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Critical review: incorporating the arrangement of mitochondria and chloroplasts into models of photosynthesis and carbon isotope discrimination

  • Nerea UbiernaEmail author
  • Lucas A. Cernusak
  • Meisha Holloway-Phillips
  • Florian A. Busch
  • Asaph B. Cousins
  • Graham D. Farquhar
Original Article

Abstract

The arrangement of mitochondria and chloroplasts, together with the relative resistances of cell wall and chloroplast, determine the path of diffusion out of the leaf for (photo)respired CO2. Traditional photosynthesis models have assumed a tight arrangement of chloroplasts packed together against the cell wall with mitochondria located behind the chloroplasts, deep inside the cytosol. Accordingly, all (photo)respired CO2 must cross the chloroplast before diffusing out of the leaf. Different arrangements have recently been considered, where all or part of the (photo)respired CO2 diffuses through the cytosol without ever entering the chloroplast. Assumptions about the path for the (photo)respiratory flux are particularly relevant for the calculation of mesophyll conductance (gm). If (photo)respired CO2 can diffuse elsewhere besides the chloroplast, apparent gm is no longer a mere physical resistance but a flux-weighted variable sensitive to the ratio of (photo)respiration to net CO2 assimilation. We discuss existing photosynthesis models in conjunction with their treatment of the (photo)respiratory flux and present new equations applicable to the generalized case where (photo)respired CO2 can diffuse both into the chloroplast and through the cytosol. Additionally, we present a new generalized Δ13C model that incorporates this dual diffusion pathway. We assess how assumptions about the fate of (photo)respired CO2 affect the interpretation of photosynthetic data and the challenges it poses for the application of different models.

Keywords

Carbon and oxygen isotope discrimination Chloroplast Mesophyll conductance Photorespiration Photosynthesis Respiration 

Notes

Funding

N.U. received no external funding and conducted the work on her own time. L.A.C. was supported by the Australian Research Council (Grant no. ARC DP150100588), M.H.P., F.A.B., and G.D.F. by the Australian Government through the Australian Research Council Centre of Excellence for Translational Photosynthesis, and A.B.C. by the Office of Basic Energy Sciences, Department of Energy (Grant No. DE-FG02-09ER16062).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11120_2019_635_MOESM1_ESM.docx (123 kb)
Supplementary material 1 (DOCX 124 KB)

References

  1. Badger MR, Andrews TJ (1974) Effects of CO2, O2 and temperature on a high-affinity form of ribulose diphosphate carboxylase-oxygenase from spinach. Biochem Biophys Res Commun 60:204–210CrossRefPubMedGoogle Scholar
  2. Badger MR, Collatz GJ (1977) Studies on the kinetic mechanism of ribulose-1,5-bisphosphate carboxylase and oxygenase reactions, with particular reference to the effect of temperature on kinetic parameters. Carnegie Inst Wash Year Book 76:355–361Google Scholar
  3. Badger MR, Price GD (1994) The role of carbonic anhydrase in photosynthesis. Annu Rev Plant Physiol Plant Molec Biol 45:369–392CrossRefGoogle Scholar
  4. Bagley J, Rosenthal DM, Ruiz-Vera UM, Siebers MH, Kumar P, Ort DR, Bernacchi CJ (2015) The influence of photosynthetic acclimation to rising CO2 and warmer temperatures on leaf and canopy photosynthesis models. Global Biogeochem Cycles 29(29):194–206CrossRefGoogle Scholar
  5. Barbour MM, Evans JR, Simonin KA, von Caemmerer S (2016) Online CO2 and H2O oxygen isotope fractionation allows estimation of mesophyll conductance in C4 plants, and reveals that mesophyll conductance decreases as leaves age in both C4 and C3 plants. New Phytol 210(3):875–889CrossRefPubMedGoogle Scholar
  6. Berghuijs HNC, Yin X, Ho QT, van der Putten PEL, Verboven P, Retta MA, Nicolaï BM, Struik PC (2015) Modeling the relationship between CO2 assimilation and leaf anatomical properties in tomato leaves. Plant Sci 238:297–311CrossRefPubMedGoogle Scholar
  7. Berghuijs H, Yin NC, Ho X, Tri Q, Driever SM, Retta MA, Nicolaï BM, Struika PC (2016) Mesophyll conductance and reaction-diffusion models for CO2 transport in C3 leaves; needs, opportunities and challenges. Plant Sci 252:62–75CrossRefPubMedGoogle Scholar
  8. Bernacchi CJ, Singsaas EL, Pimentel AR, Portis JR, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24(24):253–259CrossRefGoogle Scholar
  9. Bernacchi CJ, Portis AR, Nakano H, von Caemmerer S, Long SP (2002) Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiol 130(4):1992–1998CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bernacchi CJ, Pimentel C, Long SP (2003) In vivo temperature response functions of parameters required to model RuBP-limited photosynthesis. Plant Cell Environ 26:1419–1430CrossRefGoogle Scholar
  11. Bernacchi CJ, Rosenthal DM, Pimentel C, Long SP, Farquhar GD (2009) Modelling the temperature dependence of C3 photosynthesis. In: Laisk A, Nedbal L, Govindjee (eds) Photosynthesis in silico. Understanding complexity from molecules to ecosystems. Springer, Dordrecht, pp 231–246Google Scholar
  12. Bernacchi CJ, Bagley JE, Serbin SP, Ruiz-Vera UM, Rosenthal DM, Vanloocke A (2013) Modelling C3 photosynthesis from the chloroplast to the ecosystem. Plant Cell Environ 36:1641–1657CrossRefPubMedGoogle Scholar
  13. Berry JA, Farquhar GD (1978) The CO2 concentrating function of C4 photosynthesis: a biochemical model. In: Hall D, Coombs J, Goodwin T (eds) Proceedings of the 4th international congrss on photosynthesis, The Biochemical Society, London, pp 119–131Google Scholar
  14. Björkman O (1968) Carboxydismutase activity in shade and sun adapted species of higher plants. Physiol Plant 21:1–10CrossRefGoogle Scholar
  15. Björkman O, Holmgren P (1963) Adaptability of the photosynthetic apparatus to light intensity in ecotypes from exposed and shaded habitats. Physiol Plant 16:889–914CrossRefGoogle Scholar
  16. Bowes G, Ogren WL, Hageman RH (1971) Phosphoglycolate production catalysed by ribulose diphosphate carboxylase. Biochem Bioph Res Co 45:71116–71122CrossRefGoogle Scholar
  17. Boyd RA, Gandin A, Cousins AB (2015) Temperature responses of C4 photosynthesis: biochemical analysis of Rubisco, Phosphoenolpyruvate carboxylase, and Carbonic anhydrase in Setaria viridis. Plant Physiol 169:1850–1861PubMedPubMedCentralGoogle Scholar
  18. Burnell JN, Hatch MD (1988) Low bundle sheath carbonic anhydrase is apparently essential for effective C4 pathway operation. Plant Physiol 86:1252–1256CrossRefPubMedPubMedCentralGoogle Scholar
  19. Busch FA, Sage RF (2017) The sensitivity of photosynthesis to O2 and CO2 concentration identifies strong Rubisco control above the thermal optimum. New Phytol 213:1036–1051CrossRefPubMedGoogle Scholar
  20. Busch FA, Sage TL, Cousins AB, Sage RF (2013) C3 plants enhance rates of photosynthesis by reassimilating photorespired and respired CO2. Plant Cell Environ 36:200–212CrossRefPubMedGoogle Scholar
  21. Busch FA, Sage RF, Farquhar GD (2018) Plants increase CO2 uptake by assimilating nitrogen via the photorespiratory pathway. Nat Plants 4:46–54CrossRefPubMedGoogle Scholar
  22. Cano FJ, López R, Warren CR (2014) Implications of the mesophyll conductance to CO2 for photosynthesis and water-use efficiency during long-term water stress and recovery in two contrasting Eucalyptus species. Plant Cell Environ 37:2470–2490CrossRefPubMedGoogle Scholar
  23. Cernusak LA, Ubierna N, Winter K, Holtum JAM, Marshall JD, Farquhar GD (2013) Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants. New Phytol 200:950–965CrossRefPubMedGoogle Scholar
  24. Collatz GJ, Berry JA, Farquhar GD, Pierce J (1990) The relationship between the rubisco reaction mechanism and models of photosynthesis. Plant Cell Environ 13:219–225CrossRefGoogle Scholar
  25. Collatz GJ, Ball JT, Grivet C, Berry JA (1991) Physiological and environmental-regulation of stomatal conductance, photosynthesis and transpiration – a model that includes a laminar boundary-layer. Agric For Meteorol 54:107–136CrossRefGoogle Scholar
  26. Collatz GJ, Ribas-Carbó M, Berry JA (1992) Coupled photosynthesis-stomatal model for leaves of C4 plants. Aust J Plant Physiol 19:519–538Google Scholar
  27. Cramer W, Bondeau A, Woodward FI, Prentice C, Betts RA, Brovkin V, Cox PM, Fisher V, Foley JA, Friend AD, Kucharik C, Lomas MR, Ramankutty N, Sitch S, Smith B, White A, Young-Molling C (2001) Global response of terrestrial ecosystem structure and function to CO2 and climate change: results from six dynamic global vegetation models. Global Change Biol 7:357–373CrossRefGoogle Scholar
  28. DiMario RJ, Quebedeaux JC, Longstreth DJ, Dassanayake M, Hartman MM, Moroney JV (2016) The cytoplasmic carbonic anhydrases βCA2 and βCA4 are required for optimal plant growth at low CO2. Plant Physiol 171:280–293CrossRefPubMedPubMedCentralGoogle Scholar
  29. Douthe C, Dreyer E, Brendel O, Warren CR (2012) Is mesophyll conductance to CO2 in leaves of three Eucalyptus species sensitive to short-term changes of irradiance under ambient as well as low O2? Funct Plant Biol 38:434–447Google Scholar
  30. Drewry DT, Kumar P, Long S, Bernacchi C, Liang XZ, Sivapalan M (2010) Ecohydrological responses of dense canopies to environmental variability: 1. Interplay between vertical structure and photosynthetic pathway. J Geophys Res 115:G04022Google Scholar
  31. Ellsworth DS, Crous KY, Lambers H, Cooke J (2015) Phosphorus recycling in photorespiration maintains high photosynthetic capacity in woody species. Plant Cell Environ 38:1142–1156CrossRefPubMedGoogle Scholar
  32. Ethier GJ, Livingston NJ (2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant Cell Environ 27(2):137–153CrossRefGoogle Scholar
  33. Evans JR, von Caemmerer S (1996) Carbon dioxide diffusion inside leaves. Plant Physiol 110(2):339–346CrossRefPubMedPubMedCentralGoogle Scholar
  34. Evans JR, von Caemmerer S (2013) Temperature response of carbon isotope discrimination and mesophyll conductance in tobacco. Plant Cell Environ 36:745–756CrossRefPubMedGoogle Scholar
  35. Evans JR, Sharkey TD, Berry JA, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas-exchange to investigate CO2 diffusion in leaves of higher-plants. Aust J Plant Physiol 13(2):281–292Google Scholar
  36. Evans JR, von Caemmerer S, Setchell BA, Hudson GS (1994) The relationship between CO2 transfer conductance and leaf anatomy in transgenic tobacco with a reduced content of Rubisco. Aust J Plant Physiol 21(4):475–495Google Scholar
  37. Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) Resistances along the CO2 diffusion pathway inside leaves. J Exp Bot 60(8):2235–2248CrossRefPubMedGoogle Scholar
  38. Everson RG (1970) Carbonic anhydrase and CO2 fixation in intact chloroplasts. Phytochemistry 9:25–32CrossRefGoogle Scholar
  39. Fabre N, Reiter IM, Becuwe-Linka N, Genty B, Rumeau D (2007) Characterization and expression analysis of genes encoding alpha and beta carbonic anhydrases in Arabidopsis. Plant Cell Environ 30:617–629CrossRefPubMedGoogle Scholar
  40. Farquhar GD (1979) Models describing the kinetics of ribulose bisphosphate carboxylase-oxygenase. Arch Biochem Biophys 193:456–468CrossRefPubMedGoogle Scholar
  41. Farquhar GD (1983) On the nature of carbon isotope discrimination in C4 species. Aust J Plant Physiol 10(2):205–226Google Scholar
  42. Farquhar GD, Busch FA (2017) Changes in the chloroplastic CO2 concentration explain much of the observed Kok effect: a model. New Phytol 214:570–584CrossRefPubMedGoogle Scholar
  43. Farquhar GD, Cernusak LA (2012) Ternary effects on the gas exchange of isotopologues of carbon dioxide. Plant Cell Environ 35(7):1221–1231CrossRefPubMedGoogle Scholar
  44. Farquhar GD, Lloyd J (1993) Carbon and oxygen isotope effects in the exchange of carbon dioxide between terrestrial plants and the atmosphere. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon-water relations. Academic Press, San Diego, pp 47–70CrossRefGoogle Scholar
  45. Farquhar G, von Caemmerer S (1982) Modelling of photosynthetic responses to environmental conditions. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Physiological Plant ecology II. Encyclopedia of plant physiology, new series, vol 12B. Springer-Verlag, Heidelberg, pp 550–587Google Scholar
  46. Farquhar GD, Wong S-C (1984) An empirical model of stomatal conductance. Aust J Plant Physiol 11:191–210Google Scholar
  47. Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical-model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149(1):78–90CrossRefPubMedGoogle Scholar
  48. Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9(2):121–137Google Scholar
  49. Flexas J, Díaz-Espejo A, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbó M (2007) Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant Cell Environ 30(10):1284–1298CrossRefPubMedGoogle Scholar
  50. Flexas J, Ribas-Carbó M, Díaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31(5):602–621CrossRefPubMedGoogle Scholar
  51. Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriquí M, Díaz-Espejo A, Douthe C, Dreyer E, Ferrio JP, Gago J, Gallé A, Galmés J, Kodama N, Medrano H, Niinemets Ü, Peguero-Pina JJ, Pou A, Ribas-Carbó M, Tomás M, Tosens T, Warren CR (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Sci 193–194:70–84CrossRefPubMedGoogle Scholar
  52. Gaastra P (1959) Photosynthesis of crop plants as influenced by light, carbon dioxide, temperature and stomatal diffusion resistance. Meded Landbouwhogeschool Wageningen 59:1–68Google Scholar
  53. Gauhl E, Björkman O (1969) Simultaneous measurements on the effect of oxygen concentration on water vapor and carbon dioxide exchange. Planta 88:187–191CrossRefPubMedGoogle Scholar
  54. Genty B, Meyer S, Piel C, Badeck F, Liozon R (1998) CO2 diffusion inside leaf mesophyll of ligneous plants. In: Garab G (ed) Photosynthesis: mechanisms and effects. Kluwer Academic, Dordrecht, pp 3961–3966CrossRefGoogle Scholar
  55. Ghannam AF, Tsen W, Rowlett RS (1986) Activation parameters for the carbonic anhydrase II-catalyzed hydration of CO2. J Biol Chem 261:1164–1169PubMedGoogle Scholar
  56. Gillon JS, Griffiths H (1997) The influence of (photo)respiration on carbon isotope discrimination in plants. Plant Cell Environ 20(10):1217–1230CrossRefGoogle Scholar
  57. Gillon JS, Yakir D (2000a) Internal conductance to CO2 diffusion and C18OO discrimination in C3 leaves. Plant Physiol 123(1):201–213CrossRefPubMedPubMedCentralGoogle Scholar
  58. Gillon JS, Yakir D (2000b) Naturally low carbonic anhydrase activity in C4 and C3 plants limits discrimination against C18OO during photosynthesis. Plant Cell Environ 23:903–915CrossRefGoogle Scholar
  59. Gu L, Sun Y (2014) Artefactual responses of mesophyll conductance to CO2 and irradiance estimated with the variable J and online isotope discrimination methods. Plant Cell Environ 37:1231–1249CrossRefPubMedGoogle Scholar
  60. Gu L, Pallard SG, Tu K, Law BE, Wullschleger SD (2010) Reliable estimation of biochemical parameters from C3 leaf photosynthesis-intercellular carbon dioxide response curves. Plant Cell Environ 33:1852–1874CrossRefPubMedGoogle Scholar
  61. Hall AE, Björkman O (1975) A model of leaf photosynthesis and respiration. In: Gates D, Schmerl R (eds) Perspectives of biophysical ecology, ecological Studies, vol 12. Springer, Berlin, pp 55–72CrossRefGoogle Scholar
  62. Harley PC, Sharkey TD (1991) An improved model of C3 photosynthesis at high CO2: reversed O2 sensitivity explained by lack of glycerate reentry into the chloroplast. Photosynth Res 27:169–178PubMedGoogle Scholar
  63. Harley PC, Loreto F, Di Marco G, Sharkey TD (1992a) Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiol 98(4):1429–1436CrossRefPubMedPubMedCentralGoogle Scholar
  64. Harley PC, Thomas RB, Reynolds JF, Strain BR (1992b) Modelling photosynthesis of cotton grown in elevated CO2. Plant Cell Environ 15:271–282CrossRefGoogle Scholar
  65. Hatakeyama Y, Ueno O (2016) Intracellular position of mitochondria and chloroplasts in bundle sheath and mesophyll cells of C3 grasses in relation to photorespiratory CO2 loss. Plant Prod Sci 19:540–551CrossRefGoogle Scholar
  66. Holloway-Phillips M, Cernusak LA, Barbour MM, Song X, Cheesman A, Munksgaard N, Stuart-Williams H, Farquhar GD (2016) Leaf vein fraction influences the Péclet effect and 18O enrichment in leaf water. Plant Cell Environ 39:2414–2427CrossRefPubMedGoogle Scholar
  67. Huzisige H, Ke B (1993) Dynamics of the history of photosynthesis research. Photosynth Res 38:185–209CrossRefPubMedGoogle Scholar
  68. Jordan DB, Ogren WL (1984) The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase: dependence on ribulosebisphosphate concentration, pH and temperature. Planta 161:308–313CrossRefPubMedGoogle Scholar
  69. June T, Evans JR, Farquhar GD (2004) A simple new equation for the reversible temperature dependence of photosynthetic electron transport: a study on soybean leaf. Funct Plant Biol 31:275–283CrossRefGoogle Scholar
  70. Kattge J, Knorr W (2007) Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species. Plant Cell Environ 30:1176–1190CrossRefPubMedGoogle Scholar
  71. Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch HJ, Rosenkranz R, Stäbler N, Schönfeld B, Kreuzaler F, Peter-Hänsel C (2007) Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat Biotechnol 25:593–599CrossRefPubMedGoogle Scholar
  72. Laing WA, Ogren WL, Hageman R (1974) Regulation of soybean net photosynthetic CO2 fixation by the interaction of CO2, O2 and ribulose-1,5 diphosphate carboxylase. Plant Physiol 54:678–685CrossRefPubMedPubMedCentralGoogle Scholar
  73. Laisk A (1977) Kinetics of photosynthesis and photorespiration in C3 Plants. Nauka, Moscow, RussiaGoogle Scholar
  74. Lanigan GJ, Betson N, Griffiths H, Seibt U (2008) Carbon isotope fractionation during photorespiration and carboxylation in Senecio. Plant Physiol 148(4):2013–2020CrossRefPubMedPubMedCentralGoogle Scholar
  75. Leuning R (1990) Modelling stomatal behaviour and photosynthesis in Eucalyptus grandis. Aust J Plant Physiol 17:159–175Google Scholar
  76. Leuning R (2002) Temperature dependence of two parameters in a photosynthesis model. Plant Cell Environ 25:1205–1210CrossRefGoogle Scholar
  77. Lloyd J, Grace J, Miranda AC, Meir P, Wong SC, Miranda HS, Wright IR, Gash JHC, Mcintyre J (1995) A simple calibrated model of Amazon rainforest productivity based on leaf biochemical properties. Plant Cell Environ 18:1129–1145CrossRefGoogle Scholar
  78. Lombardozzi DL (2018) Triose phosphate limitation in photosynthesis models reduces leaf photosynthesis and global terrestrial carbon storage. Environ Res Lett 13:074025CrossRefGoogle Scholar
  79. Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot 54(392):2393–2401CrossRefPubMedGoogle Scholar
  80. Loreto F, Harley PC, Dimarco G, Sharkey TD (1992) Estimation of mesophyll conductance to CO2 flux by three different methods. Plant Physiol 98(4):1437–1443CrossRefPubMedPubMedCentralGoogle Scholar
  81. Loucos KE, Simonin KA, Barbour MM (2017) Leaf hydraulic conductance and mesophyll conductance are not closely related within a single species. Plant Cell Environ 40:203–215CrossRefPubMedGoogle Scholar
  82. McMurtrie RE, Wang YP (1993) Mathematical models of the photosynthetic response of tree stands to rising CO2 concentrations and temperature. Plant Cell Environ 16:1–13CrossRefGoogle Scholar
  83. Medvigy D, Wofsy SC, Munger JW, Hollinger DY, Moorcroft PR (2009) Mechanistic scaling of ecosystem function and dynamics in space and time: ecosystem demography model version 2∑. J Geophys Res 114,:G01002CrossRefGoogle Scholar
  84. Niemietz CM, Tyerman SD (1997) Characterization of water channels in wheat root membrane vesicles. Plant Physiol 115:561–567CrossRefPubMedPubMedCentralGoogle Scholar
  85. Ogée J, Wingate L, Genty B (2018) Mesophyll conductance from C18OO discrimination. Plant Physiol DOI.  https://doi.org/10.1104/pp.17.01031 CrossRefGoogle Scholar
  86. Parkhurst DF, Mott KA (1990) Intercellular diffusion limits to CO2 uptake in leaves: studies in air and helox. Plant Physiol 94:1024–1032CrossRefPubMedPubMedCentralGoogle Scholar
  87. Peguero-Pina JJ, Flexas J, Galmés J, Niinemets U, Sancho-Knapik D, Barredo G, Villarroya D, Gil-Pelegrín E (2012) Leaf anatomical properties in relation to differences in mesophyll conductance to CO2 and photosynthesis in two related Mediterranean Abies species. Plant Cell Environ 35:2121–2129CrossRefPubMedGoogle Scholar
  88. Peisker M (1974) A model describing the influence of oxygen on photosynthetic carboxylation. Photosynthetica 8:47–50Google Scholar
  89. Peisker M, Apel H (2001) Inhibition by light of CO2 evolution from dark respiration: comparison of two gas exchange methods. Photosynth Res 70:291–298CrossRefPubMedGoogle Scholar
  90. Penman HL, Schofield RK (1951) Some physical aspects of assimilation and transpiration. Symp Soc Exp Biol 5:115–129Google Scholar
  91. Pitman AJ (2003) The evolution of, and revolution in, land surface schemes designed for climate models. Int J Climatol 23:479–510CrossRefGoogle Scholar
  92. Pons TL, Flexas J, von Caemmerer S, Evans JR, Genty B, Ribas-Carbó M, Brugnoli E (2009) Estimating mesophyll conductance to CO2: methodology, potential errors, and recommendations. J Exp Bot 60(8):2217–2234CrossRefPubMedGoogle Scholar
  93. Price GD, Badger MR, von Caemmerer S (2011) The prospect of using cyanobacterial bicarbonate transporters to improve leaf photosynthesis in C3 crop plants. Plant Physiol 155:20–26CrossRefPubMedGoogle Scholar
  94. Rogers A, Medlyn BE, Dukes JS (2014) Improving representation of photosynthesis in earth system models. New Phytol 204:12–14CrossRefPubMedGoogle Scholar
  95. Rooney MA (1988) Short-term carbon isotope fractionation by plants. PhD thesis, University of Wisconsin, Madison, WI, USAGoogle Scholar
  96. Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30:1086–1106CrossRefPubMedGoogle Scholar
  97. Sage TL, Sage RF (2009) The functional anatomy of rice leaves: implications for refixation of photorespiratory CO2 and efforts to engineer C4 photosynthesis into rice. Plant Cell Physiol 50:756–772CrossRefPubMedGoogle Scholar
  98. Sanyal G, Maren TH (1981) Thermodynamics of carbonic anhydrase catalysis: a comparison between human isoenzymes B and C. J Biol Chem 256:608–612PubMedGoogle Scholar
  99. Sellers PJ, Randall DA, Collatz GJ, Berry JA, Field CB, Dazlich DA, Zhang C, Collelo GD, Bounoua L (1996) A revised land surface parameterization (SiB2) for atmospheric GCMs. Part 1: model formulation. J Clim 9:676–705CrossRefGoogle Scholar
  100. Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Bot Rev 51:53–105CrossRefGoogle Scholar
  101. Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30(9):1035–1040CrossRefPubMedGoogle Scholar
  102. Song X, Loucos KE, Simonin KA, Farquhar GD, Barbour MM (2014) Measurements of transpiration isotopologues and leaf water to assess enrichment models in cotton. New Phytol 206:637–646CrossRefGoogle Scholar
  103. Stryer L (1988) Biochemistry. W. H. Freeman, New YorkGoogle Scholar
  104. Sun Y, G L, Norby EDR, Pallardy RJ, Hoffman SG FM (2014) Impact of mesophyll diffusion on estimated global land CO2 fertilization. Proc Natl Acad Sci USA 111:15774–15779CrossRefPubMedGoogle Scholar
  105. Syvertsen JP, Lloyd J, McConchie C, Kriedemann PE, Farquhar GD (1995) On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves. Plant Cell Environ 18(2):149–157CrossRefGoogle Scholar
  106. Tazoe Y, von Caemmerer S, Estavillo GM, Evans JR (2011) Using tunable diode laser spectroscopy to measure carbon isotope discrimination and mesophyll conductance to CO2 diffusion dynamically at different CO2 concentrations. Plant Cell Environ 34:580–591CrossRefPubMedGoogle Scholar
  107. Tcherkez G (2006) How large is the carbon isotope fractionation of the photorespiratory enzyme glycine decarboxylase? Funct Plant Biol 33(10):911–920CrossRefGoogle Scholar
  108. Tcherkez G, Cornic G, Bligny R, Gout E, Ghashghaie J (2005) In vivo respiratory metabolism of illuminated leaves. Plant Physiol 138(3):1596–1606CrossRefPubMedPubMedCentralGoogle Scholar
  109. Tcherkez G, Boex-Fontvieille E, Mahé A, Hodges M (2012) Respiratory carbon fluxes in leaves. Curr Opin Plant Biol 15:308–314CrossRefPubMedGoogle Scholar
  110. Terashima I, Hanba YT, Tholen D, Niinemets U (2011) Leaf functional anatomy in relation to photosynthesis. Plant Physiol 155:108–116CrossRefPubMedGoogle Scholar
  111. Tholen D, Zhu XG (2011) The mechanistic basis of internal conductance: a theoretical analysis of mesophyll cell photosynthesis and CO2 diffusion. Plant Physiol 156:90–105CrossRefPubMedPubMedCentralGoogle Scholar
  112. Tholen D, Ethier G, Genty B, Pepin S, Zhu XG (2012) Variable mesophyll conductance revisited. Theoretical background and experimental implications. Plant Cell Environ 35:2087–2103CrossRefPubMedGoogle Scholar
  113. Tholen D, Ethier G, Genty B (2014) Mesophyll conductance with a twist. Plant Cell Environ 37:2456–2458CrossRefPubMedGoogle Scholar
  114. Tomás M, Flexas J, Copolovici L, Galmés J, Hallik L, Medrano HL, Ribas-Carbó M, Tosens T, Vislap V, Niinemets U (2013) Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models. J Exp Bot 64(8):2269–2281CrossRefPubMedPubMedCentralGoogle Scholar
  115. Tosens T, Niinemets U, Vislap V, Eichelmann H, Castro Díez P (2012) Developmental changes in mesophyll diffusion conductance and photosynthetic capacity under different light and water availabilities in Populus tremula: how structure constrains function. Plant Cell Environ 35:839–856CrossRefPubMedGoogle Scholar
  116. Ubierna N, Farquhar GD (2014) Advances in measurements and models of photosynthetic carbon isotope discrimination in C3 plants. Plant Cell Environ 37:1494–1498CrossRefPubMedGoogle Scholar
  117. Ubierna N, Marshall JD (2011) Estimation of canopy average mesophyll conductance using δ13C of phloem contents. Plant Cell Environ 34:1521–1535CrossRefPubMedGoogle Scholar
  118. Ubierna N, Gandin A, Boyd RA, Cousins AB (2017) Temperature response of mesophyll conductance in three C4 species calculated with two methods: 18O discrimination and in-vitro V pmax. Corrigendum-New Phytol 214:66–80.  https://doi.org/10.1111/nph.14922 CrossRefGoogle Scholar
  119. Ubierna N, Holloway-Phillips MM, Farquhar GD (2018) Using stable carbon isotopes to study C3 and C4 photosynthesis: models and calculations. In: Covshoff S (ed) Photosynthesis. Methods in molecular biology, vol 1770. Humana Press, New York, pp 155–196Google Scholar
  120. Uehlein N, Otto B, Hanson DT, Fischer M, McDowell N, Kaldenhoff R (2008) Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. Plant Cell 20:648–657CrossRefPubMedPubMedCentralGoogle Scholar
  121. von Caemmerer S (1989) A model of photosynthetic CO2 assimilation and carbon isotope discrimination in leaves of certain C3-C4 intermediate species. Planta 178:463–474CrossRefGoogle Scholar
  122. von Caemmerer S (1992) Carbon isotope discrimination in C3-C4 intermediates. Plant Cell Environ 15:1063–1072CrossRefGoogle Scholar
  123. von Caemmerer S (2000) Biochemical models of leaf photosynthesis. CSIRO publishing, CollingwoodCrossRefGoogle Scholar
  124. von Caemmerer S (2003) C4 photosynthesis in a single C3 cell is theoretically inefficient but may ameliorate internal CO2 diffusion limitations of C3 leaves. Plant Cell Environ 26:1191–1197CrossRefGoogle Scholar
  125. von Caemmerer S (2013) Steady-state models of photosynthesis. Plant Cell Environ 36:1617–1630CrossRefGoogle Scholar
  126. von Caemmerer S, Evans JR (1991) Determination of the average partial-pressure of CO2 in chloroplasts from leaves of several C3 plants. Aust J Plant Physiol 18(3):287–305Google Scholar
  127. von Caemmerer S, Evans JR (2015) Temperature responses of mesophyll conductance differ greatly between species. Plant Cell Environ 38:629–637CrossRefGoogle Scholar
  128. von Caemmerer S, Furbank RT (1999) Modeling of C4 photosynthesis. In: Monson RFSR (ed) C4 Plant biology. Academic Press, San Diego, pp 169–207Google Scholar
  129. von Caemmerer S, Evans JR, Hudson GS, Andrews TJ (1994) The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco. Planta 195:88–97CrossRefGoogle Scholar
  130. Walker B, Ariza LS, Kaines S, Badger MR, Cousins AB (2013) Temperature response of in vivo Rubisco kinetics and mesophyll conductance in Arabidopsis thaliana: comparisons to Nicotiana tabacum. Plant Cell Environ 36:2108–2119CrossRefPubMedGoogle Scholar
  131. Wareing PF, Khalifa MM, Treharne KJ (1968) Rate-limiting processes in photosynthesis at saturating light intensities. Nature 220:453–457CrossRefPubMedGoogle Scholar
  132. Warren CR, Ethier GJ, Livingston NJ, Grant NJ, Turpin DH, Harrison DL, Black TA (2003) Transfer conductance in second growth Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) canopies. Plant Cell Environ 26(8):1215–1227CrossRefGoogle Scholar
  133. Wingate L, Seibt U, Moncrieff JB, Jarvis PG, Lloyd J (2007) Variations in 13C discrimination during CO2 exchange by Picea sitchensis branches in the field. Plant Cell Environ 30(5):600–616CrossRefPubMedGoogle Scholar
  134. Wittig VE, Bernacchi CJ, Zhu XG, Calfapietra C, Ceulemans R, DeAngelis P, Gielen B, Miglietta F, Morgan PB, Long SP (2005) Gross primary production is stimulated for three Populus species grown under free-air CO2 enrichment from planting through canopy closure. Global Change Biol 11:644–656CrossRefGoogle Scholar
  135. Xiong D, Liu X, Liu L, Douthe C, LI Y, Peng S, Huang J (2015) Rapid responses of mesophyll conductance to changes of CO2 concentration, temperature and irradiance are affected by N supplements in rice. Plant Cell Environ 38:2541–2550CrossRefPubMedGoogle Scholar
  136. Yin X, Struik PC (2009) Theoretical reconsiderations when estimating the mesophyll conductance to CO2 diffusion in leaves of C3 plants by analysis of combined gas exchange and chlorophyll fluorescence measurements. Plant Cell Environ 32:1513–1524 (with corrigendum in 1533:1595)CrossRefPubMedGoogle Scholar
  137. Yin X, Struik PC (2017) Simple generalisation of a mesophyll resistance model for various intracellular arrangements of chloroplasts and mitochondria in C3 leaves. Photosynth Res 132:211–220CrossRefPubMedPubMedCentralGoogle Scholar
  138. Yin X, van Oijen M, Schapendonk AHCM (2004) Extension of a biochemical model for the generalized stoichiometry of electron transport limited C3 photosynthesis. Plant Cell Environ 27:1211–1222CrossRefGoogle Scholar
  139. Yin X, Harbinson J, Struik PC (2006) Mathematical review of literature to assess alternative electron transports and interphotosystem excitation partitioning of steady-state C3 photosynthesis under limiting light. Plant Cell Environ 29:1771–1782 (with corrigendum in Plant, Cell and Environment 1729: 2252)CrossRefPubMedGoogle Scholar
  140. Yin X, Harbinson J, Struik PC (2009a) A model of the generalised stoichiometry of electron transport limited C3 photosynthesis: development and application. In: Laisk A, Nedbal L, Govindjee (eds) Photosynthesis in silico. Understanding complexity from molecules to ecosystems. Springer, Dordrecht, pp 247–273Google Scholar
  141. Yin X, Struik PC, Romero P, Harbinson J, Evers JB, Van Der Putten PEL, Vos J (2009b) Using combined measurements of gas exchange and chlorophyll fluorescence to estimate parameters of a biochemical C3 photosynthesis model: a critical appraisal and a new integrated approach applied to leaves in a wheat (Triticum aestivum) canopy. Plant Cell Environ 32:448–464CrossRefPubMedGoogle Scholar
  142. Zhu XG, Portis AR, Long SP (2004) Would transformation of C3 crop plants with foreign Rubisco increase productivity? A computational analysis extrapolating from kinetic properties to canopy photosynthesis. Plant Cell Environ 27:155–165CrossRefGoogle Scholar
  143. Zhu XG, Long SP, Ort DR (2008) What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Curr Opin Biotech 19:153–159CrossRefPubMedGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Research School of BiologyAustralian National UniversityActonAustralia
  2. 2.College of Science and EngineeringJames Cook UniversityCairnsAustralia
  3. 3.School of Biological Sciences, Molecular Plant SciencesWashington State UniversityPullmanUSA

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