-4.CrossRefGoogle Scholar
  6. 6.
    Hamberg, M., & Gardner, H. W. (1992). Oxylipin pathway to jasmonates—biochemistry and biological significance. Biochimica et Biophysica Acta, 1165, 1–18.Google Scholar
  7. 7.
    Stenzel, I., Hause, B., Miersch, O., et al. (2003). Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thaliana. Plant Molecular Biology, 51, 895–911. doi: 10.1023/A:1023049319723.CrossRefGoogle Scholar
  8. 8.
    Anderson, J. P., Thatcher, L. F., & Singh, K. B. (2005). Plant defence responses: Conservation between models and crops. Functional Plant Biology, 32, 21–34. doi: 10.1071/FP04136.CrossRefGoogle Scholar
  9. 9.
    Stenzel, I., Hause, B., Maucher, H., et al. (2003). Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato—amplification in wound signalling. The Plant Journal, 33, 577–589. doi: 10.1046/j.1365-313X.2003.01647.x.CrossRefGoogle Scholar
  10. 10.
    Ryan, C. A. (2000). The systemin signaling pathway: Differential activation of plant defensive genes. Biochimica et Biophysica Acta, 1477, 112–121. doi: 10.1016/S0167-4838(99)00269-1.Google Scholar
  11. 11.
    Doares, S. H., Narvaezvasquez, J., Conconi, A., & Ryan, C. A. (1995). Salicylic-acid inhibits synthesis of proteinase-inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiology, 108, 1741–1746.Google Scholar
  12. 12.
    Guillermina, A., Otto, M., Robert, K., et al. (2003). Jasmonate and octadecanoid occurrence in tomato hairy roots. Endogenous level changes in response to NaCl. Plant Growth Regulation, 40, 21–27. doi: 10.1023/A:1023016412454.CrossRefGoogle Scholar
  13. 13.
    Kramell, R., Miersch, O., Atzorn, R., Parthier, B., & Wasternack, C. (2000). Octadecanoid-derived alteration of gene expression and the “Oxylipin signature” in stressed barley leaves. Implications for different signaling pathways. Plant Physiology, 123, 177–187. doi: 10.1104/pp.123.1.177.CrossRefGoogle Scholar
  14. 14.
    Penninckx, I., Thomma, B., Buchala, A., Metraux, J. P., & Broekaert, W. F. (1998). Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. The Plant Cell, 10, 2103–2113.CrossRefGoogle Scholar
  15. 15.
    Wang, H., Huang, Z. J., Chen, Q., et al. (2004). Ectopic overexpression of tomato JERF3 in tobacco activates downstream gene expression and enhances salt tolerance. Plant Molecular Biology, 55, 183–192. doi: 10.1007/s11103-004-0113-6.CrossRefGoogle Scholar
  16. 16.
    Li, S. Y., Yi, Y. J., Wang, Y. J., Zhang, Z. Z., & Beasley, R. S. (2002). Camptothecin accumulation and variations in Camptotheca. Planta Medica, 68, 1010–1016. doi: 10.1055/s-2002-35652.CrossRefGoogle Scholar
  17. 17.
    Lorence, A., & Nessler, C. L. (2004). Molecules of interest—camptothecin, over four decades of surprising findings. Phytochemistry, 65, 2735–2749. doi: 10.1016/j.phytochem.2004.09.001.CrossRefGoogle Scholar
  18. 18.
    Pi, Y., Liao, Z. H., Jiang, K. J., et al. Molecular cloning, characterization and expression of a jasmonate biosynthetic pathway gene encoding allene oxide cyclase from Camptotheca acuminata. Bioscience Reports (in press).Google Scholar
  19. 19.
    Maucher, H., Stenzel, I., Miersch, O., et al. (2004). The allene oxide cyclase of barley (Hordeum vulgare L.)—cloning and organ-specific expression. Phytochemistry, 65, 801–811. doi: 10.1016/j.phytochem.2004.01.009.CrossRefGoogle Scholar
  20. 20.
    Muller, P. Y., Janovjak, H., Miserez, A. R., & Dobbie, Z. (2002). Processing of gene expression data generated by quantitative real-time RT-PCR. BioTechniques, 32, 1372–1379.Google Scholar
  21. 21.
    Murashige, T., & Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum, 15, 473–497. doi: 10.1111/j.1399-3054.1962.tb08052.x.CrossRefGoogle Scholar
  22. 22.
    Wang, J., Zuo, K. J., Wu, W. S., et al. (2004). Expression of a novel antiporter gene from Brassica napus resulted in enhanced salt tolerance in transgenic tobacco plants. Biologia Plantarum, 48, 509–515. doi: 10.1023/B:BIOP.0000047145.18014.a3.CrossRefGoogle Scholar
  23. 23.
    Doyle, J. J., & Doyle, J. L. (1990). Isolation of plant DNA from fresh tissue. Focus, 12, 13–15.Google Scholar
  24. 24.
    Pi, Y., Liao, Z. H., Chai, Y. R., et al. (2006). Molecular cloning and characterization of a novel stem-specific gene from Camptotheca acuminata. Journal of Biochemistry and Molecular Biology, 39, 68–75.Google Scholar
  25. 25.
    Zeng, Y., & Yang, T. (2002). RNA isolation from highly viscous samples rich in polyphenols and polysaccharides. Plant Molecular Biology Reporter, 20, 417a–417e. doi: 10.1007/BF02772130.CrossRefGoogle Scholar
  26. 26.
    Wallis, J. G., Wang, H. Y., & Guerra, D. J. (1997). Expression of a synthetic antifreeze protein in potato reduces electrolyte release at freezing temperatures. Plant Molecular Biology, 35, 323–330. doi: 10.1023/A:1005886210159.CrossRefGoogle Scholar
  27. 27.
    Nunes, M. E. S., & Smith, G. R. (2003). Electrolyte leakage assay capable of quantifying freezing resistance in rose clover. Crop Science, 43, 1349–1357.Google Scholar
  28. 28.
    Shi, H. Z., Lee, B. H., Wu, S. J., & Zhu, J. K. (2003). Overexpression of a plasma membrane Na +/H + antiporter gene improves salt tolerance in Arabidopsis thaliana. Nature Biotechnology, 21, 81–85. doi: 10.1038/nbt766.CrossRefGoogle Scholar
  29. 29.
    Xiong, L. M., Schumaker, K. S., & Zhu, J. K. (2002). Cell signaling during cold, drought, and salt stress. The Plant Cell, 14, S165–S183. doi: 10.1105/tpc.010278.CrossRefGoogle Scholar
  30. 30.
    Reymond, P., & Farmer, E. E. (1998). Jasmonate and salicylate as global signals for defense gene expression. Current Opinion in Plant Biology, 1, 404–411. doi: 10.1016/S1369-5266(98)80264-1.CrossRefGoogle Scholar
  31. 31.
    Thatcher, L. F., Anderson, J. P., & Singh, K. B. (2005). Plant defence responses: What have we learnt from Arabidopsis? Functional Plant Biology, 32, 1–19. doi: 10.1071/FP04135.CrossRefGoogle Scholar
  32. 32.
    Andradea, A., Viglioccoa, A., Alemanoa, S., et al. (2005). Endogenous jasmonates and octadecanoids in hypersensitive tomato mutants during germination and seedling development in response to abiotic stress. Seed Science Research, 15, 309–318. doi: 10.1079/SSR2005219.CrossRefGoogle Scholar
  33. 33.
    Cheong, J.-J., & Choi, Y. D. (2003). Methyl jasmonate as a vital substance in plants. Trends in Genetics, 19, 409–413. doi: 10.1016/S0168-9525(03)00138-0.CrossRefGoogle Scholar
  34. 34.
    Kreps, J. A., Wu, Y., Chang, H.-S., et al. (2002). Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiology, 130, 2129–2141. doi: 10.1104/pp.008532.CrossRefGoogle Scholar
  35. 35.
    Yoshikawa, H., Honda, C., & Kondo, S. (2007). Effect of low-temperature stress on abscisic acid, jasmonates, and polyamines in apples. Plant Growth Regulation, 52, 199–206. doi: 10.1007/s10725-007-9190-2.CrossRefGoogle Scholar
  36. 36.
    Yamada, A., Saitoh, T., Mimura, T., & Ozeki, Y. (2002). Expression of mangrove allene oxide cyclase enhances salt tolerance in Escherichia coli, yeast, and tobacco cells. Plant and Cell Physiology, 43, 903–910. doi: 10.1093/pcp/pcf108.CrossRefGoogle Scholar
  37. 37.
    Emanuelsson, O., Nielsen, H., & Von Heijne, G. (1999). ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Science, 8, 978–984.CrossRefGoogle Scholar
  38. 38.
    Ziegler, J., Stenzel, I., Hause, B., et al. (2000). Molecular cloning of allene oxide cyclase—the enzyme establishing the stereochemistry of octadecanoids and jasmonates. The Journal of Biological Chemistry, 275, 19132–19138. doi: 10.1074/jbc.M002133200.CrossRefGoogle Scholar

Copyright information

© Humana Press 2008

Authors and Affiliations

  • Yan Pi
    • 1
  • Keji Jiang
    • 1
  • Ying Cao
    • 1
  • Qian Wang
    • 1
  • Zhuoshi Huang
    • 1
  • Le Li
    • 1
  • Lingchuan Hu
    • 1
  • Wei Li
    • 1
  • Xiaofen Sun
    • 1
  • Kexuan Tang
    • 1
    • 2
  1. 1.State Key Laboratory of Genetic Engineering, School of Life Sciences, Morgan-Tan International Center for Life Sciences, Fudan-SJTU-Nottingham Plant Biotechnology R&D CenterFudan UniversityShanghaiPeople’s Republic of China
  2. 2.Plant Biotechnology Research Center, School of Agriculture and Biology, Fudan-SJTU-Nottingham Plant Biotechnology R&D Center, Institute of Systems BiologyShanghai Jiao Tong UniversityShanghaiPeople’s Republic of China

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