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Control Theory Approach to the Study of Circadian Leaf Movement in Trifolium Repens

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Control Theory Approach to the Study of Circadian Leaf Movement in Trifolium Repens CONTROL THEORY APPROACH TO THE STUDY OF CIRCADIAN LEAF MOVEMENT IN TRIFOLIUM REPENS by G.R. Robinson B..Sc. Hons.) submitted in fulfilment of the requirements for the degree of Doctor of Philosophy. UNIVERSITY OF TASMANIA HOBART JANUARY, 1979 Thithesis.contains.no material which has been laccepted for the award of any.other.degree . or diploma in any university. To.the best of my knowledge and.belief, the thes is contains.no material previously published . or written by another person except where due reference is made in the text. G.R. Robinson CONTENTS Page SUMMARY ACKNOWLEDGEMENTS iv CHAPTER ONE : GENERAL INTRODUCTION CHAPTER TWO : CIRCADIAN RHYTHMS IN BIOLOGICAL SYSTEMS 1.1 Introduction 5 2.2 Occurrence 6 . 2.3 Characteristics of circadian systems. (a) Light effects 8 (b) Temperature effects . 10 (c) Chemical effects 12 2.4 ModelS:, ,-; -14 CHAPTER THREE : CONTROL THEORY AND ITS APPLICATION ' TO BIOLOGICAL SYSTEMS 5.1 Introduction 18 3.2 Basic concepts 18 3.3 Linear systems . 21 :3.4 The Laplace transformand system transfer .function 23 3.5 System frequency response 25 :3.6 .Relationahip.between frequency response and 25 impulse response 3.7 Determination of frequency.response 27 . (1) Transient inputs 27 (2) Continuous inputs :3.8 Matching a . transfer function to the 28 frequency response Page 3.9 Frequency response for a biological system 31 1.10 Examples of application to biological systems -34 1.11Pulse-phase response curves 36 CHAPTER FOUR : ANALYTICAL METHODS 4.1 Introduction 44 4.2 The discrete Fourier transform 45 4.3 Spectral analysis from a least squares viewpoint 47 4.3.1 Estimating amplitude and phase 48 4.3.2 Estimation of frequency 50 4.3.3 Several periodic terms 51 4.4 Properties of the DFT 51 4.4.1 Leakage 52 4.4.2 Aliasing 58 4.5 Reliability of spectral estimates 64 4.5.1 Presence of frequency components 64 4.5.2 Reliability of frequency, amplitude and 66 phase estimates 4.5.3 Combination of estimates 69 4.6 Oscillations with nonstationary parameters 71 4.7 Future developments 72 CHAPTER FIVE : EXPERIMENTAL METHOD . 5.1 Introduction 77 :5.2 Measurement and recording of leaf angle 78 - 5.3 Measurement and recording errors 84 . 5.3:1 Absolute leaf angle 84 :5.3.2 Leaf angle changes 85 :5.4 Control of plant environment 87 Page 5.5 Preparation of material 90 5.6 Analysis of leaf records 93 CHAPTER SIX : EXPERIMENTAL RESULTS. A : LIGHT TREATMENTS 6.1 Introduction 96 6.2 Response to continuous light 96 6.3 Responses to periodic light variations 105 6.3.1 Rectangular wave light changes 105 :6:3..2 Entrainment by sinusoidal log-light -- variations 108 6.4 Frequency response of leaf movement 113 6.5 Discussion of models 120 6.6 Response to transients 128 6.6.1 Off-on switching of a 10 c/d variation 128 6.6.2 System pulse-phase response curve 130 6.7 Examination of some nonlinear features 133 6.7.1 Dependence of response on background light intensity 133 6.7.2 Dependence of response on leaf position 135 CHAPTER SEVEN : EXPERIMENTAL RESULTS. B: CHEMICAL TREATMENTS - 7.1 Introduction 142 :7.2 -Effect of excision 143 . 7.3 'Treatment with sucrose 146 - 7.4 Varying pH 147 - 7..5 Treatments with KC1 and NaC1 150 - 7.6 Effect of ethanol •151 7.7 •zide • 154 Page CHAPTER EIGHT : EXPERIMENTAL RESULTS. C: Pali -INTO CELL POTENTIAL CHANGES 8.1 Introduction 158 •8.2 Method 160 8.2.1 Electrode preparation & potential recording 160 system . 8.2.2 .Preparation and mounting of specimens 163 . 8:2.3 Observation of potential changes • 164 . 8.3 Re sults • 164 . 8.4 Discussion 165 CHAPTER NINE : DISCUSSION OF RESULTS 9.1 Introduction • 169 9.2 Linearity of the system 169 9.3 The secondary loop 172 9.4 Interpretation of the model • 175 CHAPTER TEN : CONCLUDING REMARKS 182 APPENDICES •Appendix 1 : Residual variance for least 185 squares estimates Appendix 2 : Variance of a function dependent 187 on several variables Appendix 3 : Spectral estimation of frequency, .189 amplitude and phase in the presence of a second component Page Appendix 4 :.Leaf anglemeters and cabinet 196 .controls Appendix 5 : Influence of thorium ions on micro- 203 .electrode tip potentials. REFERENCES 206 SUMMARY This thesis describes a study of natural and forced leaf oscillations in white clover (niifoZium repens L.). Apparatus was constructed which permitted the accurate control and programmed variation of environmental conditions surrounding clover plants and also the automatic recording of changes in clover leaf angle. Records of leaf movement were examined and interpreted by applying the techniques of Fourier analysis and of control theory. Problems associated with the analysis of short oscillatory data records are discussed and the advantages and limitations of Fourier analysis are described. Particular attention is given to possible errors in spectral estimates. Experiments are described in which clover leaves were treated with constant intensity light, single light pulses, rectangular wave light changes and sinusoidal log-light variations; i.e. light oscillations forwhich the logarithm of light intensity varied sinusoidally with time. For continuous light treatment the characteristics of the natural (circadian) leaf oscillation (e.g. • frequency, damping rate, harmonic content) are considered for different light intensities. Experiments with sinusoidal log-light oscillations of various amplitude indicate that entrainment is not an all-or-none response but that frequency components due to both the natural and forcing oscillation may contribute to the leaf movement. As part of a control theory approach to analysing the clover leaf oscillator plants were treated with sinusoidal log-light oscillations ranging in frequency from 2/3 c/d (cycle per day) to 20 c/d. The amplitude and phase of the component in the leaf movement at the frequency of the forcing oscillation were determined for each case. These frequency response data are graphed as separate amplitude and phase plots (Bode plots). A feedback model having a transfer function which is consistent with these data is developed. Some nonlinear features of this system relating light changes to leaf movement are also described. A characteristic of a circadian system considered to be important by many investigators is its light -pulse phase response. :This is shown graphically by plotting the change in phase of a circadian oscillator caused by a light pulse applied at different times during the natural cycle. Pulse phase response studies are considered and the relationship between these and a frequency response analysis is examined. Results for 2 hour light pulses are given and are shown to be consistent with the mathematical model developed from the frequency response data. A phase.response.curve for - 2.5 mM 2 hour azide pulses is also presented and is shown to have a form similar to. the light phase .response curve. .Repeated KC1 and NaC1 pulses do not entrain the .cloverleaf oscillator .but do have some effect on leaf movement. Frequency changes caused by the presence of ethanol are reported. Finally circadian-rhythm for excised leaves in continuous light is shown to be markedly less heavily damped if the leaves are supplied with sucrose. Attempts were made to continuously monitor pulvinule . transme.Warane potential. Although such monitoring proved unsuccessful it is Shown that the potential for both adaXial and abaxial pulvinule cortical cells varies in a circadian fashion. These results and in particular the mathematical model developed are discussed in terms of possible physiological models for the circadian oscillator.-- iv ACKNOWLEDGEMENTS The author wishes to express his gratitude to . Dr..B.I.H. Scott for'his.constant support and guidance throughout this project. Frequent discussions with Dr..I.A..Newman were also of.corisiderable assistance. The practical help of Mr. D.F. Dainton in the construction of the controlled cabinets and other equipment used in these studies is also acknowledged, as is the advice of Miss H. Gulline on matters relating to - the chemical-treatment of clover plants. The author was supported by a.Commonwealth Post-Graduate Research award during .much of this project. CHAPTER ONE GENERAL INTRODUCTION It is well established that living organisms undergo cyclic physiological changes with day and night. In a wide range of organisms these changes have been observed to continue for many cycles even under apparently constant environmental conditions, though generally with a period somewhat different from 24 hours. Originally referred to as diurnal, this rhythmic behaviour has since been renamed circadian (circa dies - about a day), following a suggestion by Halberg (1959), the term diurnal being reserved as the complement to nocturnal. During recent years a large quantity of literature• has accumulated -concerning the- occurrence -and- properties-- of circadian rhythms. However, although general mathematical and physical models have been proposed for the endogenous oscillators (biological clocks) responsible for such rhythms, their nature and the manner in which they interact with environmental changes such as light and temperature is still far from being fully understood. By way of introduction to circadian rhythm research much of the literature concerning circadian rhythmicity is surveyed in the following chapter. A circadian system controlling rhythmic metabolic or physiological changes may be regarded as a regulatory system. Furthermore it is a system which not only assists an organism in its 2. adjustment to day-night environmental changes, but also permits some predictive behaviour; e.g. the metabolism of an organism may prepare in advance for daybreak or nightfall, guided by its internal timing system, perhaps hoarding energy reserves during some parts of each cycle in preparation for their requirement in others. Internal timing permits the temporal organisation of physiological processes. Since World War II a branch of physical science has developed which concerns itself with the theory of operation of man-made regulatory systems.
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