Photosynthetica 2014, 52(3):413-420 | DOI: 10.1007/s11099-014-0046-5

Photosynthetic electron flow during leaf senescence: Evidence for a preferential maintenance of photosystem I activity and increased cyclic electron flow

C. Kotakis1,2,*, A. Kyzeridou1, Y. Manetas1
1 Laboratory of Plant Physiology, Department of Biology, University of Patras, Patras, Greece
2 Institute of Plant Biology, Biological Research Center, Hungarian Academy of Sciences, Szeged, Hungary

Limitations in photosystem function and photosynthetic electron flow were investigated during leaf senescence in two field-grown plants, i.e., Euphorbia dendroides L. and Morus alba L., a summer- and winter-deciduous, shrub and tree, respectively. Analysis of fast chlorophyll (Chl) a fluorescence transients and post-illumination fluorescence yield increase were used to assess photosynthetic properties at various stages of senescence, the latter judged from the extent of Chl loss. In both plants, the yield of primary photochemistry of PSII and the content of PSI remained quite stable up to the last stages of senescence, when leaves were almost yellow. However, the potential for linear electron flow along PSII was limited much earlier, especially in E. dendroides, by an apparent inactivation of the oxygen-evolving complex and a lower efficiency of electron transfer to intermediate carriers. On the contrary, the corresponding efficiency of electron transfer from intermediate carriers to final acceptors of PSI was increased. In addition, cyclic electron flow around PSI was accelerated with the progress of senescence in E. dendroides, while a corresponding trend in M. alba was not statistically significant. However, there was no decrease in PSI activity even at the last stages of senescence. We argue that a switch to cyclic electron flow around PSI during leaf senescence may have the dual role of replenishing the ATP and maintaining a satisfactory nonphotochemical energy quenching, since both are limited by hindered linear electron transfer.

Keywords: alternative routes; electron flow; chlorophyll fluorescence; chloroplast; photosynthesis; senescence regulation

Received: January 14, 2014; Accepted: April 7, 2014; Published: September 1, 2014Show citation

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Kotakis, C., Kyzeridou, A., & Manetas, Y. (2014). Photosynthetic electron flow during leaf senescence: Evidence for a preferential maintenance of photosystem I activity and increased cyclic electron flow. Photosynthetica52(3), 413-420. doi: 10.1007/s11099-014-0046-5.
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References

  1. Adams, W.W., Winter, K., Schreiber, U. et al.: Photosynthesis and chlorophyll fluorescence characteristics in relationship to changes in pigment and element composition of leaves of Platanus occidentalis L. during autumnal leaf senescence. - Plant Physiol. 92: 1184-1190, 1990. Go to original source...
  2. Brown, N.J., Palmer, B.G., Stanley, S. et al.: C4 acid decarboxylases required for C4 photosynthesis are active in the mid-vein of the C3 species Arabidopsis thaliana, and are important in sugar and amino acid metabolism. - Plant J. 61: 122-133, 2010. Go to original source...
  3. Buchanan-Wollaston, V., Earl, S., Harrison, E. et al.: The molecular analysis of leaf senescence - a genomics approach. - Plant Biotechnol. J. 1: 3-22, 2003. Go to original source...
  4. Bukhov, N., Carpentier, R.: Alternative photosystem I-driven electron transport routes: mechanisms and functions. - Photosynth. Res. 82: 17-33, 2004. Go to original source...
  5. Ceppi, M.G., Oukarroum, A., Çiçek, N. et al.: The IP amplitude of the fluorescence rise OJIP is sensitive to changes in the photosystem I content of leaves: a study on plants exposed to magnesium and sulfate deficiencies, drought stress and salt stress. - Physiol. Plantarum 144: 277-288, 2012. Go to original source...
  6. Dima, E., Manetas, Y., Psaras, G.K.: Chlorophyll distribution pattern in inner stem tissues: evidence from epifluorescence microscopy and reflectance measurements in 20 woody species. - Trees-Struct. Funct. 20: 515-521, 2006. Go to original source...
  7. Edwards, G., Walker, D.A.: C3, C4: Mechanisms, and Cellular and Environmental Regulation of Photosynthesis. Pp. 97-520. Blackwell Scientific Publications, Oxford 1983.
  8. Feild, T.S., Nedbal, L., Ort, D.R.: Nonphotochemical reduction of the plastoquinone pool in sunflower leaves originates from chlororespiration. - Plant Physiol. 116: 1209-1218, 1998. Go to original source...
  9. Gitelson, A. A., Chivkunova, O.B., Merzlyak, M.N.: Nondestructive estimation of anthocyanins and chlorophylls in anthocyanic leaves. - Am. J. Bot. 96: 1861-1868, 2009.
  10. Groom, Q., Kramer, D.M., Crofts, A.R., Ort, D.R.: The non-photochemical reduction of plastoquinone in leaves. - Photosynth. Res. 36: 205-215, 1993. Go to original source...
  11. Hetherington, S.E., Smillie, R.M., Davies, W.J.: Photosynthetic activities of vegetative and fruiting tissues of tomato. - J. Exp. Bot. 49: 1173-1181, 1998. Go to original source...
  12. Hörtensteiner, S., Feller, U.: Nitrogen metabolism and remobilization during senescence. - J. Exp. Bot. 53: 927-937, 2002. Go to original source...
  13. Hörtensteiner, S.: The loss of green color during chlorophyll degradation - a prerequisite to prevent cell death? - Planta 219: 191-194, 2004. Go to original source...
  14. Ivanov, A.G., Krol, M., Sveshnikov, D. et al.: Characterization of the photosynthetic apparatus in cortical bark chlorenchyma of Scots pine. - Planta 223: 1165-1177, 2006. Go to original source...
  15. Jiang, H.X., Chen, L.S., Zheng, J.G. et al.: Aluminum-induced effects on photosystem II photochemistry in Citrus leaves assessed by the chlorophyll a fluorescence transient. - Tree Physiol. 28: 1863-1871, 2008.
  16. Kalachanis, D., Manetas, Y.: Analysis of fast chlorophyll fluorescence rise (O-K-J-I-P) curves in green fruits indicates electron flow limitations at the donor side of PSII and the acceptor sides of both photosystems. - Physiol. Plantarum 139: 313-323, 2010. Go to original source...
  17. Keskitalo, J., Bergquist, G., Gardeström, P. et al.: A cellular timetable of autumn senescence. - Plant Physiol. 139: 1635-1648, 2005. Go to original source...
  18. Kotakis, C., Petropoulou, Y., Stamatakis, K. et al.: Evidence for active cyclic electron flow in twig chlorenchyma in the presence of an extremely deficient linear electron transport activity. - Planta 225: 245-253, 2006. Go to original source...
  19. Lu, Q.T., Wen, X.G., Lu, C.M. et al.: Photoinhibition and photoprotection in senescent leaves of field-grown wheat plants. - Plant Physiol. Bioch. 41: 749-754, 2003. Go to original source...
  20. Manetas, Y.: Probing corticular photosynthesis through in vivo chlorophyll fluorescence measurements: evidence that high internal CO2 levels suppress electron flow and increase the risk of photoinhibition. - Physiol. Plantarum 120: 509-517, 2004. Go to original source...
  21. Manetas, Y., Buschmann, C.: The interplay of anthocyanin biosynthesis and chlorophyll catabolism in senescing leaves and the question of photosystem II photoprotection. - Photosynthetica 49: 515-522, 2011. Go to original source...
  22. Mano, J., Miyake, C., Schreiber, U. et al.: Photoactivation of the electron flow from NADPH to plastoquinone in spinach chloroplasts. - Plant Cell Physiol. 36: 1589-1598, 1995.
  23. Martín, M., Casano, L.M., Sabater, B.: Identification of the product of ndhA gene as a thylakoid protein synthesized in response to photooxidative treatment. - Plant Cell Physiol. 37: 293-298, 1996. Go to original source...
  24. Martín, M., Casano, L.M., Zapata, J.M. et al.: Role of thylakoid Ndh complex and peroxidase in the protection against photooxidative stress: fluorescence and enzyme activities in wildtype and ndhF-deficient tobacco. - Physiol. Plantarum 122: 443-452, 2004. Go to original source...
  25. Matile, P.: Biochemistry of Indian summer: physiology of autumnal leaf coloration. - Exp. Gerontol. 35: 145-158, 2000. Go to original source...
  26. Miersch, I., Heise, J., Zelmer, I. et al.: Differential degradation of the photosynthetic apparatus during leaf senescence in barley (Hordeum vulgare L.). - Plant Biol. 2: 618-623, 2000. Go to original source...
  27. Munné-Bosch, S., Shikanai, T., Asada, K.: Enhanced ferredoxindependent cyclic electron flow around photosystem I and α-tocopherol quinone accumulation in water-stressed ndhBinactivated tobacco mutants. - Planta 222: 502-511, 2005. Go to original source...
  28. Niyogi, K.K.: Safety valves for photosynthesis. - Curr. Opin. Plant Biol. 3: 455-460, 2000. Go to original source...
  29. Ougham, H.J., Morris, P., Thomas, H.: The colors of autumn leaves as symptoms of cellular recycling and defenses against environmental stresses. - Curr. Top. Dev. Biol. 66: 135-160, 2005. Go to original source...
  30. Oukarroum, A., Schansker, G., Strasser, R.J.: Drought stress effects on photosystem I content and photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance. - Physiol. Plantarum 137: 188-199, 2009. Go to original source...
  31. Rumeau, D., Peltier, G., Cournac, L.: Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. - Plant Cell Environ. 30: 1041-1051, 2007. Go to original source...
  32. Schansker, G., Tóth, S.Z., Strasser, R.J.: Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of Photosystem I in the Chl a fluorescence rise OJIP. - BBABioenergetics 1706: 250-261, 2005. Go to original source...
  33. Srivastava, A., Guissé, B., Greppin, H. et al.: Regulation of antenna structure and electron transport in photosystem II of Pisum sativum under elevated temperature probed by the fast polyphasic chlorophyll a fluorescence transient: OKJIP. - BBA-Bioenergetics 1320: 95-106, 1997. Go to original source...
  34. Stirbet, A., Govindjee: On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: Basics and applications of the OJIP fluorescence transient. - J. Photoch. Photobio. B. 104: 236-257, 2011. Go to original source...
  35. Strasser, R.J., Tsimilli-Michael, M., Srivastava, A.: Analysis of the chlorophyll a fluorescence transient. - In: Papageorgiou GC, Govindjee (ed.): Chlorophyll a Fluorescence. A Signature of Photosynthesis. Pp. 321-362. Springer, Dordrecht 2004. Go to original source...
  36. Tsimilli-Michael, M., Strasser, R.J.: In vivo assessment of stress impact on plants' vitality: applications in detecting and evaluating the beneficial role of mycorrhization on host plants. - In: Varma, A, (ed.): Mycorrhiza. Pp. 679-703. Springer, Berlin - Heidelberg 2008. Go to original source...
  37. Yusuf, M.A., Kumar, D., Rajwanshi, R. et al.: Overexpression of gamma-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements. - BBABioenergetics 1797: 1428-1438, 2010. Go to original source...
  38. Zapata, J.M., Guéra, A., Esteban-Carrasco, A. et al.: Chloroplasts regulate leaf senescence: delayed senescence in transgenic ndhF-defective tobacco. - Cell Death Differ. 12: 1277-1284, 2005. Go to original source...