Modulation of environmental responses of plants by circadian clocks

Plant, Cell and Environment

Volumn 30, Issue 3, 2007, Pages 333-349

  Hotta, Carlos T ^a   Gardner, Michael J ^a   Hubbard, Katharine E ^a   Baek, Seong Jin ^a   Dalchau, Neil ^a   Suhita, Dontamala ^a   Dodd, Antony N ^a   Webb, Alex A R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Abscisic acid; Arabidopsis; Circadian gating; Cold; Light; Signalling; Stomata

Indexed keywords

ABSCISIC ACID; CIRCADIAN RHYTHM; DICOTYLEDON; ENVIRONMENTAL CUE; ENVIRONMENTAL RESPONSE; FITNESS; LIGHT EFFECT; LOCAL ADAPTATION; PHOTOPERIOD; SIGNALING; TEMPERATURE EFFECT;

BIOLOGICAL RHYTHM; CIRCADIAN RHYTHM; PLANT PHYSIOLOGY; REVIEW;

BIOLOGICAL CLOCKS; CIRCADIAN RHYTHM; PLANT PHYSIOLOGY;

ARABIDOPSIS;

EID: 33846601810     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2006.01627.x     Document Type: Review

References (161)

1. Alabadí D., Oyama T., Yanovsky M.J., Harmon F.G., Más P. & Kay S.A. (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293, 880-883.
2. Alabadí D., Yanovsky M.J., Más P., Harmer S.L. & Kay S.A. (2002) Critical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis. Current Biology 12, 757-761.
3. Allen T., Koustenis A., Theodorou G., Somers D.E., Kay S.A., Whitelam G.C. & Devlin P.F. (2006) Arabidopsis FHY3 specifically gates phytochrome signaling to the circadian clock. The Plant Cell 18, 2506-2516.
4. Anderson-Bernadas C., Cornelissen G., Turne C.M. & Koukkari W.L. (1997) Rhythmic nature of thigmomorphogenesis and thermal stress of Phaseolus vulgaris L. shoots. Journal of Plant Physiology 151, 575-580.
5. Aschoff J. (1979) Circadian rhythms: influences of internal and external factors on the period measured in constant conditions. Zeitschrift für Tierpsychologie 49, 225-249.
6. Baurle I. & Dean C. (2006) The timing of developmental transitions in plants. Cell 125, 655-664.
7. Borland A.M. & Taybi T. (2004) Synchronization of metabolic processes in plants with Crassulacean acid metabolism. Journal of Experimental Biology 55, 1255-1265.
8. Boxall S.F., Foster J.M., Bohnert H.J., Cushman J.C., Nimmo H.G. & Hartwell J. (2005) Conservation and divergence of circadian clock operation in a stress-inducible Crassulacean acid metabolism species reveals clock compensation against stress. Plant Physiology 137, 969-982.
9. Carré I.A. (2002) ELF3: a circadian safeguard to buffer effects of light. Trends in Plant Science 7, 4-6.
10. Correia M.J., Pereira J.S., Chaves M.M., Rodrigues M.L. & Pacheco C.A. (1995) ABA xylem concentrations determine maximum daily leaf conductance in field-grown Vitis vinifera L. plants. Plant Cell and Environment 18, 511-521.
11. Covington M.F., Panda S., Liu X.L., Strayer C.A., Wagner D.R. & Kay S.A. (2001) ELF3 modulates resetting of the circadian clock in Arabidopsis. The Plant Cell 13, 1305-1315.
12. Devlin P.F. & Kay S.A. (2000) Cryptochromes are required for phytochrome signalling to the circadian clock but not for rhythmicity. The Plant Cell 12, 2499-2509.
13. Devlin P.F., Patel S.R. & Whitelam G.C. (1998) Phytochrome E influences internode elongation and flowering time in Arabidopsis. The Plant Cell 10, 1479-1487.
14. Devlin P.F., Robson P.R., Patel S.R., Goosey L., Sharrock R.A. & Whitelam G.C. (1999) Phytochrome D acts in the shadeavoidance syndrome in Arabidopsis by controlling elongation growth and flowering time. Plant Physiology 119, 909-915.
15. Dodd A.N., Parkinson K. & Webb A.A.R. (2004) Independent circadian regulation of assimilation and stomatal conductance in ztl-1 mutant of Arabidopsis. New Phytologist 162, 63-70.
16. 2+. Trends in Plant Science 10, 15-21.
17. Dodd A.N., Salathia N., Hall A., Kévei E., Tóoth R., Nagy F., Hibberd J.M., Millar A.J. & Webb A.A.R. (2005b) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309, 630-633.
18. 2+ signals in Arabidopsis. The Plant Journal 48, 962-973.
19. Dodge S.M., Marsh P.B. & Tallman G. (1992) Comparison of physiological responses of guard cell protoplasts of Nicotiana glauca isolated from leaves collected before dawn or at midday. Physiologia Plantarum 86, 221-230.
20. Dowson-Day M.J. & Millar A.J. (1999) Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. The Plant Journal 17, 63-71.
21. Doyle M.R., Davis S.J., Bastow R.M., McWatters H.G., Kozma-Bognár L., Nagy F., Millar A.J. & Amasino R.M. (2002) The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana. Nature 419, 74-77.
22. Dunlap J.C. (1999) Molecular bases for circadian clocks. Cell 96, 271-290.
23. Edwards K.D., Lynn J.R., Gyula P., Nagy F. & Millar A.J. (2005) Natural allelic variation in the temperature-compensation mechanisms of the Arabidopsis thaliana circadian clock. Genetics 170, 387-400.
24. Edwards K.D., Anderson P.E., Hall A., Salathia N.S., Locke J.C., Lynn J.R., Straume M., Smith J.Q. & Millar A.J. (2006) FLOWERING LOCUS C mediates natural variation in the high-temperature response of the Arabidopsis circadian clock. The Plant Cell 18, 639-650.
25. Evans N.H., McAinsh M.R. & Hetherington A.M. (2001) Calcium oscillations in higher plants. Current Opinion in Plant Biology 4, 415-420.
26. Farré E.M., Harmer S.L., Harmon F.G., Yanovsky M.J. & Kay S.A. (2005) Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Current Biology 15, 47-54.
27. Fowler S.G. & Thomashow M.G. (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. The Plant Cell 14, 1675-1690.
28. Fowler S.G., Cook D. & Thomashow M.G. (2005) Low temperature induction of Arabidopsis CBF1, 2 and 3 is gated by the circadian clock. Plant Physiology 137, 961-968.
29. Franklin K.A. & Whitelam G.C. (2005) Phytochromes and shade-avoidance responses in plants. Annals of Botany 96, 169-175.
30. Frechilla S., Zhu J., Talbott L.D. & Zeiger E. (1999) Stomata from npq1, a zeaxanthin-less Arabidopsis mutant, lack a specific response to blue light. Plant and Cell Physiology 40, 949-954.
31. Gaal T.V. & Erwin J.E. (2005) Diurnal variation in thigmotropic inhibition of stem elongation. HortTechnology 15, 291-294.
32. 2+ signalling. In Endogenous Plant Rhythms. Annual Plant Reviews 21 (eds A. Hall & H. McWatters), pp. 191-209. Blackwell Publishing, Oxford, UK.
33. Gardner M.J., Hubbard K.E., Hotta C.T., Dodd A.N. & Webb A.A.R. (2006) How plants tell the time. Biochemical Journal 397, 15-24.
34. Gilmour S.J., Sebolt A.M., Salazar M.P., Everard J.D. & Thomashow M.F. (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiology 124, 1854-1865.
35. Gorton H.L., Williams W.E., Binns M.E., Gemmell C.N., Leheny E.A. & Shepherd A.C. (1989) Circadian stomatal rhythms in epidermal peels from Vicia faba. Plant Physiology 90, 1329-1334.
36. Gorton H.L., Williams W.E. & Assman S.M. (1993) Circadian rhythms in stomatal responsiveness to red and blue light. Plant Physiology 103, 399-406.
37. Gould P.D., Locke J.C., Larue C., et al. (2006) The molecular basis of temperature compensation in the Arabidopsis circadian clock. The Plant Cell 18, 1177-1187.
38. Green R.M., Tingay S., Wang Z.Y. & Tobin E.M. (2002) Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiology 129, 576-584.
39. Hall A., Bastow R.M., Davis S.J., et al. (2003) The TIME FOR COFFEE genemaintains the amplitude and timing of Arabidopsis circadian clocks. The Plant Cell 15, 2719-2729.
40. Harmer S.L. & Kay S.A. (2005) Positive and negative factors confer phase-specific circadian regulation of transcription in Arabidopsis. The Plant Cell 17, 1926-1940.
41. Harmer S.L., Hogenesch J.B., Straume M., Chang H.S., Han B., Zhu T., Wang X., Kreps J.A. & Kay S.A. (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110-2113.
42. Harmer S.L., Panda S. & Kay S.A. (2001) Molecular bases of circadian rhythms. Annual Review of Cell and Developmental Biology 17, 215-253.
43. Hartwell J. (2005) The co-ordination of central plant metabolism by the circadian clock. Biochemical Society Transactions 33, 945-948.
44. Hayama R. & Coupland G. (2004) The molecular basis of diversity in the photoperiodic flowering responses of Arabidopsis and rice. Plant Physiology 135, 677-684.
45. Hazen S.P., Schultz T.F., Pruneda-Paz J.L., Borevitz J.O., Ecker J.R. & Kay S.A. (2005) LUXARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proceedings of the National Academy of Sciences of the United States of America 102, 10387-10392.
46. Heath O.V.S. (1984) Stomatal opening in darkness in the leaves of Commelina communis, attributed to an endogenous circadian rhythm: control of phase. Proceedings of the Royal Society of London. Series B. Biological Sciences 220, 399-414.
47. Hennessey T.L. & Field C.B. (1991) Circadian rhythms in photosynthesis: oscillations in carbon assimilation and stomatal conductance under constant conditions. Plant Physiology 96, 831-836.
48. Hennessey T.L. & Field C.B. (1992) Evidence of multiple circadian oscillators in bean plants. Journal of Biological Rhythms 7, 105-113.
49. Hennessey T.L., Freeden A.L. & Field C.B. (1993) Environmental effects on circadian rhythms of photosynthesis and stomatal opening. Planta 189, 369-376.
50. 2+ levels. Plant Cell and Environment 26, 485-496.
51. 2+ signals in plants. Annual Review of Plant Biology 55, 401-427.
52. Hetherington A.M. & Woodward F.I. (2003) The role of stomata in sensing and driving environmental change. Nature 424, 901-908.
53. Hicks K.A., Millar A.J., Carré I.A., Somers D.E., Straume M., Meeks-Wagner D.R. & Kay S.A. (1996) Conditional circadian dysfunction of the Arabidopsis early-flowering 3 mutant. Science 274, 790-792.
54. Hicks K.A., Albertson T.M. & Wagner D.R. (2001) EARLY FLOWERING 3 encodes a novel protein that regulates circadian clock function and flowering in Arabidopsis. The Plant Cell 13, 1281-1292.
55. Highkin H.R. & Hanson J.B. (1954) Possible interaction between light-dark cycles and endogenous daily rhythms on the growth of tomato plants. Plant Physiology 29, 301-302.
56. Holmes M.G. & Klein W.H. (1986) Photocontrol of dark circadian rhythms in stomata of Phaseolus vulgaris L. Plant Physiology 82, 28-33.
57. Hwang I., Chen H.C. & Sheen J. (2002) Two-component signal transduction pathways in Arabidopsis. Plant Physiology 129, 500-515.
58. Imaizumi T., Tran H.G., Swartz T.E., Briggs W.R. & Kay S.A. (2003) FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426, 302-306.
59. Imaizumi T., Schultz T.F., Harmon F.G., Ho L.A. & Kay S.A. (2005) FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309, 293-297.
60. Ishikawa M., Kiba T. & Chua N.H. (2006) The Arabidopsis SPA1 gene is required for circadian clock function and photoperiodic flowering. The Plant Journal 46, 736-746.
61. Johnson C.H., Knight M.R., Kondo T., Masson P., Sedbrook J., Haley A. & Trewavas A. (1995) Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science 269, 1863-1865.
62. Karlsson E. (1988) Phytochrome is not involved in the red light-enhancement of the stomatal blue light-response in wheat seedlings. Physiologia Plantarum 74, 544-548.
63. Kasuga M., Liu Q., Miura S., Yamaguchi-Shinozaki K. & Shinozaki K. (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nature Biotechnology 17, 287-291.
64. Kevei É., Gyula P., Hall A., et al. (2006) Forward genetic analysis of the circadian clock separates the multiple functions of ZEITLUPE. Plant Physiology 140, 933-945.
65. Kikis E.A., Khanna R. & Quail P.H. (2005) ELF4 is a phytochrome-regulated component of a negative feedback loop involving the central oscillator components CCA1 and LHY. The Plant Journal 44, 300-313.
66. Kim J.Y., Song H.R., Taylor B.L. & Carré I.A. (2003) Lightregulated translation mediates gated induction of the Arabidopsis clock protein LHY. EMBO Journal 22, 935-944.
67. Kinoshita T., Doi M., Suetsugu N., Kagawa T., Wada M. & Shimazaki K. (2001) phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414, 656-660.
68. Kinoshita T., Emi T., Tominaga M., Sakamoto K., Shigenaga A., Doi M. & Shimazaki K. (2003) Blue-light- and phosphorylation-dependent binding of a 14-3-3 protein to phototropins in stomatal guard cells of broad bean. Plant Physiology 133, 1453-1463.
69. Klein R.M. (1992) Effects of green light on biological systems. Biological Reviews of the Cambridge Philosophical Society 67, 199-284.
70. Knight M.R., Campbell A.K., Smith S.M. & Trewavas A.J. (1991) Transgenic plant aequorin reports the effects of touch and coldshock and elicitors on cytoplasmic calcium. Nature 352, 524-526.
71. Kreps J.A., Wu Y., Chang H.S., Zhu T., Wang X. & Harper J.F. (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiology 130, 2129-2141.
72. Landry L.G., Chapple C.C. & Last R.L. (1995) Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiology 109, 1159-1166.
73. Liu Q., Kasuga M., Sakuma Y., Abe H., Miura S., Yamaguchi-Shinozaki K. & Shinozaki K. (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. The Plant Cell 10, 1391-1406.
74. Liu X.L., Covington M.F., Fankhauser C., Chory J. & Wagner D.R. (2001) ELF3 encodes a circadian clock-regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. The Plant Cell 13, 1293-1304.
75. Locke J.C.W., Millar A.J. & Turner M.S. (2005a) Modelling genetic networks with noisy and varied experimental data: the circadian clock in Arabidopsis thaliana. Journal of Theoretical Biology 234, 383-393.
76. Locke J.C.W., Southern M.M., Kozma-Bognár L., Hibberd V., Brown P.E., Turner M.S. & Millar A.J. (2005b) Extension of a genetic network model by iterative experimentation and mathematical analysis. Molecular Systems Biology 1, E1-E9.
77. Locke J.C.W., Kozma-Bognár L., Gould P.D., Fehér B., Kevei É., Nagy F., Turner M.S., Hall A. & Millar A.J. (2006) Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Molecular Systems Biology 2, 59.
78. Love J., Dodd A.N. & Webb A.A.R. (2004) Circadian and diurnal calcium oscillations encode photoperiodic information in Arabidopsis. The Plant Cell 16, 956-966.
79. Ma L., Zhao H. & Deng X.W. (2003) Analysis of the mutational effects of the COP/DET/FUS loci on genome expression profiles reveals their overlapping yet not identical roles in regulating Arabidopsis seedling development. Development 130, 969-981.
80. Martin E.S. & Meidner H. (1971) Endogenous stomatal movements in Tradescantia virginiana. New Phytologist 70, 923-928.
81. Martin E.S. & Meidner H. (1972) The phase-response of the dark stomatal rhythm in Tradescantia virginiana to light and dark treatment. New Phytologist 71, 1045-1054.
82. Martínez-Garcia J.F., Huq E. & Quail P.H. (2000) Direct targeting of light signals to a promoter element-bound transcription factor. Science 288, 859-863.
83. Maruyama K., Sakuma Y., Kasuga M., Ito Y., Seki M., Goda H., Shimada Y., Yoshida S., Shinozaki K. & Yamaguchi-Shinozaki K. (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. The Plant Journal 38, 982-993.
84. Más P. (2005) Circadian clock signalling in Arabidopsis thaliana: from gene expression to physiology and development. International Journal of Development Biology 49, 491-500.
85. Más P., Alabadí D., Yanovsky M.J., Oyama T. & Kay S.A. (2003a) Dual role of TOC1 in the control of circadian and photomorphogenic responses in Arabidopsis. The Plant Cell 15, 223-236.
86. Más P., Kim W.Y., Somers D.E. & Kay S.A. (2003b) Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426, 567-570.
87. Matsushika A., Makino S., Kojima M. & Mizuno T. (2000) Circadian waves of expression of the APRR1/TOC1 family of pseudoresponse regulators in Arabidopsis thaliana: insight into the plant circadian clock. Plant Cell and Physiology 41, 1002-1012.
88. McClung C.R. (2006) Plant circadian rhythms. The Plant Cell 18, 992-803.
89. McWatters H.G., Bastow R.M., Hall A. & Millar A.J. (2000) The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature 408, 716-720.
90. Michael T.P. & McClung C.R. (2002) Phase-specific circadian clock regulatory elements in Arabidopsis. Plant Physiology 130, 627-638.
91. Michael T.P., Salomé P.A. & McClung C.R. (2003a) Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity. Proceedings of the National Academy of Sciences of the United States of America 100, 6878-6883.
92. Michael T.P., Salomé P.A., Yu H.J., Spencer T.R., Sharp E.L., McPeek M.A., Alonso J.M., Ecker J.R. & McClung C.R. (2003b) Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302, 1049-1053.
93. Millar A.J. (2004) Input signals to the plant circadian clock. Journal of Experimental Botany 55, 277-283.
94. Millar A.J. & Kay S.A. (1996) Integration of circadian and phototransduction pathways in the network controlling CAB gene transcription in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 93, 15491-15496.
95. Millar A.J., Carré I.A., Strayer C.A., Chua N.H. & Kay S.A. (1995a) Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science 267, 1161-1163.
96. Millar A.J., Straume M., Chory J., Chua N.H. & Kay S.A. (1995b) The regulation of circadian period by phototransduction pathways in Arabidopsis. Science 267, 1163-1166.
97. Mizoguchi T., Wheatley K., Hanzawa Y., Wright L., Mizoguchi M., Song H.R., Carré I.A. & Coupland G. (2002) LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Developmental Cell 2, 629-641.
98. Mizoguchi T., Wright L., Fujiwara S., et al. (2005) Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. The Plant Cell 17, 2255-2270.
99. Mizuno T. & Nakamichi N. (2005) Pseudo-Response Regulators (PRRs) or True Oscillator Components (TOCs). Plant and Cell Physiology 46, 677-685.
100. Monte E., Tepperman J.M., Al-Sady B., Kaczorowski K.A., Alonso J.M., Ecker J.R., Li X., Zhang Y. & Quail P.H. (2004) The phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development. Proceedings of the National Academy of Sciences of the United States of America 101, 16091-16098.
101. Nakamichi N., Kita M., Ito S., Yamashino T. & Mizuno T. (2005a) The Arabidopsis pseudo-response regulators, PRR5 and PRR7, coordinately play essential roles for circadian clock function. Plant and Cell Physiology 46, 609-619.
102. Nakamichi N., Kita M., Ito S., Yamashino T. & Mizuno T. (2005b) PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant and Cell Physiology 46, 686-698.
103. Nelson D.C., Lasswell J., Rogg L.E., Cohen M.A. & Bartel B. (2000) FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101, 331-340.
104. Ni M., Tepperman J.M. & Quail P.H. (1998) PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel helix-loop-helix protein. Cell 95, 657-667.
105. Ni M., Tepperman J.M. & Quail P.H. (1999) Binding of phytochrome B to its signal partner PIF3 is reversibly induced by light. Nature 400, 781-784.
106. Oda A., Fujiwara S., Kamada H., Coupland G. & Mizoguchi T. (2004) Antisense suppression of the Arabidopsis PIF3 gene does not affect circadian rhythms but causes early flowering and increases FT expression. FEBS Letters 557, 259-264.
107. Onai K. & Ishiura M. (2005) PHYTOCLOCK1 encoding a novel GARP protein essential for the Arabidopsis circadian clock. Genes to Cells 10, 963-972.
108. Ouyang Y., Andersson C.R., Kondo T., Golden S.S. & Johnson C.H. (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proceedings of the National Academy of Sciences of the United States of America 95, 8660-8664.
109. Panda S., Poirier G.G. & Kay S.A. (2002) tej defines a role for poly(ADP-ribosyl)ation in establishing period length of the Arabidopsis circadian oscillator. Development Cell 3, 51-61.
110. Pastenes C., Pimentel P. & Lillo J. (2005) Leaf movements and photoinhibition in relation to water stress in field-grown beans. Journal of Experimental Botany 56, 425-433.
111. Piechulla B., Merforth N. & Rudolph B. (1998) Identification of tomato Lhc promoter regions necessary for circadian expression. Plant Molecular Biology 38, 655-662.
112. Pittendrigh C.S. (1993) Temporal organization: reflections of a Darwinian clock-watcher. Annual Review of Physiology 55, 16-54.
113. Plieth C. (1999) Temperature sensing by plants: calcium-permeable channels as primary sensors - a model. Journal of Membrane Biology 172, 121-127.
114. Prombona A. & Argyroudi-Akoyunoglou J. (2004) Diverse signals synchronize the circadian clock controlling the oscillations in chlorophyll content of etiolated Phaseolus vulgaris leaves. Plant Science 167, 117-127.
115. Reed J.W., Nagpal P., Bastow R.M., Solomon K.S., Dowson-Day M.J., Elumalai R.P. & Millar A.J. (2000) Independent action of ELF3 and PHYB to control hypocotyl elongation and flowering time. Plant Physiology 122, 1149-1160.
116. Roden L.C., Song H.R., Jackson S., Morris K. & Carré I.A. (2002) Floral responses to photoperiod are correlated with the timing of rhythmic expression relative to dawn and dusk in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 99, 13313-13318.
117. Roennenberg T., Daan S. & Merrow M. (2002) The art of entrainment. Journal of Biological Rhythms 18, 183-194.
118. Salomé P.A. & McClung C.R. (2005a) PSEUDO-RESPONSE REGULATOR 7 and 9 are partially redundant genes essential for temperature responsiveness of the Arabidopsis circadian clock. The Plant Cell 17, 791-803.
119. Salomé P.A. & McClung C.R. (2005b) What makes the Arabidopsis clock tick on time? A review on entrainment. Plant Cell and Environment 28, 21-38.
120. Salomé P.A., To J.P., Kieber J.J. & McClung C.R. (2006) Arabidopsis response regulators ARR3 and ARR4 play cytokininin-dependent roles in the control of circadian period. The Plant Cell 18, 55-69.
121. Salter M.G., Franklin K.A. & Whitelam G.C. (2003) Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature 426, 680-683.
122. Samach A., Onouchi H., Gold S.E., Ditta G.S., Schwarz-Sommer Z., Yanofsky M.F. & Coupland G. (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288, 1600-1602.
123. Schaffer R., Ramsay N., Samach A., Corden S., Putterill J., Carré I.A. & Coupland G. (1998) The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93, 1219-1229.
124. Schaffer R., Landgraf J., Accerbi M., Simon V., Larson M. & Wisman E. (2001) Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. The Plant Cell 13, 113-123.
125. Schmitt J., Stinchcombe J.R., Heschel M.S. & Huber H. (2003) The adaptative evolution of plasticity: phytochrome-mediated shade avoidance responses. Integrative and Comparative Biology 43, 459-469.
126. Schultz T.F., Kiyosue T., Yanovsky M., Wada M. & Kay S.A. (2001) A role for LKP2 in the circadian clock of Arabidopsis. The Plant Cell 13, 2659-2670.
127. Sharrock R.A. & Clack T. (2002) Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiology 130, 442-456.
128. Smith H. (1982) Light quality, photoreception and plant strategy. Annual Review of Plant Physiology 22, 481-518.
129. Snaith P.J. & Mansfield T.A. (1985) Responses of the stomata to IAA and fusicoccin at the opposite phases of an entrained rhythm. Journal of Experimental Botany 36, 937-944.
130. Snaith P.J. & Mansfield T.A. (1986) The circadian rhythm of stomatal opening: evidence for the involvement of potassium and chloride fluxes. Journal of Experimental Botany 37, 188-199.
131. Somers D.E. (2005) Entrainment of the circadian clock. In Endogenous Plant Rhythms. Annual Plant Reviews 21 (eds A. Hall & H. McWatters), pp. 85-105. Blackwell Publishing, Oxford, UK.
132. Somers D.E., Devlin P. & Kay S.A. (1998a) Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science 282, 1488-1490.
133. Somers D.E., Webb A.A.R., Pearson M. & Kay S.A. (1998b) The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. Development 125, 485-494.
134. Somers D.E., Schultz T.F., Milnamow M. & Kay S.A. (2000) ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 101, 319-329.
135. Song H.R. & Carré I.A. (2005) DET1 regulates the proteasomal degradation of LHY, a component of the Arabidopsis circadian clock. Plant Molecular Biology 57, 761-771.
136. Staiger D., Allenbach L., Salathia N., Fiechter V., Davis S.J., Millar A.J., Chory J. & Fankhauser C. (2003) The Arabidopsis SRR1 gene mediates PHYB signalling and is required for normal circadian clock function. Genes & Development 17, 256-268.
137. Stålfelt M.G. (1963) Diurnal dark reactions in the stomatal movements. Physiologia Plantarum 16, 756-766.
138. Strayer C., Oyama T., Schultz T.F., Raman R., Somers D.E., Más P., Panda S., Kreps J.A. & Kay S.A. (2000) Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289, 768-771.
139. Suárez-López P., Wheatley K., Robson F., Onouchi H., Valverde F. & Coupland G. (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 26, 1116-1120.
140. Talbott L.D., Shmayevich I.J., Chung Y., Hammad J.W. & Zeiger E. (2003) Blue light and phytochrome-mediated stomatal opening in the npq1 and phot1 phot2 mutants of Arabidopsis. Plant Physiology 133, 1522-1529.
141. Talbott L.D., Hammad J.W., Harn L.C., Nguyen V.H., 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 and Physiology 47, 332-339.
142. Thomas B. (1998) Photoperiodism: an overview. In Biological Rhythms and Photoperiodism in Plants (eds P.J. Lumsden & A.J. Millar), pp. 151-165. Bios Scientific Publications, Oxford, UK.
143. Tóth R., Kevei E., Hall A., Millar A.J., Nagy F. & Kozma-Bognár L. (2001) Circadian clock-regulated expression of phytochrome and cryptochrome genes in Arabidopsis. Plant Physiology 127, 1607-1616.
144. Valverde F., Mouradov A., Soppe W., Ravenscroft D., Samach A. & Coupland G. (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303, 1003-1006.
145. Viczián A., Kircher S., Fejes E., Millar A.J., Schäfer E., Kozma-Bognár L. & Nagy F. (2005) Functional characterization of phytochrome interacting factor 3 for the Arabidopsis thaliana circadian clockwork. Plant and Cell Physiology 46, 1591-1602.
146. Viswanathan C. & Zhu J.K. (2002) Molecular genetic analysis of cold-regulated gene transcription. Philosophical Transactions of the Royal Society of London B: Biological Sciences 357, 877-886.
147. Vogel J.T., Zarka D.G., Van Buskirk H.A., Fowler S.G. & Thomashow M.F. (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. The Plant Journal 41, 195-211.
148. Wang Z.Y. & Tobin E.M. (1998) Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93, 1207-1217.
149. Wang Z.Y., Kenigsbuch D., Sun L., Harel E., Ong M.S. & Tobin E.M. (1997) A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. The Plant Cell 9, 491-507.
150. Webb A.A.R. (1998) Stomatal rhythms. In Biological Rhythms and Photoperiodism in Plants (eds P.J. Lumsden & A.J. Millar), pp. 66-79. Bios Scientific Publications, Oxford, UK.
151. Webb A.A.R. (2003) The physiology of circadian rhythms in plants. New Phytologist 160, 281-303.
152. Withrow A.P. & Withrow R. (1949) Photoperiodic chlorosis in tomato. Plant Physiology 24, 657-663.
153. Woelfle M.A., Ouyang Y., Phanvijhitsiri K. & Johnson C.H. (2004) The adaptive value of circadian clocks: an experimental assessment in cyanobacteria. Current Biology 14, 1481-1486.
154. Wood N.T., Haley A., Viry-Moussaid M., Johnson C.H., van der Luit A.H. & Trewavas A.J. (2001) The calcium rhythms of different cell types oscillate with different circadian phases. Plant Physiology 125, 787-796.
155. Wu Y., Sanchez J.P., Lopez-Molina L., Himmelbach A., Grill E. & Chua N.H. (2003) The abi1-1 mutation blocks ABA signalling downstream of cADPR action. Plant Journal 34, 307-315.
156. Yamashino T., Matsushika A., Fujimori T., Sato S., Kato T., Tabata S. & Mizuno T. (2003) A Link between circadian-controlled bHLH factors and the APRR1/TOC1 quintet in Arabidopsis thaliana. Plant and Cell Physiology 44, 619-629.
157. Yanovsky M.J. & Kay S.A. (2002) Molecular basis of seasonal time measurement in Arabidopsis. Nature 419, 308-312.
158. Yanovsky M.J., Mazzella M.A., Whitelam G.C. & Casal J.J. (2001) Resetting of the circadian clock by phytochromes and crypto chromes in Arabidopsis. Journal of Biological Rhythms 16, 523-530.
159. Young M.W. & Kay S.A. (2001) Time zones: a comparative genetics of circadian clocks. Nature Reviews Genetics 2, 702-715.
160. Zarka D.G., Vogel J.T., Cook D. & Thomashow M.F. (2003) Cold induction of Arabidopsis CBF genes involves multiple ICE (inducer of CBF expression) promoter elements and a coldregulatory circuit that is desensitized by low temperature. Plant Physiology 133, 910-918.
161. Zeilinger M.N., Farré E.M., Taylor S.R., Kay S.A. & Doyle F.J. (2006) A novel computational model of the circadian clock in Arabidopsis that incorporates PRR7 and PRR9. Molecular Systems Biology 2, 58.