Download PDF
Plant Biol (Stuttg) 2000; 2(5): 558-570
DOI: 10.1055/s-2000-7498
Original Paper
Georg Thieme Verlag Stuttgart ·New York

Different Tolerance to Light Stress in NO3 -- and NH4 +-Grown Phaseolus vulgaris L.

Z. Zhu 1 , J. Gerendás 2 , R. Bendixen 2,3 , K. Schinner 3 , H. Tabrizi 3 , B. Sattelmacher 2 , U-P. Hansen 3
  • 1 Department of Horticulture, Zhejiang University, Hangzhou, China
  • 2 Institute for Plant Nutrition and Soil Science, University of Kiel, Kiel, Germany
  • 3 Centre for Biochemistry and Molecular Biology, University of Kiel, Kiel, Germany
Further Information

Publication History

March 13, 2000

June 15, 2000

Publication Date:
31 December 2000 (online)

   Permissions and Reprints

Abstract

NH4 +-grown plants are more sensitive to light stress than NO3 --grown plants, as indicated by reduced growth and intervenal chlorosis of French bean (Phaseolus vulgaris L.). Measuring the time course of Fv/Fm ratios under photoinhibitory light regimes did not reveal any difference in PS II damage between NO3 -- and NH4 +-grown plants, in spite of some indications of higher energy quenching in NO3 --grown plants. Also, a direct action of NH4 + as an uncoupler at the thylakoid membrane could be excluded. Instead, biochemical analysis revealed enhanced lipid peroxidation and higher activity of scavenging enzymes in NH4 +-grown plants indicating that these plants make use of metabolic pathways with stronger radical formation. Evidence for higher rates of photorespiration in NH4 +-grown plants came from experiments showing that electron flux and O2 evolution were decreased by SHAM in NH4 +-grown plants, and by antimycin A in NO3 --grown plants. Further, the comparison of electron flux and of photoacoustic measurements of O2 evolution suggested that in NH4 +-grown plants the Mehler reaction was also increased, at least in the induction phase. However, the major cause of N form-dependent stress sensitivity is assumed to be in the coupling between photosynthesis and respiration, i.e., NO3 --grown plants can utilize the TCA cycle for the generation of C skeletons for amino acid synthesis, thus improving the ATP : reductant balance, whereas NH4 +-grown plants have enhanced rates of photorespiration.

Key words

Chlorophyll fluorescence - H2O2-scavenging enzymes - lipid peroxidation - Mehler reaction - mitochondria - photoacoustics

References

  • 01 Asada,  K., and Takahashi,  M.. (1987) Production and scavenging of active oxygen in photosynthesis. Photoinhibition. Klye, D. J., Osmond, C. B., and Arntzen, C. J., eds. Amsterdam; Elsevier pp. 227-287
    Google Scholar
  • 02 Baroli,  I., and Melis,  A.. (1996);  Photoinhibition and repair in Dunaliella salina acclimated to different growth irradiances.  Planta. 198 640-646
    Google Scholar
  • 03 Bendixen,  R.,, Sattelmacher,  B.,, and Hansen,  U. P.. (1997) The effect of nitrogen nutrition on the resistance of tobacco to light stress. Developments in Plant and Soil Science. Ando, T., Fujita, K., Mae, T., Matsumoto, H., Mori, S., and Sekiya, J., eds. Dordrecht; Kluwer Academic Publishers pp. 841-842
    Google Scholar
  • 04 Blackwell,  R. D.,, Murray,  A. J. S.,, Lea,  P. J.,, and Joy,  K. W.. (1988);  Photorespiratory amino donors, sucrose synthesis and the induction of CO2 fixation in barley leaves deficient in glutamine synthetase and/or glutamate synthase.  J. Exp. Bot.. 39 845-858
    Google Scholar
  • 05 Bradford,  M. M.. (1976);  A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.  Anal. Biochem.. 72 248-254
    Google Scholar
  • 06 Burke,  J. J.,, Gamble,  P. E.,, Hatfield,  J. L.,, and Quisenberry,  J. E.. (1985);  Plant morphological and biochemical responses to field water deficits. I. Responses of glutathione reductase activity and paraquat sensitivity.  Plant Physiol.. 79 415-419
    Google Scholar
  • 07 Cakmak,  I.. (1994);  Activity of ascorbate-dependent H2O2-scavenging enzymes and leaf chlorosis are enhanced in magnesium- and potassium-deficient leaves, but not in phosphorus-deficient leaves.  J. Exp. Bot.. 45 1259-1266
    Google Scholar
  • 08 Cakmak,  I.,, Atli,  M.,, Kaya,  R.,, Evliya,  H.,, and Marschner,  H.. (1995);  Association of high light and zinc deficiency in cold-induced leaf chlorosis in grapefruit and mandarin trees.  J. Plant Physiol.. 146 355-360
    Google Scholar
  • 09 Cakmak,  I., and Marschner,  H.. (1992);  Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves.  Plant Physiol.. 98 1222-1227
    Google Scholar
  • 10 Cakmak,  I.,, Strbac,  D.,, and Marschner,  H.. (1993);  Activities of hydrogen peroxide-scavenging enzymes in germinating wheat seeds.  J. Exp. Bot.. 44 127-132
    PubMedGoogle Scholar
  • 11 Champigny,  M.-L.. (1995);  Integration of photosynthetic carbon and nitrogen metabolism in higher plants.  Photosynth. Res.. 46 117-127
    CrossrefPubMedGoogle Scholar
  • 12 Conklin,  P. L., and Last,  R. L.. (1995);  Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone.  Plant Physiol.. 109 203-212
    CrossrefPubMedGoogle Scholar
  • 13 Dau,  H.. (1994 a);  Short-term adaptation of plants to changing light intensities and its relation to photosystem II photochemistry and fluorescence emission.  J. Photochem. Photobiol. B: Biol.. 26 3-28
    PubMedGoogle Scholar
  • 14 Dau,  H.. (1994 b);  Molecular mechanisms and quantitative models of variable photosystem II fluorescence.  Photochem. Photobiol.. 60 1-23
    PubMedGoogle Scholar
  • 15 Dau,  H., and Hansen,  U. P.. (1990);  A study of the energy dependent quenching of chlorophyll fluorescence by means of photoacoustic measurements.  Photosynth. Res.. 25 269-278
    CrossrefPubMedGoogle Scholar
  • 16 Demmig,  B.,, Winter,  K.,, Krüger,  A.,, and Czygan,  F. C.. (1988);  Zeaxanthin and the heat dissipation of excess light energy in Nerium oleander exposed to a combination of high light and water stress.  Plant Physiol.. 87 17-24
    PubMedGoogle Scholar
  • 17 De la Torre,  A.,, Delgado,  B.,, and Lara,  C.. (1991);  Nitrate-dependent O2 evolution in intact leaves.  Plant Physiol.. 96 898-901
    PubMedGoogle Scholar
  • 18 Foyer,  C. H., and Halliwell,  B.. (1976);  The presence of glutathione and glutathione reductase in chloroplasts. A proposed role in ascorbic acid metabolism.  Planta. 133 21-25
    CrossrefPubMedGoogle Scholar
  • 19 Furbank,  R. T., and Horton,  P.. (1987);  Regulation of photosynthesis in isolated barley protoplasts: the contribution of cyclic photophosphorylation.  Biochim. Biophys. Acta. 894 332-338
    PubMedGoogle Scholar
  • 20 Ganmore-Neumann,  R., and Kafkafi,  U.. (1983);  The effect of root temperature and NO3/NH4 ratio on strawberry plants. I. Growth, flowering, and root development.  Agron. J.. 75 941-947
    PubMedGoogle Scholar
  • 21 Geannopolitis,  C. N., and Ries,  S. K.. (1977);  Superoxide dismutase. I. Occurrence in higher plants.  Plant Physiol.. 59 309-314
    PubMedGoogle Scholar
  • 22 Gerendás,  J.,, Ratcliffe,  R. G.,, and Sattelmacher,  B.. (1990);  31P nuclear magnetic resonance evidence for differences in intracellular pH in the roots of maize seedlings grown with nitrate or ammonium.  J. Plant Physiol.. 137 125-128
    PubMedGoogle Scholar
  • 23 Gerendás,  J.,, Ratcliffe,  R. G.,, and Sattelmacher,  B.. (1995);  The influence of nitrogen and potassium supply on the ammonium content of maize (Zea mays L.) leaves including a comparison of measurements made in vivo and in vitro. .  Plant Soil. 173 11-20
    CrossrefPubMedGoogle Scholar
  • 24 Gerendás,  J.,, Zhu,  Z.,, Bendixen,  R.,, Ratcliffe,  R. G.,, and Sattelmacher,  B.. (1997);  Physiological and biochemical processes related to ammonium toxicity in higher plants.  Z. Pflanzenern. Bodenkunde. 160 239-251
    PubMedGoogle Scholar
  • 25 Gemel,  J., and Randall,  D. D.. (1992);  Light regulation of leaf mitochrondrial pyruvate dehydrogenase complex.  Plant Physiol.. 100 908-914
    PubMedGoogle Scholar
  • 26 Givan,  C. V.. (1979);  Metabolic detoxification of ammonia in tissues of higher plants.  Phytochem.. 18 375-382
    CrossrefPubMedGoogle Scholar
  • 27 Goss,  R.,, Richter,  M.,, and Wild,  A.. (1995);  Role of ΔpH in the mechanism of zeaxanthin-dependent amplification of qE.  J. Photochem. Photobiol. B: Biol.. 27 147-152
    PubMedGoogle Scholar
  • 28 Halliwell,  B.. (1981) Free radicals, oxygen toxicity and ageing. Age Pigments. Shal, R. S., ed. Amsterdam; Elsevier pp. 1-62
    Google Scholar
  • 29 Hansen,  U. P.,, Moldaenke,  C.,, Tabrizi,  H.,, and Ramm,  D.. (1993);  The effect of transthylakoid proton uptake on cytosolic pH and the imbalance of ATP and NAPDH/H+ production as measured by CO2- and light-induced depolarisation of the plasmalemma.  Plant Cell Physiol.. 34 681-695
    PubMedGoogle Scholar
  • 30 Harbinson,  J., and Foyer,  C.. (1991);  Relationships between the efficiencies of photosystem I and II and stromal redox state in CO2 free air.  Plant Physiol.. 97 44-47
    PubMedGoogle Scholar
  • 31 Harbinson,  J.,, Genty,  B.,, and Baker,  N. R.. (1989);  Relationship between the quantum efficiencies of photosystem I and II in pea leaves.  Plant Physiol.. 90 1029-1034
    PubMedGoogle Scholar
  • 32 Heber,  U.,, Bligny,  R.,, Streb,  P.,, and Douce,  R.. (1996);  Photorespiration is essential for the protection of the photosynthetic apparatus of C3 plants against photoinactivation under sunlight.  Bot. Acta. 109 307-315
    PubMedGoogle Scholar
  • 33 Heber,  U.,, Gerst,  U.,, Krieger,  A.,, Neimanis,  S.,, and Kobayashi,  Y.. (1995);  Coupled cyclic electron transport in intact chloroplasts and leaves of C3 plants: Does it exist? If so, what is its function?.  Photosynth. Res.. 46 269-275
    CrossrefPubMedGoogle Scholar
  • 34 Heineke,  D.,, Riens,  B.,, Grosse,  H.,, Hoferichter,  P.,, Peter,  U.,, Flügge,  U.-I.,, and Heldt,  H.. (1991);  Redox transfer across the inner chloroplast envelope membrane.  Plant Physiol.. 95 1131-1137
    PubMedGoogle Scholar
  • 35 Hille,  B.. (1992) Ionic Channels of Excitable Membranes. Sunderland MA; Sinauer Associates Inc.
    Google Scholar
  • 36 Hodge,  A.,, Paterson,  E.,, Thornton,  B.,, Millard,  P.,, and Killham,  K.. (1997);  Effects of photon flux density on carbon partitioning and rhizosphere carbon flow of Lolium perenne. .  J. Exp. Bot.. 48 1797-1805
    CrossrefPubMedGoogle Scholar
  • 37 Hormann,  H.,, Neubauer,  C.,, Asada,  K.,, and Schreiber,  U.. (1993);  Intact chloroplasts display pH 5 optimum of O2-reduction in the absence of methyl viologen: Indirect evidence for a regulatory role of superoxide protonation.  Photosynth. Res.. 37 69-80
    PubMedGoogle Scholar
  • 38 Hossain,  M. A.,, Nakano,  Y.,, and Asada,  K.. (1984);  Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide.  Plant Cell Physiol.. 25 385-395
    PubMedGoogle Scholar
  • 39 Igamberdiev,  A. U.,, Bykova,  N. V.,, and Gardeström,  P.. (1997);  Involvement of cyanide-resistant and rotenone-insensitive pathways of mitochondrial electron transport during oxidation of glycine in higher plants.  FEBS Lett.. 412 265-269
    CrossrefPubMedGoogle Scholar
  • 40 Igamberdiev,  A. U.,, Bykova,  N. V.,, and Gardeström,  P.. (1998) Operation of coupled and non-coupled pathways of mitochondrial electron transport in photosynthetic plant cell. Photosynthesis: Mechanisms and Effects, Vol. V. Garab, G., ed. Dordrecht; Kluwer Academic Publishers pp. 3665-3670
    Google Scholar
  • 41 Ivanov,  B., and Edwards,  G. E.. (1997);  Electron flow accompanying the ascorbate peroxidase cycle in maize mesophyll chloroplasts and its cooperation with linear electron flow to NADP+ and cyclic electron flow in thylakoid membrane energization.  Photosynth. Res.. 52 187-198
    CrossrefPubMedGoogle Scholar
  • 42 Kendall,  A. C.,, Wallsgrove,  R. M.,, Hall,  N. P.,, Turner,  J. C.,, and Lea,  P. J.. (1986);  Carbon and nitrogen metabolism in barley (Hordeum vulgare L.) mutants lacking ferredoxin-dependent glutamate synthase.  Planta. 168 316-323
    CrossrefPubMedGoogle Scholar
  • 43 Kolbowski,  J.,, Reising,  H.,, and Schreiber,  U.. (1990);  Computer controlled pulse modulation system for analysis of photo-acoustic signals in the time domain.  Photosynth. Res.. 25 309-316
    CrossrefPubMedGoogle Scholar
  • 44 Kooten,  O. v., and Snel,  J. F. H.. (1990);  The use of chlorophyll fluorescence in plant stress physiology.  Photosynth. Res.. 25 147-150
    CrossrefPubMedGoogle Scholar
  • 45 Krause,  G. H.,, Vernotte,  C.,, and Briantais,  J. M.. (1982);  Photoinduced quenching of chlorophyll fluorescence in intact chloroplasts and algae.  Biochim. Biophys. Acta. 679 116-124
    PubMedGoogle Scholar
  • 46 Magalhaes,  J. R., and Huber,  D. M.. (1989);  Ammonium assimilation in different plant species as affected by nitrogen form and pH control in solution culture.  Fert. Res.. 21 1-6
    CrossrefPubMedGoogle Scholar
  • 47 Magalhaes,  J. S., and Wilcox,  G. E.. (1983);  Tomato growth and mineral composition as influenced by nitrogen form and light intensity.  J. Plant Nutr.. 6 847-862
    PubMedGoogle Scholar
  • 48 Magalhaes,  J. S., and Wilcox,  G. E.. (1984);  Ammonium toxicity development in tomato plants relative to nitrogen form and light intensity.  J. Plant Nutr.. 7 1477-1496
    PubMedGoogle Scholar
  • 49 Marschner,  H.. (1995) Mineral Nutrition of Higher Plants. London; Academic Press
    Google Scholar
  • 50 Marschner,  H., and Cakmak,  I.. (1989);  High light intensity enhances chlorosis and necrosis in leaves of zinc, potassium and magnesium deficient bean (Phaseolus vulgaris) plants.  J. Plant Physiol.. 134 308-314
    PubMedGoogle Scholar
  • 51 Morales,  F.,, Abadía,  A.,, Belkhodja,  R.,, and Abadía,  J.. (1994);  Iron deficiency-induced changes in photosynthetic pigment composition of field-grown pear (Pyrus communis L.) leaves.  Plant Cell Environ.. 17 1153-1160
    PubMedGoogle Scholar
  • 52 Nakano,  Y., and Asada,  K.. (1981);  Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts.  Plant Cell Physiol.. 22 867-880
    PubMedGoogle Scholar
  • 53 Neubauer,  C., and Yamamoto,  H. Y.. (1994);  Membrane barriers and Mehler-peroxidase reaction limit the ascorbate available for violaxanthin de-epoxidase activity in intact chloroplasts.  Photosynth. Res.. 39 137-147
    CrossrefPubMedGoogle Scholar
  • 54 Noctor,  G., and Foyer,  C. H.. (1998);  A re-evaluation of the ATP: NADPH budget during C3 photosynthesis: a contribution from nitrate assimilation and its associated respiratory activity?.  J. Exp. Bot.. 49 1895-1908
    CrossrefPubMedGoogle Scholar
  • 55 Polle,  A.,, Chakrabarti,  K.,, Chakrabarti,  S.,, Seifert,  F.,, Schramel,  P.,, and Rennenberg,  H.. (1992);  Antioxidants and manganese deficiency in needles of Norway spruce (Picea abies L.) trees.  Plant Physiol.. 99 1084-1089
    PubMedGoogle Scholar
  • 56 Prasil,  O.,, Kolber,  Z.,, Berry,  J. A.,, and Falkowski,  P. G.. (1996);  Cyclic electron flow around photosystem II in vivo. .  Photosynth. Res.. 48 395-410
    CrossrefPubMedGoogle Scholar
  • 57 Purvis,  A. C.. (1997);  Role of the alternative oxidase in limiting superoxide production by plant mitochondria.  Physiol. Plant.. 100 165-170
    CrossrefPubMedGoogle Scholar
  • 58 Reising,  H., and Schreiber,  U.. (1994);  Inhibition by ethoxyzolamide of a photoacoustic uptake signal in leaves: Evidence for carbonic anhydrase catalyzed CO2 solubilisation.  Photosynth. Res.. 41 65-73
    PubMedGoogle Scholar
  • 59 Salsac,  L.,, Chaillou,  S.,, Morot-Gaudry,  J. F.,, Lesaint,  C.,, and Jolivet,  E.. (1987);  Nitrate and ammonium nutrition in plants.  Plant. Physiol. Biochem.. 25 805-812
    PubMedGoogle Scholar
  • 60 Sakaki,  T.,, Kondo,  N.,, and Sugahara,  K.. (1983);  Breakdown of photosynthetic pigments and lipids in spinach leaves with ozone fumigation: Role of active oxygens.  Physiol. Plant.. 59 28-34
    PubMedGoogle Scholar
  • 61 Schinner,  K.,, Tabrizi,  H.,, and Hansen,  U. P.. (1999) Indication for the Mehler reaction obtained from comparing photoacoustic and fluorescence-clamp measurements. Photosynthesis: Mechanisms and Effects, Vol. III. Garab, G., ed. Dordrecht, Boston, London; Kluwer Academics Publishers pp. 1759-1762
    Google Scholar
  • 62 Schoener,  S., and Krause,  G. H.. (1990);  Protective systems against active oxygen species in spinach. Response to cold acclimation in excess light.  Planta. 180 383-389
    CrossrefPubMedGoogle Scholar
  • 63 Schreiber,  U., and Bilger,  W.. (1987) Rapid assessment of stress effects on plant leaves by chlorophyll fluorescence measurements. NATO ASI Series. Plant Response to Stress. Vol. G 15. Tehunen, J. D., ed. Berlin; Springer-Verlag pp. 27-53
    Google Scholar
  • 64 Schreiber,  U., and Krieger,  A.. (1998);  Two fundamentally different types of variable chlorophyll fluorescence in vivo. .  FEBS Letters. 397 131-135
    PubMedGoogle Scholar
  • 65 Siedow,  J. N., and Umbach,  A. L.. (1995);  Plant mitochondrial electron transfer and molecular biology.  The Plant Cell. 7 821-831
    PubMedGoogle Scholar
  • 66 Smirnoff,  N., and Colombe,  S. V.. (1988);  Drought influences the activity of enzymes of the chloroplast hydrogen peroxide scavenging system.  J. Exp. Bot.. 39 1097-1108
    PubMedGoogle Scholar
  • 67 Sundby,  C.,, Chow,  W. S.,, and Anderson,  J. M.. (1993);  Effects on photosystem II, photoinhibition, and plant performance of the spontaneous mutation of serine-264 in the photosystem II reaction center D1 protein in triazine-resistant Brassica napus L.  Plant Physiol.. 103 105-113
    PubMedGoogle Scholar
  • 68 Tabrizi,  H.,, Schinner,  K.,, Spors,  J.,, and Hansen,  U. P.. (1998);  Deconvolution of the three components of the photoacoustic signal by curve fitting and the relationship of CO2 uptake to proton fluxes.  Photosynth. Res.. 57 101-115
    CrossrefPubMedGoogle Scholar
  • 69 Tasaka,  Y.,, Gombos,  Z.,, Nishiyama,  Y.,, Mohanty,  P.,, Ohba,  T.,, Ohki,  K.,, and Murata,  N.. (1996);  Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosythesis.  EMBO J.. 15 6416-6425
    PubMedGoogle Scholar
  • 70 Vanselow,  K. H.. (1993);  The effect of N-nutrients on the acceptor pool of PS I and thylakoid energization as measured by chlorophyll fluorescence of Dunaliella salina. .  J. Exp. Bot.. 44 1331-1340
    PubMedGoogle Scholar
  • 71 Verhoeven,  A. S.,, Adams III,  W. W.,, and Demmig-Adams,  B.. (1996);  Close relationship between the state of the xanthophyll cycle pigments and photosystem II efficiency during recovery from winter stress.  Physiol. Plant.. 96 567-576
    CrossrefPubMedGoogle Scholar
  • 72 Verhoeven,  A. S.,, Demmig-Adams,  B.,, and Adams III,  W. W.. (1997);  Enhanced employment of the xanthophyll cycle and thermal energy dissipation in spinach exposed to high light and N stress.  Plant Physiol.. 113 817-824
    PubMedGoogle Scholar
  • 73 Zornoza,  P.,, Caselles,  J.,, and Carpena,  O.. (1987);  Response of pepper plants to NO3 : NH4 ratio and light intensity.  J. Plant Nutr.. 10 773-783
    PubMedGoogle Scholar

B. Sattelmacher

Institut für Pflanzenernährung und Bodenkunde Christian-Albrechts-Universität

Hermann-Rodewald-Str. 2 24098 Kiel Germany

Email: bsattelmacher@plantnutrition.uni-kiel.de

Section Editor: H. Rennenberg

      >