Skip to main content
Log in

Intercellular compartmentation of basic carbon pathways in motor organs (pulvini) of leaves of Phaseolus coccineus L.

  • Published:
Planta Aims and scope Submit manuscript

Abstract

The activities of enzymes which catalyze one step in each of the five major carbon pathways in green plants were measured in secondary pulvini and other tissues of Phaseolus coccineus L. leaves. We were able to detect activities of fumarase (EC 4.2.1.2; tricarboxylic-acid pathway), NAD-glyceraldehyde-phosphate dehydrogenase (NAD-GAPDH, EC 1.2.1.12; glycolysis), 6-phosphogluconate dehydrogenase (6-PGDH, EC 1.1.1.44; oxidative pentose-phosphate pathway), ribulose-1, 5-bisphosphate carboxylase (Rubisco, EC 4.1.1.39; photosynthetic carbon-reduction pathway), and of hydroxypyruvate reductase (HP-R, EC 1.1.1.81; photosynthetic carbon-oxidation pathway). On a protein basis the activities of Rubisco and HP-R in pulvinar regions were very low (below 1 and 2 mol · (kg protein) −-1 · h−-1, respectively), but the activities of fumarase and NAD-GAPDH were between 10- and 5-fold higher compared with the laminar tissue (up to 7 and 50 mol · (kg protein)−-1 · h−-1, respectively). Similarly, the protein specific activities of 6-PGDH were increased in the pulvinus (3–4 compared with approx. 1 mol · (kg protein)−-1 · h−-1 in the leaf blade). No differences in specific activities were detected between day and night positions of the leaves. By applying quantitative histochemical techniques we determined the longitudinal and transversal compartmentation of the activities of fumarase, NAD-GAPDH, and 6-PGDH in pulvinar tissues. Levels of activity of all three enzymes increased towards the middle part of the pulvinus. Here, expressed on a dry-weight (DW) basis, the analysis of cross sections showed highest activities in the outer parts of the extensor in the order given, approx. 0.6, 5, and 0.25 mol · (kg DW)−-1 · h−-1 for fumarase, NAD-GAPDH and 6-PGDH. When related to protein, levels of activity were comparably high within the inner parts of extensor and flexor, and partly also in the abaxial part of the bundle (fumarase, 6-PGDH). The tissue-specific compartmentation of the respective activities is discussed in relation to leaf movement and shows parallels with guard-cell function.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

Chl:

chlorophyll

DW:

dry weight

GAPDH:

glyceraldehyde-phosphate dehydrogenase

HP-R:

hydroxypyruvate reductase

Rubisco:

ribulose-1,5-bisphosphate carboxylase

6-PGDH:

6-phosphogluconate dehydrogenase

References

  • Bialczyk, J., Lechowski, Z. (1986) Diurnal changes in the malic acid concentration in Phaseolus coccineus L. pulvini. Plant Cell Physiol. 27, 981–987

    Google Scholar 

  • Bialczyk, J., Lechowski, Z. (1989) Malic acid synthesis in relation to K−+ and Cl−- availability in Phaseolus coccineus L. pulvini. Biochem. Physiol. Pflanzen 184, 79–86

    Google Scholar 

  • Darwin, C. (1881) The power of movements in plants. D. Appleton and Co., New York, Reprinted New York: (1966) De Capo Press

    Google Scholar 

  • Einig, W., Hampp, R. (1990) Carbon partitioning in Norway spruce: amounts of fructose 2,6-bisphosphate and of intermediates of starch/sucrose synthesis in relation to needle age and degree of needle loss. Trees 4, 9–15

    Google Scholar 

  • Erath, F., Ruge, W.A., Mayer, W.-A., Hampp, R. (1988) Isolation of functional extensor and flexor protoplasts from Phaseolus coccineus L. pulvini: potassium induced swelling. Planta 173, 447–452

    Google Scholar 

  • Freudling, C., Starrach, N., Flach, D., Gradmann, D., Mayer, W.-E. (1988) Cell walls as reservoirs of potassium ions for reversible volume changes of pulvinar motor cells during rhythmic leaf movements. Planta 175, 193–203

    Google Scholar 

  • Gorton, H.L. (1990) Stomates and pulvini: a comparison of two rhythmic, turgor-mediated movement systems. In: The pulvinus: Motor organ for leaf movement, pp. 223–237, Satter, R.L., Gorton, H.L., Vogelmann, Th.C., eds. Am. Soc. Plant Physiol., Rockville

    Google Scholar 

  • Guttenberger, M. (1989) Untersuchungen zur Biochemie der Pilz-Baumwurzel-Symbiose. Proteinanalytik im Mikromaßstab. Dissertation, University of Tübingen, Tübingen, FRG

    Google Scholar 

  • Guttenberger, M., Neuhoff, V., Hampp, R. (1991) A dot-blot assay for quantitation of nanogram amounts of protein in the presence of carrier ampholytes and other possibly interfering substances. Anal. Biochem. 196, in press

  • Hampp, R., Outlaw, W.H. jr., Tarczynski, M.C. (1982) Profile of basic carbon pathways in guard cells and other leaf cells of Vicia faba L. Plant Physiol. 70, 1582–1585

    Google Scholar 

  • Hampp, R., Schnabl, H. (1984) Adenine and pyridine nucleotide status of isolated Vicia guard cell protoplasts during K−+-induced swelling. Plant Cell Physiol. 25, 1233–1239

    Google Scholar 

  • Hampp, R., Rieger, A., Outlaw, W.H. jr. (1990) Microdissection and biochemical analysis of plant tissues. In: Physical methods in plant sciences, pp. 124–147, Linskens, H.F., Jackson, J.F., eds. Springer-Verlag, Berlin Heidelberg New York Tokyo

    Google Scholar 

  • Hosokawa, Y., Kiyosawa, K. (1983) Diurnal K−+ and anion transport in Phaseolus pulvinus. Plant Cell Physiol. 24, 1065–1072

    Google Scholar 

  • Iglesias, A., Satter, R.L. (1983) H−+ fluxes in excised Samanea motor tissue. I. Promotion by light. Plant Physiol. 72, 564–569

    Google Scholar 

  • Inskeep, W.P., Bloom, P.R. (1985) Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80% acetone. Plant Physiol. 77, 483–485

    Google Scholar 

  • Kiyosawa, K. (1979) Unequal distribution of potassium and anions within the Phaseolus pulvinus during circadian leaf movement. Plant Cell Physiol. 20, 1621–1634

    Google Scholar 

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

    PubMed  Google Scholar 

  • Lee, Y., Satter, R.L. (1988) Effects of temperature on H−+ uptake and release during circadian rhythmic movements of excised Samanea motor organs. Plant Physiol. 86, 352–354

    Google Scholar 

  • Lowry, O.H., Passonneau, J.V. (1972) A flexible system of enzymatic analysis. Academic Press, New York San Francisco London

    Google Scholar 

  • Mayer, W.-E. (1977) Kalium-und Chloridverteilung im Laminargelenk von Phaseolus coccineus L. während der circadianen Blattbewegung im tagesperiodischen Licht-Dunkelwechsel. Z. Pflanzenphysiol. 83, 127–135

    Google Scholar 

  • Mayer, W.-E. (1981) Energy-dependent phases of the circadian clock and the clock-controlled leaf movement in Phaseolus coccineus L. Planta 152, 292–301

    Google Scholar 

  • Mayer, W.-E., Ruge, W.A., Starrach, N., Hampp, R. (1987) Chloride availability affects the malate content and its control by the circadian clock in pulvini of Phaseolus coccineus L. Z. Naturforsch. 42c, 553–558

    Google Scholar 

  • Neuhoff, V., Philipp, K., Zimmer, H.-G., Mesecke, S. (1979) A simple, versatile, sensitive and volume-independent method for quantitative protein determination which is independent of other external influences. Hoppe-Seyler's Z. Physiol. Chem. 360, 1657–1670

    Google Scholar 

  • Outlaw, W.H. jr. (1989) Critical examination of the quantitative evidence for and against photosynthetic CO2 fixation by guard cells. Physiol. Plant. 77, 275–281

    Google Scholar 

  • Outlaw, W.H. jr., Tarczynski, M.C. (1984) Guard cell starch biosynthesis regulated by effectors of ADP-glucose pyrophosphorylase. Plant Physiol. 74, 424–429

    Google Scholar 

  • Outlaw, W.H. jr., Tarczynski, M.C., Anderson, L.C. (1982) Taxonomic survey for the presence of ribulose-1,5-bisphosphate carboxylase activity in guard cells. Plant Physiol. 70, 1218–1220

    Google Scholar 

  • Outlaw, W.H. jr., Manchester, J., DiCamelli, C.A., Randall, D.D., Rapp, B., Veith, G.M. (1979) Photosynthetic carbon reduction pathway is absent in chloroplasts of Vicia faba guard cells. Proc. Natl. Acad. Sci. USA 76, 6371–6375

    Google Scholar 

  • Rieger, A., Ruge, W.A., Hampp, R. (1987) Malate gradients in secondary pulvini of Phaseolus coccineus L. (Abstr.) Plant Physiol. 83, Suppl., 158

    Google Scholar 

  • Rieger, A. (1990) Verteilung von Metaboliten und Enzymaktivitäten im Laminargelenk und anderen Blattgeweben von Phaseolus coccineus L., bestimmt unter Anwendung der quantitativen Histochemie. Dissertation, University of Tübingen, Tübingen, FRG

    Google Scholar 

  • Saeedi, S., Roblin, G. (1986) Effects of respiration inhibitors and uncouplers on dark-and light-induced leaflet movements of Cassia fasciculata. Plant Physiol. 82, 270–273

    Google Scholar 

  • Satter, R.L. (1979) Leaf movements and tendril curling. In: Encyclopedia of plant physiology, vol. 7, pp. 442–484, Springer, Berlin Heidelberg New York Tokyo

    Google Scholar 

  • Satter, R.L., Galston, A.W. (1981) Mechanism of control of leaf movements. Annu. Rev. Plant Physiol. 32, 83–110

    Google Scholar 

  • Satter, R.L., Geballe, P.B., Applewhite, P.B., Galston, A.W. (1974) Potassium flux and leaf movement in Samanea saman. I. Rhythmic movement. J. Gen. Physiol. 64, 413–430

    Google Scholar 

  • Satter, R.L., Gorton, H.L., Vogelmann, Th.C. (1990) The pulvinus: Motor organ for leaf movement, pp 1–264, Am. Soc. Plant Physiol., Rockville

    Google Scholar 

  • Schnabl, H. (1980) CO2 and malate metabolism in starch-containing and starch-lacking guard-cell protoplasts. Planta 149, 52–58

    Google Scholar 

  • Seitz, H.U., Seitz, U., Alfermann, W. (1985) Pflanzliche Gewebekultur-Ein Praktikum. Fischer, Stuttgart New York

    Google Scholar 

  • Stitt, M. (1984) Fumarase. In: Methods of enzymatic analysis (3rd edn.), vol. IV, pp. 359–362, Bergmeyer, H.U., ed. Verlag Chemie, Weinheim Deerfield Beach Basel

    Google Scholar 

  • Vanhinsberg, N., Horton, R.F. (1990) Carbon dioxide assimilation in pulvini of Phaseolus vulgaris. Biochem. Physiol. Pflanzen 186, 37–42

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This investigation was supported by a grant from the Deutsche Forschungsgemeinschaft.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rieger, A., Hampp, R. Intercellular compartmentation of basic carbon pathways in motor organs (pulvini) of leaves of Phaseolus coccineus L.. Planta 184, 415–421 (1991). https://doi.org/10.1007/BF00195345

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00195345

Key words

Navigation