CO2 Diffusion Inside Photosynthetic Organs

  • Jaume FlexasEmail author
  • Francisco Javier Cano
  • Marc Carriquí
  • Rafael E. Coopman
  • Yusuke Mizokami
  • Danny Tholen
  • Dongliang Xiong
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 44)


In the present chapter, we review the current state-of-the-art of knowledge on mesophyll (internal) CO2 diffusion conductance of photosynthetic tissues (for simplification, gm). We show that, despite concerns regarding the methodological approaches currently used for its estimation, a large and consistent body of evidence has accumulated showing that gm is finite and significantly limiting for photosynthesis, as well as being highly variable among photosynthetic organisms and in response to environmental changes. Part of this variation results from different anatomies of the photosynthetic tissues, with a particularly strong influence of chloroplast distribution and cell wall thickness. Besides these, it appears that a biochemical modulation of gm also occurs, likely involving aquaporins and, possibly, carbonic anhydrases and other metabolic components.

Further efforts are needed in the near future to improve CO2 diffusion models, both for the estimation of gm and for the precise physiological understanding of the CO2 assimilation process in different plants, as well as to increase our knowledge of the mechanistic base for gm and its regulation.



fractionation factor due to diffusion through the air in the stomatal pore and between photosynthetic tissues


fractionation factor due to diffusion through stomata, between photosynthetic tissues and boundary layers


fractionation factor associated with diffusion through the air in the boundary layers


combined fractionation factor for dissolution of CO2 and diffusion through the liquid phase


fractionation factor for the diffusion pathway through stomata and boundary layers corrected for ternary effects


combined fractionation factor for dissolution of CO2 and diffusion through the liquid phase corrected for ternary effects


net rate of photosynthesis


plasma membrane aquaporins of Arabidopsis thaliana


abscisic acid




Adenosine triphosphate


leaf absorptance


net fractionation factor associated with Rubisco and PEPC


fractionation factor associated with Rubisco


fractionation factor associated with PEPC


net fractionation factor associated with Rubisco and PEPC corrected for ternary effects


fraction of photons absorbed by photosystem II


ambient CO2 concentration


CO2 concentration just outside the stomatal pore


CO2 concentration after fixation by Rubisco, i.e. 0


three-carbon organic acids


four-carbon organic acids


chloroplast stroma CO2 concentration


sub-stomatal CO2 concentration


intercellular CO2 concentration when the carboxylation rate equals the photorespiration rate


cytosolic CO2 concentration of a mesophyll cell


surface CO2 concentration


carbonic anhydrase


Crassulacean acid metabolism


CO2 concentrating mechanisms


cavity ringdown spectroscopy


diffusion coefficient for CO2 in the gas phase


diffusion coefficient for CO2 in the aqueous phase


discrimination against 13CO2


expected amount of discrimination against 13CO2 by the tissue enclosed in a gas-exchange cuvette if mesophyll conductance is assumed infinite and in the absence of any (photo)respiratory fractionation


observed amount of discrimination against 13CO2 by the tissue enclosed in a gas-exchange cuvette


carbon isotopic composition of CO2


fractionation factor due to mitochondrial respiration in the light


fractionation factor due to mitochondrial respiration in the light corrected for ternary effects


transpiration rate


fractionation factor for photorespiration


fraction of mesophyll volume occupied by intercellular air space


fractionation factor for photorespiration corrected for ternary effects


photorespiration rate


steady state fluorescence in the light


maximal fluorescence in the light during a short saturating pulse of light


quantum yield derived from CO2 exchange in the light-limited region


photochemical yield of photosystem II


total conductance to CO2 through stomata and boundary layers


boundary layer conductance to CO2


conductance of a given component of the diffusion pathway


gas-phase conductance between the sub-stomatal cavities and the outer surface of cell walls


liquid-phase conductance between the outer surface of the cell walls and the site of carboxylation in the chloroplast stroma


mesophyll conductance to CO2


mesophyll conductance to CO2 estimate based on physical models and the anatomical properties of the leaves


stomatal conductance to CO2


total conductance to CO2


intercellular air space


molar proportion of carbon fixed by PEPC


dimensionless factor accounting for decrease of diffusion conductance in the cytosol and in the stroma compared with free diffusion in water


chloroplastic CO2 concentration when the carboxylation rate equals the photorespiration rate


Henry’s law constant for dissolution of CO2 in water


electron transport rate


whole chain electron transport rate derived from fluorescence measurements


electron transport rate related to gas-exchange measurements


maximum rate of electron transport


leaf hydraulic conductance


cyclic-pseudocyclic electron flow coefficient


diffusion path length


diffusion path length in the gas phase


nicotinamide adenine dinucleotide


reduced nicotinamide adenine dinucleotide phosphate


Off-Axis Integrated Cavity Output Spectroscopy


coefficient related with the electron transport stoichiometry associated with the regeneration of RuBP


pulse amplitude modulation


phosphoenolpyruvate carboxylase


plasma membrane intrinsic protein


photosynthetic nitrogen use efficiency


photosynthetically active photon flux density incident on the leaf




scaling factor representing the relative increase in reaction rate over a 10°C temperature range at a particular temperature


gas constant


CO2 diffusion resistance (or sum of serial diffusion resistance)


diffusion resistance of the boundary to CO2


diffusion resistance of the double membranes of the chloroplasts and the stroma


diffusion resistance of a given component of the diffusion pathway


diffusion resistance of the stomata to CO2


diffusion resistance of cell wall and plasma membrane


rate of non-photorespiratory CO2 release in the light


rate of CO2 emission in the dark




ribulose-1,5-bisphosphate carboxylase-oxygenase


chloroplast surface exposed to the intercellular airspace


diffusion path tortuosity


correction factor to account for ternary effects


cell wall thickness


absolute temperature


tricarboxylic acid pathway


transfer DNA


tunable-diode laser absorption spectroscopy


carboxylation rate


maximum rate of carboxylation


vapor pressure deficit


water use efficiency



This work was supported partially by the Plan Nacional, Spain (contract CTM2014-53902-C2-1-P from the Spanish Ministry of Economy and Competitiveness – MINECO – and the ERDF – FEDER) awarded to Jaume Flexas and by the Conselleria d’Educació, Cultura i Universitats (Govern de les Illes Balears) and European Social Fund, predoctoral fellowship FPI/1700/2014, awarded to Marc Carriquí. Dongliang Xiong thanks the China Scholarship Council (CSC) for the funding of joint PhD training. Francisco Javier Cano thanks funding by the Australian Research Council Centre of Excellence for Translational Photosynthesis (CE1401000015).


  1. Aalto T, Juurola E (2002) A three-dimensional model of CO2 transport in airspaces and mesophyll cells of a silver birch leaf. Plant Cell Environ 25:1399–1409Google Scholar
  2. Abascal F, Irisarri I, Zardoya R (2014) Diversity and evolution of membrane intrinsic proteins. Biochim Biophys Acta 1840:1468–1481PubMedCrossRefGoogle Scholar
  3. Agati G, Cerovic ZG, Moya I (2000) The effect of decreasing temperature up to chilling values on the in vivo F685/F735 chlorophyll fluorescence ratio in Phaseolus vulgaris and Pisum sativum: the role of the photosystem I contribution to the 735 nm fluorescence band. J Photoch Photob 72: 75--84PubMedCrossRefGoogle Scholar
  4. Aranda I, Rodriguez-Calcerrada J, Robson TM, Cano FJ, Alté L, Sanchez-Gomez D (2012) Stomatal and non-stomatal limitations on leaf carbon assimilation in beech (Fagus sylvatica L.) seedlings under natural conditions. Forest Systems 21:405–417CrossRefGoogle Scholar
  5. Aranjuelo I, Tcherkez G, Jauregui I, Gilard F, Ancin M, AF-S M et al (2015) Alteration by thioredoxin f over-expression of primary carbon metabolism and its response to elevated CO2 in tobacco (Nicotiana tabacum L.). Environ Exp Bot 118:40–48CrossRefGoogle Scholar
  6. Badger MR, Price GD (1994) The role of carbonic-anhydrase in photosynthesis. Annu Rev Plant Physiol 45:369–392CrossRefGoogle Scholar
  7. Ball JT, Woodrow IE, Berry JA (1987) A model predicting stomatal conductance and its contribution to the control of photosynthesis under different environmental conditions. In: Progress in photosynthesis research. Springer, Dordrecht, pp 221–224CrossRefGoogle Scholar
  8. Battie-laclau P, Laclau J-P, Beri C, Mietton L, Muniz MRA, Arenque BC, de Cassia Piccolo M, Jordan-Meille L, Bouillet J-P, Nouvellon Y (2014) Photosynthetic and anatomical responses of Eucalyptus grandis leaves to potassium and sodium supply in a field experiment. Plant Cell Environ 37:70–81CrossRefGoogle Scholar
  9. Bazihizina N, Colzi I, Giorni E, Mancuso S, Gonnelli C (2015) Photosynthesizing on metal excess: Copper differently induced changes in various photosynthetic parameters in copper tolerant and sensitive Silene paradoxa L. populations. Plant Sci 232:67–76PubMedCrossRefGoogle Scholar
  10. Berghuijs HN, Yin X, Ho QT, van der Putten PE, Verboven P, Retta MA et al (2015) Modelling the relationship between CO2 assimilation and leaf anatomical properties in tomato leaves. Plant Sci 238:297–311PubMedCrossRefGoogle Scholar
  11. 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 130:1992–1998PubMedCrossRefPubMedCentralGoogle Scholar
  12. Bernacchi C, Morgan P, Ort D, Long S (2005) The growth of soybean under free air [CO2] enrichment (FACE) stimulates photosynthesis while decreasing in vivo Rubisco capacity. Planta 220:434–446PubMedCrossRefPubMedCentralGoogle Scholar
  13. Bi Z, Merl-Pham J, Uehlein N, Zimmer I, Muehlhans S, Aichler M et al (2015) RNAi-mediated downregulation of poplar plasma membrane intrinsic proteins (PIPs) changes plasma membrane proteome composition and affects leaf physiology. J Proteomics 128:321–332PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bloemen J, McGuire MA, Aubrey DP, Teskey RO, Steppe K (2013) Assimilation of xylem-transported CO2 is dependent on transpiration rate but is small relative to atmospheric fixation. J Exp Bot 64:2129–2138PubMedCrossRefPubMedCentralGoogle Scholar
  15. Boegelein R, Hassdenteufel M, Thomas FM, Werner W (2012) Comparison of leaf gas exchange and stable isotope signature of water-soluble compounds along canopy gradients of co-occurring Douglas fir and European beech. Plant Cell Environ 35:1245–1257CrossRefGoogle Scholar
  16. Boudichevskaia A, Heckwolf M, Kaldenhoff R (2015) T-DNA insertion in aquaporin gene AtPIP1;2 generates transcription profiles reminiscent of a low CO2 response. Plant Cell Environ 38:2286–2298PubMedCrossRefPubMedCentralGoogle Scholar
  17. Boursiac Y, Chen S, Luu D-T, Sorieul M, Van Den Dries N, Maurel C et al (2005) Early effects of salinity on water transport in Arabidopsis roots . Molecular and Cellular Features of Aquaporin Expression 1. Plant Physiol 139:790–805PubMedCrossRefPubMedCentralGoogle Scholar
  18. Boursiac Y, Boudet J, Postaire O, Luu DT, Tournaire-Roux C, Maurel C (2008) Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization. Plant J 56:207–218PubMedCrossRefPubMedCentralGoogle Scholar
  19. Boyer JS (2015) Impact of cuticle on calculations of the CO2 concentration inside leaves. Planta 242:1405–1412PubMedCrossRefPubMedCentralGoogle Scholar
  20. Boyer JS, Kawamitsu Y (2011) Photosynthesis gas exchange system with internal CO2 directly measured. Environ Control Biol 49:193–207CrossRefGoogle Scholar
  21. Boyer JS, Wong SC, Farquhar GD (1997) CO2 and water vapor exchange across leaf cuticle (epidermis) at various water potentials. Plant Physiol 114:185–191PubMedCrossRefPubMedCentralGoogle Scholar
  22. Brilli F, Tsonev T, Mahmood T, Velikova V, Loreto F, Centritto M (2013) Ultradian variation of isoprene emission, photosynthesis, mesophyll conductance, and optimum temperature sensitivity for isoprene emission in water-stressed Eucalyptus citriodora saplings. J Exp Bot 64:519–528PubMedCrossRefGoogle Scholar
  23. Brodersen CR, Vogelmann TC, Williams WE, Gorton HL (2008) A new paradigm in leaf-level photosynthesis: direct and diffuse lights are not equal. Plant Cell Environ 31:159–164PubMedPubMedCentralGoogle Scholar
  24. Brodribb TJ, McAdam SAM (2011) Passive origins of stomatal control in vascular plants. Science 331:582–585PubMedCrossRefPubMedCentralGoogle Scholar
  25. Brooks A, Farquhar GD (1985) Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light : Estimates from gas-exchange measurements on spinach. Planta 165:397–406PubMedCrossRefPubMedCentralGoogle Scholar
  26. Brown HT, Escombe F (1900) Static diffusion of gases and liquids in relation to the assimilation of carbon and translocation in plants. Philos T R Soc Lond B Biol Sci 193:223–291CrossRefGoogle Scholar
  27. Brugnoli E, Farquhar GD (2000) Photosynthetic fractionation of carbon isotopes. In: Leegood RC, Sharkey TD, von Caemmerer S (eds) Photosynthesis: physiology and metabolism, Advances in photosynthesis and respiration, vol 9. Springer, Dordrecht, pp 399–434CrossRefGoogle Scholar
  28. Brugnoli E, Hubick KT, von Caemmerer S, Wong SC, Farquhar GD (1988) Correlation between the carbon isotope discrimination in leaf starch and sugars of C3 plants and the ratio of intercellular and atmospheric partial pressures of carbon dioxide. Plant Physiol 88:1418–1424PubMedCrossRefPubMedCentralGoogle Scholar
  29. Buckley TN (2015) The contributions of apoplastic, symplastic and gas phase pathways for water transport outside the bundle sheath in leaves. Plant Cell Environ 38:7–22CrossRefGoogle Scholar
  30. Buckley TN, Warren CR (2014) The role of mesophyll conductance in the economics of nitrogen and water use in photosynthesis. Photosynth Res 119:77–88PubMedCrossRefPubMedCentralGoogle Scholar
  31. Buckley TN, Grace PJ, Scoffoni C, Sack L (2017) The sites of evaporation within leaves. Plant Physiol. PubMedCrossRefPubMedCentralGoogle Scholar
  32. Bunce JA (2009) Use of the response of photosynthesis to oxygen to estimate mesophyll conductance to carbon dioxide in water-stressed soybean leaves. Plant Cell Environ 32:875–881PubMedCrossRefPubMedCentralGoogle Scholar
  33. Busch FA, Sage TL, Cousins AB, Sage RF (2013) C3 plants enhance rates of photosynthesis by reassimilating photorespired and respired CO2. Plant Cell Environ 36:200–212CrossRefGoogle Scholar
  34. Cano FJ, Sánchez-Gómez D, Gascó A, Rodríguez-Calcerrada J, Gil L, Warren C, Aranda I (2011) Light acclimation at the end of the growing season in two broadleaved oak species. Photosynthetica 49:581–592CrossRefGoogle Scholar
  35. Cano FJ, Sanchez-Gomez D, Rodriguez-Calcerrada J, Warren C, Gil L, Aranda I (2013) Effects of drought on mesophyll conductance and photosynthetic limitations at different tree canopy layers. Plant Cell Environ 36:1961–1980PubMedPubMedCentralGoogle Scholar
  36. 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 37:2470–2490PubMedCrossRefPubMedCentralGoogle Scholar
  37. Carriquí M, Cabrera HM, Conesa MA, Coopman RE, Douthe C, Gago J et al (2015) Diffusional limitations explain the lower photosynthetic capacity of ferns as compared with angiosperms in a common garden study. Plant Cell Environ 38:448–460PubMedCrossRefPubMedCentralGoogle Scholar
  38. Centritto M, Loreto F, Chartzoulakis K (2003) The use of low CO2 to estimate diffusional and non-diffusional limitations of photosynthetic capacity of salt-stressed olive saplings. Plant Cell Environ 26:585–594CrossRefGoogle Scholar
  39. Chen CP, Sakai H, Tokida T, Usui Y, Nakamura H, Hasegawa T (2014) Do the rich always become richer? Characterizing the leaf physiological response of the high-yielding rice cultivar Takanari to free-air CO2 enrichment. Plant Cell Physiol 55:381–391PubMedCrossRefPubMedCentralGoogle Scholar
  40. Chollet R, Vidal J, O’Leary MH (1996) Phosphoenol pyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annu Rev Plant Biol 47:273–298CrossRefGoogle Scholar
  41. Cowan I (1986) Economics of carbon fixation in higher plants. In: Givnish TJ (ed) On the economy of plant form and function. Cambridge University Press, Cambridge, pp 133–170Google Scholar
  42. Crous K, Quentin A, Lin Y, Medlyn B, Williams D, Barton C, Ellsworth D (2013) Photosynthesis of temperate Eucalyptus globulus trees outside their native range has limited adjustment to elevated CO2 and climate warming. Glob Change Biol 19:3790–3807CrossRefGoogle Scholar
  43. DaMatta FM, Godoy AG, Menezes-Silva PE, Martins SCV, Sanglard LMVP, Morais LE et al (2016) Sustained enhancement of photosynthesis in coffee trees grown under free-air CO2 enrichment conditions: disentangling the contributions of stomatal, mesophyll, and biochemical limitations. J Exp Bot 67:341–352PubMedCrossRefPubMedCentralGoogle Scholar
  44. Devi MT, Rajagopalan AV, Raghavendra AS (1995) Predominant localization of mitochondria enriched with glycine-decarboxylating enzymes in bundle-sheath cells of Alternanthera tenella, a C3-C4 intermediate species. Plant Cell Environ 18:589–594CrossRefGoogle Scholar
  45. Di Marco G, Manes F, Tricoli D, Vitale E (1990) Fluorescence parameters measured concurrently with net photosynthesis to investigate chloroplastic CO2 concentration in leaves of Quercus ilex L. J Plant Physiol 136:538–543CrossRefGoogle Scholar
  46. Díaz-Espejo A, Nicolas E, Fernandez JE (2007) Seasonal evolution of diffusional limitations and photosynthetic capacity in olive under drought. Plant Cell Environ 30:922–933PubMedCrossRefPubMedCentralGoogle Scholar
  47. DiMario RJ, Quebedeaux JC, Longstreth D, 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 171:280–293PubMedCrossRefPubMedCentralGoogle Scholar
  48. Ding L, Gao L, Liu W, Wang M, Gu M, Ren B et al (2016) Aquaporin plays an important role in mediating chloroplastic CO2 concentration under high-N supply in rice (Oryza sativa) plants. Physiol Plant 156:215–226PubMedCrossRefPubMedCentralGoogle Scholar
  49. Douthe C, Dreyer E, Epron D, Warren CR (2011) Mesophyll conductance to CO2, assessed from online TDL-AS records of 13CO2 discrimination, displays small but significant short-term responses to CO2 and irradiance in Eucalyptus seedlings. J Exp Bot 62:5335–5346PubMedCrossRefPubMedCentralGoogle Scholar
  50. 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 39:435–448CrossRefGoogle Scholar
  51. Duan B, Li Y, Zhang X, Korpelainen H, Li C (2009) Water deficit affects mesophyll limitation of leaves more strongly in sun than in shade in two contrasting Picea asperata populations. Tree Physiol 29:1551–1561PubMedCrossRefPubMedCentralGoogle Scholar
  52. Dubois JJB, Fiscus EL, Booker FL, Flowers MD, Reid CD (2008) Optimizing the statistical estimation of the parameters of the Farquhar-von Caemmerer-Berry model of photosynthesis. New Phytol 177:1034–1034CrossRefGoogle Scholar
  53. Eichelmann H, Laisk A (2000) Cooperation of photosystems II and I in leaves as analyzed by simultaneous measurements of chlorophyll fluorescence and transmittance at 800 nm. Plant Cell Physiol 41:138–147PubMedCrossRefPubMedCentralGoogle Scholar
  54. Endeward V, Samer AS, Itel F, Gros G (2014) How does carbon dioxide permeate cell membranes? A discussion of concepts, results and methods. Frontiers in Physiol 4:1–21CrossRefGoogle Scholar
  55. Engelman DM (2005) Membranes are more mosaic than fluid. Nature 438:578–580PubMedCrossRefGoogle Scholar
  56. 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 27:137–153CrossRefGoogle Scholar
  57. Evans JR (2009) Potential errors in electron transport rates calculated from chlorophyll fluorescence as revealed by a multilayer leaf model. Plant Cell Physiol 50:698–706PubMedCrossRefGoogle Scholar
  58. Evans JR, Vogelmann TC (2003) Profiles of 14C fixation through spinach leaves in relation to light absorption and photosynthetic capacity. Plant Cell Environ 26:547–560CrossRefGoogle Scholar
  59. Evans JR, Von Caemmerer S (2013) Temperature response of carbon isotope discrimination and mesophyll conductance in tobacco. Plant Cell Environ 36:745–756PubMedCrossRefGoogle Scholar
  60. Evans JR, Sharkey TD, Berry J, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Funct Plant Biol 13:281–292Google Scholar
  61. 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. Funct Plant Biol 21:475–495Google Scholar
  62. Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) Resistances along the CO2 diffusion pathway inside leaves. J Exp Bot 60:2235–2248PubMedCrossRefGoogle Scholar
  63. 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 30:617–629PubMedCrossRefGoogle Scholar
  64. Farquhar GD (1989) Models of integrated photosynthesis of cells and leaves. Philos Trans R Soc B Biol Sci 323:357–367CrossRefGoogle Scholar
  65. Farquhar GD, Cernusak LA (2012) Ternary effects on the gas exchange of isotopologues of carbon dioxide. Plant Cell Environ 35:1221–1231PubMedCrossRefPubMedCentralGoogle Scholar
  66. Farquhar GD, Richards R (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Funct Plant Biol 11:539–552Google Scholar
  67. Farquhar GD, Caemmerer SV, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90CrossRefGoogle Scholar
  68. Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Funct Plant Biol 9:121–137Google Scholar
  69. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Biol 40:503–537CrossRefGoogle Scholar
  70. Farquhar GD, von Caemmerer S, Berry JA (2001) Models of photosynthesis. Plant Physiol 125:42–45PubMedCrossRefPubMedCentralGoogle Scholar
  71. Ferrio JP, Pou A, Florez-Sarasa I, Gessler A, Kodama N, Flexas J, Ribas-Carbó M (2012) The Peclet effect on leaf water enrichment correlates with leaf hydraulic conductance and mesophyll conductance for CO2. Plant Cell Environ 35:611–625PubMedCrossRefGoogle Scholar
  72. Fini A, Loreto F, Tattini M, Giordano C, Ferrini F, Brunetti C, Centritto M (2016) Mesophyll conductance plays a central role in leaf functioning of Oleaceae species exposed to contrasting sunlight irradiance. Physiol Plant 157:54–68PubMedCrossRefGoogle Scholar
  73. Finkelstein A (1976) Nature of the water permeability increase induced by antidiuretic hormone (ADH) in toad urinary bladder and related tissues. J General Physiol 68:137–143CrossRefGoogle Scholar
  74. Flexas J, Ribas-Carbó M, Bota J, Galmés J, Henkle M, Martinez-Canellas S, Medrano H (2006a) Decreased Rubisco activity during water stress is not induced by decreased relative water content but related to conditions of low stomatal conductance and chloroplast CO2 concentration. New Phytol 172:73–82PubMedCrossRefGoogle Scholar
  75. Flexas J, Ribas-Carbó M, Hanson DT, Bota J, Otto B, Cifre J et al (2006b) Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. Plant J 48:427–439PubMedCrossRefGoogle Scholar
  76. Flexas J, Díaz-Espejo A, Berry J, Cifre J, Galmés J, Kaldenhoff R et al (2007a) Analysis of leakage in IRGA’s leaf chambers of open gas exchange systems: quantification and its effects in photosynthesis parameterization. J Exp Bot 58:1533–1543PubMedCrossRefGoogle Scholar
  77. Flexas J, Díaz-Espejo A, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbó M (2007b) Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant Cell Environ 30:1284–1298PubMedCrossRefPubMedCentralGoogle Scholar
  78. 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 31:602–621PubMedCrossRefPubMedCentralGoogle Scholar
  79. Flexas J, Baron M, Bota J, Ducruet JM, Galle A, Galmés J et al (2009) Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandieri x V. rupestris). J Exp Bot 60:2361–2377PubMedCrossRefGoogle Scholar
  80. Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriquí M, Díaz-Espejo A et al (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Sci 193:70–84PubMedCrossRefGoogle Scholar
  81. Flexas J, Scoffoni C, Gago J, Sack L (2013a) Leaf mesophyll conductance and leaf hydraulic conductance: an introduction to their measurement and coordination. J Exp Bot 64:3965–3981PubMedCrossRefPubMedCentralGoogle Scholar
  82. Flexas J, Niinemets Ü, Galle A, Barbour MM, Centritto M, Díaz-Espejo A et al (2013b) Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency. Photosynth Res 117:45–59PubMedCrossRefGoogle Scholar
  83. Flexas J, Díaz-Espejo A, Conesa MÀ, Coopman RE, Douthe C, Gago J et al (2015) Mesophyll conductance to CO2 and Rubisco as targets for improving intrinsic water use efficiency in C3 plants. Plant Cell Environ 39:965–982PubMedCrossRefGoogle Scholar
  84. Franck F, Juneau P, Popovic R (2002) Resolution of the Photosystem I and Photosystem II contributions to chlorophyll fluorescence of intact leaves at room temperature. Biochim Biophys Acta 1556:239–246PubMedCrossRefGoogle Scholar
  85. Gaastra P (1959) Photosynthesis of crop plants as influenced by light, carbon dioxide, temperature, and stomatal diffusion resistance. Mededelingen van de Landbouwhogeschool te Wageningen 59:1–69Google Scholar
  86. Galle A, Florez-Sarasa I, Tomas M, Pou A, Medrano H, Ribas-Carbó M, Flexas J (2009) The role of mesophyll conductance during water stress and recovery in tobacco (Nicotiana sylvestris): acclimation or limitation? J Exp Bot 60:2379–2390PubMedCrossRefGoogle Scholar
  87. Galle A, Florez-Sarasa I, Thameur A, de Paepe R, Flexas J, Ribas-Carbó M (2010) Effects of drought stress and subsequent rewatering on photosynthetic and respiratory pathways in Nicotiana sylvestris wild type and the mitochondrial complex I-deficient CMSII mutant. J Exp Bot 61:765–775PubMedCrossRefGoogle Scholar
  88. Galmés J, Medrano H, Flexas J (2006) Acclimation of Rubisco specificity factor to drought in tobacco: discrepancies between in vitro and in vivo estimations. J Exp Bot 57:3659–3667PubMedCrossRefGoogle Scholar
  89. Galmés J, Medrano H, Flexas J (2007) Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytol 175:81–93PubMedCrossRefGoogle Scholar
  90. Galmés J, Àngel Conesa M, Manuel Ochogavía J, Alejandro Perdomo J, Francis DM, Ribas-Carbó M et al (2011) Physiological and morphological adaptations in relation to water use efficiency in Mediterranean accessions of Solanum lycopersicum. Plant Cell Environ 34:245–260PubMedCrossRefGoogle Scholar
  91. Galmés J, Ochogavía JM, Gago J, Roldán EJ, Cifre J, Conesa MÀ (2013) Leaf responses to drought stress in Mediterranean accessions of Solanum lycopersicum: anatomical adaptations in relation to gas exchange parameters. Plant Cell Environ 36:920–935PubMedCrossRefGoogle Scholar
  92. Galmés J, Molins A, Flexas J, coneas MA (2017) Coordination between leaf CO2 diffusion and Rubisco properties allows maximizing photosynthetic efficiency in Limonium species. Plant Cell Environ 40(10):2081–2094CrossRefGoogle Scholar
  93. Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92CrossRefGoogle Scholar
  94. Genty B, Wonders J, Baker NR (1990) Non-photochemical quenching of Fo in leaves is emission wavelength dependent: consequences for quenching analysis and its interpretation. Photosynth Res 26:133–139PubMedCrossRefGoogle Scholar
  95. Ghashghaie J, Badeck F-W, Lanigan G, Nogues S, Tcherkez G, Deleens E et al (2003) Carbon isotope fractionation during dark respiration and photorespiration in C3 plants. Phytochem Rev 2:145–161CrossRefGoogle Scholar
  96. Gilbert M, Holbrook N, Zwieniecki M, Sadok W, Sinclair TR (2011) Field confirmation of genetic variation in soybean transpiration response to vapor pressure deficit and photosynthetic compensation. Field Crops Res 124:85–92CrossRefGoogle Scholar
  97. Gillon JS, Griffiths H (1997) The influence of (photo)respiration on carbon isotope discrimination in plants. Plant Cell Environ 20:1217–1230CrossRefGoogle Scholar
  98. Gillon JS, Yakir D (2000) Internal conductance to CO2 diffusion and C18OO discrimination in C3 leaves. Plant Physiol 123:201–213PubMedCrossRefPubMedCentralGoogle Scholar
  99. Giuliani R, Koteyeva N, Voznesenskaya E, Evans MA, Cousins AB, Edwards GE (2013) Coordination of leaf photosynthesis, transpiration, and structural traits in rice and wild relatives (genus Oryza). Plant Physiol 162:1632–1651PubMedCrossRefPubMedCentralGoogle Scholar
  100. Gong HY, Li Y, Fang G, Hu DH, Jin WB, Wang ZH, Li YS (2015) Transgenic rice expressing Ictb and FBP/Sbpase derived from cyanobacteria exhibits enhanced photosynthesis and mesophyll conductance to CO2. PLoS One 10:e0140928PubMedCrossRefPubMedCentralGoogle Scholar
  101. Gorton HL, Williams WE, Vogelmann TC (1999) Chloroplast movement in Alocasia macrorrhiza. Physiol Plant 106:421–428CrossRefGoogle Scholar
  102. Grassi G, Magnani F (2005) Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant Cell Environ 28:834–849CrossRefGoogle Scholar
  103. Griffis TJ (2013) Tracing the flow of carbon dioxide and water vapor between the biosphere and atmosphere: A review of optical isotope techniques and their application. Agr Forest Meteor 174–175:85–109CrossRefGoogle Scholar
  104. Griffiths H, Helliker BR (2013) Mesophyll conductance: internal insights of leaf carbon exchange. Plant Cell Environ 36:733–735PubMedCrossRefPubMedCentralGoogle Scholar
  105. Groszmann M, Osborn HL, Evans JR (2017) Carbon dioxide and water transport through plant aquaporins. Plant Cell Environ 40:938–961PubMedCrossRefPubMedCentralGoogle Scholar
  106. 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 37:1231–1249PubMedCrossRefPubMedCentralGoogle Scholar
  107. Hanba Y, Kogami H, Terashima I (2002) The effect of growth irradiance on leaf anatomy and photosynthesis in Acer species differing in light demand. Plant Cell Environ 25:1021–1030CrossRefGoogle Scholar
  108. Hanba YT, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K, Terashima I, Katsuhara M (2004) Overexpression of the barley aquaporin HvPIP2;1 increases internal CO2 conductance and CO2 assimillation in the leaves of transgenic rice plants. Plant Cell Physiol 45:521–529PubMedCrossRefPubMedCentralGoogle Scholar
  109. Hanson DT, Renzaglia K, Villarreal JC (2014) Diffusion limitation and CO2 concentrating mechanisms in bryophytes. In: Hanson DT, Rice SK (eds) Photosynthesis in bryophytes and early land plants, Advances in photosynthesis and respiration, vol 37, pp 95-111. Springer, DordrechtGoogle Scholar
  110. Harley PC, Loreto F, Marco GD, Sharkey TD (1992) Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiol 98:1429–1436PubMedCrossRefPubMedCentralGoogle Scholar
  111. Hassiotou F, Ludwig M, Renton M, Veneklaas EJ, Evans JR (2009) Influence of leaf dry mass per area, CO2, and irradiance on mesophyll conductance in sclerophylls. J Exp Bot 60:2303–2314PubMedCrossRefPubMedCentralGoogle Scholar
  112. Hatakeyama Y, Ueno O (2017) Intracellular position of mitochondria in mesophyll cells differs between C3 and C4 grasses. J Plant Res. PubMedCrossRefPubMedCentralGoogle Scholar
  113. Haupt-Herting S, Fock HP (2002) Oxygen exchange in relation to carbon assimilation in water-stressed leaves during photosynthesis. Ann Bot 89:851–859PubMedCrossRefPubMedCentralGoogle Scholar
  114. Heckwolf M, Pater D, Hanson DT, Kaldenhoff R (2011) The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO2 transport facilitator. Plant J 67:795–804PubMedCrossRefPubMedCentralGoogle Scholar
  115. Heinen RB, Ye Q, Chaumont F (2009) Role of aquaporins in leaf physiology. J Exp Bot 60:2971–2985CrossRefGoogle Scholar
  116. Hibberd JM, Quick WP (2002) Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. Nature 415:451–454PubMedCrossRefPubMedCentralGoogle Scholar
  117. Ho QT, Berghuijs HN, Watte R, Verboven P, Herremans E, Yin X et al (2016) Three-dimensional microscale modelling of CO2 transport and light propagation in tomato leaves enlightens photosynthesis. Plant Cell Environ 39:50–61PubMedCrossRefPubMedCentralGoogle Scholar
  118. Huang W, Hu H, Zhang S-B (2015) Photorespiration plays an important role in the regulation of photosynthetic electron flow under fluctuating light in tobacco plants grown under full sunlight. Front Plant Sci 6:621Google Scholar
  119. Igamberdiev AU, Mikkelsen TN, Ambus P, Bauwe H, Lea PJ, Gardestrom P (2004) Photorespiration contributes to stomatal regulation and carbon isotope fractionation: a study with barley, potato and Arabidopsis plants deficient in glycine decarboxylase. Photosynth Res 81:139–152CrossRefGoogle Scholar
  120. Itel F, Al-Samir S, Öberg F, Chami M, Kumar M, Supuran CT, Deen PMT, Meier W, Hedfalk K, Gros G, Endeward V (2012) CO2 permeability of cell membranes is regulated by membrane cholesterol and protein gas channels. FASEB J 26:5182–5191PubMedCrossRefPubMedCentralGoogle Scholar
  121. Jarman P (1974) The diffusion of carbon dioxide and water vapour through stomata. J Exp Bot 25:927–936CrossRefGoogle Scholar
  122. Juszczuk IM, Flexas J, Szal B, Dabrowska Z, Ribas-Carbó M, Rychter AM (2007) Effect of mitochondrial genome rearrangement on respiratory activity, photosynthesis, photorespiration and energy status of MSC16 cucumber (Cucumis sativus) mutant. Physiol Plant 131:527–541PubMedCrossRefGoogle Scholar
  123. Kaldenhoff R (2012) Mechanisms underlying CO2 diffusion in leaves. Curr Opin Plant Biol 15:276–281PubMedCrossRefGoogle Scholar
  124. Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829–832PubMedCrossRefPubMedCentralGoogle Scholar
  125. Kato M, Imaichi R (1992) Leaf anatomy of tropical fern reophytes, with its evolutionary and ecological implications. Can J Bot 70:165–174CrossRefGoogle Scholar
  126. Kawase M, Hanba YT, Katsuhara M (2013) The photosynthetic response of tobacco plants overexpressing ice plant aquaporin McMIPB to a soil water deficit and high vapor pressure deficit. J Plant Res 126:517–527PubMedCrossRefPubMedCentralGoogle Scholar
  127. Kitao M, Yazaki K, Kitaoka S, Fukatsu E, Tobita H, Komatsu M et al (2015) Mesophyll conductance in leaves of Japanese white birch (Betula platyphylla var. japonica) seedlings grown under elevated CO2 concentration and low N availability. Physiol Plant 155:435–445PubMedCrossRefGoogle Scholar
  128. Kodama N, Cousins A, Tu KP, Barbour MM (2011) Spatial variation in photosynthetic CO2 carbon and oxygen isotope discrimination along leaves of the monocot triticale (Triticum x Secale) relates to mesophyll conductance and the Peclet effect. Plant Cell Environ 34:1548–1562PubMedCrossRefGoogle Scholar
  129. Kogami H, Hanba YT, Kibe T, Terashima I, Masuzawa T (2001) CO2 transfer conductance, leaf structure and carbon isotope composition of Polygonum cuspidatum leaves from low and high altitudes. Plant Cell Environ 24:529–538CrossRefGoogle Scholar
  130. Kok B (1948) A critical consideration of the quantum yield of Chlorella photosynthesis. Enzymologia:1–56Google Scholar
  131. Laisk A (1977) Kinetics of photosynthesis and photorespiration of C3 plants. Nauka, Moscow (in Russian)Google Scholar
  132. Laisk A, Oja V (1998) Dynamics of leaf photosynthesis: rapid-response measurements and their interpretations. CSIRO Publishing, CollingwoodGoogle Scholar
  133. Laisk A, Eichelmann H, Oja V, Rasulov B, Padu E, Bichele I, Pettai H, Kull O (2005) Adjustment of leaf photosynthesis to shade in a natural canopy: rate parameters. Plant Cell Environ 28:375–388CrossRefGoogle Scholar
  134. Lake JV (1967) Respiration of leaves during photosynthesis. I. Estimates from an electrical analogue. Appl Plant Sci 20:487–493Google Scholar
  135. Lanigan GJ, Betson N, Griffiths H, Seibt U (2008) Carbon isotope fractionation during photorespiration and carboxylation in Senecio. Plant Physiol 148:2013–2020PubMedCrossRefPubMedCentralGoogle Scholar
  136. Latzko E, Kelly GJ (1983) The many-faceted function of phosphoenolpyruvate carboxylase in C3 plants. Physiol Veg 21:805–815Google Scholar
  137. Lawson T, Morison J (2006) Visualising patterns of CO2 diffusion in leaves. New Phytol 169:641–643PubMedCrossRefPubMedCentralGoogle Scholar
  138. Leuning R (1995) A critical appraisal of a combined stomatal-photosynthesis model for C3 plants. Plant Cell Environ 18:339–355CrossRefGoogle Scholar
  139. Levy PE, Meir P, Allen SJ, Jarvis PG (1999) The effect of aqueous transport of CO2 in xylem sap on gas exchange in woody plants. Tree Physiol 19:53–58PubMedCrossRefGoogle Scholar
  140. Li Y, Gao Y, Xu X, Shen Q, Guo S (2009) Light-saturated photosynthetic rate in high-nitrogen rice (Oryza sativa L.) leaves is related to chloroplastic CO2 concentration. J Exp Bot 60:2351–2360PubMedCrossRefGoogle Scholar
  141. Li G, Santoni V, Maurel C (2014) Plant aquaporins: roles in plant physiology. Biochim Biophys Acta 1840:1574–1582PubMedCrossRefGoogle Scholar
  142. Li L, Wang H, Gago J, Cui H, Qian Z, Kodama N et al (2015) Harpin Hpa1 interacts with aquaporin PIP1;4 to promote the substrate transport and photosynthesis in Arabidopsis. Sci Rep 5:17207PubMedCrossRefPubMedCentralGoogle Scholar
  143. Lloyd J, Syvertsen J, Kriedemann P, Farquhar G (1992) Low conductances for CO2 diffusion from stomata to the sites of carboxylation in leaves of woody species. Plant Cell Environ 15:873–899CrossRefGoogle Scholar
  144. 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 54:2393–2401PubMedCrossRefGoogle Scholar
  145. Long BM, Bahar NHA, Atkin OK (2015) Contributions of photosynthetic and non-photosynthetic cell types to leaf respiration in Vicia faba L. and their responses to growth temperature. Plant Cell Environ 38:2263–2276PubMedCrossRefGoogle Scholar
  146. Loreto F, Tsonev T, Centritto M (2009) The impact of blue light on leaf mesophyll conductance. J Exp Bot 60:2283–2290PubMedCrossRefGoogle Scholar
  147. Loriaux SD, Avenson TJ, Welles JM, McDermitt DK, Eckles RD, Riensche B, Genty B (2013) Closing in on maximum yield of chlorophyll fluorescence using a single multiphase flash of sub-saturating intensity. Plant Cell Environ 36:1755–1770PubMedCrossRefGoogle Scholar
  148. Markgraf T, Berry J (1990) Measurement of photochemical and non-photochemical quenching: correction for turnover of PS2 during steady-state photosynthesis. In: Baltscheffsky M (ed) Current research in photosynthesis. Springer, Dordrecht, pp 3073–3076CrossRefGoogle Scholar
  149. Martins SC, Galmés J, Molins A, DaMatta FM (2013) Improving the estimation of mesophyll conductance to CO2: on the role of electron transport rate correction and respiration. J Exp Bot 64:3285–3298PubMedCrossRefPubMedCentralGoogle Scholar
  150. Martínez-Lüscher J, Morales F, Sánchez-Díaz M, Delrot S, Aguirreolea J, Gomès E, Pascual I (2015) Climate change conditions (elevated CO2 and temperature) and UV-B radiation affect grapevine (Vitis vinifera cv. Tempranillo) leaf carbon assimilation, altering fruit ripening rates. Plant Sci 236:168–176PubMedCrossRefPubMedCentralGoogle Scholar
  151. Masumoto C, Miyazawa S-I, Ohkawa H, Fukuda T, Taniguchi Y, Murayama S et al (2010) Phosphoenolpyruvate carboxylase intrinsically located in the chloroplast of rice plays a crucial role in ammonium assimilation. Proc Natl Acad Sci USA 107:5226–5231PubMedCrossRefGoogle Scholar
  152. Maurel C, Santoni V, Luu DT, Wudick MM, Verdoucq L (2009) The cellular dynamics of plant aquaporin expression and functions. Curr Opin Plant Biol 12:690–698PubMedCrossRefGoogle Scholar
  153. McGuire MA, Marshall JD, Teskey RO (2009) Assimilation of xylem-transported 13C labelled CO2 in leaves and branches of sycamore (Platanus occidentalis L.). J Exp Bot 60:3809–3817PubMedCrossRefPubMedCentralGoogle Scholar
  154. Medeiros DB, Daloso DM, Fernie AR, Nikoloski Z, Araujo WL (2015) Utilizing systems biology to unravel stomatal function and the hierarchies underpinning its control. Plant Cell Environ 38:1457–1470PubMedCrossRefGoogle Scholar
  155. Melzer E, O’Leary MH (1987) Anapleurotic CO2 fixation by phosphoenolpyruvate carboxylase in C3 Plants. Plant Physiol 84:58–60PubMedCrossRefPubMedCentralGoogle Scholar
  156. Meyer H (1899) Zur Theorie der Alkoholnarkose. Naunyn-Schmiedeberg’s Archives of Pharmacology 42:109–118CrossRefGoogle Scholar
  157. Meyer S, Genty B (1998) Mapping intercellular CO2 mole fraction (Ci) in Rosa rubiginosa leaves fed with abscisic acid by using chlorophyll fluorescence imaging. Significance of Ci estimated from leaf gas exchange. Plant Physiol 116:947–957PubMedCrossRefPubMedCentralGoogle Scholar
  158. Meyer M, Seibt U, Griffiths H (2008) To concentrate or ventilate? Carbon acquisition, isotope discrimination and physiological ecology of early land plant life. Philos T Roy Soc B 363:2767–2778CrossRefGoogle Scholar
  159. Miyazawa S-i, Yoshimura S, Shinzaki Y, Maeshima M, Miyake C (2008) Deactivation of aquaporins decreases internal conductance to CO2 diffusion in tobacco leaves grown under long-term drought. Funct Plant Biol 35:553–564CrossRefGoogle Scholar
  160. Mizokami Y, Noguchi K, Kojima M, Sakakibara H, Terashima I (2015) Mesophyll conductance decreases in the wild type but not in an ABA-deficient mutant (aba1) of Nicotiana plumbaginifolia under drought conditions. Plant Cell Environ 38:388–398PubMedCrossRefGoogle Scholar
  161. Montpied P, Granier A, Dreyer E (2009) Seasonal time-course of gradients of photosynthetic capacity and mesophyll conductance to CO2 across a beech (Fagus sylvatica L.) canopy. J Exp Bot 60:2407–2418PubMedCrossRefGoogle Scholar
  162. Mori CM, Rhee J, Shibasaka M, Sasano S, Kaneko T, Horie T, Katsuhara M (2014) CO2 transport by PIP2 aquaporins of barley. Plant Cell Physiol 55:251–257PubMedCrossRefPubMedCentralGoogle Scholar
  163. Morison JIL, Gallouët E, Lawson T, Cornic G, Herbin R, Baker NR (2005) Lateral diffusion of CO2 in leaves is not sufficient to support photosynthesis. Plant Physiol 139:254–266PubMedCrossRefPubMedCentralGoogle Scholar
  164. Morrow PA, Slatyer RO (1971) Leaf temperature effects on measurements of diffusive resistance to water vapor transfer. Plant Physiol 47:559–561PubMedCrossRefPubMedCentralGoogle Scholar
  165. Moss DN (1966) Respiration of leaves in light and darkness. Crop Sci 6:351–354CrossRefGoogle Scholar
  166. Moss DN, Rawlins SL (1963) Concentration of carbon dioxide inside leaves. Nature 197:1320–1321CrossRefGoogle Scholar
  167. Mott KA, Peak D (2011) Alternative perspective on the control of transpiration by radiation. Proc Natl Acad Sci USA 108:19820–19823PubMedCrossRefGoogle Scholar
  168. Muir CD, Hangarter RP, Moyle LC, Davis PA (2014) Morphological and anatomical determinants of mesophyll conductance in wild relatives of tomato (Solanum lycopersicon, sect. Lycopersicoides; Solanaceae). Plant Cell Environ 37:1415–1426CrossRefGoogle Scholar
  169. Murakami N (1995) Systematics and evolutionary biology of the fern genus Hymenasplenium (Aspleniaceae). J Plant Res 108:257–268CrossRefGoogle Scholar
  170. Niinemets Ü, Cescatti A, Rodeghiero M, Tosens T (2006) Complex adjustments of photosynthetic potentials and internal diffusion conductance to current and previous light availabilities and leaf age in Mediterranean evergreen species Quercus ilex. Plant Cell Environ 29:1159–1178PubMedCrossRefGoogle Scholar
  171. Niinemets Ü, Díaz-Espejo A, Flexas J, Galmés J, Warren CR (2009) Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. J Exp Bot 60:2249–2270PubMedCrossRefGoogle Scholar
  172. O’Leary MH (1982) Phosphoenolpyruvate carboxylase: an enzymologist’s view. Annu Rev Plant Physiol 33:297–315CrossRefGoogle Scholar
  173. Ogren WL (1984) Photorespiration-pathways, regulation, and modification. Annu Rev Plant Physiol 35:415–442CrossRefGoogle Scholar
  174. Oguchi R, Hikosaka K, Hirose T (2003) Does the photosynthetic light-acclimation need change in leaf anatomy? Plant Cell Environ 26:505–512CrossRefGoogle Scholar
  175. Oguchi R, Hikosaka K, Hirose T (2005) Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant Cell Environ 28:916–927CrossRefGoogle Scholar
  176. Oikawa K, Kasahara M, Kiyosue T, Kagawa T, Suetsugu N, Takahashi F et al (2003) Chloroplast unusual positioning1 is essential for proper chloroplast positioning. Plant Cell 15:2805–2815PubMedCrossRefPubMedCentralGoogle Scholar
  177. Ort DR, Merchant SS, Alric J, Barkan A, Blankenship RE, Bock R et al (2015) Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc Natl Acad Sci USA 112:8529–8536PubMedCrossRefGoogle Scholar
  178. Otto B, Uehlein N, Sdorra S, Fischer M, Ayaz M, Belastegui-Macadam X et al (2010) Aquaporin tetramer composition modifies the function of tobacco aquaporins. J Biol Chem 285:31253–31260PubMedCrossRefPubMedCentralGoogle Scholar
  179. Overton CE (1901) Studien über die Narkose zugleich ein Beitrag zur allgemeinen Pharmakologie. Fischer, JenaGoogle Scholar
  180. Pallozzi E, Tsonev T, Marino G, Copolovici L, Niinemets Ü, Loreto F, Centritto M (2013) Isoprenoid emissions, photosynthesis and mesophyll diffusion conductance in response to blue light. Environ Exp Bot 95:50–58CrossRefGoogle Scholar
  181. Parkhurst DF (1994) Diffusion of CO2 and other gases inside leaves. New Phytol 126:449–479CrossRefGoogle Scholar
  182. Parkhurst DF, Givnish T (1986) Internal leaf structure: a three-dimensional perspective. In: Givnish TJ (ed) On the economy of plant form and function. Cambridge University Press, Cambridge, pp 215–249Google Scholar
  183. Parkhurst DF, Mott KA (1990) Intercellular diffusion limits to CO2 uptake in leaves studies in air and helox. Plant Physiol 94:1024–1032PubMedCrossRefPubMedCentralGoogle Scholar
  184. Peguero-Pina JJ, Siso S, Fernandez-Marin B, Flexas J, Galmés J, García-Plazaola JI et al (2015) Leaf functional plasticity decreases the water consumption without further consequences for carbon uptake in Quercus coccifera L. under Mediterranean conditions. Tree Physiol 36:356–367PubMedCrossRefPubMedCentralGoogle Scholar
  185. Peguero-Pina JJ, Siso S, Flexas J, Galmés J, Garcia-Nogales A, Niinemets Ü, Sancho-Knapik D, Saz MA, Gil-Pelegrin E (2017) Cell-level anatomical characteristics explain high mesophyll conductance and photosynthetic capacity in sclerophyllous Mediterranean oaks. New Phytol 214:585–596PubMedCrossRefGoogle Scholar
  186. Perdomo JA, Carmo-Silva E, Hermida-Carrera C, Flexas J, Galmes J (2016) Acclimation of biochemical and diffusive components of photosynthesis in rice, wheat, and maize to heat and water deficit: implications for modeling photosynthesis. Front Plant Sci 7:1719PubMedCrossRefPubMedCentralGoogle Scholar
  187. Perez-Martin A, Michelazzo C, Torres-Ruiz JM, Flexas J, Fernandez JE, Sebastiani L, Díaz-Espejo A (2014) Regulation of photosynthesis and stomatal and mesophyll conductance under water stress and recovery in olive trees: correlation with gene expression of carbonic anhydrase and aquaporins. J Exp Bot 65:3143–3156PubMedCrossRefPubMedCentralGoogle Scholar
  188. Perisanu ST (2001) Estimation of solubility of carbon dioxide in polar solvents. J Sol Chem 30:183–192CrossRefGoogle Scholar
  189. Pfanz H, Aschan G, Langenfeld-Heyser R, Wittmann C, Loose M (2002) Ecology and ecophysiology of tree stems: corticular and wood photosynthesis. Naturwissenschaften 89:147–162PubMedCrossRefPubMedCentralGoogle Scholar
  190. Piel C, Frak E, Le Roux X, Genty B (2002) Effect of local irradiance on CO2 transfer conductance of mesophyll in walnut. J Exp Bot 53:2423–2430PubMedCrossRefPubMedCentralGoogle Scholar
  191. Pieruschka R, Schurr U, Jensen M, Wolff WF, Jahnke S (2006) Lateral diffusion of CO2 from shaded to illuminated leaf parts affects photosynthesis inside homobaric leaves. New Phytol 169:779–788PubMedCrossRefGoogle Scholar
  192. Pinelli P, Loreto F (2003) 12CO2 emission from different metabolic pathways measured in illuminated and darkened C3 and C4 leaves at low, atmospheric and elevated CO2 concentration. J Exp Bot 54:1761–1769PubMedCrossRefPubMedCentralGoogle Scholar
  193. Poincelot R (1979) Carbonic anhydrase. In: Gibbs M, Latzko E (eds) Photosynthesis II. Springer, Dordrecht, pp 230–238CrossRefGoogle Scholar
  194. Pons TL, Welschen RAM (2003) Midday depression of net photosynthesis in the tropical rainforest tree Eperua grandiflora: contributions of stomatal and internal conductances, respiration and Rubisco functioning. Tree Physiol 23:937–947PubMedCrossRefGoogle Scholar
  195. 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 60:2217–2234PubMedCrossRefGoogle Scholar
  196. Priault P, Fresneau C, Noctor G, De Paepe R, Cornic G, Streb P (2006) The mitochondrial CMSII mutation of Nicotiana sylvestris impairs adjustment of photosynthetic carbon assimilation to higher growth irradiance. J Exp Bot 57:2075–2085PubMedCrossRefGoogle Scholar
  197. Price GD, von Caemmerer S, Evans JR, Yu JW, Lloyd J, Oja V et al (1994) Specific reduction of chloroplast carbonic-anhydrase activity by antisense RNA in transgenic tobacco plants has a minor effect on photosynthetic CO2 assimilation. Planta 193:331–340CrossRefGoogle Scholar
  198. 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 155:20–26PubMedCrossRefPubMedCentralGoogle Scholar
  199. Proctor MCF (2010) Trait correlations in bryophytes: exploring and alternative world. New Phyt 185:1–3CrossRefGoogle Scholar
  200. Rachmilevitch S, Cousins AB, Bloom AJ (2004) Nitrate assimilation in plant shoots depends on photorespiration. Proc Natl Acad Sci USA 101:11506–11510PubMedCrossRefPubMedCentralGoogle Scholar
  201. Rand RH, Cooke JR (1980) A comprehensive model for CO2 assimilation in leaves. Trans ASAE 23:601–607CrossRefGoogle Scholar
  202. Raven JA, Beardall J (2016) The ins and outs of CO2. J Exp Bot 67:1–13PubMedCrossRefPubMedCentralGoogle Scholar
  203. Rho H, Yu DJ, Kim SJ, Lee HJ (2012) Limitation factors for photosynthesis in ‘Bluecrop’ highbush blueberry (Vaccinium corymbosum) leaves in response to moderate water Stress. J Plant Biol 55:450–457CrossRefGoogle Scholar
  204. Rockwell FE, Holbrook NM, Stroock AD (2014) The competition between liquid and vapor transport in transpiring leaves. Plant Physiol 164:1741–1758PubMedCrossRefPubMedCentralGoogle Scholar
  205. Rodeghiero M, Niinemets Ü, Cescatti A (2007) Major diffusion leaks of clamp-on leaf cuvettes still unaccounted: how erroneous are the estimates of Farquhar et al. model parameters? Plant Cell Environ 30:1006–1022PubMedCrossRefPubMedCentralGoogle Scholar
  206. Roeske CA, O’Leary MH (1984) Carbon isotope effects on the enzyme-catalyzed carboxylation of ribulose bisphosphate. Biochemistry 23:6275–6284CrossRefGoogle Scholar
  207. Rosell JA, Castorena M, Laws CA, Westoby M (2015) Bark ecology of twigs vs. main stems: functional traits across eighty-five species of angiosperms. Oecologia 178:1033–1043PubMedCrossRefPubMedCentralGoogle Scholar
  208. Rumeau D, Cuiné S, Fina L, Gault N, Nicole M, Peltier G (1996) Subcellular distribution of carbonic anhydrase in Solanum tuberosum L. leaves. Planta 199:79–88PubMedCrossRefGoogle Scholar
  209. Sack L, Holbrook NM (2006) Leaf hydraulics. Annu Rev Plant Biol 57:361–381CrossRefGoogle Scholar
  210. Sack L, Streeter CM, Holbrook NM (2004) Hydraulic analysis of water flow through leaves of sugar maple and red oak. Plant Physiol 134:1824–1833PubMedCrossRefPubMedCentralGoogle Scholar
  211. Sade N, Shatil-Cohen A, Attia Z, Maurel C, Boursiac Y, Kelly G et al (2014) The role of plasma membrane aquaporins in regulating the bundle sheath-mesophyll continuum and leaf hydraulics. Plant Physiol 166:1609–1620PubMedCrossRefPubMedCentralGoogle Scholar
  212. 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 50:756–772CrossRefGoogle Scholar
  213. Scafaro AP, Von Caemmerer S, Evans JR, Atwell BJ (2011) Temperature response of mesophyll conductance in cultivated and wild Oryza species with contrasting mesophyll cell wall thickness. Plant Cell Environ 34:1999–2008PubMedCrossRefPubMedCentralGoogle Scholar
  214. Sestak Z, Catsky J, Jarvis PG (1971) Plant photosynthetic production. Manual of methods. Q Rev Biol 47:235Google Scholar
  215. Sharkey TD, Loreto F, Delwiche C (1991) High carbon dioxide and sun/shade effects on isoprene emission from oak and aspen tree leaves. Plant Cell Environ 14:333–338CrossRefGoogle Scholar
  216. Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30:1035–1040PubMedCrossRefPubMedCentralGoogle Scholar
  217. Silva EN, Silveira JAG, Ribeiro RV, Vieira SA (2015) Photoprotective function of energy dissipation by thermal processes and photorespiratory mechanisms in Jatropha curcas plants during different intensities of drought and after recovery. Environ Exp Bot 110:36–45CrossRefGoogle Scholar
  218. Singh SK, Badgujar G, Reddy VR, Fleisher DH, Bunce JA (2013) Carbon dioxide diffusion across stomata and mesophyll and photo-biochemical processes as affected by growth CO2 and phosphorus nutrition in cotton. J Plant Physiol 170:801–813PubMedCrossRefGoogle Scholar
  219. Singsaas E, Ort D, DeLucia E (2004) Elevated CO2 effects on mesophyll conductance and its consequences for interpreting photosynthetic physiology. Plant Cell Environ 27:41–50CrossRefGoogle Scholar
  220. Soolanayakanahally RY, Guy RD, Silim SN, Drewes EC, Schroeder WR (2009) Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar (Populus balsamifera L.). Plant Cell Environ 32:1821–1832PubMedCrossRefPubMedCentralGoogle Scholar
  221. Sorrentino G, Haworth M, Wahbi S, Mahmood T, Zuomin S, Centritto M (2016) Abscisic acid induces rapid reductions in mesophyll conductance to carbon dioxide. PLoS ONE 11(2):e0148554PubMedCrossRefPubMedCentralGoogle Scholar
  222. Sun Y, Gu LH, Dickinson RE, Pallardy SG, Baker J, Cao YH et al (2014) Asymmetrical effects of mesophyll conductance on fundamental photosynthetic parameters and their relationships estimated from leaf gas exchange measurements. Plant Cell Environ 37:978–994PubMedCrossRefPubMedCentralGoogle Scholar
  223. 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 18:149–157CrossRefGoogle Scholar
  224. Tazoe Y, von Caemmerer S, Badger MR, Evans JR (2009) Light and CO2 do not affect the mesophyll conductance to CO2 diffusion in wheat leaves. J Exp Bot 60:2291–2301PubMedCrossRefPubMedCentralGoogle Scholar
  225. 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 34:580–591CrossRefGoogle Scholar
  226. Tcherkez G (2006) How large is the carbon isotope fractionation of the photorespiratory enzyme glycine decarboxylase? Funct Plant Biol 33:911–920CrossRefGoogle Scholar
  227. Tcherkez G (2013) Is the recovery of (photo)respiratory CO2 and intermediates minimal? New Phytol 198:334–338PubMedCrossRefPubMedCentralGoogle Scholar
  228. Tcherkez G (2015) The mechanism of Rubisco-catalysed oxygenation. Plant Cell Environ 39:983–997PubMedCrossRefPubMedCentralGoogle Scholar
  229. Tcherkez G, Ribas-Carbó M (2012) Interactions between photosynthesis and day respiration. In: Flexas J (ed) Terrestrial photosynthesis in a changing environment – a molecular, physiological and ecological approach. Cambridge University Press, CambridgeGoogle Scholar
  230. Tcherkez G, Nogues S, Bleton J, Cornic G, Badeck F, Ghashghaie J (2003) Metabolic origin of carbon isotope composition of leaf dark-respired CO2 in French bean. Plant Physiol 131:237–244PubMedCrossRefPubMedCentralGoogle Scholar
  231. Tcherkez G, Farquhar G, Badeck F, Ghashghaie J (2004) Theoretical considerations about carbon isotope distribution in glucose of C3 plants. Funct Plant Biol 31(8):57–877Google Scholar
  232. Tcherkez G, Boex-Fontvieille E, Mahe A, Hodges M (2012) Respiratory carbon fluxes in leaves. Curr Opin Plant Biol 15:308–314PubMedCrossRefPubMedCentralGoogle Scholar
  233. Terashima I, Ono K (2002) Effects of HgCl2 on CO2 dependence of leaf photosynthesis: evidence indicating involvement of aquaporins in CO2 diffusion across the plasma membrane. Plant Cell Physiol 43:70–78PubMedCrossRefPubMedCentralGoogle Scholar
  234. Terashima I, Saeki T (1985) A new model for leaf photosynthesis incorporating the gradients of light environment and of photosynthetic properties of chloroplasts within a leaf. Ann Bot 56:489–499CrossRefGoogle Scholar
  235. Terashima I, Wong S, Osmond CB (1988) Characterisation of non-uniform photosynthesis induced by abscisic acid in leaves having different mesophyll anatomies. Plant Cell Physiol 29:385–394Google Scholar
  236. Terashima I, Hanba YT, Tazoe Y, Vyas P, Yano S (2006) Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion. J Exp Bot 57:343–354PubMedCrossRefPubMedCentralGoogle Scholar
  237. Terashima I, Fujita T, Inoue T, Chow WS, Oguchi R (2009) Green light drives leaf photosynthesis more efficiently than red light in strong white light: revisiting the enigmatic question of why leaves are green. Plant Cell Physiol 50:684–697CrossRefGoogle Scholar
  238. Terashima I, Hanba YT, Tholen D, Niinemets U (2011) Leaf functional anatomy in relation to photosynthesis. Plant Physiol 155:108–116PubMedCrossRefPubMedCentralGoogle Scholar
  239. Terashima I, Ooeda H, Fujita T, Oguchi R (2016) Light environment within a leaf. II. Progress in the past one-third century. J Plant Res 129:353–363CrossRefGoogle Scholar
  240. Théroux-Rancourt G, Gilbert ME (2017) The light response of mesophyll conductance is controlled by structure across leaf profiles. Plant Cell Environ 40:726–740PubMedCrossRefPubMedCentralGoogle Scholar
  241. Théroux-Rancourt G, Ethier G, Pepin S (2014) Threshold response of mesophyll CO2 conductance to leaf hydraulics in highly transpiring hybrid poplar clones exposed to soil drying. J Exp Bot 65:741–753PubMedCrossRefPubMedCentralGoogle Scholar
  242. Théroux-Rancourt G, Éthier G, Pepin S (2015) Greater efficiency of water use in poplar clones having a delayed response of mesophyll conductance to drought. Tree Physiol 35:172–184PubMedCrossRefPubMedCentralGoogle Scholar
  243. Tholen D (2005) Growth and Photosynthesis in Ethylene-Insensitive Plants. Utrecht University, Utrecht, The NetherlandsGoogle Scholar
  244. Tholen D, Zhu X-G (2011) The mechanistic basis of internal conductance: a theoretical analysis of mesophyll cell photosynthesis and CO2 diffusion. Plant Physiol 156:90–105PubMedCrossRefPubMedCentralGoogle Scholar
  245. Tholen D, Boom C, Noguchi K, Ueda S, Katase T, Terashima I (2008) The chloroplast avoidance response decreases internal conductance to CO2 diffusion in Arabidopsis thaliana leaves. Plant Cell Environ 31:1688–1700PubMedCrossRefPubMedCentralGoogle Scholar
  246. Tholen D, Ethier G, Genty B, Pepin S, Zhu X-G (2012a) Variable mesophyll conductance revisited: theoretical background and experimental implications. Plant Cell Environ 35:2087–2103PubMedCrossRefPubMedCentralGoogle Scholar
  247. Tholen D, Boom C, Zhu X-G (2012b) Opinion: prospects for improving photosynthesis by altering leaf anatomy. Plant Sci 197:92–101PubMedCrossRefPubMedCentralGoogle Scholar
  248. Tomas M, Flexas J, Copolovici L, Galmés J, Hallik L, Medrano H et al (2013) Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models. J Exp Bot 64:2269–2281PubMedCrossRefPubMedCentralGoogle Scholar
  249. Tomas M, Medrano H, Brugnoli E, Escalona JM, Martorell S, Pou A, Ribas-Carbó M, Flexas J (2014) Variability of mesophyll conductance in grapevine cultivars under water stress conditions in relation to leaf anatomy and water use efficiency. Aust J Grape Wine Res 20:272–280CrossRefGoogle Scholar
  250. Tominaga J, Kawamitsu Y (2015) Cuticle affects calculations of internal CO2 in leaves closing their stomata. Plant Cell Physiol 56:1900–1908PubMedCrossRefGoogle Scholar
  251. Tosens T, Niinemets Ü, Vislap V, Eichelmann H, Castro Diez P (2012a) 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 35:839–856PubMedCrossRefGoogle Scholar
  252. Tosens T, Niinemets Ü, Westoby M, Wright IJ (2012b) Anatomical basis of variation in mesophyll resistance in eastern Australian sclerophylls: news of a long and winding path. J Exp Bot 63:5105–5119PubMedCrossRefPubMedCentralGoogle Scholar
  253. Tosens T, Nishida K, Gago J, Coopman RE, Cabrera HM, Carriquí M et al (2015) The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait. New Phytol 209:1576–1590PubMedCrossRefPubMedCentralGoogle Scholar
  254. Tremmel I, Kirchhoff H, Weis E, Farquhar GD (2003) Dependence of plastoquinol diffusion on the shape, size, and density of integral thylakoid proteins. Biochim Biophys Acta 1607:97–109PubMedCrossRefGoogle Scholar
  255. Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–737PubMedCrossRefGoogle Scholar
  256. 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 20:648–657PubMedCrossRefPubMedCentralGoogle Scholar
  257. Uehlein N, Sperling H, Heckwolf M, Kaldenhoff R (2012) The Arabidopsis aquaporin PIP1;2 rules cellular CO2 uptake. Plant Cell Environ 35:1077–1083PubMedCrossRefGoogle Scholar
  258. Valentini R, Epron D, Angelis P, Matteucci G, Dreyer E (1995) In situ estimation of net CO2 assimilation, photosynthetic electron flow and photorespiration in Turkey oak (Q. cerris L.) leaves: diurnal cycles under different levels of water supply. Plant Cell Environ 18:631–640CrossRefGoogle Scholar
  259. Van Gestel K, Kohler RH, Verbelen JP (2002) Plant mitochondria move on F-actin, but their positioning in the cortical cytoplasm depends on both F-actin and microtubules. J Exp Bot 53:659–667PubMedCrossRefPubMedCentralGoogle Scholar
  260. Verdoucq L, Rodrigues O, Martinière A, Luu DT, Maurel C (2014) Plant aquaporins on the move: reversible phosphorylation, lateral motion and cycling. Curr Opin Plant Biol 22:101–107PubMedCrossRefPubMedCentralGoogle Scholar
  261. Veromann-Jürgenson LL, Tosens T, Laanisto L, Niinemets Ü (2017) Extremely thick cell walls and low mesophyll conductance: welcome to the world of ancient living. J Exp Bot 68:1639–1653PubMedCrossRefPubMedCentralGoogle Scholar
  262. Vesala T, Ahonen T, Hari P, Krissinel E, Shokhirev N (1996) Analysis of stomatal CO2 uptake by a three-dimensional cylindrically symmetric model. New Phytol 132:235–245CrossRefGoogle Scholar
  263. Vogelmann TC, Nishio JN, Smith WK (1996) Leaves and light capture: light propagation and gradients of carbon fixation within leaves. Trends Plant Sci 1:65–70CrossRefGoogle Scholar
  264. Volkova L, Bennett LT, Tausz M (2009) Effects of sudden exposure to high light levels on two tree fern species Dicksonia antarctica (Dicksoniaceae) and Cyathea australis (Cyatheaceae) acclimated to different light intensities. Aust J Bot 57:562–571CrossRefGoogle Scholar
  265. von Caemmerer S (2000) Biochemical models of leaf photosynthesis. CSIRO, CollingwoodGoogle Scholar
  266. von Caemmerer S (2013) Steady-state models of photosynthesis. Plant Cell Environ 36:1617–1630CrossRefGoogle Scholar
  267. von Caemmerer S, Evans JR (2015) Temperature responses of mesophyll conductance differ greatly between species. Plant Cell Environ 38:629–637CrossRefGoogle Scholar
  268. von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387CrossRefGoogle Scholar
  269. 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
  270. Vrabl D, Vaskova M, Hronkova M, Flexas J, Santrucek J (2009) Mesophyll conductance to CO2 transport estimated by two independent methods: effect of variable CO2 concentration and abscisic acid. J Exp Bot 60:2315–2323PubMedCrossRefGoogle Scholar
  271. Wada M, Suetsugu N (2004) Plant organelle positioning. Curr Opin Plant Biol 7:626–631PubMedCrossRefGoogle Scholar
  272. Wada M, Kagawa T, Sato Y (2003) Chloroplast movement. Annu Rev Plant Biol 54:455–468PubMedCrossRefGoogle Scholar
  273. Walker BJ, Ort DR (2015) Improved method for measuring the apparent CO2 photocompensation point resolves the impact of multiple internal conductances to CO2 to net gas exchange. Plant Cell Environ 38:2462–2474PubMedCrossRefGoogle Scholar
  274. 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 36:2108–2119PubMedCrossRefGoogle Scholar
  275. Warren C (2006) Estimating the internal conductance to CO2 movement. Funct Plant Biol 33:431–442CrossRefGoogle Scholar
  276. Warren CR, Dreyer E (2006) Temperature response of photosynthesis and internal conductance to CO2: results from two independent approaches. J Exp Bot 57:3057–3067PubMedCrossRefGoogle Scholar
  277. Warren C, Löw M, Matyssek R, Tausz M (2007) Internal conductance to CO2 transfer of adult Fagus sylvatica: variation between sun and shade leaves and due to free-air ozone fumigation. Environ Exp Bot 59:130–138CrossRefGoogle Scholar
  278. Warren CR, Aranda I, Cano FJ (2011) Responses to water stress of gas exchange and metabolites in Eucalyptus and Acacia spp. Plant Cell Environ 34:1609–1629PubMedCrossRefPubMedCentralGoogle Scholar
  279. Weissbach A, Horecker BL, Hurwitz J (1956) Enzymatic formation of phosphoglyceric acid from ribulose diphosphate and carbon dioxide. J Biol Chem 218:795–810PubMedGoogle Scholar
  280. Williams TG, Flanagan LB (1998) Measuring and modelling environmental influences on photosynthetic gas exchange in Sphagnum and Pleurozium. Plant Cell Environ 21:555–564CrossRefGoogle Scholar
  281. Williams LE, Kennedy RA (1978) Photosynthetic carbon metabolism during leaf ontogeny in Zea mays L.: enzyme Studies. Planta 142:269–274PubMedCrossRefGoogle Scholar
  282. Williams TG, Flanagan LB, Coleman JR (1996) Photosynthetic gas exchange and discrimination against 13CO2 and C18O16O in tobacco plants modified by an antisense construct to have low chloroplastic carbonic anhydrase. Plant Physiol 112:319–326PubMedCrossRefPubMedCentralGoogle Scholar
  283. 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 30:600–616PubMedCrossRefGoogle Scholar
  284. Woodruff DR, Meinzer FC, Lachenbruch B, Johnson DM (2009) Coordination of leaf structure and gas exchange along a height gradient in a tall conifer. Tree Physiol 29:261–272PubMedCrossRefGoogle Scholar
  285. Wuyts N, Massonnet C, Dauzat M, Granier C (2012) Structural assessment of the impact of environmental constraints on Arabidopsis thaliana leaf growth: a 3D approach. Plant Cell Environ 35:1631–1646PubMedCrossRefGoogle Scholar
  286. Xiong D, Yu T, Zhang T, Li Y, Peng S, Huang J (2015a) Leaf hydraulic conductance is coordinated with leaf morpho-anatomical traits and nitrogen status in the genus Oryza. J Exp Bot 66:741–748PubMedCrossRefGoogle Scholar
  287. Xiong D, Liu X, Liu L, Douthe C, Li Y, Peng S, Huang J (2015b) Rapid responses of mesophyll conductance to changes of CO2 concentration, temperature and irradiance are affected by N supplements in rice. Plant Cell Environ 38:2541–2550PubMedCrossRefGoogle Scholar
  288. Xiong D, Chen J, Yu T, Gao W, Ling X, Li Y et al (2015c) SPAD-based leaf nitrogen estimation is impacted by environmental factors and crop leaf characteristics. Sci Rep 5:13389PubMedCrossRefPubMedCentralGoogle Scholar
  289. Xiong D, Wang D, Liu X, Peng S, Huang J, Li Y (2016) Leaf density explains variation in leaf mass per area in rice between cultivars and nitrogen treatments. Ann Bot 117:963–971PubMedCrossRefPubMedCentralGoogle Scholar
  290. Yamori W, Noguchi K, Hanba YT, Terashima I (2006) Effects of internal conductance on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant Cell Physiol 47:1069–1080PubMedCrossRefGoogle Scholar
  291. Yaneff A, Sigaut L, Marquez M, Alleva K, Isabel Pietrasanta L, Amodeo G (2014) Heteromerization of PIP aquaporins affects their intrinsic permeability. Proc Natl Acad Sci USA 111:231–236PubMedCrossRefGoogle Scholar
  292. Yaneff A, Vitali V, Amodeo G (2015) PIP1 aquaporins: intrinsic water channels or PIP2 aquaporin modulators? FEBS Lett 589:3508–3515PubMedCrossRefGoogle Scholar
  293. Yang B, Fukuda N, van Hoek A, Matthay MA, Ma T, Verkman A (2000) Carbon dioxide permeability of aquaporin-1 measured in erythrocytes and lung of aquaporin-1 null mice and in reconstituted proteoliposomes. J Biol Chem 275:2686–2692PubMedCrossRefGoogle Scholar
  294. 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 132:211–220PubMedCrossRefPubMedCentralGoogle Scholar
  295. Yin X, Struik PC, Romero P, Harbinson J, Evers JB, Van Der Puten PEL, Vos J (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 32:448–464PubMedCrossRefGoogle Scholar
  296. Zhang S-B, Sun M, Cao K-F, Hu H, Zhang J-L (2014) Leaf photosynthetic rate of tropical ferns is evolutionarily linked to water transport capacity. PLoS One 9:e84682PubMedCrossRefPubMedCentralGoogle Scholar
  297. Zhu X-G, 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 36:1711–1727PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Jaume Flexas
    • 1
    Email author
  • Francisco Javier Cano
    • 2
  • Marc Carriquí
    • 1
  • Rafael E. Coopman
    • 3
  • Yusuke Mizokami
    • 4
  • Danny Tholen
    • 5
  • Dongliang Xiong
    • 6
  1. 1.Research Group on Plant Biology under Mediterranean ConditionsUniversitat de les Illes Balears – Instituto de investigaciones Agroambientales y de la Economía del Agua (INAGEA)PalmaSpain
  2. 2.ARC Center of Translational Photosynthesis and Hawkesbury Institute for the EnvironmentWestern Sydney UniversitySydneyAustralia
  3. 3.Instituto de Conservación, Biodiversidad y Territorio, Facultad de Ciencias Forestales y Recursos NaturalesUniversidad Austral de ChileValdiviaChile
  4. 4.Department of Biological Sciences, Graduate School of ScienceThe University of TokyoTokyoJapan
  5. 5.Institute of Botany, Department of Integrative Biology and Biodiversity ResearchUniversity of Natural Resources and Applied Life Sciences (BOKU) ViennaViennaAustria
  6. 6.College of Plant Science and TechnologyHuazhong Agricultural UniversityWuhanChina

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