Skip to main content
Log in

Heat sensitivity of Rubisco, Rubisco activase and Rubisco binding protein in higher plants

  • Review
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

During the past few years the investigations concerning Rubisco and the changes of its activity and properties at elevated temperature were reconsidered with special reference to the important role of Rubisco activase and Rubisco binding protein. The major changes in Rubisco, Rubisco activase and Rubisco binding protein reported recently are presented in this review. New information on these proteins, including their changes under heat stress conditions, is discussed together with open questions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

HMM:

high molecular mass

HS:

heat shock

HSP:

heat shock protein

HT:

high temperature

LS:

large subunit of Rubisco

PSII:

photosystem II

R:

Rubisco (ribulose-1,5-bisphosphate carboxylase/oxygenase)

RA:

Rubisco activase

RBP:

Rubisco binding protein

RuBP:

ribulose-1,5-bisphosphate

SS:

small subunit of Rubisco

T:

temperature

References

  • Andrews T. J., Lorimer G. H., 1987. Rubisco: structure, mechanisms, and prospects for improvement. In: The biochemistry of Plants, ed. by M. D. Hatch and N. K. Boardman, Academic Press, vol. 10: 131–218.

  • Ayala-Ochoa A., Loza-Tavera H., de Jimenez E. S., 1998. A cDNA from maize encoding ribulose-1,5-bisphosphate carboxylase/oxygenase activase (accession no. AF084478) (PGR 98-207). Plant Physiol., 118: 1535.

    Google Scholar 

  • Badger M. R., Björkman O., Armond P. A., 1982. Analysis of photosynthetic response and adaptation to temperature in higher plants: temperature acclimation in the desert evergreen Nerium oleander L. Plant Cell Environ. 5: 85–99.

    CAS  Google Scholar 

  • Barraclough R., Ellis R. J., 1980. Protein synthesis in chloroplasts. IX. Assembly of newly-synthesised large subunit into ribulose bisphosphate carboxylase in isolated pea chloroplasts. Bichim. Biphys. Acta, 608: 19–31.

    CAS  Google Scholar 

  • Berry J., Björkman O., 1980. Photosynthetic response and adaptation to temperature in higher plants. Annu Rev. Plant Physiol., 31: 491–453.

    Article  Google Scholar 

  • Bilger W., Schreiber U., Lange O. L., 1987. Chlorophyll fluorescence as an indicator of heat induced limitation of photosynthesis in Arbutus unedo L. In: Plant Responses to Stress, ed. by J. D. Tenhunen, F. M. Catarino, O. L. Lange, Springer, Berlin: 391–399.

    Google Scholar 

  • Bose A., Ghosh B., 1995a. Effect of heat stress on ribulose-1,5-bisphosphate carboxylase in rice. Phytochemistry, 38: 1115–1118.

    Article  CAS  Google Scholar 

  • Bose A., Ghosh B., 1995b. Responses of photosynthetic apparatus in rice cultivars under thermal stress. Photosynthetica, 31: 625–630.

    CAS  Google Scholar 

  • Bose A., Tiwari B. S., Chattopadhyay M. K., Gupta S., Ghosh B., 1999. Thermal stress induces differential degradation of Rubisco in heat-sensitive and heat-tolerant rice. Physiol. Plant., 105: 89–94.

    Article  CAS  Google Scholar 

  • Bukau B., Horwich A., 1998. The Hsp 70 and Hsp 60 chaperone machines. Cell, 92: 351–366.

    Article  PubMed  CAS  Google Scholar 

  • Cannon S., Wang P., Roy H., 1986. Inhibition of ribulose bisphosphate carboxylase assembly by antibody to a binding protein. J. Cell Biol., 103: 1327–1335.

    Article  PubMed  CAS  Google Scholar 

  • Crafts-Brandner S. J., van de Loo F. J., Salvucci M. E., 1997. The two forms of ribulose-1,5-bisphophate carboxylase/oxygenase activase differ in sensitivity to elevated temperature. Plant Physiol., 114: 439–444.

    PubMed  CAS  Google Scholar 

  • Crafts-Brandner S. J., Law R. D., 2000. Effect of heat stress on the inhibition and recovery of the ribulose-1,5-bisphosphate carboxylase/oxygenase activation state. Planta, 212:67–74.

    Article  PubMed  CAS  Google Scholar 

  • Crafts-Brandner S. J., Salvucci M. E., 2000. Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc. Natl. Acad. Sci. USA, 97: 13430–13435.

    Article  PubMed  CAS  Google Scholar 

  • Crafts-Brandner S. J., Salvucci M. E., 2002. Sensitivity of photosynthesis in a C4 plant, maize, to heat stress. Plant Physiol., 129:1773–1780.

    Article  PubMed  CAS  Google Scholar 

  • Eckardt N. A., Portis A. R. Jr, 1997. Heat denaturation profiles of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and Rubisco activase and the inability of Rubisco activase to restore activity of heat-denatured Rubisco. Plant Physiol., 113: 243–248.

    Article  PubMed  CAS  Google Scholar 

  • Eckardt N. A., Snyder G. W., Portis A. R. Jr., Ogren W. L., 1997. Growth and photosynthesis under high and low irradiance of Arabidopsis thaliana antisense mutants with reduced ribulose-1,5-bisphosphate carboxylase/oxygenase activase content. Plant Physiol., 113: 575–586.

    Article  PubMed  CAS  Google Scholar 

  • Edwards G. E., Furbank R. T., Hatch M. D., Osmond C. B., 2001. What does it take to be C4? Lessons from the evolution of C4 photosynthesis. Plant Physiol., 125: 46–49.

    Article  PubMed  CAS  Google Scholar 

  • Ellis R. J., van der Vies S. M., 1988. The Rubisco subunit binding protein. Photosynth. Res., 16: 101–115.

    Article  CAS  Google Scholar 

  • Esau B. D., Snyder G. W., Portis A. R. Jr., 1996. Differential effects of N and C terminal deletions on the two activities of Rubisco activase. Arch. Biochem. Biophys., 326: 100–105.

    Article  PubMed  CAS  Google Scholar 

  • Feller U., Crafts-Brandner S., Salvucci M. E., 1998. Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/oxy-genase (Rubisco) activase mediated activation of Rubisco. Plant Physiol., 116: 539–546.

    Article  CAS  PubMed  Google Scholar 

  • Gatenby A. A., Ellis, R. J., 1990. Chaperone function: The assembly of ribulose bisphosphate carboxylase-oxygenase. Annu. Rev. Cell. Biol., 6: 125–149.

    Article  PubMed  CAS  Google Scholar 

  • Gatenby A. A., Lubben T. H., Ahlquist P., Keegstra K., 1988. Imported large subunits of ribulosebisphosphate carboxylase/oxygenase, but not imported ß-ATP synthase subunits, are assembled into a holoenzyme in isolated chloroplasts. EMBO J., 7: 1307–1314.

    PubMed  CAS  Google Scholar 

  • Gatenby A. A., Viitanen P. V., 1994. Structural and functional aspects of chaperonin-mediated protein folding. Annu. Rev. Plant Physiol. Plant Mol. Biol., 45: 469–491.

    Article  CAS  Google Scholar 

  • Georgieva K., 1999. Some mechanisms of damage and acclimation of the photosynthetic apparatus due to high temperature. Bulg. J. Plant Physiol., 25: 89–99.

    CAS  Google Scholar 

  • Georgieva K., Brugnoli E., 2002. Influence of high temperature on the photosynthetic apparatus. Adv. Plant Physiol., 4: 57–74.

    Google Scholar 

  • Ghosh S., Gepstein S., Glick B. R., Heikkila J. J., Dumbroff E. B., 1989. Thermal regulation of phosphoenolpyruvate carboxylase and ribulose-1,5-bisphosphate carboxylase in C3 and C4 plants native to hot and temperature climates. Plant Physiol., 90: 1298–1304.

    PubMed  CAS  Google Scholar 

  • Gutteridge S., Gatenby A. A., 1995. Rubisco synthesis, assembly, mechanism, and regulation. Plant Cell, 7: 809–819.

    Article  PubMed  CAS  Google Scholar 

  • Havaux M., 1993. Rapid photosynthetic adaptation to heat stress triggered in potato leaves by moderately elevated temperatures. Plant Cell Physiol., 35: 757–766.

    Google Scholar 

  • Havaux M., Tardy F., 1996. Temperature-dependent adjusment of thethermal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments. Planta, 198: 324–333.

    Article  CAS  Google Scholar 

  • Havaux M., Tardy F., Ravenel J., Chanu D., Parot P., 1996. Thylakoid membrane stability to heat stress studied by flash spectroscopic measurements of the electrochromic shift in intact potato leaves: influence of the xanthophyll content. Plant Cell Environ., 19: 1359–1368.

    Article  CAS  Google Scholar 

  • He Z., von Caaemmerer S., Hudson G. S., Price G. D., Badger R., Andrews T. J., 1997. Ribulose-1,5-bisphosphate carboxylase/oxygenase activase deficiency delays senescence of ribulose-1,5-bisphosphate carboxylase/oxygenase but progressively impairs its catalysis during tobacco leaf development. Plant Physiol., 115: 1569–1580.

    Article  PubMed  CAS  Google Scholar 

  • Hemmingsen S. M., Ellis R. J., 1986. Purification and properties of ribulose bisphosphate carboxylase large subunit binding protein. Plant Physiol., 80: 269–276.

    PubMed  CAS  Google Scholar 

  • Hemmingsen S. M., Woolford C., van der Vies S., Tilly K., Dennis D. T., Georgopoulos C. P., Hendrix R. W., Ellis R. J., 1988. Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature, 333: 330–334.

    Article  PubMed  CAS  Google Scholar 

  • Hendrick J. P., Hartl F.-U., 1993. Molecular chaperone functions of heat shock proteins. Annu. Rev. Biochem., 62: 349–384.

    Article  PubMed  CAS  Google Scholar 

  • Herrmann B., Feller U., 1998. CO2, light and temperature influence senescence and protein degradation in wheat leaf segments. Physiol. Plant., 103: 320–326.

    Article  CAS  Google Scholar 

  • Herrmann B., Holzer R., Crafts-Brandner S. J., Feller U., 1998. Effects of CO2, light and temperature on Rubisco activase protein in wheat leave segments. In: Photosynthesis: Mechanisms and Effects, ed. by G. Garab, Kluwer Academic Publishers, Dordrecht-Boston-London, Vol. III: 2059–2062.

    Google Scholar 

  • Holbrook G. P., Galasinski S. C., Salvucci M. E., 1991. Regulation of 2-carboxyarabinitol 1-phosphatase. Plant Physiol., 97: 894–899.

    PubMed  CAS  Google Scholar 

  • Huang B., Gao H., 2000. Growth and carbohydrate metabolism of creeping bentgrass cultivars in response to increasing temperatures. Crop. Sci., 40: 1115–1120.

    Article  Google Scholar 

  • Huang B., Liu X., Fry J. D., 1998. Effects of high temperature and poor soil aeration on root growth and viability of creeping bentgrass. Crop. Sci., 38: 1618–1622.

    Article  Google Scholar 

  • Ishida H., Nishimori Y., Sugisawa M., Makino A., Mae T., 1997. The large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase is fragmented into 37-kDa and 16-kDa polypeptides by active oxygen in the lysates of chloroplasts from primary leaves of wheat. Plant Cell Physiol., 38(4): 471–479.

    PubMed  CAS  Google Scholar 

  • Jagtab V., Bhargava S., Streb P., Feierabend J., 1998. Comparative effect of water, heat and light stresses on photosynthetic reactions in Sorghum bicolor (L.) Moench. J. Exp. Bot., 49: 1715–1721.

    Article  Google Scholar 

  • Jordan D. B., Ogren W. L., 1984. The CO2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase: dependence on ribulose-bisphosphate concentration, pH and temperature. Planta, 161: 308–313.

    Article  CAS  Google Scholar 

  • Kobza J., Edwards G., 1987. Influence of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiol., 83: 69–74.

    PubMed  CAS  Google Scholar 

  • Kovács E., van der Vies S. M., Glatz A., Török Z., Varvasovzki V., Horváth I., Vígn L., 2001. The chaperonins of Synechocystis PCC 6803 differ in heat inducibility and chaperone activity. Biochem. Biophys. Res. Comm., 289: 908–915.

    Article  PubMed  CAS  Google Scholar 

  • Kyle D. J., 1987. The biochemical basis for photo-inhibition of photosystem II. In: Photoinhibition, ed. by D. J. Kyle, C. B. Osmond, C. J Arntzen., Elsevier, Amsterdam: 197–226.

    Google Scholar 

  • Law R., Crafts-Brandner S., 1999. Inhibition of acclimation of photosynthesis to heat stress is closely correlated with activation of Rubisco. Plant Physiol., 120: 173–181.

    Article  CAS  PubMed  Google Scholar 

  • Law R., Crafts-Brandner S., 2001. High temperature stress increases the expression of wheat leaf ribulose-1,5-bisphosphate carboxylase/oxygenase activase protein. Arch. Biochem. Biophys., 386(2): 261–267.

    Article  PubMed  CAS  Google Scholar 

  • Law R. D., Crafts-Brandner S. J., Salbvucci M. E., 2001. Heat stress induces the synthesis of a new form of ribulose-1,5-bisphosphate carboxylase/oxygenase activase in cotton leaves. Planta, 214(1): 117–125.

    Article  PubMed  CAS  Google Scholar 

  • Lormer G. H., 1981. The carboxylation and oxygenation of ribulose1,5-bisphosphate: The primary events in photosynthesis and photorespiration. Annu. Rev. Plant Physiol. 32: 349–383.

    Article  Google Scholar 

  • Luben T. H., Donaldson G. K., Vitanen P. V., Gatenby A. A., 1989. Several proteins imported into chloroplasts from stable complexes with the GroEL-related chlorplast molecular chaperone. The Plant Cell, 1: 1223–1230.

    Article  Google Scholar 

  • Mae T., Makino A., Ohira K., 1983. Changes in amount ribulose-1,5-bisphosphate carboxylase synthesized and degraded during life span of rice leaf (Oryza sativa L.). Plant Cell Physiol., 24: 1079–1086.

    CAS  Google Scholar 

  • Makino A., Nakano H., Mae T., 1994. Effects of growth temperature on responses of ribulose-1,5-bisphosphate carboxylase, electron transport components, and sucrose synthesis enzymes to leaf nitrogen in rice, and their relationships to photosynthesis. Plant Physiol., 105: 1231–1238.

    PubMed  CAS  Google Scholar 

  • Martel R., Cloney L. P., Pelcher L. E., Hemmingsen S. M., 1990. Unique composition of plastid chaperonin-60: a and b polypeptide-encoding genes are highly divergent. Gene, 94: 181–187.

    Article  PubMed  CAS  Google Scholar 

  • Mate C. J., Hudson G. S., von Caemmerer S., Evans J. R., Andrews T. J., 1993. Reduction of ribulose bisphosphate carboxylase activase levels in tobacco (Nicotiana tabacum) by antisense RNA reduces ribulose bisphosphate carboxylase carbamylation and impairs photosynthesis. Plant Physiol., 102: 1119–1128.

    Article  PubMed  CAS  Google Scholar 

  • Musgrove J. E.,, Johnson R. A., Ellis R. J., 1987. Disociating of the ribulose bisphosphate carboxylase large subunit binding protein into dissimilar subunits. Eur. J. Biochem., 163: 529–534.

    Article  PubMed  CAS  Google Scholar 

  • Portis A. R. Jr., Salvucci M. E. Ogren W. L., 1986. Activation of ribulosebisphosphate carboxylase/oxygenase at physiological CO2 and ribulosebisphosphate concentrations by Rubisco activase. Plant Physiol., 82: 967–971.

    PubMed  CAS  Google Scholar 

  • Powles S. B., 1984. Photoinhibition of photosynthesis induced by visible light. Annu. Rev. Plant Physiol., 35: 15–44.

    Article  CAS  Google Scholar 

  • Robinson S. P., Portis A. R. Jr., 1988. Release of the nocturnal inhibitor, carboxyarabinitol-phosphate, from ribulose bisphosphate carboxylase/ oxygenase by Rubisco activase. FEBS Lett., 233: 413–416.

    Article  CAS  Google Scholar 

  • Robinson S. P., Portis A. R. Jr., 1989. Adenosine triphosphate hydrolysis by purified Rubisco activase. Arch. Biochem. Biophys., 268: 93–99.

    Article  PubMed  CAS  Google Scholar 

  • Rokka A., Zhang L. X., Aro E. M., 2001. Rubisco activase: an enzyme with a temperature-dependent dual function? Plant J., 25: 463–471.

    Article  PubMed  CAS  Google Scholar 

  • Roy H., 1989. Rubisco assembly: a model system for studying the mechanism of chaperonin action. Plant Cell, 1: 1035–1042.

    Article  PubMed  CAS  Google Scholar 

  • Roy H., Hubbs A., Cannon S., 1988. Stability and dissociation of the large subunit Rubisco binding protein complex in vitro and in organello. Plant Physiol., 86: 50–53.

    PubMed  CAS  Google Scholar 

  • Sage R. F., Sharkey T. D., 1987. The effect of temperature on the occurrence of O2 and CO2 insensitive photosynthesis in field grown plants. Plant Physiol., 84: 658–664.

    PubMed  CAS  Google Scholar 

  • Salvucci M. E., 1992. Subunit interactions of Rubisco activase: polyethylene glycol promotes self-association, stimulates ATPase and activation activities, and enhances interactions with Rubisco. Arch. Biochem. Biophys., 298: 688–696.

    Article  PubMed  CAS  Google Scholar 

  • Savucci M. E., 1993. Covalent modification of a highly reactive and essential lysine residue of ribulose-1,5-bisphosphate carboxylase — oxygenase activase. Plant Physiol., 103: 501–508.

    Article  Google Scholar 

  • Salvucci M. E, Ogren W. L., 1996. The mechanism of Rubisco activase: Insights from studies of the properties and structure of the enzyme. Photosynth. Res., 47: 1–11.

    Article  CAS  Google Scholar 

  • Salvucci M. E., Osteryoung K. W., Crafts-Brandner S. J., Vierling E., 2001. Exceptional sensitivity of rubisco activase to thermal denaturatiion in vitro and in vivo. Plant Physiol., 127: 1053–1064.

    Article  PubMed  CAS  Google Scholar 

  • Salvucci M. E., Portis A. R., Ogren W. L., 1985. A soluble chloroplast protein catalyses ribulosebisphosphate carboxylase — oxygenase activation in vivo. Photosynth. Res., 7: 193–201.

    Article  CAS  Google Scholar 

  • Salvucci M. E., Portis A. R. Jr., Ogren W. L., 1986. Light and CO2 response of ribulose-1,5-bisphosphate carboxylase/oxygenase activation in Arabidopsis leaves. Plant Physiol., 80: 655–659.

    PubMed  CAS  Google Scholar 

  • Salvucci M. E., Werneke J. M., Ogren W. L., Portis A. R. Jr., 1987. Purification and species distributuion of Rubisco activase, Plant Physiol. 84: 930–36.

    PubMed  CAS  Google Scholar 

  • Sánchez de Jiménez E., Medrano L., Martinez-Barajas E., 1995. Rubisco activase, a possible new member of the molecular chaperone family. Biochemistry, 34: 2826–2831.

    Article  PubMed  Google Scholar 

  • Schmitz G., Schmidt M., Feierabend J., 1996. Comparison of the expression of a plastic chaperonin 60 in different plant tissue and under photosynthetic and non photosynthetic conditions. Planta, 200: 326–334.

    Article  PubMed  CAS  Google Scholar 

  • Sharkey T. D., Badger M. R., von Caemmerer S., Andrews T. J., 2001. Increased heat sensitivity of photosynthesis in tobacco plants with reduced Rubisco activase. Photosynthesis Research. 67: 147–156.

    Article  PubMed  CAS  Google Scholar 

  • Somers D. J., Cummis W. R., Filion W. G., 1989. Characterization of heatshock response in spinach (Spinacia oleracea L.). Biochem. Cell Biol., 67: 113–120.

    Article  CAS  Google Scholar 

  • Somerville C. R., Portis A. R. Jr., Ogren W. L., 1982. A mutant of Arabidopsis thaliana which lacks activation of RuBP carboxylase in vivo. Plant Physiol., 70, 381–387.

    PubMed  CAS  Google Scholar 

  • Spiess Ch., Beil A., Ehrmann M., 1999. A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell, 97: 339–347.

    Article  PubMed  CAS  Google Scholar 

  • Spreitzer R. J., Salvucci M., 2002. Rubisco: Structure, regulatory interactions, and possibilities for better enzyme. Annu. Rev. Plant Biol., 53: 449–75.

    Article  PubMed  CAS  Google Scholar 

  • Vierling E., 1991. The roles of heat shock proteins in plants. Annu. Rev. Plant Physiology Plant Mol. Biol., 42: 579–620.

    Article  CAS  Google Scholar 

  • Vierling E., Key J. K., 1985. Ribulose-1,5-bisphosphate carboxylase synthesis during heat shock. Plant Physiol., 78: 155–162.

    PubMed  CAS  Google Scholar 

  • von Caemmerer S., Millgate A., Farquhar G. D., Furbank R. T., 1997. Reduction of ribulose-1,5-bisphosphate carboxylase/oxygenase by by antisense RNA in the C4 plant leads to reduced assimilation rates and increased carbon isotope discrimination. Plant Physiol., 1113: 469–477.

    Google Scholar 

  • Wang Z-Y., Snyder G. W., Esau B. D., Portis A. R. Jr., Ogren W. L., 1992. Species dependent variation in the interaction of substrate-bound ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and Rubisco activase. Plant Physiol., 100: 1856–1862.

    Google Scholar 

  • Weis E., 1981a. Reversible heat-inactivation of the Calvin cycle: a possible mechanism of the temperature regulation of photosynthesis. Planta, 151: 33–39.

    Article  CAS  Google Scholar 

  • Weis E., 1981b. The temperature sensitivity of dark-inactivation and light-inactivation of the ribulose-1,5-bisphosphate carboxylase in spinach chloroplasts. FEBS Lett., 129: 197–200.

    Article  CAS  Google Scholar 

  • Wittenbach V. A., Lin W., Herbert R. R., 1982. Vacuolar localization of proteases and degradation of chloroplasts in mesophyll protoplasts from senescing primary wheat leaves. Plant Physiol., 69: 98–102.

    Article  PubMed  CAS  Google Scholar 

  • Xu Q. Z., Huang B. R., 2001. Morphological and physiological characteristics associated with heat tolerance in creeping bentgrass. Crop Sci., 41: 127–133.

    Article  Google Scholar 

  • Yordanov I. S., Dilova S., Petkova R., Pangelova T., Goltsev V., K.-H. Süss, 1986. Mechanisms of the temperature damage and acclimation of the photosynthetic apparatus. Photobiochem. Photobiophys., 12: 147–155.

    Google Scholar 

  • Zhu G., Jensen R. G., Bohnert H. J., Wildner G. F., Schlitter J., 1998. Dependence of catalysis and CO/O specificity of Rubisco on the carboxylase of the large subunit at different temperatures. Photosynth. Res., 40: 219–228.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Demirevska-Kepova, K., Feller, U. Heat sensitivity of Rubisco, Rubisco activase and Rubisco binding protein in higher plants. Acta Physiol Plant 26, 103–114 (2004). https://doi.org/10.1007/s11738-004-0050-7

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-004-0050-7

Key words

Navigation