Photoinhibition: Then and Now

  • Barry Osmond
  • Britta Förster
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 21)


This perspective advocates a holistic view of photoinhibition from the molecule to the biosphere; a view that integrates many biophysical and biochemical processes in antennae and reaction centers of the photosystems that, when acting in concert, allow plants to respond to diverse and dynamic light conditions in many different environments. We take the general view that photoinhibition refers to a reduction in the efficiency of light use in the photosynthetic apparatus (Kok, 1956). Since the 1970s, biochemical, ecophysiological, and genetic studies of photosynthetic functions in strong light, in vivoand in situ, and their interactions with biotic and abiotic stresses, have significantly advanced our understanding of photoinhibition. We trace some origins of the idea then, that slow dark reactions, such as growth, CO2 assimilation, photorespiration, and photosynthetic electron transport, ultimately limit light use in photosynthesis, and thus determine whether light is in excess and the magnitude of “excitation pressure” in the photosynthetic apparatus at any moment. This and other ideas are followed through studies of photoacclimation in leaves of plants and algae from diverse terrestrial and marine environments. We highlight two currently interesting possibilities for the photoprotective dissipation of “excitation pressure” that reduce the efficiency of photosynthesis by changes in structure and function of antenna pigment-protein complexes and in the populations of functional and non-functional PS II centers. We conclude by briefly considering challenges presented nowby the discovery of “gain of function”, very high light resistant (VHLR) mutants of Chlamydomonas, by the accessory lutein-epoxide cycle, and by technologies for remote sensing of photoinhibition in the field.


Xanthophyll Cycle Strong Light Excitation Pressure Lutein Epoxide Reaction Center Function 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adams WW III and Osmond CB (1988) Internal CO2 supply during photosynthesis of sun and shade grown CAM plants in relation to photoinhibition. Plant Physiol 86: 117–123PubMedGoogle Scholar
  2. Adams WW III, Nishida K and Osmond CB (1986) Quantum yields of CAM plants measured by photosynthetic O2 evolution. Plant Physiol 81: 297–300PubMedGoogle Scholar
  3. Adams WW III, Zarter CR, Mueh KE, Amiard V and Demmig- Adams B (2005) Energy dissipation and photoinhibition: A continuum of photoprotection. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 49–64. Springer, DordrechtGoogle Scholar
  4. Adir N, Zer H, Shochat S and Ohad I (2003) Photoinhibition - a historical perspective. Photosynth Res 76: 343–370PubMedCrossRefGoogle Scholar
  5. Allen JF and Pfannschmidt T (2000) Balancing the two photosystems: photosynthetic electron transport governs transcription of reaction center genes in chloroplasts. Phil TransRSoc Lond 355: 1351–1360CrossRefGoogle Scholar
  6. Anderson JM and Osmond CB (1987) Sun-shade responses: compromises between acclimation and photoinhibition. In: Kyle DJ, Osmond CB and Arntzen CJ. (eds). Photoinhibition, Topics in Photosynthesis, Vol. 9, pp 1–38. Elsevier, AmsterdamGoogle Scholar
  7. Anderson JM, Park Y-I and Chow WS (1997) Photoinactivation and photoprotection of photosystem II in nature. Physiol Plant 100: 214–223CrossRefGoogle Scholar
  8. Aro E-M, Virgin I and Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134PubMedCrossRefGoogle Scholar
  9. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50: 601–639PubMedCrossRefGoogle Scholar
  10. Badger MR, von Caemmerer S, Ruuska S and Nakano H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Phil Trans R Soc Lond B 355: 1433–1446CrossRefGoogle Scholar
  11. Balachandran S and Osmond CB (1994) Susceptibility of tobacco leaves to photoinhibition following infection with two strains of tobacco mosaic virus under different light and nitrogen nutrition regimes. Plant Physiol 104: 1051–1057PubMedGoogle Scholar
  12. Baroli I, Do AD, Yamane Y, and Niyogi KK (2003) Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardtii from photooxidative stress. Plant Cell 15, 992–1008.PubMedCrossRefGoogle Scholar
  13. Björkman O and Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77K among vascular plants of diverse origins. Planta 170: 489–504CrossRefGoogle Scholar
  14. Björkman O and Holmgren P (1963) Adaptability of the photosynthetic apparatus to light intensity in ecotypes from exposed and shaded habitats. Physiol Plant 16: 889–914CrossRefGoogle Scholar
  15. Bungard RA, Ruban AV, Hibberd JM, Press MC, Horton P and Scholes JC (1999) Unusual carotenoid composition and a new type of xanthophyll cycle in plants. Proc Natl Acad Sci USA 96: 1135–1139PubMedCrossRefGoogle Scholar
  16. Chow WS, Hope AB and Anderson JM (1991) Further studies on quantifying photosystem II in vivo by flash-induced oxygen yield in leaf discs. Aust J Plant Physiol 18: 397–410Google Scholar
  17. Chow WS, Lee H-Y, Park Y-I, Park Y-M, Hong Y-N and Anderson JM (2002) The role of inactive photosystem II- mediated quenching in a last-ditch community defense against high light stress in vivo. Phil Trans R Soc Lond B 357: 1441– 1450CrossRefGoogle Scholar
  18. Cornic G (1976) Effet exercé sur láctivité photosynthetique du Sinapis alba L par une inhibition temporaire de la photorespiration se déroulant dans un air sans CO2. CR Acad Sci D 282: 1955–1958Google Scholar
  19. Cornic G and Fresneau C (2002) Photosynthetic carbon reduction and oxidation cycles are the main electron sinks for photosystem II activity during mild drought. Ann Bot 89: 887–894PubMedCrossRefGoogle Scholar
  20. Delieu T and Walker DA (1983) Simultaneous measurement of oxygen evolution and chlorophyll fluorescence from leaf pieces. Plant Physiol 73: 534–541PubMedGoogle Scholar
  21. Demmig B and Björkman O (1987) Comparison of the effects of excessive light on chlorophyll fluorescence (77K) and photon yield of O2 evolution in leaves of higher plants. Planta 171: 171–184CrossRefGoogle Scholar
  22. Demmig B, Winter K, Krüger A and Czygan F-C (1987) Photoinhibition and zeaxanthin formation in intact leaves. A possible role of the xanthophyll cycle in the dissipation of excess light energy. Plant Physiol 84: 218–224PubMedGoogle Scholar
  23. Demmig-Adams B (2003) Linking the xanthophyll cycle with thermal energy dissipation. Photosynth Res 76: 73–80PubMedCrossRefGoogle Scholar
  24. Demmig-Adams B, Ebbert V, Zarter CR and Adams WW III (2005) Characteristics and species-dependent employment of flexible versus sustained thermal dissipation and photoinhibition. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 39–48. Springer, DordrechtGoogle Scholar
  25. Edelman M and Mattoo AK (2005) The D1 protein: past and future perspectives. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 23–38. Springer, DordrechtGoogle Scholar
  26. Ewart AJ (1896) On assimilatory inhibition in plants. J Linn Soc 31: 364–461Google Scholar
  27. Ferrar PJ and Osmond CB (1986) Nitrogen supply as a factor influencing photoinhibition and photosynthetic acclimation after transfer of shade grown Solanum dulcamara to bright light. Planta 168: 563–570CrossRefGoogle Scholar
  28. Förster B, Osmond CB, Boynton JE and Gillham NW (1999) Mutants of Chlamydomonas reinhardtii resistant to very high light. J Photochem Photobiol B 48: 127–135CrossRefGoogle Scholar
  29. Förster B, Osmond CB and Boynton JE (2001) Very high light resistant mutants of Chlamydomonas reinhardtii: responses of photosystem II, nonphotochemical quenching and xanthophyll pigments to light and CO2. Photosynth Res 67:5–15PubMedCrossRefGoogle Scholar
  30. Förster B, Osmond CB and Pogson BJ (2005) Improved survival of very high light and oxidative stress is conferred by spontaneous gain-of-function mutations in Chlamydomonas. Biochim Biophys Acta (in press)Google Scholar
  31. Franklin LA, Levavasseur G, Osmond CB, Henley WJ and Ramus J (1992) Two components of onset and recovery during photoinhibition of Ulva rotundata. Planta 186: 399–408CrossRefGoogle Scholar
  32. Funayama S, Terashima I and Yahara T (2001) Effects of virus infection and light environment on the population dynamics of Eupatorium makinoi (Asteraceae). Am J Bot 88: 612– 622CrossRefGoogle Scholar
  33. Gamon JA, Serrano L and Surfas JS (1997) The photochemical reflectance index: an optical indicator of photosynthetic radiation use efficiency across species, functional types and nutrient levels. Oecologia 112: 492–501CrossRefGoogle Scholar
  34. Garcia-Plazaola JI, Hernández A, Olano JM and Becerril JM. (2003) The operation of the lutein epoxide cycle correlates with energy dissipation. Functional Plant Biol 30: 319–324CrossRefGoogle Scholar
  35. Gauhl E (1976) Photosynthetic response to varying light intensity in ecotypes of Solanum dulcamara L. from shaded and exposed habitats. Oecologia 27: 278–286Google Scholar
  36. Gilmore A (2004) Excess light stress: probing excitation dissipation mechanisms through global analysis of time-and wavelength-resolved chlorophyll a fluorescence. In: Chlorophyll a Fluorescence: A Signature of Photosynthesis (Papageorgiou G C and Govindjee, eds), pp. 555–581, Springer, DordrechtGoogle Scholar
  37. Heifetz PB, Lers A, Turpin DH, Gillham NW, Boynton JE and Osmond CB (1997) dr and spr/sr mutations of Chlamydomonas reinhardtii affecting D1 protein function and synthesis define two independent steps leading to chronic photoinhibition and confer differential fitness. Plant Cell Environ 20: 1145–1157CrossRefGoogle Scholar
  38. Heifetz PB, Förster B, Osmond CB, Giles LJ and Boynton JE (2000) Effects of acetate on facultative autotrophy in Chlamydomonas reinhardtii assessed by photosynthetic measurements and stable isotope analyses. Plant Physiol 122: 1439– 1445PubMedCrossRefGoogle Scholar
  39. Henley WJ, Levavasseur G, Franklin LA, Osmond CB and Ramus J (1991) Photoacclimation and photoinhibition in Ulva rotundata as influenced by nitrogen availability. Planta 184: 235–243CrossRefGoogle Scholar
  40. Horton P, Ruban AV and Walters RG. (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47: 655–684PubMedCrossRefGoogle Scholar
  41. Jones LW and Kok B (1966) Photoinhibition of chloroplast reactions. I. Kinetics and action spectra. Plant Physiol 41: 1037– 1043PubMedCrossRefGoogle Scholar
  42. Kasahara M, kagawa T, Oikawa K, Suetsugu N, Miyao M and Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420: 829–832PubMedCrossRefGoogle Scholar
  43. Kato MC, Hikosaka K, Hirotsu N, Makino A and Hirose T (2003) The excess light energy that is neither utilized in photosynthesis nor dissipated by photoprotective mechanisms determines the rate of photoinactivation in photosystem II. Plant Cell Physiol 44: 318–325PubMedCrossRefGoogle Scholar
  44. Kok B (1956) On the inhibition of photosynthesis by intense light. Biochim Biophys Acta 21: 234–244PubMedCrossRefGoogle Scholar
  45. Kolber ZS, Prasil O and Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques. I. Defining methodology and experimental protocols. Biochim Biophys Acta 1367: 88–106PubMedCrossRefGoogle Scholar
  46. Kolber Z, KlimovD, Ananyev G, RascherU, Berry J and Osmond B. (2005) Measuring photosynthetic parameters at a distance: Laser Induced Fluorescence Transient (LIFT) method for remote measurements of PSII in terrestrial vegetation. Photosynth Res (in press)Google Scholar
  47. Kozaki H and Takeba G (1996) Photorespiration protects plants from photooxidation. Nature 384: 557–560CrossRefGoogle Scholar
  48. Krause GH (1988) Photoinhibition of photosynthesis: an evaluation of damaging and protective mechanisms. Physiol Plant 74: 566–574CrossRefGoogle Scholar
  49. Krause GH, Kirk M, Heber U and Osmond CB (1978) O2-dependent inhibition of photosynthetic capacity in intact isolated chloroplasts and isolated cells from spinach leaves illuminated in the absence of CO2. Planta 142: 229– 233CrossRefGoogle Scholar
  50. Kyle DJ, Ohad I and Arntzen CJ (1984) Membrane protein damage and repair: selective loss of a quinone-protein function in chloroplast membranes. Proc Natl Acad Sci USA 81: 4070– 4074PubMedCrossRefGoogle Scholar
  51. Laisk A and Oja V (1999) Dynamics of leaf photosynthesis: Rapid response measurements and their interpretation. CSIRO Publishing, Collingwood, AustraliaGoogle Scholar
  52. Lardans A, Förster B, Prásil O, Falkowski PG, Sobolev V, Edelman M, Osmond CB, Gillham NW and Boynton JE (1998) Biophysical, biochemical and physiological characterization of Chlamydomonas reinhardtii mutants with amino acid substitutions at the Ala251 residue in the D1 protein having varying levels of photosynthetic competence. J Biol Chem 272: 11082–11091CrossRefGoogle Scholar
  53. Lee H-Y, Hong Y-N and Chow WS (2001) Photoinactivation of photosystem II complexes and photoprotection by nonfunctional neighbours in CaPS Icum annuum L. leaves. Planta 212: 332–342PubMedCrossRefGoogle Scholar
  54. Li X-P, Gilmore AM and Niyogi K (2002) Molecular and global time-resolved analysis of a psbS gene dosage effect on pH- and xanthophyll cycle-dependent nonphotochemical quenching in photosystem II. J Biol Chem 277: 33590–33597PubMedCrossRefGoogle Scholar
  55. Lorimer GH and Andrews TJ (1973) Plant photorespiration – an inevitable consequence of the existence of atmospheric oxygen. Nature 243: 359CrossRefGoogle Scholar
  56. Lovelock J (1990) The Ages of Gaia. Bantam, New York, pp. xiiiGoogle Scholar
  57. Ludlow MM and Björkman O (1984) Paraheliotropic leaf movement in Siratro as a protectective mechanism against droughtinduced damage to primary photosynthetic reactions by excessive light and heat. Planta 61: 505–518CrossRefGoogle Scholar
  58. Matsubara S and Chow WS (2004) Populations of photoinactivated photosystem II reaction centers characterized by chlorophyll a fluorescence lifetime in vivo. Proc Natl Acad Sci USA 101, 18234–18239Google Scholar
  59. Matsubara S, Gilmore AM and Osmond CB (2001) Diurnal and acclimatory responses of violaxanthin and lutein epoxide in the Australian mistltoe Amyema miquelii. Aust J Plant Physiol 28: 793–800Google Scholar
  60. Matsubara S, Gilmore AM, Ball MC, Anderson JM and Osmond CB (2002) Sustained downregulation of photosystem II in mistletoes during winter depression of photosynthesis. Functional Plant Biol 29: 1157–1169CrossRefGoogle Scholar
  61. Matsubara S, Naumann M, Martin R, Rascher U, Nichol C, Morosinotto T, Bassi R and Osmond B. (2005) Slowly reversible de-epoxidation of lutein-epoxide in deep shade leaves of a tropical tree legume may “lock-in” lutein-based photoprotection during acclimation to strong light. J Exp Bot 56, 461–468PubMedCrossRefGoogle Scholar
  62. Müller-Moulé P, Havaux M and Niyogi KK (2003) Zeaxanthin deficiency enhances the high light sensitivity of an ascorbatedeficient mutant of Arabidopsis. Plant Physiol 133: 748–760PubMedCrossRefGoogle Scholar
  63. Nichol CJ, Huemmrich KF, Black TA, Jarvis PJ, Walthall CL, Grace J and Hall FG (2000) Remote sensing of photosynthesislight- use efficiency of Boreal Forest. Agric For Meterol 101: 131–141CrossRefGoogle Scholar
  64. Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol, 50: 333–359PubMedCrossRefGoogle Scholar
  65. Osmond CB (1981) Photorespiration and photoinhibition, some implications for the energetics of photosynthesis. Biochim Biophys Acta 639: 77–98Google Scholar
  66. Osmond CB (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker NR and Bowyer JR (eds) Photoinhibition: Molecular Mechanisms to the Field pp 1–24. Bios Scientific Publications, OxfordGoogle Scholar
  67. Osmond CB and Björkman O (1972) Simultaneous measurements of O2 effects on net photosynthesis and glycolate metabolism in C3 and C4 species of Atriplex. Carnegie Inst Wash Yearbook 71: 141–148Google Scholar
  68. Osmond CB and Chow WS (1988) Ecology of photosynthesis in the sun and shade: summary and prognostications. Aust J Plant Physiol 15: 1–9Google Scholar
  69. Osmond CB and Grace SC (1995) Photoinhibition and photorespiration: the quintessential inefficiencies of the light and dark reactions of terrestrial oxygenic photosynthesis. J Expt Bot 46: 1351–1362Google Scholar
  70. Osmond CB, Oja V and Laisk A (1988) Regulation of carboxylation and photosynthetic oscillations during sun-shade acclimation in Helianthus annuus measured with a rapid-response gas exchange system. Aust J Plant Physiol 15: 239–251Google Scholar
  71. Osmond CB, Ramus J, Levavasseur G, Franklin LA and Henley WJ (1993) Fluorescence quenching during photosynthesis and photoinhibition of Ulva rotundata. Planta 190: 97–106CrossRefGoogle Scholar
  72. Osmond B, Schwartz O and Gunning B (1999) Photoinhibitory printing on leaves, visualised by chlorophyll fluorescence imaging and confocal microscopy, is due to diminished fluorescence from grana. Aust J Plant Physiol 26: 717–724Google Scholar
  73. Öquist G, Huner NPA (2003) Photosynthesis of overwintering evergreen plants. Annu Rev Plant Biol 54: 329–355PubMedCrossRefGoogle Scholar
  74. Park Y-I, Chow WS. Osmond CB and Anderson JM (1996) Electron transport to oxygen mitigates against the photoinactivation of photosystem II in vivo by both enhanced utilization, and increased non-radiative dissipation, of excess photons. Photosynth Res 50: 23–32CrossRefGoogle Scholar
  75. Powles SB (1984) Photoinhibition of photosynthesis. Annu Rev Plant Physiol 35: 15–44CrossRefGoogle Scholar
  76. Powles SB and Björkman O (1982) Leaf movement in the shade species Oxalis oregana II. Role in the protection against injury by intense light. Carnegie Inst Wash Yearbook 81: 63– 66Google Scholar
  77. Powles SB and Osmond CB (1978) Inhibition of the capacity and efficiency of photosynthesis in bean leaflets illuminated in absence of CO2 at low O2 concentrations – a protective role for photorespiration. Aust J Plant Physiol 5: 619–629Google Scholar
  78. Robinson SA and Osmond CB (1994) Internal gradients of chlorophyll and carotenoid pigments in relation to photoprotection in thick leaves of plants with Crassulacean acid metabolism. Aust J Plant Physiol 21: 497–506CrossRefGoogle Scholar
  79. Russell AW, Critchley C, Robinson SA, Franklin LA, Seaton GGR, Chow WS, Anderson JM and Osmond CB (1996) Photosystem II regulation and dynamics of the chloroplast D1 protein in Arabidopsis leaves during photosynthesis and photoinhibition. Plant Physiol 107: 943–952Google Scholar
  80. Schreiber U, Schliwa U and BilgerW(1986) Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10: 51–62Google Scholar
  81. Shapira M, Lers A, Heifetz PB, Osmond CB, Gillham NW and Boynton JE (1997) Differential regulation of chloroplast gene expression in Chlamydomonas reinhardtii during photoacclimation. Light stress transiently suppresses synthesis of Rubisco LSU protein while enhancing synthesis of the PS II D1 protein. Plant Mol Biol 33: 1001–1011PubMedCrossRefGoogle Scholar
  82. Terashima I and Inoue Y (1985) Vertical gradient in photosynthetic properties of spinach chloroplasts dependent on intraleaf light environment. Plant Cell Physiol 26: 781–785Google Scholar
  83. Walker DA and Osmond CB (1986) Measurement of photosynthesis i nvivo with a leaf disc electrode: correlations between light dependence of steady state photosynthetic O2 evolution and chlorophyll a fluorescence transients. Proc R Soc Lond B 227: 267–280CrossRefGoogle Scholar
  84. Woodrow IE and Mott KA (1998) Quantitative assessment of the degree to which ribulosebisphosphate carboxylase/oxygenase determines the steady–state rate of photosynthesis during sunshade acclimation in Helianthus annuus L. Aust J Plant Physiol 15: 253—262Google Scholar
  85. Yamamoto HY (2005) Arandomwalk to and through the xanthophyll cycle. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 1–10. Springer, DordrechtGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Barry Osmond
    • 1
  • Britta Förster
    • 1
  1. 1.School of Biochemistry and Molecular BiologyThe Australian National UniversityCanberraAustralia

Personalised recommendations