What can mechanistic models tell us about guard cells, photosynthesis, and water use efficiency?

Blatt, M.R. and Jezek, M. and Lew, V.L. and Hills, A. (2022) What can mechanistic models tell us about guard cells, photosynthesis, and water use efficiency? Trends in Plant Science, 27 (2). pp. 166-179. ISSN 1360-1385

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Stomatal pores facilitate gaseous exchange between the inner air spaces of the leaf and the atmosphere. The pores open to enable CO 2 entry for photosynthesis and close to reduce transpirational water loss. How stomata respond to the environment has long attracted interest in modeling as a tool to understand the consequences for the plant and for the ecosystem. Models that focus on stomatal conductance for gas exchange make intuitive sense, but such models need also to connect with the mechanics of the guard cells that regulate pore aperture if we are to understand the ‘decisions made’ by stomata, their impacts on the plant and on the global environment.

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Trends in Plant Science
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Export Date: 6 October 2021 CODEN: TPSCF Correspondence Address: Blatt, M.R.; Laboratory of Plant Physiology and Biophysics, Bower Building, United Kingdom; email: Michael.Blatt@glasgow.ac.uk Funding details: Biotechnology and Biological Sciences Research Council, BBSRC Funding text 1: Development of the OnGuard platform was supported with grants BB/L001276/1 , BB/L019025/1 , BB/M001601/1 , and BB/N01832X/1 from the UK Biotechnology and Biological Sciences Research Council . We thank the many colleagues who have contributed to the OnGuard project and to formal and informal discussions over the past decade, especially Zhong-Hua Chen (Western Sydney), Yizhou Wang (Zhejiang), Tracy Lawson (Essex), Howard Griffiths (Cambridge), Anna Amtmann (Glasgow), Simon Rogers (Glasgow), Maria Papanatsiou (Glasgow), Cornelia Eisenach (Zurich), Enrico Martinoia (Zurich), Silvere Vialet-Chabrand (Essex), Diana Santelia (Zurich), Florent Pantin (Montpellier), Keith Mott (Salt Lake City), Graham Farquhar and Ross Deans (Canberra), and Tom Buckley (Davis). Funding text 2: Development of the OnGuard platform was supported with grants BB/L001276/1, BB/L019025/1, BB/M001601/1, and BB/N01832X/1 from the UK Biotechnology and Biological Sciences Research Council. We thank the many colleagues who have contributed to the OnGuard project and to formal and informal discussions over the past decade, especially Zhong-Hua Chen (Western Sydney), Yizhou Wang (Zhejiang), Tracy Lawson (Essex), Howard Griffiths (Cambridge), Anna Amtmann (Glasgow), Simon Rogers (Glasgow), Maria Papanatsiou (Glasgow), Cornelia Eisenach (Zurich), Enrico Martinoia (Zurich), Silvere Vialet-Chabrand (Essex), Diana Santelia (Zurich), Florent Pantin (Montpellier), Keith Mott (Salt Lake City), Graham Farquhar and Ross Deans (Canberra), and Tom Buckley (Davis). No interests are declared. References: Luttge, U., Ecophysiology of crassulacean acid metabolism (CAM) (2004) Ann. Bot., 93, pp. 629-652; Jezek, M., Blatt, M.R., The membrane transport system of the guard cell and its integration for stomatal dynamics (2017) Plant Physiol., 174, pp. 487-519; Lawson, T., Blatt, M.R., Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency (2014) Plant Physiol., 164, pp. 1556-1570; Berry, J.A., Stomata: key players in the earth system, past and present (2010) Curr. Opin. Plant Biol., 13, pp. 233-240; Hetherington, A.M., Woodward, F.I., The role of stomata in sensing and driving environmental change (2003) Nature, 424, pp. 901-908; Betts, A.K., The land surface-atmosphere interaction: a review based on observational and global modeling perspectives (1996) J. Geophys. Res.-Atmos., 101, pp. 7209-7225; Beljaars, A.C.M., The anomalous rainfall over the United States during July 1993: sensitivity to land surface parameterization and soil moisture (1996) Mon. Weather Rev., 124, pp. 362-383; Jasechko, S., Terrestrial water fluxes dominated by transpiration (2013) Nature, 496, pp. 347-351; UNESCO, Water for a Sustainable World—UN World Water Development Report (2015), UNESCO; Philander, S.G., Climate impacts LINK project (2012) Encyclopedia of Global Warming & Climate Change, 1, p. 287. , SAGE Publications, Inc; Endy, D., Brent, R., Modelling cellular behaviour (2001) Nature, 409, pp. 391-395; van Riel, N.A.W., Dynamic modelling and analysis of biochemical networks: mechanism-based models and model-based experiments (2006) Brief. Bioinform., 7, pp. 364-374; Stelling, J., Robustness of cellular functions (2004) Cell, 118, pp. 675-685; Willmer, C., Fricker, M.D., Stomata (1996), Chapman and Hall; Lawson, T., Photosynthesis and stomatal behaviour (2011) Prog. Bot., 72, pp. 265-304; Sack, L., Holbrook, N.M., Leaf hydraulics (2006) Annu. Rev. Plant Biol., 57, pp. 361-381; Pearcy, R.W., Sunflecks and photosynthesis in plant canopies (1990) Annu. Rev. Plant Physiol. Plant Mol. Biol., 41, pp. 421-453; Cowan, I.R., Farquhar, G.D., Stomatal function in relation to leaf metabolism and environment (1977) Symp. Soc. Exp. Biol., 31, pp. 471-505; Manzoni, S., Hydraulic limits on maximum plant transpiration and the emergence of the safety-efficiency trade-off (2013) New Phytol., 198, pp. 169-178; Vico, G., Effects of stomatal delays on the economics of leaf gas exchange under intermittent light regimes (2011) New Phytol., 192, pp. 640-652; Buckley, T.N., Schymanski, S.J., Stomatal optimisation in relation to atmospheric CO2 (2014) New Phytol., 201, pp. 372-377; Lin, Y.-S., Optimal stomatal behaviour around the world (2015) Nat. Clim. Chang., 5, pp. 459-464; Schymanski, S.J., A canopy-scale test of the optimal water-use hypothesis (2008) Plant Cell Environ., 31, pp. 97-111; Ball, M.C., Farquhar, G.D., Photosynthetic and somatal responses of 2 species, Aegiceras corniculatum and Avicennia marina, to long-term salinity and humidity conditions (1984) Plant Physiol., 74, pp. 1-6; Williams, W.E., Optimal water-use efficiency in a California shrub (1983) Plant Cell Environ., 6, pp. 145-151; Ball, J.T., A model predicting stomatal conductance and its contribution to the control of photosynthesis under different environmental conditions (1987) Progress in Photosynthesis Research, pp. 221-224. , J. Biggens Martinus-Nijhoff; Damour, G., An overview of models of stomatal conductance at the leaf level (2010) Plant Cell Environ., 33, pp. 1419-1438; Leuning, R., A critical-appraisal of a combined stomatal-photosynthesis model for C-3 plants (1995) Plant Cell Environ., 18, pp. 339-355; Manzoni, S., Optimizing stomatal conductance for maximum carbon gain under water stress: a meta-analysis across plant functional types and climates (2011) Funct. Ecol., 25, pp. 456-467; Cowan, I.R., Economics of carbon fixation in higher plants. On the economy of plant form and function, proceedings of the Sixth Maria Moors Cabot Symposium, Evolutionary Constraints on Primary Productivity, Adaptive Patterns of Energy Capture in Plants, Harvard Forest, August 1983 (1986), pp. 133-170; Katul, G., A stomatal optimization theory to describe the effects of atmospheric CO2 on leaf photosynthesis and transpiration (2010) Ann. Bot., 105, pp. 431-442; Wolf, A., Optimal stomatal behavior with competition for water and risk of hydraulic impairment (2016) Proc. Natl. Acad. Sci. U. S. A., 113, pp. E7222-E7230; Pieruschka, R., Control of transpiration by radiation (2010) Proc. Natl. Acad. Sci. U. S. A., 107, pp. 13372-13377; Santelia, D., Lawson, T., Rethinking guard cell metabolism (2016) Plant Physiol., 172, pp. 1371-1392; Palevitz, B.A., Hepler, P.K., Changes in dye coupling of stomatal cells of Allium and Commelina demonstrated by microinjection of lucifer yellow (1985) Planta, 164, pp. 473-479; Erwee, M.G., Cell–cell communication in the leaves of Commelina cyanea and other plants (1985) Plant Cell Environ., 8, pp. 173-178; Wille, A., Lucas, W., Ultrastructural and histochemical studies on guard cells (1984) Planta, 160, pp. 129-142; Fischer, R.A., Stomatal opening in isolated epidermal strips of Vicia faba I. Responses to light and CO2-free air (1968) Plant Physiol., 43, pp. 1947-1952; Blatt, M.R., Thiel, G., K+ channels of stomatal guard cells: bimodal control of the K+ inward-rectifier evoked by auxin (1994) Plant J., 5, pp. 55-68; Horaruang, W., Communication between the plasma membrane and tonoplast is an emergent property of ion transport (2020) Plant Physiol., 182, pp. 1833-1835; Franks, P.J., Stomatal function across temporal and spatial scales: deep-time trends, land-atmosphere coupling and global models (2017) Plant Physiol., 174, pp. 583-602; Chen, Z.-H., Molecular evolution of grass stomata (2017) Trends Plant Sci., 22, pp. 124-139; Cai, S., Evolutionary conservation of ABA signaling for stomatal closure (2017) Plant Physiol., 174, pp. 732-747; Minguet-Parramona, C., An optimal frequency in Ca2+ oscillations for stomatal closure is an emergent property of ion transport in guard cells (2016) Plant Physiol., 170, pp. 32-45; Blatt, M.R., Concepts and techniques in plant membrane physiology (2004) Membrane Transport in Plants, pp. 1-39. , M.R. Blatt Blackwell; Wang, Y., Unexpected connections between humidity and ion transport discovered using a model to bridge guard cell-to-leaf scales (2017) Plant Cell, 29, pp. 2921-2939; Yu, H., Overlapping and differential roles of plasma membrane calcium ATPases in Arabidopsis growth and environmental responses (2018) J. Exp. Bot., 69, pp. 2693-2703; Jeanguenin, L., AtKC1 is a general modulator of Arabidopsis inward Shaker channel activity (2011) Plant J., 67, pp. 570-582; Pilot, G., Guard cell inward K+ channel activity in Arabidopsis involves expression of the twin channel subunits KAT1 and KAT2 (2001) J. Biol. Chem., 276, pp. 3215-3221; Fluetsch, S., Guard cell starch degradation yields glucose for rapid stomatal opening in Arabidopsis (2020) Plant Cell, 32, pp. 2325-2344; Horrer, D., Blue light induces a distinct starch degradation pathway in guard cells for stomatal opening (2016) Curr. Biol., 26, pp. 362-370; Blatt, M.R., Plant physiology: redefining the enigma of metabolism in stomatal movement (2016) Curr. Biol., 26, pp. R107-R109; Grabov, A., Blatt, M.R., A steep dependence of inward-rectifying potassium channels on cytosolic free calcium concentration increase evoked by hyperpolarization in guard cells (1999) Plant Physiol., 119, pp. 277-287; Grabov, A., Blatt, M.R., Parallel control of the inward-rectifier K+ channel by cytosolic-free Ca2+ and pH in Vicia guard cells (1997) Planta, 201, pp. 84-95; MacRobbie, E.A.C., Signal transduction and ion channels in guard cells (1998) Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci., 353, pp. 1475-1488; Sanders, D., Calcium at the crossroads of signaling (2002) Plant Cell, 14, pp. S401-S417; Hills, A., OnGuard, a computational platform for quantitative kinetic modeling of guard cell physiology (2012) Plant Physiol., 159, pp. 1026-1042; Klejchova, M., Predicting the unexpected in stomatal gas exchange: not just an open-and-shut case (2020) Biochem. Soc. Trans., 48, pp. 881-889; Buckley, T.N., Mott, K.A., Modelling stomatal conductance in response to environmental factors (2013) Plant Cell Environ., 36, pp. 1691-1699; Buckley, T.N., Modeling stomatal conductance (2017) Plant Physiol., 174, pp. 572-582; Buckley, T.N., A hydromechanical and biochemical model of stomatal conductance (2003) Plant Cell Environ., 26, pp. 1767-1785; Deans, R.M., An integrated hydraulic-hormonal model of conifer stomata predicts water stress dynamics (2017) Plant Physiol., 174, pp. 478-486; Lew, V.L., A mathematical-model of the volume, pH, and ion content regulation in reticulocytes—application to the pathophysiology of sickle-cell dehydration (1991) J. Clin. Investig., 87, pp. 100-112; Lew, V.L., Behavior of transporting epithelial cells. I. Computer analysis of a basic model (1979) Proc. R. Soc. Lond. Ser. B Biol., 206, pp. 53-83; Chen, Z.H., Systems dynamic modeling of the stomatal guard cell predicts emergent behaviors in transport, signaling, and volume control (2012) Plant Physiol., 159, pp. 1235-1251; Wang, Y., Systems dynamic modelling of a guard cell Cl− channel mutant uncovers an emergent homeostatic network regulating stomatal transpiration (2012) Plant Physiol., 160, pp. 1956-1972; Peak, D., Mott, K.A., A new, vapour-phase mechanism for stomatal responses to humidity and temperature (2011) Plant Cell Environ., 34, pp. 162-178; Rockwell, F.E., The competition between liquid and vapor transport in transpiring leaves (2014) Plant Physiol., 164, pp. 1741-1758; Buckley, T.N., The sites of evaporation within leaves (2017) Plant Physiol., 173, pp. 1763-1782; Jezek, M., A constraint-relaxation-recovery mechanism for stomatal dynamics (2019) Plant Cell Environ., 42, pp. 2399-2410; Jezek, M., Guard cell endomembrane Ca2+-ATPases underpin a ‘carbon memory’ of photosynthetic assimilation that impacts on water use efficiency (2021) Nat. Plants, , Published online July 29, 2021; Doi, M., Shimazaki, K.-i., The stomata of the fern Adiantum capillus-veneris do not respond to CO2 in the dark and open by photosynthesis in guard cells (2008) Plant Physiol., 147, pp. 922-930; Olsen, R.L., Red light activates a chloroplast-dependent ion uptake mechanism for stomatal opening under reduced CO2 concentrations in Vicia spp (2002) New Phytol., 153, pp. 497-508; Morison, J.I.L., Jarvis, P.G., Direct and indirect effects of light on stomata. II. In Commelina communis L (1983) Plant Cell Environ., 6, pp. 103-109; Webb, A.A.R., Carbon dioxide induces increases in guard cell cytosolic free calcium (1996) Plant J., 9, pp. 297-304; Xue, S.W., Central functions of bicarbonate in S-type anion channel activation and OST1 protein kinase in CO2 signal transduction in guard cells (2011) EMBO J., 30, pp. 1645-1658; Vialet-Chabrand, S., Global sensitivity analysis of OnGuard models identifies key hubs for transport interaction in stomatal dynamics (2017) Plant Physiol., 174, pp. 680-688; Ando, E., Kinoshita, T., Red light-induced phosphorylation of plasma membrane H+-ATPase in stomatal guard cells (2018) Plant Physiol., 178, pp. 838-849; Inoue, S.-I., CIPK23 regulates blue light-dependent stomatal opening in Arabidopsis thaliana (2020) Plant J., 104, pp. 679-692; Hu, H.H., Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells (2010) Nat. Cell Biol., 12, pp. 87-90; Zhang, J., Insights into the molecular mechanisms of CO2-mediated regulation of stomatal movements (2018) Curr. Biol., 28, pp. R1356-R1363; Kollist, H., Closing gaps: linking elements that control stomatal movement (2014) New Phytol., 203, pp. 44-62; Mott, K.A., The role of the mesophyll in stomatal responses to light and CO2 (2008) Plant Cell Environ., 31, pp. 1299-1306; Farquhar, G.D., Sharkey, T.D., Stomatal conductance and photosynthesis (1982) Annu. Rev. Plant Physiol. Plant Mol. Biol., 33, pp. 317-345; Zhu, J., The stomatal response to CO2 is linked to changes in guard cell zeaxanthin (1998) Plant Cell Environ., 21, pp. 813-820; Yang, X., A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world (2015) New Phytol., 207, pp. 491-504; Zhu, X.G., Improving photosynthetic efficiency for greater yield (2010) Annu. Rev. Plant Biol., 61, pp. 235-261; Papanatsiou, M., Optogenetic manipulation of stomatal kinetics improves carbon assimilation and water use efficiency (2019) Science, 363, pp. 1456-1459; Betts, A.K., Understanding hydrometeorology using global models (2004) Bull. Am. Meteorol. Soc., 85, pp. 1673-1688; Gedney, N., Detection of a direct carbon dioxide effect in continental river runoff records (2006) Nature, 439, pp. 835-838; Nikoloski, Z., Inference and prediction of metabolic network fluxes (2015) Plant Physiol., 169, pp. 1443-1455; Shameer, S., Computational analysis of the productivity potential of CAM (2018) Nat. Plants, 4, pp. 165-171; Cheung, C.Y.M., A method of accounting for enzyme costs in flux balance analysis reveals alternative pathways and metabolite stores in an illuminated Arabidopsis leaf (2015) Plant Physiol., 169, pp. 1671-1682; Santelia, D., Lunn, J.E., Transitory starch metabolism in guard cells: unique features for a unique function (2017) Plant Physiol., 174, pp. 539-549; Hummel, I., Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis (2010) Plant Physiol., 154, pp. 357-372; Farooq, M., Plant drought stress: effects, mechanisms and management (2009) Agron. Sustain. Dev., 29, pp. 185-212; Hiyama, A., Blue light and CO2 signals converge to regulate light-induced stomatal opening (2017) Nat. Commun., 8, p. 1284; Shahzad, Z., A potassium-dependent oxygen sensing pathway regulates plant root hydraulics (2016) Cell, 167, pp. 87-98; Chaumont, F., Tyerman, S.D., Aquaporins: highly regulated channels controlling plant water relations (2014) Plant Physiol., 164, pp. 1600-1618; Lefoulon, C., Crassulacean acid metabolism guard cell anion channel activity follows transcript abundance and is suppressed by apoplastic malate (2020) New Phytol., 227, pp. 1847-1857; Yang, X., The Kalanchoe genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism (2017) Nat. Commun., 8, p. 1899; Wong, J.H., SAUR proteins and PP2C.D phosphatases regulate H+-ATPases and K+ channels to control stomatal movements (2021) Plant Physiol., 185, pp. 256-273; Acharya, B.R., Assmann, S.M., Hormone interactions in stomatal function (2009) Plant Mol. Biol., 69, pp. 451-462; Islam, M.M., Roles of AtTPC1, vacuolar two pore channel 1, in Arabidopsis stomatal closure (2010) Plant Cell Physiol., 51, pp. 302-311; Peiter, E., The vacuolar Ca2+ -activated channel TPC1 regulates germination and stomatal movement (2005) Nature, 434, pp. 404-408
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