Photosynthesis Research

, Volume 41, Issue 2, pp 315–326 | Cite as

Grana stacking and protection of Photosystem II in thylakoid membranes of higher plant leaves under sustained high irradiance: An hypothesis

  • Jan M. Anderson
  • Eva-Mari Aro
Regular paper

Abstract

We propose yet another function for the unique appressed thylakoids of grana stacks of higher plants, namely that during prolonged high light, the non-functional, photoinhibited PS II centres accumulate as D1 protein degradation is prevented and may act as dissipative conduits to protect other functional PS II centres. The need for this photoprotective mechanism to prevent high D1 protein turnover under excess photons in higher plants, especially those grown in shade, is due to conflicting demands between efficient use of low irradiance and protection from periodic exposure to excessive irradiance.

Key words

D1 protein light acclimation photoinhibition Photosystem II regulation thylakoid membrane domains 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adir N, Shochat S and Ohad I (1990) Light-dependent D1 protein synthesis and translocation is regulated by reaction centre II. J Biol Chem 265: 12563–12568PubMedGoogle Scholar
  2. Anderson JM (1986) Photoregualtion of the composition, function and structure of thylakoid membranes. Annu Rev Plant Physiol 37: 93–136Google Scholar
  3. Anderson JM and Andersson B (1988) The dynamic photosynthetic membrane and regulation of solar energy conversion. Trends Biochem Sci 13: 351–355CrossRefPubMedGoogle Scholar
  4. Anderson JM and Osmond CB (1987) Shade-sun responses: comprimises between acclimation and photoinhibition. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Photoinhibition, pp 1–38. Elsevier, AmsterdamGoogle Scholar
  5. Anderson JM, Chow WS and Goodchild DJ (1988) Thylakoid membrane organisation in sun/shade acclimation. Aust J Plant Physiol 15: 11–26Google Scholar
  6. Andersson B and Styring S (1991) Photosystem II: Molecular organization, function and acclimation. Current Topics in Bioenergetics 16: 1–81Google Scholar
  7. Aro EM (1982) A comparison of the chlorophyll-protein composition and chloroplast ultrastructure in two Bryophytes and two higher plants. Z Pflanzenphysiol 108: 97–105Google Scholar
  8. Aro EM, Kettunen R and Tyystjärvi E (1992) ATP and light regulate D1 protein modification and degradation. Role of D1* on photoinhibition. FEBS Lett 297: 29–33CrossRefPubMedGoogle Scholar
  9. Aro EM, McCaffery S and Anderson JM (1993a) Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances. Plant Physiol 103: 835–843PubMedGoogle Scholar
  10. Aro EM, Virgin I and Andersson B (1993b) Photoinhibition of Photosystem II — inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134PubMedGoogle Scholar
  11. Aro EM, McCaffery S and Anderson JM (1994) Recovery from photoinhibition in peas acclimated to varying growth irradiances: Role of D1 protein turnover. Plant Physiol 104: 1033–1041PubMedGoogle Scholar
  12. Barbato R, Frisco G, Giardi MT, Rigonine F and Giacometti GM (1991) Breakdown of the Photosystem II reaction center protein under photoinhibitory conditions: Identification and localization of the C-terminal degradation products. Biochem 30: 10220–10226Google Scholar
  13. Bennet J (1991) Protein phosphorylation in green plant chloroplasts. Annu Rev Plant Physiol Plant Mol Biol 42: 281–311CrossRefGoogle Scholar
  14. Callahan FE, Ghirardi ML, Sopory SK, Mehta AM, Edelman M and Mattoo AK (1990) A novel metabolic form of the 32 kDa-D1 protein in the grana-localized reaction center of Photosystem II. J Biol Chem 265: 15357–15360PubMedGoogle Scholar
  15. Chow WS (1984) Electron transport, photophosphorylation and thylakoid stacking. In: Sybesma C (ed) Advances in Photosynthesis Research, Vol III, pp 83–86. Martinus Nijhoff/Dr W. Junk Publishers, The HagueGoogle Scholar
  16. Chow WS (1994) Photoprotection and photoinhibitory damage. In: Barber J (ed) Molecular Processes of Photosynthesis, Adv Mol Cell Biol 7 (in press)Google Scholar
  17. Chow WS, Melis A and Anderson JM (1990) Adjustments of photosystem stoichiometry in chloroplasts improve the quantum effeciency of photosynthesis. Proc Natl Acad Sci USA 87: 7502–7506PubMedGoogle Scholar
  18. 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: 69–77Google Scholar
  19. Demmig-Adams B (1990) Carotenoids and photoproduction in plants; a role for the carotenoid zeaxanthin. Biochim Biophys Acta 1020: 1–24Google Scholar
  20. Demmig-Adams B and Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Mol Biol 43: 599–626CrossRefGoogle Scholar
  21. Demmig B and Björkman O (1987) Comparison of the effect on chlorophyll fluorescence (77K) and photon yield on O2 evolution in leaves of higher plants. Planta 171: 171–184Google Scholar
  22. De Vitry C, Diner BA and Popot JL (1991) Photosystem II particles from Chlamydomonas reinhardtii. J Biol Chem 266: 16614–16621PubMedGoogle Scholar
  23. Elich TD, Edelman M and Mattoo AK (1992) Identification, characterization, and resolution of the in vivo phosphorylated form of the D1 Photosystem II reaction center protein. J Biol Chem 267: 3523–3529PubMedGoogle Scholar
  24. Guenther J and Melis A (1990) The physiological significance of Photosystem II heterogeneity in chloroplasts. Photosynth Res 23: 105–109Google Scholar
  25. Haupt W and Scheuerlein R (1990) Chloroplast movement. Plant, Cell Environ 13: 595–614Google Scholar
  26. Horton P and Ruban AV (1992) Regulation of Photosystem II. Photosynth Res 34: 375–385Google Scholar
  27. Izawa S and Good NE (1966) Effect of salts and electron transport on the conformation of isolated chloroplasts. II. Electron microscopy. Plant Physiol 41: 544–552Google Scholar
  28. Kallio T, Aro EM, Jansson C and Mäenpää P (1992). Light-dependent turnover rate of the D1 polypeptide in new site-specific Synechocystis PCC 6803 mutants. In: Murata N (ed) Research in Photosynthesis, Vol IV, pp 419–422 Kluwer Academic Publishers, DordrechtGoogle Scholar
  29. Kanervo E, Mäenpää P and Aro EM (1994) D1 protein degradation and psbA transcript levels in Synechocystis PCC 6803 during photoinhibition in vivo. J Plant Physiol 142: 676–684Google Scholar
  30. Kettunen R, Tyystjärvi E and Aro EM (1991) D1 protein degradation during photoinhibition of intact leaves. A modification of the D1 protein precedes degradation. FEBS Lett 290: 153–156CrossRefPubMedGoogle Scholar
  31. Kettunen R, Lehtonen E, Tyystjärvi E and Aro EM (1992) Degradation products of the D1 protein are located in the non-appressed regions of the thylakoid membranes in vivo. In: Murata N (ed) Research in Photosynthesis, Vol IV, pp 309–316. Kluwer Academic Publishers, DordrechtGoogle Scholar
  32. 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: 4070–4074Google Scholar
  33. Mattoo AK, Hoffman-Falk H, Marder JB and Edelman M (1984) Regulation of protein metabolism: Coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32-kilodalton protein of the chloroplast membranes. Proc Natl Acad Sci USA 81: 1380–1384Google Scholar
  34. Miller KR and Lyon MK (1985) Do we really know why chloroplast membranes stack? Trends Biochem Sci 10: 219–222CrossRefGoogle Scholar
  35. Ohad I, Kyle DJ and Arntzen CJ (1984) Membrane protein damage and repair: removal and replacement of the inactivated 32-kilodalton polypeptides in chloroplast membranes. J Cell Biol 99: 481–485CrossRefPubMedGoogle Scholar
  36. Osmond CB (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker NR and Bowyer JR (eds) Photoinhibition to Photosynthesis: From Molecular Mechanisms to the Environment. Bios Scientific Publications, London (in press)Google Scholar
  37. Öquist G, Anderson JM, McCaffery S and Chow WS (1992a) Mechanistic differences in photoinhibition of sun and shade plants. Planta 18: 422–431Google Scholar
  38. Öquist G, Chow WS and Anderson JM (1992b) Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosynthesis. Plant 186: 450–460CrossRefGoogle Scholar
  39. Porra RJ, Thompson WA and Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975: 384–394Google Scholar
  40. Pràsil O, Adir N and Ohad I (1992) Dynamics of Photosystem II: mechanism of photoinhibition and recovery processes. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology, pp 295–348. Elsevier AmsterdamGoogle Scholar
  41. Raven JA (1989) Fight or flight: the economics of repair and avoidance of photoinhibition of photosynthesis. Func Ecol 3: 5–19Google Scholar
  42. Rintamäki E, Salo R and Aro EM (1992) Turnover of D1 protein during photoinhibition and recovery in a moss Ceratodon purpureus. In: Murata N (ed) Research in Photosynthesis, Vol IV, pp 431–434. Kluwer Academic Publishers, DordrechtGoogle Scholar
  43. Rintamäki E, Salo R and Aro EM (1994) Rapid turnover of the D1 reaction center protein of Photosystem II as a protection mechanism against photoinhibition in a moss, Ceratodon purpureus (Hedw.) Brid. Planta 193: 520–529Google Scholar
  44. Schnettger B, Leitsch J and Krause GH (1992) Photoinhibition of Photosystem 2 in vivo occurring without net D1 protein degradation. Photosynthetica 27: 261–265Google Scholar
  45. Schnettger B, Critchley C, Santore UJ, Graf M and Krause GH (1994) Relationship between photoinhibition of photosynthesis, D1 protein turnover and chloroplast structure: Effects of protein synthesis inhibitors. Plant Cell Environ 17: 55–64Google Scholar
  46. Schuster G, Timberg R and Ohad I (1988) Turnover of thylakoid Photosystem II proteins during photoinhibition of Chlamydomonas reinhardtii. Eur J Biochem 177: 403–410PubMedGoogle Scholar
  47. Staehelin LA (1986) Chloroplast structure and supramolecular organization of photosynthetic membranes. In: Staehelin LA and Arntzen CJ (eds) Photosynthesis III: Photosynthetic membranes and light-harvesting systems, pp 1–84. Springer-Verlag, BerlinGoogle Scholar
  48. Sundby C, McCaffery S, Chow WS and Anderson JM (1992) Photosystem II function, photoinhibition and turnover of D1 protein at different irradiances in normal and atrazine-resistant plants with an altered Qb-binding site. In: Murata N (ed) Research in Photosynthesis, Vol IV, pp 443–446. Kluwer Academic Publishers, DordrechtGoogle Scholar
  49. Sundby C, Chow WS and Anderson JM (1993a) Effects of Photosystem II function, photoinhibition, and plant performance of the spontaneous mutation of serine-264 in the Photosystem II reaction center D1 protein in triazine-resistant Brassica napus L. Plant Physiol 103: 105–113PubMedGoogle Scholar
  50. Sundby C, McCaffery S and Anderson JM (1993b) Turnover of the Photosystem II D1 protein in higher plants under photoinhibitory and non-photoinhibitory irradiance. J Biol Chem 268: 25476–25482PubMedGoogle Scholar
  51. Terashima I (1989) Productive structure of a leaf. In: Briggs WR (ed) Photosynthesis, pp 206–226. Alan R Liss Inc, New YorkGoogle Scholar
  52. Trissl HW and Wilhelm C (1993) Why do thylakoid membranes from higher plants form grana stacks? Trends Biochem Sci 18: 415–419CrossRefPubMedGoogle Scholar
  53. Tyystjärvi E, Ali-Yrkkö K, Kettunen R and Aro EM (1992) Slow degradation of the D1 protein is related to the susceptibility of low-light-grown pumpkin plants to photoinhibition. Plant Physiol 100: 1310–1317Google Scholar
  54. Van Wijk KJ and Van Hasselt P R (1993) Photoinhibition of Photosystem II in vivo is preceded by down-regulation through light-induced acidification of the lumen: Consequences for the mechanism of photoinhibition in vivo. Planta 189: 359–368Google Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • Jan M. Anderson
    • 1
    • 2
  • Eva-Mari Aro
    • 3
  1. 1.Cooperative Research Centre for Plant ScienceCanberraAustralia
  2. 2.Division of Plant IndustryCSIROCanberraAustralia
  3. 3.Department of BiologyUniversity of TurkuTurkuFinland

Personalised recommendations