Skip to main content
SpringerLink
Log in

Reduced levels of cytochrome bf complex in transgenic tobacco leads to marked photochemical reduction of the plastoquinone pool, without significant change in acclimation to irradiance

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Tobacco transgenics with decreased amounts of the FeS apoprotein were generated using an antisense RNA construct targeted against the nuclear-encoded Rieske FeS protein of cytochrome bf complex [Price et al. (1995) Aust J Plant Physiol 22: 285–297]. FeS phenotypes ranging from intermediate to low were obtained which had 69% and 26% of the Rieske FeS protein of wild type. Similar reductions in the other subunits of cytochrome bf complex, cytochrome f, cytochrome b563and the 17 kDa subunit, were demonstrated in the thylakoids of intermediate and low FeS phenotypes. Confirmation that the levels of assembled cytochrome bf in leaves matched the levels of the FeS protein was demonstrated by laser flash-induced redox absorbance changes in leaves, with the extents of cytochrome f oxidation and cytochrome b563reduction being equivalent to the decreased amounts of the subunits in isolated thylakoids of the antisense plants. Despite greatly enhanced photochemical reduction of QAand the plastoquinone pool in the antisense plants, light acclimation of the FeS phenotypes to irradiance did not occur. Furthermore, the state 1–state 2 transitions were identical in wild type and antisense plants. Our results suggest that neither QAnor the plastoquinone pool acts alone in either the redox control of gene expression or the regulation of light energy distribution between the photosystems. We suggest rather that reduced plastoquinone acting at the inner Qpsite of cytochrome bf complex is involved in molecular redox signalling.

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

References

  • Allen JF (1995) Thylakoid protein phosphorylation, state 1-state 2 transitions, and photosystem stoichiometry adjustment: Redox control at multiple levels of gene expression. Physiol Plant 93: 196-205

    Article  Google Scholar 

  • Allen JF, Alexciev K and Håkansson G (1995) Regulation by redox signalling. Current Biol 5: 869-872

    Google Scholar 

  • Anderson JM (1992) Cytochrome b 6/fcomplex: Dynamic molecular organization, function and acclimation. Photosynth Res 34: 341-357

    Google Scholar 

  • Anderson JM and Osmond CB (1987) Shade-sun responses: Compromises between acclimation and photoinhibition. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Photoinhibition, pp 1-38. Elsevier, Amsterdam

    Google Scholar 

  • Anderson JM, Chow WS and Park Y-I (1995) The grand design of photosynthesis: Acclimation of the photosynthetic apparatus to environmental cues. Photosynth Res 46: 129-139

    Google Scholar 

  • Barkan A, Miles D and Taylor WC (1986) Chloroplast gene expression in nuclear photosynthetic mutants of maize. EMBO J 5: 1421-1427

    PubMed  Google Scholar 

  • Bendall DS, Davenport HE and Hill R (1971) Cytochrome components in chloroplasts of higher plants. Meth Enzymol 23: 327-344

    Google Scholar 

  • Bennett J (1991) Protein phosphorylation in green plant chloroplasts. Annu Rev Plant Physiol Plant Mol Biol 42: 281-311

    Article  Google Scholar 

  • Bruce BD and Malkin R (1991) Biosynthesis of the chloroplast cytochrome b 6/fcomplex: Studies in a photosynthetic mutant of Lemna. The Plant Cell 3: 203-212

    PubMed  Google Scholar 

  • Buchanan BB (1991) Regulation of CO2assimilation in oxygenic photosynthesis: The ferredoxin-thioredoxin system. Arch. Biochem Biophys 228: 1-9

    Google Scholar 

  • Chow WS and Hope AB (1987) The stoichiometries of supramolecular complexes in thylakoid membranes from spinach chloroplasts. Aust J Plant Physiol 14: 21-28

    Google Scholar 

  • Chow WS, Goodchild DJ, Miller C and Anderson JM (1990a) The influence of high levels of brief or prolonged supplementary farred illumination during growth on the photosynthetic characteristics, composition and morphology of Pisum sativumchloroplasts. Plant Cell Environ 13: 135-145

    Google Scholar 

  • Chow WS, Haehnel W and Anderson JM (1987) The composition and function of thylakoid membranes from pea plants grown under white or green light with or without far-red light. Physiol Plant 70: 196-202

    Google Scholar 

  • Chow WS, Hope AB and Anderson JM (1990b) A reassessment of the use of herbicide binding to measure Photosystem II reaction centres in plant thylakoids. Photosynth Res 24: 109-113

    Google Scholar 

  • Chow WS, Melis A and Anderson JM (1990c) Adjustments of photosystem stoichiometry in chloroplasts improve the quantum effeciency of photosynthesis. Proc Natl Acad Sci USA 87: 7502-7506

    PubMed  Google Scholar 

  • Cramer WA, Soriano GM, Ponomarev M, Huang D, Zhang H, Martinez SE and Smith JL (1996) Some new structural aspects and old controversies concerning the cytochrome b 6/fcomplex of oxygenic photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 47: 477-508

    PubMed  Google Scholar 

  • Danon A and Mayfield SP (1994) Light-regulated translation of chloroplast mRNAs through redox potential. Science 266: 1717-1719

    PubMed  Google Scholar 

  • Escoubas J-M, Lomas M, LaRoche J and Falkowski PG (1995) Light intensity regulation of cabgene transcription is signaled by the redox state of the plastoquinone pool. Proc Natl Acad Sci USA 92: 10237-10241

    Google Scholar 

  • Evans JR (1987) The relationship between electron transport components and photosynthetic capacity in pea leaves grown at different irradiances. Aust J Plant Physiol 14: 157-170

    Google Scholar 

  • Frid D, Gal A, Oettmeier W, Hauska G, Berger S and Ohad I (1987) The redox-controlled light-harvesting chlorophyll a/bkinase. Deactivation by substituted quinones. J Biol Chem 267: 25908-25915

    Google Scholar 

  • Fujita Y and Murakami A (1987) Regulation of electron transport composition in cyanobacterial photosynthetic system: stoichiometry among Photosystem I and II complexes and their light-harvesting antennae and cytochrome b 6/fcomplex. Plant Cell Physiol 28: 1547-1553

    Google Scholar 

  • Fujita Y, Murakami A and Ohki K (1987) Regulation of photosystem composition in the cyanobacterial photosynthetic system: The regulation occurs in response to the redox state of the electron pool located between the two photosystems. Plant Cell Physiol 28: 283-292

    Google Scholar 

  • Gal A, Herrmann RG, Lotspeich F and Ohad I (1992) Phosphorylation of cytochrome b 6by the LHC II kinase associated with the cytochrome complex. FEBS Lett 298: 33-35

    PubMed  Google Scholar 

  • Genty B, Briantais J-M and Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 990: 87-92

    Google Scholar 

  • Hope AB, Huilgol RR, Panizza M, Thompson M and Matthews DB (1992) The flash-induced turnover of cytochrome b-563, cytochrome fand plastocyanin in chloroplasts. Models and estimation of kinetic parameters. Biochim Biophys Acta 1100: 15-26

    Google Scholar 

  • Huner NPA, Maxwell DP, Gray GR, Savitch LV, Krol M, Ivanov AG and Falk S (1996) Sensing environmental temperature change through imbalances between energy supply and energy consumption: Redox state of Photosystem II. Physiol Plant 98: 358-364

    Article  Google Scholar 

  • Hurry V, Anderson JM, Price GD and Badger MR (1997) Reduced levels of cytochrome b 6/fcomplex in transgenic tobacco increases excitation pressure without increasing sensitivity to photoinhibition in vivo. Photosynth Res 50: 159-169

    Google Scholar 

  • Kim JH, Glick RD and Melis A (1993) Dynamics of photosystem stoichiometry adjustment by light quality in chloroplasts. Plant Physiol 102: 181-189

    PubMed  Google Scholar 

  • Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 509-540

    Article  PubMed  Google Scholar 

  • Lam E and Malkin R (1985) Characterization of a photosynthetic mutant of Lemnaby another approach. Biochim Biophys Acta 810: 106-109

    PubMed  Google Scholar 

  • Maxwell DP, Laudenbach DE and Huner NPA (1995) Redox regulation of light-harvesting complex II and cabmRNA abundance in Dunaliella salina. Plant Physiol 109: 787-795

    PubMed  Google Scholar 

  • Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058: 87-106

    Google Scholar 

  • Melis A, Murakami A, Nemson JA, Aizawa K, Ohki K and Jujita Y (1996) Chromatic regulation in Chlamydomonas reinhardtiialters photosystem stoichiometry and improves the quantum efficiency of photosynthesis. Photosynth Res 47: 253-265

    Google Scholar 

  • Metz JG, Miles D and Rutherford AW (1983) Characterization of nuclear mutants that lack the cytochrome f/b-563 complex. Plant Physiol 73: 452-459

    Google Scholar 

  • Miles D (1982) The use of mutations to probe photosynthesis in higher plants. In: Edelman E, Hallick RB and Chua N-H (eds) Methods in Chloroplast Molecular Biology, pp 75-107. Elsevier Biomedical Press, Amsterdam

    Google Scholar 

  • Pearson CK, Wilson SB, Schaffer R and Ross AW (1993) NAD turnover and utilisation of metabolites for RNA synthesis in a reaction sensing the redox state of the cytochrome b 6/fcomplex in isolated chloroplasts. Eur J Biochem 218: 397-404

    PubMed  Google Scholar 

  • Porra RJ, Thompson WA and Kriedemann PE (1989) Determination of accurate coefficients and simultaneous equations for assaying chlorophylls aand bextracted with four different solvents: Verification of the chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975: 384-394

    Google Scholar 

  • Price GD, Yu J-W, von Caemmerer S, Evans JR, Chow WS, Anderson JM, Hurry V and Badger MR (1995) Chloroplast cytochrome b 6/fand ATP synthase complexes in tobacco: Transformation with antisense RNA against nuclear-encoded transcripts for the Rieske FeS and ATP δ-polypeptides. Aust J Plant Physiol 22: 285-297

    Google Scholar 

  • Rich PR, Heathcote P and Moss DA (1987) Kinetics of electron transfer in a hybrid system constructed from the cytochrome bfcomplex and Photosystem I. Biochim Biophys Acta 892: 138-151

    Google Scholar 

  • Silverstein T, Cheng L and Allen JF (1993) Redox titration of multiple protein phosphorylation in pea chloroplast thylakoids. Biochim Biophys Acta 11893: 215-220

    Google Scholar 

  • Stitt M, Krapp A, Klein D, Roper-Schwarz U and Paul D (1995) Do carbohydrates regulate photosynthesis and allocation by altering gene expression? In: Madore MM and Lucas WL (eds) Carbon Partitioning and Source Sink Interactions in Plants, pp 68-77. Am Soc Plant Physiol, Rockville, MD

    Google Scholar 

  • Stubbe W and Herrman RG (1982) Selection and maintenence of plastome mutants and interspecific genome/plastome hybrids in Oenethera. In: Edelman E, Hallick RB and Chua N-H (eds) Methods in chloroplast Molecular Biology, pp 149-165. Elsevier Biomedical Press, Amsterdam

    Google Scholar 

  • van Kooten O and Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25: 147-150

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Cooperative Research Centre for Plant Science, Research School of Biological Sciences, Australia

    Jan M. Anderson, Wah Soon Chow, Alex B. Hope & Murray R. Badger

  2. Csiro, Plant Industry, GPO Box 1600, Canberra, ACT, 2601, Australia

    Jan M. Anderson

  3. Research School of Biological Sciences, Institute of Advanced Studies, Australian National University, GPO Box 475, Canberra, ACT, 2601, Australia

    G. Dean Price, Wah Soon Chow & Murray R. Badger

Authors
  1. Jan M. Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Dean Price
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wah Soon Chow
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alex B. Hope
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Murray R. Badger
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Anderson, J.M., Dean Price, G., Soon Chow, W. et al. Reduced levels of cytochrome bf complex in transgenic tobacco leads to marked photochemical reduction of the plastoquinone pool, without significant change in acclimation to irradiance. Photosynthesis Research 53, 215–227 (1997). https://doi.org/10.1023/A:1005856615915

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1005856615915

Search

Navigation