Abstract
Biological evolution has endowed the plant Arabidopsis thaliana with genetically regulated circadian rhythms. A number of authors have published kinetic models for these oscillating chemical reactions based on a network of interacting genes. To investigate the hypothesis that the Arabidopsis circadian dynamical system is poised near a Hopf bifurcation like some other biological oscillators, we varied the kinetic parameters in the models and searched for bifurcations. Finding that each model does exhibit a supercritical Hopf bifurcation, we performed a weakly nonlinear analysis near the bifurcation points to derive the Stuart–Landau amplitude equation. To illustrate a common dynamical structure, we scaled the numerical solutions to the models with the asymptotic solutions to the Stuart–Landau equation to collapse the circadian oscillations onto two universal curves—one for amplitude, and one for frequency. However, some models are close to bifurcation while others are far, some models are post-bifurcation while others are pre-bifurcation, and kinetic parameters that lead to a bifurcation in some models do not lead to a bifurcation in others. Future kinetic modeling can make use of our analysis to ensure models are consistent with each other and with the dynamics of the Arabidopsis circadian rhythm.
Similar content being viewed by others
Code availibility
The MATLAB code to replicate the calculations in this work is available on GitHub at https://github.com/oshindel/Reductive-Perturbation-Method-A.-thaliana.
References
Alabadí D, Oyama T, Yanovsky MJ, Harmon FG, Más P, Kay SA (2001) Reciprocal regulation between toc1 and lhy/cca1 within the \(Arabidopsis\) circadian clock. Science 293(5531):880–883
Anpo M, Fukuda H, Wada T (2018) Plant factory using artificial light: adapting to environmental disruption and clues to agricultural innovation. Elsevier
Bujdoso N, Davis SJ (2013) Mathematical modeling of an oscillating gene circuit to unravel the circadian clock network of \(Arabidopsis\,\,thaliana\). Front Plant Sci 4:3
Chew YH, Smith RW, Jones HJ, Seaton DD, Grima R, Halliday KJ (2014) Mathematical models light up plant signaling. Plant Cell 26(1):5–20
De Caluwé J, Xiao Q, Hermans C, Verbruggen N, Leloup JC, Gonze D (2016) A compact model for the complex plant circadian clock. Front Plant Sci 7:74
Eguíluz VM, Ospeck M, Choe Y, Hudspeth A, Magnasco MO (2000) Essential nonlinearities in hearing. Phys Rev Lett 84(22):5232
Endo M (2016) Tissue-specific circadian clocks in plants. Curr Opin Plant Biol 29:44–49
Endo M, Shimizu H, Nohales MA, Araki T, Kay SA (2014) Tissue-specific clocks in \(Arabidopsis\) show asymmetric coupling. Nature 515(7527):419–422
Fogelmark K, Troein C (2014) Rethinking transcriptional activation in the \(Arabidopsis\) circadian clock. PLoS Comput Biol 10(7):e1003,705
Foo M, Somers DE, Kim PJ (2016) Kernel architecture of the genetic circuitry of the \(Arabidopsis\) circadian system. PLoS Comput Biol 12(2):e1004,748
Foo M, Bates DG, Akman OE (2020) A simplified modelling framework facilitates more complex representations of plant circadian clocks. PLoS Comput Biol 16(3):e1007,671
Fukuda H, Nakamichi N, Hisatsune M, Murase H, Mizuno T (2007) Synchronization of plant circadian oscillators with a phase delay effect of the vein network. Phys Rev Lett 99(9):098–102
Fukuda H, Murase H, Tokuda IT (2013) Controlling circadian rhythms by dark-pulse perturbations in \(Arabidopsis\,\,thaliana\). Sci Rep 3:1533
Gould PD, Domijan M, Greenwood M, Tokuda IT, Rees H, Kozma-Bognar L, Hall AJ, Locke JC (2018) Coordination of robust single cell rhythms in the \(Arabidopsis\) circadian clock via spatial waves of gene expression. Elife 7(e31):700
Guckenheimer J, Holmes P (1983) Local bifurcations. In: Nonlinear oscillations, dynamical systems, and bifurcations of vector fields. Springer, pp 117–165
Hassard BD, Kazarinoff ND, Wan YH (1981) Theory and applications of Hopf bifurcation, vol 41. CUP Archive
Hudspeth A, Jülicher F, Martin P (2010) A critique of the critical cochlea: Hopf’a bifurcation’is better than none. J Neurophysiol 104(3):1219–1229
Johansson M, Köster T (2019) On the move through time-a historical review of plant clock research. Plant Biol 21:13–20
Kuramoto Y (1984) Chemical oscillations, waves, and turbulence. Springer-Verlag, Berlin
Locke JC, Millar AJ, Turner MS (2005a) Modelling genetic networks with noisy and varied experimental data: the circadian clock in \(Arabidopsis\,\,thaliana\). J Theor Biol 234(3):383–393
Locke JC, Southern MM, Kozma-Bognár L, Hibberd V, Brown PE, Turner MS, Millar AJ (2005b) Extension of a genetic network model by iterative experimentation and mathematical analysis. Mol Syst Biol 1(1):0013
Locke JC, Kozma-Bognár L, Gould PD, Fehér B, Kevei E, Nagy F, Turner MS, Hall A, Millar AJ (2006) Experimental validation of a predicted feedback loop in the multi-oscillator clock of \(Arabidopsis\,\,thaliana\). Mol Syst Biol 2(1):59
Millar AJ (2016) The intracellular dynamics of circadian clocks reach for the light of ecology and evolution. Annu Rev Plant Biol 67:595–618
Mora T, Bialek W (2011) Are biological systems poised at criticality? J Stat Phys 144(2):268–302
Munoz MA (2018) Colloquium: criticality and dynamical scaling in living systems. Rev Mod Phys 90(3):031,001
Murayama Y, Kori H, Oshima C, Kondo T, Iwasaki H, Ito H (2017) Low temperature nullifies the circadian clock in cyanobacteria through Hopf bifurcation. Proc Natl Acad Sci 114(22):5641–5646
Murray J (2013) Mathematical biology. Biomathematics. Springer, Berlin
Ohara T, Fukuda H, Tokuda IT (2015) An extended mathematical model for reproducing the phase response of \(Arabidopsis\,\,thaliana\) under various light conditions. J Theor Biol 382:337–344
Ospeck M, Eguíluz VM, Magnasco MO (2001) Evidence of a Hopf bifurcation in frog hair cells. Biophys J 80(6):2597–2607
Pittendrigh CS (1960) Circadian rhythms and the circadian organization of living systems. In: Cold Spring Harbor symposia on quantitative biology, vol 25. Cold Spring Harbor Laboratory Press, pp 159–184
Pokhilko A, Hodge SK, Stratford K, Knox K, Edwards KD, Thomson AW, Mizuno T, Millar AJ (2010) Data assimilation constrains new connections and components in a complex, eukaryotic circadian clock model. Mol Syst Biol 6(1):416
Pokhilko A, Fernández AP, Edwards KD, Southern MM, Halliday KJ, Millar AJ (2012) The clock gene circuit in \(Arabidopsis\) includes a repressilator with additional feedback loops. Mol Syst Biol 8(1):574
Pokhilko A, Mas P, Millar AJ (2013) Modelling the widespread effects of toc1 signalling on the plant circadian clock and its outputs. BMC Syst Biol 7(1):23
Shampine LF, Reichelt MW (1997) The matlab ode suite. SIAM J Sci Comput 18(1):1–22
Stuart JT (1958) On the non-linear mechanics of hydrodynamic stability. J Fluid Mech 4(1):1–21
Takahashi N, Hirata Y, Aihara K, Mas P (2015) A hierarchical multi-oscillator network orchestrates the \(Arabidopsis\) circadian system. Cell 163(1):148–159
Tokuda IT, Akman OE, Locke JC (2019) Reducing the complexity of mathematical models for the plant circadian clock by distributed delays. J Theor Biol 463:155–166
Wenden B, Toner DL, Hodge SK, Grima R, Millar AJ (2012) Spontaneous spatiotemporal waves of gene expression from biological clocks in the leaf. Proc Natl Acad Sci 109(17):6757–6762
Xiao M, Cao J (2008) Genetic oscillation deduced from Hopf bifurcation in a genetic regulatory network with delays. Math Biosci 215(1):55–63
Yakir E, Hilman D, Hassidim M, Green RM (2007) Circadian clock associated 1 transcript stability and the entrainment of the circadian clock in \(Arabidopsis\). Plant Physiol 145(3):925–932
Zeilinger MN, Farré EM, Taylor SR, Kay SA, Doyle FJ (2006) A novel computational model of the circadian clock in \(Arabidopsis\) that incorporates prr7 and prr9. Mol Syst Biol 2(1):58
Acknowledgements
The authors would like to thank Harry L. Swinney for a critical reading of the manuscript and helpful conversations. This research was funded by Trinity University with a Murchison Fellowship to Y.X. and start-up funds to O.S.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Xu, Y., Asadi-Zeydabadi, M., Tagg, R. et al. Universality in kinetic models of circadian rhythms in \(Arabidopsis\,\,thaliana\). J. Math. Biol. 83, 51 (2021). https://doi.org/10.1007/s00285-021-01677-0
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00285-021-01677-0