Skip to main content
SpringerLink
Log in

Control of photosynthesis by the carbohydrate level in leaves of the C4 plant Amaranthus edulis L.

  • Published:
Planta Aims and scope Submit manuscript

Abstract

Photosynthesis was studied in relation to the carbohydrate status in intact leaves of the C4 plant Amaranthus edulis. The rate of leaf net CO2 assimilation, stomatal conductance and intercellular partial pressure of CO2 remained constant or showed little decline towards the end of an 8-h period of illumination in ambient air (340 μbar CO2, 21% O2). When sucrose export from the leaf was inhibited by applying a 4-h cold-block treatment (1°C) to the petiole, the rate of photosynthesis rapidly decreased with time. After the removal of the cold block from the petiole, further reduction in photosynthetic rate occurred, and there was no recovery in the subsequent light period. Although stomatal conductance declined with time, intercellular CO2 partial pressure remained relatively constant, indicating that the inhibition of photosynthesis was not primarily caused by changes in stomatal aperture. Analysis of the leaf carbohydrate status showed a five- to sixfold increase in the soluble sugar fraction (mainly sucrose) in comparison with the untreated controls, whereas the starch content was the same. Leaf osmotic potential increased significantly with the accumulation of soluble sugars upon petiole chilling, and leaf water potential became slightly more negative. After 14 h recovery in the dark, photosynthesis returned to its initial maximum value within 1 h of illumination, and this was associated with a decline in leaf carbohydrate levels overnight. These data show that, in Amaranthus edulis, depression in photosynthesis when translocation is impaired is closely related to the accumulation of soluble sugars (sucrose) in source leaves, indicating feedback control of C4 photosynthesis. Possible mechanisms by which sucrose accumulation in the leaf may affect the rate of photosynthesis are discussed with regard to the leaf anatomy of C4 plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

A:

net CO2 assimilation rate

Ci:

intercellular CO2 partial pressure

PEP:

phosphoenolpyruvate

RuBP:

ribulose-1,5-bisphosphate

Ψ:

water potential

π:

osmotic pressure

References

  • Arnon, D.I. (1949) Copper enzymes in isolated chloroplasts. Plant Physiol. 24, 1–15

    Google Scholar 

  • Azcón-Bieto, J. (1983) Inhibition of photosynthesis by carbohydrates in wheat leaves. Plant Physiol. 73, 681–686

    Google Scholar 

  • Azcón-Bieto, J., Osmond, C.B. (1983) Relationship between photosynthesis and respiration: The effect of carbohydrate status on the rate of CO2 production by respiration in darkened and illuminated wheat leaves. Plant Physiol. 71, 574–581

    Google Scholar 

  • Blechschmidt, S. (1981) Stofftransport in experimentell erzeugte Blatt-Sinks an den dicotylen C4-Pflanzen Amaranthus caudatus L. und Gomphrena globosa L. Diss. Univ. Göttingen

  • Chen-She, Shen-Hwa, Lewis, D.H., Walker, D.A. (1975) Stimulation of photosynthetic starch formation by sequestration of cytoplasmic orthophosphate. New Phytol. 74, 383–392

    Google Scholar 

  • Claussen, W., Biller, E. (1977) Die Bedeutung der Saccharoseund Stärkegehalte der Blätter für die Regulierung der Netto-Photosyntheseraten. Z. Pflanzenphysiol. 81, 189–198

    Google Scholar 

  • Claussen, W., Hawker, J.S., Loveys, B.R. (1985) Sucrose synthase activity, invertase activity, net photosynthetic rates and carbohydrate content of detached leaves of eggplants as affected by attached stems and shoots (sinks). J. Plant Physiol. 119, 123–131

    Google Scholar 

  • Curtis, O.F. (1929) Studies on solute translocation in plants. Experiments indicating that translocation is dependent on the activity of living cells. Am. J. Bot. 16, 154–168

    Google Scholar 

  • Downton W.J.S., Hawker, J.S. (1973) Enzymes of starch and sucrose metabolism in Zea mays leaves. Phytochemistry 12, 1551–1556

    Google Scholar 

  • Edwards, G.E., Walker, D.A. (1983) C3, C4: Mechanisms, and cellular and environmental regulation of photosynthesis. Blackwell, London

    Google Scholar 

  • Evert, R.F., Eschrich, W., Heyser, W. (1978) Leaf structure in relation to solute transport and phloem loading in Zea mays L. Planta 138, 279–294

    Google Scholar 

  • Ferrar, P.J., Osmond, C.B. (1986) Nitrogen supply as a factor influencing photoinhibition and photosynthetic acclimation after transfer of shade-grown Solanum dulcamara to bright light. Planta 168, 563–570

    Google Scholar 

  • Fisher, D.G., Evert, R.F. (1982a) Studies on the leaf of Amaranthus retroflexus (Amaranthaceae): Quantitative aspects, and solute concentration in the phloem. Am. J. Bot. 69, 1375–1388

    Google Scholar 

  • Fisher, D.G., Evert, R.F. (1982b) Studies on the leaf of Amaranthus retroflexus (Amaranthaceae): ultrastructure, plasmodesmatal frequency, and solute concentration in relation to phloem loading. Planta 155, 377–387

    Google Scholar 

  • Fondy, B.R., Geiger, D.R. (1982) Diurnal pattern of translocation and carbohydrate metabolism in source leaves of Beta vulgaris L. Plant Physiol. 70, 671–676

    Google Scholar 

  • Foyer, C.H. (1987) The basis for source-sink interaction in leaves. Plant Physiol. Biochem. 25, 649–657

    Google Scholar 

  • Foyer, C.H. (1988) Feedback inhibition of photosynthesis through source-sink regulation in leaves. Plant Physiol. Biochem. 26, 483–492

    Google Scholar 

  • Furbank, R.T., Foyer, C.H., Walker, D.R. (1987) Regulation of photosynthesis in isolated chloroplasts during orthophosphate limitation. Biochem. Biophys. Acta 894, 552–561

    Google Scholar 

  • Furbank, R.T., Stitt, M., Foyer, C. (1985) The localization of sucrose synthesis in maize leaves. Planta 164, 172–178

    Google Scholar 

  • Geiger, D.R. (1976) Effects of translocation and assimilate demand on photosynthesis. Can. J. Bot. 54, 2337–2345

    Google Scholar 

  • Geiger, D.R., Ploeger, B.J., Fox, T.C., Fondy, B.R. (1983) Sources of sucrose translocated from illuminated sugar beet source leaves. Plant Physiol. 72, 964–970

    Google Scholar 

  • Gordon, A.J., Ryle, G.J.A., Webb, G. (1980) The relationship between sucrose and starch during ‘dark’ export from leaves of uniculm barley. J. Exp. Bot. 31, 843–850

    Google Scholar 

  • Hatch, A.L., Jensen, R.G. (1980) Regulation of ribulose-1,5-bisphosphate carboxylase from tobacco: Changes in pH response and affinity for CO2 and Mg2+ induced by chloroplast intermediates. Arch. Biochem. Biophys. 205, 587–591

    Google Scholar 

  • Hatch, M.D., Osmond, B.C. (1976) Compartmentation and transport in C4 photosynthesis. In: Encyclopedia of plant physiology, N.S., vol. 3: Transport in plants III, pp. 144–184, Stocking, C.R., Heber, U., eds. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Hawker, J.S. (1967) Inhibition of sucrose phosphatase by sucrose. Biochem. J. 102, 401–406

    Google Scholar 

  • Heldt, H.W., Rapley, L. (1970) Specific transport of inorganic phosphate, 3-phosphoglycerate and dihydroxyacetone phosphate, and of dicarboxylates across the inner membrane of spinach chloroplasts. FEBS Lett. 10, 143–148

    Google Scholar 

  • Herold, A. (1980) Regulation of photosynthesis by sink activity — the missing link. New Phytol. 86, 131–144

    Google Scholar 

  • Herold, A., Lewis, D.H., Walker, D.A. (1976) Sequestration of cytoplasmic orthophosphate by mannose and its differential effect on photosynthetic starch synthesis in C3 and C4 species. New Phytol. 76, 397–407

    Google Scholar 

  • King, R.W., Wardlaw, J.F., Evans, L.T. (1967) Effect of assimilate utilization on photosynthetic rate in wheat. Planta 77, 261–276

    Google Scholar 

  • Leegood, R.C. (1985) The intercellulat compartmentation of metabolites in leaves of Zea mays L. Planta 164, 163–171

    Google Scholar 

  • Leegood, R.C., Osmond, C.B. (1988) Metabolite fluxis in C4-and CAM plants. In: Advanced plant physiology and molecular biology, Dennis, D.T., Turpin, D.J. Longmans Technical Publications, London (in press)

    Google Scholar 

  • Neales, T.F., Incoll, L.D. (1968) The control of leaf photosynthesis rate by the level of assimilate concentration in the leaf. A review of the hypothesis. Bot. Rev. 34, 107–125

    Google Scholar 

  • Ntsika, G., Delrot, S. (1986) Alterations of apoplastic/intracellular ratios of sugars in the leaf blade resulting from thermic treatments applied on the petiole. In: Plant biology, vol. 1: Phloem transport, pp. 433–434, Cronshaw, J., Lucas, W.J., Giaquinta, R.T., eds. Alan R. Liss, New York

    Google Scholar 

  • Robinson, S.P., Walker, D.A. (1981) Photosynthetic carbon reduction cycle. In: The biochemistry of plants. A comprehensive treatise, vol. 8: Photosynthesis, pp. 193–236, Hatch, M.D., Boardman, N.K., eds. Academic Press, New York

    Google Scholar 

  • Sharkey, T.D. (1985) Photosynthesis in intact leaves of C3 plants: Physics, physiology and rate limitations. Bot. Rev. 51, 53–105

    Google Scholar 

  • Sivak, M.N., Walker, D.A. (1986) Photosynthesis in vivo can be limited by phosphate supply. New Phytol. 102, 499–512

    Google Scholar 

  • Sivak, M., Rowell, J. (1988) Phosphate limits photosynthesis in a starchless mutant of Arabidopsis thaliana deficient in chloroplast phosphoglucomutase activity. Plant Physiol. Biochem. 26, 493–501

    Google Scholar 

  • Stitt, M. (1986) Regulation of photosynthetic sucrose synthesis: Integration, adaption, and limits. In: Plant biology, vol. 1: Phloem transport, pp. 331–347, Cronshaw, J., Lucas, W.J., Giaquinta, R.T., eds Alan R. Liss, New York

    Google Scholar 

  • Stitt, M., Huber, S.C., Kerr, P. (1987) Control of photosynthetic sucrose formation. In: Biochemistry of plants, vol. 10, pp. 327–409, Hatch, M.D., Boardman, N.K., eds. Academic Press, London

    Google Scholar 

  • Terashima, I., Wong, S.C., Osmond, C.B., Farquhar, G.D. (1988) Characterisation of non-uniform photosynthesis induced by abscisic acid in leaves having different mesophyll anatomies. Plant Cell Physiol. 29, 385–394

    Google Scholar 

  • von Caemmerer, S., Farquhar, G.D. (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387

    Google Scholar 

  • Walker, D.A. (1976) CO2 fixation by intact chloroplasts: photosynthetic induction and its relation to transport phenomena and control mechanisms. In: The intact chloroplast, pp. 255–278, Barber, J., ed. Elsevier, Amsterdam

    Google Scholar 

Download references

Author information

Author notes

  1. C. B. Osmond

    Present address: Department of Botany, Duke University, 27706, Durham, NC, USA

Authors and Affiliations

  1. Forstbotanisches Institut der Universität, Büsgenweg 2, D-3400, Göttingen, Federal Republic of Germany

    S. Blechschmidt-Schneider

  2. Department of Environmental Biology, Research School of Biological Sciences, Australian National University, P.O. Box 475, 2601, Canberra City, A.C.T., Australia

    P. Ferrar & C. B. Osmond

Authors
  1. S. Blechschmidt-Schneider
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Ferrar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. B. Osmond
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blechschmidt-Schneider, S., Ferrar, P. & Osmond, C.B. Control of photosynthesis by the carbohydrate level in leaves of the C4 plant Amaranthus edulis L.. Planta 177, 515–525 (1989). https://doi.org/10.1007/BF00392620

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00392620

Key words

Search

Navigation