Photosynthetica 2009, 47(4):527-535 | DOI: 10.1007/s11099-009-0078-4

Winter photoinhibition in needles of Taxus baccata seedlings acclimated to different light levels

P. Robakowski1,*, T. Wyka2
1 Department of Forestry, University of Life Sciences in Poznań, Poznań, Poland
2 Department of Biology, General Botany Laboratory, Adam Mickiewicz University, Poznań, Poland

Seasonal variability of maximum quantum yield of PSII photochemistry (Fv/Fm) was studied in needles of Taxus baccata seedlings acclimated to full light (HL, 100% solar irradiance), medium light (ML, 18% irradiance) or low light (LL, 5% irradiance). In HL plants, Fv/Fm was below 0.8 (i.e. state of photoinhibition) throughout the whole experimental period from November to May, with the greatest decline in January and February (when Fv/Fm value reached 0.37). In ML seedlings, significant declines of Fv/Fm occurred in January (with the lowest level at 0.666), whereas the decline in LL seedlings (down to 0.750) was not significant. Full recovery of Fv/Fm in HL seedlings was delayed until the end of May, in contrast to ML and LL seedlings. Fv/Fm was significantly correlated with daily mean (T mean), maximal (T max) and minimal (T min) temperature and T min was consistently the best predictor of Fv/Fm in HL and ML needles. Temperature averages obtained over 3 or 5 days prior to measurement were better predictors of Fv/Fm than 1- or 30-day averages. Thus our results indicate a strong light-dependent seasonal photoinhibition in needles of T. baccata as well as suggest a coupling of Fv/Fm to cumulative temperature from several preceding days. The dependence of sustained winter photoinhibition on light level to which the plants are acclimated was further demonstrated when plants from the three light environments were exposed to full daylight over single days in December, February and April and Fv/Fm was followed throughout the day to determine residual sensitivity of electron transport to ambient irradiance. In February, the treatment revealed a considerable midday increase in photoinhibition in ML plants, much less in HL (already downregulated) and none in LL plants. This suggested a greater capacity for photosynthetic utilization of electrons in LL plants and a readiness for rapid induction of photoinhibition in ML plants. Further differences between plants acclimated to contrasting light regimes were revealed during springtime de-acclimation, when short term regeneration dynamics of Fv/Fm and the relaxation of nonphotochemical quenching (NPQ) indicated a stronger persistent thermal mechanism for energy dissipation in HL plants. The ability of Taxus baccata to sustain winter photoinhibition from autumn until late spring can be beneficial for protection against an excessive light occurring together with frosts but may also restrict photosynthetic carbon gain by this shade-tolerant species when growing in well illuminated sites.

Additional key words: acclimation to irradiance; chlorophyll a fluorescence; photoinhibition; photoprotection; Taxus baccata; winter hardening

Received: April 16, 2009; Accepted: November 27, 2009; Published: December 1, 2009  Show citation

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Robakowski, P., & Wyka, T. (2009). Winter photoinhibition in needles of Taxus baccata seedlings acclimated to different light levels. Photosynthetica47(4), 527-535. doi: 10.1007/s11099-009-0078-4
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References

  1. Adams, W.W., III, Zarter, C.R., Ebbert, V., Demmig-Adams, B.: Photoprotective strategies of overwintering evergreens. - BioScience 54: 41-49, 2004. Go to original source...
  2. Adams, W.W., III, Demmig-Adams, B.: Carotenoid composition and down regulation of photosystem II in 3 conifer species during the winter. - Physiol. Plant. 92: 451-458, 1994. Go to original source...
  3. Adams, W.W., III, Zarter, C.R., Mueh, K.E., Amiard, V., Demmig-Adams, B.: Energy dissipation and photoinhibition. - In: Demmig Adams B., Adams, W.W., III, Mattoo, A.K. (ed.): Photoprotection, Photoinhibition, Gene Regulation and Environment. Pp. 49-64. Springer, Dodrecht 2006. Go to original source...
  4. Demmig-Adams, B., Ebbert, V., Zarter, C.R., Adams, W.W., III: Characteristics and species-dependent employment of flexible versus sustained thermal dissipation and photoinhibition. - In: Demmig-Adams, B., Adams, W.W., III, Mattoo, A.K. (ed.): Photoprotection, Photoinhibition, Gene Regulation and Environment. Pp. 39-48. Springer, Dodrecht 2006. Go to original source...
  5. Ellenberg, H., Weber, H.E., Düll, R., Wirth, V., Werner, W., Paulißen, D.: Zeigerwerte von Pflanzen in Mitteleuropa. - Scripta Geobot. 18: 1-258, 1992. [In German.]
  6. Gamper, R., Mayr, S., Bauer, H.: Similar susceptibility to excess irradiance in sun and shade acclimated saplings of Norway spruce [Picea abies (L.) Karst.] and stone pine (Pinus cembra L.). - Photosynthetica 38: 373-378, 2000. Go to original source...
  7. Genty, B., Briantais, J-M., Baker, N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. - Biochim. Biophys. Acta. 990: 87-92, 1989. Go to original source...
  8. Givnish, T.J.: Adaptive significance of evergreen vs. deciduous leaves: Solving the triple paradox. - Silva Fennica 36: 703-743, 2002. Go to original source...
  9. Groom, Q.J., Baker, N.R., Long, S.P.: Photoinhibition of holly (Ilex aquifolium) in the field during the winter. - Physiol. Plant. 83: 585-590, 1991. Go to original source...
  10. Han, Q., Shinohara, K., Kakubari, Y., Mukai, Y.: Photoprotective role of rhodoxanthin during cold acclimation in Cryptomeria japonica. - Plant, Cell and Environ. 26: 715-723, 2003. Go to original source...
  11. Han, Q.M., Katahata, S., Kakubari, Y., Mukai, Y.: Seasonal changes in the xanthophyll cycle and antioxidants in sunexposed and shaded parts of the crown of Cryptomeria japonica in relation to rhodoxanthin accumulation during cold acclimation. - Tree Physiol. 24: 609-616, 2004. Go to original source...
  12. Havaux, M., Niyogi K.K.: The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. - Proc. Natl. Acad. Sci. USA 96: 8762-8767, 1999. Go to original source...
  13. Ishida, A., Nakano, T., Matsumoto, Y., Sakoda, M., Ang, H.L.: Diurnal changes in leaf gas exchange and chlorophyll fluorescence in tropical tree species with contrasting light requirements. - Ecol. Res. 14: 77-88, 1999. Go to original source...
  14. Iszkulo, G., Boratynski, A.: Interaction between canopy tree species and European yew Taxus baccata (Taxaceae). - Pol. J. Ecol. 52: 523-531, 2004.
  15. Jifon, J.L., Syversten, J.P.: Moderate shade can increase net gas exchange and reduce photoinhibition in citrus leaves. - Tree Physiol. 23: 719-719, 2003. Go to original source...
  16. Lawson, S.T., Perkins, T.D., Adams, G.T.: Winter-time patterns of chlorophyll fluorescence in red spruce (Picea rubens Sarg.). - J. Sustainable Forest 10: 149-153, 2000. Go to original source...
  17. Lundmark, T., Bergh, J., Strand, M., Koppel, A.: Seasonal variation of maximum photochemical efficiency in boreal Norway spruce stands. - Trees 13: 63-67, 1998. Go to original source...
  18. Maxwell, K., Johnson, G.N.: Chlorophyll fluorescence - a practical guide. - J. Exp. Bot. 51: 659-668, 2000. Go to original source...
  19. Miyazawa, Y. Kikuzawa K.: Winter photosynthesis by saplings of evergreen broad-leaved trees in a deciduous temperate forest. - New Phytol. 165: 857-866, 2005. Go to original source...
  20. Müller, P., Li, X.-P., Niyogi, K.K.: Non-photochemical quenching. A response to excess light energy. - Plant Physiol. 125: 1558-1566, 2001. Go to original source...
  21. Niinemets, U., Valladares, F.: Photosynthetic acclimation to simultaneous and interacting environmental stresses along natural light gradients: Optimality and constraints. - Plant Biol. 6: 254-268, 2004. Go to original source...
  22. Nippert, J.B., Duursma, R.A., Marshall, J.D.: Seasonal variation in photosynthetic capacity of montane conifers. - Functional Ecol. 18: 876-886, 2004. Go to original source...
  23. Niyogi, K.K.: Photoprotection revisited: Genetic and molecular approaches. - Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 333-359, 1999. Go to original source...
  24. Ögren, E.: Photoinhibition of photosynthesis in willow leaves under field conditions. - Planta 175: 229-236, 1988. Go to original source...
  25. Öquist, G., Huner, N.P.A.: Photosynthesis of overwintering evergreen plants. - Annu. Rev. Plant Biol. 54: 329-355, 2003. Go to original source...
  26. Parmar, V.S., Jha, A., Bisht, K.S., Taneja, P., Singh, S.K., Kumar, A., Poonam, Jain R, Olsen, C.E.: Constituents of yew trees. - Phytochem. 50: 1267-1304, 1999. Go to original source...
  27. Porcar-Castell, A., Juurola, E., Ensminger, I., Berninger, F., Hari, P., Nikinmaa, E.: Seasonal acclimation of photosystem II in Pinus sylvestris. II. Using the rate constants of sustained thermal enegry dissipation and photochemistry to study the effect of light environment. - Tree Physiol. 28: 1483-1491, 2008. Go to original source...
  28. Robakowski, P.: Susceptibility to low-temperature photoinhibition in three conifers differing in successional status. - Tree Physiol. 25: 1151-1160, 2005. Go to original source...
  29. Robakowski, P., Wyka, T.: Down-regulation of PSII in needles of silver fir (Abies alba Mill.) seedlings growing under the canopy of European larch and Norway spruce. - Zeszyty Postepow Nauk Agronomicznych 496: 421-431, 2004.
  30. Stanisz, A.: [Course of statistics with the application of Statistica PL using examples from medicine. Linear and non-linear models]. - Statsoft Polska 2: 178-184, 2007. [In Polish.]
  31. ©punda, V., Kalina, J., Marek, M.V., Nauą, J.: Regulation of photochemical efficiency of photosystem 2 in Norway spruce at the beginning of winter and in the following spring. - Photosynthetica 33: 91-102, 1997. Go to original source...
  32. Thomas, A.P., Polwart, A.: Taxus baccata L. - J. Ecol. 91: 489-524, 2003. Go to original source...
  33. Verhoeven, A.S., Adams W. W., III, Demming-Adams, B.: Close relationship between the state of xanthophyll cycle pigments and photosystem II efficiency during recovery from winter stress. - Physiol. Plant. 96: 567-576, 1996. Go to original source...
  34. Verhoeven, A.S., Swanberg, A., Thao, M., Whiteman, J.: Seasonal changes in leaf antioxidant systems and xanhophyll cycle characteristic in Taxus×media growing in sun and shade environments. - Physiol. Plant. 123: 428-434, 2005. Go to original source...
  35. Valladares, F., Martinez-Ferri E., Balaguer, L., Perez-Corona, E., Manrique, E.: Low leaf-level response to light and nutrients in Mediterranean evergreen oaks: a conservative resource-use strategy? - New Phytol. 148: 79-91, 2000. Go to original source...
  36. Wyka, T., Robakowski, P., Żytkowiak, R.: Leaf acclimation to contrasting irradiance in juvenile trees differing in shade tolerance. - Tree Physiol. 27: 1293-1306, 2007. Go to original source...
  37. Wyka, T., Robakowski, P., Żytkowiak, R.: Leaf age as a factor in anatomical and physiological acclimative responses of Taxus baccata L. needles to contrasting irradiance environments. - Photosynth. Res. 95: 87-99, 2008. Go to original source...
  38. Yamazaki, J.-Y. Tsuchiya, S., Nagano, S., Maruta, E. Photoprotective mechanisms against winter stresses in the needles of Abies mariesii grown at the tree line on Mt. Norikura in Central Japan. - Photosynthetica 45: 547-554, 2007. Go to original source...
  39. Yokthongwattana, K., Melis, A.: Photoinhibition and recovery in oxygenic photosynthesis: Mechanism of a photosystem II damage and repair cycle. - In: Govindjee (ed.): Photoprotection, Photoinhibition, Gene Regulation, and Environment, Advances in Photosynthesis and Respiration. Vol. 21, pp. 175-191. Springer, Dordrecht 2006. Go to original source...