Photosynthetica 2004, 42(3):377-386 | DOI: 10.1023/B:PHOT.0000046156.00556.b4

Minimization of the Photon Energy Absorbed by 'Closed' Reaction Centers of Photosystem 2 as a Photoprotective Strategy in Higher Plants

D. Kornyeyev1,2, A.S. Holaday2, B.A. Logan3
1 Institute of Plant Physiology and Genetics, Ukraine
2 Department of Biological Sciences, Texas Tech University, Lubbock, USA
3 Department of Biology, Bowdoin College, USA

Photoinactivation of photosystem 2 (PS2) results from absorption of so-called "excessive" photon energy. Chlorophyll a fluorescence can be applied to quantitatively estimate the portion of excessive photons by means of the parameter E = (F - F0')/Fm', which reflects the share of the absorbed photon energy that reaches the reaction centers (RCs) of PS2 complexes with QA in the reduced state ('closed' RCs). Data obtained for cotton (Gossypium hirsutum), bean (Phaseolus vulgaris), and arabidopsis (Arabidopsis thaliana) suggest a linear relationship between the total amount of the photon energy absorbed in excess (excessive irradiation) and the decline in PS2 activity, though the slope may differ depending on the species. This relationship was sensitive not only to the leaf temperature but also to treatment with methyl viologen. Such observations imply that the intensity of the oxidative stress as well as the plant's ability to detoxify active oxygen species may interact to determine the damaging potential of the excessive photons absorbed by PS2 antennae. Energy partitioning in PS2 complexes was adjusted during adaptation to irradiation and in response to a decrease in leaf temperature to minimize the excitation energy that is trapped by 'closed' PS2 RCs. The same amount of the excessive photons absorbed by PS2 antennae led to a greater decrease in PS2 activity at warmer temperatures, however, the delay in the development of non-photochemical and photochemical energy quenching under lower temperature resulted in faster accumulation of excessive photons during induction. Irradiance response curves of EF suggest that, at high irradiance (above 700 μmol m-2 s-1), steady-state levels of this parameter tend to be similar regardless of the leaf temperature.

Additional key words: Arabidopsis; chlorophyll a fluorescence; excessive photons; Gossypium; lincomycin; methyl viologen; non-photochemical quenching; Phaseolus; photoinhibition

Published: September 1, 2004  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Kornyeyev, D., Holaday, A.S., & Logan, B.A. (2004). Minimization of the Photon Energy Absorbed by 'Closed' Reaction Centers of Photosystem 2 as a Photoprotective Strategy in Higher Plants. Photosynthetica42(3), 377-386. doi: 10.1023/B:PHOT.0000046156.00556.b4
Download citation

References

  1. Adams, W.W., III, Demmig-Adams, B., Verhoeven, A.S., Barker, D.H.: 'Photoinhibition' during winter stress: invol-vement of sustained xanthophyll cycle-dependent energy dis-sipation.-Aust. J. Plant Physiol. 22: 261-276, 1994. Go to original source...
  2. Anderson, B., Barber, J.: Mechanisms of photodamage and protein degradation during photoinhibition of photosystem II.-In: Baker, N.R. (ed.): Photosynthesis and Environment. Pp. 101-121. Kluwer Academic Publ., Dordrecht 1996. Go to original source...
  3. Aro, E.-M., Hundal, T., Carlberg, I., Andersson, B.: In vitro stu-dies on light-induced inhibition of Photosystem II and D1-protein degradation at low temperature.-Biochim. biophys. Acta 1019: 269-275, 1990. Go to original source...
  4. Aro, E.-M., McCaffery, S., Anderson, J.M.: Recovery from photoinhibition in peas (Pisum sativum L.) acclimated to varying growth irradiances. Role of D1 protein turnover.-Plant Physiol. 104: 1033-1041, 1994. Go to original source...
  5. Bilger, W., Björkman, O.: Relationships among violaxanthin deepoxidation, thylakoid membrane conformation, and non-photochemical chlorophyll fluorescence quenching in leaves of cotton (Gossypium hirsutum L.).-Planta 193: 238-246, 1994. Go to original source...
  6. Björkman, O., Demmig, B.: Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins.-Planta 170: 489-504, 1987. Go to original source...
  7. Demmig-Adams, B., Adams, W.W., III: Photoprotection and other responses of plants to high light stress.-Annu. Rev. Plant Physiol. Plant mol. Biol. 43: 599-626, 1992. Go to original source...
  8. Demmig-Adams, B., Adams, W.W., III, Baker, D.H., Logan, B.A., Bowling, D.R., Verhoeven, A.S.: Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation.-Physiol. Plant. 98: 253-264, 1996. Go to original source...
  9. Fleck, I., Aranda, X., Omari, B.L., Permanyer, J., Abadia, A., Hogan, K.P.: Light energy dissipation in Quercus ilex resprouts after fire.-Aust. J. Plant Physiol. 27: 129-137, 2000. Go to original source...
  10. Genty, B., Briantais, J.-M., Baker, N.R.: The relationship between the quantum yield of photosynthetic electron trans-port and quenching of chlorophyll fluorescence.-Biochim. biophys. Acta 990: 87-92, 1989. Go to original source...
  11. Gorbunov, M., Kobler, Z.S., Lesser, M.P., Falkowski, P.G.: Photosynthesis and photoprotection in symbiotic corals.-Limnol. Oceanogr. 46: 75-85, 2001. Go to original source...
  12. Harbinson, J., Genty, B., Baker, N.R.: Relationship between the quantum efficiencies of photosystems I and II in pea leaves.-Plant Physiol. 90: 1029-1034, 1989. Go to original source...
  13. Henmi, T., Miyao, M., Yamamoto, Y.: Release and reactive-oxygen-mediated damage of the oxygen-evolving complex subunits of PSII during photoinhibition.-Plant Cell Physiol. 45: 243-250, 2004. Go to original source...
  14. Kato, M.C., Hikosaka, K., Hirotsu, N., Makino, A., Hirose, T.: The excess light energy that is neither utilized in photosyn-thesis nor dissipated by photoprotective mechanisms deter-mines the rate of photoinactivation in photosystem II.-Plant Cell Physiol. 44: 318-325, 2003. Go to original source...
  15. Kornyeyev, D., Holaday, A.S., Logan, B.A.: Predicting the ex-tent of photosystem II photoinactivation using chlorophyll a fluorescence parameters measured during illumination.-Plant Cell Physiol. 44: 1064-1070, 2003. Go to original source...
  16. Kornyeyev, D., Logan, B.A., Holaday, A.S.: A chlorophyll fluo-rescence analysis of the allocation of radiant energy absorbed in photosystem 2 antennae of cotton leaves during exposure to chilling.-Photosynthetica 40: 77-84, 2002. Go to original source...
  17. Kornyeyev, D., Logan, B.A., Payton, P., Allen, R.D., Holaday, A.S.: Enhanced photochemical light utilization and decreased chilling-induced photoinhibition of photosystem II in cotton overexpressing genes encoding chloroplast-targeted anti-oxidant enzymes.-Physiol. Plant. 113: 324-332, 2001. Go to original source...
  18. Krall, J.P., Edwards, G.E.: Relationship between photosystem II activity and CO2 fixation in leaves.-Physiol. Plant. 86: 180-187, 1992. Go to original source...
  19. Kruse, O., Zheleva, D., Barber, J.: Stabilization of photosystem two dimers by phosphorylation: implication for the regulation of the turnover of D1 protein.-FEBS Lett. 408: 276-280, 1997. Go to original source...
  20. Lee, H.-Y., Hong, Y.-N., Chow, W.S.: Photoinactivation of photosystem II complexes and photoprotection by non-func-tional neighbours in Capsicum annuum L. leaves.-Planta 212: 332-342, 2001. Go to original source...
  21. Lima, A.L.S., DaMatta, F.M., Pinheiro, H., Totola, M.R., Loureiro, M.E.: Photochemical responses and oxidative stress in two clones of Coffea canephora under water deficit condi-tions.-Environ. exp. Bot. 47: 239-247, 2002. Go to original source...
  22. Linger, P., Brüggemann, W.: Correlation between chlorophyll fluorescence quenching parameters and photosynthesis in a segregating Lycopersicon esculentum ×L. peruvianum popula-tion as measured under constant conditions.-Photosynth. Res. 61: 145-156, 1999. Go to original source...
  23. Logan, B.A., Grace, S.C., Adams, W.W., III, Demmig-Adams, B.: Seasonal differences in xanthophyll cycle characteristics and antioxidants in Mahonia repens growing in different light environments.-Oecologia 116: 9-17, 1998. Go to original source...
  24. Manter, D.K.: Energy dissipation and photoinhibition in Douglas-fir needles with fungal-mediated reduction in photo-synthetic rates.-J. Phytopathol. 150: 674-679, 2002. Go to original source...
  25. Martin, C.E., Tuffers, A., Herppich, W.B., Willert, D.J. von: Utilization and dissipation of absorbed light energy in the epi-phytic crassulacean acid metabolism bromeliad Tillandsia oinantha.-Int. J. Plant Sci. 160: 307-313, 1999. Go to original source...
  26. Maxwell, D.P., Falk, S., Huner, N.P.A.: Photosystem II excitation pressure and development of resistance to photoinhibition.-Plant Physiol. 107: 687-694, 1995. Go to original source...
  27. Melis, A.: Photosystem-II damage and repair cycle in chloro-plasts: what modulates the rate of photodamage in vivo?-Trends Plant Sci. 4: 130-135, 1999. Go to original source...
  28. Morales, F., Belkhodja, R., Abadía, A., Abadía, J.: Photosystem II efficiency and mechanisms of energy dissipation in iron-de-ficient, field-grown pear trees (Pyrus communis L.).-Photosynth. Res. 63: 9-21, 2000. Go to original source...
  29. Niinemets, Ñ., Kull, O.: Sensitivity of photosynthetic electron transport to photoinhibition in a temperate deciduous forest canopy: Photosystem II center openness, non-radiative energy dissipation and excess irradiance under field conditions.-Tree Physiol. 21: 899-914, 2001. Go to original source...
  30. Noguchi, T.: Dual role of triplet localization on the accessory chlorophyll in the photosystem II reaction center: photo-protection and photodamage of the D1 protein.-Plant Cell Physiol. 43: 1112-1116, 2002. Go to original source...
  31. Ögren, E.: Prediction of photoinhibition of photosynthesis from measurements of fluorescence quenching components.-Planta 184: 538-544, 1991. Go to original source...
  32. Olivera, G., Penuelas, J.: Allocation of absorbed light energy in-to photochemistry and dissipation in a semi-deciduous and an evergreen Mediterranean woody species during winter.-Aust. J. Plant Physiol. 28: 471-480, 2001.
  33. Öquist, G., Chow, W.S., Anderson, J.M.: Photoinhibition of photosynthesis represents a mechanism for the long-term re-gulation of photosystem II.-Planta 186: 450-460, 1992. Go to original source...
  34. Osmond, C.B.: What is photoinhibition? Some insights from comparisons of shade and sun plants.-In: Baker, N.R., Bowyer, J.R. (ed.): Photoinhibition of Photosynthesis: from Molecular Mechanisms to the Field. Pp. 1-24. Bios Scientific Publ., Oxford 1994.
  35. Osmond, C.B., Ramus, J., Levavasseur, G., Franklin, L.A., Henley, W.J.: Fluorescence quenching during photosynthesis.D. KORNYEYEV et al. 386 and photoinhibition of Ulva rotundata Blid.-Planta 190: 97-106, 1993. Go to original source...
  36. Ottander, C., Hundal, T., Andersson, B., Huner, N.P.A., Öquist, G.: Photosystem II reaction centres stay intact during low temperature photoinhibition.-Photosynth. Res. 35: 191-200, 1993. Go to original source...
  37. Oxborough, K., Baker, N.R.: An evaluation of the potential trig-gers of photoinactivation of photosystem II in the context of a Stern-Volmer model for downregulation and the reversible ra-dical pair equilibrium model.-Phil. Trans. roy. Soc. London B 355: 1489-1498, 2000. Go to original source...
  38. Park, Y.-I., Chow, W.S., Anderson, J.M.: Light inactivation of functional photosystem II in leaves of peas grown in moderate light depends on photon exposure.-Planta 196: 401-411, 1995. Go to original source...
  39. Park, Y.-I., Chow, W.S., Anderson, J.M.: Chloroplast move-ment in the shade plant Tradescantia albiflora helps protect photosystem II against light stress.-Plant Physiol. 111: 867-875, 1996. Go to original source...
  40. Pickering, J.W., Moes, C.J.M., Sterenborg, H.J.C.M., Prahl, S.A., van Gemert, M.J.C.: Two integrative spheres with an in-verting scattering sample.-J. opt. Soc. Amer. A 9: 621-631, 1992. Go to original source...
  41. Roberts, A., Borland, A.M., Maxwell, K., Griffiths, H.: Ecophysiology of the C3-CAM intermediate Clusia minor L. in Trinidad: seasonal and short-term photosynthetic characte-ristics of sun and shade leaves.-J. exp. Bot. 49: 1563-1573, 1998. Go to original source...
  42. Rohá É ek, K.: Chlorophyll fluorescence parameters: the defi-nitions, photosynthetic meaning, and mutual relationships.-Photosynthetica 40: 13-29, 2002.
  43. Salonen, M., Aro, E.-M., Rintamäki, E.: Reversible phos-phorylation and turnover of the D1 protein under various re-dox states of Photosystem II induced by low temperature photoinhibition.-Photosynth. Res. 58: 143-151, 1998. Go to original source...
  44. Schnettger, B., Critchley, C., Santore, U.J., Graf, M., Krause, G.H.: Relationship between photoinhibition of photosynthesis, D1 protein turnover and chloroplast structure: effects of protein synthesis inhibitors.-Plant Cell Environ. 17: 55-64, 1994. Go to original source...
  45. Schreiber, U., Schliwa, U., Bilger, W.: Continuous recording of photochemical and non-photochemical chlorophyll fluo-rescence quenching with a new type of modulation fluoro-meter.-Photosynth. Res. 10: 51-62, 1986. Go to original source...
  46. Shirke, P.A., Pathre, U.V.: Diurnal and seasonal changes in photosynthesis and photosystem 2 photochemical efficiency in Prosopis juliflora leaves subjected to natural environmental stress.-Photosynthetica 41: 83-89, 2003. Go to original source...
  47. Tsonev, T.D., Hikosaka, K.: Contribution of photosynthetic electron transport, heat dissipation, and recovery of photo-inactivated photosystem II to photoprotection at different tem-peratures in Chenopodium album leaves.-Plant Cell Physiol.44: 828-835, 2003. Go to original source...
  48. Tyystjärvi, E., Aro, E.-M.: The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly propor-tional to light intensity.-Proc. nat. Acad. Sci. USA 93: 2213-2218, 1996. Go to original source...
  49. Van Kooten, O., Snel, J.F.H.: The use of chlorophyll fluores-cence nomenclature in plant stress physiology.-Photosynth. Res. 25: 147-150, 1990. Go to original source...
  50. Vavilin, D.V., Tyystjärvi, E., Aro, E.-M.: In search of a reversible stage of photoinhibition in a higher plant: No changes in the amount of functional Photosystem II accompany relaxation of variable fluorescence after exposure of lincomycin-treated Cucurbita pepo leaves to high light.-Photosynth. Res. 45: 239-247, 1995. Go to original source...
  51. Weis, E., Lechtenberg, D.: Fluorescence analysis during steady-state photosynthesis.-Phil. Trans. roy. Soc. London B 323: 253-268, 1989. Go to original source...