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Trees

, Volume 17, Issue 4, pp 359–366 | Cite as

Photosynthesis-Rubisco relationships in foliage of Pinus sylvestris in response to nitrogen supply and the proposed role of Rubisco and amino acids as nitrogen stores

  • Charles R. WarrenEmail author
  • Erwin Dreyer
  • Mark A. Adams
Original Article
  • 1.1k Downloads

Abstract

Relationships between photosynthetic capacity, and needle contents of N, Rubisco and amino acids were investigated in potted Pinus sylvestris L. trees. Three-year-old seedlings of P. sylvestris were grown for 4 years with three nutrient regimes. Concentrations of N, amino acids, amides and Rubisco were measured and expressed on a needle area basis, and the in vivo performances of Rubisco (maximum rate of carboxylation, V cmax) and of electron transport (maximum light driven electron flux, J max) were estimated via a biochemically based model of photosynthesis. Needle content of Rubisco-N was at least six times that of amino acid + amide-N and was positively related to N area. The estimated in vivo specific activity of Rubisco (V cmax/Rubisco content per unit area) was low and negatively related to N content per unit area (N area). J max/Rubisco content was negatively related to N area, whereas V cmax/J max was unrelated to N area. Hence, Rubisco content was in excess of the amount required for photosynthesis and this excess was positively related to N area. These data support the hypothesis that with increasing N area, Rubisco functions increasingly as a storage protein in addition to its catalytic functions.

Keywords

Excess nutrients Low nutrients Maximum rate of carboxylation Leaf gas exchange Photosynthesis 

Abbreviations

A

rate of net photosynthesis

CE

capillary electrophoresis

Ca

ambient CO2 concentration

Ci

intercellular CO2 concentration

Chl

chlorophyll

Jmax

maximum rate of electron transport

Kc and Ko

Michaelis-Menten constants for Rubisco carboxylation and oxygenation

Kcat

specific activity of Rubisco

Narea

N content per unit projected leaf area

Nmass

N concentration

Oi

intercellular oxygen concentration

PPFD

photosynthetic photon flux density

PVPP

polvinylpolypyrrolidone

Rd

'day' respiration (non-photorespiratory CO2 evolution)

Rubisco

Ribulose-1, 5-bisphosphate carboxylase/oxygenase

SLA

specific leaf area

Vcmax

maximum rate of Rubisco carboxylation

Notes

Acknowledgements

C.W. was supported by a department of CALM/UWA scholarship and an Australian Academy of Science award for young Australian researchers visiting Europe. The Australian Research Council is warmly thanked for financial support. Trees were grown by Jean Marie Gioria at INRA Nancy. Thanks are due to Natacha Guérard who gave access to her experimental design aimed at testing the impact of nitrogen supply on the sensitivity of Scots pines to a guild of pests and diseases. This experiment was part of a project supported by the Commission of the European Communities, Agriculture and Fisheries (FAIR) specific RTD Program CT96-1854 "Effects of water and nutrient stress on pine susceptibility to various pest and disease guilds". We gratefully acknowledge anonymous reviewers for helpful comments on this manuscript.

References

  1. Caemmerer S von, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387Google Scholar
  2. Caemmerer S von, Evans JR, Hudson GS, Andrews TJ (1994) The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco. Planta 195:88–97Google Scholar
  3. Camm E (1993) Photosynthetic responses in developing and year-old Douglas-fir needles during new shoot development. Trees 8:61–66Google Scholar
  4. Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260Google Scholar
  5. Cheng L, Fuchigami L (2000) Rubisco activation state decreases with increasing nitrogen content in apple leaves. J Exp Bot 51:1687–1694CrossRefPubMedGoogle Scholar
  6. Dreyer E, Le Roux X, Montpied P, Daudet FA, Masson F (2001) Temperature response of leaf photosynthetic capacity in seedlings from seven temperate tree species. Tree Physiol 21:223–232PubMedGoogle Scholar
  7. Edfast A-B, Näsholm T, Ericsson A (1990) Free amino acids in needles of Norway spruce and Scots pine trees on different sites in areas with two levels of nitrogen deposition. Can J For Res 20:1132–1136Google Scholar
  8. Eichelmann H, Laisk A (1999) Ribulose-1,5-bisphosphate carboxylase/oxygenase content, assimilatory charge, and mesophyll conductance in leaves. Plant Physiol 119:179–189CrossRefPubMedGoogle Scholar
  9. Epron D, Godard D, Cornic G, Genty B (1995) Limitation of net CO2 assimilation rate by internal resistance to CO2 transfer in the leaves of two tree species (Fagus sylvatica L. and Castanea sativa Mill.). Plant Cell Environ 18:43–51Google Scholar
  10. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9-19Google Scholar
  11. Evans JR, Caemmerer S von, Setchell BA, Hudson GS (1994) The relationship between CO2 transfer conductance and leaf anatomy in transgenic tobacco with a reduced content of Rubisco. Aust J Plant Physiol 21:475–495Google Scholar
  12. Farquhar GD, Caemmerer S von, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90Google Scholar
  13. Gebauer G, Melzer A, Rehder H (1984) Nitrate content and nitrate reductase activity in Rumex obtusifolius L. I. Differences in organs and diurnal changes. Oecologia 63:136–142Google Scholar
  14. Gezelius K (1986) Ribulose bisphosphate carboxylase, protein and nitrogen in Scots pine seedlings cultivated at different nutrient levels. Physiol Plant 68:245–251Google Scholar
  15. Gezelius K, Näsholm T (1993) Free amino acids and protein in Scots pine (Pinus sylvetsris L.) seedlings cultivated at different nutrient levels. Tree Physiol 13:71–86Google Scholar
  16. Guérard N (2001) Résistance du pin sylvestre aux attaques de scolytes et de leurs champignons associés: interactions avec l'alimentation hydrique et minérale. PhD, Sciences de la Vie. Université François Rabelais, Tours, FranceGoogle Scholar
  17. Harley PC, Tenhunen JD (1991) Modeling the photosynthetic response of C3 leaves to environmental factors. In: Modeling crop photosynthesis—from biochemistry to canopy, vol 19. American Society of Agronomy and Crop Science Society of America, Madison, Wis., pp 17–39Google Scholar
  18. Jach ME, Ceulemans R (2000) Effects of season, needle age and elevated atmospheric CO2 on photosynthesis in Scots pine (Pinus sylvestris). Tree Physiol 20:145–157Google Scholar
  19. Jordan DB, Ogren WL (1984) The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase. Dependence on ribulosebisphosphate concentration, pH and temperature. Planta 161:308–313Google Scholar
  20. Kang S-M, Titus JS (1980) Qualitative and quantitative changes in nitrogen compounds in senescing leaf and bark tissue of the apple. Physiol Plant 50:285–290Google Scholar
  21. Kellomäki S, Wang KJ (1997) Effects of long-term CO2 and temperature elevation on crown nitrogen distribution and daily photosynthetic performance of Scots pine. For Ecol Manage 99:309–326Google Scholar
  22. Laitinen K, Luomala E-M, Kellomäki S, Vapaavuori E (2000) Carbon assimilation and nitrogen in needles of fertilized and unfertilized field-grown Scots pine at natural and elevated concentrations of CO2. Tree Physiol 20:881–892PubMedGoogle Scholar
  23. Lawlor DW, Boyle FA, Young AT, Keys AJ, Kendall AC (1987) Nitrate nutrition and temperature effects on wheat: photosynthesis and photorespiration of leaves. J Exp Bot 38:393–408Google Scholar
  24. Meir P, Kruijt B, Broadmeadow M, Barbosa E, Kull O, Carswell F, Nobre A, Jarvis PG (2002) Acclimation of photosynthetic capacity to irradiance in tree canopies in relation to leaf nitrogen concentration and leaf mass per unit area. Plant Cell Environ 25:343–357CrossRefGoogle Scholar
  25. Millard P (1988) The accumulation and storage of nitrogen by herbaceous plants. Plant Cell Environ 11:1-8Google Scholar
  26. Millard P, Proe MF (1992) Storage and internal cycling of nitrogen in relation to seasonal growth of Sitka spruce. Tree Physiol 10:33–43Google Scholar
  27. Näsholm T, Ericsson A (1990) Seasonal changes in amino acids, protein and total nitrogen in needles of fertilized Scots pine trees. Tree Physiol 6:267–281Google Scholar
  28. Niinemets U, Tenhunen JD (1997) A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade tolerant species Acer saccharum. Plant Cell Environ 20:845–866Google Scholar
  29. Nordin A, Uggla C, Näsholm T (2001) Nitrogen forms in bark, wood and foliage of nitrogen-fertilized Pinus sylvestris. Tree Physiol 21:59–64PubMedGoogle Scholar
  30. Poorter H, Evans JR (1998) Photosynthetic nitrogen use efficiency of species that differ inherently in specific leaf area. Oecologia 116:63–72CrossRefGoogle Scholar
  31. Popp M, Lied W, Meyer AJ, Richter A, Schiller P, Schwitte H (1996) Sample preservation for determination of organic compounds: microwave versus freeze-drying. J Exp Bot 47:1469–1473Google Scholar
  32. Proe MF, Millard P (1994) Relationship between nutrient supply, nitrogen partitioning and growth in young Sitka spruce [Picea sitchensis (Bong.) Carr.]. Tree Physiol 14:75–88Google Scholar
  33. Proe MF, Midwood AJ, Craig J (2000) Use of stable isotopes to quantify nitrogen, potassium and magnesium dynamics in young Scots pine (Pinus sylvestris). New Phytol 146:461–469CrossRefGoogle Scholar
  34. Sage RF, Pearcy RW, Seemann JR (1987) The nitrogen use efficiency of C3 and C4 plants. Plant Physiol 85:355–359Google Scholar
  35. Stitt M, Schulze ED (1994) Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology. Plant Cell Environ 17:465–487Google Scholar
  36. Tissue DT, Thomas RB, Strain BR (1993) Long-term effects of elevated CO2 and nutrients on photosynthesis and Rubisco in loblolly pine seedlings. Plant Cell Environ 16:859–865Google Scholar
  37. Wang K, Kellomäki S, Laitinen K (1995) Effects of long-term temperature and CO2 treatments on the photosynthesis of Scots pine. Tree Physiol 15:211–218Google Scholar
  38. Warren CR, Adams MA (2000) Capillary electrophoresis for the determination of major amino acids and sugars in foliage: application to the nitrogen nutrition of sclerophyllous species. J Exp Bot 51:1147–1157CrossRefPubMedGoogle Scholar
  39. Warren CR, Adams MA (2001) Distribution of N, Rubisco and photosynthesis in Pinus pinaster and acclimation to light. Plant Cell Environ 24:599–612CrossRefGoogle Scholar
  40. Warren CR, Adams MA (2002) Phosphorus affects growth and partitioning of N to Rubisco in Pinus pinaster. Tree Physiol 22:11–19PubMedGoogle Scholar
  41. Warren CR, Adams MA, Chen Z (2000) Is photosynthesis related to concentrations of nitrogen and Rubisco in leaves of Australian native plants? Aust J Plant Physiol 27:407–416CrossRefGoogle Scholar
  42. Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313Google Scholar
  43. Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C3 plants—a retrospective analysis of the A/C i curves from 109 species. J Exp Bot 44:907–920Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Charles R. Warren
    • 1
    • 4
    Email author
  • Erwin Dreyer
    • 2
  • Mark A. Adams
    • 1
    • 3
  1. 1.Department of BotanyUniversity of Western AustraliaCrawleyAustralia
  2. 2.UMR INRA-UHPEcologie et Ecophysiologie ForestièresFrance
  3. 3.Forest Science CentreThe University of Melbourne/Natural Resources and EnvironmentCreswickAustralia
  4. 4.Centre for Forest BiologyUniversity of VictoriaVictoriaCanada

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