Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

The impact of decreased activity of starch-branching enzyme on photosynthetic starch synthesis in leaves of wrinkled-seeded peas

Abstract

The effect of a reduction of the activity of starch-branching enzyme (1,4-α-D-glucan, 1,4-α-D-glucan-6-glycosyl transferase; EC 2.4.1.18) on photosynthetic starch synthesis and photosynthate partitioning has been studied in leaves of pea (Pisum sativum L.). Leaves of wrinkled-seeded peas, recessive at the rugosus locus (rr), contained lower activity of branching enzyme than leaves of near-isogenic round-seeded peas, dominant at the rugosus locus (RR). Western blots showed that one isoform of the enzyme is absent from rr leaves, corresponding to the isoform that is absent from rr embryos. RR and rr leaves had identical rates of starch synthesis and photosynthesis at low irradiances. At high irradiances the rate of starch synthesis was decreased by up to 40% in rr relative to RR leaves. There was no corresponding increase of sucrose synthesis in rr leaves; instead, the rate of photosynthesis was decreased. This inhibition of photosynthesis was more marked at low than at high temperatures and was accompanied by increased oscillatory behaviour, rr leaves contained higher levels of ADP glucose and glycerate 3-phosphate than RR leaves in low and high light. The contribution of these results to our understanding of the distribution of control in the pathways of starch and sucrose synthesis is discussed.

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

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abbreviations

ADPGlc:

adeninediphosphoglucose

Chl:

chlorophyll

Fru1,6bisP:

fructose-1,6-bisphosphate

Fru2,6bisP:

fructose-2,6-bisphosphate

kDa:

kilodalton

PAR:

photosynthetically active radiation

Q A :

the primary acceptor for photosystem II

References

  1. Bhattacharyya, M.K., Smith, A.M., Ellis, T.H.N., Hedley, C., Martin, C. (1990) The wrinkled-seeded character of peas described by Mendel is caused by a transposon-like insertion in a gene encoding starch branching enzyme. Cell 60, 115–122

  2. Coxon, D.T., Davies, D.R. (1982) The effect of the ra and rb loci on the lipid content of the seed of Pisum sativum L. Theor. Appl. Genet. 64, 47–50

  3. Edwards, G., Walker, D. (1983) C3, C4. Mechanisms, and cellular and environmental regulation of photosynthesis. University of California Press, Berkeley, USA

  4. Edwards, J., Green, J.H., ap Rees, T. (1988). Activity of starch branching enzyme as a cardinal feature of the Ra locus in Pisum sativum. Phytochemistry 27, 1615–1620

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

  6. Greenwood, C.T., Thomson, J. (1962) Studies on the biosynthesis of starch granules. 2. The properties of the components of starches from smoothand wrinkled-seeded peas during growth. Biochem. J. 82, 156–164

  7. Hampp, R., Goller, M., Ziegler, H. (1982) Adenylate levels, energy charge and phosphorylation potential during dark-light and light-dark transitions in chloroplasts, mitochondria and cytosol of mesophyll protoplasts from Avena sativa L. Plant Physiol. 69, 448–455

  8. Hedley, C.L., Smith, C.M., Ambrose, M.H., Cook, S., Wang, T.L. (1986) An analysis of seed development in Pisum sativum. II The effect of the r-locus on the growth and development of the seed. Ann. Bot. 58, 371–379

  9. Heldt, H.W., Chor, C.J., Maronde, D., Herold, A., Stankovic, Z.S., Walker, D.A., Kraminer, A., Kirk, M.A., Heber, U. (1977) Role of orthophosphate and other factors in the regulation of starch formation in leaves and isolated chloroplasts. Plant Physiol. 59, 1146–1155

  10. Kooistra, E. (1962) On the differences between smooth and three types of wrinkled peas. Euphytica 11, 357–373

  11. Kruckeberg, A.L., Neuhaus, E., Feil, R., Gottlieb, L.D., Stitt, M. (1989). Decreased-activity mutants of phosphoglucose isomerase in the cytosol and chloroplast of Clarkia xantiana. Impact on mass-action ratios and fluxes to sucrose and starch and estimation of flux control coefficients and elasticity coefficients. Biochem. J. 261, 457–467

  12. Kruger, N.J., ap Rees, T. (1983) Properties of a α-glucan phosphorylase from pea chloroplasts. Phytochemistry 22, 1891–1898

  13. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685

  14. Mendel, G. (1865) Versuche über Pflanzenhybriden. Verh. Naturforsch. Ver. Brünn. 4, 3–37

  15. Neuhaus, H.E. Kruckeberg, A.L., Feu, R., Stitt, M. (1989) Reduced-activity mutants of phosphoglucose isomerase in the cytosol and chloroplast of Clarkia xantiana. II. Study of the mechanisms which regulate photosynthate partitioning. Planta 178, 110–122

  16. Preiss, J., Levi, C. (1979) Metabolism of starch in leaves. In: Encyclopedia of plant physiology, N.S., vol.6: Photosynthesis II, pp. 282–312, Gibbs, M., Latzko, E., eds. Springer, Berlin Heidelberg New York

  17. Schreiber, U., Schlima, U., Bilger, W. (1986) Continuous recording of photochemical and non-photochemical quenching with a new type of modulation fluorimeter. Photosynth. Res. 10, 51–62

  18. Sharkey, T.D., Vanderveer, PJ. (1990) Stromal phosphate concentration is low during feedback limited photosynthesis. Plant Physiol. (in press)

  19. Sivak, M.N., Walker, D.A. (1987) Oscillations and other symptoms of limitation of in vivo photosynthesis by inadequate phosphate supply to the chloroplast. Plant Physiol. Biochem. 25, 635–648

  20. Smith, A.M. (1988) Major differences in isoforms of starch-branching enzyme between developing embryos of roundand wrinkled-seeded peas. Planta 175, 270–279

  21. Stitt, M., Grosse, H. (1988a) Interactions between sucrose synthesis and photosynthesis. I. Slow transients during a biphasic induction are related to a delayed activation of sucrose synthesis. J. Plant Physiol. 133, 129–137

  22. Stitt, M., Grosse, H. (1988b) Interaction between sucrose synthesis and photosynthesis. IV. Temperature-dependent adjustment of the relation between sucrose synthesis and CO2 fixation. J. Plant Physiol. 133, 392–400

  23. Stitt, M., Schreiber, U. (1988) Interactions between sucrose synthesis and photosynthesis. III. Response of biphasic induction kinetics and oscillations to manipulation of the relation between electron transport, the Calvin cycle, and sucrose synthesis. J. Plant Physiol. 133, 263–271

  24. Stitt, M., Wirtz, W., Heldt, H.W. (1980) Metabolite levels in the chloroplast and extrachloroplast compartments of spinach protoplasts. Biochim. Biophys. Acta 593, 85–102

  25. Stitt, M., Huber, S.C., Kerr, P. (1987) Control of photosynthetic sucrose synthesis. In: The biochemistry of plants, vol. 10, pp. 327–409, Hatch, M.D., Boardman, N.K., eds. Academic Press, New York

  26. Walker, D.A., Osmond, C.B. (1986) Measurement of photosynthesis in vivo with a leaf disc electrode: correlations between lightdependence of steady state photosynthetic O2 evolution and chlorophyll a fluorescence transients. Proc. R. Soc. London Ser. B 227, 281–302

Download references

Author information

Additional information

This research was supported by the Deutsche Forschungsgemeinschaft. A visit of A.S. to Bayreuth was supported by the Organisation for Economic Cooperation and Development. We are grateful to Dr. Cliff Hedley (John Innés Institute) for the seeds of nearisogenic lines of peas, to Regina Feil (Bayreuth) for carrying out metabolite measurements, to L. Badewitz (Bayreuth) for the artwork, and to Tarn Dalzell (John Innes Institute) for typing the manuscript.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Smith, A.M., Neuhaus, H.E. & Stitt, M. The impact of decreased activity of starch-branching enzyme on photosynthetic starch synthesis in leaves of wrinkled-seeded peas. Planta 181, 310–315 (1990). https://doi.org/10.1007/BF00195881

Download citation

Key words

  • Mutant (Pisum)
  • Photosynthate partitioning
  • Photosynthesis (metabolic control)
  • Pisum (starchsynthesis)
  • Starch-branching enzyme