Advertisement

Phytochromes pp 179-192 | Cite as

Measuring Phytochrome-Dependent Light Input to the Plant Circadian Clock

  • Rachael J. Oakenfull
  • James Ronald
  • Seth J. DavisEmail author
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 2026)

Abstract

The circadian clock allows plants to synchronize their internal processes with the external environment. This synchronization occurs through daily cues, one of which is light. Phytochromes are well established as light-sensing proteins and have been identified in forming multiple signaling networks with the central circadian oscillator. However, the precise details of how these networks are formed are yet to be established. Using established promoter-luciferase lines for clock genes crossed into mutant lines, it is possible to use luciferase-based imaging technologies to determine whether specific proteins are involved in phytochrome signaling to the circadian oscillator. The methods presented here use two automated methods of luciferase imaging in Arabidopsis to allow for high-throughput measurement of circadian clock components under a range of different light conditions.

Keywords

Circadian clock Phytochrome Arabidopsis Luciferase TopCount-luminescence measurement 

Notes

Acknowledgments

This work was supported by the Biotechnology and Biological Sciences Research Council (BBSRC) award number BB/N018540/1.

References

  1. 1.
    Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, Nagy F, Hibberd JM, Millar AJ, Webb AAR (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633CrossRefGoogle Scholar
  2. 2.
    Michael TP, Salomé PA, McClung CR (2003) Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity. Proc Natl Acad Sci U S A 100:6878–6883CrossRefGoogle Scholar
  3. 3.
    Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110–2113CrossRefGoogle Scholar
  4. 4.
    Habte E, Müller LM, Shtaya M, Davis SJ, Von Korff M (2014) Osmotic stress at the barley root affects expression of circadian clock genes in the shoot. Plant Cell Environ 37:1321–1337CrossRefGoogle Scholar
  5. 5.
    Nakamichi N, Kusano M, Fukushima A, Kita M, Ito S, Yamashino T, Saito K, Sakakibara H, Mizuno T (2009) Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant Cell Physiol 50:447–462CrossRefGoogle Scholar
  6. 6.
    Bujdoso N, Davis SJ (2013) Mathematical modeling of an oscillating gene circuit to unravel the circadian clock network of Arabidopsis thaliana. Front Plant Sci 4:3CrossRefGoogle Scholar
  7. 7.
    Michael TP, Salomé PA, Yu HJ, Spencer TR, Sharp EL, McPeek MA, Alonso JM, Ecker JR, McClung CR (2003) Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302:1049–1053CrossRefGoogle Scholar
  8. 8.
    Wenden B, Kozma-Bognár L, Edwards KD et al (2011) Light inputs shape the Arabidopsis circadian system. Plant J 66:480–491CrossRefGoogle Scholar
  9. 9.
    Edwards KD, Guerineau F, Devlin PF, Millar AJ (2015) Low-temperature-specific effects of PHYTOCHROME C on the circadian clock in Arabidopsis suggest that PHYC underlies natural variation in biological timing. bioRxivGoogle Scholar
  10. 10.
    Devlin PF, Kay SA (2000) Cryptochromes are required for phytochrome signaling to the circadian clock but not for rhythmicity. Plant Cell 12:2499–2510CrossRefGoogle Scholar
  11. 11.
    Sharrock RA, Quail PH (1989) Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution, and differential expression of a plant regulatory photoreceptor family. Genes Dev 3:1745–1757CrossRefGoogle Scholar
  12. 12.
    Mathews S, Sharrock RA (1997) Phytochrome gene diversity. Plant Cell Environ 20:666–671CrossRefGoogle Scholar
  13. 13.
    Somers DE, Devlin PF, Kay SA (1998) Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science 282:1488–1490CrossRefGoogle Scholar
  14. 14.
    Franklin KA, Davis SJ, Stoddart WM, Vierstra RD, Whitelam GC (2003) Mutant analyses define multiple roles for phytochrome C in Arabidopsis photomorphogenesis. Plant Cell 15:1981–1989CrossRefGoogle Scholar
  15. 15.
    Bognár LK, Hall A, Adám E, Thain SC, Nagy F, Millar AJ (1999) The circadian clock controls the expression pattern of the circadian input photoreceptor, phytochrome B. Proc Natl Acad Sci U S A 96:14652–14657CrossRefGoogle Scholar
  16. 16.
    Toth R, Kevei E, Hall A, Millar AJ, Nagy F, Kozma-Bognar L (2001) Circadian clock-regulated expression of phytochrome and cryptochrome genes in Arabidopsis. Plant Physiol 127:1607–1616CrossRefGoogle Scholar
  17. 17.
    Más P, Devlin PF, Panda S, Kay SA (2000) Functional interaction of phytochrome B and cryptochrome 2. Nature 408:207–211CrossRefGoogle Scholar
  18. 18.
    Millar AJ, Short SR, Chua NH, Kay SA (1992) A novel circadian phenotype based on firefly luciferase expression in transgenic plants. Plant Cell 4:1075–1087PubMedGoogle Scholar
  19. 19.
    Southern MM, Millar AJ (2005) Circadian genetics in the model higher plant, Arabidopsis thaliana. In: Young MW (ed) Methods in enzymology. Academic Press, Cambridge, MA, pp 23–35Google Scholar
  20. 20.
    Hall A, Brown P (2007) Monitoring circadian rhythms in Arabidopsis thaliana using luciferase reporter genes. In: Circadian rhythms. Humana Press, Totowa, NJ, pp 143–152Google Scholar
  21. 21.
    Millar AJ, Carré IA, Strayer CA, Chua NH, Kay SA (1995) Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science 267:1161–1163CrossRefGoogle Scholar
  22. 22.
    Darrah C, Taylor BL, Edwards KD, Brown PE, Hall A, McWatters HG (2006) Analysis of phase of LUCIFERASE expression reveals novel circadian quantitative trait loci in Arabidopsis. Plant Physiol 140:1464–1474CrossRefGoogle Scholar
  23. 23.
    Boikoglou E, Ma Z, von Korff M, Davis AM, Nagy F, Davis SJ (2011) Environmental memory from a circadian oscillator: the Arabidopsis thaliana clock differentially integrates perception of photic vs. thermal entrainment. Genetics 189:655–664CrossRefGoogle Scholar
  24. 24.
    Reed JW, Nagatani A, Elich TD, Fagan M, Chory J (1994) Phytochrome A and phytochrome B have overlapping but distinct functions in Arabidopsis development. Plant Physiol 104:1139–1149CrossRefGoogle Scholar
  25. 25.
    Chun L, Kawakami A, Christopher DA (2001) Phytochrome A mediates blue light and UV-A-dependent chloroplast gene transcription in green leaves. Plant Physiol 125:1957–1966CrossRefGoogle Scholar
  26. 26.
    Salter MG, Franklin KA, Whitelam GC (2003) Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature 426:680–683CrossRefGoogle Scholar
  27. 27.
    Genoud T, Millar AJ, Nishizawa N, Kay SA, Schäfer E, Nagatani A, Chua NH (1998) An Arabidopsis mutant hypersensitive to red and far-red light signals. Plant Cell 10:889–904CrossRefGoogle Scholar
  28. 28.
    Covington MF, Panda S, Liu XL, Strayer CA, Wagner DR, Kay SA (2001) ELF3 modulates resetting of the circadian clock in Arabidopsis. Plant Cell 13:1305–1315CrossRefGoogle Scholar
  29. 29.
    Kolmos E, Davis SJ (2007) ELF4 as a central gene in the circadian clock. Plant Signal Behav 2:370–372CrossRefGoogle Scholar
  30. 30.
    McWatters HG, Bastow RM, Hall A, Millar AJ (2000) The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature 408:716–720CrossRefGoogle Scholar
  31. 31.
    Thines B, Harmon FG (2010) Ambient temperature response establishes ELF3 as a required component of the core Arabidopsis circadian clock. Proc Natl Acad Sci U S A 107:3257–3262CrossRefGoogle Scholar
  32. 32.
    McClung CR, Davis SJ (2010) Ambient thermometers in plants: from physiological outputs towards mechanisms of thermal sensing. Curr Biol 20:R1086–R1092CrossRefGoogle Scholar
  33. 33.
    Anwer MU, Boikoglou E, Herrero E, Hallstein M, Davis AM, James GV, Nagy F, Davis SJ (2014) Natural variation reveals that intracellular distribution of ELF3 protein is associated with function in the circadian clock. elife 2014:e02206CrossRefGoogle Scholar
  34. 34.
    Rensing L, Ruoff P (2002) Temperature effect on entrainment, phase shifting, and amplitude of circadian clocks and its molecular bases. Chronobiol Int 19:807–864CrossRefGoogle Scholar
  35. 35.
    Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  36. 36.
    Bläsing OE, Gibon Y, Günther M, Höhne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible W-R, Stitt M (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17:3257–3281CrossRefGoogle Scholar
  37. 37.
    Hoagland D, Arnon D (1950) The water-culture method for growing plants without soil. Circular California Agricultural Experiment Station 347:1–32Google Scholar
  38. 38.
    Hanano S, Stracke R, Jakoby M, Merkle T, Domagalska MA, Weisshaar B, Davis SJ (2008) A systematic survey in Arabidopsis thaliana of transcription factors that modulate circadian parameters. BMC Genomics 9:182CrossRefGoogle Scholar
  39. 39.
    Plautz JD, Straume M, Stanewsky R, Jamison CF, Brandes C, Dowse HB, Hall JC, Kay SA (1997) Quantitative analysis of Drosophila period gene transcription in living animals. J Biol Rhythm 12:204–217CrossRefGoogle Scholar
  40. 40.
    Dixon LE, Knox K, Kozma-Bognar L, Southern MM, Pokhilko A, Millar AJ (2011) Temporal repression of core circadian genes is mediated through EARLY FLOWERING 3 in Arabidopsis. Curr Biol 21:120–125CrossRefGoogle Scholar
  41. 41.
    Zielinski T, Moore AM, Troup E, Halliday KJ, Millar AJ (2014) Strengths and limitations of period estimation methods for circadian data. PLoS One 9:e96462CrossRefGoogle Scholar
  42. 42.
    Welsh DK, Imaizumi T, Kay SA (2005) Real-time reporting of circadian-regulated gene expression by luciferase imaging in plants and mammalian cells. In: Young MW (ed) Methods in enzymology. Academic Press, Cambridge, MA, pp 269–288Google Scholar
  43. 43.
    Schindelin J, Rueden CT, Hiner MC, Eliceiri KW (2015) The ImageJ ecosystem: an open platform for biomedical image analysis. Mol Reprod Dev 82:518–529CrossRefGoogle Scholar
  44. 44.
    Perales M, Portolés S, Más P (2006) The proteasome-dependent degradation of CKB4 is regulated by the Arabidopsis biological clock. Plant J 46:849–860CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Rachael J. Oakenfull
    • 1
  • James Ronald
    • 1
  • Seth J. Davis
    • 1
    Email author
  1. 1.Department of BiologyUniversity of YorkYorkUK

Personalised recommendations