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Expression of the psbA gene during photoinhibition and recovery in Synechocystis PCC 6714: inhibition and damage of transcriptional and translational machinery prevent the restoration of photosystem II activity

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Abstract

The D1 reaction center protein of the photosystem II complex is very sensitive to light. It is continuously being damaged, degraded and resynthesized. Under high light, photosystem II inactivation is observed. This is because the rate of D1 damage is faster than that of its replacement. This process can be reversed if exposure to high light is not too long. In this work we study the changes that occur in the transcriptional and translational machinery that could lead to irreversible photoinhibition in Synechocystis PCC 6714. In the first minutes of photoinhibition, high light induced an accumulation of psbA mRNA due to an increase in psbA transcription initiation. Although the transcription rate of other photosynthetic genes (e.g. psaE and cpcB-cpcA) declined, the high turnover of the psbA transcript was maintained for a long time. When the light stress was too long, the stability of psbA mRNA increased and the psbA transcription rate appeared to decrease. A high level of psbA mRNA was maintained even though translation no longer occurred and the cells were unable to recover. Experiments to measure newly synthesized D1 incorporation into the thylakoid membranes during recovery in the presence of rifampicin showed that the initiation of transcription was not required for translation of psbA mRNA when photoinhibition was still reversible. Since psbA translation did not depend on the level of psbA transcript or on the initiation of psbA transcription, we propose that damage to the translational machinery also occurred during light stress, leading to the inhibition of D1 synthesis and to irreversible photoinhibition.

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References

  1. Ajlani G, Kirilovsky D, Picaud M, Astier C: Molecular analysis of psbAmutations responsible for various herbicide resistance phenotypes in Synechocystis6714. PlantMol Biol 13: 469-479 (1989).

    Google Scholar 

  2. Aro E-M, Virgin I, Andersson B: Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113-134 (1993).

    Google Scholar 

  3. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K: Current Protocols in Molecular Biology. Greene Publishing Associates/Wiley-Interscience, New York (1987).

    Google Scholar 

  4. Bandyopadhyay R, Coutts M, Krowczynska A, Brawerman G: Nuclease activity associated with mammalian mRNA in its native state: possible basis for selectivity in mRNA decay. Mol Cell Biol 10: 2060-2069 (1990).

    Google Scholar 

  5. Bennett A, Bogorad L: Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol 58: 419-435 (1973).

    Google Scholar 

  6. Bouyoub A, Vernotte C, Astier C: Analysis of the function of the two homologous copies of the psbAgene in SynechocystisPCC 6714 and PCC 6803. Plant Mol Biol 21: 249-258 (1993).

    Google Scholar 

  7. Capuano V, Mazel D, Tandeau de Marsac N, Houmard J: Complete nucleotide sequence of the red-light specific set of phycocyanin genes from the cyanobacterium CalothrixPCC 7601. Nucl Acids Res 16 (4): 1626 (1988).

    Google Scholar 

  8. Chitnis PR, Reilly PA, Miedel MC, Nelson N: Structure and targeted mutagenesis of the gene encoding 8-kDa subunit of photosystem I from the cyanobacterium Synechocystissp. PCC 6803. J Biol Chem 264: 18374-18380 (1989).

    Google Scholar 

  9. Clarke AK, Soitamo A, Gustafsson P, Öquist G: Rapid interchange between two distinct forms of cyanobacterial photosystem II reaction-center protein D1 in response to photoinhibition. Proc Natl Acad Sci USA 90: 9973-9977 (1993).

    Google Scholar 

  10. Constant S, Perewoska I, Nebdal L, Miranda T, Etienne AL, Kirilovsky D: A new phenotype for a herbicide resistantmutant of Synechocystis6714 with a high sensitivity to photoinhibition. Plant Sci 115: 165-174 (1996).

    Google Scholar 

  11. Debus RJ: The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102: 269-352 (1992).

    Google Scholar 

  12. Etienne AL, Kirilovsky D: The primary structure of D1 near the QB pocket influences oxygen evolution. Photosynth Res 38: 387-394 (1993).

    Google Scholar 

  13. Erickson JM, Rochaix JD: The molecular biology of photosystem II. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology. Topics in photosynthesis, vol 11, pp. 101-177. Elsevier, Amsterdam (1992).

    Google Scholar 

  14. Golden SS, Brusslan J, Haselkorn R: Expression of a family of psbAgenes encoding a photosystem II polypeptide in the cyanobaterium Anacystis nidulansR2. EMBO J 5: 2789-2798 (1986).

    Google Scholar 

  15. Golden SS: Light-responsive gene expression in cyanobacteria. J Bact 177: 1651-1654 (1995).

    Google Scholar 

  16. Graves RA, Pandey NB, Chodchoy N, Marzluff WF: Translation is required for regulation of histone mRNA degradation. Cell 48: 615-626 (1987).

    Google Scholar 

  17. Herdman M, Deloney SF, Carr NG: A new medium for the isolation and growth of auxotrophic mutants of the blue green alga Anacystis nidulans. J Gen Microbiol 79: 233-237 (1973).

    Google Scholar 

  18. Jansson C, Debus RJ, Osiewacz HD, Gurevitz M, McIntosh L: Construction of an obligate photoheterotrophic mutant of the cyanobaterium Synechocystis6803. Plant Physiol 85: 1021- 1025 (1987).

    Google Scholar 

  19. Kanervo E, Aro EM, Murata N: Low unsaturation level of thylakoid membrane lipids limits turnover of the D1 protein of photosystem II at high irradiance. FEBS Lett 364: 239-242 (1995).

    Google Scholar 

  20. Kirilovsky D, Vernotte C, Astier C, Etienne AL: Reversible and irreversible photoinhibition in herbicide-resistant mutants of Synechocystis6714. Biochim Biophys Acta 933: 124-131 (1988).

    Google Scholar 

  21. Kirilovsky D, Ajlani G, Picaud M, Etienne AL: Mutations responsible for high light sensitivity in an atrazine-resistant mutant of Synechocystis6714. Plant Mol Biol 13: 355-363 (1989).

    Google Scholar 

  22. Kirilovsky D, Ducruet JM, Etienne AL: Primary events occuring in photoinhibition in Synechocystis6714 wild-type and an atrazine-resistant mutant. Biochim Biophys Acta 1020: 87-93 (1990).

    Google Scholar 

  23. Klaff P, Grissem W: Changes in chloroplast mRNA stability during leaf development. Plant Cell 3: 517-529 (1991).

    Google Scholar 

  24. Krause GH: The role of oxygen in photoinhibition of photosynthesis. In: Foyer CH, Mullineaux PM (eds) Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants, pp. 43-76. CRC Press, Boca Raton, FL (1994).

    Google Scholar 

  25. Kulkarni RD, Schaefer MR, Golden SS: Transcriptional and posttranscriptional components of psbAresponse to high light intensity in Synechococcussp. strain PCC 7942. J Bact 174: 3775-3781 (1992).

    Google Scholar 

  26. Kulkarni RD, Golden SS: Form II of D1 is important during transition from standard to high light intensity in Synechococcussp. strain PCC 7942. Photosynth Res 46: 435-443 (1995).

    Google Scholar 

  27. Kyle DJ, Ohad I, Arntzen CJ: Membrane protein damage and repair: selective loss of quinone protein function in chloroplast membranes. Proc Natl Acad Sci USA 81: 4070-4074 (1984).

    Google Scholar 

  28. Laemlii UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680- 685 (1970).

    Google Scholar 

  29. Mäenpää P, Kallio T, Mulo P, Salih G, Aro EM, Tyystjärvi E, Jansson C: Site-specific mutations in the D1 polypeptide affect the susceptibility of Synechocystis6803 cells to photoinhibition. Plant Mol Biol 22: 1-12 (1993).

    Google Scholar 

  30. Mattoo AK, Hoffman-Falk H, Marder JB, and Edelman M: Regulation of protein metabolism: coupling of photosynthetic electron transport to in vivodegradation of the rapidly metabolized 32-kilodalton protein of the chloroplast membranes. Proc Natl Acad Sci USA 81: 1380-1384 (1984).

    Google Scholar 

  31. Mohamed A, Jansson C: Influence of light on accumulation of photosynthesis-specific transcripts in the cyanobacterium Synechocystis6803. Plant Mol Biol 13: 693-700 (1989).

    Google Scholar 

  32. Mohamed A, Jansson C: Photosynthetic electron transport controls degradation but not production of psbAtranscripts in the cyanobacterium Synechocystis6803. Plant Mol Biol 16: 891- 897 (1991).

    Google Scholar 

  33. Mohamed A, Eriksson J, Osiewacz HD, Jansson C: Differential expression of the psbAgenes in the cyanobacterium Synechocysitis6803. Mol Gen Genet 238: 161-168 (1993).

    Google Scholar 

  34. Ohad I, Kyle DJ, Arntzen CJ: Membrane protein damage and repair removal and replacement of inactivated 32 Kd polypeptides in chloroplast membranes. J Cell Biol 99: 481-485 (1985).

    Google Scholar 

  35. Ohad N, Amir-Shapira D, Koike H, Inoue Y, Ohad I, Hirschberg J: Amino acid substitutions in the D1 protein of photosystem II affect QB-stabilization and accelerate turnover of D1. Z Naturforsch 45c: 402-407 (1990).

    Google Scholar 

  36. Perewoska I, Etienne AL, Miranda T, Kirilovsky D: S1 destabilization and higher sensitivity to light in metribuzin-resistant mutants. Plant Physiol 104: 235-245 (1994).

    Google Scholar 

  37. Petersen C: Translation andmRNAstability in bacteria: a complex relationship. In: Belasco J, Brawerman G (eds) Control of Messenger RNA Stability, pp. 117-145. Academic Press, San Diego (1993).

    Google Scholar 

  38. Powles SB: Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35: 15-44 (1984).

    Google Scholar 

  39. Prasil O, Adir N, Ohad I: Dynamics of photosystem II: mechanism of photoinhibition and recovery processes. In: Barber J (eds) The Photosystems: Structure, Function and Molecular Biology, pp. 295-348. Elsevier Science Publishers, Amsterdam (1992).

    Google Scholar 

  40. Rousseau F: Ph.D. Thesis. Paris XI University, CEA, Saclay, France (1992).

  41. Samuelsson G, Lönneborg A, Gustafsson P, Oquist G: The susceptibility of photosynthesis to photoinhibition and the capacity of recovery in high light and low light grown cyanobacteria, Anacystis nidulans. Plant Physiol 83: 438-441 (1987).

    Google Scholar 

  42. Schaefer MR, Golden SS: Differential expression of members of a cyanobacterial psbAgene family in response to light. J Bact 171: 3973-3981 (1989).

    Google Scholar 

  43. Vermaas WJF, Ikeuchi M: Photosystem II. In Bogorad L, Vasil IK (eds), The Photosynthetic Apparatus: Molecular Biology and Operation, pp. 25-111. Academic Press, SanDiego (1991).

    Google Scholar 

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  1. URA 1810, CNRS, E.N.S., 46, rue d'Ulm, 75230, Paris Cedex 05, France

    Sabine Constant, Irène Perewoska, Miguel Alfonso & Diana Kirilovsky

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  1. Sabine Constant
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  2. Irène Perewoska
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  3. Miguel Alfonso
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  4. Diana Kirilovsky
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Constant, S., Perewoska, I., Alfonso, M. et al. Expression of the psbA gene during photoinhibition and recovery in Synechocystis PCC 6714: inhibition and damage of transcriptional and translational machinery prevent the restoration of photosystem II activity. Plant Mol Biol 34, 1–13 (1997). https://doi.org/10.1023/A:1005754823218

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