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.

Water stress (WS) slows growth and photosynthesis (A(n)), but most knowledge comes from short-time studies that do not account for longer term acclimation processes that are especially relevant in tree species. Using two Eucalyptus species that contrast in drought tolerance, we induced moderate and severe water deficits by withholding water until stomatal conductance (g(sw)) decreased to two pre-defined values for 24 d, WS was maintained at the target g(sw) for 29 d and then plants were re-watered. Additionally, we developed new equations to simulate the effect on mesophyll conductance (g(m)) of accounting for the resistance to refixation of CO(2). The diffusive limitations to CO(2), dominated by the stomata, were the most important constraints to A(n). Full recovery of A(n) was reached after re-watering, characterized by quick recovery of gm and even higher biochemical capacity, in contrast to the slower recovery of g(sw). The acclimation to long-term WS led to decreased mesophyll and biochemical limitations, in contrast to studies in which stress was imposed more rapidly. Finally, we provide evidence that higher gm under WS contributes to higher intrinsic water-use efficiency (iWUE) and reduces the leaf oxidative stress, highlighting the importance of gm as a target for breeding/genetic engineering.

[1]  A. Millar,et al.  Organization and regulation of mitochondrial respiration in plants. , 2011, Annual review of plant biology.

[2]  T. Sharkey,et al.  Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants , 1986 .

[3]  J. Flexas,et al.  Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandierixV. rupestris). , 2009, Journal of experimental botany.

[4]  J. Bunce Use of the response of photosynthesis to oxygen to estimate mesophyll conductance to carbon dioxide in water-stressed soybean leaves. , 2009, Plant, cell & environment.

[5]  Nobuhiro Suzuki,et al.  Reactive oxygen species homeostasis and signalling during drought and salinity stresses. , 2010, Plant, cell & environment.

[6]  L. Gu,et al.  Artefactual responses of mesophyll conductance to CO2 and irradiance estimated with the variable J and online isotope discrimination methods. , 2014, Plant, cell & environment.

[7]  N. McDowell,et al.  A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests , 2010 .

[8]  A. Cescatti,et al.  Major diffusion leaks of clamp-on leaf cuvettes still unaccounted: how erroneous are the estimates of Farquhar et al. model parameters? , 2007, Plant, cell & environment.

[9]  E. Dreyer,et al.  Temperature response of photosynthesis and internal conductance to CO2: results from two independent approaches. , 2006, Journal of experimental botany.

[10]  J. Flexas,et al.  Rubisco activity in Mediterranean species is regulated by the chloroplastic CO2 concentration under water stress , 2011, Journal of experimental botany.

[11]  Jaume Flexas,et al.  Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. , 2007, The New phytologist.

[12]  D. Lawlor,et al.  Causes of Decreased Photosynthetic Rate and Metabolic Capacity in Water-deficient Leaf Cells: a Critical Evaluation of Mechanisms and Integration of Processes , 1996 .

[13]  M. Kirschbaum Water stress in Eucalyptus pauciflora: comparison of effects on stomatal conductance with effects on the mesophyll capacity for photosynthesis, and investigation of a possible involvement of photoinhibition , 1987, Planta.

[14]  Andrea Nardini,et al.  Xylem cavitation and hydraulic control of stomatal conductance in Laurel (Laurus nobilis L.) , 2000 .

[15]  G. Farquhar,et al.  CO2 and Water Vapor Exchange across Leaf Cuticle (Epidermis) at Various Water Potentials , 1997, Plant physiology.

[16]  F. Woodward,et al.  Global climate and the distribution of plant biomes. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[17]  D. Macherel,et al.  The crucial role of plant mitochondria in orchestrating drought tolerance. , 2009, Annals of botany.

[18]  J. Sperry Hydraulic constraints on plant gas exchange , 2000 .

[19]  L. Anderegg,et al.  Not all droughts are created equal: translating meteorological drought into woody plant mortality. , 2013, Tree physiology.

[20]  K. Asada Production and Scavenging of Reactive Oxygen Species in Chloroplasts and Their Functions1 , 2006, Plant Physiology.

[21]  F. Loreto,et al.  12CO2 emission from different metabolic pathways measured in illuminated and darkened C3 and C4 leaves at low, atmospheric and elevated CO2 concentration. , 2003, Journal of experimental botany.

[22]  Xin-Guang Zhu,et al.  The Mechanistic Basis of Internal Conductance: A Theoretical Analysis of Mesophyll Cell Photosynthesis and CO2 Diffusion1[W][OA] , 2011, Plant Physiology.

[23]  N. Turner Adaptation to water deficits: a changing perspective , 1986 .

[24]  J. R. Evans,et al.  Temperature response of carbon isotope discrimination and mesophyll conductance in tobacco. , 2013, Plant, cell & environment.

[25]  J. Flexas,et al.  Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. , 2009, Journal of experimental botany.

[26]  M. Maeshima,et al.  Deactivation of aquaporins decreases internal conductance to CO2 diffusion in tobacco leaves grown under long-term drought. , 2008, Functional plant biology : FPB.

[27]  Ü. Niinemets,et al.  Anatomical basis of vari tion in mesophyll resistance in eastern Australian sclero hylls : news of a long and winding path , 2012 .

[28]  J. Flexas,et al.  Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. , 2002, Annals of botany.

[29]  C. Douthe,et al.  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? , 2012, Functional plant biology : FPB.

[30]  H. Griffiths,et al.  Carbon Isotope Fractionation during Photorespiration and Carboxylation in Senecio1[W][OA] , 2008, Plant Physiology.

[31]  J. Araus,et al.  Epidermal conductance in different parts of durum wheat grown under Mediterranean conditions: the role of epicuticular waxes and stomata , 1991 .

[32]  J. Flexas,et al.  Acclimation of Rubisco specificity factor to drought in tobacco: discrepancies between in vitro and in vivo estimations. , 2006, Journal of experimental botany.

[33]  S. V. Caemmerer,et al.  Steady‐state models of photosynthesis , 2013 .

[34]  G. Edwards,et al.  Coordination of Leaf Photosynthesis, Transpiration, and Structural Traits in Rice and Wild Relatives (Genus Oryza)1[W][OA] , 2013, Plant Physiology.

[35]  F. Magnani,et al.  Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees , 2005 .

[36]  J. Berry,et al.  A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species , 1980, Planta.

[37]  E. Steudle,et al.  Light and turgor affect the water permeability (aquaporins) of parenchyma cells in the midrib of leaves of Zea mays. , 2007, Journal of experimental botany.

[38]  I. Aranda,et al.  Metabolomics demonstrates divergent responses of two Eucalyptus species to water stress , 2012, Metabolomics.

[39]  E. Wood,et al.  Projected changes in drought occurrence under future global warming from multi-model, multi-scenario, IPCC AR4 simulations , 2008 .

[40]  T. Sharkey,et al.  Fitting photosynthetic carbon dioxide response curves for C(3) leaves. , 2007, Plant, cell & environment.

[41]  J. Flexas,et al.  Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves , 2005 .

[42]  T. Stocker,et al.  Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation. A Special Report of Working Groups I and II of IPCC Intergovernmental Panel on Climate Change , 2012 .

[43]  J. Cushman,et al.  Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles , 2007, Functional & Integrative Genomics.

[44]  R. Serraj,et al.  Leaf gas exchange, carbon isotope discrimination, and grain yield in contrasting rice genotypes subjected to water deficits during the reproductive stage. , 2009, Journal of experimental botany.

[45]  Ichiro Terashima,et al.  Resistances along the CO2 diffusion pathway inside leaves. , 2009, Journal of experimental botany.

[46]  M. M. Chaves,et al.  Water stress and recovery in the performance of two Eucalyptus globulus clones: physiological and biochemical profiles. , 2014, Physiologia plantarum.

[47]  T. Sharkey,et al.  Theoretical Considerations when Estimating the Mesophyll Conductance to CO(2) Flux by Analysis of the Response of Photosynthesis to CO(2). , 1992, Plant physiology.

[48]  S. Running,et al.  Contrasting Climatic Controls on the Estimated Productivity of Global Terrestrial Biomes , 1998, Ecosystems.

[49]  G. Farquhar,et al.  Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light , 1985, Planta.

[50]  R. Furbank,et al.  The mechanisms contributing to photosynthetic control of electron transport by carbon assimilation in leaves , 1990, Photosynthesis Research.

[51]  J. Briantais,et al.  The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence , 1989 .

[52]  J. Flexas,et al.  Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress , 2006 .

[53]  Hervé Cochard,et al.  Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut. , 2002, Plant physiology.

[54]  Jaume Flexas,et al.  Estimating mesophyll conductance to CO2: methodology, potential errors, and recommendations. , 2009, Journal of experimental botany.

[55]  John R. Evans,et al.  The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco , 1994, Planta.

[56]  Robert B. Heinen,et al.  Role of aquaporins in leaf physiology. , 2009, Journal of experimental botany.

[57]  J. Moncrieff,et al.  Variations in 13C discrimination during CO2 exchange by Picea sitchensis branches in the field. , 2007, Plant, cell & environment.

[58]  M. Badger,et al.  Photoprotection in plants: a new light on photosystem II damage. , 2011, Trends in plant science.

[59]  C. Warren Estimating the internal conductance to CO2 movement. , 2006, Functional plant biology : FPB.

[60]  B. Genty,et al.  Variable mesophyll conductance revisited: theoretical background and experimental implications. , 2012, Plant, cell & environment.

[61]  M. Kirschbaum Recovery of photosynthesis from water stress in Eucalyptus pauciflora: a process in two stages , 1988 .

[62]  Nigel J. Livingston,et al.  On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar–von Caemmerer–Berry leaf photosynthesis model , 2004 .

[63]  M. Ball,et al.  Leaf respiration of snow gum in the light and dark. Interactions between temperature and irradiance. , 2000, Plant physiology.

[64]  J. R. Evans,et al.  The Relationship Between CO2 Transfer Conductance and Leaf Anatomy in Transgenic Tobacco With a Reduced Content of Rubisco , 1994 .

[65]  M. Hodges,et al.  Respiratory carbon fluxes in leaves. , 2012, Current opinion in plant biology.

[66]  J. Flexas,et al.  Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. , 2012, Plant science : an international journal of experimental plant biology.

[67]  M. Guevara,et al.  Drought Response in Forest Trees: From the Species to the Gene , 2012 .

[68]  J. Flexas,et al.  The role of mesophyll conductance during water stress and recovery in tobacco (Nicotiana sylvestris): acclimation or limitation? , 2009, Journal of experimental botany.

[69]  J. Flexas,et al.  Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. , 2009, Annals of botany.

[70]  J. R. Evans,et al.  Using tunable diode laser spectroscopy to measure carbon isotope discrimination and mesophyll conductance to CO₂ diffusion dynamically at different CO₂ concentrations. , 2011, Plant, cell & environment.

[71]  G. Farquhar,et al.  Variability in mesophyll conductance between barley genotypes, and effects on transpiration efficiency and carbon isotope discrimination. , 2010, Plant, cell & environment.

[72]  G. Farquhar,et al.  Ternary effects on the gas exchange of isotopologues of carbon dioxide. , 2012, Plant, cell & environment.

[73]  C. Foyer,et al.  Photosynthetic control of electron transport and the regulation of gene expression. , 2012, Journal of experimental botany.

[74]  J. Flexas,et al.  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. , 2006, The New phytologist.

[75]  D. S. Kubien,et al.  Can phenotypic plasticity in Rubisco performance contribute to photosynthetic acclimation? , 2013, Photosynthesis Research.

[76]  D. Sánchez-Gómez,et al.  Light acclimation at the end of the growing season in two broadleaved oak species , 2011, Photosynthetica.

[77]  M. Zeppel,et al.  Forest mortality due to drought: latest insights, evidence and unresolved questions on physiological pathways and consequences of tree death. , 2013, The New phytologist.

[78]  Francesc Rosselló,et al.  Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency , 2013, Photosynthesis Research.

[79]  B. Potts,et al.  The natural distribution of Eucalyptus species in Tasmania , 1996 .

[80]  K. Wilson,et al.  Quantifying stomatal and non-stomatal limitations to carbon assimilation resulting from leaf aging and drought in mature deciduous tree species. , 2000, Tree physiology.

[81]  S. Rambal,et al.  Opposite changes in leaf dark respiration and soluble sugars with drought in two Mediterranean oaks. , 2011, Functional plant biology : FPB.

[82]  C. Warren,et al.  The role of mesophyll conductance in the economics of nitrogen and water use in photosynthesis , 2014, Photosynthesis Research.

[83]  D. Sánchez-Gómez,et al.  Effects of drought on mesophyll conductance and photosynthetic limitations at different tree canopy layers. , 2013, Plant, cell & environment.

[84]  F. Manes,et al.  Fluorescence Parameters Measured Concurrently with Net Photosynthesis to Investigate Chloroplastic CO2 Concentration in Leaves of Quercus ilex L. , 1990 .

[85]  J. Flexas,et al.  Improving water use efficiency in grapevines: potential physiological targets for biotechnological improvement. , 2010 .

[86]  T. Brodribb,et al.  Hydraulic Failure Defines the Recovery and Point of Death in Water-Stressed Conifers[OA] , 2008, Plant Physiology.

[87]  J. Flexas,et al.  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 , 2011, Journal of experimental botany.

[88]  G. Farquhar,et al.  Experimental evidence for diel variations of the carbon isotope composition in leaf, stem and phloem sap organic matter in Ricinus communis. , 2008, Plant, cell & environment.

[89]  C. Warren,et al.  Soil water deficits decrease the internal conductance to CO2 transfer but atmospheric water deficits do not. , 2008, Journal of experimental botany.

[90]  Nigel J. Livingston,et al.  Transfer conductance in second growth Douglas-fir (Pseudotsuga menziesii (Mirb.)Franco) canopies , 2003 .

[91]  R. Sage,et al.  C3 plants enhance rates of photosynthesis by reassimilating photorespired and respired CO2. , 2013, Plant, cell & environment.

[92]  K. Laukens,et al.  Gradual Soil Water Depletion Results in Reversible Changes of Gene Expression, Protein Profiles, Ecophysiology, and Growth Performance in Populus euphratica, a Poplar Growing in Arid Regions1[W][OA] , 2006, Plant Physiology.

[93]  E. Nicolás,et al.  Seasonal evolution of diffusional limitations and photosynthetic capacity in olive under drought. , 2007, Plant, cell & environment.

[94]  R. Guy,et al.  Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar (Populus balsamifera L.). , 2009, Plant, cell & environment.

[95]  I. Aranda,et al.  Responses to water stress of gas exchange and metabolites in Eucalyptus and Acacia spp. , 2011, Plant, cell & environment.

[96]  R. Valentini,et al.  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 , 1995 .

[97]  J. Flexas,et al.  Physiological and morphological adaptations in relation to water use efficiency in Mediterranean accessions of Solanum lycopersicum. , 2011, Plant, cell & environment.

[98]  S. V. Caemmerer,et al.  Biochemical models of leaf photosynthesis. , 2000 .

[99]  H. Medrano,et al.  Rapid hydraulic recovery in Eucalyptus pauciflora after drought: linkages between stem hydraulics and leaf gas exchange. , 2014, Plant, cell & environment.

[100]  M. Adams,et al.  Contrasting physiological responses of six eucalyptus species to water deficit. , 2007, Annals of botany.

[101]  J. Schroeder,et al.  Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. , 2010, Annual review of plant biology.

[102]  N. McDowell,et al.  The interdependence of mechanisms underlying climate-driven vegetation mortality. , 2011, Trends in ecology & evolution.

[103]  David M Kramer,et al.  Determining the limitations and regulation of photosynthetic energy transduction in leaves. , 2007, Plant, cell & environment.

[104]  N. McDowell,et al.  Function of Nicotiana tabacum Aquaporins as Chloroplast Gas Pores Challenges the Concept of Membrane CO2 Permeability[W] , 2008, The Plant Cell Online.

[105]  J. Pereira,et al.  Understanding plant responses to drought - from genes to the whole plant. , 2003, Functional plant biology : FPB.