Mesophyll photosynthesis and guard cell metabolism impacts on stomatal behaviour.

Stomata control gaseous fluxes between the internal leaf air spaces and the external atmosphere. Guard cells determine stomatal aperture and must operate to ensure an appropriate balance between CO2 uptake for photosynthesis (A) and water loss, and ultimately plant water use efficiency (WUE). A strong correlation between A and stomatal conductance (gs ) is well documented and often observed, but the underlying mechanisms, possible signals and metabolites that promote this relationship are currently unknown. In this review we evaluate the current literature on mesophyll-driven signals that may coordinate stomatal behaviour with mesophyll carbon assimilation. We explore a possible role of various metabolites including sucrose and malate (from several potential sources; including guard cell photosynthesis) and new evidence that improvements in WUE have been made by manipulating sucrose metabolism within the guard cells. Finally we discuss the new tools and techniques available for potentially manipulating cell-specific metabolism, including guard and mesophyll cells, in order to elucidate mesophyll-derived signals that coordinate mesophyll CO2 demands with stomatal behaviour, in order to provide a mechanistic understanding of these processes as this may identify potential targets for manipulations in order to improve plant WUE and crop yield.

[1]  R. Hedrich,et al.  CO2 provides an intermediate link in the red light response of guard cells. , 2002, The Plant journal : for cell and molecular biology.

[2]  T. Lawson,et al.  Stomatal conductance does not correlate with photosynthetic capacity in transgenic tobacco with reduced amounts of Rubisco. , 2004, Journal of experimental botany.

[3]  J. Boyer.  Plant Productivity and Environment , 1982, Science.

[4]  K. Mott,et al.  Is the signal from the mesophyll to the guard cells a vapour-phase ion? , 2014, Plant, cell & environment.

[5]  M. Lehmann,et al.  Antisense Inhibition of the Iron-Sulphur Subunit of Succinate Dehydrogenase Enhances Photosynthesis and Growth in Tomato via an Organic Acid–Mediated Effect on Stomatal Aperture[W][OA] , 2011, Plant Cell.

[6]  K. Al-Rasheid,et al.  C-terminus-mediated voltage gating of Arabidopsis guard cell anion channel QUAC1. , 2013, Molecular plant.

[7]  G. Farquhar,et al.  A hydromechanical and biochemical model of stomatal conductance , 2003 .

[8]  J. Schroeder,et al.  Mutations in the SLAC1 anion channel slow stomatal opening and severely reduce K+ uptake channel activity via enhanced cytosolic [Ca2+] and increased Ca2+ sensitivity of K+ uptake channels. , 2013, The New phytologist.

[9]  R. Wallach,et al.  The Role of Tobacco Aquaporin1 in Improving Water Use Efficiency, Hydraulic Conductivity, and Yield Production Under Salt Stress1[C][W][OA] , 2009, Plant Physiology.

[10]  Rainer Hedrich,et al.  AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. , 2010, The Plant journal : for cell and molecular biology.

[11]  P. Mullineaux,et al.  Improving water use in crop production , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[12]  C. Tonelli,et al.  The Arabidopsis thaliana MYB60 promoter provides a tool for the spatio-temporal control of gene expression in stomatal guard cells , 2013, Journal of experimental botany.

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

[14]  Robert W. Pearcy,et al.  Observed and modelled stomatal responses to dynamic light environments in the shade plant Alocasia macrorrhiza , 1988 .

[15]  K. Raschke,et al.  [14C]Carbon-dioxide fixation by isolated leaf epidermes with stomata closed or open , 2004, Planta.

[16]  J. Flexas,et al.  Differential tissue-specific expression of NtAQP1 in Arabidopsis thaliana reveals a role for this protein in stomatal and mesophyll conductance of CO2 under standard and salt-stress conditions , 2014, Planta.

[17]  A. Naor,et al.  The roles of fruit sink in the regulation of gas exchange and water uptake: A case study for avocado , 2013 .

[18]  C. Lovisolo,et al.  The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions , 2003, Nature.

[19]  A. Fernie,et al.  Malate. Jack of all trades or master of a few? , 2009, Phytochemistry.

[20]  Graham D. Farquhar,et al.  An Empirical Model of Stomatal Conductance , 1984 .

[21]  D. Bowling,et al.  Effect of the Mesophyll on Stomatal Opening in Commelina communis , 1992 .

[22]  L. D. Talbott,et al.  Sugar and Organic Acid Accumulation in Guard Cells of Vicia faba in Response to Red and Blue Light , 1993, Plant physiology.

[23]  T. Sharkey,et al.  Stomatal conductance and photosynthesis , 1982 .

[24]  H. Schnabl.  CO2 and malate metabolism in starch-containing and starch-lacking guard-cell protoplasts , 1980, Planta.

[25]  R. Häusler,et al.  Effects of altered phosphoenolpyruvate carboxylase activities on transgenic C3 plant Solanum tuberosum , 1996, Plant Molecular Biology.

[26]  E. Zeiger,et al.  Role of zeaxanthin in blue light photoreception and the modulation of light-CO2 interactions in guard cells , 1998 .

[27]  K. Miura,et al.  The Arabidopsis GTL1 Transcription Factor Regulates Water Use Efficiency and Drought Tolerance by Modulating Stomatal Density via Transrepression of SDD1[W][OA] , 2010, Plant Cell.

[28]  S. Assmann,et al.  Signal transduction in guard cells. , 1993, Annual review of cell biology.

[29]  E. Martinoia,et al.  AtALMT9 is a malate-activated vacuolar chloride channel required for stomatal opening in Arabidopsis , 2013, Nature Communications.

[30]  Manuela Herman,et al.  Biochemistry And Molecular Biology Of Plants , 2016 .

[31]  S. Assmann,et al.  Light regulation of stomatal movement. , 2007, Annual review of plant biology.

[32]  K. Mott,et al.  Evidence for Involvement of Photosynthetic Processes in the Stomatal Response to CO21 , 2006, Plant Physiology.

[33]  B. Kimball,et al.  Correlation of Stomatal Conductance with Photosynthetic Capacity of Cotton Only in a CO(2)-Enriched Atmosphere: Mediation by Abscisic Acid? , 1988, Plant physiology.

[34]  T. Mansfield,et al.  Physiology of Stomata , 1908, Nature.

[35]  C. Tonelli,et al.  Gene trap-based identification of a guard cell promoter in Arabidopsis , 2008, Plant signaling & behavior.

[36]  I. Hara-Nishimura,et al.  Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis. , 2013, The New phytologist.

[37]  R. B. Jackson,et al.  Photosynthetic Electron Transport in Single Guard Cells as Measured by Scanning Electrochemical Microscopy , 1997, Plant physiology.

[38]  W. H. Outlaw,et al.  Sucrose: a solute that accumulates in the guard‐cell apoplast and guard‐cell symplast of open stomata , 1995, FEBS letters.

[39]  Shuqiu Zhang,et al.  Accumulation of an apoplastic solute in the guard-cell wall is sufficient to exert a significant effect on transpiration in Vicia faba leaflets , 2000 .

[40]  M. Badger,et al.  Specific reduction of chloroplast glyceraldehyde-3-phosphate dehydrogenase activity by antisense RNA reduces CO2 assimilation via a reduction in ribulose bisphosphate regeneration in transgenic tobacco plants , 2004, Planta.

[41]  S. Taylor,et al.  Photosynthetic Carbon Fixation in Guard Cell Protoplasts of Vicia faba L. : Evidence from Radiolabel Experiments. , 1988, Plant physiology.

[42]  T C Hsiao,et al.  Stomatal Opening in Isolated Epidermal Strips of Vicia faba. II. Responses to KCl Concentration and the Role of Potassium Absorption. , 1968, Plant physiology.

[43]  A. Hetherington,et al.  Some current aspects of stomatal physiology. , 1990 .

[44]  G. Pucella,et al.  Correction: Corrigendum: Current drive at plasma densities required for thermonuclear reactors , 2013, Nature Communications.

[45]  K. Shimazaki.  Ribulosebisphosphate carboxylase activity and photosynthetic o(2) evolution rate in vicia guard-cell protoplasts. , 1989, Plant physiology.

[46]  E. Macrobbie,et al.  Potassium content and aperture in “intact” stomatal and epidermal cells ofCommelina communis L , 1980, The Journal of Membrane Biology.

[47]  Yongwook Choi,et al.  The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2 , 2008, Nature Cell Biology.

[48]  M. Stitt,et al.  A role for fructose 2,6-bisphosphate in regulating carbohydrate metabolism in guard cells. , 1985, Plant physiology.

[49]  J. Schroeder,et al.  Arabidopsis HT1 kinase controls stomatal movements in response to CO2 , 2006, Nature Cell Biology.

[50]  P. Franks,et al.  Genetic manipulation of stomatal density influences stomatal size, plant growth and tolerance to restricted water supply across a growth carbon dioxide gradient , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[51]  R. Hedrich,et al.  Guard cells in albino leaf patches do not respond to photosynthetically active radiation, but are sensitive to blue light, CO2 and abscisic acid. , 2006, Plant, cell & environment.

[52]  I. R. Cowan,et al.  Ionic relations of guard cells. , 1987 .

[53]  E. Zeiger,et al.  Light quality and osmoregulation in vicia guard cells : evidence for involvement of three metabolic pathways. , 1988, Plant physiology.

[54]  P. Schopfer,et al.  Biomechanics of plant growth. , 2006, American journal of botany.

[55]  J. Sheen,et al.  Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[56]  T. Lawson,et al.  Heterogeneity in Stomatal Characteristics , 1997 .

[57]  F. Milthorpe,et al.  Structure, Carbon Dioxide Fixation and Metabolism of Stomata , 1974 .

[58]  W. H. Outlaw.  A Minireview: Comparative Biochemistry of Photosynthesis in Palisade Cells, Spongy Cells, and Guard Cells of C3 Leaves , 1987 .

[59]  T. Lawson,et al.  Spatial and temporal variation in gas exchange over the lower surface of Phaseolus vulgaris L. primary leaves , 1999 .

[60]  Alcalde Rovira Roure.  Plant Breeding and Drought in C 3 Cereals: What Should We Breed For? , 2002 .

[61]  E. Holme,et al.  Deficiency of mitochondrial ATP synthase of nuclear genetic origin , 2006, Neuromuscular Disorders.

[62]  R. Fischer,et al.  Stomatal Opening: Role of Potassium Uptake by Guard Cells , 1968, Science.

[63]  R. David-Schwartz,et al.  Hexose Kinases and Their Role in Sugar-Sensing and Plant Development , 2013, Front. Plant Sci..

[64]  J. Domec,et al.  Bole girdling affects metabolic properties and root, trunk and branch hydraulics of young ponderosa pine trees. , 2008, Tree physiology.

[65]  H. Griffiths.  Carbon isotope discrimination , 1993 .

[66]  R. Kaldenhoff,et al.  The Arabidopsis aquaporin PIP1;2 rules cellular CO(2) uptake. , 2012, Plant, cell & environment.

[67]  J. Shope,et al.  The role of the mesophyll in stomatal responses to light and CO2. , 2008, Plant, cell & environment.

[68]  O. Heath,et al.  Studies in Stomatal Behaviour VI. AN INVESTIGATION OF THE LIGHT RESPONSES OF WHEAT STOMATA WITH THE ATTEMPTED ELIMINATION OF CONTROL BY THE MESOPHYLL , 1954 .

[69]  T. Setter,et al.  Stomatal closure and photosynthetic inhibition in soybean leaves induced by petiole girdling and pod removal. , 1980, Plant physiology.

[70]  T. Lawson,et al.  The nature of heterogeneity in the stomatal behaviour of Phaseolus vulgaris L. primary leaves , 1998 .

[71]  H. L. Miller,et al.  Climate Change 2007: The Physical Science Basis , 2007 .

[72]  C. Willmer,et al.  Carbon dioxide fixation by epidermal and mesophyll tissues of Tulipa and Commelina , 1974, Planta.

[73]  D. Grantz,et al.  Guard cells of Commelina communis L. do not respond metabolically to osmotic stress in isolated epidermis: Implications for stomatal responses to drought and humidity , 1988, Planta.

[74]  R. A. Fischer,et al.  Wheat Yield Progress Associated with Higher Stomatal Conductance and Photosynthetic Rate, and Cooler Canopies , 1998 .

[75]  K. Noguchi,et al.  Apoplastic mesophyll signals induce rapid stomatal responses to CO2 in Commelina communis. , 2013, The New phytologist.

[76]  T. Furuichi,et al.  Closing Plant Stomata Requires a Homolog of an Aluminum-Activated Malate Transporter , 2010, Plant & cell physiology.

[77]  Alain Vavasseur,et al.  Guard cell metabolism and CO2 sensing. , 2005, The New phytologist.

[78]  N. McDowell,et al.  Tobacco aquaporin NtAQP 1 is involved in mesophyll conductance to CO 2 in vivo , 2006 .

[79]  Ulrich Schurr,et al.  The impact of decreased Rubisco on photosynthesis, growth, allocation and storage in tobacco plants which have been transformed with antisense rbcS , 1991 .

[80]  E. Schulze,et al.  Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS , 1991, Planta.

[81]  P. Jarvis,et al.  Direct and indirect effects of light on stomata II. In Commelina communis L. , 1983 .

[82]  R. Hedrich,et al.  Interconversion of fast and slow gating modes of GCAC1, a Guard Cell Anion Channel , 1994, Planta.

[83]  Chun-Peng Song,et al.  Guard-cell signalling for hydrogen peroxide and abscisic acid. , 2008, The New phytologist.

[84]  Yizhou Wang,et al.  Anion channel sensitivity to cytosolic organic acids implicates a central role for oxaloacetate in integrating ion flux with metabolism in stomatal guard cells , 2011, The Biochemical journal.

[85]  Rainer Hedrich,et al.  In the light of stomatal opening: new insights into 'the Watergate'. , 2005, The New phytologist.

[86]  K. Mott,et al.  Do Stomata Respond to CO(2) Concentrations Other than Intercellular? , 1988, Plant physiology.

[87]  K. Mott.  Opinion: stomatal responses to light and CO(2) depend on the mesophyll. , 2009, Plant, cell & environment.

[88]  S. Smeekens,et al.  Sugar effects on early seedling development in Arabidopsis , 2007, Plant Growth Regulation.

[89]  J. W. Outlaw.  Integration of Cellular and Physiological Functions of Guard Cells , 2003 .

[90]  H. Bohnert,et al.  Loss of TIP1;1 aquaporin in Arabidopsis leads to cell and plant death. , 2004, The Plant journal : for cell and molecular biology.

[91]  Tracy Lawson,et al.  The responses of guard and mesophyll cell photosynthesis to CO2, O2, light, and water stress in a range of species are similar. , 2003, Journal of experimental botany.

[92]  T. Sharkey,et al.  Effect of Light Quality on Stomatal Opening in Leaves of Xanthium strumarium L. , 1981, Plant physiology.

[93]  Filip Rolland,et al.  Role of the Arabidopsis Glucose Sensor HXK1 in Nutrient, Light, and Hormonal Signaling , 2003, Science.

[94]  M. Blatt,et al.  The trafficking protein SYP121 of Arabidopsis connects programmed stomatal closure and K⁺ channel activity with vegetative growth. , 2012, The Plant journal : for cell and molecular biology.

[95]  D. Randall,et al.  Photosynthetic carbon reduction pathway is absent in chloroplasts of Vicia faba guard cells. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[96]  A. Thistle,et al.  Stomata: Biophysical and Biochemical Aspects , 1996 .

[97]  A. S. Raghavendra,et al.  Both rubisco and phosphoenolpyruvate carboxylase are beneficial for stomatal function in epidermal strips of Commelina benghalensis , 1997 .

[98]  Bo Shen,et al.  Engineering for drought avoidance: expression of maize NADP-malic enzyme in tobacco results in altered stomatal function. , 2002, Journal of experimental botany.

[99]  J. Pereira,et al.  How plants cope with water stress in the field. Photosynthesis and growth. , 2002, Annals of botany.

[100]  Laura E. Green,et al.  Spatio-temporal decoupling of stomatal and mesophyll conductance induced by vein cutting in leaves of Helianthus annuus , 2013, Front. Plant Sci..

[101]  S. Assmann.  The cellular basis of guard cell sensing of rising CO2 , 1999 .

[102]  E. Baena-González,et al.  Sugar sensing and signaling in plants: conserved and novel mechanisms. , 2006, Annual review of plant biology.

[103]  T. Brodribb,et al.  Stomatal innovation and the rise of seed plants. , 2012, Ecology letters.

[104]  M. Stitt.  Rising Co2 Levels and Their Potential Significance for Carbon Flow in Photosynthetic Cells , 1991 .

[105]  E. Macrobbie,et al.  Ion content and aperture in “isolated” guard cells ofCommelina communis L. , 1980, The Journal of Membrane Biology.

[106]  R. Hedrich,et al.  Diurnal and Light-Regulated Expression of AtSTP1 in Guard Cells of Arabidopsis1 , 2003, Plant Physiology.

[107]  C. Willmer,et al.  Carbon dioxide metabolism in leaf epidermal tissue. , 1973, Plant physiology.

[108]  D. Bowling,et al.  The Effect of a Mesophyll Factor on the Swelling of Guard Cell Protoplasts of Commelina communis L. , 1993 .

[109]  H. Kamada,et al.  Role of malate synthesis mediated by phosphoenolpyruvate carboxylase in guard cells in the regulation of stomatal movement. , 2000, Plant & cell physiology.

[110]  W. Hartung,et al.  Differential responses of maize MIP genes to salt stress and ABA. , 2005, Journal of experimental botany.

[111]  T. Ogawa,et al.  Isotachophoretic Analysis of Ions in Guard Cells of Vicia faba , 1979 .

[112]  M. Petreikov,et al.  Overexpression of Arabidopsis Hexokinase in Tomato Plants Inhibits Growth, Reduces Photosynthesis, and Induces Rapid Senescence , 1999, Plant Cell.

[113]  S. Assmann,et al.  Roles of ion channels and transporters in guard cell signal transduction , 2007, FEBS letters.

[114]  V. Alchanatis,et al.  Relationship between Hexokinase and the Aquaporin PIP1 in the Regulation of Photosynthesis and Plant Growth , 2014, PloS one.

[115]  J. Schroeder,et al.  Exploring biophysical and biochemical components of the osmotic motor that drives stomatal movement , 1988 .

[116]  G. Farquhar,et al.  The ERECTA gene regulates plant transpiration efficiency in Arabidopsis , 2005, Nature.

[117]  R. Hedrich,et al.  Malate Dehydrogenases in Guard Cells of Pisum sativum. , 1990, Plant physiology.

[118]  P. León,et al.  Sugar and hormone connections. , 2003, Trends in plant science.

[119]  I. Rao,et al.  Light and stomatal metabolism : I. Possible involvement of light modulation of enzymes in stomatal movement. , 1983, Plant physiology.

[120]  T. Roitsch,et al.  The hexokinase inhibitor glucosamine exerts a concentration dependent dual effect on protein kinase activity in vitro , 2000 .

[121]  K. Shimazaki,et al.  Cyclic and Noncyclic Photophosphorylation in Isolated Guard Cell Chloroplasts from Vicia faba L. , 1985, Plant physiology.

[122]  A. Webb,et al.  Carbon dioxide induces increases in guard cell cytosolic free calcium , 1996 .

[123]  S. Lurie.  Photochemical properties of guard cell chloroplasts , 1977 .

[124]  S. Thomine,et al.  Sulfate is both a substrate and an activator of the voltage-dependent anion channel of Arabidopsis hypocotyl cells. , 1999, Plant physiology.

[125]  P. Andersen,et al.  Guard-cell apoplastic sucrose concentration--a link between leaf photosynthesis and stomatal aperture size in the apoplastic phloem loader Vicia faba L. , 2007, Plant, cell & environment.

[126]  Plant physiology: The ups and downs of guard cell signalling , 2001, Current Biology.

[127]  Opinion: The red-light response of stomatal movement is sensed by the redox state of the photosynthetic electron transport chain , 2014, Photosynthesis Research.

[128]  G. Tallman,et al.  Sugar Concentrations in Guard Cells of Vicia faba Illuminated with Red or Blue Light : Analysis by High Performance Liquid Chromatography. , 1992, Plant physiology.

[129]  David Stuart Thompson,et al.  How do cell walls regulate plant growth? , 2005, Journal of experimental botany.

[130]  J. Araus,et al.  Plant breeding and drought in C3 cereals: what should we breed for? , 2002, Annals of botany.

[131]  R. Hedrich,et al.  Malate‐induced feedback regulation of plasma membrane anion channels could provide a CO2 sensor to guard cells. , 1993, The EMBO journal.

[132]  G. Pavesi,et al.  Gene trap lines identify Arabidopsis genes expressed in stomatal guard cells. , 2008, The Plant journal : for cell and molecular biology.

[133]  Josep Cifre,et al.  Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. , 2006, The Plant journal : for cell and molecular biology.

[134]  J. Manchester,et al.  Guard cell starch concentration quantitatively related to stomatal aperture. , 1979, Plant physiology.

[135]  W. H. Outlaw,et al.  Transpiration rate. An important factor controlling the sucrose content of the guard cell apoplast of broad bean. , 2001, Plant physiology.

[136]  G. Farquhar,et al.  Gain of the feedback loop involving carbon dioxide and stomata: theory and measurement. , 1978, Plant physiology.

[137]  P. León,et al.  Hexokinase as a sugar sensor in higher plants. , 1997, The Plant cell.

[138]  F. Woodward,et al.  The role of stomata in sensing and driving environmental change , 2003, Nature.

[139]  C. Tinoco-Ojanguren,et al.  Stomatal dynamics and its importance to carbon gain in two rainforest Piper species , 1993, Oecologia.

[140]  Yves Gibon,et al.  Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. , 2007, The Plant journal : for cell and molecular biology.

[141]  C. Tonelli,et al.  DOF-binding sites additively contribute to guard cell-specificity of AtMYB60 promoter , 2011, BMC Plant Biology.

[142]  Graham D. Farquhar,et al.  Carbon isotope discrimination is positively correlated with grain yield and dry matter production in field-grown wheat , 1987 .

[143]  W. Allaway.  Accumulation of malate in guard cells of Vicia faba during stomatal opening , 1973, Planta.

[144]  Ingo Dreyer,et al.  The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[145]  Rosenfeld,et al.  Rates of sugar uptake by guard cell protoplasts of pisum sativum L. Related To the solute requirement for stomatal opening , 1999, Plant physiology.

[146]  S. Robinson,et al.  Food Security: The Challenge of Feeding 9 Billion People , 2010, Science.

[147]  N. Provart,et al.  Cloning and electrophysiological analysis of KST1, an inward rectifying K+ channel expressed in potato guard cells. , 1995, The EMBO journal.

[148]  S. Mehta,et al.  CO(2) signaling in guard cells: calcium sensitivity response modulation, a Ca(2+)-independent phase, and CO(2) insensitivity of the gca2 mutant. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[149]  J. Mayo,et al.  The occurrence of functional non-chlorophyllous guard cells in Paphiopedilum spp. , 1975 .

[150]  K. Tanaka,et al.  Light Activation of NADP-Malate Dehydrogenase in Guard Cell Protoplasts from Vicia faba L. , 1985, Plant physiology.

[151]  M. C. Tarczynski,et al.  Taxonomic survey for the presence of ribulose-1,5-bisphosphate carboxylase activity in guard cells. , 1982, Plant physiology.

[152]  R. Wallach,et al.  Hexokinase mediates stomatal closure. , 2013, The Plant journal : for cell and molecular biology.

[153]  E. Neufeld,et al.  CARBOHYDRATE METABOLISM. , 1965, Annual review of biochemistry.

[154]  K. Mott,et al.  Stomatal Responses to Flooding of the Intercellular Air Spaces Suggest a Vapor-Phase Signal Between the Mesophyll and the Guard Cells1[OA] , 2010, Plant Physiology.

[155]  J. Weyers,et al.  Volume changes of Commelina communis guard cell protoplasts in response to K+, light and CO2 , 1986 .

[156]  Shimazaki,et al.  The multisensory guard cell. Stomatal responses to blue light and abscisic acid , 1999, Plant physiology.

[157]  Zhen-Ming Pei,et al.  Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells , 2000, Nature.

[158]  J. Weyers,et al.  The primary processes of photosystem II in purified guard-cell protoplasts and mesophyll-cell protoplasts from Commelina communis L. , 1983, Planta.

[159]  W. H. Outlaw.  Critical examination of the quantitative evidence for and against photosynthetic CO2 fixation by guard cells , 1989 .

[160]  V. Alchanatis,et al.  The Pitfalls of Transgenic Selection and New Roles of AtHXK1: A High Level of AtHXK1 Expression Uncouples Hexokinase1-Dependent Sugar Signaling from Exogenous Sugar1[W] , 2012, Plant Physiology.

[161]  J. Preiss,et al.  Localization of Carbohydrate Metabolizing Enzymes in Guard Cells of Commelina communis. , 1987, Plant physiology.

[162]  T. Kinoshita,et al.  Guard-cell chloroplasts provide ATP required for H(+) pumping in the plasma membrane and stomatal opening. , 2001, Plant & cell physiology.

[163]  C. Pearson.  Daily Changes in Stomatal Aperture and in Carbohydrates and Malate Within Epidermis and Mesophyll of leaves of Commelina Cyanea and Vicia Faba , 1973 .

[164]  M. Blatt,et al.  The effect of elevated CO2 concentrations on K+ and anion channels of Vicia faba L. guard cells , 1997, Planta.

[165]  Toshinori Kinoshita,et al.  Blue light activates the plasma membrane H+‐ATPase by phosphorylation of the C‐terminus in stomatal guard cells , 1999, The EMBO journal.

[166]  J. Fisahn,et al.  Gas-exchange analysis of chloroplastic fructose-1,6-bisphosphatase antisense potatoes at different air humidities and at elevated CO2 , 1999, Planta.

[167]  Tracy Lawson,et al.  Responses of photosynthetic electron transport in stomatal guard cells and mesophyll cells in intact leaves to light, CO2, and humidity. , 2002, Plant physiology.

[168]  J. Pallas.  Guard-Cell Starch Retention and Accumulation in the Dark , 1964, Botanical Gazette.

[169]  E. Schulze,et al.  Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS , 1992, Planta.

[170]  Alan M. Jones,et al.  A Comparative Study of the Arabidopsis thaliana Guard-Cell Transcriptome and Its Modulation by Sucrose , 2012, PloS one.

[171]  H. Schnabl.  The compartmentation of carboxylating and decarboxylating enzymes in guard cell protoplasts , 1981, Planta.

[172]  James Larmour-Reid.  The Food Security Challenge , 2011 .

[173]  J. Berry,et al.  Effects of O(2) and CO(2) Concentration on the Steady-State Fluorescence Yield of Single Guard Cell Pairs in Intact Leaf Discs of Tradescantia albiflora: Evidence for Rubisco-Mediated CO(2) Fixation and Photorespiration in Guard Cells. , 1992, Plant physiology.

[174]  R. Scheibe,et al.  Rubisco activity in guard cells compared with the solute requirement for stomatal opening. , 1990, Plant physiology.

[175]  T. Lawson,et al.  Reductions in mesophyll and guard cell photosynthesis impact on the control of stomatal responses to light and CO2 , 2008, Journal of experimental botany.

[176]  L. Urban,et al.  Girdling decreases photosynthetic electron fluxes and induces sustained photoprotection in mango leaves. , 2007, Tree physiology.

[177]  I. R. Cowan,et al.  Stomatal conductance correlates with photosynthetic capacity , 1979, Nature.

[178]  W. Frommer,et al.  Introns control expression of sucrose transporter LeSUT1 in trichomes, companion cells and in guard cells , 2008, Plant Molecular Biology.

[179]  C. Tinoco-Ojanguren,et al.  Stomatal dynamics and its importance to carbon gain in two rainforest Piper species , 1993, Oecologia.

[180]  K. Shimazaki,et al.  Photosynthetic Properties of Guard Cell Protoplasts from Vicia faba L. , 1982 .

[181]  R. Hedrich,et al.  KAT1 is not essential for stomatal opening , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[182]  L. D. Talbott,et al.  The role of sucrose in guard cell osmoregulation , 1998 .

[183]  R. Hedrich,et al.  GORK, a delayed outward rectifier expressed in guard cells of Arabidopsis thaliana, is a K+‐selective, K+‐sensing ion channel , 2000, FEBS letters.

[184]  Corinne Le Quéré,et al.  Climate Change 2013: The Physical Science Basis , 2013 .

[185]  W. H. Outlaw.  Carbon Metabolism in Guard Cells , 1982 .

[186]  Joel E. Cohen,et al.  Human Population: The Next Half Century , 2003, Science.

[187]  V. Neuhoff,et al.  Electrophoretic Assay for Ribulose 1,5-Bisphosphate Carboxylase/Oxygenase in Guard Cells and Other Leaf Cells of Vicia faba L. , 1989, Plant physiology.

[188]  J. Schroeder,et al.  Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool , 2008, Plant Methods.

[189]  J. Olsen,et al.  Far red end-of-day treatment restores wild type-like plant length in hybrid aspen overexpressing phytochrome A. , 2002, Physiologia plantarum.

[190]  S. Assmann,et al.  The Control of Transpiration. Insights from Arabidopsis1 , 2006, Plant Physiology.

[191]  Yin Wang,et al.  Overexpression of plasma membrane H+-ATPase in guard cells promotes light-induced stomatal opening and enhances plant growth , 2013, Proceedings of the National Academy of Sciences.

[192]  M. C. Tarczynski,et al.  Elevated Levels of Both Sucrose-Phosphate Synthase and Sucrose Synthase in Vicia Guard Cells Indicate Cell-Specific Carbohydrate Interconversions , 1993, Plant physiology.

[193]  R. Kaldenhoff,et al.  The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO₂ transport facilitator. , 2011, The Plant journal : for cell and molecular biology.

[194]  Susanne von Caemmerer,et al.  The Contribution of Photosynthesis to the Red Light Response of Stomatal Conductance1[OA] , 2007, Plant Physiology.

[195]  N. Provart,et al.  Changes in stomatal function and water use efficiency in potato plants with altered sucrolytic activity. , 2012, Plant, cell & environment.

[196]  Susan S. Taylor,et al.  Calcium-Dependent and -Independent Stomatal Signaling Network and Compensatory Feedback Control of Stomatal Opening via Ca2+ Sensitivity Priming[W] , 2013, Plant Physiology.

[197]  G. Amodeo,et al.  Use of Potassium and Sucrose by Onion Guard Cells during a Daily Cycle of Osmoregulation , 1996 .

[198]  M. Stitt,et al.  Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS , 1993, Planta.

[199]  P. Gans,et al.  Relationship between Respiration and Photosynthesis in Guard Cell and Mesophyll Cell Protoplasts of Commelina communis L. , 1991, Plant physiology.

[200]  I. R. Cowan,et al.  The relative role of stomata in transpiration and assimilation , 1971, Planta.

[201]  R. Hedrich,et al.  Malate‐sensitive anion channels enable guard cells to sense changes in the ambient CO2 concentration , 1994 .

[202]  K. Iba,et al.  New Approaches to the Biology of Stomatal Guard Cells , 2013, Plant & cell physiology.

[203]  Miguel González-Guzmán,et al.  PYR/RCAR Receptors Contribute to Ozone-, Reduced Air Humidity-, Darkness-, and CO2-Induced Stomatal Regulation1[C][W][OA] , 2013, Plant Physiology.

[204]  C. Maurel,et al.  Molecular physiology of aquaporins in plants. , 2002, International review of cytology.

[205]  T. Lawson,et al.  Photosynthesis and Stomatal Behaviour , 2010 .

[206]  T. Sharkey,et al.  Separation and measurement of direct and indirect effects of light on stomata. , 1981, Plant physiology.

[207]  J. Sheen,et al.  The role of hexokinase in plant sugar signal transduction and growth and development , 2000, Plant Molecular Biology.

[208]  L. D. Talbott,et al.  The guard cell chloroplast: a perspective for the twenty-first century. , 2002, The New phytologist.

[209]  Klaus Raschke,et al.  Voltage-dependent anion channels in the plasma membrane of guard cells , 1989, Nature.

[210]  O. H. Lowry,et al.  Organic acid and potassium accumulation in guard cells during stomatal opening. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[211]  K. Raschke,et al.  Stomatal opening quantitatively related to potassium transport: evidence from electron probe analysis. , 1971, Plant physiology.

[212]  W. H. Outlaw.  Current concepts on the role of potassium in stomatal movements , 1983 .

[213]  M. Badger,et al.  The Role of Phosphoenolpyruvate Carboxylase during C4 Photosynthetic Isotope Exchange and Stomatal Conductance1[OA] , 2007, Plant Physiology.

[214]  M. Blatt.  Cellular signaling and volume control in stomatal movements in plants. , 2000, Annual review of cell and developmental biology.

[215]  E. Macrobbie,et al.  Signal transduction and ion channels in guard cells. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[216]  I. Terashima,et al.  Effects of HgCl(2) on CO(2) dependence of leaf photosynthesis: evidence indicating involvement of aquaporins in CO(2) diffusion across the plasma membrane. , 2002, Plant & cell physiology.

[217]  A. Hetherington,et al.  How do stomata sense reductions in atmospheric relative humidity? , 2013, Molecular plant.

[218]  L. D. Talbott,et al.  Central Roles for Potassium and Sucrose in Guard-Cell Osmoregulation , 1996, Plant physiology.

[219]  S. Gibson,et al.  The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. , 2000, The Plant journal : for cell and molecular biology.

[220]  G. Hammer,et al.  Characterizing drought stress and trait influence on maize yield under current and future conditions , 2014, Global change biology.

[221]  T. Andrews,et al.  Reduction of ribulose-1,5-bisphosphate carboxylase/oxygenase content by antisense RNA reduces photosynthesis in transgenic tobacco plants. , 1992, Plant physiology.

[222]  P. Lu,et al.  A New Mechanism for the Regulation of Stomatal Aperture Size in Intact Leaves (Accumulation of Mesophyll-Derived Sucrose in the Guard-Cell Wall of Vicia faba) , 1997, Plant physiology.

[223]  R. Turgeon,et al.  A comprehensive picture of phloem loading strategies , 2009, Proceedings of the National Academy of Sciences.

[224]  David M Kramer,et al.  Improving yield by exploiting mechanisms underlying natural variation of photosynthesis. , 2012, Current opinion in biotechnology.

[225]  J. Schroeder,et al.  GUARD CELL SIGNAL TRANSDUCTION. , 2003, Annual review of plant physiology and plant molecular biology.

[226]  Christophe Maurel,et al.  Plant aquaporins: membrane channels with multiple integrated functions. , 2008, Annual review of plant biology.

[227]  F. Rolland,et al.  Sugar Sensing and Signaling , 2008, The arabidopsis book.

[228]  P. Kuiper,et al.  Dependence upon Wavelength of Stomatal Movement in Epidermal Tissue of Senecio odoris. , 1964, Plant physiology.

[229]  T. Lawson,et al.  Stomatal Size, Speed, and Responsiveness Impact on Photosynthesis and Water Use Efficiency1[C] , 2014, Plant Physiology.

[230]  D. Bowling,et al.  Influence of the Mesophyll on Stomatal Opening , 1995 .

[231]  Tracy Lawson,et al.  Guard cell photosynthesis and stomatal function. , 2009, The New phytologist.

[232]  W. Davies,et al.  Stomatal Closure in Flooded Tomato Plants Involves Abscisic Acid and a Chemically Unidentified Anti-Transpirant in Xylem Sap , 1996, Plant physiology.