Evolutionary mechanisms of circadian clocks

Guillermo Rodrigo 1 , Javier Carrera 1  and Alfonso Jaramillo 2
  • 1 Depto. de Matematica Aplicada, Universidad Politecnica de Valencia, 46022, Valencia, Spain
  • 2 CNRS — UMR 7654, Ecole Polytechnique, Laboratoire de Biochimie, 91128, Palaiseau, France

Abstract

An intriguing question in biology is to know how circadian molecular networks could have evolved their particular topologies to adjust to a daily period. We analyze the mechanism of the evolution of such networks by using a computational design strategy that allows for the generation of synthetic networks with a targeted 24 hours oscillation. We have performed a systematic analysis of all possible two-gene network topologies based on a core activator-repressor frequently found in circadian mechanisms. We have considered transcriptional and post-translational regulations to implement this core. We have applied our analysis to both, eukaryotic and prokaryotic circadian machinery. Finally, we conjecture a possible mechanism for the evolution of circadian clocks.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • [1] J.C. Dunlap: “Molecular bases for circadian clocks”, Cell, Vol. 96, (1999), pp. 271–290. http://dx.doi.org/10.1016/S0092-8674(00)80566-8

  • [2] C.F. Ehret and J.J. Wille: “Photobiology of microorganisms”, Halldal, P. (Ed.), Wiley, New York (USA), 1970, pp. 369–416.

  • [3] C.H. Johnson, S.S. Golden, M. Ishiura and T. Kondo: “Circadian clocks in prokaryotes”, Mol. Microbiol., Vol. 21, (1996), pp. 5–11. http://dx.doi.org/10.1046/j.1365-2958.1996.00613.x

  • [4] M.W. Young and S.A. Kay: “Time zones: a comparative genetics of circadian clocks”, Nat. Rev. Genet., Vol. 2, (2001), pp. 702–715. http://dx.doi.org/10.1038/35088576

  • [5] J.J. Loros and J.C. Dunlap: “Genetic and molecular analysis of circadian rhythms in Neurospora”, Annu. Rev. Physiol., Vol. 63, (2001), pp. 757–794. http://dx.doi.org/10.1146/annurev.physiol.63.1.757

  • [6] T. Mori and C.H. Johnson: “Circadian programming in cyanobacteria”, Semin. Cell Dev. Biol., Vol. 12, (2001), pp. 271–278. http://dx.doi.org/10.1006/scdb.2001.0254

  • [7] L.C. Roden and I.A. Carre: “The molecular genetics of circadian rhythms in Arabidopsis”, Semin. Cell Dev. Biol., Vol. 12, (2001), pp. 305–315. http://dx.doi.org/10.1006/scdb.2001.0258

  • [8] S. Reppert and D. Weaver: “Coordination of circadian timing in mammals”, Nature, Vol. 418, (2002), pp. 935–941. http://dx.doi.org/10.1038/nature00965

  • [9] E. Herzog, J. Takahashi and G. Block: “Clock controls circadian period in isolated suprachiasmatic nucleus neurons”, Nature Neurosci., Vol. 1, (1998), pp. 708–713. http://dx.doi.org/10.1038/3708

  • [10] A. Millar: “Molecular intrigue between phototransduction and the circadian clock”, Ann. Bot., Vol. 81, (1998), pp. 581–587. http://dx.doi.org/10.1006/anbo.1998.0595

  • [11] M.B. Elowitz and S. Leibler: “A synthetic oscillatory network of transcriptional regulators”, Nature, Vol. 403, (2000), pp. 335–338. http://dx.doi.org/10.1038/35002125

  • [12] T.S. Gardner, C.R. Cantor and J.J. Collins: “Construction of a genetic toggle switch in E. Coli”, Nature, Vol. 403, (2000), pp. 339–342. http://dx.doi.org/10.1038/35002131

  • [13] A. Jaramillo, L. Wernisch, S. Hery and S.J. Wodak: “Folding free energy function selects native-like protein sequences in the core but not on the surface”, Proc. Natl. Acad. Sci. USA, Vol. 99, (2002), pp. 13554–13559. http://dx.doi.org/10.1073/pnas.212068599

  • [14] S. Basu, Y. Gerchman, C.H. Collins, F.H. Arnald and R. Weiss: “A synthetic multicellular system for programmed pattern formation”, Nature, Vol. 434, (2005), pp. 1130–1134. http://dx.doi.org/10.1038/nature03461

  • [15] J. Hasty, D. McMillen and J.J. Collins: “Engineered gene circuits”, Nature, Vol. 420, (2002), pp. 224–230. http://dx.doi.org/10.1038/nature01257

  • [16] P. Francois and V. Hakim: “Design of genetic networks with specified functions by evolution in silico”, Proc. Natl. Acad. Sci. USA, Vol. 101, (2004), pp. 580–585. http://dx.doi.org/10.1073/pnas.0304532101

  • [17] M.R. Atkinson, M.A. Savageau, J.T. Myers and A.J. Ninfa: “Development of genetic circuit exhibiting toggle switch or oscillatory behavior in Escherichia Coli”, Cell, Vol. 113, (2003), pp. 597–607. http://dx.doi.org/10.1016/S0092-8674(03)00346-5

  • [18] N. Barkai and S. Liebler: “Circadian clocks limited by noise”, Nature, Vol. 403, (1999), pp. 267–268.

  • [19] P. Francois and V. Hakim: “Core genetic module: the mixed feedback loop”, Phys. Rev. E, Vol. 72, (2005), art. 31908.

  • [20] N. Monk: “Oscillatory expression of Hes1, p53, and NF-kB driven by transcriptional time delays”, Curr. Biol., Vol. 13, (2003), pp. 1409–1413. http://dx.doi.org/10.1016/S0960-9822(03)00494-9

  • [21] H. El-Samad, M. Khammash, L. Petzold and D. Gillespie: “Stochastic modelling of gene regulatory networks”, Int. J. Robust Nonlinear Control, Vol. 15, (2005), pp. 691–711. http://dx.doi.org/10.1002/rnc.1018

  • [22] D. Gillespie: “A general method for numerically simulating the stochastic time evolution of coupled chemical reactions”, J. Comput. Phys., Vol. 22, (1976), pp. 403–434. http://dx.doi.org/10.1016/0021-9991(76)90041-3

  • [23] S. Kirkpatrick, C.D. Gelatt and M.P. Vecchi: “Optimization by simulated annealing”, Science, Vol. 220, (1983), pp. 671–680. http://dx.doi.org/10.1126/science.220.4598.671

  • [24] V. Chickarmane, S.R. Paladugu, F. Bergmann and H.M. Sauro: “Bifurcation discovery tool”, Bioinformatics, Vol. 21, (2005), pp. 3688–3690. http://dx.doi.org/10.1093/bioinformatics/bti603

  • [25] D.B. Forger and C.S. Peskin: “A detailed predictive model of the mammalian circadian clock”, Proc. Natl. Acad. Sci. USA, Vol. 100, (2003), pp. 14806–14811. http://dx.doi.org/10.1073/pnas.2036281100

  • [26] J.C. Leloup and A. Goldbeter: “Toward a detailed computational model for the mammalian circadian clock”, Proc. Natl. Acad. Sci. USA, Vol. 100, (2003), pp. 7051–7056. http://dx.doi.org/10.1073/pnas.1132112100

  • [27] Y. Xu, T. Mori and C.H. Johnson: “Cyanobacterial circadian clockwork: roles of KaiA, KaiB and the kaiBC promoter in regulating KaiC”, EMBO J., Vol. 22, (2003), pp. 2117–2126. http://dx.doi.org/10.1093/emboj/cdg168

  • [28] D. Gonze, J. Halloy and A. Goldbeter: “Robustness of circadian rhythms with respect to molecular noise”, Proc. Natl. Acad. Sci. USA, Vol. 99, (2002), pp. 673–678. http://dx.doi.org/10.1073/pnas.022628299

  • [29] W.P. Dayawansa and C.F. Martin: “Stability of phase locked oscillations in the circadian clock”, Proc. Am. Control Conf., Vol. Arlington (USA), (2001), pp. 252–256.

  • [30] J.M.G. Vilar, H.Y. Kueh, N. Barkai and S. Leibler: “Mechanisms of noise-resistance in genetic oscillators”, Proc. Natl. Acad. Sci. USA, Vol. 99, (2002), pp. 5988–5992. http://dx.doi.org/10.1073/pnas.092133899

  • [31] U. Albretch: “Regulation of mammalian circadian clock genes”, J. Appl. Physiol., Vol. 92, (2002), pp. 1348–1355.

  • [32] S. Golden, M. Ishiura, C.H. Johnson and T. Kondo: “Cyanobacterial circadian rhythms”, Annu. Rev. Plant Physiol. Plant Mol. Biol., Vol. 48, (1997), pp. 327–354. http://dx.doi.org/10.1146/annurev.arplant.48.1.327

  • [33] M. Ishiura, S. Kutsuna, S. Aoki, H. Iwasaki, C.R. Andersson, A. Tanabe, S.S. Golden, C.H. Johnson and T. Kondo: “Expression of a gene cluster kaiABC as a circadian feedback process in cyanobacteria”, Science, Vol. 281, (1998), pp. 1519–1523. http://dx.doi.org/10.1126/science.281.5382.1519

  • [34] B.A. Whitton: “Survival and dormancy of microorganisms”, Hennis, Y. (Ed.), Wiley, New York (USA), 1987, pp. 109–167.

  • [35] E. Emberly and N.S. Wingreen: “Hourglass model for a protein-based circadian oscillator”, Phys. Rev. Lett., Vol. 96, (2006), pp. 38303 1–4.

  • [36] H. Iwasaki, T. Nishiwaki, Y. Kitayama, M. Nakajima and T. Kondo: “KaiA-stimulated KaiC phosphorylation in circadian timing loops in cyanobacteria”, Proc. Natl. Acad. Sci. USA, Vol. 99, (2002), pp. 15788–15793. http://dx.doi.org/10.1073/pnas.222467299

  • [37] S. Ohno: “Evolution by Gene Duplication”, (Ed.), Springer, Berlin (Germany), 1970, pp. 1–160.

  • [38] D.B. Forger and C.S. Peskin: “Stochastic simulation of the mammalian circadian clock”, Proc. Natl. Acad. Sci. USA, Vol. 102, (2005), pp. 321–324. http://dx.doi.org/10.1073/pnas.0408465102

OPEN ACCESS

Journal + Issues

Open Life Sciences (previously Central European Journal of Biology) is a fast growing OA journal, devoted to scholarly research in all areas of life sciences. The journal assures top quality of published data through critical peer review, editorial involvement throughout the whole publication process. Thanks to OA it also offers unrestricted access to published articles for all users.

Search