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

Photosynthesis Research

Volumn 119, Issue 1-2, 2014, Pages 131-140

  Busch, Florian A ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Guard cell; Photosynthesis; Redox state of plastoquinone; Stomatal conductance

Indexed keywords

PLASTOQUINONE;

BIOLOGICAL MODEL; ELECTRON TRANSPORT; LIGHT; METABOLISM; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT STOMA; REVIEW;

ELECTRON TRANSPORT; LIGHT; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; PHOTOSYNTHESIS; PLANT STOMATA; PLASTOQUINONE;

EID: 84891626943     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-013-9805-6     Document Type: Review

References (94)

1. Allen JF (2003) State transitions - a question of balance. Science 299(5612):1530-1532. doi: 10.1126/science.1082833
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
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
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 221-224
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
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
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
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):300-308
9. i. Plant Physiol 111(1):179-185. doi: 10.1104/pp.111.1.179
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
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
12. Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21-45. doi: 10.1146/annurev.arplant.58.032806.103951
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
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
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):4781-4795
16. Ensminger I, Busch F, Hüner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126(1):28-44
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):10237-10241
18. Farquhar G, Wong S (1984) An empirical model of stomatal conductance. Funct Plant Biol 11(3):191-210. doi: 10.1071/PP9840191
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
20. +-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
21. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424(6951):901-908
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
23. + uptake and stomatal opening in Vivia faba. Plant Physiol 51(1):82-88. doi: 10.1104/pp.51.1.82
24. 2-controlled stomatal movements in guard cells. Nat Cell Biol 12(1):87-93. doi: 10.1038/ncb2009
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
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 401-421
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
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
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
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
31. A redox state and excitation energy fluxes. Photosynth Res 79(2):209-218
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
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
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
35. 2. J Exp Bot 59(13):3609-3619. doi: 10.1093/jxb/ern211
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
37. Leuning R (1990) Modelling stomatal behaviour and photosynthesis of Eucalyptus grandis. Funct Plant Biol 17(2):159-175. doi: 10.1071/PP9900159
38. 3 plants. Plant Cell Environ 18(4):339-355. doi: 10.1111/j.1365-3040.1995.tb00370.x
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
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
41. Lurie S (1978) The effect of wavelength of light on stomatal opening. Planta 140(3):245-249. doi: 10.1007/bf00390255
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
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
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
45. 2. In: Zeiger E, Farquhar GD, Cowan IR (eds) Stomatal function. Stanford University Press, Stanford, pp 229-251
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. 2 depend on the mesophyll. Plant Cell Environ 32(11):1479-1486. doi: 10.1111/j.1365-3040.2009.02022.x
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
49. 2. Planta 209(1):104-111. doi: 10.1007/s004250050611
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
51. 2 concentrations in Vicia spp. New Phytol 153(3):497-508. doi: 10.1046/j.0028-646X.2001.00337.x
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
53. Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8(1):33-41
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
55. Pfannschmidt T, Nilsson A, Allen JF (1999a) Photosynthetic control of chloroplast gene expression. Nature 397(6720):625-628
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
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
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
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
60. 2 assimilation via a reduction in ribulose bisphosphate regeneration in transgenic tobacco plants. Planta 195(3):369-378. doi: 10.1007/bf00202594
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):445-452
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
63. 2 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
64. 2 and abscisic acid. Plant Cell Environ 29(8):1595-1605. doi: 10.1111/j.1365-3040.2006.01536.x
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
66. 2 assimilation, and plant growth by overacidification of the thylakoid lumen. Plant Cell 23(1):304-321. doi: 10.1105/tpc.110.079111
67. 2 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 181-230
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
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):436-440
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 195-208
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
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
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
75. 2, and air humidity. Planta 183(4):555-566. doi: 10.1007/bf00194277
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
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):1527-1534
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
81. + pumping in the plasma membrane and stomatal opening. Plant Cell Physiol 42(8):795-802. doi: 10.1093/pcp/pce101
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
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. 2 sensing. New Phytol 165(3):665-682. doi: 10.1111/j.1469-8137.2004. 01276.x
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
86. 4 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
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
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
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):424-426
91. 2 during ontogeny. Plant Physiol 78(4):830-834. doi: 10.1104/pp.78.4.830
92. 2 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
93. 2 assimilation. III. Influences of water stress and photoinhibition. Plant Physiol 78(4):830-834. doi: 10.1104/pp.78.4.830
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