Abstract
Sap extracted from attached leaves of two-to three-week-old maize plants witt the aid of a roller device was almost devoid of bundle-sheath contamination as judged by the distribution of mesophyll and bundle-sheath markers. The extraction could be done very rapidly (less than 1 s) and the extract immediately quenched in HClO4 or reserved for enzyme assay. Comparison of the contents of metabolites in intact leaves and in the leaf extract allowed estimation of the distribution of metabolites between the bundle-sheath and the mesophyll compartments. Substantial amounts of metabolites such as malate and amino acids were present in the non-photosynthetic cells of the midrib. In the illuminated leaf, triose phosphate was predominantly located outside the bundle-sheath while the major part of the 3-phosphoglycerate was in the bundle sheath. The results indicate the existence of concentration gradients of triose phosphate and 3-phosphoglycerate in the leaf which are capable of maintaining carbon flow between the mesophyll and bundle-sheath cells during photosynthesis. There was no evidence for the existence of a gradient of pyruvate between the bundle-sheath and the mesophyll cells.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allaway, W.G., Hsiao, T.C. (1973) Preparation of rolled epidermis of Vicia faba L. so that stomata are the only viable cells: Analysis of guard cell potassium by flame photometry. Aust. J. Biol. Sci. 26, 309–318
Arnon, D.I. (1949) Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol. 24, 1–15
Berry, J.A., Downton, W.J.S., Tregunna, E.B. (1970) The photosynthetic carbon metabolism of Zea mays and Gomphrena globosa: the location of the CO2 fixation and the carboxyl transfer reactions. Can. J. Bot. 48, 777–786
Björkman, O., Gauhl, E. (1969) Carboxydismutase activity in plants with and without β-carboxylation photosynthesis. Planta 88, 197–203
Chapman, K.S.R., Hatch, M.D. (1981) Aspartate decarboxylation in bundle sheath cells of Zea mays and its possible contribution to C4 photosynthesis. Aust. J. Plant Physiol. 8, 237–248
Day, D.A., Jenkins, C.L.D., Hatch, M.D. (1981) Isolation and properties of functional mesophyll protoplasts and chloroplasts from Zea mays. Aust. J. Plant Physiol. 8, 21–29
Dietz, K.-J., Heber, U. (1984) Rate-limiting factors in leaf photosynthesis. I. Carbon fluxes in the Calvin cycle. Biochim. Biophys. Acta 767, 432–443
Downton, W.J.S., Hawker, J.S. (1973) Enzymes of starch and sucrose metabolism in Zea mays leaves. Phytochemistry 12, 1551–1556
Fliege, R., Flügge, U.-I., Werdan, K., Heldt, H.W. (1978) Specific transport of inorganic phosphate, 3-phosphoglycerate and triosephosphates across the inner membrane of the envelope in spinach chloroplasts. Biochim. Biophys. Acta 502, 232–247
Furbank, R.T., Leegood, R.C. (1984) Carbon metabolism and gas exchange in leaves of Zea mays L. Interaction between the C3 and C4 pathways during photosynthetic induction. Planta 162, 457–462
Furbank, R.T., Stitt, M., Foyer, C.H. (1985) Intercellular compartmentation of sucrose synthesis in leaves of Zea mays L. Planta 164, 172–178
Hatch, M.D. (1971) The C4-pathway of photosynthesis. Evidence for an intermediate pool of carbon dioxide and the identity of the donor C4-dicarboxylic acid. Biochem. J. 125, 425–432
Hatch, M.D. (1979) Mechanism of C4 photosynthesis in Chloris gayana: Pool sizes and kinetics of 14CO2 incorporation into 4-carbon and 3-carbon intermediates. Arch. Biochem. Biophys. 194, 117–127
Hatch, M.D., Kagawa, T. (1973) Enzymes and functional capacities of mesophyll chloroplasts from plants with C4-pathway photosynthesis. Arch. Biochem. Biophys. 159, 842–853
Hatch, M.D., Osmond, C.B. (1976) Compartmentation and transport in C4 photosynthesis. In: Encyclopedia of plant physiology, N.S., vol. 3: Intracellular interactions and transport processes, pp. 144–184, Stocking, C.R., Heber, H. eds. Springer, Berlin Heidelberg New York
Hatch, M.D., Mau, S. (1977) Association of NADP-and NAD-linked malic enzyme activities in Zea mays: relation to C4 pathway of photosynthesis. Arch. Biochem. Biophys. 179, 361–369
Hatch, M.D., Oliver, I.R. (1978) Activation and inactivation of phosphoenolpyruvate carboxylase in leaf extracts from C4 species. Aust. J. Plant Physiol. 5, 571–580
Hattersley, P.W., Watson, L. (1975) Anatomical parameters for predicting photosynthetic pathways of grass leaves: The ‘maximum lateral cell count’ and the ‘maximum cells distant count’. Phytomorphology 25, 325–333
Huber, S.C., Edwards, G.E. (1977) Transport in C4 mesophyll chloroplasts. Characterization of the pyruvate carrier. Biochim. Biophys. Acta 462, 583–602
Kanai, R., Edwards, G.E. (1973) Separation of mesophyll protoplasts and bundle sheath cells of maize leaves for photosynthetic studies. Plant Physiol. 51, 1133–1137
Karpilov, Y.S., Bill, K.Y., Gukasian, I.A. (1975a) [In Russ.] Participation of ATPase in transport of intermediate products of photosynthesis between assimilatory tissues of C4-plants. Fiziol. Rast. 22, 1113–1120
Karpilov, Y.S., Bill, K.Y., Malyshev, O.G. (1975b) [In Russ.] Effect of the ratio between malate and aspartate and the arrangement of chloroplasts in C4-plants on the rate of 14C-incorporation into the pentose phosphate cycle from dicarboxylic acids. Fiziol. Rast. 22, 910–917
Leegood, R.C., Furbank, R.T. (1984) Carbon metabolism and gas exchange in leaves of Zea mays L. Changes in photosynthetic induction CO2 fixation, chlorophyll a fluorescence and metabolite levels during photosynthetic induction. Planta 162, 450–456
Leegood, R.C., Walker, D.A. (1982) Regulation of fructose-1,6-bisphophatase activity in leaves. Planta 156, 449–456
Newsholme, E.A., Start, C. (1973) Regulation, in metabolism. pp. 139, 263. John Wiley & Sons, London
Osmond, C.B. (1971) Metabolite transport in C4 photosynthesis. Aust. J. Biol. Sci. 24, 159–163
Osmond, C.B., Smith, F.A. (1976) Symplastic transport of metabolites during C4-photosynthesis. In: Intercellular communication in plants: Studies on plasmodesmata, pp 229–241, Gunning, B.E.S., Robards, A.W. eds. Springer, Berlin Heidelberg New York
Outlaw, W.H., Fisher, D.B., Christy, A.L. (1975) Compartmentation in Vicia faba leaves. II. Kinetics of 14C-sucrose redistribution among individual tissues following pulse labeling. Plant Physiol. 55, 704–711
Slack, C.R., Hatch, M.D., Goodchild, D.J. (1969) Distribution of enzymes in mesophyll and parenchyma-sheath chloroplasts of maize leaves in relation to the C4-dicarboxylic acid pathway of photosynthesis. Biochem. J. 114, 489–498
Stitt, M., Heldt, H.W. (1985) Control of photosynthetic sucrose synthesis by fructose-2,6-bisphosphate. Intercellular metabolite distribution and properties of the cytosolic fructose bisphosphatase in leaves of Zea mays L. Planta 164, 179–188
Stitt, M., Wirtz, W., Heldt, H.W. (1980) Metabolite levels during induction in the chloroplast and extrachloroplast compartments of spinach protoplasts. Biochim. Biophys. Acta 593, 85–102
Stitt, M., Wirtz, W., Heldt, H.W. (1983) Regulation of sucrose synthesis by cytoplasmic fructosebisphosphatase and sucrose phosphate synthase during photosynthesis in varying light and carbon dioxide. Plant Physiol. 72, 767–774
Vernon, L.P. (1960) Spectrophotometric determination of chlorophylls and pheophytins in plant extracts. Anal. Chem. 32, 1144–1150
Woo, K.C., Pyliotis, N.A., Downton, W.J.S. (1971) Thylakoid aggregation and chlorophyll a/chlorophyll b ratio in C4-plants. Z. Pflanzenphysiol. 64, 400–413
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Leegood, R.C. The intercellular compartmentation of metabolites in leaves of Zea mays L.. Planta 164, 163–171 (1985). https://doi.org/10.1007/BF00396078
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00396078