Photosynthetica 2005, 43(4):501-508 | DOI: 10.1007/s11099-005-0082-2

Photoprotective effects of high level expression of C4 phosphoenolpyruvate carboxylase in transgenic rice during photoinhibition

D. M. Jiao1, X. Li1, B. H. Ji2
1 Institute of Agrobiological Genetics and Physiology, Jiangsu Academy of Agricultural Sciences, Nanjing, China
2 Life Sciences College, Nantong University, Nantong, China

With untransformed rice cv. Kitaake as control, the characteristics of carbon assimilation and photoprotection of a transgenic rice line over-expressing maize phosphoenolpyruvate carboxylase (PEPC) were investigated. The PEPC activity in untransformed rice was low, but the activity was stimulated under high irradiance or photoinhibitory condition. PEPC in untransformed rice contributed by about 5-10 % to photosynthesis, as shown by the application of the specific inhibitor 3,3-dichloro-2-(dihydroxyphosphinoylmethyl)propenoate (DCDP). When maize PEPC gene was introduced into rice, transgenic rice expressed high amount of maize PEPC protein and had high PEPC activity. Simultaneously, the activity of carbonic anhydrase (CA) transporting CO2 increased significantly. Thus the photosynthetic capacity increased greatly (50 %) under high CO2 supply. In CO2-free air, CO2 release in the leaf was less. In addition, PEPC transgenic rice was more tolerant to photoinhibition. Treating by NaF, an inhibitor of phosphatase, showed that in transgenic rice more phosphorylated light-harvesting chlorophyll a/b-binding complexes (LHC) moved to photosystem 1 (PS1) protecting thus PS2 from photo-damage. Simultaneously, the introduction of maize PEPC gene could activate or induce activities of the key enzymes scavenging active oxygen, such as superoxide dismutase (SOD) and peroxidase (POD). Hence higher PS2 photochemical efficiency and lower superoxygen anion (O2.-) generation and malonyldiadehyde (MDA) content under photoinhibition could improve protection from photo-oxidation.

Additional key words: carbon assimilation; carbonic anhydrase; chlorophyll fluorescence; 3; 3-dichloro-2-(dihydroxyphosphinoylmethyl)propenoate; enzymes scavenging active oxygen; malonyldialdehyde; Oryza; peroxidase; superoxide dismutase

Received: November 16, 2004; Accepted: January 27, 2005; Published: December 1, 2005  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Jiao, D.M., Li, X., & Ji, B.H. (2005). Photoprotective effects of high level expression of C4 phosphoenolpyruvate carboxylase in transgenic rice during photoinhibition. Photosynthetica, 43(4), 501-508. doi: 10.1007/s11099-005-0082-2
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Aoyagi, K., Bassham, J.A.: Appearance and accumulation of C4 carbon pathway enzymes in developing wheat leaves. - Plant Physiol. 80: 334-340, 1986. Go to original source...
    2. Aoyagi, K., Bassham, J.A.: Synthesis and uptake of cytoplasmically synthetized pyruvate, Pi dikinase polypeptide by chloroplasts. - Plant Physiol. 78: 807-811, 1985. Go to original source...
    3. Chen, G.-X., Liu, S.-H., Zhang, C.-J., Lu, C.-G.: Effects of drought on photosynthetic characteristics of flag leaves of a newly-developed super-high-yield rice hybrid. - Photosynthetica 42: 573-578, 2004. Go to original source...
    4. Chollet, R., Vidal, J., O'Leary, M.H.: Phosphoenolpyruvate carboxylase: A ubiquitous highly regulated enzyme in plants. - Annu. Rev. Plant Physiol. Plant mol. Biol. 47: 273-298, 1996. Go to original source...
    5. Deroche, M.E., Carrayol, E.: Nodule phosphoenolpyruvate carboxylase: a review. - Physiol. Plant. 74: 775-782, 1988. Go to original source...
    6. Dong, L.Y., Ling, J., Wang, C.M.: Ti plasmid-mediated transformation of tabacco with C4-PEPCase cDNA from Zea mays. - Acta phytophysiol. sin. 213: 281-288, 1995.
    7. El Bissati, K., Delphin, E., Murata, N.: Photosystem II fluorescence quenching in the cyanobacterium Synechocystis PCC6803: involvement of two different mechanisms. - Biochim. biophys. Acta 1457: 229-242, 2000. Go to original source...
    8. Fukayama, H., Hatch, M.D., Tamai, T., Tsuchida, H., Sudoh, S., Furbank, R.T., Miyao, M.: Activity regulation and physiological impacts of maize C4-specific phosphoenolpyruvate carboxylase overproduced in transgenic rice plants. - Photosynth. Res. 77: 227-239, 2003. Go to original source...
    9. Fushimi, T., Umeda, M., Shimazaki, T., Kato, A., Toriyama, K., Uchimiya, H.: Nucleotide sequence of a rice cDNA similar to a maize NADP-dependent malic enzyme. - Plant mol. Biol. 24: 965-967, 1994. Go to original source...
    10. Gehlen, J., Paanstruga, R., Smets, H., Merkelbach, S., Kleines, M., Porsch, P., Fladung, M., Beck, I., Rademacher, T., Hausler, R.E., Heinz, J.: Effects of altered phosphoenolyruate carboxylase activities on transgenic C3 plant Solanum tuberosum. - Plant mol. Biol. 32: 831-848, 1996. Go to original source...
    11. Genty, B., Briantais, J.-M., Baker, N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. - Biochim. biophys. Acta 900: 87-92, 1989. Go to original source...
    12. Giannopolitis, C.N., Ries. S.K.: Superoxide dismutase. - Plant Physiol. 59: 309-314, 1977. Go to original source...
    13. Gonzalez, D.H., Iglesias, A.A., Andeo, C.S.: On the regulation of phosphoenolpyruvate carboxylase activity from maize leaves by L-malate. Effect of pH. - J. Plant Physiol. 116: 425-434, 1984. Go to original source...
    14. Guo, M.L., Gao, Y.Z., Wang, Z.: [Determination of plant carbonic anhydrase activity with pH-meter.] - Plant Physiol. Commun. 6: 59-61, 1988. [In Chin.]
    15. Gupta, A.S., Webb, R.P., Holaday, A.S., Allen, R.D.: Overexpression of superoxide dismutase protects plants from oxidative stress. Induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants. - Plant Physiol. 102: 1067-1073, 1993. Go to original source...
    16. Heath, R.L., Packer, L.: Photooxidation in isolated chloroplasts. 1. Kinetics and stoichiometry of fatty acid peroxidation. - Arch. Biochem. Biophys. 125: 189-198, 1968. Go to original source...
    17. Imaizumi, N., Ku, M.S.B., Ishihara, K., Samejima, M., Kaneko, S., Matsuoka, M.: Characterization of gene from pyruvate, orthophosphate dikinase from rice, a C3 plant, and a comparison of structure and expression between C3 and C4 genes for this protein. - Plant mol. Biol. 34: 701-716, 1997. Go to original source...
    18. Jenkins, C.L.D.: Effects of the phosphoenolpyruvate carboxylase inhibitor 3,3-dichloro-2-(dihydroxyphosphinoylmethyl)propenoate on photosynthesis. - Plant Physiol. 89: 1231-1237, 1989. Go to original source...
    19. Jiao, D., Huang, X., Li, X., Chi, W., Kuang, T., Zhang, Q., Ku, M.S.B., Cho, D.: Photosynthetic characteristics and tolerance to photo-oxidation of transgenic rice expressing C4 photosynthesis enzymes. - Photosynth. Res. 72: 85-93, 2002. Go to original source...
    20. Jiao, D.M., Ji, B.H.: [Changes of the photosynthetic electron transport and photosynthetic enzyme activities of two rice varieties under photooxidation condition.] - Acta agron. sin. 22: 43-49, 1996. [In Chin.]
    21. Jiao, D.M., Kuang, T.Y., Li, X., Ge, Q.Y., Huang, X.Q., Hao, N.B., Bai, K.Z.: Physiological characteristics of the primitive CO2 concentrating mechanism in PEPC transgenic rice. - Sci. China C 46: 438-446, 2003. Go to original source...
    22. Jiao, D.M., Li, X., Huang, X.Q., Chi, W., Kuang, T.Y., Ku, S.B.M.: The characteristics of CO2 assimilation of photosynthesis and chlorophyll fluorescence in transgenic PEPC rice. - Chin. Sci. Bull. 46: 414-418, 2001. Go to original source...
    23. Kochba, J., Lave, E.S., Spiegel-Roy, P.: Difference in peroxidase activity and isozymes in embryogenic and non-embryogenic 'shamouti' organ ovular callus lines. - Plant Cell Physiol. 18: 463-467, 1992. Go to original source...
    24. Ku, M.S.B., Cho, D., Ranade, U., Hsu, T.P., Li, X., Jiao, D.M., Ehleringer, J.M., Miyao, M., Matsuoka, M.: Photosynthetic performance of transgenic rice plants overexpressing maize C4 photosynthesis enzyme. - In: Sheehy, J.E., Mitchell, P.L., Hardy, B.: Redisigning Rice Photosynthesis to Increase Yield. Pp. 193-204. Elsevier Science/IRRI, Amsterdam - Oxford 2000. Go to original source...
    25. Ku, S.B.M., Sakae, A., Mika, N., Hiroshi, F., Hiroko, T., Kazuko, O., Sakiko, H., Seichi, T., Mitsue, M., Makoto, M.: High-level expression of maize phosphoenolyruvate carboxylase in transgenic rice plants. - Nat. Biotechnol. 17: 76-80, 1999. Go to original source...
    26. Lepiniec, L., Vidal, J., Chollet, R., Gadal, P., Cretin, C.: Phosphoenolpyruvate carboxylase: Structure, regulation and evolution. - Plant Sci. 99: 111-124, 1994. Go to original source...
    27. Li, W.H., Lu, Q.T., Hao, N.B., Ge, Q.Y., Zhang, Q.D., Jiang, G.M., Du, W.G., Kuang, T.Y.: The relation between C4 pathway enzymes and PS photochemical function in soybean. - Acta bot. sin. 42: 689-692, 2000.
    28. Li, X., Jiao, D.M., Dai, C.C., Wu, S., Wang, S.H., Li, C.Q.: [Photosynthetic characteristics for rice hybrids with transgenic PEPC parent Hpter-01.] - Acta agron. sin. 27: 137-143, 2001. [In Chin.]
    29. O'Leary, M.H.: Phosphoenolpyruvate carboxylase: an enzymeologist's view. - Annu. Rev. Plant Physiol. 33: 297-315, 1982. Go to original source...
    30. Outlow, W.H., Jr.: Kinetic properties of guard-cell phosphoenolpyruvate carboxylase. - Biochem. Physiol. Pflanz. 186: 317-325, 1990. Go to original source...
    31. Powles, S.B.: Photoinhibition of photosynthesis induced by visible light. - Annu. Rev. Plant Physiol. 35: 15-44, 1984. Go to original source...
    32. Salin, M.L.: Toxic oxygen species and protective systems of the chloroplast. - Physiol. Plant. 72: 681-689, 1988. Go to original source...
    33. Walter, M.H., Grima-Pettenati, J.C.: Characterization of bean (Phaseolus vulgaris L.) malic enzyme. - Eur. J. Biochem. 224: 999-1009, 1994. Go to original source...
    34. Wang, A.G., Luo, G.H.: [Quantitative relation of hydroxylamine and superoxide anion radicals in plants.] - Plant Physiol. Commun. 6: 55-57, 1990. [In Chin.]

    Return to the content