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Rhythms in Plants: Phenomenology, Mechanisms, and Adaptive Significance

S. Mancuso S. Shabala (Eds.)

Rhythms in PlantsPhenomenology, Mechanisms, and Adaptive Significance

With 84 Figures, 3 in Color, and 5 Tables

Prof. Dr. Stefano MancusoUniversity of FlorenceDepartment of HorticultureLINV International Laboratory on Plant

NeurobiologyPolo Scientifico, Viale delle idee 3050019 Sesto Fiorentino, Italye-mail: [email protected]

Dr. Sergey ShabalaUniversity of TasmaniaSchool of Agricultural SciencePrivate Bag 54Hobart, Tas, 7001, Australiae-mail: [email protected]

Library of Congress Control Number: 2006939346

ISBN-10: 3-540-68069-1 Springer Berlin Heidelberg New YorkISBN-13: 978-3-540-68069-7 Springer Berlin Heidelberg New York

This work is subject to copyright. All rights are reserved, whether the whole or part of the materialis concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation,broadcasting, reproduction on microfilm or in any other way, and storage in data banks. Duplicationof this publication or parts thereof is permitted only under the provisions of the German CopyrightLaw of September 9, 1965, in its current version, and permissions for use must always be obtainedfrom Springer-Verlag. Violations are liable for prosecution under the German Copyright Law.

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Stefano Mancuso dedicates this volume to Professor Emeritus Franco Scaramuzzi on his 80th birthday in grateful and affectionate acknowledgement of his

enthusiastic support as teacher, friend and colleague.

Preface

Rhythm is the basis of life, not steady forward progress. The forces of cre-ation, destruction, and preservation have a whirling, dynamic interaction.

Kabbalah quote

Rhythmic phenomena are an omnipresent attribute of behavioural and phys-iological processes in biology. From cell division to flowering, clocklikerhythms pervade the activities of every physiological process in plants, oftenin tune with the day/night cycle of the earth.

Research into the rhythmic leaf movements in nyctinastic plants in theearly 18th century provided the first clue that organisms have internal clocks.However, observations about rhythmic movement in plants had been dis-cussed already in the pre-Christian era. As early as the 4th century B.C.,Androsthenes, scribe to Alexander the Great, noted that the leaves ofTamarindus indica opened during the day and closed at night (Bretzl 1903).

Some early writers noticed single movements of parts of plants in a cur-sory manner. Albertus Magnus in the 13th century and Valerius Cordus inthe 16th thought the daily periodical movements of the pinnate leaves ofsome Leguminosae worth recording (Albertus Magnus 1260; for Cordus 1544,see Sprague and Sprague 1939). John Ray, in his ‘Historia Plantarum’ towardsthe end of the 17th century (Ray 1686–1704), commences his general consid-erations on the nature of plants with a succinct account of phytodynamicalphenomena, but does not clearly distinguish between movements stemmingfrom irritability and those showing daily, periodical rhythms; the latter, hewrites, occur not only in the leaves of Leguminosae but also in almost all sim-ilar pinnate leaves. In addition to these periodical movements of leaves, hereports the periodical opening and closing of the flowers of Calendula,Convolvulus, Cichorium and others.

In 1729, the French physicist Jean Jacques d’Ortous de Mairan discoveredthat mimosa plants kept in darkness continued to raise and lower their leaveswith a ~24 h rhythm. He concluded that plants must contain some sort ofinternal control mechanism regulating when to open or close the leaves.

Carolus Linnaeus studied the periodical movements of flowers in 1751 andthose of leaves in 1755, but offered no mechanical explanation (Linnaeus1770). He contented himself with describing the external conditions of thesephenomena in many species, classifying them and giving a new name – sleep

of plant – to those periodical movements observed at night, considering thatthe plants had then assumed a position of sleep. Indeed, he did not use theword at all in a metaphoric sense, for he saw in this sleep of plants a phe-nomenon entirely analogous to that in animals. It should also be mentionedthat he stated correctly that the movements connected with the sleep of plantswere not caused by changes in temperature but rather by change in light,since these took place at uniform temperature in a conservatory. Knowingthat each species of flower has a unique time of day for opening and closing,Linnaeus designed a garden clock in which the hours were represented by dif-ferent varieties of flowers. His work supported the idea that different speciesof organisms demonstrate unique rhythms.

Building on these classical findings, the last decades have experienced aperiod of unprecedented progress in the study of rhythmical phenomena inplants. Innovations in molecular biology, micro- and nanotechnology andapplied mathematics (e.g. hidden patterns, chaos theory) are providing newtools for understanding how environmental signals and internal clocks regu-late rhythmic gene expression and development. Needless to say, this fast,nearly astounding pace of discoveries shows how extremely this subject haschanged, and this is well reflected in the various chapters of this book whichcovers aspects of plant physiology neither recognisable nor quantifiable onlya few years ago.

The capacity to experience oscillations is a characteristic inherent to livingorganisms. Many rhythms, at different levels extending from the cell to theentire plant, persist even in complete isolation from major known environ-mental cycles. Actually, 24-h rhythms (circadian rhythms) are not the onlybiological rhythms detectable in plants – there are also those extending overlonger periods (infradian rhythms), either a month, year or a number ofyears, as well as shorter rhythms (ultradian rhythms) lasting several hours,minutes, seconds, etc. Accordingly, natural rhythms can be considered to lieoutside the periods of geophysical cycles. This means that living matter hasits own time, i.e. the ‘biological time’ is a specific parameter of living func-tions which can not be neglected, as has often been the case in traditionalplant biology.

Unlike circadian rhythms, ultradian rhythms have received little attentionfrom plant biologists. Among the causes of this underestimation is the factthat ultradian rhythms are readily overlooked in experiments in whichobservations are made only intermittently, or are treated as unwanted noise.Classically, oscillations of data during discontinuous measurements are eitherignored or attributed to sampling inaccuracy or error in the technique used,rather than to biological rhythmicity. In addition, the common practice ofpooling and averaging data collected from different specimens will serve –given that no two specimens are likely to be completely in phase – to obscurerhythmicity. On the whole, modern plant biology is poorly equipped for thestudy of ultradian rhythms. These are best studied in single specimens, usinghigh-resolution, non-invasive, uninterrupted recording techniques. Such a

viii Preface

holistic approach to physiology runs counter-current to the prevalent reduc-tionism which emphasizes the use of averaged data collected by means ofinvasive measurements in as many samples as possible.

It must be noted that, since biological rhythms are genetically transmitted,these phenomena necessarily have an inherited character. Researchers areaware of the fact that plants live and act in time. Therefore, the concept ofcyclic biological time is not entirely extraneous to scientific doctrine.Traditionally, however, plant biologists consider time as an implicit quantity,relegating it to a role of external factor.

It has been suggested that the gene inherits not only the capacity to clonebut also the capacity to endure (chronon). The concept of chronon refersto the expression of genes as a function of chronological time. The conceptof chronome relates to the expression of genes as a function of biological time,which is cyclical, irreversible and recursive. Accordingly, chronologicaltime could be seen as the summation of iterated periods, which constitutethe time base of biological rhythms.

The cycles of life are ultimately biochemical in mechanism but many of theprinciples which dominate their orchestration are essentially mathematical.Thus, the task of understanding the origins of rhythmic processes in plants,apart from numerous experimental questions, challenges theoretical prob-lems at different levels, ranging from molecules to plant behaviour. The studyof data on biological fluctuations can be the means of discovering the exis-tence of underlying rhythms. It might be of interest, for example, to accountfor periodic variability in measurements of hormone concentrations, mem-brane transport rates, ion fluxes, protein production, etc. Nevertheless,before engaging in the necessary statistical processing for the detection ofcycles in a system, it is essential to represent the system to be studied bymeans of a model: one that is explicative or one that is representative andpredictive.

This volume concentrates on modelling approaches from the level of cellsto the entire plant, focusing on phenomenological models and theoreticalconcepts. The book has been subdivided into four main parts, namely:

1. Physiological implications of oscillatory processes in plants;2. Stomata oscillations;3. Rhythms, clocks and development;4. Theoretical aspects of rhythmical plant behaviour,

assembled for an intended audience composed of the large and heteroge-neous group of science students and working scientists who must, due to thenature of their work, deal with the study and modelling of data originatingfrom rhythmic systems in plants. Hopefully, the wide range of subjects willexcite the interest of readers from many branches of science: physicists orchemists who wish to learn about rhythms in plant biology, and biologistswho wish to learn how these rhythmic models are generated.

Preface ix

Finally, the Editors gratefully acknowledge the assistance of a number ofpeople and institutions without whose help this project could not have beencarried out. First of all, we are most deeply indebted to the contributors of thechapters presented here, whose enthusiasm and dedication have made thisbook a reality. We also acknowledge the Fondazione Ente Cassa di Risparmiodi Firenze for financial support given to the LINV – Laboratorio Internazio-nale di Neurobiologia Vegetale, University of Firenze, as well as the AustralianResearch Council for supporting research on membrane transport oscillatorsat the University of Tasmania. Last but not least, we express our sincere appre-ciation to Dr. Andrea Schlitzberger and Dr. Christina Eckey, at Springer, fortheir guidance and assistance during the production of the book.

December 2006 Stefano MancusoSergey Shabala

References

Albertus Magnus (1260) De vegetabilibus. Wissenschaftliche Verlagsgesellschaft, Stuttgart, 1992edn

Bretzl H (1903) Botanische Forschungen des Alexanderzuges. Teubner, LeipzigCordus V (1544) Historia Plantarum. (cf. text)d’Ortous de Mairan JJ (1729) Observation botanique. Histoire de l’Académie Royale des

Sciences, ParisLinnaeus C (1770) Philosophia Botanica. Joannis Thomae nob. de Trattnern, ViennaRay J (1686–1704) Historia plantarum, species hactenus editas aliasque insuper multas noviter

inventas & descriptas complectens. Mariae Clark, LondonSprague TA, Sprague MS (1939) The herbal of Valerius Cordus. Linnean Society, London

x Preface

Contents

Part 1Physiological Implications of Oscillatory Processes in Plants . . . . . . . . . . . . . . . . . . . 1

1 Rhythmic Leaf Movements: Physiological and Molecular Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3NAVA MORAN

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

1.1.1 Historical Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31.1.2 The Types of Leaf Movements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

1.2 The Mechanism of Leaf Movement: the Osmotic Motor . . . . . . . . . . . . . . . 71.2.1 Volume Changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71.2.2 The Ionic Basis for the Osmotic Motor . . . . . . . . . . . . . . . . . . . . . . . 81.2.3 Plasma Membrane Transporters . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101.2.4 Tonoplast Transporters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

1.3 Mechanisms of Regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171.3.1 Regulation by Protein Modification – Phosphorylation . . . . . . . . . 171.3.2 The Perception of Light . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 211.3.3 Intermediate Steps . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231.3.4 Regulation by Other Effectors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28

1.4 Unanswered Questions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 301.4.1 Acute, Fast Signalling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 311.4.2 The Clock Input and Output . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32

2 The Pollen Tube Oscillator: Integrating Biophysics and Biochemistry into Cellular Growth and Morphogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39NUNO MORENO, RENATO COLAÇO AND JOSÉ A. FEIJÓ

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 392.1 Finding Stability in Instability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 392.2 Why Pollen Tubes? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .422.3 Growth Oscillations: Trembling with Anticipation? . . . . . . . . . . . . . . . . . . 422.4 Under Pressure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 452.5 Another Brick in the Cell Wall . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 462.6 Cytosolic Approaches to Oscillations: the Ions Within . . . . . . . . . . . . . . . . 472.7 On the Outside: Ions and Fluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 512.8 Actin Cytoskeleton: Pushing it to the Limit . . . . . . . . . . . . . . . . . . . . . . . . . 54

2.9 Membrane Trafficking and Signalling on the Road . . . . . . . . . . . . . . . . . . 552.10 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58

3 Ultradian Growth Oscillations in Organs: Physiological Signal or Noise? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63TOBIAS I. BASKIN

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 633.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63

3.1.1 Oscillations as Window into Growth . . . . . . . . . . . . . . . . . . . . . . . 633.1.2 Growth Versus Movement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65

3.2 Circumnutation: Growing Around in Circles? . . . . . . . . . . . . . . . . . . . . . . 653.3 In Search of Ultradian Growth Oscillations . . . . . . . . . . . . . . . . . . . . . . . . 683.4 The Power of Bending in Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 703.5 Conclusion and Perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73

4 Nutation in Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77SERGIO MUGNAI, ELISA AZZARELLO, ELISA MASI, CAMILLA PANDOLFI

AND STEFANO MANCUSO

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 774.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 774.2 Theories and Models for Circumnutation . . . . . . . . . . . . . . . . . . . . . . . . . . 81

4.2.1 ‘Internal Oscillator’ Model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 834.2.2 ‘Gravitropic Overshoot’ Model . . . . . . . . . . . . . . . . . . . . . . . . . . . . 844.2.3 The ‘Mediating’ Model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85

4.3 Root Circumnutation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88

Part 2Stomata Oscillations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91

5 Oscillations in Plant Transpiration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93ANDERS JOHNSSON

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 935.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 935.2 Models for Rhythmic Water Transpiration . . . . . . . . . . . . . . . . . . . . . . . . 95

5.2.1 Overall Description – “Lumped” Model . . . . . . . . . . . . . . . . . . . . . 955.2.2 Overall Description – “Composed” Models . . . . . . . . . . . . . . . . . . 975.2.3 Self-Sustained Guard Cell Oscillations –

(Ca2+)cyt Oscillations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 985.2.4 Water Channels . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 985.2.5 Comments on Modelling Transpiration Rhythms . . . . . . . . . . . . . 99

5.3 Basic Experimental Methods Used . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 995.4 Experimental Findings on Transpiration Oscillations . . . . . . . . . . . . . . 100

5.4.1 Occurrence of Transpiration Rhythms: Period of Rhythms . . . . 1015.4.2 Some Environmental Parameters Influencing Oscillations . . . . 1015.4.3 Singularities of Transpiration Rhythms: Test of Models . . . . . . . 104

xii Contents

5.5 Ionic Interference with Transpiration Oscillations . . . . . . . . . . . . . . . . . . 1055.6 Patchy Water Transpiration from Leaf Surface . . . . . . . . . . . . . . . . . . . . . 1065.7 Period Doubling and Bifurcations in Transpiration –

a Way to Chaos? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1075.8 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111

6 Membrane Transport and Ca2+ Oscillations in Guard Cells . . . . . . . . . . . . . . . . 115MICHAEL R. BLATT, CARLOS GARCIA-MATA AND SERGEI SOKOLOVSKI

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1156.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1156.2 Oscillations and the Membrane Platform . . . . . . . . . . . . . . . . . . . . . . . . . . 1166.3 Elements of Guard Cell Ion Transport . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1196.4 Ca2+ and Voltage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 121

6.4.1 The Ca2+ Theme . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1226.4.2 [Ca2+]i Oscillations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1236.4.3 Voltage Oscillations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1246.4.4 Membrane Voltage and the ‘[Ca2+]i Cassette’ . . . . . . . . . . . . . . . . . 125

6.5 Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 128

7 Calcium Oscillations in Guard Cell Adaptive Responses to the Environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135MARTIN R. MCAINSH

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1357.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1357.2 Guard Cells and Specificity in Ca2+ Signalling . . . . . . . . . . . . . . . . . . . . . . 1377.3 Ca2+ Signatures: Encoding Specificity in Ca2+ Signals . . . . . . . . . . . . . . . . 138

7.4.1 Guard Cell Ca2+ Signatures: Correlative Evidence . . . . . . . . . . . . . 1407.4.2 Guard Cell Ca2+ Signatures: Evidence

for a Causal Relationship . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1467.4.3 Guard Cell Ca2+ Signatures: the Role of Oscillations . . . . . . . . . . . 147

7.5 The Ca2+ Sensor Priming Model of Guard Cell Ca2+ Signalling . . . . . . . . 1487.6 Decoding Ca2+ Signatures in Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1497.7 Challenging Prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152

8 Circadian Rhythms in Stomata: Physiological and Molecular Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 157KATHARINE E. HUBBARD, CARLOS T. HOTTA, MICHAEL J. GARDNER, SOENG JIN BAEK, NEIL DALCHAU, SUHITA DONTAMALA, ANTONY N. DODD AND ALEX A.R. WEBB

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1578.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1578.2 Mechanisms of Stomatal Movements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1598.3 The Circadian Clock . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1628.4 Circadian Regulation of Stomatal Aperture . . . . . . . . . . . . . . . . . . . . . . . . 1648.5 Structure of the Guard Cell Clock . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 166

Contents xiii

8.6 Mechanisms of Circadian Control of Guard Cell Physiology . . . . . . . . 1688.6.1 Calcium-Dependent Models for Circadian

Stomatal Movements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1698.6.2 Calcium-Independent Models for Circadian

Stomatal Movements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1708.7 Circadian Regulation of Sensitivity of Environmental

Signals (‘Gating’) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1718.8 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 172References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 172

Part 3Rhythms, Clocks and Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 179

9 How Plants Identify the Season by Using a Circadian Clock . . . . . . . . . . . . . . 181WOLFGANG ENGELMANN

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1819.1 Introduction and History . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1819.2 Examples for Photoperiodic Reactions . . . . . . . . . . . . . . . . . . . . . . . . . . 1849.3 Bünning Hypothesis and Critical Tests . . . . . . . . . . . . . . . . . . . . . . . . . 1859.4 The Circadian Clock and its Entrainment to the Day . . . . . . . . . . . . . . 1899.5 Seasonal Timing of Flower Induction . . . . . . . . . . . . . . . . . . . . . . . . . . . 191References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194

10 Rhythmic Stem Extension Growth and Leaf Movements as Markers of Plant Behaviour: the Integral Output from Endogenous and Environmental Signals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 199JOHANNES NORMANN, MARCO VERVLIET-SCHEEBAUM, JOLANA T.P. ALBRECHTOVÁ AND EDGAR WAGNER

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19910.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 200

10.1.1 Life is Rhythmic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20010.1.2 Rhythm Research: Metabolic and Genetic

Determination of Rhythmic Behaviour . . . . . . . . . . . . . . . . . . . 20110.2 Rhythmicity in Chenopodium spp. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203

10.2.1 Rhythmic Changes in Interorgan Communication of Growth Responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 206

10.2.2 Local Hydraulic Signalling: the Shoot Apex in Transition . . . 20910.2.3 Membrane Potential as the Basis for Hydro-

Electrochemical Signalling, Interorgan Communication and Metabolic Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 212

10.3 Conclusions and Perspectives: Rhythms in Energy Metabolism asDeterminants for Rhythmic Growth and Leaf Movements . . . . . . . . . . 213

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 215

11 Rhythms and Morphogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 219PETER W. BARLOW AND JACQUELINE LÜCK


xiv Contents

11.2 Developmental Theories and Their Application to RhythmicMorphogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 220

11.3 Rhythmic Patterns of Cellular Development Within Cell Files . . . . . . 22111.4 Organogenetic Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 227

11.4.1 Angiosperm Shoot Apices and Their Phyllotaxies . . . . . . . . . . 22811.4.2 The Plastochron . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23111.4.3 A Petri Net Representation of the Plastochron . . . . . . . . . . . . 23211.4.4 Rhythms of Cell Determination and the Plastochron . . . . . . . 236

11.5 The Cycle of Life . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23711.6 A Glimpse of Cell Biology and Morphogenetic Rhythms . . . . . . . . . . . 238References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 240

12 Molecular Aspects of the Arabidopsis Circadian Clock . . . . . . . . . . . . . . . . . . . 245TRACEY ANN CUIN


12.1.1 Defining Features of Circadian Rhythms . . . . . . . . . . . . . . . . . 24612.1.2 Overview of the Circadian System in Arabidopsis . . . . . . . . . . 246

12.2 Entrainment – Inputs to the Clock . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24712.2.1 Light . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24712.2.2 Pathways to the Central Oscillator . . . . . . . . . . . . . . . . . . . . . . 24912.2.3 Negative Regulation of Photoentrainment . . . . . . . . . . . . . . . . 25312.2.4 Temperature Entrainment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 253

12.3 The Central Oscillator . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25412.3.1 The CCA1/LHY-TOC1 Model for the Arabidopsis

Central Oscillator . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25412.3.2 Is There more than One Oscillator Within Plants? . . . . . . . . . 25612.3.3 Regulation of the Circadian Oscillator . . . . . . . . . . . . . . . . . . . 257

12.4 Outputs of the Circadian System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25812.5 Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259

Part 4Theoretical Aspects of Rhythmical Plant Behaviour . . . . . . . . . . . . . . . . . . . . . . . . . 265

13 Rhythms, Clocks and Deterministic Chaos in Unicellular Organisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 267DAVID LLOYD

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26713.1 Time in Biology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26813.2 Circadian Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 270

13.2.1 Circadian Timekeeping in Unicellular Organisms . . . . . . . . . . 27013.2.2 Cyanobacterial Circadian Rhythms . . . . . . . . . . . . . . . . . . . . . . 270

13.3 Ultradian Rhythms: the 40-Min Clock in Yeast . . . . . . . . . . . . . . . . . . . 27113.4 Oscillatory Behaviour During the Cell Division Cycles

of Lower Organisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27713.5 Ultradian Gating of the Cell Division Cycle . . . . . . . . . . . . . . . . . . . . . . 278

13.5.1 Experimental Systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 278

Contents xv

13.5.2 The Model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27913.5.3 Computer Simulations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 279

13.6 Chaos in Biochemistry and Physiology . . . . . . . . . . . . . . . . . . . . . . . . . . 28213.7 Functions of Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28413.8 Biological Functions of Chaotic Performance . . . . . . . . . . . . . . . . . . . . 28613.9 Evolution of Rhythmic Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . 286References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 288

14 Modelling Ca2+ Oscillations in Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 295GERALD SCHÖNKNECHT AND CLAUDIA BAUER

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29514.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29614.2 Developing a Mathematical Model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29714.3 Discussion of the Model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 304References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 309

15 Noise-Induced Phenomena and Complex Rhythms: TheoreticalConsiderations, Modelling and Experimental Evidence . . . . . . . . . . . . . . . . . . 313MARC-THORSTEN HÜTT AND ULRICH LÜTTGE

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31315.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31415.2 Case Study I – Crassulacean Acid Metabolism (CAM) . . . . . . . . . . . . . 31515.3 Case Study II – Stomatal Patterns . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32315.4 Experimental Observations of Complex Rhythms in Plants . . . . . . . . . 32715.5 A Path Towards Systems Biology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 330References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 335

16 Modelling Oscillations of Membrane Potential Difference . . . . . . . . . . . . . . . 341MARY JANE BEILBY

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34116.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34116.2 Single Transporter Oscillations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 342

16.2.1 Proton Pump and the Background State in Charophytes . . . . 34216.2.2 Putative K+ Pump and the Background State

in Ventricaria ventricosa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34616.3 Two Transporter Interaction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 346

16.3.1 Proton Pump and the Background State in HypertonicRegulation in Lamprothamnium spp. . . . . . . . . . . . . . . . . . . . . 346

16.3.2 Interaction of the Proton Pump and the Proton Channel in Chara spp. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 348

16.4 Multiple Transporter Interaction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35016.4.1 Hypotonic Regulation in Salt-Tolerant Charophytes . . . . . . . 35016.4.2 Repetitive Action Potentials in Salt-Sensitive

Charophytes in High Salinity . . . . . . . . . . . . . . . . . . . . . . . . . . . 35216.5 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 354References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 354

Subject Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 357

xvi Contents

List of Contributors

ALBRECHTOVÁ, JOLANA T.P.Institut für Biologie II, Albert-Ludwigs-Universität Freiburg, Schaenzlestr.1, 79104 Freiburg, Germany

AZZARELLO, ELISA

LINV–International Lab for Plant Neurobiology, Department ofHorticulture, Polo Scientifico, University of Florence, viale delle idee 30,50019 Sesto Fiorentino (FI), Italy

BAEK, SOENG JIN

Department of Plant Sciences, University of Cambridge, Downing Street,Cambridge CB2 3EA, UK

BARLOW, PETER W.School of Biological Sciences, University of Bristol, Woodland Road, BristolBS8 1UG, UK, e-mail: [email protected]

BASKIN, TOBIAS I.Biology Department, University of Massachusetts, Amherst, MA 01003,USA, e-mail: [email protected]

BAUER, CLAUDIA

Department of Biomedical Sciences, University of Sheffield, Western Bank,Sheffield S10 2TN, UK

BEILBY, MARY JANE

School of Physics, The University of New South Wales, NSW 2052,Australia, e-mail: [email protected]

BLATT, MICHAEL R.Laboratory of Plant Physiology and Biophysics, Institute of Biomedical andLife Sciences, University of Glasgow, Glasgow G12 8QQ, UK, e-mail: [email protected]

COLAÇO, RENATO

Centro de Biologia do Desenvolvimento, Instituto Gulbenkian de Ciência,2780-156 Oeiras, Portugal

CUIN, TRACEY ANN

School of Agricultural Science, University of Tasmania, Private Bag 54,Hobart, Tasmania 7001, Australia, e-mail: [email protected]

DALCHAU, NEIL


DODD, ANTONY N.Department of Plant Sciences, University of Cambridge, Downing Street,Cambridge CB2 3EA, UK

DONTAMALA, SUHITA


ENGELMANN, WOLFGANG

University of Tübingen, Physiologische Ökologie der Pflanzen, Auf derMorgenstelle 1, 72076 Tübingen, Germany, e-mail: [email protected]

FEIJÓ, JOSÉ A.Centro de Biologia do Desenvolvimento, Instituto Gulbenkian de Ciência,PT-2780-156 Oeiras, Portugal; Universidade de Lisboa, Faculdade deCiências, Dept. Biologia Vegetal, Campo Grande C2, 1749-016 Lisboa,Portugal, e-mail: [email protected]

GARCIA-MATA, CARLOS

Laboratory of Plant Physiology and Biophysics, Institute of Biomedical andLife Sciences, University of Glasgow, Glasgow G12 8QQ, UK

GARDNER, MICHAEL J.Department of Plant Sciences, University of Cambridge, Downing Street,Cambridge CB2 3EA, UK

HOTTA, CARLOS T.Department of Plant Sciences, University of Cambridge, Downing Street,Cambridge CB2 3EA, UK

HUBBARD, KATHARINE E.Department of Plant Sciences, University of Cambridge, Downing Street,Cambridge CB2 3EA, UK

HÜTT, MARC-THORSTEN

Computational Systems Biology, School of Engineering and Science,International University Bremen, Campus Ring 1, 28759 Bremen, Germany

xviii List of Contributors

JOHNSSON, ANDERS

Department of Physics, Norwegian University of Science and Technology,NTNU, 7491 Trondheim, Norway, e-mail: [email protected]

LLOYD, DAVID

Microbiology (BIOSI 1), Cardiff School of Biosciences, Cardiff University,P.O. Box 915, Cardiff CF10 3TL, Wales, UK, e-mail: [email protected]

LÜCK, JACQUELINE

Atelier de Structuralisme Végétal, 1226 Chemin du Val d’Arenc, 83330 LeBeausset, France

LÜTTGE, ULRICH

Institut für Botanik, Technische Universität Darmstadt, Schnittspahnstraße3-5, 64287 Darmstadt, Germany, e-mail: [email protected]

MANCUSO, STEFANO

LINV–International Lab for Plant Neurobiology, Department ofHorticulture, Polo Scientifico, University of Florence, viale delle idee 30,50019 Sesto Fiorentino (FI), Italy, e-mail: [email protected]

MASI, ELISA


MCAINSH, MARTIN R.Lancaster Environment Centre, Department of Biological Sciences,Lancaster University, Lancaster LA1 4YQ, UK, e-mail: [email protected]

MORAN, NAVA

The R.H. Smith Institute of Plant Sciences and Genetics in Agriculture,Faculty of Agricultural, Food and Environmental Quality Sciences, TheHebrew University of Jerusalem, Rehovot 76100, Israel, e-mail: [email protected]

MORENO, NUNO

Centro de Biologia do Desenvolvimento, Instituto Gulbenkian de Ciência,2780-156 Oeiras, Portugal

MUGNAI, SERGIO


List of Contributors xix

NORMANN, JOHANNES

Institut für Biologie II, Albert-Ludwigs-Universität Freiburg, Schaenzlestr. 1,79104 Freiburg, Germany

PANDOLFI, CAMILLA


SCHÖNKNECHT, GERALD

Department of Botany, Oklahoma State University, Stillwater, OK 74078,USA, e-mail: [email protected]

SOKOLOVSKI, SERGEI

Laboratory of Plant Physiology and Biophysics, Institute of Biomedical andLife Sciences, University of Glasgow, Glasgow G12 8QQ, UK

VERVLIET-SCHEEBAUM, MARCO

Institut für Biologie II, Albert-Ludwigs-Universität Freiburg, Schaenzlestr. 1,79104 Freiburg, Germany

WAGNER, EDGAR

Institut für Biologie II, Albert-Ludwigs-Universität Freiburg, Schaenzlestr. 1, 79104 Freiburg, Germany, e-mail: [email protected]

WEBB, ALEX A.R.Department of Plant Sciences, University of Cambridge, Downing Street,Cambridge CB2 3EA, UK, e-mail: [email protected]

xx List of Contributors

Part 1Physiological Implications of Oscillatory Processes in Plants

1 Rhythmic Leaf Movements: Physiological and Molecular Aspects

NAVA MORAN

Abstract

Daily periodic plant leaf movements, known since antiquity, are dramaticmanifestations of “osmotic motors” regulated by the endogenous biologicalclock and by light, perceived by phytochrome and, possibly, by phototropins.Both the reversible movements and their regulation usually occur in special-ized motor leaf organs, pulvini. The movements result from opposing volumechanges in two oppositely positioned parts of the pulvinus. Water fluxes intothe motor cells in the swelling part and out of the motor cells in the con-comitantly shrinking part are powered by ion fluxes into and out of thesecells, and all of these fluxes occur through tightly regulated membranal pro-teins: pumps, carriers, and ion and water channels. This chapter attempts topiece together those findings and insights about this mechanism which haveaccumulated during the past one and a half decades.

1.1 Introduction

1.1.1 Historical Perspective

Almost every text on chronobiology tells us that the ancients were alreadyaware of the rhythmic movements of plants, and even relied on them inscheduling their prayers. The first documented experiment attemptingto resolve if this rhythm was inherent to the plant, rather than beingstimulated by sunlight, was that of the French astronomer, De Mairan. Hissensitive plant (probably Mimosa pudica) continued moving its leaves evenwhen kept in darkness (De Mairan 1729). Since De Mairan’s days, and forover 2 centuries, leaf movements served as the sole indicators of the internalworking of plants, and increasingly intricate designs were conceived for

S. Mancuso and S. Shabala (Eds.)Rhythms in Plants: Phenomenology, Mechanisms, and Adaptive Significance© Springer-Verlag Berlin Heidelberg 2007

The R.H. Smith Institute of Plant Sciences and Genetics in Agriculture, Faculty of Agricultural, Foodand Environmental Quality Sciences, The Hebrew University of Jerusalem, Rehovot 76100, Israel, e-mail: [email protected]

movement-monitoring devices (see also Nozue and Maloof 2006). During the18th and the 19th centuries, experiments with the “sleep movements” ofleaves (a name coined by Linnaeus) led to the gradual emergence of the con-cept of the osmotic motor (Pfeffer 1877), and of the concept of an internaloscillator – an endogenous biological clock – for which leaf movements serveas “clock hands”. In the 20th century, biological clocks began to be studiedalso in animals. Beatrice Sweeney presented a detailed and vivid account ofthis conceptual evolution (Sweeney 1987).

Among the best studied rhythmic movements are those of the pulvini ofthe compound leaves of the legumes Albizzia, Mimosa, Samanea, Robiniaand Phaseolus. While observing the “hands of the clock”, investigatorsprobed the internal mechanism, in an attempt to map the susceptibility of theoscillator and, thus, to deduce its chemical nature. They altered the illumina-tion regimes, varied the light intensity and quality, and applied various phar-macological agents to the pulvinus (e.g. see the review by Satter and Galston1981 and, more recently, work by Mayer et al. 1997, and Gomez et al. 1999).During the past few decades, an increasing arsenal of technological develop-ments enabled more sophisticated measurements and monitoring of vari-ables other than only leaf displacement. The forces involved in the movementhave been determined (Gorton 1990; Irving et al. 1997; Koller 2001), immuno-histochemistry has been applied (e.g. in the cellular immuno-gold localiza-tion of phytochrome, the photoreceptor affecting leaf movement; Moyssetet al. 2001), the related distribution of various ions and other elements hasbeen studied using ion-selective microelectrodes (e.g. Lee and Satter 1989;Lowen and Satter 1989), and X-ray microanalysis (e.g. Satter et al. 1982;Fromm and Eschrich 1988c; Moysset et al. 1991), patch-clamp and molecularbiology analyses of pulvinar channels have begun (Moran et al. 1988; Stoeckeland Takeda 1993; Jaensch and Findlay 1998; Moshelion et al. 2002a, b).

Initial answers to the intriguing questions about how leaf movement isexecuted, and how the endogenous rhythm – and external signals, mainlylight – affect the pulvinar “motor” have been collected in a small but thoroughcompendium on the pulvinus by Satter et al. (1990). During the following16 years, these questions have been addressed with an increasing resolution,sometimes “borrowing” from the molecular insights developed in the muchmore numerous and extensive studies of stomatal guard cells (as in Fanet al. 2004). These later findings and insights into leaf movements are themain focus of this chapter.

1.1.2 The Types of Leaf Movements

Leaf movements can be repetitious and rhythmic, or provoked (Fig. 1.1).Stimulated movements can be classified according to their directionality:tropic movements are related to the direction of the stimulus which causedthem whereas nastic movements are stimulus unrelated. Thus, leaf unfolding

4 Nava Moran

in response to the turning on of diffuse light is photonastic whereas leaf fold-ing with the onset of darkness is scotonastic; the turning of leaves towardsdirected light is termed phototropic and, towards the sun, heliotropic(Fig. 1.1c). Movement in response to touch – such as the clasping of theVenus fly trap (Dionaea muscipula) leaf lobes when irritated by an insect, orthe curling of a gently stroked pea tendril – is termed thigmonastic; the folding down of the Mimosa pudica leaf upon shaking the plant is seismonasticand, upon exposure to the heat of a flame, thermonastic; the turning of leavesupwards after the shoot is placed horizontally is negatively gravitropic.Frequently, leaves perform more than one type of movements, and differentparts of a leaf can perform different types of movements. For example, theMimosa primary pulvinus exhibits also nyctinasty, seismonasty and thig-monasty whereas the secondary pulvinus does not respond to seismonasticstimuli (Fig. 1.1b; Fromm and Eschrich 1988b). Samanea leaf movements arelargely insensitive to touch and shaking.

Rhythmic Leaf Movements: Physiological and Molecular Aspects 5

DAY NIGHTNON -stim

Stim

p

PI

NON -stim

Stim

PII

ra

PIII

rs

B

6:00 7:30 10:00 12:00 16:00

C

vb

F

E

rs

ra

PIII

PII

DAY

NIGHT

A

Fig. 1.1 Types of leaf movements. A Nyctinastic movements of the terminal pinnae of the com-pound leaf of Samanea saman (Jacq.) Merrill. Insets A schematic drawing of a pulvinus: E exten-sor, F flexor, vb vascular bundle, PII, PIII secondary and tertiary pulvini, ra rachilla, rs rachis(reproduced with permission, Moshelion et al. 2002a). B Seismonastic and nyctinastic leafmovement of Mimosa pudica L.: p pinnae, PI primary pulvinus; other abbreviations as in A(reproduced with permission, Fromm and Eschrich 1988b). C Primary (laminar) leaves ofPhaseolus vulgaris L., showing paraheliotropism in the field (reproduced with permission, Berg1986). Note the movement of the leaf blades (arrows), adjusting the angle of the incident light(dashed arrows) at the indicated hours. A “purely” nyctinastic movement in the laboratorywould occur between a horizontal and a vertical-down position of both leaves (not shown)

Rhythmic leaf movements can be related to growth and be non-reversible,such as those of cotyledons of Arabidopsis seedlings or the leaves of growingtobacco plants. The epinastic leaf movement of tobacco, for example, is basedon alternating spurts of growth of the upper and lower leaf surface, and thisuneven growth reveals a control by light and the circadian clock (Siefritz et al.2004). Other examples can be found in a review by Wetherell (1990). Whilethe tissue expansion likely occurs via a mechanism similar to that for pulv-inar tissues (see below), the irreversibility of these growth processes isthought to be related to interstitial deposits in cell wall material and todecrease in wall extensibility (Wetherell 1990, and references therein).

Rhythmic leaf movements can be completely reversible, such as the nycti-nastic movements of many legumes (Samanea saman, Accacia lophanta,Albizzia julibrissin, Phaseolus vulgaris, Desmodium gyrans and the above-mentioned Mimosa pudica), and also of some plants of a few other families,e.g. wood sorrels (Oxalidaceae) and mallows (Malvaceae). These reversiblemovements originate in the pulvinus (Fig. 1.1), a mature, specialized motororgan at the leaf base, and their daily persistence is a manifestation of regu-lation by light and the circadian clock. In the dark or under constant low-levelillumination, the circadian rhythm displays its “free-running”, geneticallydictated periodicity which can range from roughly 20 to 29 h. Period lengthand its manifestation depend also on other factors. For example, in Phaseoluscoccineus, the circadian laminar leaf movement started 9 days after sowing insoil. The period length decreased progressively with pulvinus maturation(from 31.3 to 28.6 h under constant illumination), and these periods becamemore than 1 h shorter when the leaves were cut off and watered via petioles(Mayer et al. 1999).

Normally, however, daily light resets the phase of the rhythm and adjustsit to a 24-h period. Rhythmic movements can additionally comprise one ormore ultradian rhythms (with significantly shorter periods – between tens ofminutes to several hours; Millet et al. 1988; Engelmann and Antkowiak 1998;see also chapter [3] on ultradian rhythms).

Light has a profound effect on the rhythmic leaf movement, and it is alsoeasily quantifiable. Therefore, this stimulus is very widely used to perturb leafmovement rhythms, to change their phase, and to alter their period.Changing these two rhythm properties is a key criterion for having affectedthe internal “oscillator”. Red, far-red and blue light have different effects onthe rhythm (reviewed by Satter and Galston 1981; Sweeney 1987).

Acute Versus Circadian It is important to note that the same stimuli evokealso short-lived, or acute, responses lasting for only one to a few periods fol-lowing the stimulus. These transient responses are superimposed on(“mask”) the responses attributable to changes in the clock (shifting thephase and changing the period length), which persist during many cycles. Inthe very schematic general portrayal of the system shown in Fig. 1.2, theclock-resetting stimulus acts along an input pathway to the clock, altering the

6 Nava Moran

way the clock directs the osmotic motor of the leaf movement, while the acutestimulus bypasses the clock and acts directly on the osmotic motor.Employing “acute” stimuli in the study of the clock’s role in regulating leafmovement is justified by the underlying assumptions (1) that the mechanismof the execution of the movements, i.e. of the volume and turgor changes, isidentical for both types of movements, the stimulated and the rhythmic, and(2) that the photoreceptors in both pathways are identical (which, in plants,has not yet been disproved). Thus, both pathways are assumed to differwholly, or partially, “only” in the transduction cascades, i.e. in the chemicalreactions between light perception and the regulation of the transporters.

1.2 The Mechanism of Leaf Movement: the Osmotic Motor

1.2.1 Volume Changes

1.2.1.1 The Mechanics of Movement

Since the movement of a leaf or leaflet results from the changes in the shapeof its subtending pulvinus, volume changes must occur anisotropically inthe pulvinar tissues. Indeed, the pulvinar motor consists of two distinct,positionally and functionally opposed regions: an “extensor” – whichextends longitudinally during leaf opening, and a “flexor”, which appearscontracting (“flexing”) longitudinally at the same time. During leaf closure,the reverse changes occur. Radial inflexibility of the epidermis constrainsthese changes to the longitudinal axis but the flexibility of the vascular core,along with its inextendability, cause the curvature of the pulvinus without,in fact, affecting its length (Koller and Zamski 2002). It appears that exten-sors and flexors differ also in the extent of generating the movement-drivingpressures. For example, in the Phaseolus vulgaris laminar pulvinus, the


aLIGHT

VOLUME CHANGES

CLOCK b

c

R

~

~

Fig. 1.2 Light stimulates cell volume changes. A model of clock-mediated (circadian) andclock-independent (“acute”) pathways. a Light, perceived by one or more light receptor(s), R,affects the clock. b The clock governs volume changes, imparting fluctuations (~) in activityor in abundance to the pathway intermediates. c Light affects directly the volume changes(bidirectional arrow)

excision of the flexor did not seem to alter any of the properties of the circa-dian leaf oscillation – period, phase and amplitude – whereas, when themajor part of the extensor was cut away, the amplitude was greatly reduced(although the period and the phase of the leaf movements remainedunchanged; Millet et al. 1989).

1.2.1.2 Volume Changes of Isolated Protoplasts

The turgor changes in the pulvinar motor tissues reflect the turgor changes ofthe individual motor cells and these, in turn, reflect the elastic propertiesof the cell walls, together with the volume changes. Confounding effects of thecell wall may be avoided if experiments are performed on protoplasts.Indeed, protoplasts appear to be an appropriate physiological system forstudying the circadian rhythm of volume changes. Flexor protoplasts isolatedfrom the bean (P. coccineus) laminar pulvini swelled and shrunk under con-tinuous light for over 200 h with a 28-h period, resembling the period of thepulvinar cells in situ under similar conditions (Mayer and Fischer 1994).Extensor protoplasts seemed to exhibit the same rhythm and, curiously, theycycled with the same phase as the flexors, at least during the initial 70 h, as iftheir internal clock had shifted by 180° relative to their original in-siturhythm. Nevertheless, the extensors could be entrained to a 24-h rhythm bycycles of 14 h light/10 h dark, this time shrinking “appropriately” in darkness(Mayer and Fischer 1994). Thus, the isolated pulvinar protoplasts seem to“remember” their origin and retain the physiological properties of theirsource tissues. Moreover, the motor cells of the pulvinus are themselves thesite of the rhythm generator, containing both the “oscillator” and the“motor”, as evident from the rhythmic volume changes of isolated proto-plasts (in Phaseolus, Mayer and Fischer 1994, and also as shown for flexors ofSamanea by Moran et al. 1996).

1.2.2 The Ionic Basis for the Osmotic Motor

1.2.2.1 The Current Model

The currently accepted model for the volume changes of pulvinar cells doesnot differ in principle from that accepted for the stomata guard cells, withan exception that in contrast to guard cells, in the intact pulvinus the soluteand water fluxes may occur to some extent also via plasmodesmatainterconnecting the pulvinar motor cells (Morse and Satter 1979; Satteret al. 1982).

In the swelling phase, an activated proton pump (a P-type H+-ATPase)hyperpolarizes the cell, which creates the electrochemical gradient for theinflux of K+ via K channels (e.g., Kim et al. 1992, 1993) and the proton-motive

8 Nava Moran

force for the uphill uptake of Cl−, possibly via a proton-anion symporter(Satter et al. 1987), and which also open the gates of K+-influx channels.Eventually, K+ and Cl− accumulate in the cell vacuole. In the absence of exter-nal Cl−, the malate content of the swelling tissues increases (Mayer et al. 1987;Satter et al. 1987). Water, driven by the changing water potential differenceacross the cell membrane, increases the cell volume and turgor, entering thecells via the membrane matrix and via aquaporins.

In the shrinking phase, the proton pump halts and the motor cell depolar-izes. Depolarization may be aided by passive influx of Ca2+ via Ca channelsand passive efflux of Cl− via anion channels. K+-influx channels close whileK+-release channels open. The electrochemical gradient now drives also K+

efflux. Loss of solutes (KCl) drives water efflux via the membrane matrix andaquaporins. The volume and turgor of the motor cells decrease.

1.2.2.2 Membrane Potential

Changes in membrane potential provided early clues about the ionic basis ofleaf movement. Racusen and Satter measured the membrane potential inSamanea flexors and extensors in whole, continuously darkened, secondaryterminal pulvini impaled with microelectrodes, and found it to oscillate witha ca. 24-h rhythm between −85 and −40 mV (extensor) and between −100and −35 mV (flexors), with the extensors “sinusoid” preceding that ofthe flexors by about 8 h (Racusen and Satter 1975). Membrane potential var-ied also in response to light signals which caused leaf movement (see Sect.1.3.2.1 below, and Racusen and Satter 1975, and also Sect. 1.3.2.2). Latermeasurements of membrane potential, using a membrane-soluble fluores-cent dye (3,3′-dipropylthiadicarbocyanine iodide, DiS-C3(5)), providedadditional details about the translocation of ions (Kim et al. 1992, and seeSect. 1.2.3.4 below).

1.2.2.3 Mechanisms Underlying Volume Changes

Ions Involved in Leaf Movements Results of X-ray microanalysis suggestthat the solute concentration changes are primarily those of potassium andchloride, consistent with the occurrence of their massive fluxes across theplasma membrane into the swelling cells and out of the shrinking cells (Satterand Galston 1974; Kiyosawa 1979; Satter et al. 1982; Gorton and Satter 1984;Moysset et al. 1991). At the same time, measurements with ion-sensitiveelectrodes enabled dynamic, real-time observations of changes in theapoplastic activity of protons (Lee and Satter 1989) and potassium ions(Lowen and Satter 1989; Starrach and Meyer 1989). Generally, proton and K+

activities varied in opposite directions (see also Starrach and Meyer 1989 andreferences therein, and Lee 1990).


Non-Ionic Regulation Osmotically driven shrinking based on the efflux ofions normally suffices to explain volume changes on the scale of minutes. Thepuzzling rate of the seismonastic response of Mimosa pudica (leaflet foldingon the scale of seconds) invited additional investigations. Thus, seismonasticstimulation of the leaf caused sudden unloading of 14C-labelled sucrose fromthe phloem into the pulvinar apoplast in the primary pulvinus, loweringthe water potential beneath that of the extensors and probably enhancing theirshrinkage, leading to leaf closure within a few seconds. This was accompaniedby a brief membrane depolarization of the sieve-element, recorded via anaphid stylet serving as an intracellular microelectrode. During re-swelling, theextensors accumulated the labelled material (Fromm and Eschrich 1988a).

Could cytoskeletal elements – actin filaments, microtubuli – activelyperform fast shrinking, as suggested already by Toriyama and Jaffe (1972)?Although both types of proteins were localized to the Mimosa primary pulvinus(using antibodies against muscular actin and a protozoan tubulin; FleuratLessard et al. 1993), a combination of pharmacological and immunocytochem-ical approaches implicated only actin in the seismonastic responses, addition-ally indicating the involvement of its phosphorylation by a tyrosine kinase(distinct from a serine/threonine kinase; Kanzawa et al. 2006). Interestingly, theactin-depolymerizing agent cytochalasin D promoted stomatal opening bylight and potentiated (independently of the activity of the H+-ATPase) theactivation (by hyperpolarization) of K+-influx channels, and the filamentous-actin-stabilizing agent phalloidin inhibited stomatal opening and the activationof K+-influx channels (Hwang et al. 1997), suggesting that actin may perhaps beinvolved not only in the “dramatic” movements of the pulvinus but also in theregulation of its “mundane”, rhythmic (nastic) movements.

1.2.3 Plasma Membrane Transporters

What transporters are involved in the ion fluxes across the pulvinar cell mem-brane? Although it is obvious that the fluxes of K+, Cl− and water occur betweenthe vacuole and the apoplast, i.e. across two membranes, there is practically noinformation about the tonoplast transporters of the pulvinar motor cells. So far,the function of only a few plasma membrane transporters in the pulvini has beenobserved in situ and partially characterized. Some of the details are given below.

1.2.3.1 H+-Pump Activity

The activity of the proton pump in the plasma membrane in the Samaneapulvini was assayed indirectly via changes in the light-stimulated acidifica-tion of the medium bathing extensor and flexor tissues (Iglesias and Satter1983; Lee and Satter 1989). Blue light (BL) acidified the extensorapoplast, consistent with pump activation, and alkalinized the flexor

10 Nava Moran

apoplast, consistent with cessation of pump activity (Lee and Satter 1989).In accord with this, in patch-clamp experiments with intact Samanea flexorprotoplasts, BL depolarized the flexor cells, probably by halting the action ofthe H+ pump (Suh et al. 2000; but see the inexplicable opposite response inKim et al. 1992). Red light or dark, following BL, activated the H+ pumpin flexors (acidifying the flexor apoplast and hyperpolarizing the flexor proto-plast; Lee and Satter 1989, Suh et al. 2000), and inactivated the pump inextensors (alkalinizing the extensor apoplast; Lee and Satter 1989).

The motor cells of the Phaseolus laminar pulvinus (both extensors andflexors) reacted to BL in a manner similar to that of the Samanea flexors:shrinking (Koller et al. 1996), depolarizing (Nishizaki 1990, 1994) and alka-linizing their external milieu (as a suspension of protoplasts; Okazaki 2002).Vanadate, which blocks P-type proton ATPases, inhibited the BL-induceddepolarization (Nishizaki 1994). Additionally, the inhibitory effect of BL wasdemonstrated directly on the vanadate-sensitive H+-ATPase activity ofmembranes from disrupted Phaseolus pulvinar protoplasts (Okazaki 2002).

Extensors protoplasts isolated from the Phaseolus coccineus pulvinusreacted to white light (WL) and dark (D) similarly to extensors of Samanea:they swelled in WL and shrunk in D (Mayer et al. 1997). This, too, may betaken as indirect evidence of the activation/deactivation of the proton pumpby WL and D respectively.

1.2.3.2 H+/Cl− Symporter

The presence of an H+/anion symporter has been suggested based on experi-ments in which the net H+ efflux from excised Samanea flexor tissue pieces,bathed in a weakly buffered medium, was greater with the impermeant imin-odiacetate anions than with the permeant Cl− in the external solution (Satteret al. 1987).

1.2.3.3 K+-Release Channels

These channels are presumed to mediate K+ efflux from pulvinar motorcells during their shrinking. Patch-clamp studies revealed depolarization-dependent, K+-release (KD) channels in the plasma membrane of pulvinarcell protoplasts (Moran et al. 1988; Stoeckel and Takeda 1993; Jaensch andFindlay 1998).

Ion Selectivity The selectivity for K+ of the Samanea KD channel was some-what higher than for Rb+, and much higher than for Na+ and Li+, and thechannel was blocked by Cs+, Ba2+, Cd2+ and Gd3+ (Moran et al. 1990), and alsoby TEA (Moran et al. 1988). KD channels in extensors were slightly less K+

selective than in flexors (Moshelion and Moran 2000). Extensors and flexors


differed also in the details of the cytosolic Ca2+ sensitivity of the KD channelsgating, but the overall effect of cytosolic Ca2+ on these channels was ratherminor (Moshelion and Moran 2000). By contrast, the Mimosa KD channelcurrents, although generally similar in their voltage dependence and simi-larly blockable by external Ba2+ and TEA (Stoeckel and Takeda 1993), wereseverely attenuated (they “ran down”) by treatments presumed to increasecytosolic Ca2+ (Stoeckel and Takeda 1995). Surprisingly, they were notblocked by external La3+ and Gd3+ at concentrations comparable to the block-ing Gd3+ concentration in Samanea. In fact, both lanthanide ions preventedthe “rundown” of the Mimosa KD channels.

Regulation by Light Using patch-clamp, Suh et al. (2000) demonstrated anincrease in the activity of KD channels in cell-attached membrane patches ofintact Samanea flexor protoplasts within a few minutes illumination withblue light, and a decrease in their activity within a few minutes of darkness,preceded by a brief red-light pulse (Fig. 1.3; Suh et al. 2000). No circadiancontrol, however, was evident in the responsiveness of the flexor KD channelsto blue light. The authors resolved the blue-light effect in terms of twoprocesses: (1) membrane depolarization-dependent KD channel activation(a consequence of a blue light-induced arrest of the proton pump), and (2) a voltage-independent increase of KD channel availability.

Molecular Identity Among the four putative K channel genes cloned fromthe Samanea saman pulvinar cDNA library, which possess the universal K channel-specific pore signature, TXXTXGYG, the Samanea-predicted pro-tein sequence of SPORK1 is similar to SKOR and GORK, the only Arabidopsisoutward-rectifying Shaker-like K channels. SPORK1 was expressed in allparts of the pulvinus and in the leaf blades (mainly mesophyll; Fig. 1.1), asdemonstrated in Northern blots of total mRNA. SPORK1 expression was reg-ulated diurnally and also in a circadian manner in extensor and flexor but notin the vascular bundle (rachis) nor in the leaflet blades (Moshelion et al.2002a). Although the functional expression of SPORK1 has yet to be achieved,these findings strongly indicate that SPORK1 is the molecular entity underly-ing the pulvinar KD channels.

1.2.3.4 K+-Influx Channels

Using patch-clamp in the whole-cell configuration, Yu et al. described hyper-polarization gated K+-influx (KH) channels in the plasma membrane ofSamanea extensor and flexor protoplasts (Yu et al. 2001). Paradoxically, thesechannels were blocked by external protons, contrary to what would beexpected of channels presumed to mediate the K+ fluxes during cell swellingwhich is concurrent with external acidification. This was particularly surpris-ing in view of the external-acidification-promoted K+-influx channels in

12 Nava Moran

guard cells (Blatt 1992; Ilan et al. 1996). The authors were able to resolve thisparadox by quantitative comparisons of the actual vs. the required K+ influx,in particular when they “recruited” into their calculations also the relativelylarge voltage-independent and acidification-insensitive leak-like currentsrecorded along with currents activated by hyperpolarization (Yu et al. 2001).No diurnal variation in the activity of the K+-influx channel was noted in thepatch-clamp experiments.

K+-selective channels were reportedly observed during membrane hyper-polarization also in extensor protoplasts from pulvini of Phaseolus (Jaenschand Findlay 1998). However, hyperpolarizing pulses failed to activate suchchannels in protoplasts from the primary pulvini of Mimosa (Stoeckel andTakeda 1993).

Regulation by Light Kim et al. (1992) monitored membrane potential inisolated Samanea extensor and flexor protoplasts using the fluorescent dyeDiS-C3(5) and pulses of elevated external K+ concentration to specifically


A

B

30

20

10

0

−10

−20

10

0

−10

−20

∆Vre

v(m

V)

∆G@

40(p

S)

BL (12)

BL (12)

DK (6)

DK (15)

*

*****

*

******

***

Fig. 1.3 Blue light enhances the activity of the Samanea KD (K+-release) channels in flexorprotoplasts. A Light-induced shift of the membrane potential, manifested as shifts of the reversalpotential, Vrev of KD-channel currents in single cell-attached membrane patches during alternationbetween blue light (BL) and dark (DK). A negative shift of Vrev indicates membrane depolariza-tion (mean±SE). The asterisks indicate the significance level of difference from zero: * P<0.05,** P<0.01, *** P<0.005; n number of membrane patches. B BL-induced, membrane-potential-independent changes of KD-channel activity, manifested as changes in G@40, the mean patchconductance at 40 mV depolarization relative to the Vrev of the patch (mean±SE). The asterisksand n, as in a (reproduced with permission, Suh et al. 2000)

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