Mesophyll diffusion conductance to CO2: An unappreciated central player in photosynthesis

Plant Science

Volumn 193-194, Issue , 2012, Pages 70-84

  Flexas, Jaume ^a   Barbour, Margaret M ^b   Brendel, Oliver ^c,d   Cabrera, Hernán M ^a,e   Carriquí, Marc ^a   Díaz Espejo, Antonio ^f   Douthe, Cyril ^b,c,d   Dreyer, Erwin ^c,d   Ferrio, Juan P ^g   Gago, Jorge ^a   Gallé, Alexander ^a   Galmés, Jeroni ^a   Kodama, Naomi ^h   Medrano, Hipólito ^a   Niinemets, Ülo ⁱ   Peguero Pina, José J ^a   Pou, Alicia ^a   Ribas Carbó, Miquel ^a   Tomás, Magdalena ^a   Tosens, Tiina ⁱ   Warren, Charles R ^b   more..

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^b UNIVERSITY OF SYDNEY   (Australia)

^c LERFoB   (France)

^d UNIVERSITÉ DE LORRAINE   (France)

^e CENTRO DE ECOLOGÍA APLICADA LTDA   (Chile)

^f INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SEVILLA   (Spain)

^g UNIVERSITY OF LLEIDA   (Spain)

^h NATIONAL INSTITUTE FOR AGRO ENVIRONMENTAL SCIENCES   (Japan)

ⁱ ESTONIAN UNIVERSITY OF LIFE SCIENCES   (Estonia)

Author keywords

Aquaporins; Climate change; Conductance; Diffusion; Leaf anatomy; Photosynthesis; Plant hydraulics

Indexed keywords

CARBON DIOXIDE; CHLOROPHYLL;

CELL WALL; CHLOROPLAST; CYTOLOGY; DIFFUSION; MESOPHYLL CELL; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; REVIEW; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CARBON DIOXIDE; CELL WALL; CHLOROPHYLL; CHLOROPLASTS; DIFFUSION; MESOPHYLL CELLS; PHOTOSYNTHESIS; PLANT LEAVES;

EID: 84862249872     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plantsci.2012.05.009     Document Type: Review

References (157)

1. 2 resistance: photosynthetic implications of variations with growth conditions and plant species. Physiologia Plantarum 1977, 40:137-144.
2. Nobel P.S. Biophysical Plant Physiology and Ecology 1983, W.H. Freeman and Company, San Francisco.
3. Gaastra P. Photosynthesis of Crop Plants as Influenced by Light, Carbon Dioxide, Temperature, and Stomatal Diffusion Resistance 1959, vol. 59. Mededelingen van Landbouwhogeschool te Wageningen, Nederland, pp. 1-68.
4. 2 diffusion in leaves of higher plants. Functional Plant Biology 1986, 13:281-292.
5. 2. Plant Physiology 1992, 98:1429-1436.
6. Bongi G., Loreto F. Gas-exchange properties of salt-stressed olive (Olea europaea L.) leaves. Plant Physiology 1989, 90:1408-1416.
7. 2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant, Cell and Environment 2004, 27:137-153.
8. Niinemets Ü., Cescatti A., Rodeghiero M., Tosens T. Leaf internal diffusion conductance limits photosynthesis more strongly in older leaves of Mediterranean evergreen broad-leaved species. Plant, Cell and Environment 2005, 28:1552-1566.
9. 2 movement. Functional Plant Biology 2006, 33:431-442.
10. 2: Methodology, potential errors, and recommendations. Journal of Experimental Botany 2009, 60:2217-2234.
11. 2 diffusion in leaves of C3 plants by analysis of combined gas exchange and chlorophyll fluorescence measurements. Plant, Cell and Environment 2009, 32:1513-1524.
12. 2: Current knowledge and future prospects. Plant, Cell and Environment 2008, 31:602-621.
13. 2 diffusion pathway inside leaves. Journal of Experimental Botany 2009, 60:2235-2248.
14. Niinemets U., Diaz-Espejo A., Flexas J., Galmes J., Warren C.R. Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. Journal of Experimental Botany 2009, 60:2249-2270.
15. Tosens T., Niinemets Ü., Vislap V., Eichelmann H., Castro-Díez P. Developmental changes in mesophyll diffusion conductance and photosynthetic capacity under different light and water availabilities in Populus tremula: How structure constrains function. Plant, Cell and Environment 2012, 35:839-856.
16. Terashima I., Hanba Y.T., Tholen D., Niinemets Ü. Leaf functional anatomy in relation to photosynthesis. Plant Physiology 2011, 155:108-116.
17. Meyer M., Seibt U., Griffiths H. To concentrate or ventilate? Carbon acquisition, isotope discrimination and physiological ecology of early land plant life forms. Philosophical Transactions of the Royal Society B: Biological Sciences 2008, 363:2767-2778.
18. Feild T.S., Brodribb T.J., Iglesias A., Chatelet D.S., Baresch A., Upchurch G.R.J., Gomez B., Mohr B.A., Coiffard C., Kvacek J., Jaramillo C. Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:8363-8366.
19. 2 and water vapor exchange across leaf cuticle (epidermis) at various water potentials. Plant Physiology 1997, 114:185-191.
20. Niinemets Ü., Reichstein M. Controls on the emission of plant volatiles through stomata: A sensitivity analysis. Journal of Geophysical Research, Atmospheres 2003, 108:4211. 10.1029/2002JD002626.
21. 2- and their dependence on isotopic mass. Geochimica et Cosmochimica Acta 2011, 75:2483-2498.
22. 2 assimilation. Planta 1994, 193:331-340.
23. 16O in tobacco plants modified by an antisense construct to have low chloroplastic carbonic anhydrase. Plant Physiology 1996, 112:319-326.
24. 18OO discrimination in C3 leaves. Plant Physiology 2000, 123:201-213.
25. Fabre N., Reiter I.M., Becuwe-Linka N., Genty B., Rumeau D. Characterization and expression analysis of genes encoding α and β carbonic anhydrases in Arabidopsis. Plant, Cell and Environment 2007, 30:617-629.
26. 2 channels. ChemPhysChem 2011, 12:1017-1019.
27. 2 permeation through membrane channels still controversial. ChemPhysChem 2011, 12:1021-1022.
28. Missner A., Kügler P., Saparov S.M., Sommer K., Mathai J.C., Zeidel M.L., Pohl P. Carbon dioxide transport through membranes. Journal of Biological Chemistry 2008, 283:25340-25347.
29. 2 permeability of Xenopus oocytes expressing aquaporin 1 or its C189S mutant. American Journal of Physiology 1998, 275:1481-1486.
30. 2 transport across the human erythrocyte membrane. FASEB Journal 2006, 20:1974-1981.
31. 2 permeability of Xenopus oocytes. American Journal of Physiology 1998, 274:C543-C548.
32. 2 transport facilitator. Plant Journal 2011, 67:795-804.
33. 2 permeability. Plant Cell 2008, 20:648-657.
34. 2 pore with physiological functions. Nature 2003, 425:734-737.
35. 2 in vivo. Plant Journal 2006, 48:427-439.
36. 2 assimilation in the leaves of transgenic rice plants. Plant and Cell Physiology 2004, 45:521-529.
37. 2 diffusion and contents of aquaporin localized at plasma membrane in tobacco plants grown under drought conditions. Photosynthesis. Energy from the Sun: 14th International Congress on Photosynthesis 2008, 805-808. Springer, Berlin. J.F. Allen, E. Gantt, J.H. Golbeck, B. Osmond (Eds.).
38. 2 diffusion in tobacco leaves grown under long-term drought. Functional Plant Biology 2008, 35:553-564.
39. 2 diffusion across the plasma membrane. Plant and Cell Physiology 2002, 43:70-78.
40. Aharon R., Shahak Y., Wininger S., Bendov R., Kapulnik Y., Galili G. Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell 2003, 15:439-447.
41. Niinemets U., Diaz-Espejo A., Flexas J., Galmes J., Warren C.R. Importance of mesophyll diffusion conductance in estimation of plant photosynthesis in the field. Journal of Experimental Botany 2009, 60:2271-2282.
42. Grassi G., Magnani F. Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant, Cell and Environment 2005, 28:834-849.
43. 2 concentrations. Global Change Biology 1999, 5:455-470.
44. Niinemets Ü., Tenhunen J.D. A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant, Cell and Environment 1997, 20:845-866.
45. 2 permeate through aquaporin-1?. Biophysical Journal 2006, 91:842-848.
46. Hub J.S., de Groot B.L. Mechanism of selectivity in aquaporins and aquaglyceroporins. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:1198-1203.
47. Hub J.S., Grubmüller H., Groot B.L., Beitz E. Dynamics and energetics of permeation through aquaporins. What do we learn from molecular dynamics simulations?. Handbook of Experimental Pharmacology 2009, Springer, Berlin, Heidelberg, pp. 57-76.
48. Maurel C. Plant aquaporins: Novel functions and regulation properties. FEBS Letters 2007, 581:2227-2236.
49. Maurel C., Verdoucq L., Luu D.-T., Santoni V. Plant aquaporins: Membrane channels with multiple integrated functions. Annual Review of Plant Biology 2008, 59:595-624.
50. Otto B., Uehlein N., Sdorra S., Fischer M., Ayaz M., Belastegui-Macadam X., Heckwolf M., Lachnit M., Pede N., Priem N., Reinhard A., Siegfart S., Urban M., Kaldenhoff R. Aquaporin tetramer composition modifies the function of tobacco aquaporins. Journal of Biological Chemistry 2010, 285:31253-31260.
51. Uehlein N., Sperling H., Heckwolf M., Kaldenhoff R. The Arabidopsis aquaporin PIP1;2 rules cellular CO2 uptake. Plant, Cell and Environment 2012, 35:1077-1083.
52. Laisk A., Oja V., Rahi M. Diffusion resistances as related to the leaf anatomy. Fiziologiya Rastenii 1970, 17:40-48.
53. Nobel P.S. Physicochemical and Environmental Plant Physiology 1991, Academic Press, Inc, San Diego, New York, Boston, London, Sydney, Tokyo, Toronto. 4th edn.
54. Nobel P.S., Zaragoza L.T., Smith W.K. Relation between mesophyll surface area, photosynthetic rate, and illumination level during development for leaves of Plectranthus parviflorus Henckel. Plant Physiology 1975, 55:1067-1070.
55. Rahi M. Ob anatomicheskih parametrah lista v svyazi s diffuzionnymi soprotivleniyami. (The characteristics of leaf anatomy and diffusion resistances). Proceedings of the Academy of Sciences of the Estonian SSR: Biology 1971, 20:85-94.
56. 3-plants) 1977, Nauka, Moscow.
57. Oguchi R., Hikosaka K., Hirose T. Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant, Cell and Environment 2005, 28:916-927.
58. Terashima I., Araya T., Miyazawa S.-I., Sone K., Yano S. Construction and maintenance of the optimal photosynthetic systems of the leaf, herbaceous plant and tree: An eco-developmental treatise. Annals of Botany 2005, 95:507-519.
59. 2 diffusion. Journal of Experimental Botany 2006, 57:343-354.
60. J.J. Peguero-Pina, J. Flexas, J. Galmés, D. Sancho-Knapik, G. Barredo, D. Villarroya, E. Gil-Pelegrín, Leaf anatomical properties in relation to differences in mesophyll conductance to CO2 and photosynthesis in two related Mediterranean Abies species, Plant, Cell and Environment, doi:10.1111/j.1365-3040.2012.02540.x.
61. Niinemets Ü., Wright I.J., Evans J.R. Leaf mesophyll diffusion conductance in 35 Australian sclerophylls covering a broad range of foliage structural and physiological variation. Journal of Experimental Botany 2009, 60:2433-2449.
62. Hassiotou F., Renton M., Ludwig M., Evans J.R., Veneklaas E.J. Photosynthesis at an extreme end of the leaf trait spectrum: how does it relate to high leaf dry mass per area and associated structural parameters?. Journal of Experimental Botany 2010, 61:3015-3028.
63. Oguchi R., Hikosaka K., Hiura T., Hirose T. Leaf anatomy and light acclimation in woody seedlings after gap formation in a cool-temperate forest. Oecologia 2006, 149:571-582.
64. Flexas J., Baron M., Bota J., Ducruet J.-M., Galle A., Galmes J., Jimenez M., Pou A., Ribas-Carbo M., Sajnani C., Tomas M., Medrano H. Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandieri×V. rupestris). Journal of Experimental Botany 2009, 60:2361-2377.
65. Galle A., Florez-Sarasa I., Tomas M., Pou A., Medrano H., Ribas-Carbo M., Flexas J. The role of mesophyll conductance during water stress and recovery in tobacco (Nicotiana sylvestris): Acclimation or limitation?. Journal of Experimental Botany 2009, 60:2379-2390.
66. Hu L.X., Wang Z.L., Huang B.R. Diffusion limitations and metabolic factors associated with inhibition and recovery of photosynthesis from drought stress in a C-3 perennial grass species. Physiologia Plantarum 2010, 139:93-106.
67. Warren C.R., Aranda I., Cano F.J. Responses to water stress of gas exchange and metabolites in Eucalyptus and Acacia spp. Plant, Cell and Environment 2011, 34:1609-1629.
68. Bunce J.A. Use of the response of photosynthesis to oxygen to estimate mesophyll conductance to carbon dioxide in water-stressed soybean leaves. Plant, Cell and Environment 2009, 32:875-881.
69. Galle A., Florez-Sarasa I., Aououad H.E., Flexas J. The Mediterranean evergreen Quercus ilex and the semi-deciduous Cistus albidus differ in their leaf gas exchange regulation and acclimation to repeated drought and re-watering cycles. Journal of Experimental Botany 2011, 62:5207-5216.
70. Centritto M., Lauteri M., Monteverdi M.C., Serraj R. Leaf gas exchange, carbon isotope discrimination, and grain yield in contrasting rice genotypes subjected to water deficits during the reproductive stage. Journal of Experimental Botany 2009, 60:2325-2339.
71. Gulias J., Cifre J., Jonasson S., Medrano H., Flexas J. Seasonal and inter-annual variations of gas exchange in thirteen woody species along a climatic gradient in the Mediterranean island of Mallorca. Flora 2009, 204:169-181.
72. Varone L., Ribas-Carbo M., Cardona C., Galle A., Medrano H., Gratani L., Flexas J. Stomatal and non-stomatal limitations to photosynthesis in seedlings and saplings of Mediterranean species pre-conditioned and aged in nurseries: Different response to water stress. Environmental and Experimental Botany 2012, 75:235-247.
73. Resco V., Ewers B.E., Sun W., Huxman T.E., Weltzin J.F., Williams D.G. Drought-induced hydraulic limitations constrain leaf gas exchange recovery after precipitation pulses in the C3 woody legume, Prosopis velutina. New Phytologist 2009, 181:672-682.
74. Bown H.E., Watt M.S., Mason E.G., Clinton P.W., Whitehead D. The influence of nitrogen and phosphorus supply and genotype on mesophyll conductance limitations to photosynthesis in Pinus radiata. Tree Physiology 2009, 29:1143-1151.
75. 2 concentration. Journal of Experimental Botany 2009, 60:2351-2360.
76. 2 assimilation at different temperatures is influenced by the leaf nitrogen content in several C3 crop species. Plant, Cell and Environment 2011, 34:764-777.
77. Han Q. Height-related decreases in mesophyll conductance, leaf photosynthesis and compensating adjustments associated with leaf nitrogen concentrations in Pinus densiflora. Tree Physiology 2011, 31:976-984.
78. Woodruff D.R., Meinzer F.C., Lachenbruch B., Johnson D.M. Coordination of leaf structure and gas exchange along a height gradient in a tall conifer. Tree Physiology 2009, 29:261-272.
79. Whitehead D., Barbour M.M., Griffin K.L., Turnbull M.H., Tissue D.T. Effects of leaf age and tree size on stomatal and mesophyll limitations to photosynthesis in mountain beech (Nothofagus solandrii var. cliffortiodes). Tree Physiology 2011, 31:985-996.
80. Jin S.H., Huang J.Q., Li X.Q., Zheng B.S., Wu J.S., Wang Z.J., Liu G.H., Chen M. Effects of potassium supply on limitations of photosynthesis by mesophyll diffusion conductance in Carya cathayensis. Tree Physiology 2011, 31:1142-1151.
81. 2 are the main limitations to photosynthesis in sugar beet (Beta vulgaris) plants grown with excess zinc. New Phytologist 2010, 187:145-158.
82. 2, and isoprenoid emissions in Populus nigra plants exposed to excess nickel. Environmental Pollution 2011, 159:1058-1066.
83. 2 enrichment (FACE) stimulates photosynthesis while decreasing in vivo Rubisco capacity. Planta 2005, 220:434-446.
84. 2 effects on mesophyll conductance and its consequences for interpreting photosynthetic physiology. Plant, Cell and Environment 2003, 27:41-50.
85. Bunce J.A. Variable responses of mesophyll conductance to substomatal carbon dioxide concentration in common bean and soybean. Photosynthetica 2010, 48:507-512.
86. 2 and irradiance in Eucalyptus seedlings. Journal of Experimental Botany 2011, 62:5335-5346.
87. 2 concentration around leaves. Plant, Cell and Environment 2007, 30:1284-1298.
88. 2, and irradiance on mesophyll conductance in sclerophylls. Journal of Experimental Botany 2009, 60:2303-2314.
89. 2 concentrations. Plant, Cell and Environment 2011, 34:580-591.
90. 2 and high temperature. Environmental Pollution 2009, 157:2629-2637.
91. 2 concentration and abscisic acid. Journal of Experimental Botany 2009, 60:2315-2323.
92. 2 diffusion in wheat leaves. Journal of Experimental Botany 2009, 60:2291-2301.
93. 2 transfer to chloroplasts in leaves of grapevine (Vitis vinifera L.). Vitis 2003, 42:65-68.
94. 2 flux by three different methods. Plant Physiology 1992, 98:1437-1443.
95. 2 diffusion. Plant Physiology 2011, 156:90-105.
96. C. Douthe, Relationship between leaf gas exchange and 13C discrimination during photosynthesis: Estimations and rapid variations of mesophyll conductance to CO2, PhD Disseratation, 2011.
97. Jones H.G. Moderate-term water stresses and associated changes in some photosynthetic parameters in cotton. New Phytologist 1973, 72:1095-1105.
98. Galmes J., Medrano H., Flexas J. Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytologist 2007, 175:81-93.
99. Diaz-Espejo A., Nicolas E., Fernandez J.E. Seasonal evolution of diffusional limitations and photosynthetic capacity in olive under drought. Plant, Cell and Environment 2007, 30:922-933.
100. Grassi G., Vicinelli E., Ponti F., Cantoni L., Magnani F. Seasonal and interannual variability of photosynthetic capacity in relation to leaf nitrogen in a deciduous forest plantation in northern Italy. Tree Physiology 2005, 25:349-360.
101. Limousin J.-M., Misson L., Lavoir A.-V., Martin N.K., Rambal S. Do photosynthetic limitations of evergreen Quercus ilex leaves change with long-term increased drought severity?. Plant, Cell and Environment 2010, 33:863-875.
102. 2 in Vitis vinifera and Olea europaea. Journal of Experimental Botany 2009, 60:2391-2405.
103. Egea G., Verhoef A., Vidale P.L. Towards an improved and more flexible representation of water stress in coupled photosynthesis-stomatal conductance models. Agricultural and Forest Meteorology 2011, 151:1370-1384.
104. Misson L., Limousin J.-M., Rodriguez R., Letts M.G. Leaf physiological responses to extreme droughts in Mediterranean Quercus ilex forest. Plant, Cell and Environment 2010, 33:1898-1910.
105. Egea G., Verhoef A., Vidale P.L. Towards an improved and more flexible representation of water stress in coupled photosynthesis-stomatal conductance models. Agricultural and Forest Meteorologyis 2011, 151:1370-1384.
106. Zhang S.B. Temperature acclimation of photosynthesis in Meconopsis horridula var. racemosa Prain. Botanical Studies 2010, 51:457-464. (Chinese Source).
107. Warren C.R., Ethier G.J., Livingston N.J., Grant N.J., Turpin D.H., Harrison D.L., Black T.A. Transfer conductance in second growth Douglas-fir (Pseudotsuga menziesii (Mirb.)Franco) canopies. Plant, Cell and Environment 2003, 26:1215-1227.
108. Niinemets Ü., Cescatti A., Rodeghiero M., Tosens T. Complex adjustments of photosynthetic capacity and internal mesophyll conductance to current and previous light availabilities and leaf age in Mediterranean evergreen species Quercus ilex. Plant, Cell and Environment 2006, 29:1159-1178.
109. 2 across a beech (Fagus sylvatica L.) canopy. Journal of Experimental Botany 2009, 60:2407-2418.
110. Mullin L.P., Sillett S.C., Koch G.W., Tu K.P., Antoine M.E. Physiological consequences of height-related morphological variation in Sequoia sempervirens foliage. Tree Physiology 2009, 29:999-1010.
111. Niinemets Ü. Stomatal conductance alone does not explain the decline in foliar photosynthetic rates with increasing tree age and size in Picea abies and Pinus sylvestris. Tree Physiology 2002, 22:515-535.
112. Ryan M.G., Yoder B.J. Hydraulic limits to tree height and tree growth. What keeps trees from growing beyond a certain height?. BioScience 1997, 47:235-242.
113. Steppe K., Niinemets Ü., Teskey R.O. Tree size- and age-related changes in leaf physiology and their influence on carbon gain. Size- and Age-related Changes in Tree Structure and Function 2011, 235-253. Springer, Berlin. F.C. Meinzer, T. Dawson, B. Lachenbruch (Eds.).
114. Yoder B.J., Ryan M.G., Waring R.H., Schoettle A.W., Kaufmann M.R. Evidence of reduced photosynthetic rates in old trees. Forest Science 1994, 40:513-527.
115. Kull O., Koppel A. Net photosynthetic response to light intensity of shoots from different crown positions and age in Picea abies (L.) Karst. Scandinavian Journal of Forest Research 1987, 2:157-166.
116. Niinemets Ü. Distribution patterns of foliar carbon and nitrogen as affected by tree dimensions and relative light conditions in the canopy of Picea abies. Trees - Structure and Function 1997, 11:144-154.
117. Woodruff D.R., Meinzer F.C., Lachenbruch B. Height-related trends in leaf xylem anatomy and shoot hydraulic characteristics in a tall conifer: Safety versus efficiency in water transport. New Phytologist 2008, 180:90-99.
118. Williams M., Rastetter E.B., Fernandes D.N., Goulden M.L., Wofsy S.C., Shaver G.R., Melillo J.M., Munger J.W., Fan S.M., Nadelhoffer K.J. Modelling the soil-plant-atmosphere continuum in a Quercus-Acer stand at Harvard Forest: the regulation of stomatal conductance by light, nitrogen and soil/plant hydraulic properties. Plant, Cell and Environment 1996, 19:911-927.
119. 2 transfer in the leaves of two tree species (Fagus sylvatica L. and Castanea sativa Mill.). Plant, Cell and Environment 1995, 18:43-51.
120. Ohsumi A., Kanemura T., Homma K., Horie T., Shiraiwa T. Genotypic variation of stomatal conductance in relation to stomatal density and length in rice (Oryza sativa L.). Plant Production Science 2007, 10:322-328.
121. 2 in a coastal Douglas-fir forest. Plant, Cell and Environment 2008, 31:435-453.
122. Keenan T., Sabate S., Gracia C. The importance of mesophyll conductance in regulating forest ecosystem productivity during drought periods. Global Change Biology 2010, 16:1019-1034.
123. 13C discrimination: Results from a field study. Journal of Experimental Botany 2010, 61:3223-3233.
124. Farquhar G.D., Cernusak L.A. Ternary effects on the gas exchange of isotopologues of carbon dioxide. Plant, Cell and Environment 2012, 10.1111/j.1365-3040.2012.02484.x.
125. 2 in a land-surface scheme: Measurement and modeling of photosynthesis in Populus nigra. Agricultural and Forest Meteorologyis 2012, 152:240-251.
126. 13C of phloem contents. Plant, Cell and Environment 2011, 34:1521-1535.
127. Sack L., Streeter C.M., Holbrook N.M. Hydraulic analysis of water flow through leaves of sugar maple and red oak. Plant Physiology 2004, 134:1824-1833.
128. Steudle E., Frensch J. Water transport in plants: Role of the apoplast. Plant and Soil 1996, 187:67-79.
129. 2 carbon and oxygen isotope discrimination along leaves of the monocot triticale (Triticum×Secale) relates to mesophyll conductance and the Peclet effect. Plant, Cell and Environment 2011, 34:1548-1562.
130. Duan B., Li Y., Zhang X., Korpelainen H., Li C. Water deficit affects mesophyll limitation of leaves more strongly in sun than in shade in two contrasting Picea asperata populations. Tree Physiolohy 2009, 29:1551-1561.
131. Soolanayakanahally R.Y., Guy R.D., Silim S.N., Drewes E.C., Schroeder W.R. Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar (Populus balsamifera L.). Plant, Cell and Environment 2009, 32:1821-1832.
132. Flexas J., Galmes J., Galle A., Gulias J., Pou A., Ribas-Carbo M., Tomas M., Medrano H. Improving water use efficiency in grapevines: Potential physiological targets for biotechnological improvement. Australian Journal of Grape and Wine Research 2010, 16:106-121.
133. Galmes J., Conesa M.A.N., Ochogavia J.M., Perdomo J.A., Francis D.M., Ribas-Carbo M., Save R., Flexas J., Medrano H., Cifre J. Physiological and morphological adaptations in relation to water use efficiency in Mediterranean accessions of Solanum lycopersicum. Plant, Cell and Environment 2011, 34:245-260.
134. Sack L., Holbrook N.M. Leaf hydraulics. Annual Review of Plant Biology 2006, 57:361-381.
135. Aasamaa K., Sober A. Hydraulic conductance and stomatal sensitivity to changes of leaf water status in six deciduous tree species. Biologia Plantarum 2001, 44:65-73.
136. Brodribb T.J., Feild T.S., Jordan G.J. Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 2007, 144:1890-1898.
137. 2 transfer conductance and leaf stable carbon isotope ratio for some evergreen tree species in Japanese warm-temperate forests. Functional Ecology 1999, 13:632-639.
138. Sack L., Cowan P.D., Jaikumar N., Holbrook N.M. The 'hydrology' of leaves: Co-ordination of structure and function in temperate woody species. Plant, Cell and Environment 2003, 26:1343-1356.
139. Sack L., Frole K. Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology 2006, 87:483-491.
140. 2 in chloroplasts from leaves of several C3 plants. Functional Plant Biology 1991, 18:287-305.
141. Bunce J.A. How do leaf hydraulics limit stomatal conductance at high water vapour pressure deficits?. Plant, Cell and Environment 2006, 29:1644-1650.
142. Li Y.A.N., Xu H.A.O., Cohen S. Long-term hydraulic acclimation to soil texture and radiation load in cotton. Plant, Cell and Environment 2005, 28:492-499.
143. Cochard H., Nardini A., Coll L. Hydraulic architecture of leaf blades: Where is the main resistance?. Plant, Cell and Environment 2004, 27:1257-1267.
144. Mott K.A. Leaf hydraulic conductivity and stomatal responses to humidity in amphistomatous leaves. Plant, Cell and Environment 2007, 30:1444-1449.
145. Ferrio J.P., Cuntz M., Offermann C., Siegwolf R., Saurer M., Gessler A. Effect of water availability on leaf water isotopic enrichment in beech seedlings shows limitations of current fractionation models. Plant, Cell and Environment 2009, 32:1285-1296.
146. 2. Plant, Cell and Environment 2012, 35:611-625.
147. 18O enrichment of leaf water and its impact on 'effective path length'. New Phytologist 2009, 184:619-630.
148. Zhou Y., Grice K., Chikaraishi Y., Stuart-Williams H., Farquhar G.D., Ohkouchi N. Temperature effect on leaf water deuterium enrichment and isotopic fractionation during leaf lipid biosynthesis: Results from controlled growth of C3 and C4 land plants. Phytochemistry 2011, 72:207-213.
149. Craig H., Gordon L.I. Deuterium and Oxygen 18 Variations in the Ocean and Marine Atmosphere, Marine Geochemistry, Narragansett Marine Laboratory 1965, vol. 3. University of Rhode Island, pp. 277-374.
150. 18O in the leaves of transpiring plants. Radiation and Environmental Biophysics 1974, 11:41-52.
151. Farquhar G.D., Lloyd J. Carbon and oxygen isotope effects in the exchange of carbon dioxide between terrestrial plants and the atmosphere. Stable Isotopes and Plant Carbon-Water Relations 1993, 47-70. Academic Press, San Diego. J.R. Ehleringer, A.E. Hall, G.D. Farquhar (Eds.).
152. Barbour M.M., Fischer R.A., Sayre K.D., Farquhar G.D. Oxygen isotope ratio of leaf and grain material correlates with stomatal conductance and grain yield in irrigated wheat. Functional Plant Biology 2000, 27:625-637.
153. Cuntz M., Ogee J., Farquhar G.D., Peylin P., Cernusak L.A. Modelling advection and diffusion of water isotopologues in leaves. Plant, Cell and Environment 2007, 30:892-909.
154. 2] to estimate diffusional and non-diffusional limitations of photosynthetic capacity of salt-stressed olive saplings. Plant, Cell and Environment 2003, 26:585-594.
155. 2 concentration and abscisic acid. Plant, Cell and Environment 2011, 34:127-136.
156. Gomes F.P., Oliva M.A., Mielke M.S., de Almeida A.A.F., Leite H.G., Aquino L.A. Photosynthetic limitations in leaves of young Brazilian Green Dwarf coconut (Cocos nucifera L. 'nana') palm under well-watered conditions or recovering from drought stress. Environmental and Experimental Botany 2008, 62:195-204.
157. Grassi G., Ripullone F., Borghetti M., Raddi S., Magnani F. Contribution of diffusional and non-diffusional limitations to midday depression of photosynthesis in Arbutus unedo L. Trees - Structure and Function 2009, 23:1149-1161.