Plant Biol (Stuttg) 2001; 3(4): 417-425
DOI: 10.1055/s-2001-16461
Original Paper
Georg Thieme Verlag Stuttgart ·New York

Growth and Photosynthetic Carbon Metabolism in Tobacco Plants under an Oscillating CO2 Concentration in the Atmosphere

M. M. Chaves 1, 2 , E. Pantschitz 3 , E.-D. Schulze 3
  • 1 Instituto Superior de Agronomia, Tapada da Ajuda, 1399 Lisboa codex, Portugal
  • 2 Instituto de Tecnologia Quimica e Biológica, Apartado 127, 2781-901 Oeiras, Portugal
  • 3 Max-Planck-Institut for Biogeochemistry, Carl-Zeiss-Promenade 10, 07745 Jena, Germany
Further Information

Publication History

January 8, 2001

May 14, 2001

Publication Date:
16 August 2001 (online)

Abstract

The hypothesis for the present work was that photosynthetic acclimation to increased atmospheric CO2 in Nicotiana tabacum could be prevented by an oscillating supply of CO2. This was tested by growing half of the plants (for the 20 day period after sowing) at 700 μmol mol-1 CO2 (S+ plants) and half at 350 μmol mol-1 CO2 (S- plants) and thereafter switching them every 48 h from high to low CO2 and vice versa. These plants were compared with plants continuously kept (from sowing onwards) at 350 μmol mol-1 CO2 (C- plants) and 700 μmol mol-1 CO2 (C+ plants). Switching plants from high to low CO2 and vice versa (S+ and S-) did not improve plant growth efficiency, as hypothesized. The extra carbon fixed by the leaves under increased CO2 in the atmosphere, supplied either continuously or intermittently, was mostly stored as starch and not used to build additional structural biomass. The differences in final plant biomass, observed between S+ and S- plants, are explained by the CO2 concentration in the atmosphere during the first 20 days after sowing, the oscillation in CO2 supply thereafter is playing a smaller role in this response. Switching plants from high to low CO2 and vice versa, also did not prevent down-regulation of photosynthesis, despite lower leaf sugar concentrations than in C+ plants. Nitrate concentration decreased dramatically in C+, S+ and S- plants. The leaf C/N ratio was highest in C+ plants (ranging from 8 to 13), intermediate in S+ and S- plants (from 7 to 11) and lowest in C- plants (from 6 to 8). This supports the view that the balance between carbohydrates and nitrogen may have a triggering role in plant response under elevated CO2. Carbon export rates by the leaves seem to be independent of total carbon assimilation, suggesting a sink limiting effect on tobacco growth and phototsynthesis under elevated CO2.

References

  • 01 Arp,  W. J.. (1991);  Effect of source-sink relations on photosynthetic acclimation to elevated CO2.  Plant, Cell and Environment. 14 869-875
  • 02 Bazzaz,  F. A.. (1990);  The response of natural ecosystems to the rising global CO2 levels.  Annual Review Ecological Systems. 21 167-196
  • 03 Bazzaz,  F. A.. (1993) Use of plant growth analyses in global change studies: modules, individuals, and populations. Design and execution of experiments in CO2 enrichment. Schulze, E.-D. and Mooney, H. A., eds. Brussels; Ecosystems Research Report, 6. CEC pp. 53-71
  • 04 Cardon,  Z. G.,, Berry,  J. A.,, and Woodrow,  I. E.. (1995);  Fluctuating CO2 drives species-specific changes in water use efficiency.  Journal of Biogeography. 22 203-208
  • 05 Christ,  R. A.. (1989);  Records of source-sink relations by means of respiration measurements.  Journal of Experimental Botany. 40 503-509
  • 06 Christ,  R. A., and Körner,  C.. (1995);  Responses of shoot and root gas exchange, leaf blade expansion and biomass production to pulses of elevated CO2 in hydroponics wheat.  Journal of Experimental Botany. 46 1661-1667
  • 07 Delhon,  P.,, Gojon,  A.,, Tillard,  P.,, and Passama,  L.. (1995);  Diurnal regulation of NO3 uptake in soybean plants.  Journal of Experimental Botany. 46 1585-1594
  • 08 den Hertog,  J.,, Stulen,  I.,, Fonseca,  F.,, and Delea,  P.. (1996);  Modulation of carbon and nitrogen allocation in Urtica dioica and Plantago major by elevated CO2: Impact of accumulation of non-structural carbohydrates and ontogenetic drift.  Physiologica Plantarum. 98 77-88
  • 09 Drake,  B. G.,, González-Meler,  M. A.,, and Long,  S. P.. (1997);  More efficient plants: Consequence of rising atmospheric CO2.  Annual Review of Plant Physiology and Plant Molecular Biology. 48 609-639
  • 10 Evans,  L. S., and Hendrey,  G. R.. (1992) Responses of cotton foliage to short-term fluctuations in CO2 partial pressures. FACE: Free-air CO2 enrichment for plant research in the field. Hendrey, G. H., ed. Boca Raton, FL; CRC Press pp. 203-212
  • 11 Fales,  F. W.. (1951);  The assimilation and degradation of carbohydrates by yeast cells.  Journal of Biological Chemistry. 193 113-124
  • 12 Farrar,  J. F., and Gunn,  S.. (1996) Effects of temperature and atmospheric carbon dioxide on source-sink relations in the context of climate change. Photoassimilate distribution in plants and crops. Source and sink relationships. Zamski, E., Schaffer, A. A., eds. New York; Marcel Dekker pp. 389-406
  • 13 Fitchner,  K.,, Quick,  W. P.,, Schulze,  E. D.,, Mooney,  H. A.,, Rodermel,  S. R.,, Bogorad,  L.,, and Stitt,  M.. (1993);  Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with ”antisense” rbcS. V. Relationship between photosynthetic rate, storage strategy, biomass allocation and vegetative plant growth at three different nitrogen supplies.  Planta. 190 1-9
  • 14 Garcia,  R. L.,, Long,  S. P.,, Wall,  G. W.,, Osborne,  C. P.,, Kimbal,  B. A.,, Nie,  G. Y.,, Pinter  Jr, P. J.,, Lamorte,  R. L.,, and Wechsung,  F.. (1998);  Photosynthesis and conductance of spring-wheat leaves: field response to continuous free-air atmospheric CO2 enrichment.  Plant, Cell and Environment. 21 659-669
  • 15 Gebauer,  R. L.,, Reynolds,  J. F.,, and Strain,  B. R.. (1996);  Allometric relations and growth in Pinus taeda: the effect of elevated CO2 and changing N availability.  New Phytol.. 134 85-93
  • 16 Gebauer,  G.,, Melzer,  A.,, and Rehder,  H.. (1984);  Nitrate content and nitrate reductase activity in Rumex obtusifolia L. I. Differences in organs and diurnal changes.  Oecologia. 92 236-241
  • 17 Geiger,  M.,, Walch-Liu,  P.,, Engels,  C.,, Harnecker  J.,, Schulze,  E.-D.,, Ludewig,  F.,, Sonnewald,  U.,, Scheible  W.-R.,, and Stitt  M.. (1998);  Enhanced carbon dioxide leads to a modified diurnal rhythm of nitrate reductase activity in older plants, and a large stimulation of nitrate reductase activity and higher levels of amino acids in tobacco plants.  Plant, Cell and Environment. 21 253-268
  • 18 Gibson,  S. I.. (2000);  Plant sugar-response pathways. Part of a complex regulatory web.  Plant Physiology. 124 1532-1539
  • 19 Hendrey,  G. R.,, Long,  S. P.,, McKee,  I. F.,, and Baker,  N. R.. (1997);  Can photosynthesis respond to short-term fluctuations in atmospheric carbon dioxide?.  Photosynthesis Research. 51 179-184
  • 20 Jang,  J.-C., and Sheen,  J.. (1997);  Sugar sensing in higher plants.  Trends in Plant Science. 2 208-213
  • 21 Koch,  K. E.. (1996);  Carbohydrate-modulated gene expression in plants.  Annual Reviews of Plant Physiology and Plant Molecular Biology. 47 509-540
  • 22 Körner,  C.,, Pelaez-Riedl,  S.,, and Van Bell,  A. J. E.. (1995);  CO2 responsiveness of plants: a possible link to phloem loading.  Plant, Cell and Environment. 18 595-600
  • 23 Krapp,  A.,, Hoffman,  B.,, Schafer,  C.,, and Stitt,  M.. (1993);  Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: a mechanism of the sink regulation of photosynthesis.  The Plant Journal. 3 817-828
  • 24 Leegood,  R. C.,, Walker,  D. A.,, and Foyer,  C. H.. (1985) Regulation of the Benson-Calvin cycle. Photosynthetic mechanisms and the environment. Barber, J. and Baker, N. R., eds. Amsterdam; Elsevier Science Publ. pp. 189-258
  • 25 Ludewig,  F.,, Sonnewald,  U.,, Kauder,  F.,, Heineke,  D.,, Geiger,  M.,, Stitt,  M.,, Bernd,  T.,, Müller-Röber,  B. T.,, Gillissen,  B.,, Kühn,  C.,, and Frommer  W. B.. (1998);  The role of transient starch in acclimation to elevated atmospheric CO2.  FEBS Letters. 429 147-151
  • 26 Moore,  B. D.,, Cheng,  S.-H.,, Sims,  D.,, and Seemann,  J. R.. (1999);  The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2.  Plant, Cell and Environment. 22 567-582
  • 27 Nielsen,  T. H.,, Krapp,  A.,, Röper-Schwarz,  U.,, and Stitt,  M.. (1998);  The sugar-mediated regulation of genes encoding the small subunit of Rubisco and the regulatory subunit of ADP glucose pyrophosphorylase is modified by phosphate and nitrogen.  Plant, Cell and Environment. 21 443-454
  • 28 Paul,  M. J., and Driscoll,  S. P.. (1997);  Sugar repression of photosynthesis: the role of carbohydrates in signalling nitrogen deficiency through source: sink imbalance.  Plant, Cell and Environment. 20 110-116
  • 29 Pearcy,  M., and Pfitsch,  W. A.. (1993);  The consequences of sunflecks for photosynthesis and growth of forest understory plants.  Ecological Studies. 100 343-360
  • 30 Poorter,  H.,, Roumet,  C.,, and Campbell,  B. D.. (1996) Interspecific variation in the growth response of plants to elevated CO2: A search for functional types. Carbon dioxide, population and communities. Körner, C. and Bazzaz, F. A., eds. New York; Academic Press pp. 375-411
  • 31 Rey,  A., and Jarvis,  P. G.. (1998);  Long-term photosynthetic acclimation to increased CO2 concentration in young birch trees (Betula pendula). .  Tree Physiology. 18 441-450
  • 32 Sage,  F. R.. (1994);  Acclimation of photosynthesis to increasing atmospheric CO2: the gas exchange perspective.  Photosynthesis Research. 39 351-368
  • 33 Sage,  F. R.,, Sharkay,  T. D.,, and Seemann,  J. R.. (1989);  Acclimatization of photosynthesis to elevated CO2 concentration in five C3 species.  Plant Physiol.. 89 590-596
  • 34 Saxe,  H.,, Ellsworth,  D. S.,, and Heath  J.. (1998);  Tree and forest functioning in an enriched CO2 atmosphere.  New Phytologist. 139 395-436
  • 35 Sicher,  R. C., and Kremer,  D. F.. (1994);  Responses of Nicotiana tabacum to carbon dioxide enrichment at low-photon flux density.  Physiologia Plantarum. 92 383-388
  • 36 Sicher,  R. C.,, Kremer,  D. F.,, and Rodermel,  S. R.. (1994);  Photosynthetic acclimation to elevated CO2 occurs in transformed tobacco with decreased ribulose-1,5-bisphosphate carboxylase oxygenase content.  Plant Physiology. 104 409-415
  • 37 Sims,  D. A.,, Luo,  Y.,, and Seemann,  J. R.. (1998);  Importance of leaf versus plant CO2 environment for photosynthetic acclimation.  Plant, Cell and Environment. 21 1189-1196
  • 38 Sheen,  J.. (1994);  Feedback control of gene-expression.  Photosynthesis Research. 39 427-438
  • 39 Stitt,  M.. (1991);  Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells.  Plant, Cell and Environment. 14 741-762
  • 40 Stitt,  M., and Krapp,  A.. (1999);  The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background.  Plant, Cell and Environment. 22 583-621
  • 41 Thomas,  J. F.,, Raper,  C. D.,, Anderson,  C. E.,, and Down,  R. J.. (1975);  Growth of young tobacco plants as affected by carbon dioxide and nutrient variables.  Agronomy Journal. 67 685-689
  • 42 Turnbull,  M. H.,, Tissue,  D. T.,, Griffin,  K. L.,, Rogers,  G. N. D.,, and Whitehead,  D.. (1998);  Photosynthetic acclimation to long-term exposure to elevated CO2 concentration in Pinus radiata D. Don. is related to age of needles.  Plant, Cell and Environment. 21 1019-1028
  • 43 Van Oosten,  J. J.,, Wilkins,  D.,, and Besford,  R. T.. (1994);  Regulation of the expression of photosynthetic nuclear genes by CO2 is mimicked by regulation by carbohydrates: a mechanism for the acclimation of photosynthesis to high CO2?.  Plant, Cell and Environment. 17 913-923
  • 44 Van Oosten,  J. J.,, and Besford,  R. T.. (1994);  Sugar feeding mimics the effect of acclimation to high CO2 - rapid down regulation of Rubisco small subunit transcripts but not of the large subunit transcripts.  Journal of Plant Physiology. 143 306-312
  • 45 Vu,  J. C. V.,, Allen,  J. R.,, Boote,  K. J.,, and Bowes,  G.. (1997);  Effects of elevated CO2 and temperature on photosynthesis and Rubisco in rice and soybean.  Plant, Cell and Environment. 20 68-76
  • 46 Wilson,  J. B.. (1988);  A review of evidence on the control of shoot:root ratio, in relation to models.  Annals of Botany. 61 433-449
  • 47 Woodrow,  I. E.. (1994);  Optimal acclimation of C3 photosynthetic system under enhanced CO2.  Photosynthetis Research. 39 401-412

M. M. Chaves

Instituto Superior de Agronomia
Tapada da Ajuda

1399 Lisboa codex
Portugal

Email: mchaves@isa.utl.pt

Section Editor: M Riederer

    >