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The Effects of Salt Stress on Photosynthetic Electron Transport and Thylakoid Membrane Proteins in the Cyanobacterium Spirulina platensis

  • Sudhir, Putty-Reddy (Department of Biochemistry, Sri Venkateswara University) ;
  • Pogoryelov, Denys (Institute of Plant Biology, Biological Research Center, Hungarian cademy of Sciences) ;
  • Kovacs, Laszlo (Institute of Plant Biology, Biological Research Center, Hungarian cademy of Sciences) ;
  • Garab, Gyozo (Institute of Plant Biology, Biological Research Center, Hungarian cademy of Sciences) ;
  • Murthy, Sistla D.S. (Department of Biochemistry, Sri Venkateswara University)
  • Published : 2005.07.31

Abstract

The response of Spirulina (Arthrospira) platensis to high salt stress was investigated by incubating the cells in light of moderate intensity in the presence of 0.8 M NaCl. NaCl caused a decrease in photosystem II (PSII) mediated oxygen evolution activity and increase in photosystem I (PSI) activity and the amount of P700. Similarly maximal efficiency of PSII (Fv/Fm) and variable fluorescence (Fv/Fo) were also declined in salt-stressed cells. Western blot analysis reveal that the inhibition in PSII activity is due to a 40% loss of a thylakoid membrane protein, known as D1, which is located in PSII reaction center. NaCl treatment of cells also resulted in the alterations of other thylakoid membrane proteins: most prominently, a dramatic diminishment of the 47-kDa chlorophyll protein (CP) and 94-kDa protein, and accumulation of a 17-kDa protein band were observed in SDS-PAGE. The changes in 47-kDa and 94-kDa proteins lead to the decreased energy transfer from light harvesting antenna to PSII, which was accompanied by alterations in the chlorophyll fluorescence emission spectra of whole cells and isolated thylakoids. Therefore we conclude that salt stress has various effects on photosynthetic electron transport activities due to the marked alterations in the composition of thylakoid membrane proteins.

Keywords

References

  1. Allakhverdiev, S. I., Nishiyama, Y., Miyairi, S., Yamamoto, H., Inagaki, N., Kanesaki Y. and Murata, N. (2002) Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiol. 130, 1443-1453 https://doi.org/10.1104/pp.011114
  2. Allakhverdiev, S. I., Sakamoto, A., Nishiyama, Y., Inaba, M. and Murata, N. (2000) Ionic and osmotic effects of NaCl-induced inactivation of photosystem I and II in Synechococcus sp. Plant Physiol. 123, 1047-1056 https://doi.org/10.1104/pp.123.3.1047
  3. Aro, E. M., McCaffery, S. and Anderson, J. (1993) Photo inhibition and D1 protein degradation in peas acclimated to different growth conditions. Plant Physiol. 103, 835-843
  4. Bhagwat, A. A. and Apte, S. K. (1989) Comparative analysis of proteins induced by heat shock, salinity, and osmotic stress in the nitrogen-fixing cyanobacterium Anabaena sp. Strain L-31. J. Bacteriol. 171, 5187-5189
  5. Garnier, F., Dubacq, J.-P. and Thomas, J.-C. (1994) Evidence for a transient association of new proteins with the Spirulina maxima phycobilisomes in relation to light intensity. Plant Physiol. 106, 747-754
  6. Giardi, M. T., Masojidek, J. and Godde, D. (1997) Effects of abiotic stresses on the turnover of the $D_1$ reaction center II protein. Physiol. Plant. 101, 635-642 https://doi.org/10.1111/j.1399-3054.1997.tb01048.x
  7. Gilmour, D. J., Hipkins, M. F. and Boney, A. D. (1982) The effect of salt stress on the primary processes of photosynthesis in Dunalielia tertiolecta. Plant Sci. Lett. 26, 325-330 https://doi.org/10.1016/0304-4211(82)90107-9
  8. Hagemann, M., Wolfel, L. and Kruger, B. (1990) Alterations of protein synthesis in the cyanobacterium Synechocystis sp. PCC 6803 after a salt shock. J. Gen. Microbiol. 136, 1393-1399 https://doi.org/10.1099/00221287-136-7-1393
  9. Hagio, M., Gombos, Z., Varkonyi, Z., Masamoto, K., Sato, N., Tsuzuki, M. and Wada, H. (2000) Direct evidence for requirement of phosphotidylglycerol in photosystem II of photosynthesis. Plant Physiol. 124, 795-804 https://doi.org/10.1104/pp.124.2.795
  10. Hiyama, T. and Ke, B. (1972) Difference spectra and extinction coefficients of P700. Biochim. Biophys. Acta 267, 160-171 https://doi.org/10.1016/0005-2728(72)90147-8
  11. Jeanjean, R., Matthijs, H. C. P., Onana, B., Havax, M. and Joset, F. (1993) Exposure of cyanobacterium Synechocystis PCC6803 to salt stress induces concerted changes in respiration and photosynthesis. Plant and Cell Physiol. 34, 1073-1079
  12. Joset, F., Jeanjean, R. and Hagemann, M. (1996) Dynamics of the response of cyanobacteria to salt stress: deciphering the molecular events. Physiol. Plant. 96, 738-744 https://doi.org/10.1111/j.1399-3054.1996.tb00251.x
  13. Kuwabara, T. and Murata, N. (1983) Inactivation of photosynthetic oxygen evolution and concomitant release of three polypeptides in the photosystem II particles of spinach chloroplasts. Plant Cell Physiol. 23, 533-539
  14. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage $T_4$. Nature 227, 680-685 https://doi.org/10.1038/227680a0
  15. Lu, C. and Vonshak, A. (1999) Characterization of PSII photochemistry in salt-adapted cells of cyanobacterium Spirulina platensis. New Phytol. 141, 231-239 https://doi.org/10.1046/j.1469-8137.1999.00340.x
  16. Lu, C. and Vonshak, A. (2002) Effects of salinity stress on photosystem II function in cyanobacterial Spirulina platensis cells. Physiol. Plant. 114, 405-413 https://doi.org/10.1034/j.1399-3054.2002.1140310.x
  17. Lu, C. and Zhang, J. (2000) Role of light in the response of PSII photochemistry to salt stress in the cyanobacterium Spirulina platensis. J. Exp. Bot. 51, 911-917 https://doi.org/10.1093/jexbot/51.346.911
  18. MacKinney, G. (1991) Absorption of light by chlorophyll solutions. J. Biol. Chem. 140, 315-322
  19. Murata, N., Mohanty, P. S., Hayashi, H. and Papageorgiou, G. C. (1992) Glycinebetaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen evolving complex. FEBS Lett. 296, 187-189 https://doi.org/10.1016/0014-5793(92)80376-R
  20. Murthy, S. D. S., Mohanty, N. and Mohanty, P. (1995) Prolonged incubation of mercury alters energy transfer and chlorophyll (Chl) a protein complexes in Synechococcus 6301: changes in Chl a absorption and emission characteristics and loss of the F695 emission band. Biometals 8, 237-242 https://doi.org/10.1007/BF00143382
  21. Nishiyama, Y., Kovacs, E., Lee, C. B., Hayashi, H., Watanabe, T. and Murata, N. (1993) Photosynthetic adaptation to high temperature associated with thylakoid membranes of Synechococcus PCC7002. Plant Cell Physiol. 34, 337-343
  22. Ohad, I., Kyle, D. J. and Arntzen, C. J. (1984) Membrane protein damage and repair removal and replacement of inactivated 32 kD polypeptides in chloroplast membranes. J. Cell Biol. 99, 481-485 https://doi.org/10.1083/jcb.99.2.481
  23. Pogoryelov, D., Sudhir P.-R., Kovacs, L., Gombos, G., Brown, I. and Garab, G. (2003) Sodium-dependency of the photosynthetic electron transport in the alkaliphilic cyanobacterium Arthrospira platensis. J. Bioenerg. Biomembr. 35, 427-437 https://doi.org/10.1023/A:1027339814544
  24. Rajagopal, S., Murthy, S. D. S. and Mohanty, P. (2000) Effect of ultraviolet-B radiation on intact cells of the cyanobacterium Spirulina platensis: characterization of the alterations in the thylakoid membranes. J. Photochem. Photobiol. B: Biol. 54, 61-66 https://doi.org/10.1016/S1011-1344(99)00156-6
  25. Rintamaki, E., Riitta, S. and Aro, E. M. (1994) Rapid turnover of D1 reaction-center protein of photosystem II as a protection mechanism against photoinhibition in a moss Ceratodon purpureus (Hedw.) Bird. Planta 193, 520-529 https://doi.org/10.1007/BF02411557
  26. Schubert, H. and Hagemann, M. (1990) Salt effects on 77K fluorescence and photosynthesis in the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol. Lett. 71, 169-172 https://doi.org/10.1111/j.1574-6968.1990.tb03817.x
  27. Sudhir, P. and Murthy, S. D. S. (2004) Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42, 481-486 https://doi.org/10.1007/S11099-005-0001-6
  28. Towbin, H., Stachelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4354
  29. Verma, K. and Mohanty, P. (2000) Changes of the photosynthetic apparatus in Spirulina cyanobacterium by sodium stress. Z. Naturforsch. 55, 16-22
  30. Vonshak, A., Kancharaksa, N., Bunnag, B. and Tanticharoen, M. (1996) Role of light and photosynthesis on the acclimation process of the cyanobacterium Spirulina platensis to salinity stress. J. Applied phycol. 8, 119-124 https://doi.org/10.1007/BF02186314
  31. Zarrouk, C. (1966) Contribution a l'etude d'une cyanophycee. Influence de diverse facteurs physique et chimiques sur la croissance et photosynthese le Spirulina maxima Geitler, Ph.D. Thesis, University of Paris
  32. Zeng, T. M. and Vonshak, A. (1998) Adaptation of Spirulina platensis to salinity stress. Comp. Biochem. Physiol. 20, 113-118

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