Skip to main content
Log in

Chloroplast redox regulation of nuclear gene transcription during photoacclimation

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The role of the redox state of ferredoxin/thioredoxin within the chloroplast is well established for the feedback regulation of enzyme activity in the Calvin cycle. However, evidence has emerged also suggesting that chloroplast electron transport components regulate plastid and nuclear gene expression. Using the unicellular green alga, Dunaliella tertiolecta, as a model organism, we have shown that the cell acclimates to changes in growth irradiance by altering the abundance and activities of photosynthetic components, in particular the light harvesting complexes (LHC). Pharmacological data suggests that light intensity is sensed through the redox status of the plastoquinone pool leading to the regulation of nuclear encoded genes, such as Lhcb. This signal may be transduced through a redox regulated protein kinase that (in)directly interacts with the nuclear transcription apparatus. The redox state of the plastoquinone pool seems to play a pivotal role in sensing cellular energy status and in regulating photosynthetic capacity. Other cellular pathways, including carbon fixation, carbohydrate metabolism and nutrient assimilation have been shown to have feedback influences on photosynthesis, that may be sensed by the redox state of the plastoquinone pool.

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

References

  • Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098: 275-335

    PubMed  Google Scholar 

  • Allen JF (1993) Redox control of transcription: sensors, reponse regulators, activators and repressors. FEBS Lett 332(3): 203-207.

    PubMed  Google Scholar 

  • Allen JF (1995) Thylakoid protein phosphorylation, state1-state 2 transitions, and photosystem stoichiometry adjustment: redox control at multiple levels of gene expression. Physiol Plantarum 93: 196-205

    Google Scholar 

  • Anderson JM, Chow WS and Goodchild DJ (1988). Thylakoid membrane organisation in sun/shade acclimation. Aust J Plant Physiol 15: 11-26.

    Google Scholar 

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

    Google Scholar 

  • Apel K and Kloppstech K (1980) The effect of light on the biosynthesis of the light-harvesting chlorophyll a/bprotein. Planta 150: 426-430

    Google Scholar 

  • Beale SI and Appleman D (1971) Chlorophyll synthesis in Chlorella. Plant Physiol. 47: 230-235

    Google Scholar 

  • Bennett J (1983) Regulation of photosynthesis by reversible phosphorylation of the light harvesting chlorophyll a/bprotein. Biochem J 212: 1-13

    PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Bennett J, Schwender JR, Shaw EK, Tempel N, Ledbetter M and Williams RS (1987) Failure of corn leaves to acclimate to low irradiance. Role of protochlorophyllide reductase in regulating levels of five chlorophyll-binding proteins. Biochim Biophys Acta 892: 118-129

    Google Scholar 

  • Bhalla P and Bennett J (1987) Chloroplast phosphoproteins: Phosphorylation of a 12-kDa stromal protein by the redox-controlled kinase of thylakoid membranes. Arch Biochem Biophys 252(1): 97-104

    PubMed  Google Scholar 

  • Boardman NK (1977) Comparative photosynthesis of sun and shade plants. Ann Rev Plant Physiol. 28: 355-377

    Google Scholar 

  • Bonaventura C and J. Myers (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim Biophys Acta 189: 366-383

    PubMed  Google Scholar 

  • Bowler C, Neuhaus G, Yamagata H and Chua NH (1994) Cyclic GMP and calcium mediate phytochrome phototransduction. Cell 77: 73-81

    Article  PubMed  Google Scholar 

  • Buchanan BB (1991) Regulation of CO2assimilation in oxygenic photosynthesis: The ferredoxin/thioredoxin system. Arch Biochem Biophys 288(1): 1-9

    PubMed  Google Scholar 

  • Burgess DG and Taylor WC (1987) Chloroplast photooxidation affects the accumulation of cytosolic mRNAs encoding chloroplast proteins in maize. Planta 170: 520-527

    Article  Google Scholar 

  • Burgess DG and Taylor WC (1988) The chloroplast affects the transcription of a nuclear gene family. Mol Gen Genet 214: 89-96

    Google Scholar 

  • Campbell D, Houmard J and Tandeau de Marsac N (1993) Electron transport regulates cellular differentiation in the filamentous cyanobacteria Calothrix. Plant Cell 5: 451-463

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Davison IR (1991) Environmental effects on algal photosynthesis: temperature. J Phycol 27: 2-8

    Google Scholar 

  • Demmig-Adams B and Adams WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1(1): 21-26

    Google Scholar 

  • Escoubas JM, 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 

  • Falkowski PG and LaRoche J (1991) Acclimation to spectral irradiance in algae. J Phycol 27: 8-14

    Google Scholar 

  • Falkowski PG, Greene R and Kolber Z (1994) Light utilization and photoinhibition of photosynthesis in marine phytoplankton. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis, pp 407-432. BIOS Scientific Publishers, Oxford

    Google Scholar 

  • Fisher T, Shurtz-Swirski R, Gepstein S and Dubinsky Z (1989) Changes in the levels of Ribulose-1,5-bisphosphate Carboxylase/Oxygenase (Rubisco) in Tetraedron minimum(Chlorophyta) during light and shade adaption. Plant Cell Physiol 30: 221-228

    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(2): 283-292

    Google Scholar 

  • Furuya M and Schäfer E (1996) Photoperception and signalling of induction reactions by different phytochromes. Trends Plant Sci 1: 301-307

    Article  Google Scholar 

  • Grossman AR, Schaefer MR, Chiang GG and Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57(3): 725-749

    PubMed  Google Scholar 

  • Hermsmeier D, Mala E, Schulz R, Thielmann J, Galland P and Senger H (1991) Antagonistic blue-and red-light regulation of cab-gene expression durning photosynthetic adaptation in Scenedesmus obliquus. J Photochem Photobiol B: Biol. 11: 189-202

    Google Scholar 

  • Hughes J, Lamparter T, Mittmann F, Hartmann E, Gärtner W, Wilde A and Börner (1997) A prokaryotic phytochrome. Science 386: 663

    Google Scholar 

  • Humbeck K, Hoffmann B and Senger H (1988) Influence of energy flux and quality of light on the molecular organization of the photosynthetic apparatus in Scenedesmus. Planta 173: 205-212

    Google Scholar 

  • Huppe HC and Turpin DH (1994) Integration of carbon and nitrogen metabolism in plant and algal cells. Annu Rev Plant Physiol Plant Mol Biol 45: 577-607

    Article  Google Scholar 

  • Jang JC and Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6: 1665-1679

    Article  PubMed  Google Scholar 

  • Jasper F, Quednau B, Kortenjann M and Johanningmeier (1991) Control of cabgene expression in synchronized Chlamydomonas reinhardtiicells. J Photochem Photobiol B: Biol 11: 139-150

    Google Scholar 

  • Johanningmeier U and Howell SH (1984) Regulation of light-harvesting chlorophyll-binding protein mRNA accumulation in Chlamydomonas reinhardtii. J Biol Chem 259: 13541-13549

    PubMed  Google Scholar 

  • Kehoe DM and Grossman AR (1996) Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273: 1409-1412

    PubMed  Google Scholar 

  • Kilb B, Wietoska H and Godde D (1996) Changes in the expression of photosynthetic genes precede loss of photosynthetic activities and chlorophyll when glucose is supplied to mature spinach leaves. Plant Sci 115: 225-235

    Google Scholar 

  • Kim JE, Glick RE and Melis A (1993) Dynamics of photosystem stoichiometry adjustment by light quality in chloroplasts. Plant Physiol 102: 181-190

    PubMed  Google Scholar 

  • Kindle KL (1987) Expression of a gene for a light-harvesting chlorophyll a/b-binding protein in Chlamydomonas reinhardtii: Effects of light and acetate. Plant Mol Biol 9: 547-563

    Google Scholar 

  • Kirk, JTO (1994) Light and Photosynthesis in Aquatic Ecosystems. Cambridge University Press, Cambridge

    Google Scholar 

  • Koenig F (1990) Shade adaptation in cyanobacteria. Photosynth Res 26: 29-37

    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 

  • Krapp A, Hofmann B, Schaefer C and Stitt M (1993) Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: a mechanism for the ‘sink regulation’ of photosynthesis? Plant J 3: 817-828

    Article  Google Scholar 

  • LaRoche J, Mortain-Bertrand A and PG Falkowski PG (1991) Light intensity-induced changes in cabmRNA and light harvesting complex II apoprotein levels in the unicellular chlorophyte Dunaliella tertiolecta. Plant Physiol 97: 147-153

    Google Scholar 

  • Levasseur ME, Morissette JC, Popovic R and Harrison PJ (1990) Effects of long term exposure to low temperature on the photosynthetic apparatus of Dunaliella tertiolecta(Chlorophyceae). J Phycol 26: 479-484

    Google Scholar 

  • Levings III CS and Siedow JN (1995) Regulation by redox poise in chloroplasts. Science 268: 695-696

    Google Scholar 

  • Ley AC and Mauzerall DC (1982) Absolute absorption cross sections for Photosystem II and the minimum quantum requirement for photosynthesis in Chlorella vulgaris. Biochim Biophys Acta 680: 95-106

    Google Scholar 

  • Machalek KM, Davison IR and Falkowski PG (1996) Thermal acclimation and photoacclimation of photosynthesis in the brown alga Laminaria saccharina. Plant Cell Environ 19: 1005-1016

    Google Scholar 

  • Matters GL and Beale SI (1994) Structure and light-regulated expression of the gsagene encoding the chlorophyll biosynthetic enzyme, glutamate 1-semialdehyde aminotransferase, in Chlamydomonas reinhardtii. Plant Mol Biol 24: 617-629

    Article  PubMed  Google Scholar 

  • Matters GL and Beale SI (1995) Blue-light-regulated expression of genes for two early steps of chlorophyll biosynthesis in Chlamydomonas reinhardtii. Plant Physiol 109: 471-479

    PubMed  Google Scholar 

  • Maxwell DP, Falk S, Trick CG and Huner NPA (1994) Growth at low temperature mimics high-light acclimation in Chlorella vulgaris. Plant Physiol 105: 535-543

    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 

  • Mayfield SP and Taylor WC (1984) Carotenoid-deficient maize seedlings fail to accumulate light-harvesting chlorophyll a/bbinding protein (LHCP) mRNA. Eur J Biochem 144: 79-84

    PubMed  Google Scholar 

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

    Google Scholar 

  • Michel H, Tellenbach M and Boschetti A (1983) A chlorophyll b-less mutant of Chlamydomonas reinhardtiilacking in the light-harvesting chlorophyll a/b-protein complex but not in its apoproteins. Biochim Biophys Acta 725: 417-424

    Google Scholar 

  • Morand LZ, Kidd DG and Lagarias JC (1993) Phytochrome levels in the green alga Mesotaenium caldariorumare light regulated. Plant Physiol 101: 97-103

    PubMed  Google Scholar 

  • Morris I and Glover HE (1974) Questions on the mechanism of temperature adaptation in marine phytoplankton. Mar Biol 24: 147-154

    Google Scholar 

  • Mortain-Bertrand A, Bennett J and Falkowski PG (1990) Photoregulation of the light-harvesting chlorophyll protein complex associated with photosystem II in Dunaliella tertiolecta. Plant Physiol 94: 304-311

    Google Scholar 

  • Mortain-Bertrand A, Descolas-Gros C and Jupin H (1988) Growth, photosynthesis and carbon metabolism in the temperature marine diatom Skeletonema costatumadapted to low temperature and low photon-flux density. Mar Biol 100: 135-141

    Google Scholar 

  • Munzner P and Viogt J (1992) Blue light regulation of cell division in Chlamydomonas reinhardtii. Plant Physiol 99: 1370-1375

    Google Scholar 

  • Murakami A and Fujita Y (1991a) Steady state of photosynthetic electron transport in cells of the cyanophyte SynechocystisPCC 6714 having different stoichiometry between PS I and PS II: Analysis of flash-induced oxidation-reduction of cytochrome fand P700 under steady state of photosynthesis. Plant Cell Physiol 32(2): 213-222

    Google Scholar 

  • Murakami A and Fujita Y (1991b) Regulation of photosystem stoichiometry in the photosynthetic system of the cyanophyte SynechocystisPCC 6714 in response to light intensity. Plant Cell Physiol 32(2): 223-230

    Google Scholar 

  • Murakami A and Fujita Y (1993) Regulation of stoichiometry between PSI and PSII in response to light regime for photosynthesis observed with SynechocystisPCC 6741: Relationship between redox state of the Cyt b6f complex and the regulation of PSI formation. Plant Cell Physiol 34(8): 1175-1180

    Google Scholar 

  • Nauš J and Melis A (1992) Response of the photosynthetic apparatus in Dunaliella salinato sublethal concentrations of the herbicide 3-(3′,4′-dichlorophenyl)-1,1-dimethyl urea. Photosynthetica 26(1): 67-78

    Google Scholar 

  • Nisho J, Sun J and Vogelmann TC (1994) Photoinhibition and the light environment within leaves In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis, pp 407-432. BIOS Scientific Publishers, Oxford

    Google Scholar 

  • Oelmüller R (1989) Photooxidative destruction of chloroplasts and its effect on nuclear gene expression and extraplastidic enzyme levels. Photochem Photobiol 49(2): 229-239

    Google Scholar 

  • Oelmüller R and Mohr H (1986) Photooxidative destruction of chloroplasts and its consequences for expression of nuclear genes. Planta 167: 106-113

    Google Scholar 

  • Plumley FG and Schmidt GW (1989) Nitrogen-dependent regulation of photosynthetic gene expression. Proc Natl Acad Sci USA 86: 2678-2682

    Google Scholar 

  • Post AF, Dubinsky Z, Wyman K and Falkowski PG (1984) Kinetics of light-intensity adaptation in a marine planktonic diatom. Mar Biol 83, 231-238

    Google Scholar 

  • Reinbothe S and Reinbothe C (1996) The regulation of enzymes involved in chlorophyll biosynthesis. Eur J Biochem 237: 323-343

    PubMed  Google Scholar 

  • Reinbothe S, Reinbothe C, Lebedev N and Apel K (1996) PORA and PORB, two light-dependent protochlorophyllide-reducing enzymes of angiosperm chlorophyll biosynthesis. Plant Cell 8: 763-769

    PubMed  Google Scholar 

  • Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2: 1027-1038

    Article  PubMed  Google Scholar 

  • Sheen J (1994) Feedback control of gene expression. Photosynth Res 39: 427-438

    Google Scholar 

  • Short TW and Briggs WR (1994) The transduction of blue light signals in higher plants. Annu Rev Plant Physiol Plant Mol Biol 45: 143-171

    Article  Google Scholar 

  • Smith BM, Morrissey PJ, Guenther JE, Nemson JA, Harrison MA, Allen JF and Melis A (1990) Response of the photosynthetic apparatus in Dunaliella salina(green algae) to irradiance stress. Plant Physiol 93: 1433-1440

    Google Scholar 

  • Smith H (1995) Physiological and ecological function within the phytochrome family. Annu Rev Plant Physiol Plant Mol Biol 46: 289-315

    Article  Google Scholar 

  • Sukenik A, Bennett J and Falkowski PG (1987a) Light-saturated photosynthesis limitation by electron transport or carbon fixation? Biochim Biophys Acta 891: 205-215

    Google Scholar 

  • Sukenik A, Bennett J, Mortain-Bertrand A and Falkowski PG (1990) Adaptation of the photosynthetic apparatus to irradiance in Dunaliella tertiolecta. Plant Physiol 92: 891-898

    Google Scholar 

  • Sukenik A, Wyman KD, Bennett J and Falkowski PG (1987b) A novel mechanism for regulating the excitation of Photosystem II in a green alga. Nature 327: 704-707

    Google Scholar 

  • Susek RE, Ausubel FM and Chory J (1993) Signal transduction mutants of Arabidopsisuncouple nuclear Caband RbcSgene expression from chloroplast development. Cell 74: 787-799

    Article  PubMed  Google Scholar 

  • Taylor WC (1989) Regulatory interactions between nuclear and plastid genomes. Ann Rev Plant Physiol Plant Mol Biol 40: 211-233

    Google Scholar 

  • Terzaghi WB and Cashmore AR (1995) Light-regulated transcription. Annu Rev Plant Physiol Plant Mol Biol 46: 445-474

    Article  Google Scholar 

  • Thompson PA, Guo MX and Harrison PJ (1992) Effects on variation in temperature on the biochemical composition of eight species of marine phytoplankton. J Phycol 28: 481-488

    Google Scholar 

  • Trebst A (1980) Inhibitors in electron flow: tools for the functional and structural localization of carriers and energy conservation sites. Meth Enzymol 69: 675-715

    Google Scholar 

  • Turpin DH (1991) Effects of inorganic N availability on algal photosynthesis and carbon metabolism. J Phycol 27: 14-20

    Google Scholar 

  • Turpin DH and Bruce D (1990) Regulation of photosynthetic light harvesting by nitrogen assimilation in the green alga Selenastrum minutum. FEBS Lett 263: 99-103

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Durnford, D.G., Falkowski, P.G. Chloroplast redox regulation of nuclear gene transcription during photoacclimation. Photosynthesis Research 53, 229–241 (1997). https://doi.org/10.1023/A:1005815725371

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1005815725371

Navigation