Abstract
Wild-type tobacco (Nicotiana tabacum L.) plants and transgenic tobacco transformed with antisense rbcS to decrease expression of ribulose-1,5-bisphosphate carboxylase-oxygenase (Rubisco; EC 4.1.1.39) were grown at 300 mol-m−2 · s−1 irradiance and 20° C at either 0.1, 0.7 or 5 mM NH4NO3. In high nitrogen (N), growth was reduced in parallel with the inhibition of photosynthesis when Rubisco was decreased by genetic manipulation. In limiting N, photosynthesis was reduced strongly when Rubisco was decreased by genetic manipulation, but growth was hardly affected. At all N levels, decreased expression of Rubisco led to a decrease in the amount of starch accumulated in the leaves. There was a large increase of the specific leaf area (SLA; leaf area maintained per unit dry weight in the leaf) in plants with decreased Rubisco. Increased SLA was associated with an increased inorganic and a decreased carbon contribution to leaf structural dry weight. The increased SLA represents a more efficient investment of photosynthate with respect to maximisation of leaf area and light interception, and partly compensates for the decreased rate of photosynthesis in plants with decreased expression of Rubisco. The changes of starch content and SLA were particularly large in limiting N, when growth rate was effectively independent of the rate of photosynthesis. Increased N availability led to a large increase of the shoot/ root ratio, but only a small increase in SLA. It is argued that N availability and the availability of photosynthate both regulate storage and allocation of biomass to optimize resource utilization, but achieve this via different mechanisms.
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Abbreviations
- DW:
-
dry weight
- N:
-
nitrogen
- rbcS:
-
nuclear-encoded gene for the small subunit of Rubisco
- RGR:
-
relative growth rate, equivalent to the daily increase in biomass per biomass already present in the plant (g DW·g−1 DW·d−1)
- Rubisco:
-
ribulose-1,5-bisphosphate carboxylase-oxygenase
- SLA:
-
specific leaf area (leaf area maintained per DW of the leaf)
References
Bastow-Wilson, J. (1988) A review of evidence on the control of shoot:root ratio in relation to models. Ann. Bot. 61, 433–439
Björkman, O. (1981) Responses to different quantum flux densities. In: Encyclopedia of plant physiology, N.S., vol. 12A: Physiological plant ecology I. Responses to the physical environment, pp. 57–107, Lange, O.L., Nobel, P.S., Osmond, C.B., Ziegler, H., eds. Springer, Berlin Heidelberg New York
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principal of protein-dye binding. Anal. Biochem. 72, 248–254
Chapin, F.S. III, Schulze, E.-D., Mooney, H.A. (1990) The ecology and economics of storage in plants. Annu. Rev. Ecol. System. 21, 423–447
Cure, J.D., Israel, D.W., Rufty, TW. Jr. (1988) Nitrogen stress effects on growth and seed yield of non-nodulated soybean exposed to elevated carbon dioxide. Crop Sci. 28, 671–677
Dijkstra, P. (1990) Cause and effect of differences in specific leaf area. In: Causes and consequences of variation in growth rate and productivity of higher plants, pp. 125–140, Lambers, H., Cambridge, M.L., Konings, H., Pons, T.L., eds. SPB Academic Publishing, The Hague
Duncan, W.G., Hesketh, J.D. (1968) Net photosynthetic rate, relative leaf growth rates and leaf numbers of 22 races of maize grown at eight temperatures. Crop Sci. 8, 670–674
Fichtner, K., Schulze, E.-D. (1992) The effect of nitrogen nutrition on annuals originating from habitats of different nitrogen availability. Oecologia 92, 236–241
Garbutt, K., Williams, W.E., Bazzaz, F.A. (1990) Analysis of the differential response of five annuals to elevated CO2 during growth. Ecology 71, 1185–1194
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, 136–142
Gifford, R.M., Thorne, J.M., Hitz, W.D., Giaquinta, R.T. (1984) Crop productivity and photosynthate partitioning. Science 225, 801–808
Hirose, T (1986) Nitrogen uptake and plant growth. II. An empirical model of vegetative growth and partitioning. Ann. Bot. 58, 487–496
Hubert, S.C. (1989) Biochemical mechanism for regulation of su-crose accumulation in leaves during photosynthesis. Plant Physiol. 91, 656–662
McDonald, A.J.S. (1990) Phenotypic variation in growth rate as affected by N-supply: its effects on NAR, LWR and SLA. In: Causes and consequences of variation in growth rate and productivity of higher plants, pp. 35–44, Lambers, H., Cambridge, M.L., Konings, H., Pons, T.L., eds. SPB Academic Publishing, The Hague
Nelson, C.J. (1988) Genetic associations between photosynthesis characteristics and yield: review of the evidence. Plant Physiol. Biochem. 26, 543–554
Poorter, H., Remkes, C. (1990) Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83, 553–559
Poorter, H., Remkes, C., Lambers, H. (1990) Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiol. 73, 553–559
Potter, J.R., Jones, J.W. (1977) Leaf area partioning as an important factor in growth. Plant Physiol. 59, 10–14
Quick, W.P., Schurr, U., Scheibe, R., Schulze, E.-D., Rodermel S.R., Bogorad, L., Stitt, M. (1991a) Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS I. Impact on photosynthesis in ambient growth conditions. Planta 183, 542–554
Quick, W.P., Schurr, U., Fichtner, K., Schulze, E.-D., Rodermel, S.R., Bogorad, L., Stitt, M. (1991b) The impact of decreased Rubisco on photosynthesis, growth, allocation and storage in tobacco plants which have been transformed with antisense rbcS. Plant J. 1, 51–58
Quick, W.P., Fichtner, K., Wendler, R., Schulze, E.-D., Rodermel, S.R., Bogorad, L., Stitt, M. (1992) Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS. IV. Impact on photosynthesis in conditions of altered nitrogen supply. Planta 188, 522–531
Radin, J.W., Eidenbock, M.P. (1986) Carbon accumulation during photosynthesis in leaves of nitrogen- and phosphorus-stressed cotton. Plant Physiol. 82, 869–871
Rodermel, S.R., Abbott, M.S., Bogorad, L. (1988) Nuclearorganelle interactions: nuclear antisense gene inhibits ribulose bisphosphate carboxylase enzyme levels in transformed tobacco plants. Cell 55, 673–681
Rufty, T.W. Jr., Raper, D.C. Jr., Huber, S.C., (1984) Alterations in internal partitioning of carbon in soybean plants in response to nitrogen stress. Can. J. Bot. 62, 501–508
Rufty, T.W. Jr., MacKown, C.T., Huber, S.C. (1989) Effects of altered carbohydrate availability on whole-plant assimilation of 15NO −3 . Plant Physiol. 89, 457–463
Sage, R.F., Pearcy, R.W. (1987) The nitrogen use efficiency of C3 and C4 plants. I. Leaf nitrogen, growth and biomass partitioning in Chenopodium album (L.) and Amaranthus retroflexus (L.). Plant Physiol. 84, 954–958
Schramel, P., Wolf, A., Seif, R., Klose, B.-J. (1980) Eine neue Apparatur zur Druckveraschung von biologischem Material. Fresenius Z. Anal. Chem. 302, 62–64
Schulze, E.-D. (1982) Plant life forms as related to plant carbon, water and nutrient relations. In: Encyclopedia of plant physiology, N.S., vol. 12B: Physiological plant ecology II. Water relations and carbon assimilation, pp. 615–676, Lange, O.L., Nobel, P.S., Osmond, C.B., Ziegler, H., eds. Springer, Berlin Heidelberg New York
Schulze, W., Stitt, M., Schulze, E.-D., Neuhaus, H.E., Fichtner, K. (1991) A quantification of the significance of assimilatory starch for growth of Arabidopsis thaliana L. Heynh. Plant Physiol. 95, 890–895
Stitt, M., Quick, W.P., Schurr, U., Schulze, E.-D., Rodermel, S.R., Bogorad, L. (1991a) Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS II. Flux-control coefficients for photosynthesis in varying light, CO2, and air humidity. Planta 183, 555–566
Tolley-Hendry, L., Radin C.D. (1986) Expansion and photosynthetic rates of soybean leaves during onset of an recovery from nitrogen stress. Bot. Gaz. 147, 400–406
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This work was supported by the Deutsche Forschungsgemeinschaft (SFB 137). We thank Dr. G. Gebauer for the assistance with the nitrate determination and Dr. P. Schramel for the analysis of the macronutrients.
Note: Quick et al. (1991b) is paper III in this series on “Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco”.
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Fichtner, K., Quick, W.P., Schulze, ED. et al. Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS. Planta 190, 1–9 (1993). https://doi.org/10.1007/BF00195668
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DOI: https://doi.org/10.1007/BF00195668