Summary
C4 photosynthesis involves intercellular metabolite transport, between the mesophyll and bundle-sheath, and intracellular shuttling of metabolites between the chloroplasts, cytosol and, in some cases, the mitochondria. In this chapter, the role of diffusion driven intercellular transport of metabolites via plasmodesmata is discussed, together with the impact on the ability of the bundle-sheath to concentrate CO2 The chapter also considers the nature and role of organelle transporters for phosphorylated compounds, organic and amino acids in relation to C4 photosynthesis in the mesophyll and bundle-sheath.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Aoki N and Kanai R (1995) The role of phosphoenolpyruvate in proton/pyruvate cotransport into mesophyll chloroplasts of maize. Plant Cell Physiol 36: 187–189
Aoki N and Kanai R (1997) Reappraisal of the role of sodium in the light-dependent active transport of pyruvate into mesophyll chloroplasts of C4 plants. Plant Cell Physiol 38: 1217–1225
Aoki N, Ohnishi J and Kanai R (1992) Two different mechanisms for transport of pyruvate into mesophyll chloroplasts of C4 plants—a comparative study. Plant Cell Physiol 33: 805–809
Aoki N, Ohnishi J and Kanai R (1994) Proton/pyruvate cotransport intomesophyllchloroplasts of C4 plants. Plant Cell Physiol 35: 801–806
Boag S and Jenkins CLD (1985) CO2 assimilation and malate decarboxylation by isolated bundle sheath chloroplasts from Zea mays. Plant Physiol 79: 165–170
Boag S and Jenkins CLD (1986) The involvement of aspartate and glutamate in the decarboxylation of malate by isolated bundle sheath chloroplasts of Zea mays. Plant Physio l80: 115–119
Botha CEJ (1992) Plasmodesmatal distribution, structure and frequency in relation to assimilation in C3 and C4 grasses in southern Africa. Planta 187: 348–358
Botha CEJ and Evert RF (1988) Plasmodesmatal distribution and frequency in vascular bundles and contiguous tissues of the leaf of Themeda triandra. Planta 173: 433–41
Brown RH and Byrd TG (1993) Estimation of bundle sheath cell conductance in C4 species and O2 sensitivity of photosynthesis. Plant Physiol 103: 1183–1188
Brownell PF and Crossland CJ (1972) The requirement for sodium as a micronutrient by species having the C4 dicarboxylic photosynthetic pathway. Plant Physiol 49: 794–797
Brownell PF, Bielig LM and Grof CPL (1991) Increased carbonic anhydrase activity inleaves of sodium-deficient C4 plants. Aust J Plant Physiol 18: 589–592
Burnell JN (1988) An enzymic method for measuring the molecular exclusion limit of plasmodesmata of bundle sheath cells of C4 plants. J Exp Bot 39: 1575–1580
Carnal NW, Agostino A and Hatch MD (1993) Photosynthesis in phosphoenolpyruvate carboxykinase-type C4 plants: Mechanism and regulation of C4 acid decarboxylation in bundle sheath cells. Arch Biochem Biophys 306: 360–367
Chapman KSR and Hatch MD (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 DA and Hatch MD (1981) Dicarboxylate transport in maize mesophyll chloroplasts. Arch Biochem Biophys 211: 738–742
Day DA and Wiskich JT (1984) Transport processes of isolated mitochondria. Physiol Veg 22: 241–261
Dengler NC and Nelson T (1999) Leaf structure and development in C4 plants. In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 133–172. Academic Press, San Diego
Dever LV, Bailey KJ, Leegood RC and Lea PJ (1995) Control of photosynthesis in Amaranthus edulis mutants with reduced amounts of PEP carboxylase. Aust J Plant Physiol 24: 469–476
Doncaster HD and Leegood RC (1987) Regulation of phosphoenolpyruvate carboxylase activity in maize leaves. Plant Physiol 84: 82–87
Douce R, Aubert S and Neuburger M (1997) Metabolite exchange between the mitochondrion and the cytosol. In: Dennis DT, Layzell DB, Lefebvre DD and Turpin DH (eds), Plant Metabolism, pp 234–251. Longman, London
Fischer K, Arbinger B, Kammerer B, Busch C, Brink S, Wallmeier H, Sauer N, Eckerskorn C and Flügge U-I (1994) Cloning and in vivo expression of functional triose phosphate/phosphate translocators from C3-and C4-plants: Evidence for the putative participation of specific amino acid residues in the recognition of phosphoenolpyruvate. Plant J 5: 215–226
Flügge UI, Stitt M and Heldt HW (1985) Light-driven uptake of pyruvate into mesophyll chloroplasts from maize. FEBS Lett 183: 335–339
Furbank RT and Hatch MD (1987) Mechanism of C4 photosynthesis. The size and composition of the inorganic carbon pool in bundle-sheath cells. Plant Physiol 85: 958–964
Furbank RT and Leegood RC (1984) Carbon metabolism and gas exchange in leaves of Zea mays L. Interaction between the C3 and C4 pathways during photosynthetic induction. Planta 162: 457–162
Furbank RT, Jenkins CLD and Hatch MD (1989) CO2 concentrating mechanism of C4 photosynthesis: permeability of isolated bundle sheath cells to inorganic carbon. Plant Physiol 91: 1364–1371
Furbank RT, Jenkins CLD and Hatch MD (1990a) C4 photosynthesis: quantum requirements, C4 acid overcycling and Q-cycle involvement. Aust J Plant Physiol 17: 1–7
Furbank RT, Agostino A and Hatch MD (1990b) C4 acid decarboxylation and photosynthesis in bundle-sheath cells of NAD-malicenzyme-type C4 plants: Mechanism and the role of malate and orthophosphate. Arch Biochem Biophys 276: 374–381
Hatch MD and Osmond CB (1976) Compartmentation and transport in C4 photosynthesis. In: Stocking CR and Heber U (eds) Encyclopedia of Plant Physiology, New Series Vol 3, pp. 144–184, Springer-Verlag, Berlin
Hatch MD, Dröuscher L, Flügge U-I and Heldt HW (1984) A specific translocator for oxaloacetate transport in chloroplasts. FEBS Lett 178: 15–19
Hatch MD, Agostino A and Jenkins CLD (1995) Measurement of the leakage of CO2 from bundle-sheath cells of leaves during C4 photosynthesis. Plant Physiol 108: 173–181
Hattersley PW (1992) C4 photosynthetic pathway variation in grasses (Poaceae): Its significance for arid and semi arid lands. In: Chapman GP (ed) Desertified Grassland: Their Biology and Managements, Linnean Society Symposium Series, Vol 13, pp 181–212. Academic Press, London
Hattersley PW and Browning AJ (1981) Occurrence of the suberised lamella in leaves of grasses of different photosynthetic type. I. In parenchymatous bundle sheath and PCR (‘Kranz’) sheaths. Protoplasma 109: 371–401
Hattersley PW and Watson L (1992) Diversification of photosynthesis. In: Chapman GP (ed) Grass Evolution and Domestication, pp 38–116. Cambridge University Press, Cambridge
Heldt, HW and Flügge, UI (1992) Metabolite transport in plant cells. In: Tobin AK (ed) Plant Organelles, pp 21–47. Cambridge University Press, Cambridge
Henderson SA, von Caemmerer S and Farquhar GD (1992) Short-term measurements of carbon isotope discrimination in several C4 species. Aust J Plant Physiol 19: 263–285
Jenkins CLD, Furbank RT and Hatch MD (1989a) Inorganic carbon diffusion between C4 mesophyll and bundle sheath cells: Direct bundle sheath CO2 assimilation in intact leaves in the presenceof aninhibitor of the C4 pathway. Plant Physiol 91: 1356–1363
Jenkins CLD, Furbank RT and Hatch MD (1989b) Mechanism of C4 photosynthesis. A model describing the inorganic carbon pool in the bundle sheath cells. Plant Physiol 91: 1372–1381
Kanai R and Edwards GE (1999) The biochemistry of C4 photosynthesis. In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 49–87. Academic Press, San Diego
Karpilov YS (1970) Cooperative photosynthesis in xerophytes. Proc Moldavian Inst Irrigation Agric Res 11: 3–66 (in Russian)
Kawamitsu Y, Hakoyama S, Agata W and Takeda T (1985) Leaf interveinal distances corresponding to anatomical types in grasses. Plant Cell Physiol 26: 589–593
Keeley JE (1998) C4 photosynthetic modifications in the evolutionary transition from land towater in aquatic grasses. Oecologia 116: 85–97
Krall JK and Pearcy RW (1993) Concurrent measurements of oxygen and carbon dioxide exchange during lightflecks in maize (Zea mays L.) Plant Physiol 103: 823–828
Laetsch WM (1974) The C4 syndrome: A structural analysis. Ann Rev Plant Physiol 25: 27–52
Leegood RC (1985) The intercellular compart mentation of metabolites in leaves of Zea mays. Planta 164: 163–171
Leegood RC and Furbank RT (1984) Carbon metabolism and gas exchange in leaves of Zea mays L. Changes in CO2 fixation, chlorophyll fluorescence and metabolite levels during photosynthetic induction. Planta 162: 450–156
Leegood RC and von Caemmerer S (1988) The relationship between contents of photosynthetic intermediates and the rate of photosynthetic carbon assimilation in leaves of Amaranthus edulis L. Planta 174: 253–262
Leegood RC and von Caemmerer S (1989) Some relationships between the contents of photosynthetic intermediates and the rate of photosynthetic carbon assimilation in leaves of Zea mays L. Planta 178: 258–266
Leegood RC and von Caemmerer S (1994) Regulation of photosynthetic carbon assimilation in leaves of C3-C4 intermediate species of Moricandia and Flaveria. Planta 192: 232–238
Lucas WJ, Ding B and van der Schoot C (1993) Plasmodesmata and the supracellular nature of plants. New Phytol 125: 435–476
Meister M, Agostino A and Hatch MD (1996) The roles of malate and aspartate in C4 photosynthetic metabolism of Flaveria bidentis (L.). Planta 199: 262–269
Monson RK, Moore B, Ku MSB and Edwards GE (1986) Cofunction of C3 and C4 photosynthetic pathways in C3, C4 and C3-C4 intermediate Flaveria species. Planta 168: 493–502
Murata S, Kobayashi M, Matoh T and Sekiya J (1992) Sodium stimulates regeneration of phosphoenolpyruvate in mesophyll chloroplasts of Amaranthus tricolor. Plant Cell Physiol 33: 1247–1250
Nishikido T and Takanashi H (1973) Glycine activation of PEP carboxylase from monocotyledonous C4 plants. Biochem Biophys Res Comm 53: 126–133
Ohnishi J and Kanai R (1988) Glycerate uptake into mesophyll and bundle sheath chloroplasts of a C4 plant, Panicum miliaceum. J Plant Physiol 133: 119–121
Ohnishi J and Kanai R (1990) Pyruvate uptake induced by a pH jump in mesophyll chloroplasts of maize and sorghum, NADP-malic enzyme type C4 species. FEBS Lett 269: 122–124
Ohnishi J, Flügge UI and Heldt HW (1989) Phosphate translocator of mesophyll and bundle sheath chloroplasts of the C4 plant, Panicum miliaceum. Identification and kinetic characterization. Plant Physiol 91: 1507–1511
Ohnishi J, Flügge UI, Heldt HW and Kanai R (1990) Involvement of Na+ in active uptake of pyruvate in mesophyll chloroplasts of some C4 plants: Na+/pyruvate transport. Plant Physiol 94: 950–959
Oleson P (1975) Plasmodesmata between mesophyll and bundle sheath cells in relation to the exchange of C4-acids. Planta 123: 199–202
Osmond CB (1971). Metabolite transport in C4 photosynthesis. Aust J Biol Sci 24: 159–163
Raghavendra AS and Das VSR (1978) (Na+−K+-stimulated stimulated ATPase in leaves of C4 plants: Possible involvement in active transport of acids. J Exp Bot 29: 39–47
Stitt M and Heldt HW (1985a) 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 and Heldt HW (1985b) Generation and maintenance of concentration gradients between the mesophyll and bundle-sheath in maize leaves. Biochim Biophys Acta 808: 400–414
Taniguchi M and Sugiyama T (1996) Isolation, characterization and expression of cDNA clones encoding a mitochondrial malate translocator from Panicum miliaceum L. Plant Mol Biol 30: 51–64
Usuda H (1986) Non-autocatalytic build-up of ribulose 1,5-bisphosphate during the initial phase of photosynthetic induction in maize leaves. Plant Cell Physiol 27: 745–749
Usuda H (1987a) Changes in levels of intermediates of the C4 cycle and reductive pentose phosphate pathway under various concentrations of CO2 in maize leaves. Plant Physiol 83: 29–32
Usuda H (1987b) Changes in levels of intermediates of the C4 cycle and reductive pentose phosphate pathway under various light intensities in maize leaves. Plant Physiol 84: 549–554
Valle EM, Craig S, Hatch MD and Heldt HW (1989) Permeability and ultrastructure of bundle sheath cells isolated from C4 plants: Structure-function studies and the role of plasmo-desmata. Bot Acta 102: 276–282
von Caemmerer S and Furbank RT (1999) Modeling C4 photosynthesis. In: Sage RF and Monson RK (eds) Plant Biology, pp 173–211. Academic Press, San Diego
Weiner H and Heldt HW (1992) Inter-and intracellular distribution of amino acids and other metabolites in maize (Zea mays L.) leaves. Planta 187: 342–246
Weiner H, Burnell JN, Woodrow IE, Heldt HW and Hatch MD (1988) Metabolite diffusion into bundle sheath cells from C4 plants. Relation to C4 photosynthesis and plasmodesmatal function. Plant Physiol 88: 815–822
Wingler A, Walker RP, Chen Z-H and Leegood RC (1999) Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize. Plant Physiol 120: 539–545
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2000 Kluwer Academic Publishers
About this chapter
Cite this chapter
Leegood, R.C. (2000). Transport During C4 Photosynthesis. In: Leegood, R.C., Sharkey, T.D., von Caemmerer, S. (eds) Photosynthesis. Advances in Photosynthesis and Respiration, vol 9. Springer, Dordrecht. https://doi.org/10.1007/0-306-48137-5_19
Download citation
DOI: https://doi.org/10.1007/0-306-48137-5_19
Publisher Name: Springer, Dordrecht
Print ISBN: 978-0-7923-6143-5
Online ISBN: 978-0-306-48137-6
eBook Packages: Springer Book Archive