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

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Photosynthetica

Abstract

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.

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Abbreviations

Chl:

chlorophyll

F0 :

minimal fluorescence yield

FJ or FI :

fluorescence intensity at 2 ms or 30 ms, respectively

Fm :

maximal fluorescence yield

Fv :

maximal variable fluorescence

OEC:

oxygen-evolving complex

RC:

reaction centers

RE:

reduction of end electron acceptors

VI :

relative variable fluorescence at 30 ms

VJ :

relative variable fluorescence at 2 ms

VK :

relative variable fluorescence at 300 μs

δR0 :

the efficiency of electron transfer between intermediate carriers to the RE of PSI

φP0 :

maximal quantum yield of PSII primary photochemistry, taken as equal to Fv/Fm

ψE0 :

the efficiency of trapped energy to move an electron further than QA

References

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Bukhov, N., Carpentier, R.: Alternative photosystem I-driven electron transport routes: mechanisms and functions. — Photosynth. Res. 82: 17–33, 2004.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Edwards, G., Walker, D.A.: C3, C4: Mechanisms, and Cellular and Environmental Regulation of Photosynthesis. Pp. 97–520. Blackwell Scientific Publications, Oxford 1983.

    Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Hörtensteiner, S., Feller, U.: Nitrogen metabolism and remobilization during senescence. — J. Exp. Bot. 53: 927–937, 2002.

    Article  PubMed  Google Scholar 

  • Hörtensteiner, S.: The loss of green color during chlorophyll degradation — a prerequisite to prevent cell death? — Planta 219: 191–194, 2004.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Keskitalo, J., Bergquist, G., Gardeström, P. et al.: A cellular timetable of autumn senescence. — Plant Physiol. 139: 1635–1648, 2005.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Matile, P.: Biochemistry of Indian summer: physiology of autumnal leaf coloration. — Exp. Gerontol. 35: 145–158, 2000.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Niyogi, K.K.: Safety valves for photosynthesis. — Curr. Opin. Plant Biol. 3: 455–460, 2000.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to C. Kotakis.

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All the above fluorescence parameters refer to dark-adapted state.

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Kotakis, C., Kyzeridou, A. & Manetas, Y. Photosynthetic electron flow during leaf senescence: Evidence for a preferential maintenance of photosystem I activity and increased cyclic electron flow. Photosynthetica 52, 413–420 (2014). https://doi.org/10.1007/s11099-014-0046-5

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  • DOI: https://doi.org/10.1007/s11099-014-0046-5

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