Skip to main content
Log in

Chromatic regulation inChlamydomonas reinhardtii alters photosystem stoichiometry and improves the quantum efficiency of photosynthesis

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The work addressed the adjustment of the photosystem ratio in the green algaChlamydomonas reinhardtii. It is shown that green algae, much like cyanophytes and higher plants, adjust and optimize the ratio of the two photosystems in chloroplasts in response to the quality of irradiance during growth. Such adjustments are compensation reactions and helpC. reinhardtii to retain a quantum efficiency of oxygen evolution near the theoretical maximum. Results show variable amounts of PS I and a fairly constant amount of PS II in chloroplasts and suggest that photosystem stoichiometry adjustments, occurring in response to the quality of irradiance during plant growth, are mainly an adjustment in the concentration of PS I. The work delineates chromatic effects on chlorophyll accumulation in the chloroplast ofC. reinhardtii from those pertaining to the regulation of the PS I/PS II ratio. The detection of the operation of a molecular feedback mechanism for the PS I/PS II ratio adjustment in green algae strengthens the notion of the highly conserved nature of this mechanism among probably all oxygen evolving photosynthetic organisms. Findings in this work are expected to serve as the basis of future biochemical and mutagenesis experiments for the elucidation of the photosystem ratio adjustment in oxygenic photosynthesis.

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

Chl:

chlorophyll

PS:

photosystem

LHC:

light-harvesting complex

QA :

primary electronaccepting plastoquinone of PS II

Pchlide:

protochlorophyllide

Proto:

protoporphyrin

References

  • Aizawa K, Shimizu T, Hiyama T, Satoh K, Nakamura Y and Fujita Y (1992) Changes in composition of membrane proteins accompanying the regulation of PS I/PS II stoichiometry observed with Synechocystis PCC 6803, Photosynth Res 32: 131–138

    Google Scholar 

  • Anderson JM (1986) Photoregulation of the composition, function and structure of thylakoid membranes. Annu Rev Plant Physiol 37: 93–136

    Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase inBeta vulgaris. Plant Physiol 24: 1–15

    Google Scholar 

  • Björkman O and Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170: 489–504

    Google Scholar 

  • Björkman O and Ludlow MM (1972) Characterization of the light climate on the floor of a Queensland rainforest. In: Carnegie Inst Washington Yearbook, Vol 71, pp 85–94

  • Björkman O, Boardman NK, Anderson JM, Thorne SW, Goodchild DJ and Pyliotis NA (1972) Effect of light intensity during growth ofAtriplex patula on the capacity of photosynthetic reactions, chloroplast components and structure. In: Carnegie Inst Washington Yearbook, Vol 71, 115–135

  • Brody M and Emerson R (1959) The quantum yield of photosynthesis inPorphyridium cruentum, and the role of chlorophylla in the photosynthesis of red algae. J Gen Physiol 43: 251–264

    PubMed  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. Physiologia Plantarum 70: 196–202

    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 characteristic composition and morphology ofPisum sativum chloroplasts. Plan Cell Environ 13: 135–145

    Google Scholar 

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

    PubMed  Google Scholar 

  • Chow WS, Miller C and Anderson JM (1991) Surface charges, the heterogeneous lateral distribution of the two photosystems, and thylakoid stacking. Biochim Biophys Acta 1057: 69–77

    Google Scholar 

  • Chua N-H and Bennoun P (1975) Thylakoid membrane polypeptides ofChlamydomonas reinhardtii in wild-type and mutant strains deficient in Photosystem-II reaction center. Proc Natl Acad Sci USA 72: 2175–2179

    PubMed  Google Scholar 

  • Cramer WA and Whitmarsh J (1977) Photosynthetic cytochromes. Ann Rev Plant Physiol 28: 133–172

    Google Scholar 

  • Cunningham FX, Dennenberg RJ, Jursinic PA and Gantt E (1990) Growth under red light enhances Photosystem II relative to Photosystem I and phycobilisomes in the red algaePorphyridium cruentum. Plant Physiol 93: 888–895

    Google Scholar 

  • Cunningham FX, Vonshak A and Gantt E (1992) Photoacclimation in the red algaPorphyridium cruentum. Changes in photosynthetic enzymes, electron carriers, and light-saturated rate of photosynthesis as a function of irradiance and spectral quality. Plant Physiol 100: 1142–1149

    Google Scholar 

  • Duysens LNM (1956) The flattening of the absorption spectrum of suspensions, as compared to that of solutions. Biochim Biophys Acta 19: 1–12

    PubMed  Google Scholar 

  • Duysens LNM and Sweers HE (1963) Mechanism of two photochemical reactions in algae as studied by means of fluorescence. In: Microalgae Photosynthetic Bacteria, Special Issue of Plant Cell Physiology, pp 353–372. University of Tokyo Press Tokyo

    Google Scholar 

  • Evans JR (1987) The dependence of quantum yield on and growth irradiance. Aust J Plant Physiol 14: 69–79

    Google Scholar 

  • Falbel TG and Staehelin LA (1994) Characterization of a family of chlorophyll-deficient wheat (Triticum) and barley (Hordeum vulgare) mutants with defects in the magnesium-insertion step of chlorophyll biosynthesis. Plant Physiol 104: 639–648

    PubMed  Google Scholar 

  • Fujita Y (1990) Regulation of stoichiometry among thylakoid components in response to light regime: A story of the dynamic nature of the thylakoid system in cyanophytes. Bot Mag Tokyo Special Issue 2: 29–42

    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 lightharvesting antennae and cytochromeb 6/f complex. Plant Cell Physiol 28: 1547–1553

    Google Scholar 

  • 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

    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 

  • Fujita Y, Murakami A, Aizawa K and Ohki K (1994) Short-term and long-term adaptation of the photosynthetic apparatus: homeostatic properties of thylakoids. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 677–692. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Fujita Y, Murakami A and Aizawa K (1995) The accumulation of protochlorophyllide in cells ofSynechocystis PCC 6714 with a low PS I/PS II stoichiometry. Plant Cell Physiol 36: 575–582

    Google Scholar 

  • Ghirardi ML and Melis A (1984) Photosystem electron-transport capacity and light-harvesting antenna size in maize chloroplasts. Plant Physiol 74: 993–998

    Google Scholar 

  • Glick RE and Melis A (1988) Minimum photosynthetic unit size in system I and system II of barley chloroplasts. Biochim Biophys Acta 934: 151–155

    Google Scholar 

  • Glick RE, McCauley SW and Melis A (1985) Effect of light quality on chloroplast-membrane organization and function in pea. Planta 164: 487–494

    Google Scholar 

  • Greene BA, Allred DR, Morishige DT and Staehelin LA (1988) Hierarchical response of light-harvesting chlorophyll-proteins in a light-sensitive chlorophyllb-deficient mutant of maize. Plant Physiol 87: 357–364

    Google Scholar 

  • Guenther JE, Nemson JA and Melis A (1990) Development of PS II in dark grownChlamydomonas reinhardtii. A light-dependent conversion of PS IIβ, QB-nonreducing centers to the PS IIα, QB-reducing form. Photosynth Res 24: 35–46

    Google Scholar 

  • Jursinic P and Dennenberg R (1989) Measurement of stoichiometry of Photosystem II to Photosystem I reaction centers. Photosynth Res 21: 197–200

    Google Scholar 

  • 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

    Google Scholar 

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

    PubMed  Google Scholar 

  • Kirk JTO (1983) Light and Photosynthesis in Aquatic Ecosystems, Cambridge University Press, London

    Google Scholar 

  • Koski M, French CS and Smith JHC (1951) The action spectrum for the transformation of protochlorophyll to chlorophylla in normal and albino corn seedlings. Arch Biochem Biophys 31: 1–17

    Google Scholar 

  • Leong TA and Anderson JM (1986) Light-quality and irradiance adaptation of the composition and function of pea-thylakoid membranes. Biochim Biophys Acta 850: 57–63

    Google Scholar 

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

    Google Scholar 

  • Lichtenthaler HK and Meier D (1984) Regulation of chloroplast photomorphogenesis by light intensity and light quality, In: Ellis RJ (ed) Chloroplast Biogenesis, pp 261–281. Cambridge University Press, UK

    Google Scholar 

  • Manodori A and Melis A (1986) Cyanobacterial acclimation to Photosystem I or Photosystem II light. Plant Physiol 82: 185–189

    Google Scholar 

  • Meeks JC (1974) Chlorophylls. In: Steward WDP (ed) Algal Physiology and Biochemistry, pp 161–175. University of California Press Berkeley, CA

    Google Scholar 

  • Melis A (1984) Light regulation of photosynthetic membrane structure, organization and function. J Cell Biochem 24: 271–285

    PubMed  Google Scholar 

  • Melis A (1990) Regulation of photosystem stoichiometry in oxygenic photosynthesis. Bot Mag Tokyo Special Issue 2: 9–28

    Google Scholar 

  • Melis A and Anderson JM (1983) Structural and functional organization of the photosystems in spinach chloroplasts: Antenna size, relative electron-transport capacity, and chlorophyll composition. Biochim Biophys Acta 724: 473–484

    Google Scholar 

  • Melis A and Brown JS (1980) Stoichiometry of system I and system II reaction centers and of plastoquinone in different photosynthetic membranes. Proc Natl Acad Sci USA 77: 4712–4716

    Google Scholar 

  • Melis A and Harvey GW (1981) Regulation of photosystem stoichiometry, chiometry, chlorophylla and chlorophyllb content and relation to chloroplast ultrastructure. Biochim Biophys Acta 637: 138–145

    Google Scholar 

  • 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

    Google Scholar 

  • 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 Teil C 44c: 109–118

    Google Scholar 

  • 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 PS I/PS II composition. Plant Cell Physiol 29: 305–311

    Google Scholar 

  • Murata N, Nishimura M and Takamiya A (1966) Fluorescence of chlorophyll in photosynthetic systems. I. Analysis of ‘weak light effect‘ in isolated spinach chloroplasts. Biochim Biophys Acta 112: 213–222

    PubMed  Google Scholar 

  • Murata N, Nishimura M and Takamiya A (1966) Fluorescence of chlorophyll in photosynthetic systems. II. Induction of fluorescence in isolated spinach chloroplasts. Biochim Biophys Acta 120: 23–33

    PubMed  Google Scholar 

  • Myers J, Graham JR and Wang RT (1980) Light-harvesting inAnacystis nidulans studied in pigment mutants. Plant Physiol 66: 1144–1149

    Google Scholar 

  • Myers J, Graham JR and Wang RT (1982) Protochlorophyll(ide) in a blue-green alga. Plant Physiol 69: 549–550

    Google Scholar 

  • Neale PJ and Melis A (1986) Algal photosynthetic membrane complexes and the photosynthesis-irradiance curve: A comparison of light-adaptation responses inChlamydomonas reinhardtii. J Phycol 22: 531–538

    Google Scholar 

  • Sager R and Granick S (1954) Nutritional control of sexuality inChlamydomonas reinhardtii: J Gen Physiol 37: 729–742

    PubMed  Google Scholar 

  • Smith H, Samson G and Fork DC (1993) Photosynthetic acclimation to shade-probing the role of phytochromes using photomorphogenetic mutants of tomato. Plant Cell Environ 16: 929–937

    Google Scholar 

  • Sueoka N (1960) Mitotic replication of deoxyribonucleic acid inChlamydomonas reinhardtii. Proc Natl Acad Sci USA 46: 83–91

    Google Scholar 

  • Terashima I and Saeki T (1983) Light environment within a leaf I. Optical properties of paradermal sections of Camellia leaves with special reference to differences in the optical properties of palisade and spongy tissues. Plant Cell Physiol 24: 1493–1501

    Google Scholar 

  • Thielen APGM and vanGorkom HJ (1981) Quantum efficiency and antenna size of Photosystem IIα, IIβ and I in tobacco chloroplasts. Biochim Biophys Acta 635: 111–120

    PubMed  Google Scholar 

  • Towbin H, Staehelin T and Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350–4353

    PubMed  Google Scholar 

  • Yocum CS and Blinks LR (1958) Light-induced efficiency and pigment alterations in red algae. J Gen Physiol 41: 1113–1117

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Melis, A., Murakami, A., Nemson, J.A. et al. Chromatic regulation inChlamydomonas reinhardtii alters photosystem stoichiometry and improves the quantum efficiency of photosynthesis. Photosynth Res 47, 253–265 (1996). https://doi.org/10.1007/BF02184286

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02184286

Key words

Navigation