Abstract
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.
Similar content being viewed by others
Abbreviations
- APX:
-
ascorbate peroxidase
- ci :
-
intercellular CO2 concentration
- Chl:
-
chlorophyll
- gs :
-
stomatal conductance
- FM:
-
fresh mass
- Ja :
-
the rate of alternative electron transport
- Jf :
-
the electron transport rate through PS2
- Jg :
-
the rate of electron transport required to maintain photosynthetic carbon reduction cycle (PCR) and photorespiratory carbon oxidation cycle (PCO)
- Jo :
-
the rate of electron transport though photorespiration
- MDA:
-
malonyldialdehyde
- O ·−2 :
-
superoxide radical
- PN :
-
net photosynthetic rate
- PCO:
-
photorespiratory carbon oxidation cycle
- PCR:
-
photosynthetic carbon reduction cycle
- PPFD:
-
photosynthetic photon flux density
- Pr:
-
protein
- PS 2:
-
photosystem 2
- qP :
-
photochemical quenching
- qN :
-
non-photochemical quenching
- SOD:
-
superoxide dismutase
- TBA:
-
barbiturate
- TCA:
-
trichloroacetic acid
- ΦPS2 :
-
effective PS2 quantum yield
References
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.
Agarwal, S., Pandey, V.: Antioxidant enzyme responses to NaCl stress in Cassia angustifolia.-Biol. Plant. 48: 555–560, 2004.
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.
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.
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.
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.
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.
Elstner, E.F., Heupel, A.: Inhibition of nitrite formation from hydroxylammonium-chloride simple assay for superoxide dismutase.-Anal. Biochem. 70: 616–620, 1976.
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.
Farquhar, G.D., Sharkey, T.D.: Stomatal conductance and photosynthesis.-Annu. Rev. Plant Physiol. 33: 317–345, 1982.
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.
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.
Ghorbanli, M., Ebrahimzadeh, H., Sharifi, M.: Effects of NaCl and mycorrhizal fungi on antioxidative enzymes in soybean.-Biol. Plant. 48: 575–581, 2004.
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.
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.
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.
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.
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.
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.]
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.
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.
Lovelock, C.E., Winter, K.: Oxygen-dependent electron transport and protection from photoinhibition in leaves of tropical trees species.-Planta 198: 580–587, 1996.
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.
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.
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.
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.
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.
Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts.-Plant Cell Physiol. 22: 867–880, 1981.
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.
Niyogi, K.K.: Photoprotection revisited: genetic and molecular approaches.-Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 333–359, 1999.
Niyogi, K.K.: Safety valves for photosynthesis.-Curr. Opinion Plant Biol. 3: 455–460, 2000.
Pieters, A.J., Paul, M.J., Lawlor, D.W.: Low sink demand limits photosynthesis under Pi deficiency.-J. exp. Bot. 52: 1083–1091, 2001.
Qiu, I., Israel, D.W.: Carbohydrate accumulation and utilization in soybean plants in response to altered phosphorus nutrition.-Physiol. Plant. 90: 722–728, 1994.
Rahnama, H., Ebrahimzadeh, H.: The effect of NaCl on antioxidant enzyme activities in potato seedlings.-Biol. Plant. 49: 93–97, 2005.
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.
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.
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.
Von Caemmerer, S., Farquhar, G.D.: Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.-Planta 153: 376–387, 1981.
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Weng, X.Y., Xu, H.X., Yang, Y. et al. Water-water cycle involved in dissipation of excess photon energy in phosphorus deficient rice leaves. Biol Plant 52, 307–313 (2008). https://doi.org/10.1007/s10535-008-0064-x
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10535-008-0064-x