Advertisement

Photosynthesis Research

, Volume 117, Issue 1–3, pp 45–59 | Cite as

Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency

  • Jaume Flexas
  • Ülo Niinemets
  • Alexander Gallé
  • Margaret M. Barbour
  • Mauro Centritto
  • Antonio Diaz-Espejo
  • Cyril Douthe
  • Jeroni Galmés
  • Miquel Ribas-Carbo
  • Pedro L. Rodriguez
  • Francesc Rosselló
  • Raju Soolanayakanahally
  • Magdalena Tomas
  • Ian J. Wright
  • Graham D. Farquhar
  • Hipólito Medrano
Review

Abstract

A key objective for sustainable agriculture and forestry is to breed plants with both high carbon gain and water-use efficiency (WUE). At the level of leaf physiology, this implies increasing net photosynthesis (A N) relative to stomatal conductance (g s). Here, we review evidence for CO2 diffusional constraints on photosynthesis and WUE. Analyzing past observations for an extensive pool of crop and wild plant species that vary widely in mesophyll conductance to CO2 (g m), g s, and foliage A N, it was shown that both g s and g m limit A N, although the relative importance of each of the two conductances depends on species and conditions. Based on Fick’s law of diffusion, intrinsic WUE (the ratio A N/g s) should correlate on the ratio g m/g s, and not g m itself. Such a correlation is indeed often observed in the data. However, since besides diffusion A N also depends on photosynthetic capacity (i.e., V c,max), this relationship is not always sustained. It was shown that only in a very few cases, genotype selection has resulted in simultaneous increases of both A N and WUE. In fact, such a response has never been observed in genetically modified plants specifically engineered for either reduced g s or enhanced g m. Although increasing g m alone would result in increasing photosynthesis, and potentially increasing WUE, in practice, higher WUE seems to be only achieved when there are no parallel changes in g s. We conclude that for simultaneous improvement of A N and WUE, genetic manipulation of g m should avoid parallel changes in g s, and we suggest that the appropriate trait for selection for enhanced WUE is increased g m/g s.

Keywords

Photosynthesis Water-use efficiency Stomatal conductance Mesophyll conductance Meta-analysis 

Notes

Acknowledgments

This work was partly supported by the Plan Nacional, Spain, contracts AGL2002-04525-CO2-01 (H.M.), BFU2008-1072-E/BFI and BFU2011-23294 (M.R.-C. and J.F.), AGL2009-07999 (J.G.), and MTM2009-07165 (F.R.); the Foundation for Research, Science and Technology, New Zealand, contract C09X0701 (M.M.B); the Australian Research Council, contract FT0992063 (M.M.B), FT100100910 (I.J.W), and DP1097276 (G.D.F.); the Estonian Ministry of Science and Education, (institutional grant IUT-8-3); the European Commission through the European Regional Fund (the Center of Excellence in Environmental Adaptation) (Ü.N.); and a collaboration project between the Estonian Academy of Sciences and the Spanish CSIC (H.M., Ü.N.).

Supplementary material

11120_2013_9844_MOESM1_ESM.xls (89 kb)
Data compilation in different species and conditions (see Online Resource 3 for a complete list of the references used). Supplementary material 1 (XLS 89 kb)
11120_2013_9844_MOESM2_ESM.doc (46 kb)
Complete list of references from which data in Online Resource 2 and 4 were compiled. Supplementary material 2 (DOC 46 kb)
11120_2013_9844_MOESM3_ESM.xls (34 kb)
Data compilation for specific genetic manipulations. Supplementary material 3 (XLS 34 kb)
11120_2013_9844_MOESM4_ESM.doc (524 kb)
The relationship between g m/g s and g m in a multi-species dataset. Data and symbols as in Fig. 1. Supplementary material 4 (DOC 523 kb)

References

  1. Araus JL, Slafer GA, Royo C, Dolores Serre M (2008) Breeding for yield potential and stress adaptation in cereals. Crit Rev Plant Sci 27:377–412Google Scholar
  2. Barbour MM, Fischer RA, Sayre KD, Farquhar GD (2000) Oxygen isotope ratio of leaf and grain material correlates with stomatal conductance and grain yield in irrigated wheat. Aust J Plant Physiol 27:625–637Google Scholar
  3. Barbour MM, Warren CR, Farquhar GD, Forrester G, Brown H (2010) Variability in mesophyll conductance between barley genotypes, and effects on transpiration efficiency and carbon isotope discrimination. Plant Cell Environ 33:1176–1185PubMedGoogle Scholar
  4. Bickford CP, Hanson DT, McDowell NG (2010) Influence of diurnal variation in mesophyll conductance on modeled 13C discrimination: results from a field study. J Exp Bot 61:3223–3233PubMedGoogle Scholar
  5. Blum A (2005) Drought resistance, water-use efficiency, and yield potential—are they compatible, dissonant, or mutually exclusive? Aust J Agric Res 56:1159–1168Google Scholar
  6. Borel C, Frey A, Marion-Poll A, Tardieu F, Simmoneau T (2001) Does engineering abscisic acid biosynthesis in Nicotiana plumbaginifolia modify stomatal response to drought? Plant Cell Environ 24:477–489Google Scholar
  7. Borlaug N (2000) The green revolution revisited and the road ahead. Nobelprize.org.24. http://www.nobelprize.org/nobel_prizes/peace/laureates/1970/borlaug-article.html. Accessed 15 Jan 2013
  8. Boyer JS (1996) Advances in drought tolerance in plants. Adv Agron 56:187–218Google Scholar
  9. Centritto M, Lauteri M, Monteverdi MC, Serraj R (2009) Leaf gas exchange, carbon isotope discrimination, and grain yield in contrasting rice genotypes subjected to water deficits during the reproductive stress. J Exp Bot 60:2325–2339PubMedGoogle Scholar
  10. Christmann A, Hoffmann T, Teplova I, Grill E, Müller A (2005) Generation of active pools of abscisic acid revealed by in vivo imaging of water-stressed Arabidopsis. Plant Physiol 137:209–219PubMedGoogle Scholar
  11. Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004) Breeding for high water-use efficiency. J Exp Bot 55:2447–2460PubMedGoogle Scholar
  12. CSIRO Plant Industry (2004) Drysdale—a world’s first. CSIRO Plant Industry Communication Group. http://www.csiro.au/files/files/p2jr.pdf. Accessed 15 Jan 2013
  13. Dai A (2011) Drought under global warming: a review. Clim Change 2:45–65Google Scholar
  14. De Lucia EH, Whitehead W, Clearwater MJ (2003) The relative limitation of photosynthesis by mesophyll conductance in co-occurring species in a temperate rainforest dominated by the conifer Dacrydium cupressinum. Funct Plant Biol 30:1197–1204Google Scholar
  15. Diaz-Espejo A, Nicolás E, Fernández JE (2007) Seasonal evolution of diffusional limitations and photosynthetic capacity in olive under drought. Plant Cell Environ 30:922–933PubMedGoogle Scholar
  16. Edgerton MD (2009) Increasing crop productivity to meet global needs for feed, food, and fuel. Plant Physiol 149:7–13PubMedGoogle Scholar
  17. Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) Resistances along the CO2 diffusion pathway inside leaves. J Exp Bot 60:2235–2248PubMedGoogle Scholar
  18. Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345Google Scholar
  19. Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90Google Scholar
  20. Farquhar GD, Buckley TN, Miller JM (2002) Optimal stomatal control in relation to leaf area and nitrogen content. Silva Fennica 36:625–637Google Scholar
  21. Fereres E, Connor D (2004) Sustainable water management in agriculture. In: Challenges of the new water policies for the XXI century: Proceedings of the seminar on challenges of the new water policies for the 21st century, Valencia, 29–31 October 2002, Taylor & Francis, London, p. 157Google Scholar
  22. Flexas J, Bota J, Escalona JM, Sampol B, Medrano H (2002) Effects of drought on photosynthesis in grapevines under field conditions: an evaluation of stomatal and mesophyll limitations. Funct Plant Biol 29:461–471Google Scholar
  23. Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol 6:269–279PubMedGoogle Scholar
  24. Flexas J, Ribas-Carbó M, Hanson DT, Bota J, Otto B, Cifre J, McDowell N, Medrano H, Kaldenhoff R (2006a) Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. Plant J 48:427–439PubMedGoogle Scholar
  25. Flexas J, Ribas-Carbó M, Bota J, Galmés J, Henkle M, Martínez-Cañellas S, Medrano H (2006b) 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 172:73–82PubMedGoogle Scholar
  26. Flexas J, Diaz-Espejo A, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbo M (2007) Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant Cell Environ 30:1284–1298PubMedGoogle Scholar
  27. Flexas J, Ribas-Carbo M, Diaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–631PubMedGoogle Scholar
  28. Flexas J, Galmés J, Gallé A, Gulías J, Pou A, Ribas-Carbo M, Tomàs M, Medrano H (2010) Improving water use efficiency in grapevines: potential physiological targets for biotechnological improvement. Aust J Grape Wine Res 16:106–121Google Scholar
  29. Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriquí M, Diaz-Espejo A, Douthe C, Dreyer E, Ferrio JP, Gago J, Gallé A, Galmés J, Kodama N, Medrano H, Niinemets Ü, Peguero-Pina JJ, Pou A, Ribas-Carbó M, Tomás M, Tosens T, Warren CR (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Sci 193–194:70–84PubMedGoogle Scholar
  30. Franks PJ, Farquhar GD (1999) A relationship between humidity response, growth form and photosynthetic operating point in C3 plants. Plant Cell Environ 22:1337–1349Google Scholar
  31. Gaastra P (1959) Photosynthesis of crop plants as influenced by light, carbon dioxide, temperature and stomatal diffusion resistance. Meded Landbouwhogeseh Wageningen 59(13):1–68Google Scholar
  32. Galmés J, Flexas J, Keys AJ, Cifre J, Mitchell RAC, Madgwick PJ, Haslam RP, Medrano H, Parry MAJ (2005) Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant Cell Environ 28:571–579Google Scholar
  33. 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 175:81–93PubMedGoogle Scholar
  34. Galmés J, Conesa MÀ, Ochogavía JM, Perdomo JA, Francis DM, Ribas-Carbó M, Savé R, Flexas J, Medrano H, Cifre J (2011) Physiological and morphological adaptations in relation to water use efficiency in Mediterranean accessions of Solanum lycopersicum. Plant Cell Environ 34:245–260PubMedGoogle Scholar
  35. 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 28:834–849Google Scholar
  36. Gregory PJ (2004) Agronomic approaches to increasing water use efficiency. In: Bacon MA (ed) Water use efficiency in plant biology. Blackwell Publishing Ltd., Oxford, pp 142–167Google Scholar
  37. Hanba YT, Miyazawa S-I, Terashima I (1999) The influence of leaf thickness on the CO2 transfer conductance and leaf stable carbon isotope ratio for some evergreen tree species in Japanese warm temperate forests. Funct Ecol 13:632–639Google Scholar
  38. 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 assimilation in the leaves of transgenic rice plants. Plant Cell Physiol 45:521–529PubMedGoogle Scholar
  39. Harley PC, Loreto F, Dimarco G, Sharkey TD (1992) Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiol 98:1429–1436PubMedGoogle Scholar
  40. Holbrook NM, Shashidhar VR, James RA, Munns R (2002) Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying. J Exp Bot 53:1503–1514PubMedGoogle Scholar
  41. Huang J, Pray C, Rozelle S (2002) Enhancing the crops to feed the poor. Nature 418:678–684PubMedGoogle Scholar
  42. IPCC (2007) Climate change 2007: the physical science basis. In: Solomon SD, Qin M, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  43. Jackson RB, Carpenter SR, Dahm CN, McKnight DM, Naiman RJ, Postel SL, Running SW (2001) Water in a changing world. Ecol Appl 11:1027–1045Google Scholar
  44. Jobbagy EG, Jackson RB (2004) Groundwater use and salinization with grassland afforestation. Glob Change Biol 10:1299–1312Google Scholar
  45. Juszczuk IM, Flexas J, Szal B, Dabrowska Z, Ribas-Carbo M, Rychter AM (2007) Effect of mitochondrial genome rearrangement on respiratory activity, photosynthesis, photorespiration, and energy status of MSC16 cucumber (Cucumis sativus L.) mutant. Physiol Plant 131:527–541PubMedGoogle Scholar
  46. Kaldenhoff R, Ribas-Carbo M, Flexas J, Lovisolo C, Heckwolf M, Uehlein N (2008) Aquaporins and plant water balance. Plant Cell Environ 31:658–666PubMedGoogle Scholar
  47. Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch H-J, Rosenkranz R, Stäbler N, Schönfeld B, Kreuzaler F, Peterhänsel C (2007) Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat Biotechnol 25:593–599PubMedGoogle Scholar
  48. Kogami H, Hanba YT, Kibe T, Terashima I, Mazusawa T (2001) CO2 transfer conductance, leaf structure and carbon isotope composition of Polygonum cuspidatum leaves from low and high altitudes. Plant Cell Environ 24:529–538Google Scholar
  49. Lauteri M, Scartazza A, Guido MC, Brugnoli E (1997) Genetic variation in photosynthetic capacity, carbon isotope discrimination and mesophyll conductance in provenances of Castanea sativa adapted to different environments. Funct Ecol 11:675–683Google Scholar
  50. Leegood RC (2002) C4 photosynthesis: principles of CO2 concentration and prospects for its introduction into C3 plants. J Exp Bot 53:581–590PubMedGoogle Scholar
  51. Lloyd J, Syvertsen JP, Kriedemann PE, Farquhar GD (1992) Low conductances for CO2 diffusion from stomata to the sites of carboxylation in leaves of woody species. Plant Cell Environ 15:873–899Google Scholar
  52. 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 54:2393–2401PubMedGoogle Scholar
  53. Loreto F, Harley PC, Di Marco G, Sharkey TD (1992) Estimation of mesophyll conductance to CO2 flux by three different methods. Plant Physiol 98:1437–1443PubMedGoogle Scholar
  54. Martin B, Nienhuis J, King G, Schaefer A (1989) Restriction fragment length polymorphisms associated with water-use efficiency in tomato. Science 243:1725–1728PubMedGoogle Scholar
  55. Masle J, Gilmore SR, Farquhar GD (2005) The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436:866–870PubMedGoogle Scholar
  56. Merlot S, Leonhardt N, Fenzi F, Valon C, Costa M, Piette L, Vavasseur A, Genty B, Boivin K, Müller A, Giraudat J, Leung J (2007) Constitutive activation of a plasma membrane H+-ATPase prevents abscisic acid-mediated stomatal closure. EMBO J 26:3216–3226PubMedGoogle Scholar
  57. Miyazawa S-I, Yoshimura S, Shinazaki 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 35:553–564Google Scholar
  58. Morison JIL, Baker NR, Mullineaux PM, Davies WJ (2008) Improving water use in crop production. Philos Trans R Soc B 363:639–658Google Scholar
  59. Munoz P, Voltas J, Araus JL, Igartua E, Romagosa I (1998) Changes over time in the adaptation of barley releases in north-eastern Spain. Plant Breed 117:531–535Google Scholar
  60. Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089–3099PubMedGoogle Scholar
  61. Nelson DE, Repetti PP, Adams TR, Creelman RA, Wu J, Warner DC, Anstrom DC, Bensen RJ, Castiglioni PP, Donnarummo MG, Hinchey BS, Kumimoto RW, Maszle DR, Canales RD, Kroliwoski KA, Dotson SB, Gutterson N, Ratcliffe OJ, Heard JE (2007) Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proc Natl Acad Sci USA 104:16450–16455PubMedGoogle Scholar
  62. Niinemets U, Cescatti A, Rodeghiero M, Tosens T (2005) Leaf internal diffusion conductance limits photosynthesis more strongly in older leaves of Mediterranean evergreen broad-leaved species. Plant Cell Environ 28:1552–1566Google Scholar
  63. Niinemets U, 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 28:1552–1566Google Scholar
  64. Niinemets Ü, Diaz-Espejo A, Flexas J, Galmés J, Warren CR (2009a) Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. J Exp Bot 60:2249–2270PubMedGoogle Scholar
  65. Niinemets Ü, Diaz-Espejo A, Flexas J, Galmés J, Warren CR (2009b) Importance of mesophyll diffusion conductance in estimation of plant photosynthesis in the field. J Exp Bot 60:2271–2282PubMedGoogle Scholar
  66. Niinemets Ü, Flexas J, Peñuelas J (2011) Evergreens favored by higher responsiveness to increased CO2. Trends Ecol Evol 26:136–142PubMedGoogle Scholar
  67. Niklas KJ, Cobb ED, Niinemets Ü, Reich PB, Sellin A, Shipley B, Wright IJ (2007) “Diminishing returns” in the scaling of functional leaf traits across and within species groups. Proc Natl Acad Sci USA 104:8891–8896PubMedGoogle Scholar
  68. Nilson SE, Assmann SM (2007) The control of transpiration. Insights from Arabidopsis. Plant Physiol 143:19–27PubMedGoogle Scholar
  69. Osmond CB, Björkman O, Anderson DJ (1980) Physiological processes in plant ecology. Towards a synthesis with Atriplex. Springer, BerlinGoogle Scholar
  70. Parry MAJ, Flexas J, Medrano H (2005) Prospects for crop production under drought: research priorities and futures directions. Ann Appl Biol 147:211–226Google Scholar
  71. Peguero-Pina JJ, Flexas J, Galmés J, Niinemets U, Sancho-Knapik D, Barredo G, Villarroya D, Gil-Pelegrín E (2012) Leaf anatomical properties in relation to differences in mesophyll conductance to CO2 and photosynthesis in two related Mediterranean Abies species. Plant Cell Environ 35:2121–2129PubMedGoogle Scholar
  72. Peterhansel C, Maurino VG (2011) Photorespiration redesigned. Plant Physiol 155:49–55PubMedGoogle Scholar
  73. 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 53:2423–2430PubMedGoogle Scholar
  74. Priault P, Tcherkez G, Cornic G, De Paepe R, Naik R, Ghashghaie J, Streb P (2006) The lack of mitochondrial complex I in a CMSII mutant of Nicotiana sylvestris increases photorespiration through an increased internal resistance to CO2 diffusion. J Exp Bot 57:3195–3207PubMedGoogle Scholar
  75. Price D, von Caemmerer S, Evans JR, Yu JW, Lloyd J, Oja V, Kell P, Harrison K, Gallagher A, Badger M (1994) Specific reduction of chloroplast carbonic anhydrase activity by antisense RNA in transgenic tobacco plants has a minor effect on photosynthetic CO2 assimilation. Planta 193:331–340Google Scholar
  76. Price D, Badger MR, von Caemmerer S (2011) The prospect of using cyanobacterial bicarbonate transporters to improve leaf photosynthesis in C3 crop plants. Plant Physiol 155:20–26PubMedGoogle Scholar
  77. Rebetzke GJ, Condon AG, Richards RA, Farquhar GD (2002) Selection for reduced carbon isotope discrimination increases aerial biomass and grain yield of rainfed bread wheat. Crop Sci 42:739–745Google Scholar
  78. Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, Blumwald E (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci USA 104:19631–19636PubMedGoogle Scholar
  79. Rockström J, Lannerstad M, Falkenmark M (2007) Assessing the water challenge of a new green revolution in developing countries. PNAS 104:6253–6260PubMedGoogle Scholar
  80. Rubio S, Rodrigues A, Saez A, Dizon MB, Gallé A, Kim T-H, Santiago J, Flexas J, Schroeder JI, Rodriguez PL (2009) Triple loss of function of protein phosphatases TYPE 2C leads to partial constitutive response to endogenous abscisic acid. Plant Physiol 150:1345–1355PubMedGoogle Scholar
  81. Rytter RM (2005) Water use efficiency, carbon isotope discrimination and biomass production of two sugar beet varieties under well-watered and dry conditions. J Agron Crop Sci 191:426–438Google Scholar
  82. Sack L, Dietrich EM, Streeter C, Sánchez-Gómez D, Holbrook NM (2008) Leaf palmate venation and vascular redundancy confer tolerance of hydraulic disruption. Proc Natl Acad Sci USA 105:1567–1572PubMedGoogle Scholar
  83. Saez A, Robert N, Maktabi MH, Schroeder JI, Serrano R, Rodríguez PL (2006) Enhancement of abscisic acid sensitivity and reduction of water consumption in Arabidopsis by combined inactivation of the protein phosphatases type 2C ABI1 and HAB11. Plant Physiol 141:1389–1399PubMedGoogle Scholar
  84. Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signaling and engineering drought hardiness in plants. Nature 410:327–330PubMedGoogle Scholar
  85. Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155:441–454PubMedGoogle Scholar
  86. Sharkey TD, Vassey TL, Vanderveer PJ, Vierstra RD (1991) Carbon metabolism enzymes and photosynthesis in transgenic tobacco (Nicotiana tabaccum L.) having excess phytochrome. Planta 185:287–296Google Scholar
  87. Sheffield J, Wood EF, Roderick ML (2012) Little change in global drought over the past 60 years. Nature 491:435–438PubMedGoogle Scholar
  88. Shi Z, Liu S, Liu X, Centritto M (2006) Altitudinal variation in photosynthetic capacity, diffusional conductance and δ13C of butterfly bush (Buddleja davidii) plants growing at high elevations. Physiol Plant 128:722–731Google Scholar
  89. 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 32:1821–1832PubMedGoogle Scholar
  90. 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 18:149–157Google Scholar
  91. Tholen D, Boom C, Noguchi K, Ueda S, Kata T, Terashima I (2008) The chloroplast avoidance response decreases internal conductance to CO2 diffusion in Arabidopsis thaliana leaves. Plant Cell Environ 31:1688–1700PubMedGoogle Scholar
  92. Tholen D, Ethier G, Genty B, Pepin S, Zhu XG (2012) Variable mesophyll conductance revisited: theoretical background and experimental implications. Plant Cell Environ 35:2087–2103Google Scholar
  93. Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677PubMedGoogle Scholar
  94. Tomás M, Flexas J, Copolovici L, Galmés J, Hallik L, Medrano H, Tosens T, Vislap V, Niinemets Ü (2013) Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models. J Exp Bot. doi: 10.1093/jxb/ert086
  95. Tosens T, Niinemets Ü, Westoby M, Wright IJ (2012) Anatomical basis of variation in mesophyll resistance in eastern Australian sclerophylls: news of a long and winding path. J Exp Bot 63:5105–5119PubMedGoogle Scholar
  96. Uehlein N, Kaldenhoff R (2008) Aquaporins and plant leaf movements. Ann Bot 101:1–4PubMedGoogle Scholar
  97. Vrábl 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 60:2315–2323PubMedGoogle Scholar
  98. Warren CR (2006) Estimating the internal conductance to CO2 movement. Funct Plant Biol 33:431–442Google Scholar
  99. Warren CR (2008a) Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer. J Exp Bot 59:1475–1487PubMedGoogle Scholar
  100. Warren CR (2008b) Soil water deficits decrease the internal conductance to CO2 transfer but atmospheric water deficits do not. J Exp Bot 59:324–327Google Scholar
  101. Warren CR, Adams MA (2006) Internal conductance does not scale with photosynthetic capacity: implications for carbon isotope discrimination and the economics of water and nitrogen use in photosynthesis. Plant Cell Environ 29:192–201PubMedGoogle Scholar
  102. Warren CR, Dreyer E (2006) Temperature response of photosynthesis and internal conductance to CO2: results from two independent approaches. J Exp Bot 57:3057–3067PubMedGoogle Scholar
  103. Whitney M, Houtz RL, Alonso H (2011) Advancing our understanding and capacity to engineer nature’s CO2-sequestering enzyme, Rubisco. Plant Physiol 155:27–35PubMedGoogle Scholar
  104. Wilkinson S, Corlett JE, Oger L, Davies WJ (1998) Effects of xylem pH on transpiration from wild-type and flacca tomato leaves. A vital role for abscisic acid in preventing excessive water loss even from well-watered plants. Plant Physiol 117:703–709PubMedGoogle Scholar
  105. 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 112:319–326PubMedGoogle Scholar
  106. Wong SC, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282:424–426Google Scholar
  107. Wright IJ, Reich PB, Westoby M (2003) Leaf-cost input mixtures of water and nitrogen for photosynthesis. Am Nat 161:98–111PubMedGoogle Scholar
  108. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin FS, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulías J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas E, Villar R (2004) The world-wide leaf economics spectrum. Nature 428:821–827PubMedGoogle Scholar
  109. Zhang X, Wollenweber B, Jiang D, Liu F, Zhao J (2008) Water deficits and heat shock effects on photosynthesis of a transgenic Arabidopsis thaliana constitutively expressing ABP9, a bZIP transcription factor. J Exp Bot 59:839–848PubMedGoogle Scholar
  110. Zhu X-G, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61:235–261PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Jaume Flexas
    • 1
  • Ülo Niinemets
    • 2
  • Alexander Gallé
    • 1
    • 3
  • Margaret M. Barbour
    • 4
  • Mauro Centritto
    • 5
  • Antonio Diaz-Espejo
    • 6
  • Cyril Douthe
    • 1
  • Jeroni Galmés
    • 1
  • Miquel Ribas-Carbo
    • 1
  • Pedro L. Rodriguez
    • 7
  • Francesc Rosselló
    • 8
  • Raju Soolanayakanahally
    • 9
  • Magdalena Tomas
    • 1
  • Ian J. Wright
    • 10
  • Graham D. Farquhar
    • 11
  • Hipólito Medrano
    • 1
  1. 1.Research Group on Plant Biology under Mediterranean Conditions, Departament de BiologiaUniversitat de les Illes BalearsPalma de MallorcaSpain
  2. 2.Institute of Agricultural and Environmental SciencesEstonian University of Life SciencesTartuEstonia
  3. 3.Bayer CropScience NVZwijnaardeBelgium
  4. 4.Faculty of Agriculture, Food and Natural ResourcesThe University of SydneyNarellanAustralia
  5. 5.Institute for Plant ProtectionNational Research CouncilSesto FiorentinoItaly
  6. 6.Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS, CSIC)Irrigation and Crop Ecophysiology GroupSevillaSpain
  7. 7.Instituto de Biología Molecular y Celular de PlantasConsejo Superior de Investigaciones Científicas-Universidad Politécnica de ValenciaValenciaSpain
  8. 8.Computational Biology and Bioinformatics Research Group, Departament de Ciències Matemàtiques i InformàticaUniversitat de les Illes BalearsPalma de MallorcaSpain
  9. 9.Science and Technology BranchAgriculture and Agri-Food Canada, Indian HeadSaskatchewanCanada
  10. 10.Department of Biological SciencesMacquarie UniversityNorth RydeAustralia
  11. 11.Research School of BiologyThe Australian National UniversityCanberraAustralia

Personalised recommendations