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Coordination Between Photosynthesis and Stomatal Behavior

  • Tracy LawsonEmail author
  • Ichiro Terashima
  • Takashi Fujita
  • Yin Wang
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 44)

Summary

Stomata open and close in response to internal and external signals to balance CO2 uptake for photosynthesis and water loss through transpiration. For a plant to function efficiently, this balance is essential to ensure adequate CO2 uptake for mesophyll demands and sufficient water loss to maintain transpiration and optimal leaf temperature from evaporative cooling for maximal photosynthetic performance, while also ensuring an appropriate whole plant water status. Both stomata and mesophyll respond to external and internal cues and there is a close synchrony between stomata movements and mesophyll photosynthesis. However, the mechanism(s) that co-ordinate these two responses are unknown. Here we examine evidence for a mesophyll driven signal and discuss possible candidates for such a signal. We also provide a brief review of some of the experimental approaches adopted for exploring mesophyll-stomatal interactions. We discuss a possible role for guard cell chloroplasts and guard cell photosynthesis as a mechanism for this co-ordination. Finally, we show that stomatal responses are different on adaxial and abaxial leaf surfaces, raising further questions regarding mesophyll driven signals co-ordinating behavior. We conclude that despite numerous studies, the mesophyll signal remains to be elucidated, and that further research is needed to determine the mechanisms and signal transduction pathways that facilitate the well observed correlation between mesophyll photosynthetic rates and stomatal conductance.

Abbreviations

A

rate of photosynthetic CO2 uptake

ABA

abscisic acid

ATP

adenosine triphosphate

Ca

concentration of CO2 in the atmosphere surrounding a leaf

Ci

concentration of CO2 internal to the leaf tissue

DCMU

3,4-dichlorophenyl-1,1 –dimethylurea

Dw

diffusivity of water vapor in air at 25 °C

GCAC1

an anion-release channel in the plasma membrane of guard cells

\( {g}_{\mathrm{max}} \)

maximum stomatal conductance

gs

stomatal conductance

HXK

hexokinase

H+-ATPase

proton transporter that spans the cell membrane

min

minutes

NADPH

nicotinamide adenine dinucleotide phosphate

pamax

maximum stomatal pore area

pd.

stomatal pore depth

PHOT

phototropin

SD

stomatal density

SLAC1

a guard cell S-type anion channel

TCA

tricarboxylic acid

v

molar volume of air

VPD

vapor pressure deficit between the inside of the leaf and the atmosphere

WUE

water use efficiency

WT

wild type

Notes

Acknowledgments

We would like BBSRC grant no.BB/L001187/1 & BB/N021061/1 for support for T.L along with the School of Biological Sciences, University of Essex; a Sasagawa scientific research grant from The Japan Science Society and a grant-in-aid for JSPS Fellows (no. 12 J08951) for T.F; a MEXT Grant-in-Aid for Scientific Research on Innovative Areas (no. 21114007) from and JSPS Grants-in-Aid for Exploratory Studies (nos. 23657029 and 15 K14537) for I.T; and a JSPS research fellowship for young scientists (no. 2010431) for Y.W.

References

  1. Araújo WL, Fernie AR, Nunes-Nesi A (2011) Control of stomatal aperture. Plant Signal Behav 6:1305–1311PubMedPubMedCentralCrossRefGoogle Scholar
  2. Araújo WL, Nunes-Nesi A, Osorio S, Usadel B, Fuentes D, Nagy R, Balbo I, Lehmann M, Studart-Witkowski C, Tohge T, Martinoia E, Jordana X, DaMatta FM, Fernie AR (2012) 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. Plant Cell 23:600–627CrossRefGoogle Scholar
  3. Araújo WL, Nunes-Nesi A, Fernie AR (2013) On the role of plant mitochondrial metabolism and its impact on photosynthesis in both optimal and sub-optimal growth conditions. Photosynth Res 119:141–156PubMedCrossRefPubMedCentralGoogle Scholar
  4. Assmann SM (1993) Signal transduction in guard cells. Annu Rev Cell Biol 9:345–375PubMedCrossRefPubMedCentralGoogle Scholar
  5. Azoulay-Shemer T, Palomares A, Bagheri A, Israelsson-Nordstrom M, Engineer CB, Bargmann BO, Stephan AB, Schroeder JI (2015) Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO2- and ABA-induced stomatal closing. Plant J 83:567–581PubMedPubMedCentralCrossRefGoogle Scholar
  6. Ball TJ, Berry JA (1982) C i/C s ratio: a basis for predicting stomatal control of photosynthesis. Carnegie Inst Wash Year Book 81:88–92Google Scholar
  7. Baroli I, Price GD, Badger MR, von Caemmerer S (2008) The contribution of photosynthesis to the red light response of stomatal conductance. Plant Physiol 146:737–747PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bates GW, Rosenthal DM, Sun J, Chattopadhyay M, Peffer E, Yang J, Ort DR, Jones AM (2012) A comprative study of the Arabidopsis thaliana guard-cell transcriptome and its modulation by sucrose. PLoS One 7:e49641PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bowling DJF (1987) Measurement of the apoplastic activity of K+ and Cl in the leaf epidermis of Commelina communis in relation to stomatal activity. J Exp Bot 38:1351–1355CrossRefGoogle Scholar
  10. Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA (2009) Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proc R Soc London B 276:1771–1776CrossRefGoogle Scholar
  11. Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890–1898PubMedPubMedCentralCrossRefGoogle Scholar
  12. Buckley TN, Mott KA (2013) Modeling stomatal conductance in response to environmental factors. Plant Cell Environ 36:1691–1699PubMedCrossRefPubMedCentralGoogle Scholar
  13. Buckley TN, Mott KA, Farquhar GD (2003) A hydromechanical and biochemical model of stomatal conductance. Plant Cell Environ 26:1767–1785CrossRefGoogle Scholar
  14. 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 119:131–140PubMedCrossRefPubMedCentralGoogle Scholar
  15. Büssis D, von Groll U, Fisahn J, Altmann TA (2006) Stomatal aperture can compensate altered stomatal density in Arabidopsis thaliana at growth light conditions. Funct Plant Biol 33:1037–1043CrossRefGoogle Scholar
  16. Cockburn W, Ting IP, Sternberg LO (1979) Relationships between stomatal behavior and internal carbon dioxide concentration in Crassulacean acid metabolism plants. Plant Physiol 63:1029–1032PubMedPubMedCentralCrossRefGoogle Scholar
  17. Dale JE (1961) Investigations into the stomatal physiology of upland cotton. I. The effects of hour of day, solar radiation, temperature and leaf water-content on stomatal behaviour. Ann Bot 25:39–52CrossRefGoogle Scholar
  18. Daloso DM, Antunes WC, Pinheiro DP, Waquim JP, Araújo WL, Loureiro ME, Fernie AR, Williams TC (2015) Tobacco guard cells fix CO2 by both Rubisco and PEPcase while sucrose acts as a substrate during light-induced stomatal opening. Plant Cell Env 38:2353–2371CrossRefGoogle Scholar
  19. Daloso DM, Anjos L, Fernie AR (2016) Roles of sucrose in guard cell regulation. New Phytol 211:809–818PubMedCrossRefPubMedCentralGoogle Scholar
  20. Darwin F (1898) Observations on stomata. Philos T Roy Soc B 190:531–621CrossRefGoogle Scholar
  21. 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 210:1219–1228PubMedPubMedCentralCrossRefGoogle Scholar
  22. 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 T Roy Soc B 367:547–555CrossRefGoogle Scholar
  23. Dow GJ, Berry JA, Bergmann DC (2014) The physiological importance of developmental mechanisms that enforce proper stomatal spacing in Arabidopsis thaliana. New Phytol 201:1205–1217PubMedCrossRefPubMedCentralGoogle Scholar
  24. Edwards MC, Smith GN, Bowling DJF (1988) Guard cells extrude protons prior to stomatal opening – A study using fluorescence microscopy and pH micro-electrodes. J Exp Bot 39:1541–1547CrossRefGoogle Scholar
  25. Ewert MS, Outlaw WH Jr, Zhang S, Aghoram K, Riddle KA (2000) Accumulation of an apoplastic solute in the guard-cell wall is sufficient to exert a significant effect on transpiration in Vicia faba leaflets. Plant Cell Env 23:195–203CrossRefGoogle Scholar
  26. Farquhar GD, Raschke K (1978) On the resistance to transpiration of the sites of evaporation within the leaf. Plant Physiol 61:1000–1005PubMedPubMedCentralCrossRefGoogle Scholar
  27. Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345CrossRefGoogle Scholar
  28. Farquhar GD, Wong SC (1984) An empirical model of stomatal conductance. Aust J Plant Physiol 11:191–210CrossRefGoogle Scholar
  29. Fernie AR, Martinoia E (2009) Malate. Jack of all trades or master of a few? Phytochemistry 70:828–832PubMedCrossRefPubMedCentralGoogle Scholar
  30. Fischer RA, Rees D, Sayre KD, Lu ZM, Condon AG, Saavedra AL (1998) Wheat yield progress associated with higher stomatal conductance and photosynthetic rate, and cooler canopies. Crop Sci 38:1467–1475CrossRefGoogle Scholar
  31. Franks PJ, Beerling DJ (2009a) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. P Natl Acad Sci USA 106:10343–10347CrossRefGoogle Scholar
  32. Franks PJ, Beerling DJ (2009b) CO2-forced evolution of plant gas exchange capacity and water-use efficiency over the Phanerozoic. Geobiology 7:227–236PubMedCrossRefPubMedCentralGoogle Scholar
  33. Franks PJ, Farquhar GD (2007) The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiol 86:700–705Google Scholar
  34. Franks PJ, Doheny-Adams T, Britton-Harper ZJ, Gray JE (2015) Increasing water-use efficiency directly through genetic manipulation of stomatal density. New Phytol 207:188–195PubMedCrossRefPubMedCentralGoogle Scholar
  35. Frechilla S, Talbott L, Bogomoln R, Zeiger E (2000) Reversal of blue light-stimulated stomatal opening by green light. Plant Cell Physiol 41:171–176PubMedCrossRefPubMedCentralGoogle Scholar
  36. Fujita T, Noguchi K, Terashima I (2013) Apoplastic mesophyll signals induce rapid stomatal responses to CO2 in Commelina communis. New Phytol 199:395–406PubMedCrossRefPubMedCentralGoogle Scholar
  37. Goh CH, Oku T, Shimazaki K-i (1995) Properties of proton pumping in response to blue light and fusicoccin in guard cell protoplasts isolated from adaxial epidermis of Vicia leaves. Plant Physiol 109:187–194PubMedPubMedCentralCrossRefGoogle Scholar
  38. Goh CH, Oku T, Shimazaki K-i (1997) Photosynthetic properties of adaxial guard cells from Vicia leaves. Plant Sci 127:149–159CrossRefGoogle Scholar
  39. Goh CH, Dietrich P, Steinmeyer R, Schreiber U, Nam HG, Hedrich R (2002) Parallel recordings of photosynthetic electron transport and K+-channel activity in single guard cells. Plant J 32:623–630PubMedCrossRefPubMedCentralGoogle Scholar
  40. Granot D, David-Schwartz R, Kelly G (2013) Hexose kinases and their role in sugar-sensing and plant development. Front Plant Sci 4: Article 44(1--17)Google Scholar
  41. Grantz DA, Schwartz A (1988) Guard cells of Commelina communis L. do not respond metabolically to osmotic stress in isolated epidermis: Implications for stomatal responses to drought and humidity. Planta 174:166–173PubMedCrossRefPubMedCentralGoogle Scholar
  42. Heath OVS (1949) Studies in stomatal behaviour. II. Role of starch in the light response of stomata. Part I. Review of the literature and experiments on the relation bewtween aperture and starch content in the stomata of Perlargonium zonale. New Phytol 48:186–209CrossRefGoogle Scholar
  43. Hedrich R, Marten I (1993) Malate-induced feedback regulation of plasma mambrane anion channels could provide a CO2 sensor to guard cells. EMBO J 12:897–901PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hedrich R, Marten I, Lohse G, Dietrich P, Winter H, Lohaus G, Heldt HW (1994) Malate sensitive anion channels enable guard cells to sense changes in the ambient CO2 concentration. Plant J 6:741–748CrossRefGoogle Scholar
  45. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908CrossRefGoogle Scholar
  46. Horrer D, Flütsch S, Pazmino D, Matthews JSA, Thalmann M, Nigro A, Leonhardt N, Lawson T, Santelia D (2016) Blue light induces a distinct starch degradation pathway in guard cells for stomatal opening. Current Biol 26:362–370CrossRefGoogle Scholar
  47. Hosler JP, Yocum CF (1987) Regulation of cyclic photophosphorylation during ferredoxin-mediated electron transport. Effect pf DCMU and the NADPH/NADP+ ratio. Plant Physiol 83:965–969PubMedPubMedCentralCrossRefGoogle Scholar
  48. IPCC (2013) Climate change 2013: The physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Cambridge University Press, Cambridge/New YorkGoogle Scholar
  49. Jones HG (1987) Breeding for stomatal characters, Stanford. Stanford University PressGoogle Scholar
  50. Kang YUN, 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 Env. 30:551–558CrossRefGoogle Scholar
  51. Kelly G, David-Schwartz R, Sade N, Moshelion M, Levi A, Alchanatis V, Granot D (2012) The pitfalls of transgenic selection and new roles of AtHXK1: a high level of AtHXK1 expression uncouples hexokinase 1-dependent sugar signaling from exogenous sugar. Plant Physiol 159:47–51PubMedPubMedCentralCrossRefGoogle Scholar
  52. Kelly G, Moshelion M, David-Schwartz R, Halperin O, Wallach R, Attia Z, Belausov E, Granot D (2013) Hexokinase mediates stomatal closure. Plant J 75:977–988PubMedCrossRefPubMedCentralGoogle Scholar
  53. Kinoshita T, Dowe M, Suetsugu N, Kagawa T, Wada M, Shimazaki K (2001) phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414:656–660PubMedCrossRefPubMedCentralGoogle Scholar
  54. Kirschbaum MUF, Gross LJ, Pearcy RW (1988) Observed and modeled stomatal responses to dynamic light environments in the shade plant Alocasia macrorrhiza. Plant Cell Env 11:111–121Google Scholar
  55. Kuiper P (1964) Dependence upon wavelength of stomatal movement in epidermal tissue of Senecio odoris. Plant Physiol 39:952–955PubMedPubMedCentralCrossRefGoogle Scholar
  56. Lawson T (2009) Guard cell photosynthesis and stomatal function. New Phytol 181:13–34PubMedCrossRefPubMedCentralGoogle Scholar
  57. Lawson T, Blatt M (2014) Stomatal size, speed and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol 164:1556–1570PubMedPubMedCentralCrossRefGoogle Scholar
  58. Lawson T, McElwain JC (2016) Evolutionary trade-offs in stomatal spacing. New Phytol 210:1149–1151PubMedCrossRefPubMedCentralGoogle Scholar
  59. Lawson T, Morison JI (2004) Stomatal function and physiology. In: Hemsley AR, Poole I (eds) The evolution of plant physiology: from whole plants to ecosystem. Elsevier Academic Press, Cambridge, pp 217–242CrossRefGoogle Scholar
  60. Lawson T, Weyer JDB (1999) Spatial and temporal variation in gas exchange over the lower surface of Phaseolus vulgaris L. primary leaves. J Exp Bot 50:1381–1391CrossRefGoogle Scholar
  61. Lawson T, Lefebvre S, Baker NR, Morison JI, Raines CA (2008) Reductions in mesophyll and guard cell photosynthesis impact on the control of stomatal responses to light and CO2. J Exp Bot 59:3609–3619PubMedPubMedCentralCrossRefGoogle Scholar
  62. Lawson T, von Caemmerer S, Baroli I (2010) Photosynthesis and stomatal behaviour. In: Lüttge U, Beyschlag W, Büdel B, Francis D (eds) Progress in botany, vol 72. Springer, Berlin/Heidelberg, pp 265–304Google Scholar
  63. Lawson T, Kramer DM, Raines CA (2012) Improving yield by exploiting mechanisms underlying natural variation of photosynthesis. Current Opin Biotechnol 23:215–220CrossRefGoogle Scholar
  64. Lee J, Bowling DJF (1992) Effect of the mesophyll on stomatal opening in Commelina communis. J Exp Bot 43:951–957CrossRefGoogle Scholar
  65. Lee J, Bowling DJF (1993) The effect of a msophyll factor on the swellilng of guard cell protoplasts of Commelina communis L. J Plant Physiol 142:203–207CrossRefGoogle Scholar
  66. Lee J, Bowling DJF (1995) Influence of the mesophyll on stomatal opening. Aust J Plant Physiol 22:357–363CrossRefGoogle Scholar
  67. Lee M, Burla B, Kim YY, Jeon B, aeshima M, Yoo JY, Martinoia E, Lee Y (2008) The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2. Nat Cell Biol 10:1217–1223PubMedCrossRefPubMedCentralGoogle Scholar
  68. Lu P, Outlaw WK Jr, Riddle K (1995) Sucrose: a solute that accumulates in the guard-cell apoplast and guard-cell symplast of open stomata. FEBS Lett 10:219–223Google Scholar
  69. Lu P, Ourlaw 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 114:109–118PubMedPubMedCentralCrossRefGoogle Scholar
  70. Lu Z, Pearcy RG, Qualset CO, Zeiger E (1998) Stomatal conductance predicts yield in irrigated Pima cotton and bread wheat grown at high temperatures. J Exp Bot 49:453–460CrossRefGoogle Scholar
  71. Mansfield T, Hetherington A, Atkinson C (1990) Some current aspects of stomatal physiology. Annu Rev Plant Biol 41:55–75CrossRefGoogle Scholar
  72. Marten H, Hyun T, Gomi K, Seo S, Hedrich R, Roelfsema MRG (2008) Silencing of NtMPK4 impairs CO2-induced stomatal closure, activation of anion channels and cytosolic Ca2+ signals in Nicotiana tabacum guard cells. Plant J 55:698–708PubMedCrossRefPubMedCentralGoogle Scholar
  73. Mawson BT (1993) Regulation of blue-light-induced proton pumping by Vicia faba L. guard-cell protoplasts: Energetic contributions by chloroplastic and mitochondrial activities. Planta 191:293–301CrossRefGoogle Scholar
  74. McAusland L, Vialet-Chabrand S, Matthews J, Lawson T (2015) Spatial and temporal responses in stomatal behaviour, photosynthesis and implications for water-use efficiency. In: Mancuso S, Shabala S (eds) Rhythms in plants. Springer, Heidelberg/New York/Dordrecht/London, pp 97–119CrossRefGoogle Scholar
  75. McAusland L, Vialet-Chabrand S, Davey PA, Baker NR, Brendel O, Lawson T (2016) Effects of kinetics of light-induced stomatal responses on photosynthesis and water use efficiency. New Phytol 211:1209–1220PubMedPubMedCentralCrossRefGoogle Scholar
  76. 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 209:94–103PubMedCrossRefPubMedCentralGoogle Scholar
  77. Messinger SM, Buckley TN, Mott KA (2006) Evidence for involvement of photosynthetic processes in the stomatal response to CO2. Plant Physiol 140:771–778PubMedPubMedCentralCrossRefGoogle Scholar
  78. Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light and hormonal signaling. Science 300:332–336PubMedCrossRefPubMedCentralGoogle Scholar
  79. Mott KA (1988) Do stomata respond to CO2 concentrations other than intercellular? Plant Physiol 86:200–203PubMedPubMedCentralCrossRefGoogle Scholar
  80. Mott KA, Sibbernsen ED, Shope JC (2008) The role of the mesophyll in stomatal responses to light and CO2. Plant Cell Env 31:1299–1306CrossRefGoogle Scholar
  81. Mott KA, Berg DG, Hunt SM, Peak D (2014) Is the signal from the mesophyll to the guard cells a vapour-phase ion? Plant Cell Env 37:1184–1191CrossRefGoogle Scholar
  82. Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada M, Uchimiya H, Hashimoto M, Iba K (2008) CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452:483–486PubMedCrossRefPubMedCentralGoogle Scholar
  83. Nelson SD, Mayo JM (1975) The occurrence of functional non-chlorophyllous guard cells in Paphiopedilum spp. Can J Bot 53:1–7CrossRefGoogle Scholar
  84. Nunes-Nesi A, Sulpice R, Gibon Y, Fernie AR (2008) The enigmatic contribution of mitochondrial function in photosynthesis. J Exp Bot 59:1675–1684PubMedCrossRefPubMedCentralGoogle Scholar
  85. Ohgishi M, Saji K, Okada K, Sakai T (2004) Functional analysis of each blue light receptor, cry1, cry2, phot1, and phot2, by using combinatorial multiple mutants in Arabidopsis. P Natl Acad Sci USA 101:2223–2228CrossRefGoogle Scholar
  86. Olsen RL, Pratt RB, Gump P, Kemper A, Tallman G (2002) Red light activates a chloroplast-dependent ion uptake mechanism for stomatal opening under reduced CO2 concentrations in Vicia spp. New Phytol 153:497–508CrossRefGoogle Scholar
  87. Outlaw WH Jr (2003) Integration of cellular and physiological functions of guard cells. Critic Rev Plant Sci 22:503–529CrossRefGoogle Scholar
  88. Outlaw WH Jr, De Vlieghere-He X (2001) Transpiration rate, an important factor controllong the sucrose content of the guard cell apoplast of broad bean. Plant Physiol 126:1716–1724PubMedPubMedCentralCrossRefGoogle Scholar
  89. Parlange JY, Waggoner PE (1970) Stomatal dimensions and resistance to diffusion. Plant Physiol 46:337–342PubMedPubMedCentralCrossRefGoogle Scholar
  90. Pemadasa MA (1979) Movement of abaxial and adaxial stomata. New Phytol 82:69–80CrossRefGoogle Scholar
  91. Pemadasa MA (1982) Abaxial and adaxial stomatal responses to light of different wavelengths and to phenylacetic acid on isolated epidermis of Commelina communis L. J Exp Bot 33:92–99CrossRefGoogle Scholar
  92. Radin JW, Hartung W, Kimball BA, Mauney JR (1988) Correlation of stomatal conductance with photosynthetic capacity of cotton only in a CO2-enriched atmosphere: mediation by abscisic acid? Plant Physiol 88:1058–1062PubMedPubMedCentralCrossRefGoogle Scholar
  93. Raschke K (1975) Stomatal action. Annu Rev Plant Physiol 26:309–340CrossRefGoogle Scholar
  94. Roelfsema MRG, Steinmeyer R, Staal M, Hedrich R (2001) Single guard cell recordings in intact plants: light-induced hyperpolarization of the plasma membrane. Plant J 26:1–13PubMedCrossRefPubMedCentralGoogle Scholar
  95. Roelfsema MRG, Hanstein S, Felle HH, Hedrich R (2002) CO2 provides an intermediate link in the red light response of guard cells. Plant J 32:65–75PubMedCrossRefPubMedCentralGoogle Scholar
  96. Roelfsema M, Konrad KR, Marten H, Psaras GK, Hartung W, Hedrich R (2006a) Guard cells in albino leaf patches do not respond to photosynthetically active radiation, but are sensitive to blue light, CO2 and abscisic acid. Plant Cell Env 29:1595–1605CrossRefGoogle Scholar
  97. Roelfsema MRG, Steinmeyer R, Staal M, Hedrich R (2006b) Single guard cell recordings in intact plants: light-induced hypoerpolarization of the plasma membrane. Plant Cell 7:1655–1666Google Scholar
  98. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: Conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709PubMedCrossRefPubMedCentralGoogle Scholar
  99. Schwartz A, Zeiger Z (1984) Metabolic energy for stomatal opening. Roles of photophosphorylation and oxidative phosphorylation. Planta 161:129–136PubMedCrossRefPubMedCentralGoogle Scholar
  100. Serrano EE, Zeiger E, Hagiwara S (1988) Red light stimulates an electrogenic proton pump in Vicia guard cell protoplasts. P Natl Acad Sci USA 85:436–440CrossRefGoogle Scholar
  101. Sharkey TD, Raschke K (1981a) Effect of light quality on stomatal opening in leaves of Xanthium strumarium L. Plant Physiol 68:1170–1174PubMedPubMedCentralCrossRefGoogle Scholar
  102. Sharkey TD, Raschke K (1981b) Separation and measurement of direct and indirect effects of light on stomata. Plant Physiol 68:33–40PubMedPubMedCentralCrossRefGoogle Scholar
  103. Shimazaki K-i, Zeiger E (1985) Cyclic and noncyclic photophosphorylation in isolated guard cell chloroplasts from Vicia faba L. Plant Physiol 78:211–214PubMedPubMedCentralCrossRefGoogle Scholar
  104. Shimazaki K-i, Doi M, Assmann SM, Kinoshita T (2007) Light regulation of stomatal movement. Annu Rev Plant Biol 58:219–247PubMedCrossRefPubMedCentralGoogle Scholar
  105. 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 cell. Plant Physiol 153:1435–1442PubMedPubMedCentralCrossRefGoogle Scholar
  106. Stadler R, Bu M, Ache P, Hedrich R, Ivashikina N, Melzer M, Shearson SM, Smith SM, Sauer N, Germany RS (2003) Diurnal and light-regulated expression of AtSTP1 in guard cells of Arabidopsis. Plant Physiol 133:528–537PubMedPubMedCentralCrossRefGoogle Scholar
  107. Steinitz B, Ren Z, Poff KL (1985) Blue and green light-induced phototropism in Arabidopsis thaliana and Lactuca sativa L. seedlings. Plant physiol 77:248–251PubMedPubMedCentralCrossRefGoogle Scholar
  108. Sun JD, Nishio JN, Vogelmann TC (1998) Green light drives CO2 fixation deep within leaves. Plant Cell Physiol 39:1020–1026CrossRefGoogle Scholar
  109. Talbott L, Nikolova G, Ortiz A, Shmayevich I, Zeiger E (2002) Green light reversal of blue-light-stimulated stomatal opening is found in a diversity of plant species. Amer J Bot 89:366–368CrossRefGoogle Scholar
  110. Talbott L, Hammad J, Harn L, Nguyen V, Patel J, Zeiger E (2006) Reversal by green light of blue light-stimulated stomatal opening in intact, attached leaves of Arabidopsis operates only in the potassium-dependent, morning phase of movement. Plant Cell Physiol 47:332–339PubMedCrossRefPubMedCentralGoogle Scholar
  111. Tanaka Y, Sugano SS, Shimada T, Hara-Nishimura I (2013) Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis. New Phytol 198:757–764PubMedCrossRefPubMedCentralGoogle Scholar
  112. Taylor A, Assmann SM (2001) Apparent absence of a redox requirement for blue light activation of pump current in broad bean guard cells. Plant Physiol 125:329–338PubMedPubMedCentralCrossRefGoogle Scholar
  113. Terashima I, Hikosaka K (1995) Comparative ecophysiology of leaf and canopy photosynthesis. Plant Cell Env 18:1111–1128CrossRefGoogle Scholar
  114. Terashima I, Fujita T, Inoue T, Chow WS, Oguchi R (2009) Green light drives leaf photosynthesis more efficiently than red light in strong white light: revisiting the enigmatic question of why leaves are green. Plant Cell Physiol 50:684–697CrossRefGoogle Scholar
  115. Tinoco-Ojanguren C, Pearcy R (1993) Stomatal dynamics and its importance to carbon gain in two rain forest Piper species. I. VPD Effects on the transient stomatal response to light flecks. Oecologia 94:388–394PubMedCrossRefPubMedCentralGoogle Scholar
  116. Tominaga M, Kinoshita T, Shimazaki K-i (2001) Guard-cell chloroplasts provide ATP required for H+ pumping in the plasma membrane and stomatal opening. Plant Cell Physiol 42:795–802PubMedCrossRefPubMedCentralGoogle Scholar
  117. Travis AJ, Mansfield TA (1981) Light saturation of stomatal opening on the adaxial and abaxial epidermis of Commelina communis. J Exp Bot 32:1169–1179CrossRefGoogle Scholar
  118. Turner NC (1970) Repsonse of adaxial and abaxial stomata to light. New Phytol 69:647–653CrossRefGoogle Scholar
  119. Vahisalu T, Kollist H, Wang Y-F, Nishimura N, Chan W-Y, Valerio G, Lamminmäki A, Brosché M, Moldau H, Desikan R, Schroeder JI, Kangasjärvi J (2008) SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452:487–491PubMedPubMedCentralCrossRefGoogle Scholar
  120. Vavasseur A, Raghavendra AS (2005) Guard cell metabolism and CO2 sensing. New Phytol 165:665–682PubMedCrossRefPubMedCentralGoogle Scholar
  121. 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 55:1157–1166CrossRefGoogle Scholar
  122. Wang P, Song CP (2008) Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytologist 178:703–718PubMedCrossRefPubMedCentralGoogle Scholar
  123. Wang Y, Noguchi K, Terashima I (2008) Distinct light responses of the adaxial and abaxial stomata in intact leaves of Helianthus annuus L. Plant Cell Env. 31:1307–1316CrossRefGoogle Scholar
  124. Wang Y, Noguchi K, Terashima I (2011) Photosynthesis-dependent and -independent responses of stomata to blue, red and green monochromtic light: differences bewteen the normally oriented and inverted leaves of sunflower. Plant Cell Physiol 652:479–489CrossRefGoogle Scholar
  125. Weise A, Lalonde S, Kühn C, Frommer WB, Ward JM (2008) Introns control expression of sucrose transporter LeSUT1 in trichomes, companion cells and in guard cells. Plant Mol Biol 68:251–262PubMedCrossRefPubMedCentralGoogle Scholar
  126. Weyers JDB, Lawson T (1997) Heterogeneity in stomatal characteristics. Adv Bot Res 26:317–352CrossRefGoogle Scholar
  127. Weyers JDB, Meidner H (1990) Methods in Stomatal Research. Longman, HarlowGoogle Scholar
  128. Willmer C, Fricker M (1996) Stomata. Chapman & Hall. In: LondonGoogle Scholar
  129. Wong SC, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Plant Physiol 78:830–834CrossRefGoogle Scholar
  130. Wong SC, Cowan IR, Farquhar GD (1985a) Leaf conductance in relation to rate of CO2 assimilation I. Influcence of nitrogen nutrition, phosphorus nutrition, photon flux density, and ambient partial pressure of CO2 during ontogeny. Plant Physiol 78:821–825PubMedPubMedCentralCrossRefGoogle Scholar
  131. Wong SC, Cowan IR, Farquhar GD (1985b) Leaf conductance in relation to rate of CO2 assimilation II. Effects of short-term exposures to different photon flux densities. Plant Physiol 78:826–829PubMedPubMedCentralCrossRefGoogle Scholar
  132. Wong SC, Cowan IR, Farquhar GD (1985c) Leaf conductance in relation to rate of CO2 assimilation III. Influences of water stress and photoinhibition. Plant Physiol 78:830–834PubMedPubMedCentralCrossRefGoogle Scholar
  133. Wu W, Assmann SM (1993) Photosynthesis by guard cell chloroplasts of Vicia faba L.: effects of factors associated with stomatal movements. Plant Cell Physiol 34:1015–1022Google Scholar
  134. 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 49:433–442CrossRefGoogle Scholar
  135. Zeiger E, Talbott LD, Frechilla S, Srivastava A, Zhu J (2002) The guard cell chloroplast: a perspective for the twenty-first century. New Phytol 153:415–424CrossRefGoogle Scholar
  136. Zhang T, Maruhnich SA, Folta KM (2011) Green light induces shade avoidance symptoms. Plant Physiol 157:1528–1536PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Tracy Lawson
    • 1
    Email author
  • Ichiro Terashima
    • 2
  • Takashi Fujita
    • 2
  • Yin Wang
    • 3
  1. 1.School of Biological SciencesUniversity of EssexColchesterUK
  2. 2.Department of Biological Sciences, Graduate School of ScienceThe University of TokyoTokyoJapan
  3. 3.Institute of Transformative Bio-Molecules (ITbM)Nagoya UniversityNagoyaJapan

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