Summary
C4 plants can be divided into three groups based on differences in activities of three decarboxylating enzymes: NADP-malic enzyme, NAD-malic enzyme, and phosphopyruvate carboxykinase.
In the Gramineae the three C4 groups are distinguished by anatomical and ultrastructural characteristics of bundle-sheath chloroplasts. NADP-malic enzyme species lack well-developed grana in bundle-sheath chloroplasts (grana reduced) and the bundle-sheath chloroplasts are in the centrifugal position. NAD-malic enzyme species have bundle-sheath chloroplasts in the centripetal position and contain grana. Phosphopyruvate carboxykinase species have bundle-sheath chloroplasts in the centrifugal position and they contain grana. NADP-malic enzyme species of the Gramineae have only been found in the subfamilies Aristidoideae and Panicoideae. With the exception of the genera Panicum, and Urochloa, NAD-malic enzyme species and phosphopyruvate carboxykinase species have only been found in the subfamily Eragrostoideae. C4 species of the genus Panicum are found among all three of the C4 groups.
The dicotyledonous C4 species examined fall into two groups: those having high NADP-malic enzyme and those having high NAD-malic enzyme. No phosphopyruvate carboxykinase C4 species have been found among the dicotyledons. The NADP-malic enzyme C4 species of the dicotyledons like NADP-malic enzyme species of the Gramineae have bundle-sheath chloroplasts with reduced grana but in contrast to NADP-malic enzyme species of the Gramineae the bundle-sheath chloroplasts are in the centripetal position. The NAD-malic enzyme species of the dicotyledons like the NAD-malic enzyme species of the Gramineae have bundlesheath chloroplasts in the centripetal position with well developed grana.
The results are discussed in terms of evolutionary and functional diversification of C4 plants.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Anderson, J. M., Woo, K. C., Boardman, N. K.: Photochemical systems in mesophyll and bundle sheath chloroplasts of C4 plants. Biochim. biophys. Acta (Amst.) 245, 398–408 (1971)
Andrews, T. J., Johnson, H. S., Slack, R. C., Hatch, M. D.: Malic enzyme and aminotransferases in relation to 3-phosphoglycerate formation in plants with the C4-dicarboxylic acid pathway of photosynthesis. Phytochemistry 10, 2005–2013 (1971)
Bender, M. M.: Mass spectrometric studies of carbon 13 variations in corn and other grasses. Amer. J. Sci. Radiocarbon Suppl. 10, 468–472 (1968)
Bender, M. M.: Variations in the 13C/12C ratios of plants in relation to the pathway of photosynthetic carbon dioxide fixation. Phytochemistry 10, 1239–1244 (1971)
Berry, J. A., Downton, W. J. S., Tregunna, E. B.: The photosynthetic carbon metabolism of Zea mays and Gomphrena globosa: the location of the CO2 and carboxyl transfer reactions. Canad. J. Bot. 48, 777–786 (1970)
Bisalputra, T., Downton, W. J. S., Tregunna, E. B.: The distribution and ultrastructure of chloroplasts in leaves differing in photosynthetic carbon metabolism. I. Wheat, sorghum, and Aristida (Gramineae). Canad. J. Bot. 47, 15–21 (1969)
Black, C. C.: Photosynthetic carbon fixation in relation to net CO2 uptake. Ann. Rev. Plant Physiol. 24, 253–286 (1973)
Black, C. C., Mollenhauer, H. H.: Structure and distribution of chloroplasts and other organelles in leaves with various rates of photosynthesis. Plant. Physiol. 47, 15–23 (1971)
Brown, R. H., Gracen, V. E.: Distribution of the post-illumination CO2 burst among grasses. Crop Sci. 12, 30–33 (1972)
Brown, W. V.: Leaf anatomy in grass systematics. Bot. Gaz. 119, 170–178 (1958)
Brown, W. V.: A cytological difference between the Eupanicoideae and the Chloridoideae (Gramineae). Southwestern Naturalist 5, 7–11 (1960)
Brown, W. V.: Grass leaf anatomy: Its use in systematics. Recent Advances in Bot. 1, 105–108 (1961)
Brown, W. V., Smith, B. N.: Grass evolution, the Kranz syndrome, 13C/12C ratios, and continental drift. Nature (Lond.) 239, 345–346 (1972)
Chen, T. M., Campbell, W. H., Dittrich, P., Black, C. C.: Distribution of carboxylation and decarboxylation enzymes in isolated mesophyll cells and bundle sheath strands of C4 plants. Biochem. biophys. Res. Commun. 51, 461–467 (1973)
Downton, W. J. S.: Preferential C4-dicarboxylic acid synthesis, the post-illumination CO2 burst, carboxyl transfer step, and grana configuration in plants with C4-photosynthesis. Canad. J. Bot. 18, 1795–1800 (1970)
Downton, W. J. S.: The chloroplasts and mitochondria of bundle sheath cell in relation to C4 photosynthesis. In: Photosynthesis and photorespiration, p. 419–425, M. D. Hatch, C. B. Osmond, R. O. Slatyer, eds. New York: Wiley-Interscience 1971
Downton, W. J. S., Berry, J. A., Tregunna, E. B.: C4-photosynthesis: noncyclic electron flow and grana development in bundle sheath chroroplasts. Z. Pflanzenphysiol. 63, 194–198 (1970)
Downton, W. J. S., Tregunna, E. B.: Carbon dioxide compensation—its relation to photosynthetic carboxylation reactions, systematics of the Gramineae and leaf anatomy. Canad. J. Bot. 46, 207–215 (1968).
Edwards, G. E., Black, C. C.: Photosynthesis in mesophyll cells and bundle sheath cells isolated from Digitaria sanguinalis (L.) Scop. leaves. In: Photosynthesis and photorespiration, p. 153–168, M. D. Hatch, C. B. Osmond, R. O. Slatyer, eds. New York: Wiley-Interscience 1971
Edwards, G. E., Gutierrez, M.: Metabolic activities in extracts of mesophyll and bundle sheath cells of Panicum miliaceum (L.) in relation to the C4-dicarboxylic acid pathway of photosynthesis. Plant Physiol. 50, 728–732 (1972)
Edwards, G. E., Kanai, R., Black, C. C.: Phosphoenolpyruvate carboxykinase in leaves of certain plants which fix CO2 by the C4-dicarboxylic acid pathway of photosynthesis. Biochem. biophys. Res. Commun. 45, 278–285 (1971)
Edwards, G. E., Kanai, R., Ku, S. B., Gutierrez, M., Huber, S. C.: Compartmentation and coordination of CO2 assimilation in isolated mesophyll protoplasts and bundle sheath cells of C4 plants. In: Mechanism of regulation of plant growth, p. 203–211, R. L. Bieleski, A. R. Ferguson, M. M. Cresswell, eds., Bull. No. 12, Roy. Soc. New Zealand, Wellington, N. Z. (1974)
Frederick, S. E., Newcomb, E. H.: Ultrastructure and distribution of microbodies in leaves of grasses with and without CO2-photorespiration. Planta (Berl.) 96, 152–174 (1971)
Gracen, V. E., Hilliard, J. H., Brown, R. H., West, S. H.: Peripheral reticulum in chloroplasts of plants differing in CO2 fixation pathways and photorespiration. Planta (Berl.) 107, 189–204 (1972)
Gutierrez, M., Kanai, R., Huber, S. C., Ku, S. B., Edwards, G. E.: Photosynthesis in mesophyll protoplasts and bundle sheath cells of various types of C4 plants. I. Carboxylases and CO2 fixation studies. Z. Pflanzenphysiol. 72, 305–319 (1974)
Hatch, M. D.: Mechanism and function of the C4 pathway of photosynthesis. In: Photosynthesis and photorespiration, p. 139–152, M. D. Hatch, C. B. Osmond, R. O. Slatyer, eds. New York: Wiley-Interscience, 1971
Hatch, M. D., Kagawa, T.: NAD-malic enzyme in leaves with C4 photosynthesis and its role in C4 acid decarboxylation. Arch. Biochem. Biophys. 160, 346–349 (1974)
Hatch, M. D., Slack, C. R.: The C4-dicarboxylic acid pathway of photosynthesis. Progr. Phytochem. 2, 35–106 (1970)
Hodge, A. J., McLean, J. D., Mercer, F. C.: Ultrastructure of the lamellae and grana in the chloroplasts of Zea mays L. J. biophys. biochem. Cytol. 1, 605–619 (1955)
Huber, S. C., Kanai, R., Edwards, G. E.: Decarboxylation of malate by isolated bundle sheath cells of certain plants having the C4-dicarboxylic acid pathway of photosynthesis. Planta (Berl.) 113, 53–66 (1973)
Johnson, S. C.: An electron microscope study of the photosynthetic apparatus in plants, with special reference to the Gramineae. Doct. Diss., No. 64-8013, Univ. of Texas, Austin (1964)
Johnson, S. C., Brown, W. V.: Grass leaf ultrastructural variations. Amer. J. Bot. 60, 727–735 (1973)
Kanai, R., Edwards, G. E.: Enzymatic separation of mesophyll protoplasts and bundle sheath cells from leaves of C4 plants. Naturwissenschaften 60, 157–158 (1973a)
Kanai, R., Edwards, G. E.: Separation of mesophyll protoplasts and bundle sheath cells from maize leaves for photosynthetic studies. Plant. Physiol. 51, 1133–1137 (1973b)
Ku, S. B., Gutierrez, M., Edwards, G. E.: Localization of the C4 and C3 pathways of photosynthesis in the leaves of Pennisetum purpureum and other C4 species. Insignificance of phenol oxidase. Planta (Berl.) 119, 267–278 (1974b)
Ku, S. B., Gutierrez, M., Kanai, R., Edwards, G. E.: Photosynthesis in mesophyll protoplasts and bundle sheath cells of various types of C4 plants. II. Chlorophyll and Hill reaction studies. Z. Pflanzenphysiol. 72, 320–337 (1974a)
Laetsch, W. M.: Chloroplast specialization in dicotyledons possessing the C4-dicarboxylic acid pathway of photosynthetic CO2 fixation. Amer. J. Bot. 55, 875–883 (1968)
Laetsch, W. M.: Relationship between chloroplast structure and photosynthetic carbon-fixation pathways. Sci. Progr. (Oxf.) 57, 323–351 (1969)
Laetsch, W. M.: Chloroplast structural relationships in leaves of C4 plants. In: Photosynthesis and photorespiration, p. 323–349, M. D. Hatch, C. B. Osmond, R. O. Slatyer, eds. New York: Wiley-Interscience 1971
Laetsch, W. M., Stetler, D. A., Vlitos A. J.: The ultrastructure of sugarcane chloroplasts. Z. Pflanzenphysiol. 54, 472–474 (1966)
Mayne, B. C., Dee, A. M., Edwards, G. E.: Photosynthesis in mesophyll protoplasts and bundle sheath cells of various types of C4 plants. III. Fluorescence emission spectra, delayed light emission, and P700 content. Z. Pflanzenphysiol., in press
Mayne, B. C., Edwards, G. E., Black, C. C.: Spectral, physical, and electron transport activities in the photosynthetic apparatus of mesophyll cells and bundle sheath cells of Digitaria sanguinalis (L.) Scop. Plant Physiol. 47, 600–605 (1971)
Osmond, C. B.: Carbon reduction and photosystem II deficiency in leaves of C4 plants. Aust. J. Plant Physiol. 1, 41–50 (1974)
Osmond, C. B., Troughton, J. H., Goodchild, D. J.: Physiological, biochemical, and structural studies of photosynthesis and photorespiration in two species of Atriplex. Z. Pflanzenphysiol. 61, 218–237 (1969)
Smith, B. N., Brown, W. V.: The Kranz syndrome in the Gramineae as indicated by carbon isotopic ratios. Amer. J. Bot. 60, 505–513 (1973)
Spurr, A. R.: A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26, 31–43 (1969)
Tregunna, E. B., Smith, B. N., Berry, J. A., Downton, W. J. S.: Some methods for studying the photosynthetic taxonomy of the angiosperms. Can. J. Bot. 48, 1209–1214 (1970)
Wintermans, J. F. G. M., De Mots, A.: Spectrophotometric characteristics of chlorophyll and their pheophytins in ethanol. Biochim. biophys. Acta (Amst.) 109, 448–453 (1965)
Woo, K. C., Pyliotis, N. A., Downton, W. J. S.: Thylakoid aggregation and chlorophyll a/chlorophyll b ratio in C4-plants. Z. Pflanzenphysiol. 64, 400–413 (1971)
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Gutierrez, M., Gracen, V.E. & Edwards, G.E. Biochemical and cytological relationships in C4 plants. Planta 119, 279–300 (1974). https://doi.org/10.1007/BF00388331
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00388331