Stochastic models of cellular circadian rhythms in plants help to understand the impact of noise on robustness and clock structure

Frontiers in Plant Science

Volumn 5, Issue OCT, 2014, Pages

  Guerriero, Maria L ^a   Akman, Ozgur E ^b   van Ooijen, Gerben ^c  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF EXETER   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Arabidopsis thaliana; Circadian clocks; Extrinsic noise; Intrinsic noise; Modeling; Ostreococcus tauri; Plants; Stochasticity

Indexed keywords

EID: 84908234129     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00564     Document Type: Article

References (57)

1. Abraham, U., Granada, A. E., Westermark, P. O., Heine, M., Kramer, A., and Herzel, H. (2010). Coupling governs entrainment range of circadian clocks. Mol. Syst. Biol. 6:438. doi: 10.1038/msb.2010.92
2. Akman, O. E., Ciocchetta, F., Degasperi, A., and Guerriero, M. L. (2009). "Modelling biological clocks with Bio-PEPA: stochasticity and robustness for the Neurospora crassa circadian network," in Computational Methods in Systems Biology, eds P. Degano and R. Gorrieri (Berlin: Springer-Verlag), 52-67.
3. Akman, O. E., Guerriero, M. L., Loewe, L., and Troein, C. (2010a). Complementary approaches to understanding the plant circadian clock. Proc. FBTC 10, 1-19.
4. Akman, O. E., Rand, D. A., Brown, P. E., and Millar, A. J. (2010b). Robustness from flexibility in the fungal circadian clock. BMC Syst. Biol. 4:88. doi: 10.1186/1752-0509-4-88
5. Akman, O. E., Locke, J. C., Tang, S., Carré, I., Millar, A. J., and Rand, D. A. (2008). Isoform switching facilitates period control in the Neurospora crassa circadian clock. Mol. Syst. Biol. 4:164. doi: 10.1038/msb.2008.5
6. Baker, C. L., Loros, J. J., and Dunlap, J. C. (2012). The circadian clock of Neurospora crassa. FEMS Microbiol. Rev. 36, 95-110. doi: 10.1111/j.1574-6976.2011.00288.x
7. Bujdoso, N., and Davis, S. J. (2013). Mathematical modeling of an oscillating gene circuit to unravel the circadian clock network of Arabidopsis thaliana. Front. Plant Sci. 4:3. doi: 10.3389/fpls.2013.00003
8. Cao, Y., Gillespie, D. T., and Petzold, L. R. (2007). Adaptive explicit-implicit tau-leaping method with automatic tau selection. J. Chem. Phys. 126:224101. doi: 10.1063/1.2745299
9. Cheng, P., Yang, Y., and Liu, Y. (2001). Interlocked feedback loops contribute to the robustness of the Neurospora circadian clock. Proc. Natl. Acad. Sci. U.S.A. 98, 7408-7413. doi: 10.1073/pnas.121170298
10. Collos, Y., Bec, B., Jauzein, C., Abadie, E., Laugier, T., Lautier, J.,et al. (2009). Oligotrophication and emergence of picocyanobacteria and a toxic dinoflagellate in Thau lagoon, southern France. J. Sea Res. 61, 68-75. doi: 10.1016/j.seares.2008.05.008
11. Corellou, F., Schwartz, C., Motta, J. P., Djouani-Tahri el, B., Sanchez, F., and Bouget, F. Y. (2009). Clocks in the green lineage: comparative functional analysis of the circadian architecture of the picoeukaryote Ostreococcus. Plant Cell 21, 3436-3449. doi: 10.1105/tpc.109.068825
12. Courties, C., Vaquer, A., Troussellier, M., Lautier, J., Chretiennot-Dinet, M. J., Neveux, J.,et al. (1994). Smallest eukaryotic organism. Nature 370, 255-255. doi: 10.1038/370255a0
13. Dalchau, N., Hubbard, K. E., Robertson, F. C., Hotta, C. T., Briggs, H. M., Stan, G. B.,et al. (2010). Correct biological timing in Arabidopsis requires multiple light-signaling pathways. Proc. Natl. Acad. Sci. U.S.A. 107, 13171-13176. doi: 10.1073/pnas.1001429107
14. Derelle, E., Ferraz, C., Rombauts, S., Rouze, P., Worden, A. Z., Robbens, S.,et al. (2006). Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc. Natl. Acad. Sci. U.S.A. 103, 11647-11652. doi: 10.1073/pnas.0604795103
15. Dixon, L. E., Hodge, S. K., van Ooijen, G., Troein, C., Akman, O. E., and Millar, A. J. (2014). Light and circadian regulation of clock components aids flexible responses to environmental signals. New Phytol. 203, 568-577. doi: 10.1111/nph.12853
16. Dodd, A. N., Salathia, N., Hall, A., Kevei, E., Toth, R., Nagy, F.,et al. (2005). Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309, 630-633. doi: 10.1126/science.1115581
17. Domijan, M., and Rand, D. A. (2011). Balance equations can buffer noisy and sustained environmental perturbations of circadian clocks. Interface Focus 1, 177-186. doi: 10.1098/rsfs.2010.0007
18. Dunlap, J. C., Loros, J. J., and Decoursey, P. J. (2003). Chronobiology: Biological Timekeeping. Sunderland, MA: Sinauer.
19. Edwards, K. D., Akman, O. E., Knox, K., Lumsden, P. J., Thomson, A. W., Brown, P. E.,et al. (2010). Quantitative analysis of regulatory flexibility under changing environmental conditions. Mol. Syst. Biol. 6:424. doi: 10.1038/msb.2010.81
20. Enoki, R., Ono, D., Hasan, M. T., Honma, S., and Honma, K. (2012). Single-cell resolution fluorescence imaging of circadian rhythms detected with a Nipkow spinning disk confocal system. J. Neurosci. Methods 207, 72-79. doi: 10.1016/j.jneumeth.2012.03.004
21. Forger, D. B., and Peskin, C. S. (2005). Stochastic simulation of the mammalian circadian clock. Proc. Natl. Acad. Sci. U.S.A. 102, 321-324. doi: 10.1073/pnas.0408465102
22. Gibson, M. A., and Bruck, J. (2000). Efficient exact stochastic simulation of chemical systems with many species and many channels. J. Phys. Chem. A 104, 1876-1889. doi: 10.1021/jp993732q
23. Gillespie, D. (1977). Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem. 81, 2340-2361. doi: 10.1021/j100540a008
24. Gonze, D., Halloy, J., and Goldbeter, A. (2002a). Deterministic versus stochastic models for circadian rhythms. J. Biol. Phys. 28, 637-653. doi: 10.1023/A:1021286607354
25. Gonze, D., Halloy, J., and Goldbeter, A. (2002b). Robustness of circadian rhythms with respect to molecular noise. Proc. Natl. Acad. Sci. U.S.A. 99, 673-678. doi: 10.1073/pnas.022628299
26. Gould, P. D., Ugarte, N., Domijan, M., Costa, M., Foreman, J., Macgregor, D.,et al. (2013). Network balance via CRY signalling controls the Arabidopsis circadian clock over ambient temperatures. Mol. Syst. Biol. 9:650. doi: 10.1038/msb.2013.7
27. Graf, A., Schlereth, A., Stitt, M., and Smith, A. M. (2010). Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc. Natl. Acad. Sci. U.S.A. 107, 9458-9463. doi: 10.1073/pnas.0914299107
28. Guerriero, M. L., Pokhilko, A., Fernandez, A. P., Halliday, K. J., Millar, A. J., and Hillston, J. (2012). Stochastic properties of the plant circadian clock. J. R. Soc. Interface 9, 744-756. doi: 10.1098/rsif.2011.0378
29. Harmer, S. L. (2009). The circadian system in higher plants. Annu. Rev. Plant Biol. 60, 357-377. doi: 10.1146/annurev.arplant.043008.092054
30. Haydon, M. J., Mielczarek, O., Robertson, F. C., Hubbard, K. E., and Webb, A. A. R. (2013). Photosynthetic entrainment of the Arabidopsis thaliana circadian clock. Nature 502, 689-692. doi: 10.1038/nature12603
31. Henderson, G. P., Gan, L., and Jensen, G. J. (2007). 3-D ultrastructure of O. tauri: electron cryotomography of an entire eukaryotic cell. PLoS ONE 2:e749. doi: 10.1371/journal.pone.0000749
32. Herrero, E., Kolmos, E., Bujdoso, N., Yuan, Y., Wang, M., Berns, M. C.,et al. (2012). EARLY FLOWERING4 recruitment of EARLY FLOWERING3 in the nucleus sustains the Arabidopsis circadian clock. Plant Cell 24, 428-443. doi: 10.1105/tpc.111.093807
33. Huang, W., Perez-Garcia, P., Pokhilko, A., Millar, A. J., Antoshechkin, I., Riechmann, J. L.,et al. (2012). Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336, 75-79. doi: 10.1126/science.1219075
34. James, A. B., Monreal, J. A., Nimmo, G. A., Kelly, C. L., Herzyk, P., Jenkins, G. I.,et al. (2008). The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots. Science 322, 1832-1835. doi: 10.1126/science.1161403
35. Lee, P., Gaige, T., and Hung, P. (2011). Microfluidic systems for live cell imaging. Methods Cell Biol. 102, 77-103. doi: 10.1016/B978-0-12-374912-3.00004-3
36. Locke, J. C., and Elowitz, M. B. (2009). Using movies to analyse gene circuit dynamics in single cells. Nat. Rev. Microbiol. 7, 383-392. doi: 10.1038/nrmicro2056
37. Locke, J. C., Kozma-Bognar, L., Gould, P. D., Feher, B., Kevei, E., Nagy, F.,et al. (2006). Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol. Syst. Biol. 2:59. doi: 10.1038/msb4100102
38. Locke, J. C., Millar, A. J., and Turner, M. S. (2005). Modelling genetic networks with noisy and varied experimental data: the circadian clock in Arabidopsis thaliana. J. Theor. Biol. 234, 383-393. doi: 10.1016/j.jtbi.2004.11.038
39. Mas, P., Kim, W. Y., Somers, D. E., and Kay, S. A. (2003). Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426, 567-570. doi: 10.1038/nature02163
40. McAdams, H. H., and Arkin, A. (1999). It's a noisy business! Genetic regulation at the nanomolar scale. Trends Genet. 15, 65-69. doi: 10.1016/S0168-9525(98)01659-X
41. Merrow, M., Spoelstra, K., and Roenneberg, T. (2005). The circadian cycle: daily rhythms from behaviour to genes. EMBO Rep. 6, 930-935. doi: 10.1038/sj.embor.7400541
42. Nusinow, D. A., Helfer, A., Hamilton, E. E., King, J. J., Imaizumi, T., Schultz, T. F.,et al. (2011). The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475, 398-402. doi: 10.1038/nature10182
43. O'Neill, J. S., van Ooijen, G., Dixon, L. E., Troein, C., Corellou, F., Bouget, F. Y.,et al. (2011). Circadian rhythms persist without transcription in a eukaryote. Nature 469, 554-558. doi: 10.1038/nature09654
44. Pokhilko, A., Fernandez, A. P., Edwards, K. D., Southern, M. M., Halliday, K. J., and Millar, A. J. (2012). The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol. Syst. Biol. 8, 574. doi: 10.1038/msb.2012.6
45. Pokhilko, A., Hodge, S. K., Stratford, K., Knox, K., Edwards, K. D., Thomson, A. W.,et al. (2010). Data assimilation constrains new connections and components in a complex, eukaryotic circadian clock model. Mol. Syst. Biol. 6:416. doi: 10.1038/msb.2010.69
46. Resco, V., Hartwell, J., and Hall, A. (2009). Ecological implications of plants ability to tell the time. Ecol. Lett. 12, 583-592. doi: 10.1111/j.1461-0248.2009.01295.x
47. Ruoff, P., Zakhartsev, M., and Westerhoff, H. V. (2007). Temperature compensation through systems biology. FEBS J. 274, 940-950. doi: 10.1111/j.1742-4658.2007.05641.x
48. Schaum, E., Rost, B., Millar, A. J., and Collins, S. (2013). Variation in plastic responses of a globally distributed picoplankton species to ocean acidification. Nat. Clim. Chang. 3, 298-302. doi: 10.1038/nclimate1774
49. Smolen, P., Baxter, D. A., and Byrne, J. H. (2001). Modeling circadian oscillations with interlocking positive and negative feedback loops. J. Neurosci. 21, 6644-6656.
50. Song, H. R., and Carré, I. A. (2005). DET1 regulates the proteasomal degradation of LHY, a component of the Arabidopsis circadian clock. Plant Mol. Biol. 57, 761-771. doi: 10.1007/s11103-005-3096-z
51. Troein, C., Corellou, F., Dixon, L. E., van Ooijen, G., O'Neill, J. S., Bouget, F. Y.,et al. (2011). Multiple light inputs to a simple clock circuit allow complex biological rhythms. Plant J. 66, 375-385. doi: 10.1111/j.1365-313X.2011.04489.x
52. Troein, C., Locke, J. C., Turner, M. S., and Millar, A. J. (2009). Weather and seasons together demand complex biological clocks. Curr. Biol. 19, 1961-1964. doi: 10.1016/j.cub.2009.09.024
53. van Ooijen, G., Dixon, L. E., Troein, C., and Millar, A. J. (2011). Proteasome function is required for biological timing throughout the twenty-four hour cycle. Curr. Biol. 21, 869-875. doi: 10.1016/j.cub.2011.03.060
54. Wang, D., and Bodovitz, S. (2010). Single cell analysis: the new frontier in "omics". Trends Biotechnol. 28, 281-290. doi: 10.1016/j.tibtech.2010.03.002
55. Wenden, B., Toner, D. L., Hodge, S. K., Grima, R., and Millar, A. J. (2012). Spontaneous spatiotemporal waves of gene expression from biological clocks in the leaf. Proc. Natl. Acad. Sci. U.S.A. 109, 6757-6762. doi: 10.1073/pnas.1118814109
56. Yang, Q., Pando, B. F., Dong, G., Golden, S. S., and van Oudenaarden, A. (2010). Circadian gating of the cell cycle revealed in single cyanobacterial cells. Science 327, 1522-1526. doi: 10.1126/science.1181759
57. Zhang, E. E., and Kay, S. A. (2010). Clocks not winding down: unravelling circadian networks. Nat. Rev. Mol. Cell Biol. 11, 764-776. doi: 10.1038/nrm2995