A comparison of high-throughput techniques for assaying circadian rhythms in plants

Plant Methods

Volumn 11, Issue 1, 2015, Pages

  Tindall, Andrew J ^a   Waller, Jade ^a   Greenwood, Mark ^a   Gould, Peter D ^a   Hartwell, James ^a   Hall, Anthony ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Circadian clock; Delayed fluorescence; High throughput assay; Infra red gas exchange; Leaf movement; Luciferase

Indexed keywords

EID: 84939255533     PISSN: None     EISSN: 17464811     Source Type: Journal    
DOI: 10.1186/s13007-015-0071-9     Document Type: Review

References (89)

1. Wijnen H, Young MW. Interplay of circadian clocks and metabolic rhythms. Annu Rev Genet. 2006; 40:409-8.
2. McClung CR. Beyond Arabidopsis: the circadian clock in non-model plant species. Semin Cell Dev Biol. 2013; 24(5):430-6.
3. Harmer SL. The circadian system in higher plants. Annu Rev Plant Biol. 2009; 60:357-77.
4. Covington MF, Maloof JN, Straume M, Kay Sa, Harmer SL. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol. 2008; 9(8):130.
5. Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature. 2001; 410(6832):1116-20.
6. Roden LC, Ingle RA. Lights, rhythms, infection: the role of light and the circadian clock in determining the outcome of plant-pathogen interactions. Plant Cell. 2009; 21(9):2546-52.
7. Wang W, Barnaby JY, Tada Y, Li H, Tör M, Caldelari D, et al. Timing of plant immune responses by a central circadian regulator. Nature. 2011; 470(7332):110-4.
8. Zhang C, Xie Q, Anderson RG, Ng G, Seitz NC, Peterson T, et al. Crosstalk between the circadian clock and innate immunity in Arabidopsis. PLoS Pathog. 2013; 9(6):e1003370.
9. Dunford RP, Yano M, Kurata N, Sasaki T, Huestis G, Rocheford T, et al. Comparative mapping of the barley Ppd-H1 photoperiod response gene region, which lies close to a junction between two rice linkage segments. Genetics. 2002; 161(2):825-34.
10. Turner A, Beales J, Faure S, Dunford RP, Laurie DA. The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science. 2005; 310(5750):1031-34.
11. Mockler TC, Michael TP, Priest HD, Shen R, Sullivan CM, Givan SA, et al. The diurnal project: Diurnal and circadian expression profiling, model-based pattern matching, and promoter analysis. Cold Spring Harbor Symposia Quantitative Biol. 2007; 72:353-63.
12. Shaw LM, Turner AS, Laurie DA. The impact of photoperiod insensitive Ppd-1a mutations on the photoperiod pathway across the three genomes of hexaploid wheat (Triticum aestivum). Plant J. 2007; 71:71-84.
13. Kloosterman B, Abelenda JA, Gomez MDMC, Oortwijn M, de Boer JM, Kowitwanich K, et al. Naturally occurring allele diversity allows potato cultivation in northern latitudes. Nature. 2013; 495:246-50.
14. Filichkin SA, Breton G, Priest HD, Dharmawardhana P, Jaiswal P, Fox SE, et al. Global profiling of rice and poplar transcriptomes highlights key conserved Circadian-controlled pathways and cis-regulatory modules. PLoS One. 2011; 6(6):16907.
15. Preuss SB, Meister R, Xu Q, Urwin CP, Tripodi Fa, Screen SE, et al. Expression of the Arabidopsis thaliana BBX32 gene in soybean increases grain yield. PLoS One. 2012; 7(2):30717.
16. McClung CR. The genetics of plant clocks. Adv Genet. 2011; 74:105-39.
17. Pruneda-Paz JL, Kay Sa. An expanding universe of circadian networks in higher plants. Trends Plant Sci. 2010; 15(5):259-65.
18. Alabadí D, Oyama T, Yanovsky MJ, Harmon FG, Más P, Kay SA. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science. 2001; 293(5531):880-3.
19. Locke JCW, Millar AJ, Turner MS. Modelling genetic networks with noisy and varied experimental data: the circadian clock in Arabidopsis thaliana. J Theor Bio. 2005; 234(3):383-93.
20. Locke JCW, Kozma-Bognár L, Gould PD, Fehér B, Kevei E, Nagy F, et al. Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol Syst Biol. 2006; 2:59.
21. Salomé PA, McClung CR. PSEUDO-RESPONSE REGULATOR 7 and 9 are partially redundant genes essential for the temperature responsiveness of the Arabidopsis circadian clock. Plant Cell. 2005; 17(3):791-803.
22. Kim WY, Fujiwara S, Suh SS, Kim J, Kim Y, Han L, et al. ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature. 2007; 449(7160):356-60.
23. Pokhilko A, Hodge SK, Stratford K, Knox K, Edwards KD, Thomson AW, et al. Data assimilation constrains new connections and components in a complex, eukaryotic circadian clock model. Mol Syst Biol. 2010; 6:416.
24. Pruneda-Paz JL, Breton G, Para A, Kay SA. A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock. Science. 2009; 323(5920):1481-5.
25. Michael TP, McClung CR. Enhancer trapping reveals widespread circadian clock transcriptional control in Arabidopsis. Plant Physiol. 2003; 132:629-39.
26. Yakir E, Hilman D, Harir Y, Green RM. Regulation of output from the plant circadian clock. FEBS J. 2007; 274(2):335-45.
27. Somers DE, Devlin PF, Kay SA. Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science. 1998; 282(5393):1488-90.
28. Devlin PF, Kay SA. Cryptochromes are required for phytochrome signaling to the circadian clock but not for rhythmicity. Plant Cell. 2000; 12(12):2499-510.
29. Gould PD, Locke JCW, Larue C, Southern MM, Davis SJ, Hanano S, et al. The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant Cell. 2006; 18(5):1177-87.
30. Hanano S, Domagalska MA, Nagy F, Davis SJ. Multiple phytohormones influence distinct parameters of the plant circadian clock. Genes Cells. 2006; 11(12):1381-92.
31. Wang ZY, Tobin EM. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell. 1998; 93(7):1207-17.
32. Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carré IA, et al. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell. 1998; 93(7):1219-29.
33. Schaffer R, Landgraf J, Accerbi M, Simon V, Larson M, Wisman E. Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell. 2001; 13(1):113-23.
34. Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, Fox SE, et al. Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res. 2010; 20(1):45-58.
35. Millar AJ, Short SR, Hiratsuka K, Chua NH, Kay Sa. Firefly luciferase as a reporter of regulated gene expression in higher plants. Genome Res. 1992; 10(14):324-37.
36. Southern MM, Brown PE, Hall A. Luciferases as Reporter Genes. In: Arabidopsis Methods, vol. 323: 2006. p. 293-305.
37. Sherf BA, Wood KV. Firefly Luciferase Engineered for Improved Genetic Reporting. Promega Notes Mag. 1994; 49:14-21.
38. Millar A, Kay S. Circadian control of cab gene transcription and mRNA accumulation in Arabidopsis. Plant Cell. 1991; 3(5):541-50.
39. Millar AJ, Straume M, Chory J, Chua NH, Kay SA. The regulation of circadian period by phototransduction pathways in Arabidopsis. Science. 1995; 267(5201):1163-6.
40. Hall A, Brown P. Monitoring circadian rhythms in Arabidopsis thaliana using luciferase reporter genes. Methods Mol Biol. 2007; 362:143-52.
41. Millar AJ, Carré IA, Strayer CA, Chua NH, Kay SA. Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science. 1995; 267(5201):1161-3.
42. Thines B, Harmon FG. Ambient temperature response establishes ELF3 as a required component of the core Arabidopsis circadian clock. Proc Natl Acad Sci U S A. 2010; 107(7):3257-62.
43. Kusakina J, Gould PD, Hall A. A fast circadian clock at high temperatures is a conserved feature across Arabidopsis accessions and likely to be important for vegetative yield. Plant Cell Environ. 2014; 37:327-40.
44. Nagel DH, Pruneda-Paz JL, Kay Sa. FBH1 affects warm temperature responses in the Arabidopsis circadian clock. Proc Natl Acad Sci U S A. 2014; 111:14595-600.
45. Dalchau N, Baek SJ, Briggs HM, Robertson FC, Dodd AN, Gardner MJ, et al. The circadian oscillator gene GIGANTEA mediates a long-term response of the Arabidopsis thaliana circadian clock to sucrose. Proc Natl Acad Sci U S A. 2011; 108(12):5104-9.
46. Muranaka T, Kubota S, Oyama T. A single-cell bioluminescence imaging system for monitoring cellular gene expression in a plant body. Plant Cell Physiol. 2013; 54(12):2085-93.
47. Endo M, Shimizu H, Nohales MA, Araki T, Kay SA. Tissue-specific clocks in Arabidopsis show asymmetric coupling. Nature. 2014; 515(7527):419-22.
48. Sugiyama N, Izawa T, Oikawa T. Light regulation of circadian clock-controlled gene expression in rice. Plant J. 2001; 26(6):607-15.
49. Belhaj K, Chaparro-Garcia A, Kamoun S, Nekrasov V. Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Med. 2013; 9(1):39.
50. Strehler BL, Arnold W. Light Production By Green Plants. J Gen Physiol. 1951; 34(6):809-20.
51. Rutherford AW, Govindjee, Inoue Y. Charge accumulation and photochemistry in leaves studied by thermoluminescence and delayed light emission. Proc Natl Acad Sci U S A. 1984; 81(4):1107-11.
52. Arnold W, Davidson JB. The identity of the fluorescent and delayed light emission spectra in Chlorella. J Gen Physiol. 1954; 37(5):677-84.
53. Jursinic PA. Delayed fluorescence: current concepts and status In: Govindjee Amesz J, Fork DC, editors. Light Emission by Plants and Bacteria. New York: Academic Press: 1986. p. 291-328.
54. Van Wijk R, Scordino A, Triglia A, Musumeci F. 'Simultaneous' measurements of delayed luminescence and chloroplast organization in Acetabularia acetabulum. J Photochem Photobiol B. 1999; 49(2-3):142-9.
55. Blankenship RE. Molecular Mechanisms of Photosynthesis. Oxford: Blackwell Science Ltd; 2002.
56. Goltsev V, Zaharieva I, Lambrev P, Yordanov I, Strasser R. Simultaneous analysis of prompt and delayed chlorophyll a fluorescence in leaves during the induction period of dark to light adaptation. J Theor Biol. 2003; 225(2):171-83.
57. Berden-zrimec M, Drinovec L, Zrimec A. Delayed Fluoresence In: Suggett DJ, Prášil O, Borowitzka MA, editors. Chlorophyll a fluorescence in aquatic sciences: methods and applications. Dordrecht: Springer: 2011. p. 293-309.
58. Gould PD, Diaz P, Hogben C, Kusakina J, Salem R, Hartwell J, et al. Delayed fluorescence as a universal tool for the measurement of circadian rhythms in higher plants. Plant J. 2009; 58(5):893-901.
59. Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, et al. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science. 2000; 290(5499):2110-3.
60. Gawronski P, Ariyadasa R, Himmelbach A, Poursarebani N, Kilian B, Stein N, et al. Genetics. 2014; 196(4):1253-61.
61. Gyllenstrand N, Karlgren A, Clapham D, Holm K, Hall A, Gould PD, et al. No time for spruce: Rapid dampening of circadian rhythms in picea abies (L. Karst). Plant Cell Physiol. 2014; 55(3):535-40.
62. Farré EM. The regulation of plant growth by the circadian clock. Plant Biol. 2012; 14(3):401-10.
63. Engelmann W, Johnsson A. Rhythms in Organ Movement In: Lumsden PJ, Millar AJ, editors. Biological rhythms and photoperiodism in plants. 1st ed. Oxford: BIOS Scientific Publishers: 1998. p. 35-48.
64. Dornbusch T, Michaud O, Xenarios I, Fankhauser C. Differentially phased leaf growth and movements in Arabidopsis depend on coordinated circadian and light regulation. Plant Cell. 2014; 26(10):3911-21.
65. d'Ortous De Mairan J-J. Hist Acad R Sci. 1792:35-6.
66. Dowson-Day MJ, Millar AJ. Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. Plant J. 1999; 17(1):63-71.
67. Edwards KD, Millar AJ. Analysis of circadian leaf movement rhythms in Arabidopsis thaliana. Methods Mol Biol. 2007; 362:103-13.
68. Kim JS, Nam HG. Instrumentation and software for analysis of Arabidopsis Circadian leaf movement. 2009. doi:10.4051/ibc.2009.1.0005.
69. Bours R, Muthuraman M, Bouwmeester H, van der Krol A. OSCILLATOR: A system for analysis of diurnal leaf growth using infrared photography combined with wavelet transformation. Plant Methods. 2012; 8(1):29.
70. Spoehr HA, McGee JM. Studies in Plant Respiration and Photosynthesis. Washington, DC: The Carnegie Institution of Washington; 1923.
71. Neeb CX. Hydrodictyon als Objekt einer vergleichenden Untersuchung physiologischer Grossen. Flora. 1952; 139:39-95.
72. Schon J. Periodische Schwankungen der Photosynthese und Atmung bei Hydrodictyon. Flora. 1955; 142:347-80.
73. Bohn A, Geist A, Rascher U, Lüttge U. Responses to different external light rhythms by the circadian rhythm of Crassulacean acid metabolism in Kalanchoe daigremontiana. Plant Cell Environ. 2001; 24:811-20.
74. Dever LV, Boxall SF, Kneřová J, Hartwell J. Transgenic perturbation of the decarboxylation phase of Crassulacean acid metabolism alters physiology and metabolism but has only a small effect on growth. Plant Physiol. 2014; 167:44-59.
75. Somers DE, Webb AA, Pearson M, Kay SA. The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. Development. 1998; 125(3):485-94.
76. Edwards KD, Akman OE, Knox K, Lumsden PJ, Thomson AW, Brown PE, et al. Quantitative analysis of regulatory flexibility under changing environmental conditions. Mol Syst Biol. 2010; 6(424):4.
77. Johnson BML, Frasier SG. Nonlinear Least Squares Analysis. Methods Enzymol. 1985; 117:301-42.
78. Martin S, Fraiser-Cadoret SG, Johnson ML, Vol. 2. Least-squares analysis of fluorescence data; 2002, pp. 177-240.
79. Burg JP. The relationship between maximum entropy and maximum likelihood spectra. Geophysics. 1972; 37(2):375-6.
80. Costa MJ, Finkenstädt B, Roche V, Lévi F, Gould PD, Foreman J, et al. Inference on periodicity of circadian time series. Biostatistics. 2013; 14(4):792-806.
81. Zielinski T, Moore AM, Troup E, Halliday KJ, Millar AJ. Strengths and limitations of period estimation methods for circadian data. PLoS One. 2014; 9(5):85754.
82. Shor E, Hassidim M, Green RM. The Use of Fluorescent Proteins to Analyze Circadian Rhythms In: Staiger D, editor. Plant circadian networks: methods & protocols. Methods in Molecular Biology. New York: Springer: 2014. p. 209-13. Chap. 14.
83. Yakir E, Hilman D, Kron I, Hassidim M, Melamed-Book N, Green RM. Posttranslational regulation of CIRCADIAN CLOCK ASSOCIATED1 in the circadian oscillator of Arabidopsis. Plant Physiol. 2009; 150(2):844-57.
84. Yakir E, Hassidim M, Melamed-Book N, Hilman D, Kron I, Green RM. Cell autonomous and cell-type specific circadian rhythms in Arabidopsis. Plant J. 2011; 68:520-31.
85. Thain SC, Hall A, Millar AJ. Functional independence of circadian clocks that regulate plant gene expression. Curr Biol. 2000; 10(16):951-6.
86. James AB, Monreal JA, Nimmo GA, Kelly CL, Herzyk P, Jenkins GI, et al. The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots. Science. 2008; 322(December):1832-5.
87. Wenden B, Kozma-Bognár Lo, Edwards KD, Hall AJW, Locke JCW, Millar AJ. Light inputs shape the Arabidopsis circadian system. Plant J. 2011; 66(3):480-91.
88. Fukuda H, Ukai K, Oyama T. Self-arrangement of cellular circadian rhythms through phase-resetting in plant roots. Phys Rev E Stat Nonlin Soft Matter Phys. 2012; 86(4):041917.
89. Rosato E. Circadian rhythms: methods and protocols vol. 362. New York: Springer; 2007.