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

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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.

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Notes

  1. Notice that g s is expressed in mol CO2 m−2 s−1 in all the equations above to fulfill the internal units’ requirements of the equations. However, when A N/g s is used as a surrogate for intrinsic WUE, g s should be expressed in mol H2O m−2 s−1. While we will use A N/g s in μmol CO2 mol−1 CO2 throughout the paper, values can be easily converted to the most common unit, μmol CO2 mol−1 H2O, by simply dividing them by 1.6 (which is the ratio of H2O/CO2 diffusivities in air).

References

  • Araus JL, Slafer GA, Royo C, Dolores Serre M (2008) Breeding for yield potential and stress adaptation in cereals. Crit Rev Plant Sci 27:377–412

    Google Scholar 

  • 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 27:625–637

    CAS  Google Scholar 

  • 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 33:1176–1185

    PubMed  Google Scholar 

  • 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 61:3223–3233

    PubMed  CAS  Google Scholar 

  • Blum A (2005) Drought resistance, water-use efficiency, and yield potential—are they compatible, dissonant, or mutually exclusive? Aust J Agric Res 56:1159–1168

    Google Scholar 

  • 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 24:477–489

    CAS  Google Scholar 

  • 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

  • Boyer JS (1996) Advances in drought tolerance in plants. Adv Agron 56:187–218

    Google Scholar 

  • 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 60:2325–2339

    PubMed  CAS  Google Scholar 

  • 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 137:209–219

    PubMed  CAS  Google Scholar 

  • Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004) Breeding for high water-use efficiency. J Exp Bot 55:2447–2460

    PubMed  CAS  Google Scholar 

  • 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

  • Dai A (2011) Drought under global warming: a review. Clim Change 2:45–65

    Google Scholar 

  • 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 30:1197–1204

    CAS  Google Scholar 

  • Diaz-Espejo A, Nicolás E, Fernández JE (2007) Seasonal evolution of diffusional limitations and photosynthetic capacity in olive under drought. Plant Cell Environ 30:922–933

    PubMed  CAS  Google Scholar 

  • Edgerton MD (2009) Increasing crop productivity to meet global needs for feed, food, and fuel. Plant Physiol 149:7–13

    PubMed  CAS  Google Scholar 

  • Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) Resistances along the CO2 diffusion pathway inside leaves. J Exp Bot 60:2235–2248

    PubMed  CAS  Google Scholar 

  • Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345

    CAS  Google Scholar 

  • Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Google Scholar 

  • Farquhar GD, Buckley TN, Miller JM (2002) Optimal stomatal control in relation to leaf area and nitrogen content. Silva Fennica 36:625–637

    Google Scholar 

  • 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. 157

  • 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 29:461–471

    Google Scholar 

  • 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 6:269–279

    PubMed  CAS  Google Scholar 

  • 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 48:427–439

    PubMed  CAS  Google Scholar 

  • 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 172:73–82

    PubMed  CAS  Google Scholar 

  • 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 30:1284–1298

    PubMed  CAS  Google Scholar 

  • 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 31:602–631

    PubMed  CAS  Google Scholar 

  • 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 16:106–121

    CAS  Google Scholar 

  • 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 193–194:70–84

    PubMed  Google Scholar 

  • Franks PJ, Farquhar GD (1999) A relationship between humidity response, growth form and photosynthetic operating point in C3 plants. Plant Cell Environ 22:1337–1349

    Google Scholar 

  • Gaastra P (1959) Photosynthesis of crop plants as influenced by light, carbon dioxide, temperature and stomatal diffusion resistance. Meded Landbouwhogeseh Wageningen 59(13):1–68

    Google Scholar 

  • 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 28:571–579

    Google Scholar 

  • 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 175:81–93

    PubMed  Google Scholar 

  • 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 34:245–260

    PubMed  Google Scholar 

  • 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 28:834–849

    CAS  Google Scholar 

  • 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 142–167

    Google Scholar 

  • 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 13:632–639

    Google Scholar 

  • 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 45:521–529

    PubMed  CAS  Google Scholar 

  • 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 98:1429–1436

    PubMed  CAS  Google Scholar 

  • 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 53:1503–1514

    PubMed  CAS  Google Scholar 

  • Huang J, Pray C, Rozelle S (2002) Enhancing the crops to feed the poor. Nature 418:678–684

    PubMed  CAS  Google Scholar 

  • 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, Cambridge

  • Jackson RB, Carpenter SR, Dahm CN, McKnight DM, Naiman RJ, Postel SL, Running SW (2001) Water in a changing world. Ecol Appl 11:1027–1045

    Google Scholar 

  • Jobbagy EG, Jackson RB (2004) Groundwater use and salinization with grassland afforestation. Glob Change Biol 10:1299–1312

    Google Scholar 

  • 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 131:527–541

    PubMed  CAS  Google Scholar 

  • Kaldenhoff R, Ribas-Carbo M, Flexas J, Lovisolo C, Heckwolf M, Uehlein N (2008) Aquaporins and plant water balance. Plant Cell Environ 31:658–666

    PubMed  CAS  Google Scholar 

  • 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 25:593–599

    PubMed  CAS  Google Scholar 

  • 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 24:529–538

    CAS  Google Scholar 

  • 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 11:675–683

    Google Scholar 

  • Leegood RC (2002) C4 photosynthesis: principles of CO2 concentration and prospects for its introduction into C3 plants. J Exp Bot 53:581–590

    PubMed  CAS  Google Scholar 

  • 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 15:873–899

    CAS  Google Scholar 

  • 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 54:2393–2401

    PubMed  CAS  Google Scholar 

  • Loreto F, Harley PC, Di Marco G, Sharkey TD (1992) Estimation of mesophyll conductance to CO2 flux by three different methods. Plant Physiol 98:1437–1443

    PubMed  CAS  Google Scholar 

  • Martin B, Nienhuis J, King G, Schaefer A (1989) Restriction fragment length polymorphisms associated with water-use efficiency in tomato. Science 243:1725–1728

    PubMed  CAS  Google Scholar 

  • Masle J, Gilmore SR, Farquhar GD (2005) The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436:866–870

    PubMed  CAS  Google Scholar 

  • 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 26:3216–3226

    PubMed  CAS  Google Scholar 

  • 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 35:553–564

    CAS  Google Scholar 

  • Morison JIL, Baker NR, Mullineaux PM, Davies WJ (2008) Improving water use in crop production. Philos Trans R Soc B 363:639–658

    CAS  Google Scholar 

  • 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 117:531–535

    Google Scholar 

  • 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 14:3089–3099

    PubMed  CAS  Google Scholar 

  • 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 104:16450–16455

    PubMed  CAS  Google Scholar 

  • 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 28:1552–1566

    Google Scholar 

  • 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 28:1552–1566

    Google Scholar 

  • 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 60:2249–2270

    PubMed  CAS  Google Scholar 

  • 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 60:2271–2282

    PubMed  CAS  Google Scholar 

  • Niinemets Ü, Flexas J, Peñuelas J (2011) Evergreens favored by higher responsiveness to increased CO2. Trends Ecol Evol 26:136–142

    PubMed  Google Scholar 

  • 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 104:8891–8896

    PubMed  CAS  Google Scholar 

  • Nilson SE, Assmann SM (2007) The control of transpiration. Insights from Arabidopsis. Plant Physiol 143:19–27

    PubMed  CAS  Google Scholar 

  • Osmond CB, Björkman O, Anderson DJ (1980) Physiological processes in plant ecology. Towards a synthesis with Atriplex. Springer, Berlin

    Google Scholar 

  • Parry MAJ, Flexas J, Medrano H (2005) Prospects for crop production under drought: research priorities and futures directions. Ann Appl Biol 147:211–226

    Google Scholar 

  • 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 35:2121–2129

    PubMed  CAS  Google Scholar 

  • Peterhansel C, Maurino VG (2011) Photorespiration redesigned. Plant Physiol 155:49–55

    PubMed  CAS  Google Scholar 

  • 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 53:2423–2430

    PubMed  CAS  Google Scholar 

  • 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 57:3195–3207

    PubMed  CAS  Google Scholar 

  • 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 193:331–340

    CAS  Google Scholar 

  • 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 155:20–26

    PubMed  CAS  Google Scholar 

  • 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 42:739–745

    Google Scholar 

  • 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 104:19631–19636

    PubMed  CAS  Google Scholar 

  • Rockström J, Lannerstad M, Falkenmark M (2007) Assessing the water challenge of a new green revolution in developing countries. PNAS 104:6253–6260

    PubMed  Google Scholar 

  • 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 150:1345–1355

    PubMed  CAS  Google Scholar 

  • 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 191:426–438

    Google Scholar 

  • 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 105:1567–1572

    PubMed  CAS  Google Scholar 

  • 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 141:1389–1399

    PubMed  CAS  Google Scholar 

  • Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signaling and engineering drought hardiness in plants. Nature 410:327–330

    PubMed  CAS  Google Scholar 

  • Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155:441–454

    PubMed  Google Scholar 

  • Sharkey TD, Vassey TL, Vanderveer PJ, Vierstra RD (1991) Carbon metabolism enzymes and photosynthesis in transgenic tobacco (Nicotiana tabaccum L.) having excess phytochrome. Planta 185:287–296

    CAS  Google Scholar 

  • Sheffield J, Wood EF, Roderick ML (2012) Little change in global drought over the past 60 years. Nature 491:435–438

    PubMed  CAS  Google Scholar 

  • 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 128:722–731

    CAS  Google Scholar 

  • 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 32:1821–1832

    PubMed  CAS  Google Scholar 

  • 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 18:149–157

    Google Scholar 

  • 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 31:1688–1700

    PubMed  CAS  Google Scholar 

  • Tholen D, Ethier G, Genty B, Pepin S, Zhu XG (2012) Variable mesophyll conductance revisited: theoretical background and experimental implications. Plant Cell Environ 35:2087–2103

    Google Scholar 

  • Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677

    PubMed  CAS  Google Scholar 

  • 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

  • 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 63:5105–5119

    PubMed  CAS  Google Scholar 

  • Uehlein N, Kaldenhoff R (2008) Aquaporins and plant leaf movements. Ann Bot 101:1–4

    PubMed  CAS  Google Scholar 

  • 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 60:2315–2323

    PubMed  Google Scholar 

  • Warren CR (2006) Estimating the internal conductance to CO2 movement. Funct Plant Biol 33:431–442

    CAS  Google Scholar 

  • Warren CR (2008a) Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer. J Exp Bot 59:1475–1487

    PubMed  CAS  Google Scholar 

  • Warren CR (2008b) Soil water deficits decrease the internal conductance to CO2 transfer but atmospheric water deficits do not. J Exp Bot 59:324–327

    Google Scholar 

  • 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 29:192–201

    PubMed  CAS  Google Scholar 

  • Warren CR, Dreyer E (2006) Temperature response of photosynthesis and internal conductance to CO2: results from two independent approaches. J Exp Bot 57:3057–3067

    PubMed  CAS  Google Scholar 

  • Whitney M, Houtz RL, Alonso H (2011) Advancing our understanding and capacity to engineer nature’s CO2-sequestering enzyme, Rubisco. Plant Physiol 155:27–35

    PubMed  CAS  Google Scholar 

  • 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 117:703–709

    PubMed  CAS  Google Scholar 

  • 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 112:319–326

    PubMed  CAS  Google Scholar 

  • Wong SC, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282:424–426

    Google Scholar 

  • Wright IJ, Reich PB, Westoby M (2003) Leaf-cost input mixtures of water and nitrogen for photosynthesis. Am Nat 161:98–111

    PubMed  Google Scholar 

  • 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 428:821–827

    PubMed  CAS  Google Scholar 

  • 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 59:839–848

    PubMed  CAS  Google Scholar 

  • Zhu X-G, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61:235–261

    PubMed  CAS  Google Scholar 

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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.).

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  1. Alexander Gallé

    Present address: Bayer CropScience NV, Technologiepark 38, 9052, Zwijnaarde, Belgium

Authors and Affiliations

  1. Research Group on Plant Biology under Mediterranean Conditions, Departament de Biologia, Universitat de les Illes Balears, Carretera de Valldemossa Km 7.5, 07122, Palma de Mallorca, Illes Balears, Spain

    Jaume Flexas, Alexander Gallé, Cyril Douthe, Jeroni Galmés, Miquel Ribas-Carbo, Magdalena Tomas & Hipólito Medrano

  2. Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Kreutzwaldi 1, 51014, Tartu, Estonia

    Ülo Niinemets

  3. Faculty of Agriculture, Food and Natural Resources, The University of Sydney, Private Bag 4011, Narellan, NSW, 2567, Australia

    Margaret M. Barbour

  4. Institute for Plant Protection, National Research Council, Via Madonna del Piano 10, 50019, Sesto Fiorentino, FI, Italy

    Mauro Centritto

  5. Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS, CSIC), Irrigation and Crop Ecophysiology Group, Avenida Reina Mercedes 10, 41012, Sevilla, Spain

    Antonio Diaz-Espejo

  6. Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas-Universidad Politécnica de Valencia, 46022, Valencia, Spain

    Pedro L. Rodriguez

  7. Computational Biology and Bioinformatics Research Group, Departament de Ciències Matemàtiques i Informàtica, Universitat de les Illes Balears, Carretera de Valldemossa Km 7.5, 07122, Palma de Mallorca, Illes Balears, Spain

    Francesc Rosselló

  8. Science and Technology Branch, Agriculture and Agri-Food Canada, Indian Head, Saskatchewan, S0G 2K0, Canada

    Raju Soolanayakanahally

  9. Department of Biological Sciences, Macquarie University, North Ryde, NSW, 2109, Australia

    Ian J. Wright

  10. Research School of Biology, The Australian National University, Canberra, ACT, 2601, Australia

    Graham D. Farquhar

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  1. Jaume Flexas
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  2. Ülo Niinemets
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  3. Alexander Gallé
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Corresponding author

Correspondence to Jaume Flexas.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11120_2013_9844_MOESM1_ESM.xls

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

Complete list of references from which data in Online Resource 2 and 4 were compiled. Supplementary material 2 (DOC 46 kb)

Data compilation for specific genetic manipulations. Supplementary material 3 (XLS 34 kb)

11120_2013_9844_MOESM4_ESM.doc

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)

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Flexas, J., Niinemets, Ü., Gallé, A. et al. Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency. Photosynth Res 117, 45–59 (2013). https://doi.org/10.1007/s11120-013-9844-z

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  • DOI: https://doi.org/10.1007/s11120-013-9844-z

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