, Volume 197, Issue 1, pp 176–183 | Cite as

Seasonal changes in photosystem II organisation and pigment composition in Pinus sylvestris

  • Christina Ottander
  • Douglas Campbell
  • Gunnar Öquist


Conifers of the boreal zone encounter considerable combined stress of low temperature and high light during winter, when photosynthetic consumption of excitation energy is blocked. In the evergreen Pinus sylvestris L. these stresses coincided with major seasonal changes in photosystem II (PSII) organisation and pigment composition. The earliest changes occurred in September, before any freezing stress, with initial losses of chlorophyll, the D1-protein of the PSII reaction centre and of PSII light-harvesting-complex (LHC II) proteins. In October there was a transient increase in F0, resulting from detachment of the light-harvesting antennae as reaction centres lost D1. The D1-protein content eventually decreased to 90%, reaching a minimum by December, but PSII photochemical efficiency [variable fluorescence (Fv)/maximum fluorescence (Fm)] did not reach the winter minimum until mid-February. The carotenoid composition varied seasonally with a twofold increase in lutein and the carotenoids of the xanthophyll cycle during winter, while the epoxidation state of the xanthophylls decreased from 0.9 to 0.1 from October to January. The loss of chlorophyll was complete by October and during winter much of the remaining chlorophyll was reorganised in aggregates of specific polypeptide composition, which apparently efficiently quench excitation energy through non-radiative dissipation. The timing of the autumn and winter changes indicated that xanthophyll de-epoxidation correlates with winter quenching of chlorophyll fluorescence while the drop in photochemical efficiency relates more to loss of D1-protein. In April and May recovery of the photochemistry of PSII, protein synthesis, pigment rearrangements and zeaxanthin epoxidation occurred concomitantly. Indoor recovery of photosynthesis in winter-stressed branches under favourable conditions was completed within 3 d, with rapid increases in F0, the epoxidation state of the xanthophylls and in light-harvesting polypeptides, followed by recovery of D1-protein content and Fv/Fm, all without net increase in chlorophyll. The fall and winter reorganisation allow Pinus sylvestris to maintain a large stock of chlorophyll in a quenched, photoprotected state, allowing rapid recovery of photosynthesis in spring.

Key words

Carotenoid Chlorophyll binding polypeptide Low temperature stress Photoinhibition Photo-protection Pinus 



early light-induced proteins


epoxidation state


instantaneous fluorescence


maximum fluorescence


variable fluorescence


light-harvesting complex of PSII


lithium dodecyl sulfate


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  1. Adams, III WW, Demmig-Adams B (1994) Carotenoid composition and down regulation of photosystem II in three conifer species during the winter. Physiol Plant 92: 451–458CrossRefGoogle Scholar
  2. Andersen B, Koch B, Scheller HV (1992) Structural and functional analysis of the reducing side of photosystem I. Physiol Plant 84: 154–161Google Scholar
  3. Anderson JM, Aro E-M (1994) Grana stacking and protection of photosystem II in thylakoid membranes of higher plant leaves under sustained high irradiance: An hypothesis. Photosynth Res 41: 315–326Google Scholar
  4. Bartels D, Hanke C, Schneider K, Michel D, Salamini F (1992) A desiccation related Elip-like gene from the resurrection plant Craterostigma plantagineum is regulated by light and ABA. EMBO J 11: 2271–2778Google Scholar
  5. Britton G (1993) Carotenoids in chloroplast pigment-protein complexes. In: Sundqvist C (ed) Pigment protein complexes in plastids: Synthesis and assembly (Cell biology: A series of monographs). Academic Press, San Diego, pp 447–483Google Scholar
  6. Butler WL (1978) Energy distribution in the photochemical apparatus of photosynthesis. Annu Rev Plant Physiol 29: 345–378CrossRefGoogle Scholar
  7. Campbell DA, Basalyga S, Hayden DB (1991) Characterization of maize mesophyll photosystem II light-harvesting complexes separated by a mildly-denaturing electrophoretic method. Plant Physiol Biochem 29: 615–621Google Scholar
  8. Cattivelli L, Bartels D (1992) Biochemistry and molecular biology of cold-inducible enzymes and proteins in higher plants. Soc Exp Biol Sem Ser 49: 267–288Google Scholar
  9. Clarke AK, Critchley C (1992) The identification of a heat-shock protein complex in chloroplast of barley leaves. Plant Physiol 100: 2081–2089Google Scholar
  10. Clarke AK, Soitamo A, Gustafsson P, Öquist G (1993) Rapid interchange between two distinct form of cyanobacterial photosystem II reaction-center protein D1 in response to photoinhibition. Proc Natl Acad Sci USA 90: 9973–9977Google Scholar
  11. Demmig-Adams B (1990) Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020: 1–24CrossRefGoogle Scholar
  12. Demmig-Adams B, Adams, III WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43: 599–626CrossRefGoogle Scholar
  13. Eickmeier WG, Casper C, Osmond CB (1993) Chlorophyll fluorescence in the resurrection plant Selaginella leipidophylla (Hook. & Grev.) Spring during high-light and desiccation stress, and evidence for zeaxanthin-associated photoprotection. Planta 189: 30–38Google Scholar
  14. Fling SP, Gregerson DS (1986) Peptide and protein molecular weight determination by electrophoresis using a high-molarity Tris-buffer system without urea. Anal Biochem 155: 83–88Google Scholar
  15. Frank HA, Cua A, Chynwat V, Young A, Gosztola D, Wasielewski MR (1994) Photophysics of the Carotenoids associated with the xanthophyll cycle in photosynthesis. Photosynth Res 41: 389–395Google Scholar
  16. Funk C, Schröder WP, Green BR, Renger G, Andersson B (1994) The intrinsic 22 kDa protein is a chlorophyll-binding subunit of photosystem II. FEBS Lett 342: 261–266Google Scholar
  17. Gilmore AM, Yamamoto HY (1991) Resolution of lutein and zeaxanthin using a non-endcapped, lightly carbon-loaded C18 high-performance liquid Chromatographic column. J Chromatogr 543: 137–145Google Scholar
  18. Gilmore AM, Yamamoto HY (1993) Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. Photosynth Res 35: 67–78Google Scholar
  19. Greer DH, Berry JA, Björkman O (1986) Photoinhibition of photosynthesis in intact bean leaves: role of light and temperature, and requirement for chloroplast-protein synthesis during recovery. Planta 168: 253–260Google Scholar
  20. Hällgren J-E, Lundmark T, Strand M (1990) Photosynthesis of Scots pine in the field after night frosts during summer. Plant Physiol Biochem 28: 437–445Google Scholar
  21. Henrysson T, Schröder WP, Spangfort M, Åkerlund H-E (1989) Isolation and characterization of the chlorophyll a/b protein complex CP29 from spinach. Biochim Biophys Acta 977: 301–308Google Scholar
  22. Huner NPA, Krol M, Williams JP, Maissan E, Low PS, Roberts D, Thompson JP (1987) Low temperature development induces a specific decrease in trans-delta3-hexadecenoic acid content which influences LHC II organisation. Plant Physiol 84: 12–18Google Scholar
  23. Irrgang K-D, Kablitz B, Vater J, Renger G (1993) Identification, isolation and partial characterization of a 14–15 kDa pigment binding protein complex of PS II from spinach. Biochim Biophys Acta 1143: 173–182Google Scholar
  24. Krupa Z, Öquist G, Gustafsson P (1991) Photoinhibition of photosynthesis and growth responses at different light levels in psbA gene mutants of the cyanobacterium Synechoccus. Physiol Plant 82: 1–8Google Scholar
  25. Lers A, Levy H, Zamir A (1991) Co-regulation of a gene homologous to early light-induced genes in higher plants and β-carotene biosynthesis in the alga Dunaliella bardawil. J Biol Chem266: 13698–13705Google Scholar
  26. Levitt J (1980) Responses of plants to environmental stresses, 2nd edn. Vol. 1. Chilling, freezing and high temperature stresses. Academic Press, New YorkGoogle Scholar
  27. Levy H, Gokhman I, Zamir A (1992) Regulation and light-harvesting complex II association of a Dunaliella protein homologous to early light-induced proteins in higher plants. J Biol Chem267: 18831–18836Google Scholar
  28. Levy H, Tamar T, Shaish A, Zamir A (1993) Cbr, an algal homology of plant early light-induced proteins, is a putative zeaxanthin binding protein. J Biol Chem 268: 20892–20896Google Scholar
  29. Ljungberg U, Åkerlund H-E, Andersson B (1986) Isolation and characterization of the 10-kDa and 22-kDa polypeptides of higher plant photosystem II. Eur J Biochem 158: 477–482Google Scholar
  30. Martin B, Mårtensson O, Öquist G (1978) Seasonal effects on photosynthetic electron transport and fluorescence properties in isolated chloroplasts of Pinus sylvestris. Physiol Plant 44: 102–109Google Scholar
  31. Martin B, Öquist G (1979) Seasonal and experimentally induced changes in the ultrastructure of chloroplasts of Pinus sylvestris. Physiol Plant 46: 42–49Google Scholar
  32. Näsholm T, Ericsson A (1990) Seasonal changes in amino acids, protein and total nitrogen in needles of fertilized Scots pine trees. Tree Physiol 6: 267–281Google Scholar
  33. Öquist G, Ögren E (1985) Effects of winter stress on photosynthetic electron transport and energy distribution between the two photosystems of pine as assayed by chlorophyll fluorescence kinetics. Photosynth Res 7: 19–30Google Scholar
  34. Öquist G, Malmberg G (1989) Light and temperature dependent inhibition of photosynthesis in frost-hardened and un-hardened seedlings of pine. Photosynth Res 20: 261–277Google Scholar
  35. Ottander C, Öquist G (1991) Recovery of photosynthesis in winterstressed Scots pine. Plant Cell Environ 14: 345–349Google Scholar
  36. Ottander C, Hundal T, Andersson B, Huner NPA, Öquist G (1993) Photosystem II reaction centres stay intact during low temperature photoinhibition. Photosynth Res 35: 191–200Google Scholar
  37. Peterson GL (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83: 346–356PubMedGoogle Scholar
  38. Porra RJ, Thompson WA, 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
  39. Pötter E, Kloppstech K (1993) Effects of light stress on the expression of early light-inducible proteins. Eur J Biochem 214: 779–786Google Scholar
  40. Samuelsson G, Lönneborg A, Rosenqvist E, Gustafsson P, Öquist G (1985) Photoinhibition and reactivation of photosynthesis in the cyanobacterium Anacystis nidulans. Plant Physiol 79: 922–995Google Scholar
  41. Selstam E, Öquist G (1985) Effects of frost hardening on the composition of galactolipids and phospholipids occurring during isolation of chloroplast thylakoids from needles of Scots pine. Plant Sci 42: 41–48Google Scholar
  42. Selstam E, Gezelius K, Ottander C (1990) Lipid composition, photosynthetic activity and Rubisco activity in frost hardened Scots pine needles after freezing and recovery. Abstract No. 604. Physiol Plant 79: 106Google Scholar
  43. Senser M, Schötz F, Beck E (1975) Seasonal changes in structure and function of spruce chloroplasts. Planta 126: 1–10Google Scholar
  44. Soikkeli S (1980) Ultrastructure of the mesophyll in Scots pine and Norway spruce: Seasonal variation and molarity of the fixative buffer. Protoplasma 103: 241–252Google Scholar
  45. Strand M, Öquist G (1985) Inhibition of freezing temperatures and high light levels in cold-acclimated seedlings of Scots pine (Pinus sylvestris). I. Effects on the light-limited and light-saturated rates of CO2 assimilation. Physiol Plant 64: 425–430Google Scholar
  46. Strand M, Öquist G (1988) Effects of frost hardening, dehardening and freezing stress on in vivo chlorophyll fluorescence of Scots pine seedlings (Pinus sylvestris L.). Plant Cell Environ 11: 231–238Google Scholar
  47. Thayer SS, Björkman O (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynth Res 23: 311–343Google Scholar
  48. Waldron JC, Anderson JA (1979) Chlorophyll-protein complexes from thylakoids of a mutant barley lacking chlorophyll b. Eur J Biochem 102: 357–362Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • Christina Ottander
    • 1
  • Douglas Campbell
    • 1
  • Gunnar Öquist
    • 1
  1. 1.Department of Plant PhysiologyUniversity of UmeåUmeåSweden

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