Summary
Light-energy conversion in thylakoids is accomplished by cooperative interactions between two photoreactions. The balance between these two photoreactions determines the efficiency of energy conversion. The efficiency of energy conversion is maintained at a high level by at least two regulatory mechanisms: short-term adaptation and long-term adaptation. Short-term adaptation, i.e. the state transition, is a regulatory mechanism that controls the distribution of excitation energy transfer from the light-harvesting antenna complexes, the phycobilisomes (PBS), to the two photosystems. The transfer of energy trapped by PBS to the Chl a of Photosystem I (PS I) or Photosystem II (PS II) is regulated either at the transfer point from the PBS to the two photosystems or at a transfer point between the Chl a of PS II and PS I. Energy transfer from the PBS to PS I increases, and to PS II decreases, when most of PS II centers are closed, and the opposite occurs upon a shift to conditions under which most PS I centers are closed. This regulation occurs in response to the state of balance between the two photoreactions through monitoring of the redox status of electron transport between the two photosystems or through monitoring the electrochemical potential of the membrane around the two photosystem complexes. This regulatory process is called’ short-term adaptation’ because this regulation can occur rather rapidly (usually completed within several minutes or less). ‘Long-term adaptation’ refers to a regulated change in the stoichiometry of PS I and PS II in the thylakoids. The PS LPS II ratio becomes greater-values of 2.0 to 3.0 are typical-when cells are grown under conditions where most PS II centers are closed (e.g., green-rich light). The ratio becomes small, approximately 1.0 , upon a shift to conditions where most of PS I centers are closed (e.g., growth in red-rich light). The PS LPS II ratio is also regulated in response to the redox state of electron transport between two photosystems. Regulation of PS I synthesis appears to be the general pattern in cyanobacteria. Synthesis of PS I complexes apparently is controlled at the assembly level but not at the level of apoprotein synthesis. This regulation seems to occur by controlling Chl a synthesis or transport to the site for PS I assembly. The regulation of PS I synthesis is as rapid as state transition. However, the PS I:PS II ratio changes more slowly over a period of hours or days, and hence this process is referred to as ‘long-term adaptation.’ These short-term and long-term adaptation regulatory responses operate together to produce fine-and coarse-tuning adjustments, respectively, and to balance the activities of the two photoreactions in response to changing photosynthetic environments. The phenomena associated with these responses as well as possible mechanisms for their regulation are discussed.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Adhikary SP, Murakami A, Ohki K and Fujita Y (1990) Photoregulation of respiratory activity in the cyanophyte Synechocystis PCC 6714: the possibility of the simultaneous regulation of the amount of PSI complex and the activity of respiratory terminal oxidase in thylakoids. Plant Cell Physiol 31: 527–532.
Aizawa K and Fujita Y (1992) Regulation of PSI formation induced by light quality observed with Synechocystis PCC 6714. In: Murata N (ed) Research in Photosynthesis, Vol IV, pp 329–332. Kluwer, Dordrecht.
Aizawa K, Shimizu T, Hiyama T, Satoh K, Nakamura Y and Fujita Y (1992) Changes in composition of membrane proteins accompanying the regulation of PSI/PSII stoichiometry observed with Synechocystis PCC 6803. Photosynthesis Res 32: 131–138.
Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098: 275–335.
Allen JF and Holmes NG (1986) A general model for regulation of photosynthetic unit function by protein phosphorylation. FEBS Lett 202: 175–181.
Allen JF, Sanders CE and Holmes NG (1985) Correlation of membrane protein phosphorylation with excitation energy distribution in the cyanobacterium Synechococcus 6301. FEBS Lett 193: 271–275.
Anderson JM (1986) Photoregulation of the composition, function, and structure of thylakoid membranes. Annu Rev Plant Physiol 37: 93–136.
Barber J (1983) Membrane conformational changes due to phosphorylation and the control of energy transfer in photosynthesis. Photobiochem Photobiophys 5: 181–190.
Bennett J (1991) Protein phosphorylation in green plant chloroplasts. Annu Rev Plant Physiol Plant Mol Biol 42: 281–311.
Bennett J, Shaw EK and Michel H (1988) Cytochrome b 6 f complex is required for phosphorylation of light-harvesting chlorophyll a/b complex II in chloroplast photosynthetic membranes. Eur J Biochem 171: 95–100.
Biggins J and Bruce D (1989) Regulation of excitation energy transfer in organisms containing phycobilins. Photosynthesis Res 20: 1–34.
Biggins J, Campbell CL and Bruce D (1984a) Mechanism of the light state transition in photosynthesis. II. Analysis of phosphorylated polypeptides in the red alga, Porphyridium cruentum. Biochim Biophys Acta 767: 138–144.
Biggins J, Campbell CL, Creswell LL and Wood EA (1984b) Mechanism of the light state transition in Porphyridium cruentum. In: Sybesma C (ed) Advances in Photosynthesis Research, Vol III, pp 303–306. Martinus Nijhoff/Dr W. Junk Publishers, The Hague.
Bonaventura C and Myers J (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim Biophys Acta 189: 366–383.
Brody M and Emerson R (1959) The quantum yield of photosynthesis in Porphyridium cruentum, and the role of chlorophyll a in the photosynthesis of red algae. J Gen Physiol 43: 251–264.
Bruce D, Brimble S and Bryant DA (1989) State transition in a phycobilisome-less mutant of the cyanobacterium Synechococcus sp. PCC 7002. Biochim Biophys Acta 974: 66–73.
Bruce D and Salehian O (1992) Laser-induced optoacoustic calorimetry of cyanobacteria. The efficiency of primary photosynthetic processes in state 1 and state 2. Biochim Biophys Acta 1100: 242–250.
Canaani O (1986) Photoacoustic detection of oxygen evolution and state 1-state 2 transitions in cyanobacteria. Biochim Biophys Acta 852: 74–80.
Coughlan SJ (1988) Chloroplast thylakoid protein phosphorylation is influenced by mutations in the cytochrome bf complex. Biochim Biophys Acta 933: 413–422.
Coughlan SJ and Hind J (1986) Purification and characterization of a membrane-bound protein kinase from spinach thylakoids. J Biol Chem 261: 11378–11385.
Cunnigham FX Jr, Dennenberg RJ Jursinic PA and Gantt E (1990) Growth under red light enhances Photosystem II relative to Photosystem I and phycobilisomes in the red alga Porphyridium cruentum. Plant Physiol 93: 888–895.
Eichacker LA, Soll J, Lauterbach P, Rüdiger W, Klein RR and Mullet JE (1990) In vitro synthesis of chlorophyll a in the dark triggers accumulation of chlorophyll a apoproteins in barley etioplasts. J Biol Chem 265: 13566–13567.
Eley JH (1971) Effect of carbon dioxide concentration on pigmentation in the blue-green alga Anacystis nidulans. Plant Cell Physiol 12: 311–316.
Emerson R and Lewis CM (1942) The photosynthetic efficiency of phycocyanin in Chroococcus, and the problem of carotenoid participation in photosynthesis. J Gen Physiol 25: 579–595.
Emerson R and Rabinowitch E (1960) Red drop and role of auxiliary pigments in photosynthesis. Plant Physiol 35: 477–485.
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 f complex. Plant Cell Physiol 28: 1547–1553.
Fujita Y, Ohki K and Murakami A (1985) Chromatic regulation of photosystem composition in the photosynthetic system of red and blue-green algae. Plant Cell Physiol 26: 1541–1548.
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.
Fujita Y, Murakami A, Ohki K and Hagiwara N (1988) Regulation of photosystem composition in cyanobacterial photosynthetic system: Evidence indicating that Photosystem I formation is controlled in response to the electron transport state. Plant Cell Physiol 29: 557–564.
Fujita Y, Iwama Y, Ohki K, Murakami A and Hagiwara N (1989) Regulation of the size of light-harvesting antennae in response to light intensity in the green alga Chlorella pyrenoidosa. Plant Cell Physiol 30: 1029–1037.
Fujita Y, Murakami A and Ohki K (1990) Regulation of the stoichiometry of thylakoid components in the photosynthetic system of cyanophytes: Model experiments showing that control of the synthesis or supply of Chl a can change the stoichiometric relationship between the two photosystems. Plant Cell Physiol 31: 145–153.
Fujita Y, Murakami A and Aizawa K (1992) Light acclimation of thylakoid system in cyanophytes: Regulation of PSI formation in response to light regime. In: Murata N (ed) Research in Photosynthesis, Vol IV, pp 301–308. Kluwer, Dordrecht.
Gal A, Shahak Y, Schuster G and Ohad I (1987) Specific loss of LHCII phosphorylation in the Lemna mutant 1073 lacking the cytochrome b 6 f complex. FEBS Lett 221: 205–210.
Gal A, Schuster G, Frid D, Canaani O, Schwieger HG and Ohad (1988) Role of cytochrome b 6 f complex in the redox controlled activity of Acetabularia thylakoid protein kinase. J Biol Chem 263: 7785–7791.
Gal A, Hauska G, Herrmann R and Ohad I (1990) Interaction between light-harvesting chlorophyll-a/b protein (LHC II) kinase and cytochrome b 6 f complex. In vitro control of kinase activity. J Biol Chem 265: 19742–19749.
Glick RE, McCauley SW, Gruissem W and Melis A (1986) Light quality regulates expression of chloroplast genes and assembly of photosynthetic membrane complexes. Proc Natl Acad Sci USA 83: 4287–4291.
Horton P, Allen JF, Black MT and Bennett J (1981) Regulation of phosphorylation of chloroplast membrane polypeptides by the redox state of plastoquinone. FEBS Lett 125: 193–196.
Jerlov NG (1976) Marine Optics. Elsevier Scientific, Amsterdam.
Jones LW and Myers J (1964) Enhancement in the blue-green alga, Anacystis nidulans. Plant Physiol 39: 938–946.
Katoh T and Gantt E (1979) Photosynthetic vesicles with bound phycobilisomes from Anabaena variabilis. Biochim Biophys Acta 546: 383–393.
Kawamura M, Mimuro M and Fujita Y (1979) Quantitative relationship between two reaction centers in the photosynthetic system of blue-green algae. Plant Cell Physiol 20: 697–705.
Kirschner J and Senger H (1986) Thylakoid protein phosphorylation in the red algae Porphyridium cruentum. In: Akoyunoglou G and Senger H (eds) Regulation of Chloroplast Differentiation, pp 339–344. Alan R Liss Inc, New York.
Klein RR, Gamble PE and Mullet JE (1988a) Light-dependent accumulation of radiolabeled plastid-encoded chlorophyll a-apoproteins requires chlorophyll a. I. Analysis of chlorophyll deficient mutants and phytochrome involvement. Plant Physiol 88: 1246–1256.
Klein RR, Mason HS and Mullet JE (1988b) Light-regulated translation of chloroplast proteins. I. Transcripts of psaA-psaB, psbA and rbcL are associated with polysomes in darkgrown and illuminated barley seedlings. J Cell Biol 106: 289–301.
Lemaire C, Girard-Bascou J and Wollman FA (1987) Characterization of the b 6 f complex subunits and studies on the LHC-kinase in Chlamydomonas reinhardtii using mutant strains altered in the b 6 f complex. In: Biggins J (ed) Progress in Photosynthesis Research, Vol IV, pp 655–658. Martinus Nijhoff, Dordrecht.
Leong TY and Anderson JM (1986) Light-quality and irradiance adaptation of the composition and function of pea-thylakoid membranes. Biochim Biophys Acta 850: 57–63.
Ley AC and Butler WL (1980) Energy distribution in the photochemical apparatus of Porphyridium cruentum in state I and state II. Biochim Biophys Acta 592: 349–363.
Malkin S, Herbert SK and Fork DC (1990) Light distribution, transfer and utilization in the marine red alga Porphyra perforata from photoacoustic energy-storage measurements. Biochim Biophys Acta 1016: 177–189.
Manodori A and Melis A (1984) photochemical apparatus organization in Anacystis nidulans (Cyanophyceae). Effect of CO2 concentration during cell growth. Plant Physiol 74: 67–71.
Manodori A and Melis A (1986) Cyanobacterial acclimation to Photosystem I or Photosystem II light. Plant Physiol 82: 185–189.
Melis A, Manodori A, Glick RE, Ghirardi ML, McCauley SW and Neale PJ (1985) The mechanism of photosynthetic membrane adaptation to environmental stress conditions: A hypothesis on the role of electron-transport capacity and of ATP/NADPH pool in the regulation of thylakoid membrane organization and function. Physiol Veg 23: 757–765.
Melis A, Mullineaux CW and Allen JF (1989) Acclimation of the photosynthetic apparatus to Photosystem I or Photosystem II light: Evidence from quantum yield measurements and fluorescence spectroscopy of cyanobacterial cells. Z Naturforsch 44c: 109–118.
Mullineaux CW (1992) Excitation energy transfer from phycobilisomes to Photosystem I in a cyanobacterium. Biochim Biophys Acta 1100: 285–292.
Mullineaux CW and Allen JF (1990) State 1-state 2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between Photosystem I and II. Photosynthesis Res 23: 297–311.
Mullineaux CW and Holzwarth AR (1991) Kinetics of excitation energy transfer in the cyanobacterial phycobilisome-Photosystem II complex. Biochim Biophys Acta 1098: 68–78.
Mullineaux CW, Bittersmann E, Allen JF and Holzwarth AR (1990) Picosecond time-resolved fluorescence emission spectra indicate decreased energy transfer from the phycobilisome to Photosystem II in light-state 2 in the cyanobacterium Synechococcus 6301. Biochim Biophys Acta 1015: 231–242.
Murakami A and Fujita Y (1988) Steady state of photosynthesis in cyanobacterial photosynthetic systems before and after regulation of electron transport composition: Overall rate of photosynthesis and PSI/PSII composition. Plant Cell Physiol 29: 305–311.
Murakami A and Fujita Y (1991a) Steady state of photosynthetic electron transport in cells of the cyanophyte Synechocystis PCC 6714 having different stoichiometry between PSI and PSII: Analysis of flash-induced oxidationreduction of cytochrome/and P700 under steady state of photosynthesis. Plant Cell Physiol 32: 213–222.
Murakami A and Fujita Y (1991b) Regulation of photosystem stoichiometry in the photosynthetic system of the cyanophyte Synechocystis PCC 6714 in response to light-intensity. Plant Cell Physiol 32: 223–230.
Murata N (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172: 242–251.
Murata N (1970) Control of excitation transfer in photosynthesis IV. Kinetics of chlorophyll a fluorescence in Porphyra yezoensis. Biochim Biophys Acta 205: 379–389.
Myers J (1963) Enhancement. In: Kok B and Jagendorf AT (ed) Photosynthetic Mechanisms of Green Plants, pp 301–317. National Academy of Sciences—National Research Council, Washington, DC.
Myers J, Graham J-R and Wang RT (1980) Light harvesting in Anacystis nidulans studied in pigment mutants. Plant Physiol 66: 1144–1149.
Myers J, Graham J-R and Wang RT (1982) Protochlorophyll(ide) in a blue-green alga. Plant Physiol 69: 549–550.
Ohki K, Okabe Y, Murakami A and Fujita Y (1987) A comparative study of quantitative relationship between phycobiliproteins and Photosystem II in cyanobacteria and red algae. Plant Cell Physiol 28: 1219–1226.
Salehian O and Bruce D (1992) Distribution of excitation energy in photosynthesis: quantification of fluorescence yields from intact cyanobacteria. J Lumin 51: 91–98.
Sanders CE and Allen JF (1987) The 18.5 kD phosphoprotein of the cyanobacterium Synechococcus 6301: A component of the phycobilisome. In: Biggins J (ed) Progress in Photosynthesis Research, Vol II, pp 761–764. Martinus Nijhoff, Dordrecht.
Sanders CE, Melis A and Allen JF (1989) In vivo phosphorylation of proteins in the cyanobacterium Synechococcus 6301 after chromatic acclimation to Photosystem I or Photosystem II light. Biochim Biophys Acta 976: 168–172.
Satoh K and Fork DC (1983) A new mechanism for adaptation to changes in light intensity and quality in the red alga, Porphyra perforata. I. Relation to state 1-state 2 transitions. Biochim Biophys Acta 722: 190–196.
Schopf JW and Walter MR (1982) Origin and early evolution of cyanobacteria: the geological evidence. In: Carr NG and Whitton BA (eds) The Biology of Cyanobacteria, pp 543–564. Blackwell Scientific Publishers, Oxford.
Schluchter WM, Zhao J and Bryant (1993) Isolation and characterization of the ndhF gene of Synechococcus sp. PCC 7002 and initial characterization of an interposon mutant. J Bacteriol 175: 3343–3352.
Williams WP and Allen JF (1987) State I/state 2 changes in higher plants and algae. Photosynthesis Res 13: 19–45.
Yocum CS and Blinks LR (1958) Light-induced efficiency and pigment alterations in red algae. J Gen Physiol 41: 1113–1117.
Yokoyama E, Murakami A, Sakurai H and Fujita Y (1991) Effect of supra-high irradiation on the photosynthetic system of the cyanophyte Synechocystis PCC 6714. Plant Cell Physiol 32: 827–834.
Yu L, Zhao J, Mühlenhoff U, Bryant DA, and Golbeck JH (1993) PsaE is required for cyclic electron flow around Photosystem I in the cyanobacterium Synechococcus sp. PCC 7002. Plant Physiol 103: 171–180.
Zhao J, Zhou J and Bryant DA (1992) Energy transfer processes in phycobilisomes as deduced from analyses of mutants of Synechococcus sp. PCC 7002. In: Murata N (ed) Research in Photosynthesis, Vol 1, pp 25–32. Kluwer, Dordrecht.
Zhao J, Snyder WB, Mühlenhoff U, Rhiel E, Warren PV, Golbeck JH and Bryant DA (1993) Cloning and characterization of the psaE gene of the cyanobacterium Synechococcus sp. PCC 7002: characterization of a psaE mutant and overproduction of the protein in Escherichia coli. Mol Microbiol 9: 183–194.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1994 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Fujita, Y., Murakami, A., Aizawa, K., Ohki, K. (1994). Short-term and Long-term Adaptation of the Photosynthetic Apparatus: Homeostatic Properties of Thylakoids. In: Bryant, D.A. (eds) The Molecular Biology of Cyanobacteria. Advances in Photosynthesis, vol 1. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-0227-8_22
Download citation
DOI: https://doi.org/10.1007/978-94-011-0227-8_22
Publisher Name: Springer, Dordrecht
Print ISBN: 978-0-7923-3273-2
Online ISBN: 978-94-011-0227-8
eBook Packages: Springer Book Archive