Advertisement

Leaf C4 Photosynthesis in silico: The CO2 Concentrating Mechanism

  • Agu Laisk
  • Gerald Edwards
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 29)

A computer model comprised of light reactions in PS II and PS I, electron—proton transport reactions in mesophyll and bundle sheath (BS) chloroplasts, all enzymatic reactions, and most of the known regulatory functions of NADP-malic enzyme type C4 photosynthesis, has been developed as a system of differential budget equations for intermediate compounds. Rate-equations were designed on principles of multisubstrate-multiproduct enzyme kinetics. The model provided good simulations for rates of photosynthesis and pool sizes of intermediates under varying light, CO2 and O2. A principle novelty of the model for NADP-ME type species is the hypothesis that electrons transported into the BS chloro-plasts via the malate shuttle enter the electron transport chain with the help of NAD(P)H-plastoquinone oxyreductase (NDH, or an enzyme of similar function). In the model, the electrons from reduced plastoquinone pass through the Q-cycle and photosystem I (PS I) only once, without cycling around PS I, as commonly assumed. With this the ratio of 2 ATP/NADPH, satisfying the energy requirements process, is fixed, provided that 2 H+/e are transported by the Q-cycle and 2 H+/e by NDH, and 4 H+are utilized per ATP generated. The hypothesis is based on modeling results showing that there must be fine control of the ATP/NADPH ratio in BS chloroplasts for optimum function of C4 photosynthesis. The CO2 concentrating function of NADP-ME type C4 photosynthesis, which occurs as the rate of the C4 cycle exceeds the rate of CO2 assimilation in BS cells (overcycling), can be explained on the basis of two processes. First, alternative consumption of some ATP in BS chloroplasts to support other processes (e.g. starch and protein synthesis) reduces the ATP/NADPH ratio available in BS. As a result, some CO2 imported into BS remains unassimilated and accumulates, resulting in overcycling back to the mesophyll. Second, the residual photorespiratory activity alternatively consumes some ribulose 1,5-bisphosphate for oxygenation; as with the alternative consumption of ATP, some CO2 imported into BS remains unassimilated and accumulates, causing overcycling. The CO2 evolved from photorespiration in BS also contributes to the CO2 pump in C4 plants.

Keywords

Bundle Sheath Acceptor Side Cyclic Electron Transport Bundle Sheath Cell Mesophyll Chloroplast 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson LE, Gatla N and Carol AA (2005) Enzyme co-localization in pea chloroplasts: glyceraldehyde-3-P dehy-drogenase, triose-P isomerase, aldolase and seduheptulose bisphosphatase. Photosynth Res. 83: 317–328PubMedCrossRefGoogle Scholar
  2. Arnon DI (1959) Conversion of light into chemical energy in photosynthesis. Nature 184: 10–21PubMedGoogle Scholar
  3. Arnon DI and Chain RK (1975) Regulation of ferredoxin-catalyzed photosynthetic phophorylation. Proc Natl Acad Sci USA 72: 4961–4965PubMedCrossRefGoogle Scholar
  4. Arnon DI and Chain RK (1979) Regulatory electron transport pathways in cyclic photophosphorylation. FEBS Lett 102: 133–138PubMedCrossRefGoogle Scholar
  5. Arnon DI, Whatley FR and Allen MB (1958) Assimilatory power in photosynthesis. Science 127: 1026–1034PubMedCrossRefGoogle Scholar
  6. Avenson TJ, Kanazawa A, Cruz JA, Takizawa K, Ettinger WE and Kramer DM (2005) Integrating the proton circuit into photosynthesis: progress and challenges. Plant Cell Environ 28: 97–109CrossRefGoogle Scholar
  7. Berry J and Farquhar GD (1978) The CO2 concentration function of C4 photosynthesis: a biochemical model. In: Hall D, Coombs J and Goodwin T (eds) Proceedings of the 4th International Congress on Photosynthesis, pp 119– 131. Biochemical Society, LondonGoogle Scholar
  8. Campbell WJ and Ogren WL (1990) Electron transport through photosystem I stimulates light activation of ribu-lose bisphosphate carboxylase/oxygenase (Rubisco) by rubisco activase. Plant Physiol 94: 479–484PubMedCrossRefGoogle Scholar
  9. Campbell WJ and Ogren WL (1992) Light activation of Rubisco by Rubisco activase and thylakoid membranes. Plant Cell Physiol 33: 751–756Google Scholar
  10. Canvin DT, Berry JA, Badger MR, Fock H and Osmond B (1980) Oxygen exchange in leaves in the light. Plant Physiol 66: 302–307PubMedCrossRefGoogle Scholar
  11. Cassan N, Lagouette B and Setif P (2005) Ferredoxin-NADP+ reductase. Kinetics of electron transfer, transient intermediates, and catalytic activities studied by flashabsorption spectroscopy with isolated photosystem I and ferredoxin. J Biol Chem 280: 25960–25972PubMedCrossRefGoogle Scholar
  12. Clarke JE and Johnson GN (2001) In vivo temperature dependence of cyclic and pseudocyclic electron transport in barley. Planta 212: 808–816PubMedCrossRefGoogle Scholar
  13. Collatz GJ, Ribas-Carbo M and Berry JA (1992) Coupled photosynthesis-stomatal conductance model for leaves of C4 plants. Aust J Plant Physiol 19: 519–538Google Scholar
  14. Cruz JA, Sacksteder CA, Kanazawa A and Kramer DM (2001) Contribution of electric field (▵ψ) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into ▵ψ and ▵pH by ionic strength. Biochemistry 40: 1226–1237PubMedCrossRefGoogle Scholar
  15. Cseh Z, Vianelli A, Rajagopal S, Krumova S, Kovacs L, Papp E, Barzda V, Jennings R and Garab G (2005) Thermo-optically induced reorganizations in the main light harvesting antenna of plants. I. Non-Arrhenius type temperature dependence and linear light-intensity dependencies. Photosynth Res 86: 263–273PubMedCrossRefGoogle Scholar
  16. Dilley RA (1991) Energy coupling in chloroplasts: a calcium-gated switch controls proton fluxes between localized and delocalized proton gradients. Current Topics in Bioenergetics 16: 265–317Google Scholar
  17. Doncaster HD and Leegood RC (1987) Regulation of phos-phoenolpyruvate carboxylase activity in maize leaves. Plant Physiol 84: 82–87PubMedCrossRefGoogle Scholar
  18. Edwards GE (1986) Carbon fixation and partitioning in the leaf. In: Shannon JC, Knievel DP and Boyer CD (eds) Regulation of Carbon and Nitrogen Reduction and Utilization in Maize, pp 51–65. Waverly Press, Baltimore, MDGoogle Scholar
  19. Edwards GE and Ku MSB (1987) The biochemistry of C3–C4 intermediates. In: Hatch MD and Boardman NK (eds) The Biochemistry of Plants, pp 275–325. Academic, New YorkGoogle Scholar
  20. Edwards GE and Voznesenskaya E (2009) C4 photosynthesis: Kranz forms and single-cell C4 in terrestrial plants. In: Raghavendra A and Sage RF (eds) Photosynthesis and Related CO2 Concentrating Mechanisms. Advances in Photosynthesis and Respiration. Springer, Dordrecht, in pressGoogle Scholar
  21. Edwards GE and Walker DA (1983) C3,C4: Mechanisms, and Cellular and Environmental Regulation, of Photosynthesis. Blackwell, Oxford/LondonGoogle Scholar
  22. Eichelmann H and Laisk A (1999) Ribulose-1,5-bisphosphate carboxylase/oxygenase content, assimi-latory charge and mesophyll conductance in leaves. Plant Physiol 119: 179–189PubMedCrossRefGoogle Scholar
  23. Eichelmann H, Talts E, Oja V, Rasulov B, Padu E and Laisk A (2008) Rubisco activity is is related to photosystem I in leaves. In: Allen JF, Gantt E, Golbeck JH and Osmond B (eds) Photosynthesis. Energy from the Sun: 14th International Congress on Photosynthesis, pp 853–856. Springer, Dordrecht, The NetherlandsGoogle Scholar
  24. Farquhar GD, Von Caemmerer S and Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149: 78–90CrossRefGoogle Scholar
  25. Furbank RT and Badger MR (1982) Photosynthetic oxygen exchange in attached leaves of C4 monocotyledons. Aust J Plant Physiol 9: 553–558Google Scholar
  26. Furbank RT, Stitt M and Foyer CH (1985) Intercellular com-partmentation of sucrose synthesis in leaves of Zea mays L. Planta 164: 172–178CrossRefGoogle Scholar
  27. Furbank RT, Jenkins CLD and Hatch MD (1989) CO2 concentrating mechanism of C4 photosynthesis. Plant Physiol 91: 1364–1371PubMedCrossRefGoogle Scholar
  28. Gao Y and Woo KC (1996) Regulation of phosphoenolpyru-vate carboxylase in Zea mays by protein phosphorylation and metabolites and their roles in photosynthesis. Aust J Plant Physiol 23: 25–32Google Scholar
  29. Gerst U, Schönknecht G and Heber U (1994) ATP and NADPH as the driving force of carbon reduction in leaves in relation to thylakoid energization by light. Planta 193: 421–429CrossRefGoogle Scholar
  30. Golbeck JH (1987) Structure, function and organization of the photosystem I reaction center complex. Biochim Bio-phys Acta 895: 167–204Google Scholar
  31. Golding AJ and Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218: 107–114PubMedCrossRefGoogle Scholar
  32. Golding AJ, Finazzi G and Johnson GN (2004) Reduction of the thylakoid electron transport chain by stromal reduc-tants — evidence for activation of cyclic electron transport upon dark adaptation under drought. Planta 220: 356–363PubMedCrossRefGoogle Scholar
  33. Hatch MD (1987) C4 photosynthesis: A unique blend of modified biochemistry, anatomy and ultrastructure. Biochim Biophys Acta 895: 81–106Google Scholar
  34. He D and Edwards G (1996) Estimation of diffusive resistance of bundle sheath cells to CO2 from modeling of C4 photosynthesis. Photosynth Res 49: 195–208CrossRefGoogle Scholar
  35. 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: 263–285Google Scholar
  36. Hosler JP and Yocum CF (1985) Evidence for two cyclic photophosphorylation reactions concurrent with ferredoxin-catalyzed non-cyclic electron transport. Biochim Biophys Acta 808: 21–31CrossRefGoogle Scholar
  37. Hosler JP and Yocum CF (1987) Regulation of cyclic photophosphorylation during ferredoxin-mediated electron transport. Effect of DCMU and the NADPH/NADP+ ratio. Plant Physiol 83: 965–969PubMedCrossRefGoogle Scholar
  38. Huber JL, Hite DRC, Outlaw WH Jr and Huber SC (1991) Inactivation of highly activated spinach leaf sucrose-phosphate synthase by dephosphorylation. Plant Physiol 95: 291–297PubMedCrossRefGoogle Scholar
  39. Ivanov B, Asada K and Edwards GE (2007) Analysis of donors of electrons to photosystem I and cyclic electron flow by redox kinetics of 700 in chloroplasts of isolated bundle sheath strands of maize. Photosynth Res 92: 65–74PubMedCrossRefGoogle Scholar
  40. Jiao JA and Chollet R (1988) Light/dark regulation of maize leaf phosphoenolpyruvate carboxylase by in vivo phos-phorylation. Arch Biochem Biophys 261: 409–417PubMedCrossRefGoogle Scholar
  41. Johnson G (2003) Thiol regulation of the thylakoid electron transport chain — a missing link in the regulation of photosynthesis. Biochemistry 42: 3040–3044PubMedCrossRefGoogle Scholar
  42. Kanai R, Edwards EE (1999) The biochemistry of C4 photosynthesis. In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 49–87. Academic Press, NewYorkCrossRefGoogle Scholar
  43. Kanazawa A and Kramer DM (2002) In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase. Proc Natl Acad Sci USA 99: 12789–12794PubMedCrossRefGoogle Scholar
  44. Keleti T (1990) Coupled reactions and channelling: their role in the control of metabolism. In: Cornish-Bowden A and Càrdenas ML (eds) Control of Metabolic Processes, pp 259–270. Plenum Press, New YorkGoogle Scholar
  45. Kiirats O, Lea PJ, Franceschi VR and Edwards GE (2002) Bundle sheath diffusive resistance to CO2 and effectiveness of C4 photosynthesis and refixation of photorespired CO2 in a C4 cycle mutant and wild-type Amaranthus edulis. Plant Physiol 130: 964–976PubMedCrossRefGoogle Scholar
  46. Kirchhoff H, Schöttler MA and Maurer JWE (2004) Plas-tocyanin redox kinetics in spinach chloroplasts: evidence for disequilibrium in the high potential chain. Biochim Biophys Acta 1659: 63–72PubMedCrossRefGoogle Scholar
  47. Klughammer C and Schreiber U (1994) An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+ -absorbance changes at 830 nm. Planta 192: 261–268CrossRefGoogle Scholar
  48. Kramer DM, Avenson TJ and Edwards GE (2004) Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci 9: 349–357PubMedCrossRefGoogle Scholar
  49. Ku MSB and Edwards GE (1975) Photosynthesis in mesophyll protoplasts and bundle sheath cells of various type of C4 plants. IV. Enzymes of respiratory metabolism and energy utilizing enzymes of photosynthetic pathways. Z. Pflanzenphysiol 77: 16–32Google Scholar
  50. Kubasek J, Setlik J, Dwyer S and Santrucek J (2007) Light and temperature alter carbon isotope discrimination and estimated bundle sheath leakiness in C4 grasses and dicots. Photosynth Res 91: 47–58PubMedCrossRefGoogle Scholar
  51. Kubicki A, Funk E, Westhoff P and Steinmüller K (1996) Differential expression of plastome-encoded ndh genes in mesophyll and bundle sheath chloroplasts of the C4 plant Sorghum bicolor indicates that the complex I-homologous NAD(P)H-plastoquinone oxidoreductase is involved in cyclic electron transport. Planta 199: 276–281CrossRefGoogle Scholar
  52. Laisk A (1970) A model of leaf photosynthesis and photorespiration. In: Shetlik I (ed) Prediction and Measurement of Photosynthetic Productivity, pp 295–306. PUDOC, WageningenGoogle Scholar
  53. Laisk A (1993) Mathematical modeling of free-pool and channeled electron transport in photosynthesis: evidence for a functional supercomplex around photosystem I. Proc R Soc Lond B 251: 243–251CrossRefGoogle Scholar
  54. Laisk A and Edwards GE (1997) CO2 and temperature-related induction of photosynthesis in C4 plants: an approach to the hierarchy of rate-limiting processes. Aust J Plant Physiol 24: 505–516CrossRefGoogle Scholar
  55. Laisk A and Edwards GE (1998) Oxygen and electron flow in C4 photosynthesis: Mehler reaction, photorespiration and CO2 concentration in bundle sheath. Planta 205: 632–645CrossRefGoogle Scholar
  56. Laisk A and Edwards GE (2000) A mathematical model of C4 photosynthesis: The mechanism of concentrating CO2 in NADP-malic enzyme type species. Photosynth Res 66: 199–224PubMedCrossRefGoogle Scholar
  57. Laisk A and Oja V (1994) Range of the photosynthetic control of postillumination P700 reduction rate in sunflower leaves. Photosynth Res 39: 39–50CrossRefGoogle Scholar
  58. Laisk A and Oja V (1998) Dynamic Gas Exchange of Leaf Photosynthesis. Measurement and Interpretation. CSIRO, Collingwood, AustraliaGoogle Scholar
  59. Laisk A and Sumberg A (1994) Partitioning of the leaf CO2 exchange into components using CO2 exchange and fluorescence measurements. Plant Physiol 106: 689–695PubMedGoogle Scholar
  60. Laisk A, Oja V, Rasulov B, Rämma H, Eichelmann H, Kas-parova I, Pettai H, Padu E and Vapaavuori E (2002) A computer-operated routine of gas exchange and optical measurements to diagnose photosynthetic apparatus in leaves. Plant Cell Env 25: 923–943CrossRefGoogle Scholar
  61. Laisk A, Eichelmann H, Oja V and Peterson RB (2005) Control of cytochrome b6f at low and high light intensity and cyclic electron transport in leaves. Biochim Biophys Acta 1708: 79–90PubMedCrossRefGoogle Scholar
  62. Laisk A, Eichelmann H and Oja V (2006) C3 photosynthesis in silico. Photosynth Res 90: 45–66PubMedCrossRefGoogle Scholar
  63. Laisk A, Eichelmann H, Oja V, Talts E and Scheibe R (2007) Rates and roles of cyclic and alternative electron flow in potato leaves. Plant Cell Physiol 48: 1575–1588PubMedCrossRefGoogle Scholar
  64. Leegood RC and Von Caemmerer S (1989) Some relationships between contents of photosynthetic intermediates and the rate of photosynthetic carbon assimilation in leaves of Zea mays L. Planta 178: 258–266CrossRefGoogle Scholar
  65. Mahler HR and Cordes EH (1966) Biological Chemistry. Harper & Row, New YorkGoogle Scholar
  66. Majeran W, Zybailov B, Ytterberg AJ, Dunsmore J, Sun Q and Van Wijk KJ (2008) Consequences of C4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheath cells. Mol Cell Proteomics 7: 1609–1638PubMedCrossRefGoogle Scholar
  67. Mitchell P (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol Rev 41: 445–502PubMedCrossRefGoogle Scholar
  68. Monson RK, Edwards GE and Ku MSB (1984) C3–C4 intermediate photosynthesis in plants. Bioscience 34: 563–574CrossRefGoogle Scholar
  69. Noctor G and Foyer CH (2000) Homeostasis of adenylate status during photosynthesis in a fluctuating environment. J Exp Bot 51: 347–356PubMedCrossRefGoogle Scholar
  70. Oja V, Eichelmann H, Peterson RB, Rasulov B and Laisk A (2003) Decyphering the 820 nm signal: redox state of donor side and quantum yield of photosystem I in leaves. Photosynth Res 78: 1–15PubMedCrossRefGoogle Scholar
  71. Oja V, Eichelmann H and Laisk A (2007) Calibration of simultaneous measurements of photosynthetic carbon dioxide uptake and oxygen evolution in leaves. Plant Cell Physiol 48: 198–203PubMedCrossRefGoogle Scholar
  72. Oja V, Eichelmann H and Laisk A (2008) Equilibrium or disequilibrium? A dual-wavelength investigation of photosystem I donors. In: Allen JF, Gantt E, Golbeck JH and Osmond B (eds) Photosynthesis. Energy from the Sun: 14th International Congress on Photosynthesis, pp 687– 690. Springer, Dordrecht, The NetherlandsGoogle Scholar
  73. Peisker M (1979) Conditions for low and oxygen-independent CO2 compensation concentrations in C4 plants as derived from a simple model. Photosynthetica 13: 198–207Google Scholar
  74. Ruban AV, Berera R, Ilioaia C, Van Stokkum IHM, Kennis JTM, Pascal AA, Van Amerongen H, Bruno R, Horton P and Van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450: 575–578PubMedCrossRefGoogle Scholar
  75. Rumberg B, Schubert K, Strelow F and Tran-Anh T (1990) The H+/ATP coupling ratio at the H+-ATP-synthase of spinach chloroplasts is four. In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol. III, pp 125–128. Kluwer, Dordrecht, The NetherlandsGoogle Scholar
  76. Ruuska SA, Badger MR, Andrews TJ and Von Caem-merer S (2000) Photosynthetic electron sinks in in trans-genic tobacco with reduced amounts of rubisco: little evidence for significant Mehler reaction. J Exp Bot 51: 357–368PubMedCrossRefGoogle Scholar
  77. Sacksteder CA, Kanazawa A, Jacoby ME and Kramer DM (2000) The proton to electron stoichiometry of steady-state photosynthesis in living plants: a proton-pumping Q cycle is continuously engaged. Proc Natl Acad Sci USA 97: 14283–14288PubMedCrossRefGoogle Scholar
  78. Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161: 341–370CrossRefGoogle Scholar
  79. Scheuring S, Fotiadis D, Möller C, Müller SA, Engel A and Müller DJ (2001) Single proteins observed by atomic force microscopy. Single Mol 2: 59–67CrossRefGoogle Scholar
  80. Seelert H, Poetsch A, Dencher NA, Engel A, Stahlberg H and Müller DJ (2000) Proton powered turbine of a plant motor. Nature 405: 418–419PubMedCrossRefGoogle Scholar
  81. Seelert H, Dencher NA and Müller DJ (2003) Fourteen protomers compose the oligomer II of the proton-rotor in spinach chloroplast ATP synthase. J Mol Biol 333: 337–344PubMedCrossRefGoogle Scholar
  82. Stitt M and Heldt HW (1985) Intercellular metabolite distribution and properties of the cytosolic fructosebisphos-phatase in leaves of Zea mays L. Planta 164: 179–188CrossRefGoogle Scholar
  83. Sumberg A and Laisk A (1995) Measurement of the CO2/O2 specificity of Rubisco in leaves. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, Vol. V, pp 615–618. Kluwer, Dordrecht/Boston, MA/LondonGoogle Scholar
  84. Süss K-H, Prokhorenko I and Adler K (1995) In situ association of calvin cycle enzymes, ribulose-1,5-bisphosphate carboxylase/oxygenase activase, ferredoxin-NADP+reductase, and nitrite reductase with thylacoid and pyrenoid membranes of Chlamydomonas reinhardtii chloroplasts as revealed by immunoelectron microscopy. Plant Physiol 107: 1387–1397PubMedGoogle Scholar
  85. Takabayashi A, Kishine M, Asada K, Endo T and Sato F (2005) Differential use of two cyclic electron flows around photosystem I for driving CO2-concentration mechanism in C4 photosynthesis. Proc Natl Acad Sci USA 102: 16898–16903PubMedCrossRefGoogle Scholar
  86. Talts E, Oja V, Rämma H, Rasulov B, Anijalg A and Laisk A (2007) Dark inactivation of ferredoxin-NADP reductase and cyclic electron flow under far-red light in sunflower leaves. Photosynth Res 94: 109–120PubMedCrossRefGoogle Scholar
  87. Tremmel IG, Kirchhoff H, Weis E and Farquhar GD (2003) Dependence of plastoquinol diffusion on the shape, size, and density of integral thylakoid proteins. Biochim Bio-phys Acta 1607: 97–109CrossRefGoogle Scholar
  88. Usuda H (1987) Change in levels of intermediates of the C4 cycle and reductive pentose phosphate pathway under various light intensities in maize leaves. Plant Physiol 84: 549–554PubMedCrossRefGoogle Scholar
  89. Vallon O, Bulte L, Dainese P, Olive J, Bassi R and Wollman F-A (1991) Lateral redistribution of cytochrome b6/f complexes along thylakoid membranes upon state transitions. Proc Natl Acad Sci USA 88: 8262–8266PubMedCrossRefGoogle Scholar
  90. Viil J, Laisk A, Oja V and Pärnik T (1972) Positive influence of oxygen on photosynthesis. Doklady AN SSSR (Proc Acad Sci USSR) 204 (5): 1269–1271 (in Russian)Google Scholar
  91. Viil J, Laisk A, Oja V and Pärnik T (1977) Enhancement of photosynthesis caused by oxygen under saturating irra-diance and high CO2 concentrations. Photosynthetica 11 (3): 251–259Google Scholar
  92. Von Caemmerer S (2000) Biochemical Models of Leaf Photosynthesis. CSIRO Publ, Collingwood, AustraliaGoogle Scholar
  93. Von Caemmerer S and Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153: 376–387CrossRefGoogle Scholar
  94. Von Caemmerer S and Furbank RT (1999) Modeling C4 photosynthesis. In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 173–211. Academic, San Diego, CA/ London/Boston, MA/NewYork/Sydney/Tokyo/TorontoCrossRefGoogle Scholar
  95. Weiner H, Burnell JN, Woodrow IE, Heldt HW and Hatch MD (1988) Metabolite diffusion into bundle sheath cells from C4 Plants. Plant Physiol 88: 815–822PubMedCrossRefGoogle Scholar
  96. Winter H, Robinson DG and Heldt HW (1993) Subcellular volumes and metabolite concentrations in barley leaves. Planta 191: 180–190CrossRefGoogle Scholar
  97. Winter H, Robinson DG and Heldt HW (1994) Subcellular volumes and metabolite concentrations in spinach leaves. Planta 193: 530–535CrossRefGoogle Scholar
  98. Zhang H, Whitelegge JP and Cramer WA (2001) Ferredoxin: NADP+oxidoreductase is a subunit of the chloroplast cytochrome b6f complex. J Biol Chem 276: 38159–38165PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Agu Laisk
    • 1
  • Gerald Edwards
    • 2
  1. 1.Institute of Molecular and Cell BiologyTartu UniversityTartuEstonia
  2. 2.School of Biological SciencesWashington State UniversityPullmanUSA

Personalised recommendations