Efficiency of the Photosynthetic Apparatus in Developing Needles of Norway Spruce (Picea abies L. Karst.)

Abstract

The photosynthetic performance of developing spruce (Picea abies L. Karst.) needles was investigated. As revealed by previous reports, the biosynthesis of chlorophylls and carotenoids was not following the characteristic chloroplast ultrastructure building up during needle elongation process. The aim of our study was to investigate photosynthetic capability (evaluated by oxygen evolution and chlorophyll a fluorescence kinetics measurements), the dynamics of chloroplast pigments biosynthesis and the expression of major photosynthetic proteins as well as to find out possible correlation between components of issue. Low amounts of chlorophylls and carotenoids, LHC II and Rubisco LSU were detected in the embryonic shoot of vegetative buds. Although PS II was functional, oxygen production was not sufficient to compensate for respiration in the same developmental stage. The light compensation point of respiration was successively lowered during the needle elongation. Nevertheless the significant increase in photosynthetic pigments as well as the high level of expression of LHC II and Rubisco LSU proteins was observed in the later stages of needle development. Our results suggest that, besides light, some other environmental factors could be critical for producing fully functional chloroplasts in rapidly growing young needles.

References

  1. 1.

    Akoyunoglou, G., Argyroudi-Akoyunoglou, J. (1986) Post-translational regulation of chloroplast differentiation. In: Akoyunoglou, G., Senger, H. (eds) Regulation of Chloroplast Differentiation. Proc. Int. Meeting Regulation of Chloroplast Differentiation, Rhodes, Greece, pp. 571–582.

    Google Scholar 

  2. 2.

    Barber, J., Nield, J., Morris, E. P., Zheleva, D., Hankamer, B. (1997) The structure, function and dynamics of photosystem two. Physiol. Plant. 100, 817–827.

    CAS  Article  Google Scholar 

  3. 3.

    Bartlett, D. W., Dodge, A. D. (1980) Chlorophyll formation and the development of photosynthesis in dark grown seedlings of Picea abies. Physiol. Plant. 49, 473–476.

    CAS  Article  Google Scholar 

  4. 4.

    Bilkova, J., Albrechtova, J., Opatrna, J. (1999) Histochemical detection and image analysis of nonspecific esterase activity and the amount of polyphenols during annual bud development in Norway spruce. J. Exp. Bot. 35, 1129–1138.

    Article  Google Scholar 

  5. 5.

    Boekema, E. J., van Roon, H., van Breeman, J. F. L., Dekker, J. P. (1999) Supramolecular organisation of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Eur. J. Biochem. 266, 444–452.

    CAS  Article  Google Scholar 

  6. 6.

    Boekema, E. J., van Breeman, J. F. L., van Roon, H., Dekker, J. P. (2000) Conformational changes in photosystem II supercomplexes upon removal of extrinsic subunits. Biochem. 39, 12907–12915.

    CAS  Article  Google Scholar 

  7. 7.

    Bogdanović, M. (1973) Chlorophyll formation in the dark. I. Chlorophyll in pine seedlings. Physiol. Plant. 29, 17–18.

    Article  Google Scholar 

  8. 8.

    Cesar, V., Bornman, C. H. (1996) Anatomy of vegetative buds of Norway spruce (Picea abies) with special reference to their exchange from winter to spring. Nat. Croat. 5, 99–108.

    Google Scholar 

  9. 9.

    Cesar, V., Lepeduŝ, H., Has-Schőn, E. (2001) Total soluble proteins amount in vegetative buds and needles of Norway spruce during the bursting time. Acta Bot. Hung. 43, 299–309.

    CAS  Article  Google Scholar 

  10. 10.

    Demmig-Adams, B., Adams III, W. W. (1996) The role of the xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci. 1, 21–26.

    Article  Google Scholar 

  11. 11.

    Eastman, P. A. K., Camm, E. L. (1995) Regulation of photosynthesis in interior spruce during water stress: changes in gas exchange and chlorophyll fluorescence. Tree Physiol. 15, 229–235.

    CAS  Article  Google Scholar 

  12. 12.

    Egger, B., Hampp, R. (1996) Activities of enzymes of starch metabolism in developing Norway spruce [Picea abies (L.) Karst] needles. Trees 11, 72–75.

    Google Scholar 

  13. 13.

    Fischbach, R. J., Kossmann, B., Panten, H., Steinbrecher, R., Heller, W., Seidlitz, H. K., Sandermann, H., Hertkorn, N., Schnitzler, J. P. (1999) Seasonal accumulation of ultraviolet-B screening pigments in needles of Norway spruce (Picea abies (L.) Karst.). Plant, Cell and Environment 22, 27–37.

    CAS  Article  Google Scholar 

  14. 14.

    Forreiter, C., Apel, K. (1993) Light-independent and light-dependent protochlorophyllide-reducing activities and two distinct NADPH-protochlorophyllide oxidoreductase polypeptides in mountain pine (Pinus mugo). Planta 190, 536–545.

    CAS  Article  Google Scholar 

  15. 15.

    Fulgosi, H., Lepedus, H., Cesar, V., Ljubesic, N. (2005) Differential accumulation of preprotein translocon components during spruce (Picea abies L. Karst.) needle development. Biol. Chem. 386, 777–783.

    CAS  Article  Google Scholar 

  16. 16.

    Galliano, H., Heller, W., Sandermann, H. Jr. (1993) Ozone induction and purification of spruce cyn-namyl alcohol dehydrogenase. Phytochem. 32, 557–563.

    CAS  Article  Google Scholar 

  17. 17.

    Gordon, D. C., Percy, K. E., Riding, R. T. (1998) Effects of u.v.-B radiation on epicuticular wax production and chemical composition of four Picea species. New Phytol. 138, 441–449.

    CAS  Article  Google Scholar 

  18. 18.

    Hampp, R., Egger, B., Effenberger, S., Einig, W. (1994) Carbon allocation in developing spruce needles. Enzymes and intermediates of sucrose metabolism. Physiol. Plant. 90, 299–306.

    CAS  Article  Google Scholar 

  19. 19.

    Hejnowicz, A., Obarska, E. (1995) Structure and development of vegetative buds, form the lower crown of Picea abies. Ann. Sci. For. 52, 433–447.

    Article  Google Scholar 

  20. 20.

    Krall, J. P., Edwards, G. E. (1992) Relationship between photosystem II activity and CO2 fixation in leaves. Physiol. Plant. 86, 180–187.

    CAS  Article  Google Scholar 

  21. 21.

    Kraus, C. A., Spitteller, G. (1997) Phenolic compounds from ageing shoots of Picea abies. X. Naturforsch 52c, 308–312.

    Google Scholar 

  22. 22.

    Kűhlbrandt, W. (1994) Structure and function of the plant light harvesting complex, LHC-II. Curr. Biol. 4, 519–528.

    Article  Google Scholar 

  23. 23.

    Jilani, A., Kar, S., Bose, S., Tripathy, B. C. (1996) Regulation of carotenoids content and chloroplast development by levulinic acid. Physiol. Plant. 96, 139–145.

    CAS  Article  Google Scholar 

  24. 24.

    Lepeduš, H., Cesar, V., Ljubešić, N. (2001) Chloroplast ultrastructure and chlorophyll levels in vegetative buds and needles of Norway spruce (Picea abies L. Karst.). Period. Biol. 103, 61–65.

    Google Scholar 

  25. 25.

    Lepeduš, H., Cesar, V., Ljubešić, N., Has-Schon, E. (2003) Photo synthetic pigments, chloroplast distribution and fine structure in vegetative buds of two spruce species. Biologia 58, 867–873.

    Google Scholar 

  26. 26.

    Lichtenthaler, H. K. (1987) Chlorophyll and carotenoids: pigments of photosythetic biomembranes. Methods Enzymol. 148, 350–382.

    CAS  Article  Google Scholar 

  27. 27.

    Lipavska, H., Svobodova, H., Albrechtova, J. (2000) Annual dynamics of the content of non-structural saccharides in the context of structural development of vegetative buds of Norway spruce. J. Plant Physiol. 157, 365–373.

    CAS  Article  Google Scholar 

  28. 28.

    Muraja Ljubičić, J., Wrischer, M., Ljubesic, N. (1998) Formation of the photo synthetic apparatus in plastids during greening of potato microtubers. Plant Physiol. Biochem. 36, 747–752.

    Article  Google Scholar 

  29. 29.

    Muramatsu, S., Kojima, K., Igasaki, T., Yoshitaka, A., Shinohara, K. (2001) Inhibition of the light-independent synthesis of chlorophyll in pine cotyledons at low temperature. Plant Cell Physiol. 42, 868–872.

    CAS  Article  Google Scholar 

  30. 30.

    Polle, A., Otter, T., Seifert, F. (1994) Apoplastic peroxidases and lignification in needles of Norway spruce (Picea abies L.). Plant Physiol. 106, 53–60.

    CAS  Article  Google Scholar 

  31. 31.

    Plumely, G., Schmidt, G. W. (1995) Light-harvesting chlorophyll a/b complexes: Interdependent pigment synthesis and protein assembly. Plant Cell 7, 689–704.

    Article  Google Scholar 

  32. 32.

    Schreiber, U., Bilger, W., Neubauer, C. (1994) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. Ecological Studies 100, 49–70.

    CAS  Google Scholar 

  33. 33.

    Sieferman-Harms, D. (1987) The light-harvesting and protective functions of carotenoids in photo-syntetic membranes. Physiol. Plant. 69, 561–568.

    Article  Google Scholar 

  34. 34.

    Senser, M., Schotz, F., Beck, E. (1975) Seasonal changes in structure and function of spruce chloro-plasts. Planta (Berl.) 126, 1–10.

    CAS  Article  Google Scholar 

  35. 35.

    Slimestad, R., Hostettmann, K. (1996) Characterisation of phenolic constituents from juvenile and mature needles of Norway spruce by means of high performance liquid chromatography - mass spec-tormetry. Phytochem. Anal. 7, 42–48.

    CAS  Article  Google Scholar 

  36. 36.

    Tenberge, K. B. (1992) Ultrastructure and development of the outer epidermal wall of spruce (Picea abies) needles. Can. J. Bot. 70, 1467–1487.

    Article  Google Scholar 

  37. 37.

    Teramoto, H., Nakamori, A., Minagawa, J., Ono, T. A. (2002) Light-intensity-dependent expression of Lhc gene faimily encoding light-harvesting chlorophyll-a/b proteins of photosystem II in Chlamydomonas reihardtii. Plant Physiol. 130, 325–333.

    CAS  Article  Google Scholar 

  38. 38.

    Yamamoto, H. Y., Bassi, R. (1996) Carotenoids: Localisation and function. In: Ort, D. R., Yocum, C. F. (eds) Oxygenic Photosynthesis: The Light Reactions. Kluwer Academic Publishers, Dordrecht, Boston, London, pp. 539–563.

    Google Scholar 

  39. 39.

    Webb, W. L., Newton, M., Starr, D. (1974) Carbon dioxide exchange of Alnus rubra: a mathematical model. Oecologia 17, 281–291.

    Article  Google Scholar 

  40. 40.

    Wrischer, M., Ljubesic, N., Salopek, B. (1998) The role of carotenoids in the structural and functional stability of thylakoids in plastids of dark-grown spruce seedlings. J. Plant Physiol. 153, 46–52.

    CAS  Article  Google Scholar 

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Acknowledgements

The authors are grateful to the Federation of European Biochemical Societies (FEBS) for supporting this research. We are thanking to Prof. Dr. Karin Krupinska (University of Kiel, Germany) for enabling Hrvoje Lepeduš to do the experimental work in the Laboratory of Cell Biology (Institute of Botany, University of Kiel). Hrvoje Lepeduš is also thanking to Dr. Mark Schlensog for hosting and supporting the chlorophyll fluorescence and oxygen-production measurements.

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Lepeduš, H., Fulgosi, H., Benšić, M. et al. Efficiency of the Photosynthetic Apparatus in Developing Needles of Norway Spruce (Picea abies L. Karst.). BIOLOGIA FUTURA 59, 217–232 (2008). https://doi.org/10.1556/ABiol.59.2008.2.8

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Keywords

  • Picea abies
  • chloroplast biogenesis
  • photosynthesis
  • needle development