, Volume 192, Issue 2, pp 211–220 | Cite as

Short-term effects of nitrate, nitrite and ammonium assimilation on photosynthesis, carbon partitioning and protein phosphorylation in maize

  • C. H. Foyer
  • G. Noctor
  • M. Lelandais
  • J. C. Lescure
  • M. H. Valadier
  • J. P. Boutin
  • P. Horton


Maize (Zea mays L. cv. Contessa) was grown with a nitrogen supply that was just sufficient to support maximal biomass production. The third leaves from 14-to 21-d-old plants were harvested and net photosynthesis allowed to attain steady-state rates at an irradiance of either 250 or 700 μmol·m−2·s−1. Nitrogen in the form of either KNO3, KNO2 or NH4Cl was then supplied to the leaves through the transpiration stream. In all cases the addition of the nitrogen source resulted in an approximate doubling of the total amino-acid content of the leaves within 1 h. The glutamine pool increased to ten times the level found in control leaves in the light in the absence of added nitrogen. Glutamine accounted for about 21–24% of the total amino-acid content in leaves fed with 40 mM NH4Cl. Nitrate caused a rapid, but transient inhibition of the rate of net CO2 assimilation, accompanied by an increase in the activity of phosphoenolpyruvate carboxylase and a decrease in the maximum extractable activity of sucrose-phosphate synthase. This demonstrates that the activities of phospho-enolpyruvate carboxylase and sucrose-phosphate synthase are modulated by NO 3 in the C4 plant maize, in a similar manner to that observed in C3 plants. Nitrite or ammonium feeding resulted in decreased rates of CO2 assimilation for as long as the nitrogen source was supplied. In all cases the degree of inhibition was greatest at high irradiance and least at low irradiance, even though the total amino-acid contents of the leaves were comparable at the time when maximum inhibition of CO2 assimilation occurred. Measurements of chlorophyll-a fluorescence showed that the quantum efficiency of PSII decreased and non-radiative dissipation of excitation energy increased as CO2 assimilation was inhibited by nitrate or nitrite. These metabolites had no direct effect on thylakoid PSII-based electron transport. Ammonium ions weakly inhibited O2 evolution at high concentrations. The addition of nitrogen (KNO 3 , KNO2 or NH4Cl) caused a significant decrease in the phosphorylation state of the light-harvesting chlorophyll-a/b-binding protein of the thylakoid membranes. We conclude that the response of photosynthetic carbon assimilation and electron transport in maize is essentially similar whether nitrogen is supplied in the form of nitrate, nitrite or ammonium, with the noteworthy exception that the nitrogen-induced inhibition of photosynthesis is transient when leaves are supplied with NO 3 but sustained when NO 2 or NH 4 + is provided. We suggest that the observed modulation of phosphoenolpyruvate carboxylase and sucrose-phosphate synthase is mediated by the increase in the endogenous level of glutamine. Furthermore, the transient nature of the inhibition of CO2 assimilation in the case of NO 3 , but not NO 2 or NH 4 + , may be due to regulation of nitrate reductase.

Key words

Chlorophyll-a/b-binding protein complex Nitrogen assimilation Phosphoenolpyruvate carboxylase Photosynthesis Sucrose phosphate synthase Zea (photosynthesis) 

Abbreviations and Symbol








glutamic acid


index of the rate of thermal energy dissipation within the PSII antenna


light-harvesting chlorophyll-a/b-binding protein


phosphoenolpyruvate carboxylase


photon flux density


sucrose-phosphate synthase


relative quantum efficiency for electron transport by PSII


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  1. Becker, T.W., Perrot-Rechnmann, C., Suzuki, A., Hirel, B. (1993) Subcellular and immunocytochemical localisation of the enzymes involved in ammonia assimilation in mesophyll and bundle-sheath cells of maize leaves. Planta, in pressGoogle Scholar
  2. Boussac, A., Rutherford, A.W., Styring, S. (1990) Interaction of ammonia with the water-splitting enzyme in photosystem II. Biochemistry29, 24–32PubMedGoogle Scholar
  3. Bloom, A.J., Caldwell, R.M., Finazzo, J., Warner, R.L., Weissbart, J. (1989) Oxygen and carbon dioxide fluxes from barley shoots depend on nitrate assimilation. Plant. Physiol.91, 352–356Google Scholar
  4. Champigny, M.-L., Foyer, C.H. (1992) Nitrate activation of cytosolic protein kinases diverts photosynthetic carbon from sucrose to amino acid biosynthesis: basis for a new concept. Plant Physiol.100, 7–12Google Scholar
  5. Champigny, M.-L., Van Quy, L., Valadier, M.-H., Moyse, A. (1991) Effet immédiat des nitrates sur la photoassimilation du CO2 et la synthèse de saccharose dans les feuilles de blé. C. R. Acad. Sci. (Paris)312, 469–476Google Scholar
  6. Clausen, T. (1968) Measurement of32P activity in a liquid scintillation counter without the use of scintillator. Anal. Biochem.22, 70–73PubMedGoogle Scholar
  7. Demmig-Adams, B., Adams, III, W.W., Heber, U., Neimanis, S., Winter, K., Krüger, A., Czygan, F.-C., Bilger, W, Björkman, O. (1990) Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiol.92, 293–301Google Scholar
  8. De LaTorre, A., Delgado, B., Lara, C. (1991) Nitrate-dependent O2 evolution in intact leaves. Plant Physiol.96, 898–901Google Scholar
  9. Elrifi, I.R., Turpin, D.H. (1986) Nitrate and ammonium-induced photosynthetic suppression in N-limitedSelenastrum minutum. Plant Physiol.81, 273–279Google Scholar
  10. Elrifi, I.R., Turpin, D.H. (1987) The path of carbon flow during NO3-induced photosynthetic suppression in N-limitedSelenastrum minutum. Plant Physiol.83, 97–104Google Scholar
  11. Elrifi, I.R., Holmes, J.J., Weger, H.G., Mayo, W.P., Turpin, D.H. (1988) RuBP limitation of photosynthetic carbon fixation during NH3 assimilation. Plant Physiol.87, 395–401Google Scholar
  12. Furbank, R.T., Foyer, C.H. (1988) C4 plants as model experimental systems for the study of photosynthesis. New Phytol.109, 265–277Google Scholar
  13. Furbank, R.T., Stitt, M., Foyer, C.H. (1985) Intercellular compartmentation of sucrose synthesis in leaves ofZea mays L. Planta164, 172–178Google Scholar
  14. Galtier, N., Foyer, C.H., Huber, J., Voelker, T.A., Huber, S.C. (1993) Effects of elevated sucrose-phosphate synthase activity on photosynthesis, assimilate partitioning and growth in tomato (Ly copersicon esculentum var. UC82B). Plant Physiol.101, 535–543PubMedGoogle Scholar
  15. Genty, B., Briantais, J.M., Baker, N.R. (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta990, 87–92Google Scholar
  16. Hite, D.R.C., Outlaw, W.H.Jr, Tarczynski, M.C. (1993) Elevated levels of both sucrose-phosphate synthase and sucrose synthase inVicia guard cells indicate cell specific carbohydrate interconversions. Plant Physiol.101, 1217–1221PubMedGoogle Scholar
  17. Horton, P., Noctor, G., Rees, D. (1990) Regulation of light harvesting and electron transport in Photosystem II. In: Perpectives in biochemical and genetic regulation of photosynthesis, pp. 145–158, Zelich, I., ed. Wiley-Liss Inc, New YorkGoogle Scholar
  18. Huber, J.L., Campbell, W.H., Redinbaugh, M.G. (1992a) Reversible light/dark modulation of spinach leaf nitrate reductase activity involves protein phosphorylation. Arch. Biochem. Biophys.296, 58–65PubMedGoogle Scholar
  19. Huber, J.L., Campbell, W.H., Redinbaugh, M.G. (1992b) Apparent dependence of the light activation of nitrate reductase and sucrose-phosphate synthase activities in spinach leaves on protein synthesis. Plant Cell Physiol.33, 639–646Google Scholar
  20. Kaiser, W.M., Forster, J. (1989) Low CO2 prevents nitrate reduction in leaves. Plant Physiol.91, 970–974Google Scholar
  21. Kaiser, W.M., Spill, D. (1991) Rapid modulation of spinach leaf nitrate reductase by photosynthesis. II. In vitro modulation by ATP and AMP. Plant Physiol.96, 368–375Google Scholar
  22. Kaiser, W.M., Spill, D., Brendle-Behnisch, E. (1992) Rapid light-dark modulation of assimilatory nitrate reductase in spinach leaves involves adenine nucleotiudes. Planta186, 236–240Google Scholar
  23. Khamis, S., Lamaze, T. (1990) Maximal biomass production can occur in corn (Zea mays) in the absence of NO3 accumulation in either leaves or roots. Physiol. Plant.78, 388–394Google Scholar
  24. Khamis, S., Lamaze, T, Lemoine, Y, Foyer, C.H. (1990) Adaptation of the photosynthetic apparatus in maize leaves as a result of nitrogen limitation. Plant Physiol.94, 1436–1443Google Scholar
  25. Larsson, M., Olsson, T., Larsson, C.-M. (1985) Distribution of reducing power between photosynthetic carbon and nitrogen assimilation inScenedesmus. Planta164, 246–253Google Scholar
  26. Manh, C.T., Bismuth, E., Boulin, J.P., Provot, M., Champigny, M.L. (1993) Metabolite effectors for short-term enhancement of phosphoenolpyruvate carboxylase activity and decrease of net sucrose synthesis in wheat leaves. Plant Physiol., in pressGoogle Scholar
  27. Nimmo, G.A., McNaughton, G.A.L., Fewson, C.A., Wilkins, H.B., Nimmo, H.G. (1987) changes in the kinetic properties and phosphorylation state of phosphoenolpyruvate carboxylase inZea mays leaves in response to light and dark. FEBS Lett.213, 18–22Google Scholar
  28. Outlaw, W.H.Jr (1983) Current concepts on the role of potassium in stomatal movements. Plant Physiol.59, 302–311Google Scholar
  29. Purczeld, P., Chon, C.J., Portis, A.R., Heldt, H.W., Heber, U. (1978) The mechanism of the control of carbon fixation by the pH in the chloroplast stroma. Studies with nitrite-mediated proton transfer across the envelope. Biochim. Biophys. Acta501, 488–498PubMedGoogle Scholar
  30. Robinson, J.M. (1986) Carbon dioxide and nitrite photoassimilatory processes do not intercompete for reducing equivalents in spinach and soybean leaf chloroplasts. Plant Physiol.80, 676–684Google Scholar
  31. Robinson, J.M. (1988) Spinach leaf chloroplast CO2 and NO2 photoassimilations do not compete for photogenerated reductant. Plant Physiol.88, 1373–1380Google Scholar
  32. Rufty, TW., Volk, R.J. (1986) Alterations in enrichment of NO3 and reduced-N in xylem exudate during and after entended plant exposure to15NO3. Plant Soil91, 329–332Google Scholar
  33. Sakakibara H., Kawabata, S., Hase, T., Sugiyama, T. (1992) Differential effects of nitrate and light on the expression of glutamine synthases and ferredoxin-dependent glutamate synthase in maize. Plant Cell Physiol.33, 1193–1198Google Scholar
  34. Smith, R.G., Vanlerberghe, G.C., Stitt, M., Turpin, D.H. (1989) Short-term metabolite changes during transient ammonium assimilation by the N-limited green algaSelenastrum minutum. Plant Physiol.91, 749–755Google Scholar
  35. Sugiharto, B., Sugiyama, T. (1992) Effects of nitrate and ammonium on gene expression of phosphoenolpyruvate carboxylase and nitrogen metabolism in maize leaf tissue during recovery from nitrogen stress. Plant Physiol.98, 1403–1408Google Scholar
  36. Sugiharto, B., Miyata, K., Nakamoto, H., Sasakawa, H., Sugiyama, T. (1990) Regulation of expression of carbon-assimilating enzymes by nitrogen in maize leaf. Plant Physiol.92, 963–969Google Scholar
  37. Sugiharto, B., Suzuki, I., Burnell, J.N., Sugiyama, T. (1992) Glutamine induces the N-dependent accumulation of mRNA's encoding phosphoenolpyruvate carboxylase and carbonic anhydrase in detached maize leaf tissue. Plant Physiol.100, 2066–2070Google Scholar
  38. Vanlerberghe, G.C., Schuller, K.A., Smith, R.G., Feil, R., Plaxton, W.C., Turpin, D.H. (1990) Relationship between NH4+ assimilation rate and in vivo phosphoenolpyruvate carboxylase activity. Regulation of anaplerotic carbon flow in the green algaeSelenastrum minutum. Plant Physiol.94, 284–290Google Scholar
  39. Van Quy, L., Lamaze, T., Champigny, M.L. (1991a) Short-term effects of nitrate on sucrose synthesis in wheat leaves. Planta185, 53–57Google Scholar
  40. Van Quy, L., Foyer, C.H., Champigny, M.L. (1991b) Effects of light and NO3 on wheat leaf phosphoenolpyruvate carboxylase activity. Evidence for covalent modulation of the C3 enzyme. Plant Physiol.97, 1476–1482Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • C. H. Foyer
    • 1
  • G. Noctor
    • 2
  • M. Lelandais
    • 1
  • J. C. Lescure
    • 1
  • M. H. Valadier
    • 1
  • J. P. Boutin
    • 1
  • P. Horton
    • 2
  1. 1.Laboratoire du Métabolisme, Institut National de la Recherche AgronomiqueVersailles cedexFrance
  2. 2.Department of Molecular Biology and BiotechnologyRobert Hill InstituteSheffieldUK

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