Advertisement

A generalised dynamic model of leaf-level C3 photosynthesis combining light and dark reactions with stomatal behaviour

  • Chandra Bellasio
Original Article
  • 152 Downloads

Abstract

Global food demand is rising, impelling us to develop strategies for improving the efficiency of photosynthesis. Classical photosynthesis models based on steady-state assumptions are inherently unsuitable for assessing biochemical and stomatal responses to rapid variations in environmental drivers. To identify strategies to increase photosynthetic efficiency, we need models that account for the timing of CO2 assimilation responses to dynamic environmental stimuli. Herein, I present a dynamic process-based photosynthetic model for C3 leaves. The model incorporates both light and dark reactions, coupled with a hydro-mechanical model of stomatal behaviour. The model achieved a stable and realistic rate of light-saturated CO2 assimilation and stomatal conductance. Additionally, it replicated complete typical assimilatory response curves (stepwise change in CO2 and light intensity at different oxygen levels) featuring both short lag times and full photosynthetic acclimation. The model also successfully replicated transient responses to changes in light intensity (light flecks), CO2 concentration, and atmospheric oxygen concentration. This dynamic model is suitable for detailed ecophysiological studies and has potential for superseding the long-dominant steady-state approach to photosynthesis modelling. The model runs as a stand-alone workbook in Microsoft® Excel® and is freely available to download along with a video tutorial.

Keywords

Mechanistic model Microsoft® Excel® Stomatal model Time Transients Stomatal conductance Assimilation Photorespiration Light fleck 

Notes

Acknowledgements

I am deeply grateful to the Editor of this special issue, Nerea Ubierna Lopez, for editing that improved the clarity and readability, to Joe Quirk for a substantial contribution to writing the first version, I thank Ross Deans (Australian National University, ANU) for unpublished spinach leaf gas exchange data, and Florian Busch (ANU) for help, review, and critical discussion. I am funded through a H2020 Marie Skłodowska-Curie individual fellowship (DILIPHO, ID: 702755).

Compliance with ethical standards

Conflict of interest

I have no conflict of interest.

Supplementary material

11120_2018_601_MOESM1_ESM.pdf (186 kb)
Supplementary material 1 (PDF 186 KB)
11120_2018_601_MOESM2_ESM.xlsm (350 kb)
Supplementary material 2 (XLSM 350 KB)

References

  1. Allen WA, Richardson AJ (1968) Interaction of light with a plant canopy. J Opt Soc Am 58(8):1023–1028.  https://doi.org/10.1364/Josa.58.001023 CrossRefGoogle Scholar
  2. Beerling DJ (2015) Gas valves, forests and global change: a commentary on Jarvis (1976) ‘The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field’. Philos Trans R Soc B.  https://doi.org/10.1098/rstb.2014.0311 CrossRefGoogle Scholar
  3. Bellasio C (2017) A generalised stoichiometric model of C3, C2, C2 + C4, and C4 photosynthetic metabolism. J Exp Bot 68(2):269–282.  https://doi.org/10.1093/jxb/erw303 CrossRefPubMedGoogle Scholar
  4. Bellasio C, Griffiths H (2014) The operation of two decarboxylases (NADPME and PEPCK), transamination and partitioning of C4 metabolic processes between mesophyll and bundle sheath cells allows light capture to be balanced for the maize C4 pathway. Plant Physiol 164:466–480.  https://doi.org/10.1111/pce.12194 CrossRefPubMedGoogle Scholar
  5. Bellasio C, Burgess SJ, Griffiths H, Hibberd JM (2014) A high throughput gas exchange screen for determining rates of photorespiration or regulation of C4 activity. J Exp Bot 65(13):3769–3779.  https://doi.org/10.1093/jxb/eru238 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bellasio C, Beerling DJ, Griffiths H (2016a) Deriving C4 photosynthetic parameters from combined gas exchange and chlorophyll fluorescence using an Excel tool: theory and practice. Plant Cell Environment 39(6):1164–1179.  https://doi.org/10.1111/pce.12626 CrossRefGoogle Scholar
  7. Bellasio C, Beerling DJ, Griffiths H (2016b) An Excel tool for deriving key photosynthetic parameters from combined gas exchange and chlorophyll fluorescence: theory and practice. Plant Cell Environ 39(6):1180–1197.  https://doi.org/10.1111/pce.12560 CrossRefPubMedGoogle Scholar
  8. Bellasio C, Quirk J, Buckley TN, Beerling D (2017) A dynamic hydro-mechanical and biochemical model of stomatal conductance for C4 photosynthesis. Plant Physiol.  https://doi.org/10.1104/pp.17.00666 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Berry JA, Beerling DJ, Franks PJ (2010) Stomata: key players in the earth system, past and present. Curr Opin Plant Biol 13(3):232–239.  https://doi.org/10.1016/j.pbi.2010.04.013 CrossRefGoogle Scholar
  10. Bonan GB, Williams M, Fisher RA, Oleson KW (2014) Modeling stomatal conductance in the earth system: linking leaf water-use efficiency and water transport along the soil–plant–atmosphere continuum. Geosci Model Dev 7(5):2193–2222.  https://doi.org/10.5194/gmd-7-2193-2014 CrossRefGoogle Scholar
  11. Buckley TN (2017) Modeling stomatal conductance. Plant Physiol.  https://doi.org/10.1104/pp.16.01772 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Buckley TN, Mott KA, Farquhar GD (2003) A hydromechanical and biochemical model of stomatal conductance. Plant Cell Environ 26(10):1767–1785.  https://doi.org/10.1046/j.1365-3040.2003.01094.x CrossRefGoogle Scholar
  13. Busch FA (2014) Opinion: the red-light response of stomatal movement is sensed by the redox state of the photosynthetic electron transport chain. Photosynth Res 119(1–2):131–140.  https://doi.org/10.1007/s11120-013-9805-6 CrossRefPubMedGoogle Scholar
  14. 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(3):1036–1051.  https://doi.org/10.1111/nph.14258 CrossRefPubMedGoogle Scholar
  15. Busch FA, Sage RF, Farquhar GD (2017) Plants increase CO2 uptake by assimilating nitrogen via the photorespiratory pathway. Nat Plants.  https://doi.org/10.1038/s41477-017-0065-x CrossRefPubMedGoogle Scholar
  16. Damour G, Simonneau T, Cochard H, Urban L (2010) An overview of models of stomatal conductance at the leaf level. Plant Cell Environ 33(9):1419–1438.  https://doi.org/10.1111/j.1365-3040.2010.02181.x CrossRefPubMedGoogle Scholar
  17. Davis PA, Caylor S, Whippo CW, Hangarter RP (2011) Changes in leaf optical properties associated with light-dependent chloroplast movements. Plant Cell Environ 34(12):2047–2059CrossRefGoogle Scholar
  18. Driever SM, Simkin AJ, Alotaibi S, Fisk SJ, Madgwick PJ, Sparks CA, Jones HD, Lawson T, Parry MAJ, Raines CA (2017) Increased SBPase activity improves photosynthesis and grain yield in wheat grown in greenhouse conditions. Philos Trans R Soc B.  https://doi.org/10.1098/rstb.2016.0384 CrossRefGoogle Scholar
  19. Farquhar G, Wong S (1984) An empirical model of stomatal conductance. Funct Plant Biol 11(3):191–210.  https://doi.org/10.1071/PP9840191 CrossRefGoogle Scholar
  20. Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical-model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149(1):78–90.  https://doi.org/10.1007/bf00386231 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Foyer CH, Lelandais M, Harbinson J (1992) Control of the quantum efficiencies of photosystems I and II, electron flow, and enzyme activation following dark-to-light transitions in pea leaves: relationship between NADP/NADPH ratios and NADP-malate dehydrogenase activation state. Plant Physiol 99(3):979–986CrossRefGoogle Scholar
  22. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63(4):1637–1661.  https://doi.org/10.1093/jxb/ers013 CrossRefPubMedGoogle Scholar
  23. Gross LJ (1982) Photosynthetic dynamics in varying light environments: a model and its application to whole leaf carbon gain. Ecology 63(1):84–93CrossRefGoogle Scholar
  24. Gross LJ, Kirschbaum MUF, Pearcy RW (1991) A dynamic-model of photosynthesis in varying light taking account of stomatal conductance, C3-cycle intermediates, photorespiration and rubisco activation. Plant Cell Environ 14(9):881–893.  https://doi.org/10.1111/j.1365-3040.1991.tb00957.x CrossRefGoogle Scholar
  25. Heineke D, Riens B, Grosse H, Hoferichter P, Peter U, Flügge U-I, Heldt HW (1991) Redox transfer across the inner chloroplast envelope membrane. Plant Physiol 95(4):1131–1137CrossRefGoogle Scholar
  26. Hendrey G, Long S, McKee I, Baker N (1997) Can photosynthesis respond to short-term fluctuations in atmospheric carbon dioxide? Photosynth Res 51(3):179–184CrossRefGoogle Scholar
  27. Ho QT, Berghuijs HNC, WattÉ R, Verboven P, Herremans ELS, Yin X, Retta MA, Aernouts BEN, Saeys W, Helfen L, Farquhar GD, Struik PC, NicolaÏ BM (2015) Three-dimensional microscale modelling of CO2 transport and light propagation in tomato leaves enlightens photosynthesis. Plant Cell Environ.  https://doi.org/10.1111/pce.12590 CrossRefPubMedGoogle Scholar
  28. Ishikawa N, Takabayashi A, Sato F, Endo T (2016) Accumulation of the components of cyclic electron flow around photosystem I in C4 plants, with respect to the requirements for ATP. Photosynth Res.  https://doi.org/10.1007/s11120-016-0251-0 CrossRefPubMedGoogle Scholar
  29. Joliot P, Johnson GN (2011) Regulation of cyclic and linear electron flow in higher plants. Proc Natl Acad Sci 108(32):13317–13322.  https://doi.org/10.1073/pnas.1110189108 CrossRefPubMedGoogle Scholar
  30. Kaiser E, Morales A, Harbinson J, Kromdijk J, Heuvelink E, Marcelis LFM (2014) Dynamic photosynthesis in different environmental conditions. J Exp Bot.  https://doi.org/10.1093/jxb/eru406 CrossRefPubMedGoogle Scholar
  31. Kirschbaum M, Küppers M, Schneider H, Giersch C, Noe S (1997) Modelling photosynthesis in fluctuating light with inclusion of stomatal conductance, biochemical activation and pools of key photosynthetic intermediates. Planta 204(1):16–26CrossRefGoogle Scholar
  32. Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155(1):70–78.  https://doi.org/10.1104/pp.110.166652 CrossRefPubMedGoogle Scholar
  33. Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354(6314):857–861.  https://doi.org/10.1126/science.aai8878 CrossRefPubMedGoogle Scholar
  34. Laisk A, Edwards GE (2000) A mathematical model of C4 photosynthesis: the mechanism of concentrating CO2 in NADP-malic enzyme type species. Photosynth Res 66(3):199–224.  https://doi.org/10.1023/a:1010695402963 CrossRefPubMedGoogle Scholar
  35. Laisk A, Edwards G (2009) Leaf C4 photosynthesis in silico: the CO2 concentrating mechanism. In: Laisk A, Nedbal L, Govindjee (eds) Photosynthesis in silico, vol 29. Advances in photosynthesis and respiration. Springer, Amsterdam, pp 323–348.  https://doi.org/10.1007/978-1-4020-9237-4_14 CrossRefGoogle Scholar
  36. Laisk A, Eichelmann H (1989) Towards understanding oscillations: a mathematical model of the biochemistry of photosynthesis. Phil Trans R Soc Lond B 323(1216):369–384CrossRefGoogle Scholar
  37. Laisk A, Eichelmann H, Oja V, Eatherall A, Walker DA (1989) A mathematical model of the carbon metabolism in photosynthesis. Difficulties in explaining oscillations by fructose 2, 6-bisphosphate regulation. Proc R Soc Lond B 237(1289):389–415CrossRefGoogle Scholar
  38. Laisk A, Siebke K, Gerst U, Eichelmann H, Oja V, Heber U (1991) Oscillations in photosynthesis are initiated and supported by imbalances in the supply of ATP and NADPH to the Calvin cycle. Planta 185(4):554–562.  https://doi.org/10.1007/bf00202966 CrossRefPubMedGoogle Scholar
  39. Laisk A, Eichelmann H, Oja V (2009) Leaf C3 photosynthesis in silico: integrated carbon/nitrogen metabolism. In: Laisk A, Nedbal L, Govindjee (eds) Photosynthesis in silico, vol 29. Advances in photosynthesis and respiration. Springer, Amsterdam, pp 295–322.  https://doi.org/10.1007/978-1-4020-9237-4_13 CrossRefGoogle Scholar
  40. Lawlor DW (1993) Photosynthesis: molecular, physiological and environmental processes, 2nd edn. Longman Scientific & Technical, HarlowGoogle Scholar
  41. Lawson T, Blatt MR (2014) Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol 164(4):1556–1570.  https://doi.org/10.1104/pp.114.237107 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Lehmeier C, Pajor R, Lundgren MR, Mathers A, Sloan J, Bauch M, Mitchell A, Bellasio C, Green A, Bouyer D, Schnittger A, Sturrock C, Osborne CP, Rolfe S, Mooney S, Fleming AJ (2017) Cell density and airspace patterning in the leaf can be manipulated to increase leaf photosynthetic capacity. Plant J 92(6):981–994.  https://doi.org/10.1111/tpj.13727 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Long SP (1993) The significance of light-limited photosynthesis to crop canopy carbon gain and productivity—a theoretical analysis. In: Abrol YP, Mohanty P, Govindjee (eds) Photosynthesis: photoreactions to plant productivity. Oxford & IBH Publishing, New Delhi, pp 547–560CrossRefGoogle Scholar
  44. Long SP, Farage PK, Garcia RL (1996) Measurement of leaf and canopy photosynthetic CO2 exchange in the field. J Exp Bot 47(304):1629–1642.  https://doi.org/10.1093/jxb/47.11.1629 CrossRefGoogle Scholar
  45. Long SP, Ainsworth EA, Leakey ADB, Nösberger J, Ort DR (2006) Food for thought: Lower-than-expected crop yield stimulation with rising CO2 concentrations. Science 312(5782):1918–1921.  https://doi.org/10.1126/science.1114722 CrossRefPubMedGoogle Scholar
  46. Long SP, Marshall-Colon A, Zhu X-G (2015) Meeting the global food demand of the future by engineering crop photosynthesis and yield potential. Cell 161(1):56–66.  https://doi.org/10.1016/j.cell.2015.03.019 CrossRefPubMedGoogle Scholar
  47. McAusland L, Vialet-Chabrand S, Davey P, Baker NR, Brendel O, Lawson T (2016) Effects of kinetics of light-induced stomatal responses on photosynthesis and water-use efficiency. New Phytol 211(4):1209–1220.  https://doi.org/10.1111/nph.14000 CrossRefPubMedPubMedCentralGoogle Scholar
  48. McQualter RB, Bellasio C, Gebbie L, Petrasovits LA, Palfreyman R, Hodson M, Plan M, Blackman D, Brumbley S, Nielsen L (2016) Systems biology and metabolic modelling unveils limitations to polyhydroxybutyrate accumulation in sugarcane leaves; lessons for C4 engineering. Plant Biotechnol J 14(2):567–580.  https://doi.org/10.1111/pbi.12399 CrossRefPubMedGoogle Scholar
  49. Messinger SM, Buckley TN, Mott KA (2006) Evidence for involvement of photosynthetic processes in the stomatal response to CO2. Plant Physiol 140(2):771–778.  https://doi.org/10.1104/pp.105.073676 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Miyake C, Yokota A (2000) Determination of the rate of photoreduction of O2 in the water-water cycle in watermelon leaves and enhancement of the rate by limitation of photosynthesis. Plant Cell Physiol 41(3):335–343CrossRefGoogle Scholar
  51. Morales A, Kaiser E, Yin X, Harbinson J, Molenaar J, Driever SM, Struik PC (2018) Dynamic modelling of limitations on improving leaf CO2 assimilation under fluctuating irradiance. Plant Cell Environ 41(3):589–604.  https://doi.org/10.1111/pce.13119 CrossRefPubMedGoogle Scholar
  52. Mott KA, Berg DG, Hunt SM, Peak D (2014) Is the signal from the mesophyll to the guard cells a vapour-phase ion? Plant Cell Environ 37(5):1184–1191.  https://doi.org/10.1111/pce.12226 CrossRefPubMedGoogle Scholar
  53. Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125(4):1558–1566CrossRefGoogle Scholar
  54. Naumburg E, Ellsworth DS (2002) Short-term light and leaf photosynthetic dynamics affect estimates of daily understory photosynthesis in four tree species. Tree Physiol 22(6):393–401.  https://doi.org/10.1093/treephys/22.6.393 CrossRefPubMedGoogle Scholar
  55. Ostle NJ, Smith P, Fisher R, Ian Woodward F, Fisher JB, Smith JU, Galbraith D, Levy P, Meir P, McNamara NP, Bardgett RD (2009) Integrating plant–soil interactions into global carbon cycle models. J Ecol 97(5):851–863.  https://doi.org/10.1111/j.1365-2745.2009.01547.x CrossRefGoogle Scholar
  56. Pearcy RW (1990) Sunflecks and photosynthesis in plant canopies. Annu Rev Plant Physiol Plant Mol Biol 41(1):421–453.  https://doi.org/10.1146/annurev.pp.41.060190.002225 CrossRefGoogle Scholar
  57. Pearcy RW, Osteryoung K, Calkin HW (1985) Photosynthetic responses to dynamic light environments by Hawaiian trees: time course of CO2 uptake and carbon gain during sunflecks. Plant Physiol 79(3):896–902.  https://doi.org/10.1104/pp.79.3.896 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Pearcy RW, Gross LJ, He D (1997) An improved dynamic model of photosynthesis for estimation of carbon gain in sunfleck light regimes. Plant Cell Environ 20(4):411–424.  https://doi.org/10.1046/j.1365-3040.1997.d01-88.x CrossRefGoogle Scholar
  59. Portis AR, Salvucci ME, Ogren WL (1986) Activation of ribulosebisphosphate carboxylase/oxygenase at physiological CO2 and ribulosebisphosphate concentrations by Rubisco activase. Plant Physiol 82(4):967–971CrossRefGoogle Scholar
  60. Ray DK, Ramankutty N, Mueller ND, West PC, Foley JA (2012) Recent patterns of crop yield growth and stagnation. Nat Commun 3:1293.  https://doi.org/10.1038/ncomms2296 CrossRefPubMedGoogle Scholar
  61. Ray DK, Mueller ND, West PC, Foley JA (2013) Yield trends are insufficient to double global crop production by 2050. PLoS ONE 8(6):e66428.  https://doi.org/10.1371/journal.pone.0066428 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Retta M, Ho QT, Yin X, Verboven P, Berghuijs HNC, Struik PC, Nicolaï BM (2016) A two-dimensional microscale model of gas exchange during photosynthesis in maize (Zea mays L.) leaves. Plant Sci 246(Supplement C):37–51.  https://doi.org/10.1016/j.plantsci.2016.02.003 CrossRefPubMedGoogle Scholar
  63. Roach T, Krieger-Liszkay A (2014) Regulation of photosynthetic electron transport and photoinhibition. Curr Protein Pept Sci 15(4):351–362CrossRefGoogle Scholar
  64. Rodriguez-Dominguez CM, Buckley TN, Egea G, de Cires A, Hernandez-Santana V, Martorell S, Diaz-Espejo A (2016) Most stomatal closure in woody species under moderate drought can be explained by stomatal responses to leaf turgor. Plant Cell Environ 39(9):2014–2026.  https://doi.org/10.1111/pce.12774 CrossRefPubMedGoogle Scholar
  65. Sage RF, Cen Y-P, Li M (2002) The activation state of Rubisco directly limits photosynthesis at low CO2 and low O2 partial pressures. Photosynth Res 71(3):241.  https://doi.org/10.1023/a:1015510005536 CrossRefPubMedGoogle Scholar
  66. Sander R (2015) Compilation of Henry’s law constants (version 4.0) for water as solvent. Atmos Chem Phys 15(8):4399–4981.  https://doi.org/10.5194/acp-15-4399-2015 CrossRefGoogle Scholar
  67. Santarius KA, Heber U (1965) Changes in the intracellular levels of ATP, ADP, AMP and Pi and regulatory function of the adenylate system in leaf cells during photosynthesis. Biochim Biophys Acta (BBA): Biophys Incl Photosyn 102 (1):39–54.  https://doi.org/10.1016/0926-6585(65)90201-3 CrossRefGoogle Scholar
  68. Sato H, Kumagai TO, Takahashi A, Katul GG (2015) Effects of different representations of stomatal conductance response to humidity across the African continent under warmer CO2-enriched climate conditions. J Geophys Res: Biogeosci 120(5):979–988.  https://doi.org/10.1002/2014JG002838 CrossRefGoogle Scholar
  69. Schreiber U, Neubauer C (1990) O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth Res 25(3):279–293CrossRefGoogle Scholar
  70. Seemann JR, Kirschbaum MU, Sharkey TD, Pearcy RW (1988) Regulation of ribulose-1, 5-bisphosphate carboxylase activity in Alocasia macrorrhiza in response to step changes in irradiance. Plant Physiol 88(1):148–152CrossRefGoogle Scholar
  71. Song Q, Zhang G, Zhu X-G (2013) Optimal crop canopy architecture to maximise canopy photosynthetic CO2 uptake under elevated CO2-a theoretical study using a mechanistic model of canopy photosynthesis. Funct Plant Biol 40(2):108–124.  https://doi.org/10.1071/FP12056 CrossRefGoogle Scholar
  72. Taylor SH, Long SP (2017) Slow induction of photosynthesis on shade to sun transitions in wheat may cost at least 21% of productivity. Philos Trans R Soc B.  https://doi.org/10.1098/rstb.2016.0543 CrossRefGoogle Scholar
  73. Tholen D, Ethier G, Genty B, Pepin S, Zhu XG (2012) Variable mesophyll conductance revisited: theoretical background and experimental implications. Plant Cell Environ 35(12):2087–2103CrossRefGoogle Scholar
  74. Trinkunas G, Connelly JP, Müller MG, Valkunas L, Holzwarth AR (1997) Model for the excitation dynamics in the light-harvesting complex II from higher plants. J Phys Chem B 101(37):7313–7320.  https://doi.org/10.1021/jp963968j CrossRefGoogle Scholar
  75. Valladares F, Allen MT, Pearcy RW (1997) Photosynthetic responses to dynamic light under field conditions in six tropical rainforest shrubs occurring along a light gradient. Oecologia 111(4):505–514.  https://doi.org/10.1007/s004420050264 CrossRefPubMedGoogle Scholar
  76. Vialet-Chabrand S, Dreyer E, Brendel O (2013) Performance of a new dynamic model for predicting diurnal time courses of stomatal conductance at the leaf level. Plant Cell Environ 36(8):1529–1546CrossRefGoogle Scholar
  77. Vialet-Chabrand S, Matthews JSA, Brendel O, Blatt MR, Wang Y, Hills A, Griffiths H, Rogers S, Lawson T (2016) Modelling water use efficiency in a dynamic environment: an example using Arabidopsis thaliana. Plant Sci 251:65–74.  https://doi.org/10.1016/j.plantsci.2016.06.016 CrossRefPubMedPubMedCentralGoogle Scholar
  78. von Caemmerer S (2000) Biochemical models of leaf photosynthesis. Techniques in plant science. CSIRO Publishing, CollingwoodGoogle Scholar
  79. von Caemmerer S, Edmondson DL (1986) Relationship between steady-state gas-exchange, invivo ribulose bisphosphate carboxylase activity and some carbon-reduction cycle intermediates in Raphanus-sativus. Aust J Plant Physiol 13(5):669–688Google Scholar
  80. Walker D (1992) Concerning oscillations. Photosynth Res 34(3):387–395CrossRefGoogle Scholar
  81. Wang Y, Bräutigam A, Weber APM, Zhu X-G (2014a) Three distinct biochemical subtypes of C4 photosynthesis? A modelling analysis. J Exp Bot.  https://doi.org/10.1093/jxb/eru058 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Wang Y, Long SP, Zhu X-G (2014b) Elements required for an efficient NADP-malic enzyme type C4 photosynthesis. Plant Physiol 164(4):2231–2246.  https://doi.org/10.1104/pp.113.230284 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Wang S, Tholen D, Zhu X-G (2017) C4 photosynthesis in C3 rice: a theoretical analysis of biochemical and anatomical factors. Plant Cell Environ 40(1):80–94.  https://doi.org/10.1111/pce.12834 CrossRefPubMedGoogle Scholar
  84. Warneck P, Williams J (2012) Rate coefficients for gas-phase reactions. In: the atmospheric chemist’s companion. Springer, Amsterdam, pp 227–269Google Scholar
  85. Way DA, Pearcy RW (2012) Sunflecks in trees and forests: from photosynthetic physiology to global change biology. Tree Physiol 32(9):1066–1081.  https://doi.org/10.1093/treephys/tps064 CrossRefPubMedGoogle Scholar
  86. Way DA, Oren R, Kim HS, Katul GG (2011) How well do stomatal conductance models perform on closing plant carbon budgets? A test using seedlings grown under current and elevated air temperatures. J Geophys Res: Biogeosci (2005–2012).  https://doi.org/10.1029/2011JG001808 CrossRefGoogle Scholar
  87. Wong SC (1979) Elevated atmospheric partial-pressure of CO2 and plant-growth.1. Interactions of nitrogen nutrition and photosynthetic capacity in C3 and C4 plants. Oecologia 44(1):68–74.  https://doi.org/10.1007/Bf00346400 CrossRefPubMedGoogle Scholar
  88. Yamori W, Shikanai T (2016) Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annu Rev Plant Biol 67(1):81–106.  https://doi.org/10.1146/annurev-arplant-043015-112002 CrossRefPubMedGoogle Scholar
  89. Yin XY, Struik PC (2012) Mathematical review of the energy transduction stoichiometries of C4 leaf photosynthesis under limiting light. Plant Cell Environ 35(7):1299–1312.  https://doi.org/10.1111/j.1365-3040.2012.02490.x CrossRefPubMedGoogle Scholar
  90. Yin X, Van Oijen M, Schapendonk A (2004) Extension of a biochemical model for the generalized stoichiometry of electron transport limited C3 photosynthesis. Plant Cell Environ 27(10):1211–1222CrossRefGoogle Scholar
  91. Yin X, Struik PC, Romero P, Harbinson J, Evers JB, Van Der Putten PEL, Vos JAN (2009) 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(5):448–464.  https://doi.org/10.1111/j.1365-3040.2009.01934.x CrossRefPubMedGoogle Scholar
  92. Yin X, Belay D, van der Putten PL, Struik P (2014) Accounting for the decrease of photosystem photochemical efficiency with increasing irradiance to estimate quantum yield of leaf photosynthesis. Photosynth Res 122(3):323–335.  https://doi.org/10.1007/s11120-014-0030-8 CrossRefPubMedGoogle Scholar
  93. Zaks J, Amarnath K, Kramer DM, Niyogi KK, Fleming GR (2012) A kinetic model of rapidly reversible nonphotochemical quenching. Proc Natl Acad Sci 109(39):15757–15762.  https://doi.org/10.1073/pnas.1211017109 CrossRefPubMedGoogle Scholar
  94. Zhang N, Portis AR (1999) Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. Proc Natl Acad Sci 96(16):9438–9443CrossRefGoogle Scholar
  95. Zhu X-G, de Sturler E, Long SP (2007) Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm. Plant Physiol 145(2):513–526.  https://doi.org/10.1104/pp.107.103713 CrossRefPubMedPubMedCentralGoogle Scholar
  96. Zhu XG, Wang Y, Ort DR, Long SP (2013) e-photosynthesis: a comprehensive dynamic mechanistic model of C3 photosynthesis: from light capture to sucrose synthesis. Plant Cell Environ 36(9):1711–1727CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Research School of BiologyAustralian National UniversityActonAustralia
  2. 2.University of the Balearic IslandsPalmaSpain
  3. 3.Trees and Timber InstituteNational Research Council of ItalyFlorenceItaly

Personalised recommendations