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Annual Review of Plant Biology

Volume 71, 2020

Guard Cell Metabolism and Stomatal Function

Abstract

The control of gaseous exchange between the leaf and external atmosphere is governed by stomatal conductance (); therefore, stomata play a critical role in photosynthesis and transpiration and overall plant productivity. Stomatal conductance is determined by both anatomical features and behavioral characteristics. Here we review some of the osmoregulatory pathways in guard cell metabolism, genes and signals that determine stomatal function and patterning, and the recent work that explores coordination between and carbon assimilation () and the influence of spatial distribution of functional stomata on underlying mesophyll anatomy. We also evaluate the current literature on mesophyll-driven signals that may coordinate stomatal behavior with mesophyll carbon assimilation and explore stomatal kinetics as a possible target to improve and water use efficiency. By understanding these processes, we can start to provide insight into manipulation of these regulatory pathways to improve stomatal behavior and identify novel unexploited targets for altering stomatal behavior and improving crop plant productivity.

Keyword(s): guard cells, mesophyll, osmoregulation, photosynthesis, stomata, subsidiary cells
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/content/journals/10.1146/annurev-arplant-050718-100251
2020-04-29
2024-04-25
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Literature Cited

  1. 1. 
    Ache P, Becker D, Ivashikina N, Dietrich P, Roelfsema MRG, Hedrich R 2000. GORK, a delayed outward rectifier expressed in guard cells of Arabidopsis thaliana, is a K+‐selective, K+‐sensing ion channel. FEBS Lett 486:293–98
     [Google Scholar]
  2. 2. 
    Ackerson RC, Hebert RR. 1981. Osmoregulation in cotton in response to water stress: I. Alterations in photosynthesis, leaf conductance, translocation, and ultrastructure. Plant Physiol 67:3484–88
     [Google Scholar]
  3. 3. 
    Allaway WG, Hsiao TC. 1973. Preparation of rolled epidermis of Vicia faba L. so that stomata are the only viable cells: analysis of guard cell potassium by flame photometry. Aust. J. Biol. Sci. 26:2309–18
     [Google Scholar]
  4. 4. 
    Amodeo G, Talbott LD, Zeiger E 1996. Use of potassium and sucrose by onion guard cells during a daily cycle of osmoregulation. Plant Cell Physiol 37:5575–79
     [Google Scholar]
  5. 5. 
    Antunes WC, de Menezes Daloso D, Pinheiro DP, Williams TCR, Loureiro ME 2017. Guard cell-specific down-regulation of the sucrose transporter SUT1 leads to improved water use efficiency and reveals the interplay between carbohydrate metabolism and K+ accumulation in the regulation of stomatal opening. Environ. Exp. Bot. 135:73–85
     [Google Scholar]
  6. 6. 
    Antunes WC, Provart NJ, Williams TC, Loureiro ME 2012. Changes in stomatal function and water use efficiency in potato plants with altered sucrolytic activity. Plant Cell Environ 35:4747–59
     [Google Scholar]
  7. 7. 
    Assmann SM, Shimazaki KI. 1999. The multisensory guard cell: stomatal responses to blue light and abscisic acid. Plant Physiol 119:3809–16
     [Google Scholar]
  8. 8. 
    Azoulay-Shemer T, Bagheri A, Wang C, Palomares A, Stephan AB et al. 2016. Starch biosynthesis in guard cells but not in mesophyll cells is involved in CO2-induced stomatal closing. Plant Physiol 171:2788–98
     [Google Scholar]
  9. 9. 
    Azoulay‐Shemer T, Palomares A, Bagheri A, Israelsson‐Nordstrom M, Engineer CB et al. 2015. Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO2‐ and ABA‐induced stomatal closing. Plant J 83:4567–81
     [Google Scholar]
  10. 10. 
    Ballard T, Peak D, Mott K 2019. Blue and red light effects on stomatal oscillations. Funct. Plant Biol. 46:2146–51
     [Google Scholar]
  11. 11. 
    Baroli I, Price GD, Badger MR, Caemmerer S Von 2008. The contribution of photosynthesis to the red light response of stomatal conductance. Plant Physiol 146:737–47
     [Google Scholar]
  12. 12. 
    Bates GW, Rosenthal DM, Sun J, Chattopadhyay M, Peffer E et al. 2012. A comparative study of the Arabidopsis thaliana guard-cell transcriptome and its modulation by sucrose. PLOS ONE 7:11e49641
     [Google Scholar]
  13. 13. 
    Bauer H, Ache P, Wohlfart F, Al-Rasheid KA, Sonnewald S et al. 2013. How do stomata sense reductions in atmospheric relative humidity. Mol. Plant 6:51703–6
     [Google Scholar]
  14. 14. 
    Blatt MR. 1988. Potassium-dependent, bipolar gating of K+ channels in guard cells. J. Membr. Biol. 102:3235–46
     [Google Scholar]
  15. 15. 
    Blatt MR. 2000. Cellular signaling and volume control in stomatal movements in plants. Annu. Rev. Cell Dev. Biol. 16:221–41
     [Google Scholar]
  16. 16. 
    Blatt MR, Armstrong F. 1993. K+ channels of stomatal guard cells: abscisic-acid-evoked control of the outward rectifier mediated by cytoplasmic pH. Planta 191:3330–41
     [Google Scholar]
  17. 17. 
    Blatt MR, Garcia-Mata C, Sokolovski S 2007. Membrane transport and Ca2+ oscillations in guard cells. In Rhythms in Plants 1 S Mancuso, S Shabala 115–34 Berlin: Springer
     [Google Scholar]
  18. 18. 
    Blatt MR, Gradmann D. 1997. K+-sensitive gating of the K+ outward rectifier in Vicia guard cells. J. Membr. Biol. 158:3241–56
     [Google Scholar]
  19. 19. 
    Blatt MR, Wang Y, Leonhardt N, Hills A 2014. Exploring emergent properties in cellular homeostasis using OnGuard to model K+ and other ion transport in guard cells. J. Plant Physiol. 171:9770–78
     [Google Scholar]
  20. 20. 
    Boyer JS. 2015. Turgor and the transport of CO2 and water across the cuticle (epidermis) of leaves. J. Exp. Bot. 66:92625–33
     [Google Scholar]
  21. 21. 
    Brodribb TJ, Feild TS. 2010. Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecol. Lett. 13:2175–83
     [Google Scholar]
  22. 22. 
    Brodribb TJ, Feild TS, Jordan GJ 2007. Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890–98
     [Google Scholar]
  23. 23. 
    Brodribb TJ, Holbrook NM, Zwieniecki MA, Palma B 2005. Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. New Phytol 165:839–46
     [Google Scholar]
  24. 24. 
    Büchsenschütz K, Marten I, Becker D, Philippar K, Ache P, Hedrich R 2005. Differential expression of K+ channels between guard cells and subsidiary cells within the maize stomatal complex. Planta 222:6968–76
     [Google Scholar]
  25. 25. 
    Buckley TN, Mott KA. 2013. Modelling stomatal conductance in response to environmental factors. Plant Cell Environ 36:1691–99
     [Google Scholar]
  26. 26. 
    Busch FA. 2014. Opinion: the red-light response of stomatal movement is sensed by the redox state of the photosynthetic electron transport chain. Photosynth. Res. 119:1–2131–40
     [Google Scholar]
  27. 27. 
    Caine RS, Yin X, Sloan J, Harrison EL, Mohammed U et al. 2019. Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions. New Phytol 221:1371–84
     [Google Scholar]
  28. 28. 
    Caird MA, Richards JH, Donovan LA 2007. Nighttime stomatal conductance and transpiration in C3 and C4 plants. Plant Physiol 143:14–10
     [Google Scholar]
  29. 29. 
    Carins Murphy MR, Jordan GJ, Brodribb TJ 2014. Acclimation to humidity modifies the link between leaf size and the density of veins and stomata. Plant Cell Environ 37:1124–31
     [Google Scholar]
  30. 30. 
    Carmo-Silva E, Andralojc PJ, Scales JC, Driever SM, Mead A et al. 2017. Phenotyping of field-grown wheat in the UK highlights contribution of light response of photosynthesis and flag leaf longevity to grain yield. J. Exp. Bot. 68:133473–86
     [Google Scholar]
  31. 31. 
    Chapin FS, Matson PA, Mooney HA 2002. Carbon input to terrestrial ecosystems. Principles of Terrestrial Ecosystem Ecology97–122 New York: Springer
     [Google Scholar]
  32. 32. 
    Chen YH, Hu L, Punta M, Bruni R, Hillerich B et al. 2010. Homologue structure of the SLAC1 anion channel for closing stomata in leaves. Nature 467:73191074
     [Google Scholar]
  33. 33. 
    Chen ZH, Hills A, Bätz U, Amtmann A, Lew VL, Blatt MR 2012. Systems dynamic modeling of the stomatal guard cell predicts emergent behaviors in transport, signaling, and volume control. Plant Physiol 159:31235–51
     [Google Scholar]
  34. 34. 
    Cowan IR, Troughton JH. 1971. The relative role of stomata in transpiration and assimilation. Planta 97:4325–36
     [Google Scholar]
  35. 35. 
    Croxdale JL. 2000. Stomatal patterning in angiosperms. Am. J. Bot. 87:81069–80
     [Google Scholar]
  36. 36. 
    Dai N, Schaffer A, Petreikov M, Shahak Y, Giller Y et al. 1999. Overexpression of Arabidopsis hexokinase in tomato plants inhibits growth, reduces photosynthesis, and induces rapid senescence. Plant Cell 11:71253–66
     [Google Scholar]
  37. 37. 
    Daloso DM, Antunes WC, Pinheiro DP, Waquim JP, AraúJo WL et al. 2015. Tobacco guard cells fix CO2 by both Rubisco and PEPcase while sucrose acts as a substrate during light‐induced stomatal opening. Plant Cell Environ 38:112353–71
     [Google Scholar]
  38. 38. 
    Daloso DM, Dos Anjos L, Fernie AR 2016. Roles of sucrose in guard cell regulation. New Phytol 211:809–18
     [Google Scholar]
  39. 39. 
    Daloso DM, Medeiros DB, Dos Anjos L, Yoshida T, Araújo WL, Fernie AR 2017. Metabolism within the specialized guard cells of plants. New Phytol 216:41018–33
     [Google Scholar]
  40. 40. 
    de Boer HJ, Price CA, Wagner‐Cremer F, Dekker SC, Franks PJ, Veneklaas EJ 2016. Optimal allocation of leaf epidermal area for gas exchange. New Phytol 210:41219–28
     [Google Scholar]
  41. 41. 
    Doheny-Adams T, Hunt L, Franks PJ, Beerling DJ, Gray JE 2012. Genetic manipulation of stomatal density influences stomatal size, plant growth and tolerance to restricted water supply across a growth carbon dioxide gradient. Philos. Trans. R. Soc. B 367:1588547–55
     [Google Scholar]
  42. 42. 
    Doi M, Wada M, Shimazaki KI 2006. The fern Adiantum capillus-veneris lacks stomatal responses to blue light. Plant Cell Physiol 47:6748–55
     [Google Scholar]
  43. 43. 
    Dow GJ, Berry JA, Bergmann DC 2014. The physiological importance of developmental mechanisms that enforce proper stomatal spacing in Arabidopsis thaliana. New Phytol 201:41205–17
     [Google Scholar]
  44. 44. 
    Downton WJS, Loveys BR, Grant WJR 1988. Stomatal closure fully accounts for the inhibition of photosynthesis by abscisic acid. New Phytol 108:3263–66
     [Google Scholar]
  45. 45. 
    Drake PL, Froend RH, Franks PJ 2013. Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance. J. Exp. Bot. 64:495–505
     [Google Scholar]
  46. 46. 
    Dutton C, Hõrak H, Hepworth C, Mitchell A, Ton J et al. 2019. Bacterial infection systemically suppresses stomatal density. Plant Cell Environ 42:2411–21
     [Google Scholar]
  47. 47. 
    Edwards D, Axe L. 1992. Stomata and mechanics of stomatal functioning in some early land plants. Courier Forschungsinstitut Senckenberg 147:59–73
     [Google Scholar]
  48. 48. 
    Edwards D, Kerp H, Hass H 1998. Stomata in early land plants: an anatomical and ecophysiological approach. J. Exp. Bot. 49:255–78
     [Google Scholar]
  49. 49. 
    Eisenach C, Papanatsiou M, Hillert EK, Blatt MR 2014. Clustering of the K+ channel GORK of Arabidopsis parallels its gating by extracellular K+. Plant J 78:2203–14
     [Google Scholar]
  50. 50. 
    Elliott-Kingston C, Haworth M, Yearsley JM, Batke SP, Lawson T, McElwain JC 2016. Does size matter? Atmospheric CO2 may be a stronger driver of stomatal closing rate than stomatal size in taxa that diversified under low CO2. Front. Plant Sci. 7:1253
     [Google Scholar]
  51. 51. 
    Faralli M, Matthews J, Lawson T 2019. Exploiting natural variation and genetic manipulation of stomatal conductance for crop improvement. Curr. Opin. Plant Biol. 49:1–7
     [Google Scholar]
  52. 52. 
    Farquhar GD, Sharkey TD. 1982. Stomatal conductance and photosynthesis. Annu. Rev. Plant Physiol. 33:317–45
     [Google Scholar]
  53. 53. 
    Farquhar GD, von Caemmerer SV, Berry JA 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:178–90
     [Google Scholar]
  54. 54. 
    Farquhar GD, Wong SC. 1984. An empirical model of stomatal conductance. Funct. Plant Biol. 11:3191–210
     [Google Scholar]
  55. 55. 
    Fiorin L, Brodribb TJ, Anfodillo T 2016. Transport efficiency through uniformity: organization of veins and stomata in angiosperm leaves. New Phytol 209:1216–27
     [Google Scholar]
  56. 56. 
    Fischer RA, Rebetzke GJ. 2018. Indirect selection for potential yield in early-generation, spaced plantings of wheat and other small-grain cereals: a review. Crop Pasture Sci. 69:439–59
     [Google Scholar]
  57. 57. 
    Fischer RA, Rees D, Sayre KD, Lu Z-M, Condon AG, Saavedra AL 1998. Wheat yield progress associated with higher stomatal conductance and photosynthetic rate, and cooler canopies. Crop Sci. 38:61467–75
     [Google Scholar]
  58. 58. 
    Franks PJ, Beerling DJ. 2009. Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. PNAS 106:10343–47
     [Google Scholar]
  59. 59. 
    Franks PJ, Doheny‐Adams TW, Britton‐Harper ZJ, Gray JE 2015. Increasing water‐use efficiency directly through genetic manipulation of stomatal density. New Phytol 207:1188–95
     [Google Scholar]
  60. 60. 
    Franks PJ, Farquhar GD. 2007. The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiol 143:178–87
     [Google Scholar]
  61. 61. 
    Fujita T, Noguchi K, Terashima I 2013. Apoplastic mesophyll signals induce rapid stomatal responses to CO2 in Commelina communis. New Phytol 199:2395–406
     [Google Scholar]
  62. 62. 
    Gago J, de Menezes Daloso D, Figueroa CM, Flexas J, Fernie AR, Nikoloski Z 2016. Relationships of leaf net photosynthesis, stomatal conductance, and mesophyll conductance to primary metabolism: a multispecies meta-analysis approach. Plant Physiol 171:1265–79
     [Google Scholar]
  63. 63. 
    Gao XQ, Li CG, Wei PC, Zhang XY, Chen J, Wang XC 2005. The dynamic changes of tonoplasts in guard cells are important for stomatal movement in Vicia faba. Plant Physiol 139:31207–16
     [Google Scholar]
  64. 64. 
    Głowacka K, Kromdijk J, Kucera K, Xie J, Cavanagh AP et al. 2018. Photosystem II subunit S overexpression increases the efficiency of water use in a field-grown crop. Nat. Commun. 9:1868
     [Google Scholar]
  65. 65. 
    Grabov A, Blatt MR. 1998. Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells. PNAS 95:84778–83
     [Google Scholar]
  66. 66. 
    Granot D, Kelly G. 2019. Evolution of guard-cell theories: the story of sugars. Trends Plant Sci 24:507–18
     [Google Scholar]
  67. 67. 
    Hanson DT, Stutz SS, Boyer JS 2016. Why small fluxes matter: the case and approaches for improving measurements of photosynthesis and (photo) respiration. J. Exp. Bot. 67:103027–39
     [Google Scholar]
  68. 68. 
    Hedrich R, Marten I. 1993. Malate‐induced feedback regulation of plasma membrane anion channels could provide a CO2 sensor to guard cells. EMBO J 12:3897–901
     [Google Scholar]
  69. 69. 
    Hedrich R, Marten I, Lohse G, Dietrich P, Winter H et al. 1994. Malate‐sensitive anion channels enable guard cells to sense changes in the ambient CO2 concentration. Plant J 6:5741–48
     [Google Scholar]
  70. 70. 
    Hei S, Liu Z, Huang A, She X 2018. The regulator of G-protein signalling protein mediates D-glucose-induced stomatal closure via triggering hydrogen peroxide and nitric oxide production in Arabidopsis. Funct. Plant Biol 45:5509–18
     [Google Scholar]
  71. 71. 
    Hepworth C, Doheny‐Adams T, Hunt L, Cameron DD, Gray JE 2015. Manipulating stomatal density enhances drought tolerance without deleterious effect on nutrient uptake. New Phytol 208:2336–41
     [Google Scholar]
  72. 72. 
    Hetherington AM, Brownlee C. 2004. The generation of Ca2+ signals in plants. Annu. Rev. Plant Biol. 55:401–27
     [Google Scholar]
  73. 73. 
    Hetherington AM, Woodward FI. 2003. The role of stomata in sensing and driving environmental change. Nature 424:901–8
     [Google Scholar]
  74. 74. 
    Hills A, Chen ZH, Amtmann A, Blatt MR, Lew VL 2012. OnGuard, a computational platform for quantitative kinetic modeling of guard cell physiology. Plant Physiol 159:1026–42
     [Google Scholar]
  75. 75. 
    Horrer D, Flütsch S, Pazmino D, Matthews JS, Thalmann M et al. 2016. Blue light induces a distinct starch degradation pathway in guard cells for stomatal opening. Curr. Biol. 26:3362–70
     [Google Scholar]
  76. 76. 
    Hosy E, Vavasseur A, Mouline K, Dreyer I, Gaymard F et al. 2003. The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration. PNAS 100:95549–54
     [Google Scholar]
  77. 77. 
    Hughes J, Hepworth C, Dutton C, Dunn JA, Hunt L et al. 2017. Reducing stomatal density in barley improves drought tolerance without impacting on yield. Plant Physiol 174:2776–87
     [Google Scholar]
  78. 78. 
    Imamura S. 1943. Untersuchungen über den Mechanismus der Turgorschwankung der Spalttöffnungsschliesszellen. Jpn. J. Bot. 12:251–346
     [Google Scholar]
  79. 79. 
    Inoue SI, Kinoshita T. 2017. Blue light regulation of stomatal opening and the plasma membrane H+-ATPase. Plant Physiol 174:531–38
     [Google Scholar]
  80. 80. 
    Jang JC, León P, Zhou L, Sheen J 1997. Hexokinase as a sugar sensor in higher plants. Plant Cell 9:15–19
     [Google Scholar]
  81. 81. 
    Jezek M, Blatt MR. 2017. The membrane transport system of the guard cell and its integration for stomatal dynamics. Plant Physiol 174:2487–519
     [Google Scholar]
  82. 82. 
    Jezek M, Hills A, Blatt MR, Lew VL 2019. A constraint–relaxation–recovery mechanism for stomatal dynamics. Plant Cell Environ 42:2399–410
     [Google Scholar]
  83. 83. 
    Johansson I, Wulfetange K, Porée F, Michard E, Gajdanowicz P et al. 2006. External K+ modulates the activity of the Arabidopsis potassium channel SKOR via an unusual mechanism. Plant J 46:2269–81
     [Google Scholar]
  84. 84. 
    Jones HG. 1998. Stomatal control of photosynthesis and transpiration. J. Exp. Bot. 49:387–98
     [Google Scholar]
  85. 85. 
    Kang Y, Outlaw WH Jr., Andersen PC, Fiore GB 2007. Guard-cell apoplastic sucrose concentration: a link between leaf photosynthesis and stomatal aperture size in the apoplastic phloem loader Vicia faba L. Plant Cell Environ 30:551–58
     [Google Scholar]
  86. 86. 
    Keenan TF, Hollinger DY, Bohrer G, Dragoni D, Munger JW et al. 2013. Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise. Nature 499:324–27
     [Google Scholar]
  87. 87. 
    Kelly G, David-Schwartz R, Sade N, Moshelion M, Levi A et al. 2012. The pitfalls of transgenic selection and new roles of AtHXK1: a high level of AtHXK1 expression uncouples hexokinase1-dependent sugar signaling from exogenous sugar. Plant Physiol 159:147–51
     [Google Scholar]
  88. 88. 
    Kelly G, Lugassi N, Belausov E, Wolf D, Khamaisi B et al. 2017. The Solanum tuberosum KST1 partial promoter as a tool for guard cell expression in multiple plant species. J. Exp. Bot. 68:112885–97
     [Google Scholar]
  89. 89. 
    Kelly G, Moshelion M, David-Schwartz R, Halperin O, Wallach R et al. 2013. Hexokinase mediates stomatal closure. Plant J 75:977–88
     [Google Scholar]
  90. 90. 
    Kinoshita T, Shimazaki K. 2001. Analysis of the phosphorylation level in guard-cell plasma membrane H+-ATPase in response to fusicoccin. Plant Cell Physiol 42:424–32
     [Google Scholar]
  91. 91. 
    Kirschbaum MU, Pearcy RW. 1988. Gas exchange analysis of the relative importance of stomatal and biochemical factors in photosynthetic induction in Alocasia macrorrhiza. Plant Physiol 86:782–85
     [Google Scholar]
  92. 92. 
    Lasceve G, Leymarie J, Vavasseur A 1997. Alterations in light‐induced stomatal opening in a starch‐deficient mutant of Arabidopsis thaliana L. deficient in chloroplast phosphoglucomutase activity. Plant Cell Environ 20:3350–58
     [Google Scholar]
  93. 93. 
    Lawson T. 2009. Guard cell photosynthesis and stomatal function. New Phytol 181:13–34
     [Google Scholar]
  94. 94. 
    Lawson T, Blatt MR. 2014. Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol 164:1556–70
     [Google Scholar]
  95. 95. 
    Lawson T, Craigon J, Black CR, Colls JJ, Tulloch AM, Landon G 2001. Effects of elevated carbon dioxide and ozone on the growth and yield of potatoes (Solanum tuberosum) grown in open-top chambers. Environ. Pollut. 111:3479–91
     [Google Scholar]
  96. 96. 
    Lawson T, James W, Weyers1 J 1998. A surrogate measure of stomatal aperture. J. Exp. Bot. 49:1397–403
     [Google Scholar]
  97. 97. 
    Lawson T, Lefebvre S, Baker NR, Morison JIL, Raines CA 2008. Reductions in mesophyll and guard cell photosynthesis impact on the control of stomatal responses to light and CO2. J. Exp. Bot. 59:3609–19
     [Google Scholar]
  98. 98. 
    Lawson T, Morison JIL. 2004. Stomatal function and physiology. Evolution of Plant Physiology AR Hemsley, I Poole 217–42 San Diego, CA: Elsevier
     [Google Scholar]
  99. 99. 
    Lawson T, Oxborough K, Morison JI, Baker NR 2002. Responses of photosynthetic electron transport in stomatal guard cells and mesophyll cells in intact leaves to light, CO2, and humidity. Plant Physiol 128:152–62
     [Google Scholar]
  100. 100. 
    Lawson T, Oxborough K, Morison JI, Baker NR 2003. The responses of guard and mesophyll cell photosynthesis to CO2, O2, light, and water stress in a range of species are similar. J. Exp. Bot. 54:3881743–52
     [Google Scholar]
  101. 101. 
    Lawson T, Simkin AJ, Kelly G, Granot D 2014. Mesophyll photosynthesis and guard cell metabolism impacts on stomatal behaviour. New Phytol 203:1064–81
     [Google Scholar]
  102. 102. 
    Lawson T, Terashima I, Fujita T, Wang Y 2018. Coordination between photosynthesis and stomatal behavior. The Leaf: A Platform for Performing Photosynthesis WW Adams III, I Terashima 141–61 Cham, Switz.: Springer
     [Google Scholar]
  103. 103. 
    Lawson T, Vialet‐Chabrand S. 2019. Speedy stomata, photosynthesis and plant water use efficiency. New Phytol 221:193–98
     [Google Scholar]
  104. 104. 
    Lawson T, von Caemmerer S, Baroli I 2011. Photosynthesis and stomatal behaviour. In Progress in Botany 72 UE Lüttge, W Beyschlag, B Büdel, D Francis 265–304 Berlin: Springer
     [Google Scholar]
  105. 105. 
    Lawson T, Weyers J. 1999. Spatial and temporal variation in gas exchange over the lower surface of Phaseolus vulgaris L. primary leaves. J. Exp. Bot. 50:3371381–91
     [Google Scholar]
  106. 106. 
    Lawson T, Weyers J, A'Brook R 1998. The nature of heterogeneity in the stomatal behaviour of Phaseolus vulgaris L. primary leaves. J. Exp. Bot. 49:3251387–95
     [Google Scholar]
  107. 107. 
    Leakey AD, Ferguson JN, Pignon CP, Wu A, Jin Z et al. 2019. Water use efficiency as a constraint and target for improving the resilience and productivity of C3 and C4 crops. Annu. Rev. Plant Biol. 70:781–808
     [Google Scholar]
  108. 108. 
    Lee J, Bowling DJF. 1992. Effect of the mesophyll on stomatal opening in Commelina communis. J. Exp. Bot 43:7951–57
     [Google Scholar]
  109. 109. 
    Lee JS, Bowling DJF. 1995. Influence of the mesophyll on stomatal opening. Funct. Plant Biol. 22:3357–63
     [Google Scholar]
  110. 110. 
    Lee M, Choi Y, Burla B, Kim YY, Jeon B et al. 2008. The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2. Nat. Cell Biol. 10:101217
     [Google Scholar]
  111. 111. 
    Lehmann P, Or D. 2015. Effects of stomata clustering on leaf gas exchange. New Phytol 207:41015–25
     [Google Scholar]
  112. 112. 
    Lehmeier C, Pajor R, Lundgren MR, Mathers A, Sloan J et al. 2017. Cell density and airspace patterning in the leaf can be manipulated to increase leaf photosynthetic capacity. Plant J 92:6981–94
     [Google Scholar]
  113. 113. 
    Li Y, Xu S, Gao J, Pan S, Wang G 2016. Glucose- and mannose‐induced stomatal closure is mediated by ROS production, Ca2+ and water channel in Vicia faba. Physiol. Plant 156:3252–61
     [Google Scholar]
  114. 114. 
    Lima VF, dos Anjos L, Medeiros DB, Cândido‐Sobrinho SA, Souza LP et al. 2019. The sucrose‐to‐malate ratio correlates with the faster CO2 and light stomatal responses of angiosperms compared to ferns. New Phytol 223:1873–87
     [Google Scholar]
  115. 115. 
    Lima VF, Medeiros DB, Dos Anjos L, Gago J, Fernie AR, Daloso DM 2018. Toward multifaceted roles of sucrose in the regulation of stomatal movement. Plant Signal. Behav. 13:8e1494468
     [Google Scholar]
  116. 116. 
    Lloyd FE. 1908. The physiology of stomata Publ. 82 Carnegie Inst. Wash Washington, DC:
  117. 117. 
    Lu P, Outlaw WH Jr., Smith BG, Freed GA 1997. 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. Plant Physiol 114:109–18
     [Google Scholar]
  118. 118. 
    Lu P, Zhang SQ, Outlaw WH, Riddle KA 1995. Sucrose: a solute that accumulates in the guard-cell apoplast and guard-cell symplast of open stomata. FEBS Lett 362:180–84
     [Google Scholar]
  119. 119. 
    Lugassi N, Kelly G, Fidel L, Yaniv Y, Attia Z et al. 2015. Expression of Arabidopsis hexokinase in citrus guard cells controls stomatal aperture and reduces transpiration. Front. Plant. Sci. 6:1114
     [Google Scholar]
  120. 120. 
    Lundgren MR, Mathers A, Baillie AL, Dunn J, Wilson MJ et al. 2019. Mesophyll porosity is modulated by the presence of functional stomata. Nat. Commun. 10:12825
     [Google Scholar]
  121. 121. 
    MacRobbie EA. 2006. Control of volume and turgor in stomatal guard cells. J. Membr. Biol. 210:2131–42
     [Google Scholar]
  122. 122. 
    MacRobbie EAC, Lettau J. 1980. Ion content and aperture in “isolated” guard cells of Commelina communis L. J. Membr. Biol. 53:3199–205
     [Google Scholar]
  123. 123. 
    Majore I, Wilhelm B, Marten I 2002. Identification of K+ channels in the plasma membrane of maize subsidiary cells. Plant Cell Physiol 43:844–52
     [Google Scholar]
  124. 124. 
    Mansfield TA, Hetherington AM, Atkinson CJ 1990. Some current aspects of stomatal physiology. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 41:55–75
     [Google Scholar]
  125. 125. 
    Matthews JSA, Vialet-Chabrand S, Lawson T 2017. Diurnal variation in gas exchange: The balance between carbon fixation and water loss. Plant Physiol 174:614–23
     [Google Scholar]
  126. 126. 
    Matthews JSA, Vialet-Chabrand SR, Lawson T 2018. Acclimation to fluctuating light impacts the rapidity of response and diurnal rhythm of stomatal conductance. Plant Physiol 176:31939–51
     [Google Scholar]
  127. 127. 
    McAinsh MR, Pittman JK. 2009. Shaping the calcium signature. New Phytol 181:275–94
     [Google Scholar]
  128. 128. 
    McAusland L, Vialet-Chabrand S, Davey P, Baker NR, Brendel O, Lawson T 2016. Effects of kinetics of light-induced stomatal responses on photosynthesis and water-use efficiency. New Phytol 211:1209–20
     [Google Scholar]
  129. 129. 
    McDonald EP, Erickson JE, Kruger EL 2002. Can decreased transpiration limit plant nitrogen acquisition in elevated CO2. Funct. Plant Biol. 29:1115–20
     [Google Scholar]
  130. 130. 
    McElwain JC, Chaloner WG. 1995. Stomatal density and index of fossil plants track atmospheric carbon dioxide in the Palaeozoic. Ann. Bot. 76:4389–95
     [Google Scholar]
  131. 131. 
    McElwain JC, Yiotis C, Lawson T 2016. Using modern plant trait relationships between observed and theoretical maximum stomatal conductance and vein density to examine patterns of plant macroevolution. New Phytol 209:194–103
     [Google Scholar]
  132. 132. 
    McGrath JM, Lobell DB. 2013. Reduction of transpiration and altered nutrient allocation contribute to nutrient decline of crops grown in elevated CO2 concentrations. Plant Cell Environ 36:3697–705
     [Google Scholar]
  133. 133. 
    Medeiros DB, Perez Souza L, Antunes WC, Araújo WL, Daloso DM, Fernie AR 2018. Sucrose breakdown within guard cells provides substrates for glycolysis and glutamine biosynthesis during light‐induced stomatal opening. Plant J 94:4583–94
     [Google Scholar]
  134. 134. 
    Meidner H. 1986. Cuticular conductance and the humidity response of stomata. J. Exp. Bot. 37:4517–25
     [Google Scholar]
  135. 135. 
    Meinhard M, Schnabl H. 2001. Fusicoccin- and light-induced activation and in vivo phosphorylation of phosphoenolpyruvate carboxylase in Vicia guard cell protoplasts. Plant Sci 160:4635–46
     [Google Scholar]
  136. 136. 
    Melis A, Zeiger E. 1982. Chlorophyll a fluorescence transients in mesophyll and guard cells: modulation of guard cell photophosphorylation by CO2. Plant Physiol 69:3642–47
     [Google Scholar]
  137. 137. 
    Melotto M, Underwood W, He SY 2008. Role of stomata in plant innate immunity and foliar bacterial diseases. Annu. Rev. Phytopathol. 46:101–22
     [Google Scholar]
  138. 138. 
    Messinger SM, Buckley TN, Mott KA 2006. Evidence for involvement of photosynthetic processes in the stomatal response to CO2. Plant. Physiol. 140:771–78
     [Google Scholar]
  139. 139. 
    Metcalfe CR, Chalk L. 1950. Anatomy of the Dicotyledons I Oxford, UK: Clarendon
  140. 140. 
    Morison JIL. 2003. Plant water use: stomatal control. Encyclopedia of Water Science BA Stewart, TA Howell 680–85 New York: Marcel Dekker
     [Google Scholar]
  141. 141. 
    Morison JIL, Gallouët E, Lawson T, Cornic G, Herbin R, Baker NR 2005. Lateral diffusion of CO2 in leaves is not sufficient to support photosynthesis. Plant Physiol 139:1254–66
     [Google Scholar]
  142. 142. 
    Mott KA, Cardon ZG, Berry JA 1993. Asymmetric patchy stomatal closure for the two surfaces of Xanthium strumarium L. leaves at low humidity. Plant Cell Environ 16:125–34
     [Google Scholar]
  143. 143. 
    Mott KA, Peak D. 2013. Testing a vapour‐phase model of stomatal responses to humidity. Plant Cell Environ 36:5936–44
     [Google Scholar]
  144. 144. 
    Mott KA, Sibbernsen ED, Shope JC 2008. The role of the mesophyll in stomatal responses to light and CO2. Plant Cell Environ 31:91299–306
     [Google Scholar]
  145. 145. 
    Nadeau JA, Sack FD. 2002. Control of stomatal distribution on the Arabidopsis leaf surface. Science 296:55731697–700
     [Google Scholar]
  146. 146. 
    Olsen JE, Junttila O. 2002. Far red end‐of‐day treatment restores wild type‐like plant length in hybrid aspen overexpressing phytochrome A. Physiol. Plant. 115:3448–57
     [Google Scholar]
  147. 147. 
    Outlaw WH Jr 1983. Current concepts on the role of potassium in stomatal movements. Physiol. Plant. 59:2302–11
     [Google Scholar]
  148. 148. 
    Outlaw WH Jr 1989. Critical examination of the quantitative evidence for and against photosynthetic CO2 fixation by guard cells. Physiol. Plant. 77:2275–81
     [Google Scholar]
  149. 149. 
    Outlaw WH. 2003. Integration of cellular and physiological functions of guard cells. CRC Crit. Rev. Plant Sci. 22:503–29
     [Google Scholar]
  150. 150. 
    Outlaw WH, De Vlieghere-He X 2001. Transpiration rate: an important factor controlling the sucrose content of the guard cell apoplast of broad bean. Plant Physiol 126:41716–24
     [Google Scholar]
  151. 151. 
    Outlaw WH, Manchester J. 1979. Guard cell starch concentration quantitatively related to stomatal aperture. Plant Physiol 64:179–82
     [Google Scholar]
  152. 152. 
    Pallaghy CK. 1971. Stomatal movement and potassium transport in epidermal strips of Zea mays: the effect of CO2. Planta 101:4287–95
     [Google Scholar]
  153. 153. 
    Pandey R, Chacko PM, Choudhary ML, Prasad KV, Pal M 2007. Higher than optimum temperature under CO2 enrichment influences stomata anatomical characters in rose (Rosa hybrida). Sci. Hort. 113:174–81
     [Google Scholar]
  154. 154. 
    Papanatsiou M, Amtmann A, Blatt MR 2016. Stomatal spacing safeguards stomatal dynamics by facilitating guard cell ion transport independent of the epidermal solute reservoir. Plant Physiol 172:1254–63
     [Google Scholar]
  155. 155. 
    Papanatsiou M, Petersen J, Henderson L, Wang Y, Christie JM, Blatt MR 2019. Optogenetic manipulation of stomatal kinetics improves carbon assimilation, water use, and growth. Science 363:64341456–59
     [Google Scholar]
  156. 156. 
    Parlange JY, Waggoner PE. 1970. Stomatal dimensions and resistance to diffusion. Plant Physiol 46:2337–42
     [Google Scholar]
  157. 157. 
    Penny MG, Bowling DJF. 1974. A study of potassium gradients in the epidermis of intact leaves of Commelina communis L. in relation to stomatal opening. Planta 119:117–25
     [Google Scholar]
  158. 158. 
    Poffenroth M, Green DB, Tallman G 1992. Sugar concentrations in guard cells of Vicia faba illuminated with red or blue light: analysis by high performance liquid chromatography. Plant Physiol 98:41460–71
     [Google Scholar]
  159. 159. 
    Poole I, Weyers JDB, Lawson T, Raven JA 1996. Variations in stomatal density and index: implications for palaeoclimatic reconstructions. Plant Cell Environ 19:6705–12
     [Google Scholar]
  160. 160. 
    Prasch CM, Ott KV, Bauer H, Ache P, Hedrich R, Sonnewald U 2015. β-amylase1 mutant Arabidopsis plants show improved drought tolerance due to reduced starch breakdown in guard cells. J. Exp. Bot. 66:196059–67
     [Google Scholar]
  161. 161. 
    Raissig MT, Matos JL, Gil MXA, Kornfeld A, Bettadapur A et al. 2017. Mobile MUTE specifies subsidiary cells to build physiologically improved grass stomata. Science 355:63301215–18
     [Google Scholar]
  162. 162. 
    Raschke K. 1975. Stomatal action. Annu. Rev. Plant Physiol. 26:309–40
     [Google Scholar]
  163. 163. 
    Raschke K, Dittrich P. 1977. [14 C] Carbon-dioxide fixation by isolated leaf epidermes with stomata closed or open. Planta 134:169–75
     [Google Scholar]
  164. 164. 
    Raschke K, Fellows MP. 1971. Stomatal movement in Zea mays: shuttle of potassium and chloride between guard cells and subsidiary cells. Planta 101:4296–316
     [Google Scholar]
  165. 165. 
    Raven JA. 2014. Speedy small stomata. J. Exp. Bot. 65:1415–24
     [Google Scholar]
  166. 166. 
    Reckmann U, Scheibe R, Raschke K 1990. Rubisco activity in guard cells compared with the solute requirement for stomatal opening. Plant Physiol 92:1246–53
     [Google Scholar]
  167. 167. 
    Resco de Dios V, Loik ME, Smith R, Aspinwall MJ, Tissue DT 2016. Genetic variation in circadian regulation of nocturnal stomatal conductance enhances carbon assimilation and growth. Plant Cell Environ 39:13–11
     [Google Scholar]
  168. 168. 
    Robaina-Estévez S, Daloso DM, Zhang Y, Fernie AR, Nikoloski Z 2017. Resolving the central metabolism of Arabidopsis guard cells. Sci. Rep. 7:18307
     [Google Scholar]
  169. 169. 
    Roelfsema MRG, Hedrich R. 2005. In the light of stomatal opening: new insights into ‘the Watergate. .’ New Phytol 167:665–91
     [Google Scholar]
  170. 170. 
    Santelia D, Lawson T. 2016. Rethinking guard cell metabolism. Plant Physiol 172:1371–92
     [Google Scholar]
  171. 171. 
    Santelia D, Lunn JE. 2017. Transitory starch metabolism in guard cells: unique features for a unique function. Plant Physiol 174:539–49
     [Google Scholar]
  172. 172. 
    Schnabl H. 1980. CO2 and malate metabolism in starch-containing and starch-lacking guard-cell protoplasts. Planta 149:152–58
     [Google Scholar]
  173. 173. 
    Schnabl H, Raschke K. 1980. Potassium chloride as stomatal osmoticum in Allium cepa L., a species devoid of starch in guard cells. Plant Physiol 65:188–93
     [Google Scholar]
  174. 174. 
    Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D 2001. Guard cell signal transduction. Annu. Rev. Plant Biol. 52:1627–58
     [Google Scholar]
  175. 175. 
    Serna L, Fenoll C. 1997. Tracing the ontogeny of stomatal clusters in Arabidopsis with molecular markers. Plant J 12:4747–55
     [Google Scholar]
  176. 176. 
    Serna L, Fenoll C. 2000. Stomatal development in Arabidopsis: how to make a functional pattern. Trends Plant Sci 5:11458–60
     [Google Scholar]
  177. 177. 
    Sharkey TD, Raschke K. 1981. Separation and measurement of direct and indirect effects of light on stomata. Plant Physiol 68:33–40
     [Google Scholar]
  178. 178. 
    Shimazaki KI, Doi M, Assmann SM, Kinoshita T 2007. Light regulation of stomatal movement. Annu. Rev. Plant Biol. 58:219–47
     [Google Scholar]
  179. 179. 
    Sibbernsen E, Mott KA. 2010. Stomatal responses to flooding of the intercellular air spaces suggest a vapor-phase signal between the mesophyll and the guard cells. Plant Physiol 153:31435–42
     [Google Scholar]
  180. 180. 
    Smith S, Weyers JDB, Berry WG 1989. Variation in stomatal characteristics over the lower surface of Commelina communis leaves. Plant Cell Environ 12:6653–59
     [Google Scholar]
  181. 181. 
    Squire GR, Mansfield TA. 1972. A simple method of isolating stomata on detached epidermis by low pH treatment: observations of the importance of the subsidiary cells. New Phytol 71:61033–43
     [Google Scholar]
  182. 182. 
    Stadler R, Büttner M, Ache P, Hedrich R, Ivashikina N et al. 2003. Diurnal and light-regulated expression of AtSTP1 in guard cells of Arabidopsis. Plant Physiol 133:2528–37
     [Google Scholar]
  183. 183. 
    Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A et al. 2010. Stomagen positively regulates stomatal density in Arabidopsis. Nature 463:241–44
     [Google Scholar]
  184. 184. 
    Suhita D, Raghavendra AS, Kwak JM, Vavasseur A 2004. Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure. Plant Physiol 134:41536–45
     [Google Scholar]
  185. 185. 
    Takemiya A, Sugiyama N, Fujimoto H, Tsutsumi T, Yamauchi S et al. 2013. Phosphorylation of BLUS1 kinase by phototropins is a primary step in stomatal opening. Nat. Commun. 4:2094
     [Google Scholar]
  186. 186. 
    Talbott LD, Zeiger E. 1993. Sugar and organic acid accumulation in guard cells of Vicia faba in response to red and blue light. Plant Physiol 102:41163–69
     [Google Scholar]
  187. 187. 
    Talbott LD, Zeiger E. 1996. Central roles for potassium and sucrose in guard-cell osmoregulation. Plant Physiol 111:41051–57
     [Google Scholar]
  188. 188. 
    Talbott LD, Zeiger E. 1998. The role of sucrose in guard cell osmoregulation. J. Exp. Bot. 49:329–37
     [Google Scholar]
  189. 189. 
    Tallman G, Zeiger E. 1988. Light quality and osmoregulation in Vicia guard cells: evidence for involvement of three metabolic pathways. Plant Physiol 88:3887–95
     [Google Scholar]
  190. 190. 
    Tanaka Y, Sugano SS, Shimada T, Hara‐Nishimura I 2013. Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis. New Phytol 198:3757–64
     [Google Scholar]
  191. 191. 
    Tarczynski MC, Outlaw WH, Arold N, Neuhoff V, Hampp R 1989. Electrophoretic assay for ribulose 1,5-bisphosphate carboxylase/oxygenase in guard cells and other leaf cells of Vicia faba L. Plant Physiol 89:41088–93
     [Google Scholar]
  192. 192. 
    Tinoco-Ojanguren C, Pearcy RW. 1993. Stomatal dynamics and its importance to carbon gain in two rainforest Piper species. II. Stomatal versus biochemical limitations during photosynthetic induction. Oecologia 94:395–402
     [Google Scholar]
  193. 193. 
    Tominaga M, Kinoshita T, Shimazaki KI 2001. Guard-cell chloroplasts provide ATP required for H+ pumping in the plasma membrane and stomatal opening. Plant Cell Physiol 42:8795–802
     [Google Scholar]
  194. 194. 
    Urban J, Ingwers MW, McGuire MA, Teskey RO 2017. Increase in leaf temperature opens stomata and decouples net photosynthesis from stomatal conductance in Pinus taeda and Populus deltoides x nigra. J. Exp. Bot 68:71757–67
     [Google Scholar]
  195. 195. 
    Valerio C, Costa A, Marri L, Issakidis-Bourguet E, Pupillo P et al. 2010. Thioredoxin-regulated β-amylase (BAM1) triggers diurnal starch degradation in guard cells, and in mesophyll cells under osmotic stress. J. Exp. Bot. 62:2545–55
     [Google Scholar]
  196. 196. 
    van Cotthem WRF. 1970. A classification of stomatal types. Bot. J. Linn. Soc. 63:3235–46
     [Google Scholar]
  197. 197. 
    Vavasseur A, Raghavendra AS. 2005. Guard cell metabolism and CO2 sensing. New Phytol 165:3665–82
     [Google Scholar]
  198. 198. 
    Vialet‐Chabrand, Dreyer SE, Brendel O 2013. Performance of a new dynamic model for predicting diurnal time courses of stomatal conductance at the leaf level. Plant Cell Environ 36:81529–46
     [Google Scholar]
  199. 199. 
    Vialet-Chabrand S, Hills A, Wang Y, Griffiths H, Lew VL et al. 2017. Global sensitivity analysis of OnGuard models identifies key hubs for transport interaction in stomatal dynamics. Plant Physiol 174:2680–88
     [Google Scholar]
  200. 200. 
    Vialet-Chabrand S, Matthews JSA, Simkin AJ, Raines CA, Lawson T 2017. Importance of fluctuations in light on the acclimation of Arabidopsis thaliana. Plant Physiol 173:2163–79
     [Google Scholar]
  201. 201. 
    Vialet-Chabrand SRM, Matthews JSA, McAusland L, Blatt MR, Griffiths H, Lawson T 2017. Temporal dynamics of stomatal behavior: modeling and implications for photosynthesis and water use. Plant Physiol 174:603–13
     [Google Scholar]
  202. 202. 
    Vico G, Manzoni S, Palmroth S, Katul G 2011. Effects of stomatal delays on the economics of leaf gas exchange under intermittent light regimes. New Phytol 192:3640–52
     [Google Scholar]
  203. 203. 
    Von Caemmerer S, Lawson T, Oxborough K, Baker NR, Andrews TJ, Raines CA 2004. Stomatal conductance does not correlate with photosynthetic capacity in transgenic tobacco with reduced amounts of Rubisco. J. Exp. Bot. 55:1157–66
     [Google Scholar]
  204. 204. 
    Wang H, Yan S, Xin H, Huang W, Zhang H et al. 2019. A subsidiary cell-localized glucose transporter promotes stomatal conductance and photosynthesis. Plant Cell 31:61328–43
     [Google Scholar]
  205. 205. 
    Wang P, Song CP. 2008. Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytol 178:703–18
     [Google Scholar]
  206. 206. 
    Wang Y, Blatt MR. 2011. Anion channel sensitivity to cytosolic organic acids implicates a central role for oxaloacetate in integrating ion flux with metabolism in stomatal guard cells. Biochem. J. 439:1161–70
     [Google Scholar]
  207. 207. 
    Wang Y, Hills A, Blatt MR 2014. Systems analysis of guard cell membrane transport for enhanced stomatal dynamics and water use efficiency. Plant Physiol 164:1593–99
     [Google Scholar]
  208. 208. 
    Wang Y, Hills A, Vialet-Chabrand S, Papanatsiou M, Griffiths H et al. 2017. Unexpected connections between humidity and ion transport discovered using a model to bridge guard cell-to-leaf scales. Plant Cell 29:112921–39
     [Google Scholar]
  209. 209. 
    Wang Y, Papanatsiou M, Eisenach C, Karnik R, Williams M et al. 2012. Systems dynamic modeling of a guard cell Cl− channel mutant uncovers an emergent homeostatic network regulating stomatal transpiration. Plant Physiol 160:41956–67
     [Google Scholar]
  210. 210. 
    Weyers JD, Lawson T. 1997. Heterogeneity in stomatal characteristics. Adv. Bot. Res. 26:317–352
     [Google Scholar]
  211. 211. 
    Wille AC, Lucas WJ. 1984. Ultrastructural and histochemical studies on guard cells. Planta 160:2129–42
     [Google Scholar]
  212. 212. 
    Willmer C, Fricker M. 1996. Stomata London: Springer
  213. 213. 
    Willmer CM, Pallas JE Jr 1973. A survey of stomatal movements and associated potassium fluxes in the plant kingdom. Can. J. Bot. 51:137–42
     [Google Scholar]
  214. 214. 
    Wong SC, Cowan IR, Farquhar GD 1979. Stomatal conductance correlates with photosynthetic capacity. Nature 282:424–26
     [Google Scholar]
  215. 215. 
    Woodward FI, Lake JA, Quick WP 2002. Stomatal development and CO2: ecological consequences. New Phytol 153:3477–84
     [Google Scholar]
  216. 216. 
    Yao Y, Liu X, Li Z, Ma X, Rennenberg H et al. 2013. Drought-induced H2O2 accumulation in subsidiary cells is involved in regulatory signaling of stomatal closure in maize leaves. Planta 238:1217–27
     [Google Scholar]
  217. 217. 
    Zeiger E. 1983. The biology of stomatal guard cells. Annu. Rev. Plant Physiol. 34:441–75
     [Google Scholar]
  218. 218. 
    Zeiger E, Talbott LD, Frechilla S, Srivastava A, Zhu J 2002. The guard cell chloroplast: a perspective for the twenty‐first century. New Phytol 153:3415–24
     [Google Scholar]
  219. 219. 
    Zeiger E, Zhu J. 1998. Role of zeaxanthin in blue light photoreception and the modulation of light-CO2 interactions in guard cells. J. Exp. Bot. 49:433–42
     [Google Scholar]
  220. 220. 
    Zwieniecki MA, Melcher PJ, Boyce CK, Sack L, Holbrook NM 2002. Hydraulic architecture of leaf venation in Laurus nobilis L. Plant Cell Environ 25:111445–50
     [Google Scholar]
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Guard Cell Metabolism and Stomatal Function
Annual Review of Plant Biology 71, 273 (2020); https://doi.org/10.1146/annurev-arplant-050718-100251
/content/journals/10.1146/annurev-arplant-050718-100251
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