Skip to main content
SpringerLink
Log in

Occurrence of the 32-kDa QB-binding protein of photosystem II in vegetative cells, heterocysts and akinetes ofAzolla carotiniana cyanobionts

  • Published:
Planta Aims and scope Submit manuscript

Abstract

Transmission electron microscopy and immunocytological labeling were used to localize the 32-kilodalton (kDa) protein (DI polypeptide) of photosystem II in different cell types of the cyanobionts within leaf cavities ofAzolla caroliniana Willd. The 32-kDa protein binds the secondary electron acceptor QB, and is highly conserved between plants and cyanobacteria. Three antisera, specific for different epitopes of the 32-kDa protein, were used as primary antibodies. Immunologically recognizable 32-kDa protein was localized on membranes ofAzolla chloroplasts, vegetative cyanobacterial cells, akinetes, and heterocysts that were at all stages of the differentiation process. The 32-kDa protein was not detected in nonphotosynthetic endosymbiotic bacteria found within leaf cavities. The amount of the 32-kDa protein observed in different cyanobacterial cell types was dependent upon the primary antiserum used and membrane orientation within a cell with respect to the plane of sectioning. Therefore, although 32-kDa protein was present in all three cyanobacterial cell types and clear trends in labeling patterns could be elucidated, it was not possible to quantitate the amounts of protein with respect to either cell type or leaf-cavity age.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

Ab:

antibody

kDa:

kilodalton(s)

PSII:

photosystem II

References

  • Adams, D.G., Carr, N. (1981) The developmental biology of heterocyst and akinete formation in cyanobacteria. CRC Crit. Rev. Microbiol.9, 45–100

    Google Scholar 

  • Alberte, R.S., Tel-Or, E., Packer, L., Thornber, J.P. (1980) Functional organization of the photosynthetic apparatus in heterocysts of nitrogen-fixing cyanobacteria. Nature284, 481–483

    Google Scholar 

  • Allen, M.M., Turnburke, A.C., Lagace, E.A., Steinback, K.E. (1983) Effects of photosystem II herbicides on the photosynthetic membranes of the cyanobacteriumAphanocapsa 6308. Plant Physiol.71, 388–392

    Google Scholar 

  • Almon, H., Böhme, H. (1980) Components and activity of the photosynthetic electron transport system of intact heterocysts isolated from the blue-green algaNostoc muscorum. Biochim. Biophys. Acta592, 113–120

    Google Scholar 

  • Arntzen, C.J., Darr, S.C., Mullet, J.E., Steinback, K.E., Pfister, K. (1982) Polypeptide determinants of plastoquinone function in photosystem II in chloroplasts. In: Functions of quinones in energy conserving systems, pp. 443–452, Trumpower, B., ed. Academic Press, New York

    Google Scholar 

  • Becking, J.H. (1987) Endophyte transmission and activity in theAnabaena-Azolla association. Plant Soil100, 183–212

    Google Scholar 

  • Becking, J.H., Donze, M. (1981) Pigment distribution and nitrogen fixation inAnabaena azollae. Plant Soil61, 203–226

    Google Scholar 

  • Bergman, B., Lindblad, P., Rai, A.N. (1986) Nitrogenase in freeliving and symbiotic cyanobacteria: immunoelectron microscopic localization. FEMS Microbiol. Lett.35, 75–78

    Google Scholar 

  • Bradley, S., Carr, N.G. (1971) The absence of a functional photosystem II in heterocysts ofAnabaena cylindrica. J. Gen. Microbiol.68, xiii

    Google Scholar 

  • Braun-Howland, E.B., Nierzwicki-Bauer, S.A. (1990) Biochemistry, physiology, ultrastructure and molecular biology of theAzolla-Anabaena symbiosis. In: Handbook of symbiotic cyanobacteria, pp. 65–117, Rai, A.N., ed. CRC Press, Boca Raton, Fla., USA

    Google Scholar 

  • Braun-Howland, E.B., Lindblad, P., Nierzwicki-Bauer, S.A., Bergman, B. (1988) Dinitrogenase reductase (Fe-protein) of nitrogenase in the cyanobacterial symbionts of threeAzolla species: Localization and sequence of appearance during heterocyst differentiation. Planta176, 319–332

    Google Scholar 

  • Bühler, T., Sann, R., Monter, U., Dingler, C., Kuhla, J., Oelze, J. (1987) Control of dinitrogen fixation in ammonium-assimilating cultures ofAzotobacter vinelandii. Arch. Microbiol.148, 247–251

    Google Scholar 

  • Curtis, S.E., Haselkorn, R. (1984) Isolation, sequence and expression of two members of the 32 kDa thylakoid membrane protein gene family from the cyanobacterumAnabaena 7120. Plant Mol. Biol.3, 249–258

    Google Scholar 

  • Donze, M., Haveman, J., Schiereck, P. (1972) Absence of photosystem 2 in heterocysts of the blue-green algaAnabaena. Biochim. Biophys. Acta256, 157–161

    Google Scholar 

  • Fay, P., Cox, R.M. (1967) Oxygen inhibition of nitrogen fixation in cell-free preparations of blue-green algae. Biochim. Biophys. Acta143, 562–569

    Google Scholar 

  • Golden, S.S., Haselkorn, R. (1985) Mutation to herbicide resistance maps within the psbA gene ofAnacystis nidulans R2. Science229, 1104–1107

    Google Scholar 

  • Golden, J.W., Robinson, S.J., Haselkorn, R. (1985) Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacteriumAnabaena. Nature314, 419–423

    Google Scholar 

  • Goloubinoff, P., Brusslan, J., Golden, S.S., Haselkorn, R., Edelman, M. (1988) Characterization of the photosystem II 32 kDa protein inSynechococcus PCC7942. Plant Mol. Biol.11, 441–447

    Google Scholar 

  • Haselkorn, R., Curtis, S.E., Golden, J.W., Nierzwicki-Bauer, S.A., Robinson, S.J., Tumer, N.E. (1984) Organization and transcription ofAnabaena genes regulated during heterocyst differentiation. In: Molecular form and function of the plant genome, pp. 443–453, Van Vloten-Doting, L., Groot, G.S.P., Hall, T.C., eds. Plenum Press, New York

    Google Scholar 

  • Herdman, M. (1987) Akinetes: structure and function. In: The Cyanobacteria, pp. 227–250, Fay, P., Van Baalen, C., eds. Elsevier, Amsterdam

    Google Scholar 

  • Hill, D.J. (1975) The pattern of development ofAnabaena in theAzolla-Anabaena symbiosis. Planta122, 179–184

    Google Scholar 

  • Hill, D.J. (1977) The role ofAnabaena in theAzolla-Anabaena symbiosis. New Phytol.78, 611–616

    Google Scholar 

  • Hoffman-Falk, H., Mattoo, A.K., Marder, J.B., Edelman, M., Ellis, J. (1982) General occurrence and structural similarity of the rapidly synthesized, 32000-dalton protein of the chloroplast membrane. J. Biol. Chem.257, 4583–4587

    Google Scholar 

  • Jansson, C., Debus, R.J., Osiewacz, H.D., Gurevitz, M., McIntosh, L. (1987) Construction of an obligate photoheterotrophic mutant of the cyanobacteriumSynechocystis 6803. Plant Physiol.85, 1021–1025

    Google Scholar 

  • Kaplan, D., Peters, G.A. (1988) Interaction of carbon metabolism in theAzolla-Anabaena symbiosis. Symbiosis6, 53–68

    Google Scholar 

  • Leach, C.K., Carr, N.G. (1974) In vitro protein synthesis and measurement of the stability of messenger RNA in the blue-green algaAnabaena variabilis. J. Gen. Microbiol.81, 47–58

    Google Scholar 

  • Lönneborg, A., Kalla, S.R., Samuelsson, G., Gustafsson, P., Oquist, G. (1988) Light-regulated expression of the psbA transcript in the cyanobacteriumAnacystis nidulans. FEBS Lett.240, 110–114

    Google Scholar 

  • Mattoo, A.K., Pick, U., Hoffman-Falk, H., Edelman, M. (1981) The rapidly metabolized 32000 dalton polypeptide of the chloroplast is the proteinaceous shield regulating photosystem II electron transport and mediating diuron herbicide sensitivity in chloroplasts. Proc. Natl. Acad. Sci. USA78, 1572–1576

    Google Scholar 

  • Mei, R., Green, J.P., Sayre, R.T., Frasch, W.D. (1989) Manganesebinding proteins of the oxygen-evolving complex. Biochem.28, 5560–5567

    Google Scholar 

  • Mörschel, E., Rheil, E. (1987) Phycobilisomes and thylakoids: The light harvesting systems of cyanobacteria and red algae. In: Electron microscopy of proteins, vol. 6: Membranous structures, Harris, G.R., Horne, R.W., eds. Academic Press, London

    Google Scholar 

  • Mulligan, B., Schultes, N., Chen, L., Bogorad, L. (1984) Nucleotide sequence of a multiple-copy gene for the B protein of photosystem II of a cyanobacterium. Proc. Natl. Acad. Sci. USA81, 2693–2697

    Google Scholar 

  • Murry, M.A., Hallenbeck, P.C., Benemann, J.R. (1984) Immunochemical evidence that nitrogenase is restricted to the heterocysts inAnabaena cylindrica. Arch. Microbiol.137, 194–199

    Google Scholar 

  • Newton, J.W., Cavins, J.F. (1976) Altered nitrogenous pools induced by theAzolla-Anabaena azollae symbiosis. Plant Physiol.58, 798–799

    Google Scholar 

  • Newton, J.W., Tyler, D.D. (1987) Involvement of photosystem II in the ammonia metabolism of a heterotrophic cyanobacterium. Biochim. Biophys. Acta891, 49–55

    Google Scholar 

  • Nierzwicki-Bauer, S.A., Haselkorn, R. (1986) Differences in mRNA levels inAnabaena living freely or in symbiotic association withAzolla. EMBO J.5, 29–35

    Google Scholar 

  • Nierzwicki-Bauer, S.A., Aulfinger, H., Braun-Howland, E.B., Gebhardt, J.S., Padbidri, A.Y. (1990) Structural and molecular studies of theAzolla-Anabaena symbiosis. In: Int. Symp. on Biological Nitrogen Fixation, (in press), Ramchandani, I., ed. Oxford IBH Publishing Co., New Delhi, India

    Google Scholar 

  • Ohad, I. Kyle, D.J., Hirschberg, J. (1985) Light-dependent degradation of the QB-protein in isolated pea thylakoids. EMBO J.4, 1655–1659

    Google Scholar 

  • Orr, J., Haselkorn, R. (1982) Regulation of glutamine synthetase activity and synthesis in free-living and symbioticAnabaena spp. J. Bacteriol.152, 626–635

    Google Scholar 

  • Peters, G.A. (1975) TheAzolla-Anabaena azollae relationship III. Studies on metabolic capabilities and a further characterization of the symbiont. Arch. Microbiol.103, 113–122

    Google Scholar 

  • Peters, G.A., Mayne, B.C. (1974) TheAzolla-Anabaena azollae relationship. I. Initial characterization of the association. Plant Physiol.53, 813–819

    Google Scholar 

  • Peterson, R.B., Dolan, E., Calvert, H.E., Ke, B. (1981) Energy transfer from phycobiliproteins to photosystem I in vegetative cells and heterocysts ofAnabaena variabilis. Biochim. Biophys. Acta634, 237–248

    Google Scholar 

  • Ray, T.B., Peters, G.A., Toia, R.E., Jr., Mayne, B.C. (1978)AzollaAnabaena relationship. VII. Distribution of ammonia assimilating enzymes, protein, and chlorophyll between host and symbiont. Plant Physiol62, 463–467

    Google Scholar 

  • Rippka, R., Stanier, R.Y. (1978) The effects of anaerobiosis on nitrogenase synthesis and heterocyst development by Nostocacean cyanobacteria. J. Gen. Microbiol.105, 83–94

    Google Scholar 

  • Sayre, R.T., Andersson, B., Bogorad, L. (1986) The topology of a membrane protein: the orientation of the 32 kd QB-binding chloroplast thylakoid membrane protein. Cell47, 601–608

    Google Scholar 

  • Schaefer, M.R., Golden, S.S. (1989) Differential expression of members of a cyanobacterialpsbA gene family in response to light. J. Bacteriol.171, 3973–3981

    Google Scholar 

  • Sutherland, J.M., Herdman, M., Stewart, W.D.P. (1979) Akinetes of the cyanobacteriumNostoc PCC 7524: macromolecular composition, structure and control of differentiation. J. Gen. Microbiol.115, 273–287

    Google Scholar 

  • Tel-Or, E., Stewart, W.D.P. (1977) Photosynthetic components and activities of nitrogen-fixing isolated heterocysts ofAnabaena cylindrica. Proc. R. Soc. Lond.198, 61–86

    Google Scholar 

  • Thomas, J. (1970) Absence of the pigments of photosystem II of photosynthesis in heterocysts of a blue-green alga. Nature228, 181–183

    Google Scholar 

  • Watanabe, I., Espiñas, C.R., Berja, N.S., Alimaguo, B.V. (1977) The utilization of theAzolla-Anabaena complex as a nitrogen fertilizer for rice. Int. Rice Res. Inst. Paper Ser. No.11, 1–15

    Google Scholar 

  • Wealand, J.L., Myers, J.A., Hirschberg, R. (1989) Changes in gene expression during nitrogen starvation inAnabaena variabilis ATCC 29413. J. Bacteriol.171, 1309–1313

    Google Scholar 

  • Wolk, C.P. (1982) Heterocysts. In: The biology of cyanobacteria. (Bot. Monog. vol. 19) pp. 359–386, Carr, N.G., Whitton, B.A., eds. Blackwell, London

    Google Scholar 

  • Yamamoto, Y. (1975) Effect of desiccation on the germination of akinetes ofAnabaena cylindrica. Plant Cell Physiol.16, 749–752

    Google Scholar 

  • Zurawski, G., Bohnert, HJ., Whitfield, P.R., Bottomley, W. (1982) Nucleotide sequence for the M 32000 thylakoid membrane protein fromSpinacia oleracea andNicotiana debneyi predicts a totally conserved primary translation product of M 38950. Proc. Natl. Acad. Sci. USA79, 7699–7703

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Plant Research Group, Department of Biology, MRC 306, Rensselaer Polytechnic Institute, 12180-3590, Troy, NY, USA

    Ellen B. Braun-Howland & Sandra A. Nierzwicki-Bauer

Authors
  1. Ellen B. Braun-Howland
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sandra A. Nierzwicki-Bauer
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

This work was supported by Grant No. 1 RO1 GM37051-01 awarded by the National Institute of General Medical Sciences to S.A.N.-B. We are grateful to Drs. Harry Roy and Michael Hanna for helpful discussions during the course of this work. The contributions of Mrs. Mary Ann Sessions to the final draft of the manuscript are also gratefully acknowledged. Special thanks are due to Drs. J. Oelze, L. McIntosh and R. Sayre for providing the antisera used in these studies.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Braun-Howland, E.B., Nierzwicki-Bauer, S.A. Occurrence of the 32-kDa QB-binding protein of photosystem II in vegetative cells, heterocysts and akinetes ofAzolla carotiniana cyanobionts. Planta 180, 361–371 (1990). https://doi.org/10.1007/BF01160391

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01160391

Key words

Search

Navigation