Photosynthesis Research

, Volume 119, Issue 1–2, pp 131–140 | Cite as

Opinion: The red-light response of stomatal movement is sensed by the redox state of the photosynthetic electron transport chain

Review
First Online:
Received:
Accepted:

Abstract

Guard cells regulate CO2 uptake and water loss of a leaf by controlling stomatal movement in response to environmental factors such as CO2, humidity, and light. The mechanisms by which stomata respond to red light are actively debated in the literature, and even after decades of research it is still controversial whether stomatal movement is related to photosynthesis or not. This review summarizes the current knowledge of the red-light response of stomata. A comparison of published evidence suggests that stomatal movement is controlled by the redox state of photosynthetic electron transport chain components, in particular the redox state of plastoquinone. Potential consequences for the modeling of stomatal conductance are discussed.

Keywords

Guard cell Photosynthesis Stomatal conductance Redox state of plastoquinone 

Abbreviations

Anet

Net CO2 assimilation rate

DCMU

3-(3,4-Dichlorophenyl)-1,1-dimethylurea

ETR

Photosynthetic electron transport rate

FR

Far-red

gs

Stomatal conductance

PQ

Plastoquinone

PS

Photosystem

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Notes

Acknowledgments

I thank Nerea Ubierna, Crystal Vincent, and Susanne von Caemmerer for stimulating discussions and comments on a draft of this manuscript.

References

  1. Allen JF (2003) State transitions—a question of balance. Science 299(5612):1530–1532. doi: 10.1126/science.1082833 PubMedCrossRefGoogle Scholar
  2. Anderson JM, Dean Price G, Soon Chow W, Hope AB, Badger MR (1997) Reduced levels of cytochrome bf complex in transgenic tobacco leads to marked photochemical reduction of the plastoquinone pool, without significant change in acclimation to irradiance. Photosynth Res 53(2):215–227. doi: 10.1023/a:1005856615915 CrossRefGoogle Scholar
  3. Assmann SM (1993) Signal transduction in guard cells. Annu Rev Cell Biol 9(1):345–375. doi: 10.1146/annurev.cb.09.110193.002021 PubMedCrossRefGoogle Scholar
  4. Ball JT, Woodrow IE, Berry JA (1987) A model predicting stomatal conductance and its contribution to the control of photosynthesis under different environmental conditions. In: Briggins J (ed) Progress in photosynthesis research, vol IV. Martinus Nijhoff Publishers, Dordrecht, pp 221–224CrossRefGoogle Scholar
  5. 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(2):737–747. doi: 10.1104/pp.107.110924 Google Scholar
  6. Boccalandro HE, Giordano CV, Ploschuk EL, Piccoli PN, Bottini R, Casal JJ (2012) Phototropins but not cryptochromes mediate the blue light-specific promotion of stomatal conductance, while both enhance photosynthesis and transpiration under full sunlight. Plant Physiol 158(3):1475–1484. doi: 10.1104/pp.111.187237 Google Scholar
  7. Bräutigam K, Dietzel L, Kleine T, Ströher E, Wormuth D, Dietz K-J, Radke D, Wirtz M, Hell R, Dörmann P, Nunes-Nesi A, Schauer N, Fernie AR, Oliver SN, Geigenberger P, Leister D, Pfannschmidt T (2009) Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis. Plant Cell 21(9):2715–2732. doi: 10.1105/tpc.108.062018 PubMedCentralPubMedCrossRefGoogle Scholar
  8. Brewer PE, Arntzen CJ, Slife FW (1979) Effects of atrazine, cyanazine, and procyazine on the photochemical reactions of isolated chloroplasts. Weed Sci 27(3):300–308Google Scholar
  9. Brodribb T (1996) Dynamics of changing intercellular CO2 concentration (ci) during drought and determination of minimum functional ci. Plant Physiol 111(1):179–185. doi: 10.1104/pp.111.1.179 Google Scholar
  10. Buckley TN, Mott KA, Farquhar GD (2003) A hydromechanical and biochemical model of stomatal conductance. Plant Cell Environ 26(10):1767–1785. doi: 10.1046/j.1365-3040.2003.01094.x Google Scholar
  11. Chen C, Xiao Y-G, Li X, Ni M (2012) Light-regulated stomatal aperture in Arabidopsis. Mol Plant 5(3):566–572. doi: 10.1093/mp/sss039 PubMedCrossRefGoogle Scholar
  12. Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21–45. doi: 10.1146/annurev.arplant.58.032806.103951 Google Scholar
  13. Damour G, Simonneau T, Cochard H, Urban L (2010) An overview of models of stomatal conductance at the leaf level. Plant Cell Environ 33(9):1419–1438. doi: 10.1111/j.1365-3040.2010.02181.x PubMedGoogle Scholar
  14. Dietz K-J, Pfannschmidt T (2011) Novel regulators in photosynthetic redox control of plant metabolism and gene expression. Plant Physiol 155(4):1477–1485. doi: 10.1104/pp.110.170043 Google Scholar
  15. Dwyer SA, Chow WS, Yamori W, Evans JR, Kaines S, Badger MR, von Caemmerer S (2012) Antisense reductions in the PsbO protein of photosystem II leads to decreased quantum yield but similar maximal photosynthetic rates. J Exp Bot 63(13):4781–4795PubMedCrossRefGoogle Scholar
  16. Ensminger I, Busch F, Hüner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126(1):28–44CrossRefGoogle Scholar
  17. Escoubas JM, Lomas M, LaRoche J, Falkowski PG (1995) Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc Natl Acad Sci U S A 92(22):10237–10241PubMedCentralPubMedCrossRefGoogle Scholar
  18. Farquhar G, Wong S (1984) An empirical model of stomatal conductance. Funct Plant Biol 11(3):191–210. doi: 10.1071/PP9840191 Google Scholar
  19. Haake V, Zrenner R, Sonnewald U, Stitt M (1998) A moderate decrease of plastid aldolase activity inhibits photosynthesis, alters the levels of sugars and starch, and inhibits growth of potato plants. Plant J 14(2):147–157. doi: 10.1046/j.1365-313X.1998.00089.x PubMedCrossRefGoogle Scholar
  20. Hajirezaei M-R, Peisker M, Tschiersch H, Palatnik JF, Valle EM, Carrillo N, Sonnewald U (2002) Small changes in the activity of chloroplastic NADP+-dependent ferredoxin oxidoreductase lead to impaired plant growth and restrict photosynthetic activity of transgenic tobacco plants. Plant J 29(3):281–293. doi: 10.1046/j.0960-7412.2001.01209.x PubMedCrossRefGoogle Scholar
  21. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424(6951):901–908PubMedCrossRefGoogle Scholar
  22. Holmes MG, Klein WH (1985) Evidence for phytochrome involvement in light-mediated stomatal movement in Phaseolus vulgaris L. Planta 166(3):348–353. doi: 10.1007/bf00401172 PubMedCrossRefGoogle Scholar
  23. Hsiao TC, Allaway WG, Evans LT (1973) Action spectra for guard cell Rb+ uptake and stomatal opening in Vivia faba. Plant Physiol 51(1):82–88. doi: 10.1104/pp.51.1.82 Google Scholar
  24. Hu H, Boisson-Dernier A, Israelsson-Nordstroem M, Boehmer M, Xue S, Ries A, Godoski J, Kuhn JM, Schroeder JI (2010) Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells. Nat Cell Biol 12(1):87–93. doi: 10.1038/ncb2009 Google Scholar
  25. Hudson GS, Evans JR, von Caemmerer S, Arvidsson YBC, Andrews TJ (1992) Reduction of ribulose-1,5-bisphosphate carboxylase/oxygenase content by antisense RNA reduces photosynthesis in transgenic tobacco plants. Plant Physiol 98(1):294–302. doi: 10.1104/pp.98.1.294 Google Scholar
  26. Hüner NPA, Öquist G, Melis A (2003) Photostasis in plants, green algae and cyanobacteria: the role of light harvesting antenna complexes. In: Green BR, Parson WW (eds) Advances in photosynthesis and respiration: light harvesting antennas in photosynthesis, vol 13. Kluwer Academic Publishers, Dordrecht, pp 401–421CrossRefGoogle Scholar
  27. Hüner NPA, Bode R, Dahal K, Busch FA, Possmayer M, Szyszka B, Rosso D, Ensminger I, Krol M, Ivanov AG, Maxwell DP (2013) Shedding some light on cold acclimation, cold adaptation, and phenotypic plasticity. Botany 91:127–136. doi: 10.1139/cjb-2012-0174 Google Scholar
  28. Jarvis AJ, Davies WJ (1998) The coupled response of stomatal conductance to photosynthesis and transpiration. J Exp Bot 49:399–406. doi: 10.1093/jexbot/49.suppl_1.399 Google Scholar
  29. Joliot P, Joliot A, Kok B (1968) Analysis of the interactions between the two photosystems in isolated chloroplasts. Biochim Biophys Acta 153(3):635–652. doi: 10.1016/0005-2728(68)90191-6 PubMedCrossRefGoogle Scholar
  30. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284(5414):654–657. doi: 10.1126/science.284.5414.654 PubMedCrossRefGoogle Scholar
  31. Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79(2):209–218PubMedCrossRefGoogle Scholar
  32. Kuiper PJC (1964) Dependence upon wavelength of stomatal movement in epidermal tissue of Senecio odoris. Plant Physiol 39(6):952–955. doi: 10.1104/pp.39.6.952 Google Scholar
  33. Lauerer M, Saftic D, Quick WP, Labate C, Fichtner K, Schulze ED, Rodermel SR, Bogorad L, Stitt M (1993) Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with ‘antisense’ rbcS. VI. Effect on photosynthesis in plants grown at different irradiance. Planta 190(3):332–345. doi: 10.1007/bf00196962 CrossRefGoogle Scholar
  34. Lawson T (2009) Guard cell photosynthesis and stomatal function. New Phytol 181(1):13–34. doi: 10.1111/j.1469-8137.2008.02685.x PubMedCrossRefGoogle Scholar
  35. 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(13):3609–3619. doi: 10.1093/jxb/ern211 PubMedCrossRefGoogle Scholar
  36. Lee J, Bowling D (1995) Influence of the mesophyll on stomatal opening. Aust J Plant Physiol 22(3):357–363. doi: 10.1071/PP9950357 CrossRefGoogle Scholar
  37. Leuning R (1990) Modelling stomatal behaviour and photosynthesis of Eucalyptus grandis. Funct Plant Biol 17(2):159–175. doi: 10.1071/PP9900159 Google Scholar
  38. Leuning R (1995) A critical appraisal of a combined stomatal-photosynthesis model for C3 plants. Plant Cell Environ 18(4):339–355. doi: 10.1111/j.1365-3040.1995.tb00370.x CrossRefGoogle Scholar
  39. Liebig M (1942) Untersuchungen über die Abhängigkeit der Spaltweite der Stomata von Intensität und Qualität der Strahlung. Planta 33(2):206–257. doi: 10.1007/bf01916519 CrossRefGoogle Scholar
  40. Lombardozzi D, Levis S, Bonan G, Sparks JP (2012) Predicting photosynthesis and transpiration responses to ozone: decoupling modeled photosynthesis and stomatal conductance. Biogeosciences 9(8):3113–3130. doi: 10.5194/bg-9-3113-2012 CrossRefGoogle Scholar
  41. Lurie S (1978) The effect of wavelength of light on stomatal opening. Planta 140(3):245–249. doi: 10.1007/bf00390255 CrossRefGoogle Scholar
  42. Medlyn BE, Duursma RA, Eamus D, Ellsworth DS, Prentice IC, Barton CVM, Crous KY, De Angelis P, Freeman M, Wingate L (2011) Reconciling the optimal and empirical approaches to modelling stomatal conductance. Glob Change Biol 17(6):2134–2144. doi: 10.1111/j.1365-2486.2010.02375.x CrossRefGoogle Scholar
  43. Messinger SM, Buckley TN, Mott KA (2006) Evidence for involvement of photosynthetic processes in the stomatal response to CO2. Plant Physiol 140(2):771–778. doi: 10.1104/pp.105.073676 Google Scholar
  44. Monteith JL (1995) A reinterpretation of stomatal responses to humidity. Plant Cell Environ 18(4):357–364. doi: 10.1111/j.1365-3040.1995.tb00371.x CrossRefGoogle Scholar
  45. Morison JIL (1987) Intercellular CO2 concentration and stomatal response to CO2. In: Zeiger E, Farquhar GD, Cowan IR (eds) Stomatal function. Stanford University Press, Stanford, pp 229–251Google Scholar
  46. Morison JIL, Jarvis PG (1983) Direct and indirect effects of light on stomata. II. In Commelina communis L. Plant Cell Environ 6(2):103–109. doi: 10.1111/j.1365-3040.1983.tb01882.x
  47. Mott KA (2009) Opinion: stomatal responses to light and CO2 depend on the mesophyll. Plant Cell Environ 32(11):1479–1486. doi: 10.1111/j.1365-3040.2009.02022.x PubMedCrossRefGoogle Scholar
  48. Mott KA, Parkhurst DF (1991) Stomatal responses to humidity in air and helox. Plant Cell Environ 14(5):509–515. doi: 10.1111/j.1365-3040.1991.tb01521.x CrossRefGoogle Scholar
  49. Muschak M, Willmitzer L, Fisahn J (1999) Gas-exchange analysis of chloroplastic fructose-1,6-bisphosphatase antisense potatoes at different air humidities and at elevated CO2. Planta 209(1):104–111. doi: 10.1007/s004250050611 PubMedCrossRefGoogle Scholar
  50. Ogawa T, Ishikawa H, Shimada K, Shibata K (1978) Synergistic action of red and blue light and action spectra for malate formation in guard cells of Vicia faba L. Planta 142(1):61–65. doi: 10.1007/bf00385121 CrossRefGoogle Scholar
  51. 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(3):497–508. doi: 10.1046/j.0028-646X.2001.00337.x CrossRefGoogle Scholar
  52. Pemadasa MA (1982) Abaxial and adaxial stomatal responses to light of different wavelengths and to phenylacetic acid on isolated epidermes of Commelina communis L. J Exp Bot 33(1):92–99. doi: 10.1093/jxb/33.1.92 CrossRefGoogle Scholar
  53. Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8(1):33–41PubMedCrossRefGoogle Scholar
  54. Pfannschmidt T, Yang CH (2012) The hidden function of photosynthesis: a sensing system for environmental conditions that regulates plant acclimation responses. Protoplasma 249:125–136. doi: 10.1007/s00709-012-0398-2 CrossRefGoogle Scholar
  55. Pfannschmidt T, Nilsson A, Allen JF (1999a) Photosynthetic control of chloroplast gene expression. Nature 397(6720):625–628CrossRefGoogle Scholar
  56. Pfannschmidt T, Nilsson A, Tullberg A, Link G, Allen JF (1999b) Direct transcriptional control of the chloroplast genes psbA and psaAB adjusts photosynthesis to light energy distribution in plants. IUBMB Life 48(3):271–276. doi: 10.1080/713803507 PubMedGoogle Scholar
  57. Pfannschmidt T, Bräutigam K, Wagner R, Dietzel L, Schröter Y, Steiner S, Nykytenko A (2009) Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding. Ann Bot 103(4):599–607. doi: 10.1093/aob/mcn081 PubMedCrossRefGoogle Scholar
  58. Piippo M, Allahverdiyeva Y, Paakkarinen V, Suoranta U-M, Battchikova N, Aro E-M (2006) Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress. Physiol Genomics 25(1):142–152. doi: 10.1152/physiolgenomics.00256.2005 PubMedCrossRefGoogle Scholar
  59. Poffenroth M, Green DB, Tallman G (1992) Sugar concentrations in guard cells of Vicia faba illuminated with red or blue light. Plant Physiol 98(4):1460–1471. doi: 10.1104/pp.98.4.1460 Google Scholar
  60. Price GD, Evans JR, Caemmerer S, Yu J-W, Badger MR (1995) Specific reduction of chloroplast glyceraldehyde-3-phosphate dehydrogenase activity by antisense RNA reduces CO2 assimilation via a reduction in ribulose bisphosphate regeneration in transgenic tobacco plants. Planta 195(3):369–378. doi: 10.1007/bf00202594 PubMedCrossRefGoogle Scholar
  61. Price GD, von Caemmerer S, Evans JR, Siebke K, Anderson JM, Badger MR (1998) Photosynthesis is strongly reduced by antisense suppression of chloroplastic cytochrome bf complex in transgenic tobacco. Aust J Plant Physiol 25(4):445–452CrossRefGoogle Scholar
  62. Quick WP, Schurr U, Scheibe R, Schulze ED, Rodermel SR, Bogorad L, Stitt M (1991) Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS. I. Impact on photosynthesis in ambient growth conditions. Planta 183(4):542–554. doi: 10.1007/bf00194276 PubMedCrossRefGoogle Scholar
  63. 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(1):65–75. doi: 10.1046/j.1365-313X.2002.01403.x PubMedCrossRefGoogle Scholar
  64. Roelfsema MRG, Konrad KR, Marten H, Psaras GK, Hartung W, Hedrich R (2006) 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 Environ 29(8):1595–1605. doi: 10.1111/j.1365-3040.2006.01536.x PubMedCrossRefGoogle Scholar
  65. Roth-Bejerano N, Itai C (1981) Involvement of phytochrome in stomatal movement: effect of blue and red light. Physiol Plant 52(2):201–206. doi: 10.1111/j.1399-3054.1981.tb08494.x CrossRefGoogle Scholar
  66. Rott M, Martins NF, Thiele W, Lein W, Bock R, Kramer DM, Schöttler MA (2011) ATP synthase repression in tobacco restricts photosynthetic electron transport, CO2 assimilation, and plant growth by overacidification of the thylakoid lumen. Plant Cell 23(1):304–321. doi: 10.1105/tpc.110.079111 PubMedCentralPubMedCrossRefGoogle Scholar
  67. Schulze E-D, Hall AE (1982) Stomatal responses, water loss and CO2 assimilation rates of plants in contrasting environments. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Physiological plant ecology II. Water relations and carbon assimilation. Springer-Verlag, Berlin, pp 181–230CrossRefGoogle Scholar
  68. Schwartz A, Zeiger E (1984) Metabolic energy for stomatal opening. Roles of photophosphorylation and oxidative phosphorylation. Planta 161(2):129–136. doi: 10.1007/bf00395472 PubMedCrossRefGoogle Scholar
  69. Serrano EE, Zeiger E, Hagiwara S (1988) Red light stimulates an electrogenic proton pump in Vicia guard cell protoplasts. Proc Natl Acad Sci U S A 85(2):436–440PubMedCentralPubMedCrossRefGoogle Scholar
  70. Sharkey TD, Ogawa T (1987) Stomatal responses to light. In: Zeiger E, Farquhar GD, Cowan IR (eds) Stomatal function. Stanford University Press, Stanford, pp 195–208Google Scholar
  71. Sharkey TD, Raschke K (1981a) Effect of light quality on stomatal opening in leaves of Xanthium strumarium L. Plant Physiol 68(5):1170–1174. doi: 10.1104/pp.68.5.1170
  72. Sharkey TD, Raschke K (1981b) Separation and measurement of direct and indirect effects of light on stomata. Plant Physiol 68(1):33–40. doi: 10.1104/pp.68.1.33 Google Scholar
  73. Shimazaki K, Doi M, Assmann SM, Kinoshita T (2007) Light regulation of stomatal movement. Annu Rev Plant Biol 58:219–247. doi: 10.1146/annurev.arplant.57.032905.105434 Google Scholar
  74. 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(3):1435–1442. doi: 10.1104/pp.110.157685 Google Scholar
  75. Stitt M, Quick WP, Schurr U, Schulze ED, Rodermel SR, Bogorad L (1991) Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with ‘antisense’ rbcS. II. Flux-control coefficients for photosynthesis in varying light, CO2, and air humidity. Planta 183(4):555–566. doi: 10.1007/bf00194277 PubMedCrossRefGoogle Scholar
  76. Talbott LD, Zhu JX, Han SW, Zeiger E (2002) Phytochrome and blue light-mediated stomatal opening in the orchid, Paphiopedilum. Plant Cell Physiol 43(6):639–646. doi: 10.1093/pcp/pcf075
  77. Talbott LD, Shmayevich IJ, Chung Y, Hammad JW, Zeiger E (2003) Blue light and phytochrome-mediated stomatal opening in the npq1 and phot1 phot2 mutants of Arabidopsis. Plant Physiol 133(4):1522–1529. doi: 10.1104/pp.103.029587 Google Scholar
  78. Taylor AR, Assmann SM (2001) Apparent absence of a redox requirement for blue light activation of pump current in broad bean guard cells. Plant Physiol 125(1):329–338. doi: 10.1104/pp.125.1.329
  79. Tazawa M, Shimmmen T (1980) Direct demonstration of the involvement of chloroplasts in the rapid light-induced potential change in tonoplast-free cells of Chara australis. Replacement of Chara chloroplasts with spinach chloroplasts. Plant Cell Physiol 21(8):1527–1534Google Scholar
  80. Tjoelker MG, Volin JC, Oleksyn J, Reich PB (1995) Interaction of ozone pollution and light effects on photosynthesis in a forest canopy experiment. Plant Cell Environ 18(8):895–905. doi: 10.1111/j.1365-3040.1995.tb00598.x CrossRefGoogle Scholar
  81. Tominaga M, Kinoshita T, K Shimazaki (2001) Guard-cell chloroplasts provide ATP required for H+ pumping in the plasma membrane and stomatal opening. Plant Cell Physiol 42(8):795–802. doi: 10.1093/pcp/pce101 PubMedCrossRefGoogle Scholar
  82. Travis AJ, Mansfield TA (1981) Light saturation of stomatal opening on the adaxial and abaxial epidermis of Commelina communis. J Exp Bot 32(6):1169–1179. doi: 10.1093/jxb/32.6.1169 CrossRefGoogle Scholar
  83. Trebst A (1980) Inhibitors in electron flow: tools for the functional and structural localization of carriers and energy conservation sites. In: San Pietro A (ed) Methods in enzymology, vol 69. Academic Press, pp 675–715. doi: 10.1016/s0076-6879(80)69067-3
  84. Vavasseur A, Raghavendra AS (2005) Guard cell metabolism and CO2 sensing. New Phytol 165(3):665–682. doi: 10.1111/j.1469-8137.2004.01276.x PubMedCrossRefGoogle Scholar
  85. Vener AV, Ohad I, Andersson B (1998) Protein phosphorylation and redox sensing in chloroplast thylakoids. Curr Opin Plant Biol 1(3):217–223. doi: 10.1016/s1369-5266(98)80107-6 PubMedCrossRefGoogle Scholar
  86. von Caemmerer S, Millgate A, Farquhar GD, Furbank RT (1997) Reduction of ribulose-1,5-bisphosphate carboxylase/oxygenase by antisense RNA in the C4 plant Flaveria bidentis leads to reduced assimilation rates and increased carbon isotope discrimination. Plant Physiol 113(2):469–477. doi: 10.1104/pp.113.2.469 Google Scholar
  87. 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(400):1157–1166. doi: 10.1093/jxb/erh128 CrossRefGoogle Scholar
  88. Wang F-F, Lian H-L, Kang C-Y, Yang H-Q (2010) Phytochrome B is involved in mediating red light-induced stomatal opening in Arabidopsis thaliana. Mol Plant 3(1):246–259. doi: 10.1093/mp/ssp097 Google Scholar
  89. Wang Y, Noguchi K, Terashima I (2011) Photosynthesis-dependent and -independent responses of stomata to blue, red and green monochromatic light: differences between the normally oriented and inverted leaves of sunflower. Plant Cell Physiol 52(3):479–489. doi: 10.1093/pcp/pcr005
  90. Wong SC, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282(5737):424–426CrossRefGoogle Scholar
  91. Wong S-C, Cowan IR, Farquhar GD (1985a) Leaf conductance in relation to rate of CO2 assimilation. I. Influence of nitrogen nutrition, phosphorus nutrition, photon flux density, and ambient partial pressure of CO2 during ontogeny. Plant Physiol 78(4):830–834. doi: 10.1104/pp.78.4.830 Google Scholar
  92. Wong S-C, 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(4):826–829. doi: 10.1104/pp.78.4.826 Google Scholar
  93. Wong S-C, Cowan IR, Farquhar GD (1985c) Leaf conductance in relation to rate of CO2 assimilation. III. Influences of water stress and photoinhibition. Plant Physiol 78(4):830–834. doi: 10.1104/pp.78.4.830 Google Scholar
  94. Zeiger E, Assmann SM, Meidner H (1983) The photobiology of Paphiopedilum stomata: opening under blue but not red light. Photochem Photobiol 38(5):627–630. doi: 10.1111/j.1751-1097.1983.tb03394.x CrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Plant Science Division, Research School of Biology, College of Medicine Biology and the EnvironmentThe Australian National UniversityCanberraAustralia

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