Biological Rhythms and Photoperiodism in Plants
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1 P.J. LUMSDEN Department ofapplied Biology, University of Central Lancashire, Preston PRl 2HE, UK AJ. MILLAR Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, UK Biological Rhythms and Photoperiodism in Plants fios 'SCIENTIFIC PUBLISHERS Oxford Washington DC
2 Contents Contributors Abbreviations Preface ix xi xiii 1. A clockwork green: circadian programs in photosynthetic organisms 1 C.H. Johnson, M. Knight, A. Trewavas and T. Kondo Circadian timekeepers were first discovered in plants 1 Circadian rhythms are ubiquitous 2 Analogies for the functions of circadian timekeepers 2 Fundamental criteria of circadian rhythms 3 The organization of circadian systems 8 A biochemical 'clockwork green' 13 Input and entrainment: keeping the clock on time 15 Output pathways - 'hands' 20 Linking everything together: coupling pathways 22 Are circadian programs really adaptive? 25 How did circadian clocks evolve 27 References Rhythms in organ movement 35 W. Engelmann and A. Johnsson Introduction 35 Automobile Desmodium: ultradian rhythms 35 The pulvinus: circadian rhythms and an acute response to light 38 Kalanchoe petal movement: limit cycle and singular state 39 The three leaflet system of Oxalis: interaction of oscillators 40 Single oscillators and coupled oscillators: ultradian rhythms in stomata 42 Circumnutation in Arabidopsis tbaliana and other plants 43 Tropic feedback mechanisms 45 Where will organs move next? 48 References The cellular organization of circadian rhythms in plants: not one but many clocks 51 A.J. Millar Why talk of multiple clocks? 51 Models of multiple oscillators 53 Formal evidence for multiple oscillators: the rhythms of whole organisms 53 Distinguishing oscillators by anatomy and genetics 57 Multiple oscillators within single cells 60 Communication among clocks 61 Future prospects and evolutionary considerations 64 References 65 V
3 vi CONTENTS 4. Stomatal rhythms 69 A.A.R. Webb Introduction 69 The circadian regulation of stomatal behaviour 71 Entraining stomatal rhythms 72 Cellular mechanisms underlying circadian stomatal behaviour 73 Physiological benefits of the circadian control of stomatal behaviour 74 Conclusions 77 References Genetic approaches to the analysis of circadian rhythms in plants 81 D.E. Somers and S.A. Kay Introduction 81 Early work 82 Arabidopsis 85 Conclusions and future directions 94 References Molecular analysis of circadian clock-regulated gene expression in plants: features of the 'output' pathways 99 E. Fejes and F. Nagy Introduction 99 Genes regulated by a circadian rhythm in higher plants 100 Circadian clock regulated expression of Lhc genes 105 In vitro and in vivo approaches to identify cis- and trans-acting elements of the circadian output pathway 108 Interaction of the circadian clock and phytochrome to regulate Lhc gene expression 111 Phytochrome-independent circadian rhythms 113 Conclusion 113 References Circadian rhythmicity in Neurospora crassa \ 119 PL. Lakin-Thomas Introduction 119 Photoreceptors and the light input pathway ' 120 Clock-controlled gene expression 122 Limit cycle behaviour 123 Thefrq gene as state variable 125 Other clock mutations 128 The/rv? gene as input component 129 References Photoentrainment in the vertebrates: a comparative analysis 135 R.G. Foster Introduction 135 Photoentrainment in non-mammalian vertebrates 136 Photoentrainment in mammals 138 The sensory ecology of photoentrainment 141 The role of the input pathway in defining circadian behaviour 143
4 CONTENTS, vii Conclusions, 145 References Photoperiodism: an overview 151 B. Thomas Introduction 151 Examples of photoperiodism 153 The discovery of photoperiodism 154 Photopenodic mechanisms 156 Photoperiodism in plants 157 Conclusions 163 References Photoperiodic induction in short-day plants 167 P.J. Lumsden Introduction 167 Rhythmic output 169 Input pathways 172 The oscillator involved in photoperiodic timing 176 Conclusions 180 References The photoperiodic control of tuberization in potato 183 S.D. Jackson and B. Thomas Introduction 183 The tuberization stimulus 184 Conclusions 190 References Dormancy: night timekeeping and day timekeeping for the photoperiodic control of budset in Norway spruce 195 D. Clapham, I. Ekberg, I. Dormling, G. Eriksson, M. Qamaruddin and D. Vince-Prue Budset in forest tree species as a photoperiodic phenomenon 195 The timing mechanism for the photoperiodic control of budset 197 Relative importance of 'night' and 'day' timekeeping 205 Future investigations of dormancy 206 References Developmental processes in insects: circadian rhythms and photoperiodism in the blow fly, Calliphora vicina 211 D.S. Saunders Introduction 211 Locomotor activity: overt circadian rhythmicity 212 Photoperiodic induction of diapause 215 The circadian basis of photoperiodic timing: covert circadian rhythmicity 218 Anatomical location of photoreceptors, oscillators and their outputs 222 Similarities and differences between the locomotor activity rhythm and photoperiodic timing in C. vicina 225 References 226
5 viii CONTENTS 14. Rhythms and photoperiodism in birds 231 B.K. Follett, V.M. King, S.L. Meddle Introduction 231 Evidence that a circadian rhythm is the basis of time measurement 231 Multiple oscillators operate in birds 236 Photoperiodic induction in real time: events downstream of the circadian system 237 References Photoperiodic regulation of flowering time in Arabidopsis 243 G. Coupland Introduction 243 Arabidopsis and pea: complementary models to study the promotion of flowering in response to long days 244 The effect of photoreceptor mutations on flowering time in response to photoperiod 245 Analysis of late flowering mutants 247 Early flowering mutants 250 Future perspectives: extending the molecular-genetic approach 252 References Genetic dissection of the photoperiod-sensing mechanism in the long-day plant Arabidopsis thaliana 257 LA. Carre Introduction 257 Photoreceptors for the perception of daylength 259 Rhythmic outputs from the photoperiodic system 260 Approaching the mechanisms involved in photoperiodic timing 262 Conclusions from a genetic approach 266 References 267 Glossary 271 Index 277
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