Changes in the transcriptional activity of barley plastome genes under heat shock

  • Ya. O. Zubo
  • E. A. Lysenko
  • A. Yu. Aleinikova
  • V. V. Kusnetsov
  • N. L. Pshibytko
Research Papers


Plants use a wide range of molecular reactions for adaptation of their photosynthetic apparatus to high temperature. To understand the role of plastome genes in this process, we studied transcription of photosynthetic and household genes in plastids of 7-day-old barley (Hordeum vulgare L.) seedlings and found that the genes of both groups are involved in the adaptation to heat shock. Transcription of genes encoding apoproteins of the photosystem I and photosystem II reaction centers was enhanced in 1.5 h after temperature elevation and reduced after 3 h, whereas transcription of some other genes (NADPH plastoquinone oxidoreductase, ribosomal proteins, and multisubunit RNA polymerase) was enhanced after 3 h of exposure to high temperature. Transcription of plastome genes rpl23-rpl2 and rps16 was activated by heating either the whole plant or isolated chloroplasts. This permits a supposition that changes in transcription of plastome genes occur not only due to changes in nuclear transcription of the genes encoding plastid transcription factors but also due to changes in the properties of transcription factors inside chloroplasts.

Key words

Hordeum vulgare heat shock adaptation chloroplasts plastome transcription 



plastid encoded RNA polymerase




sodium citrate buffer comprising 0.15 M NaCl and 0.015 M sodium citrate, pH 7.0


  1. 1.
    Stress of Life: From Molecules to Man, Csermely, P., Ed., New York: Ann. Acad. Sci., 1998.Google Scholar
  2. 2.
    Takeuchi, T.S. and Thornber, J.P., Heat-Induced Alterations in Thylakoid Membrane Protein Composition in Barley, Aust. J. Plant Physiol., 1994, vol. 21, pp. 759–770.CrossRefGoogle Scholar
  3. 3.
    Bukhov, N.G., Wiese, C., Neimanis, S., and Heber, U., Heat Sensitivity of Chloroplasts and Leaves: Leakage of Protons from Thylakoids and Reversible Activation of Cyclic Electron Transport, Photosynth. Res., 1999, vol. 59, pp. 81–93.CrossRefGoogle Scholar
  4. 4.
    Crafts-Brandner, S.J. and Salvucci, M.E., Sensitivity of Photosynthesis in a C4 Plant, Maize, to Heat Stress, Plant Physiol., 2002, vol. 129, pp. 1773–1780.PubMedCrossRefGoogle Scholar
  5. 5.
    Yoshioka, M., Uchida, S., Mori, H., Komayama, K., Ohira, S., Morita, N., Nakanishi, T., and Yamamoto, Y., Quality Control of Photosystem II. Cleavage of Reaction Center D1 Protein in Spinach Thylakoids by FtsH Protease under Moderate Heat Stress, J. Biol. Chem., 2006, vol. 281, pp. 21 660–21 669.CrossRefGoogle Scholar
  6. 6.
    Heckathorn, S.A., Downs, C.A., Sharkey, T.D., and Coleman, J.S., The Small, Methionine-Rich Chloroplast Heat-Shock Protein Protects Photosystem II Electron Transport during Heat Stress, Plant Physiol., 1998, vol. 116, pp. 439–444.PubMedCrossRefGoogle Scholar
  7. 7.
    Bhadula, S.K., Elthon, T.E., Habben, J.E., Helentjaris, T.G., Jiao, S., and Ristic, Z., Heat-Stress Induced Synthesis of Chloroplast Protein Synthesis Elongation Factor (EF-Tu) in a Heat-Tolerant Maize Line, Planta, 2001, vol. 212, pp. 359–366.PubMedCrossRefGoogle Scholar
  8. 8.
    Sinvany-Villalobo, G., Davydov, O., Ben-Ari, G., Zaltsman, A., Raskind, A., and Adam, Z., Expression in Multigene Families. Analysis of Chloroplast and Mitochondrial Proteases, Plant Physiol., 2004, vol. 135, pp. 1336–1345.PubMedCrossRefGoogle Scholar
  9. 9.
    Wang, P., Duan, W., Takabayashi, A., Endo, T., Shikanai, T., Ye, J.Y., and Mi, H., Chloroplastic NADPH Dehydrogenase in Tobacco Leaves Functions in Alleviation of Oxidative Damage Caused by Temperature Stress, Plant Physiol., 2006, vol. 141, pp. 465–474.PubMedCrossRefGoogle Scholar
  10. 10.
    Komayama, K., Khatoon, M., Takenaka, D., Horie, J., Yamashita, A., Yoshioka, M., Nakayama, Y., Yoshida, M., Ohira, S., Morita, N., Velitchkova, M., Enami, I., and Yamamoto, Y., Quality Control of Photosystem II: Cleavage and Aggregation of Heat-Damaged D1 Protein in Spinach Thylakoids, Biochim. Biophys. Acta, 2007, vol. 1767, pp. 838–846.PubMedCrossRefGoogle Scholar
  11. 11.
    Danilenko, N.G. and Davydenko, O.G., Miry genomov organell (Worlds of Organelle Genomes), Minsk: Tekhnalogiya, 2003.Google Scholar
  12. 12.
    Allison, L.A., Simon, L.D., and Maliga, P., Deletion of rpoB Reveals a Second Distinct Transcription System in Plastids of Higher Plants, EMBO J., 1996, vol. 15, pp. 2802–2809.PubMedGoogle Scholar
  13. 13.
    Zubko, M.K. and Day, A., Stable Albinism Induced without Mutagenesis: A Model for Ribosome-Free Plastid Inheritance, Plant J., 1998, vol. 15, pp. 265–271.PubMedCrossRefGoogle Scholar
  14. 14.
    Kusnetsov, V.V., Mikulovich, T.P., Kukina, I.M., Cherepneva, G.N., Herrmann, R.G., and Kulaeva, O.N., Changes in the Level of Chloroplast Transcripts in Pumpkin Cotyledons during Heat Shock, FEBS Lett., 1993, vol. 321, pp. 189–193.PubMedCrossRefGoogle Scholar
  15. 15.
    Nakajima, Y. and Mulligan, R.M., Heat Stress Results in Incomplete C-to-U Editing of Maize Chloroplast mRNAs and Correlates with Changes in Chloroplast Transcription Rate, Curr. Genet., 2001, vol. 40, pp. 209–213.PubMedCrossRefGoogle Scholar
  16. 16.
    Pshibytko, N.L., Kalitukho, L.N., and Kabashnikova, L.F., Effects of High Temperature and Water Deficit on Photosystem II in Hordeum vulgare Leaves of Various Ages, Russ. J. Plant Physiol., 2003, vol. 50, pp. 44–51.CrossRefGoogle Scholar
  17. 17.
    Pshibytko, N.L., Kalitukho, L.N., Zhavoronkova, N.B., and Kabashnikova, L.F., Effect of Heat Shock and Water Deficit on Photosynthetic Membrane State in Hordeum vulgare Leaves of Various Ages, Biol. Membr. (Moscow), 2003, vol. 20, pp. 121–127.Google Scholar
  18. 18.
    Pshybytko, N.L., Kalituho, L.N., and Kabashnikova, L.F., The Various Mechanisms of Photosynthesis Limitation in Heated Barley Seedlings of Different Ages, Bulg. J. Plant Physiol., 2003, spec. iss., pp. 304–313.Google Scholar
  19. 19.
    Maiseyenkava, Y.A., Pshybytko, N.L., and Kabashnikova, L.F., Barley Seedlings under High Temperature, Gen. Appl. Plant Physiol., 2005, vol. 31, pp. 3–14.Google Scholar
  20. 20.
    Satoh, J., Baba, K., Nakahira, Y., Shiina, T., and Toyoshima, Y., Characterization of Dynamics of the psbD Light-Induced Transcription in Mature Wheat Chloroplasts, Plant Mol. Biol., 1997, vol. 33, pp. 267–278.PubMedCrossRefGoogle Scholar
  21. 21.
    Brown, R. and Rickless, P., A New Method for Study of Cell Division and Cell Extension with Some Preliminary Effect of Temperature and Nutrient, Proc. Roy. Soc. B: Biol. Sci., 1949, vol. 136, pp. 110–125.CrossRefGoogle Scholar
  22. 22.
    Gaudino, R.J. and Pikaard, C.S., Cytokinin Induction of RNA Polymerase I Transcription in Arabidopsis thaliana, J. Biol. Chem., 1997, vol. 272, pp. 6799–6804.PubMedCrossRefGoogle Scholar
  23. 23.
    Bookjanns, G., Stummann, B.M., and Henningsen, K.W., Preparation of Chloroplast DNA from Pea Plastids Isolated in a Medium of High Ionic Strength, Anal. Biochem., 1984, vol. 141, pp. 244–247.CrossRefGoogle Scholar
  24. 24.
    Rochaix, J.D., Perron, K., Dauvillee, D., Laroche, F., Takahashi, Y., and Goldschmidt-Clermont, M., Post-Transcriptional Steps Involved in the Assembly of Photosystem I in Chlamydomonas, Biochem. Soc. Trans., 2004, vol. 32, pp. 567–570.PubMedCrossRefGoogle Scholar
  25. 25.
    Gamble, P.E. and Mullet, J.E., Blue Light Regulates the Accumulation of Two psbD-psbC Transcripts in Barley Chloroplasts, EMBO J., 1989, vol. 8, pp. 2785–2794.PubMedGoogle Scholar
  26. 26.
    Nagashima, A., Hanaoka, M., Shikanai, T., Fujiwara, M., Kanamaru, K., Takahashi, H., and Tanaka, K., The Multiple-Stress Responsive Plastid Sigma Factor, Sig5, Directs Activation of the psbD Blue Light-Responsive Promoter (LRP) in Arabidopsis thaliana, Plant Cell Physiol., 2004, vol. 45, pp. 357–368.PubMedCrossRefGoogle Scholar
  27. 27.
    Tsunoyama, Y., Ishizaki, Y., Morikawa, K., Kobori, M., Nakahira, Y., Takeba, G., Toyoshima, Y., and Shiina, T., Blue Light-Induced Transcription of Plastid-Encoded psbD Gene Is Mediated by a Nuclear-Encoded Transcription Initiation Factor, AtSig5, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 3304–3309.PubMedCrossRefGoogle Scholar
  28. 28.
    Lysenko, E.A., Plant Sigma Factors and Their Role in Plastid Transcription, Plant Cell Rep., 2007, vol. 26, pp. 845–859.PubMedCrossRefGoogle Scholar
  29. 29.
    Yamamoto, Y., Quality Control of Photosystem II, Plant Cell Physiol., 2001, vol. 42, pp. 121–128.PubMedCrossRefGoogle Scholar
  30. 30.
    Christopher, D.A. and Mullet, J.E., Separate Photosensory Pathways Co-Regulate Blue Light/Ultraviolet-A-Activated psbD-psbC Transcription and Light-Induced D2 and CP43 Degradation in Barley (Hordeum vulgare) Chloroplasts, Plant Physiol., 1994, vol. 104, pp. 1119–1129.PubMedCrossRefGoogle Scholar
  31. 31.
    Lysenko, E.A., Analysis of the Evolution of the Family of the Sig Genes Encoding Plant Sigma Factors, Russ. J. Plant Physiol., 2006, vol. 53, pp. 605–614.CrossRefGoogle Scholar

Copyright information

© MAIK Nauka 2008

Authors and Affiliations

  • Ya. O. Zubo
    • 1
  • E. A. Lysenko
    • 1
  • A. Yu. Aleinikova
    • 1
  • V. V. Kusnetsov
    • 1
  • N. L. Pshibytko
    • 2
  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  2. 2.Institute of Biophysics and Cell EngineeringNational Academy of BelarusMinskBelarus

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