Biologia Plantarum

, 52:307 | Cite as

Water-water cycle involved in dissipation of excess photon energy in phosphorus deficient rice leaves

  • X. -Y. Weng
  • H. -X. Xu
  • Y. Yang
  • H. -H. Peng
Original Papers


The water-water cycle which may be helpful for dissipating the excitation pressure over electron transport chain and minimizing the risk of photoinhibition and photodamage was investigated in rice after 10-d P-deficient treatment. Net photosynthetic rate decreased under P-deficiency, thus the absorption of photon energy exceeded the energy required for CO2 assimilation. A more sensitive response of effective quantum yield of photosystem 2 (ΦPS2) to O2 concentration was observed in plants that suffered P starvation, indicating that more electrons were transported to O2 in the P-deficient leaves. The electron transport rate through photosystem 2 (PS 2) (Jf) was stable, and the fraction of electron transport rate required to sustain CO2 assimilation and photorespiration (Jg/Jf) was significantly decreased accompanied by an increase in the alternative electron transport (Ja/Jf), indicating that a considerable electron amount had been transported to O2 during the water-water cycle in the P-deficient leaves. However, the fraction of electron transport to photorespiration (Jo/Jf) was also increased in the P-deficient leaves and it was less sensitive than that of water-water cycle. Therefore, water-water cycle could serve as an efficient electron sink. The higher non-photochemical fluorescence quenching (qN) in the P-deficient leaves depended on O2 concentration, suggesting that the water-water cycle might also contribute to non-radiative energy dissipation. Hence, the enhanced activity of the water-water cycle is important for protecting photosynthetic apparatus under P-deficiency in rice.

Additional key words

Oryza sativa net photosynthetic rate stomatal conductance intercellular CO2 concentration photosystem 2 chlorophyll a fluorescence non-photochemical and photochemical quenching photorespiration 



ascorbate peroxidase


intercellular CO2 concentration




stomatal conductance


fresh mass


the rate of alternative electron transport


the electron transport rate through PS2


the rate of electron transport required to maintain photosynthetic carbon reduction cycle (PCR) and photorespiratory carbon oxidation cycle (PCO)


the rate of electron transport though photorespiration




superoxide radical


net photosynthetic rate


photorespiratory carbon oxidation cycle


photosynthetic carbon reduction cycle


photosynthetic photon flux density



PS 2

photosystem 2


photochemical quenching


non-photochemical quenching


superoxide dismutase




trichloroacetic acid


effective PS2 quantum yield


  1. Abadia, J. Rao, I.M., Terry, N: Changes in leaf phosphate status have only small effects on the photochemical apparatus of sugar beet leaves.-Plant Sci. 50: 49–55, 1987.CrossRefGoogle Scholar
  2. Agarwal, S., Pandey, V.: Antioxidant enzyme responses to NaCl stress in Cassia angustifolia.-Biol. Plant. 48: 555–560, 2004.CrossRefGoogle Scholar
  3. Asada, K.: The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons.-Annu. Rev. Plant Physiol.-Plant mol. Biol. 50: 601–639, 1999.PubMedCrossRefGoogle Scholar
  4. Biehler, K., Fock, H.: Evidence for the contribution of the Mehler-peroxidase reaction in dissipating excess electrons in drought-stressed wheat.-Plant Physiol. 112: 265–272, 1996.PubMedGoogle Scholar
  5. Bradford, M.M.: A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding.-Anal. Biochem. 72: 248–254, 1976.PubMedCrossRefGoogle Scholar
  6. Brooks, A., Farquar, G.D.: Effects of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light.-Planta 165: 397–406, 1985.CrossRefGoogle Scholar
  7. Demmig-Adams, B., Adams, W.W., III: Photoprotection and other responses of plants to high light stress.-Annu. Rev. Plant Physiol. Plant mol. Biol. 43: 599–626, 1992.CrossRefGoogle Scholar
  8. Elstner, E.F., Heupel, A.: Inhibition of nitrite formation from hydroxylammonium-chloride simple assay for superoxide dismutase.-Anal. Biochem. 70: 616–620, 1976.PubMedCrossRefGoogle Scholar
  9. Epron, D., Godard, D., Cornic, G., Genty, B.: Limitation of net CO2 assimilation rate by internal resistance to CO2 tranfer in the leaves of two tree species (Fagus sylvation L. and Castanea sativa Mill).-Plant Cell Environ. 18: 43–51, 1995.CrossRefGoogle Scholar
  10. Farquhar, G.D., Sharkey, T.D.: Stomatal conductance and photosynthesis.-Annu. Rev. Plant Physiol. 33: 317–345, 1982.CrossRefGoogle Scholar
  11. Fredeen, A.L., Raab, T.K., Rao, I.M., Terry, N.:Effects of phosphorus nutrition on photosynthesis in Glycine max L. Merr.-Planta 181: 399–405, 1990.CrossRefGoogle Scholar
  12. 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.Google Scholar
  13. Ghorbanli, M., Ebrahimzadeh, H., Sharifi, M.: Effects of NaCl and mycorrhizal fungi on antioxidative enzymes in soybean.-Biol. Plant. 48: 575–581, 2004.CrossRefGoogle Scholar
  14. Harley, P.C., Poreto, F., Marco, G.D., Sharkey, T.D.: Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2.-Plant Physiol. 98: 1429–1436, 1992.PubMedCrossRefGoogle Scholar
  15. Huang, Z.A., Jiang, D.A., Yang, Y., Sun, J.W., Jin, S.H.: Effects of nitrogen deficiency on gas exchange, chlorophyll fluorescence, and antioxidant enzymes in leaves of rice plants.-Photosynthetica 42: 357–364, 2004.CrossRefGoogle Scholar
  16. Jacob, J., Lawlor, D.W.: Stomatal and mesophyll limitations of photosynthesis in phosphate deficient sunflower, maize and wheat plants.-J. exp. Bot. 42: 1003–1011, 1991.CrossRefGoogle Scholar
  17. Jacob, J., Lawlor, D.W.: Dependence of photosynthesis of sunflower and maize leaves on phosphate supply, ribulose-1,5-bisphosphate carboxylase/oxygenase activity, and ribulose-1,5-bisphosphate pool size.-Plant Physiol. 98: 801–807, 1992.PubMedGoogle Scholar
  18. Jacob, J., Lawlor, D.W.: In vivo photosynthetic electron transport does not limit photosynthetic capacity in phosphate-deficient sunflower and maize leaves.-Plant Cell Environ. 16: 785–795, 1993.CrossRefGoogle Scholar
  19. Jiang, D.A., Rao, L.H., Peng, Z.Q.: [Some physiological effects of potassium on yield formation of rice.]-Acta Agr. Univ. Zhejiang 13: 441–444, 1987. [In Chinese.]Google Scholar
  20. Koca, H., Ozdemir, F., Turkan I.: Effect of salt stress on lipid peroxidation and superoxide dismutase and peroxidase activities of Lycopersicon esculentum and L. pennellii.-Biol. Plant. 50: 745–748, 2006.CrossRefGoogle Scholar
  21. Lauer, M.J., Pallardy, S.G., Belvins, D.G., Randall, D.D.: Whole leaf carbon exchange characteristics of phosphate deficient soybeans (Glycine max L.).-Plant Physiol. 91: 848–854, 1989.PubMedGoogle Scholar
  22. Lovelock, C.E., Winter, K.: Oxygen-dependent electron transport and protection from photoinhibition in leaves of tropical trees species.-Planta 198: 580–587, 1996.CrossRefGoogle Scholar
  23. Makino, A., Miyake, C., Yokota, A.: Physiological function of the water-water cycle (Mehler reaction) and the cyclic electron flow around PS1 in rice leaves.-Plant Cell Physiol. 43: 1017–1026, 2002.PubMedCrossRefGoogle Scholar
  24. Maleszewski, S., Clereszko, I., Skowroñska, A., Mieczejko, E., Kozłowska-Szerenos, B.: Changes induced by low oxgen concentration in photosynthetic and respiratory CO2 exchange in phosphate-deficient bean leaves.-Biol. Plant. 48: 401–405, 2004.CrossRefGoogle Scholar
  25. Mehler, A.H.: Studies on reactions of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents.-Arch. Biochem. Biophys. 33: 65–77, 1951.CrossRefGoogle Scholar
  26. Milivojević, D.B., Nikolić, B.R., Drinić, G.: Effects of arsenic on phosphorus content in different organs and chlorophyll fluorescence in primary leaves of soybean.-Biol. Plant. 50: 149–151, 2006.CrossRefGoogle Scholar
  27. Miyake, C., Yokota, A.: Determination of the rate of photoreduction of O2 in the water-water cycle in watermelon leaves and enhancement of the rate by limitation of photosynthesis.-Plant Cell Physiol. 42: 508–515, 2000.CrossRefGoogle Scholar
  28. Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts.-Plant Cell Physiol. 22: 867–880, 1981.Google Scholar
  29. Neubauer, C., Yamamoto, H.Y.: Mehler-peroxidase reaction mediates zeaxanthin formation and zeaxanthin-related fluorescence quenching in intact chloroplasts.-Plant Physiol. 99: 1354–1361, 1992.PubMedGoogle Scholar
  30. Niyogi, K.K.: Photoprotection revisited: genetic and molecular approaches.-Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 333–359, 1999.PubMedCrossRefGoogle Scholar
  31. Niyogi, K.K.: Safety valves for photosynthesis.-Curr. Opinion Plant Biol. 3: 455–460, 2000.CrossRefGoogle Scholar
  32. Pieters, A.J., Paul, M.J., Lawlor, D.W.: Low sink demand limits photosynthesis under Pi deficiency.-J. exp. Bot. 52: 1083–1091, 2001.PubMedCrossRefGoogle Scholar
  33. Qiu, I., Israel, D.W.: Carbohydrate accumulation and utilization in soybean plants in response to altered phosphorus nutrition.-Physiol. Plant. 90: 722–728, 1994.CrossRefGoogle Scholar
  34. Rahnama, H., Ebrahimzadeh, H.: The effect of NaCl on antioxidant enzyme activities in potato seedlings.-Biol. Plant. 49: 93–97, 2005.CrossRefGoogle Scholar
  35. Rao, I.M., Terry, N.: Leaf phosphate status, photosynthesis and carbon partitioning in sugar beet. I. Changes in growth, gas exchange and Calvin cycle enzymes.-Plant Physiol. 90: 814–819, 1989.PubMedGoogle Scholar
  36. Schreiber, U., Neubauer, C.: O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence.-Photosynth. Res. 25: 279–293, 1990.CrossRefGoogle Scholar
  37. Starck, Z,, Niemyska, B., Bogdan, J., Akour Tawalbeh, R.N.: Response of tomato plants to chilling stress in association with nutrient or phosphorus starvation.-Plant Soil 226: 99–106, 2000.CrossRefGoogle Scholar
  38. Von Caemmerer, S., Farquhar, G.D.: Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.-Planta 153: 376–387, 1981.CrossRefGoogle Scholar
  39. Wang, H.W., Mi, H., Ye, J.Y., Deng, Y., Shen, Y.K.: Low concentrations of NaHSO3 increase cyclic photo-phosphorylation and photosynthesis in cyanobacterium Synechocystis PCC6803.-Photosynth. Res. 75: 151–159, 2003.PubMedCrossRefGoogle Scholar

Copyright information

© Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Praha 2008

Authors and Affiliations

  • X. -Y. Weng
    • 1
  • H. -X. Xu
    • 1
  • Y. Yang
    • 1
  • H. -H. Peng
    • 1
  1. 1.National Laboratory of Plant Physiology and Biochemistry, Department of Biological Science, College of Life ScienceZhejiang UniversityHangzhou, ZhejiangChina

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