Rhythms in Plants: Phenomenology, Mechanisms, and Adaptive Significance S. Mancuso S. Shabala (Eds.) Rhythms in Plants Phenomenology, Mechanisms, and Adaptive Significance With 84 Figures, 3 in Color, and 5 Tables Prof. Dr. Stefano Mancuso Dr. Sergey Shabala University of Florence University of Tasmania Department of Horticulture School of Agricultural Science LINV International Laboratory on Plant Private Bag 54 Neurobiology Hobart, Tas, 7001, Australia Polo Scientifico, Viale delle idee 30 e-mail: [email protected] 50019 Sesto Fiorentino, Italy e-mail: [email protected] Library of Congress Control Number: 2006939346 ISBN-10: 3-540-68069-1 Springer Berlin Heidelberg New York ISBN-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 material is 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. Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permissions for use must always be obtained from Springer-Verlag. Violations are liable for prosecution under the German Copyright Law. Springer is a part of Springer Science+Business Media springer.com © Springer-Verlag Berlin Heidelberg 2007 The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Editor: Dr. Christina Eckey, Heidelberg, Germany Desk editor: Dr. Andrea Schlitzberger, Heidelberg, Germany Cover design: WMXDesign GmbH, Heidelberg, Germany Production and typesetting: SPi Printed on acid-free paper SPIN 11608950 149/3100 5 4 3 2 1 0 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, clocklike rhythms pervade the activities of every physiological process in plants, often in tune with the day/night cycle of the earth. Research into the rhythmic leaf movements in nyctinastic plants in the early 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 of Tamarindus indicaopened 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 in the 16th thought the daily periodical movements of the pinnate leaves of some Leguminosaeworth recording (Albertus Magnus 1260; for Cordus 1544, see Sprague and Sprague 1939). John Ray, in his ‘Historia Plantarum’ towards the end of the 17th century (Ray 1686–1704), commences his general consid- erations on the nature of plants with a succinct account of phytodynamical phenomena, but does not clearly distinguish between movements stemming from irritability and those showing daily, periodical rhythms; the latter, he writes, occur not only in the leaves of Leguminosaebut also in almost all sim- ilar pinnate leaves. In addition to these periodical movements of leaves, he reports the periodical opening and closing of the flowers of Calendula, Convolvulus, Cichoriumand others. In 1729, the French physicist Jean Jacques d’Ortous de Mairan discovered that mimosa plants kept in darkness continued to raise and lower their leaves with a ~24 h rhythm. He concluded that plants must contain some sort of internal control mechanism regulating when to open or close the leaves. Carolus Linnaeus studied the periodical movements of flowers in 1751 and those of leaves in 1755, but offered no mechanical explanation (Linnaeus 1770). He contented himself with describing the external conditions of these phenomena in many species, classifying them and giving a new name – sleep viii Preface of plant– to those periodical movements observed at night, considering that the plants had then assumed a position of sleep. Indeed, he did not use the word 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 mentioned that he stated correctly that the movements connected with the sleep of plants were not caused by changes in temperature but rather by change in light, since these took place at uniform temperature in a conservatory. Knowing that 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 species of organisms demonstrate unique rhythms. Building on these classical findings, the last decades have experienced a period of unprecedented progress in the study of rhythmical phenomena in plants. Innovations in molecular biology, micro- and nanotechnology and applied mathematics (e.g. hidden patterns, chaos theory) are providing new tools 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 has changed, and this is well reflected in the various chapters of this book which covers aspects of plant physiology neither recognisable nor quantifiable only a few years ago. The capacity to experience oscillations is a characteristic inherent to living organisms. Many rhythms, at different levels extending from the cell to the entire plant, persist even in complete isolation from major known environ- mental cycles. Actually, 24-h rhythms (circadian rhythms) are not the only biological rhythms detectable in plants – there are also those extending over longer periods (infradian rhythms), either a month, year or a number of years, as well as shorter rhythms (ultradian rhythms) lasting several hours, minutes, seconds, etc. Accordingly, natural rhythms can be considered to lie outside the periods of geophysical cycles. This means that living matter has its 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 traditional plant biology. Unlike circadian rhythms, ultradian rhythms have received little attention from plant biologists. Among the causes of this underestimation is the fact that ultradian rhythms are readily overlooked in experiments in which observations are made only intermittently, or are treated as unwanted noise. Classically, oscillations of data during discontinuous measurements are either ignored or attributed to sampling inaccuracy or error in the technique used, rather than to biological rhythmicity. In addition, the common practice of pooling and averaging data collected from different specimens will serve – given that no two specimens are likely to be completely in phase – to obscure rhythmicity. On the whole, modern plant biology is poorly equipped for the study of ultradian rhythms. These are best studied in single specimens, using high-resolution, non-invasive, uninterrupted recording techniques. Such a Preface ix holistic approach to physiology runs counter-current to the prevalent reduc- tionism which emphasizes the use of averaged data collected by means of invasive 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 are aware of the fact that plants live and act in time. Therefore, the concept of cyclic 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 clone but also the capacity to endure (chronon). The concept of chronon refers to the expression of genes as a function of chronological time. The concept ofchronome relates to the expression of genes as a function of biological time, which is cyclical, irreversible and recursive. Accordingly, chronological time could be seen as the summation of iterated periods, which constitute thetime base of biological rhythms. The cycles of life are ultimately biochemical in mechanism but many of the principles 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 study of data on biological fluctuations can be the means of discovering the exis- tence of underlying rhythms. It might be of interest, for example, to account for 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 of cycles in a system, it is essential to represent the system to be studied by means of a model: one that is explicative or one that is representative and predictive. This volume concentrates on modelling approaches from the level of cells to the entire plant, focusing on phenomenological models and theoretical concepts. 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 the nature of their work, deal with the study and modelling of data originating from rhythmic systems in plants. Hopefully, the wide range of subjects will excite the interest of readers from many branches of science: physicists or chemists who wish to learn about rhythms in plant biology, and biologists who wish to learn how these rhythmic models are generated. x Preface Finally, the Editors gratefully acknowledge the assistance of a number of people and institutions without whose help this project could not have been carried out. First of all, we are most deeply indebted to the contributors of the chapters presented here, whose enthusiasm and dedication have made this book a reality. We also acknowledge the Fondazione Ente Cassa di Risparmio di Firenzefor financial support given to the LINV – Laboratorio Internazio- nale di Neurobiologia Vegetale, University of Firenze, as well as the Australian Research Council for supporting research on membrane transport oscillators at the University of Tasmania. Last but not least, we express our sincere appre- ciation to Dr. Andrea Schlitzberger and Dr. Christina Eckey, at Springer, for their guidance and assistance during the production of the book. December 2006 Stefano Mancuso Sergey Shabala References Albertus Magnus (1260) De vegetabilibus. Wissenschaftliche Verlagsgesellschaft, Stuttgart, 1992 edn Bretzl H (1903) Botanische Forschungen des Alexanderzuges. Teubner, Leipzig Cordus V (1544) Historia Plantarum. (cf. text) d’Ortous de Mairan JJ (1729) Observation botanique. Histoire de l’Académie Royale des Sciences, Paris Linnaeus C (1770) Philosophia Botanica. Joannis Thomae nob. de Trattnern, Vienna Ray J (1686–1704) Historia plantarum, species hactenus editas aliasque insuper multas noviter inventas & descriptas complectens. Mariae Clark, London Sprague TA, Sprague MS (1939) The herbal of Valerius Cordus. Linnean Society, London Contents Part 1 Physiological Implications of Oscillatory Processes in Plants . . . . . . . . . . . . . . . . . . .1 1 Rhythmic Leaf Movements: Physiological and Molecular Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .3 NAVAMORAN Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .3 1.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .3 1.1.1 Historical Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .3 1.1.2 The Types of Leaf Movements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .4 1.2 The Mechanism of Leaf Movement: the Osmotic Motor . . . . . . . . . . . . . . .7 1.2.1 Volume Changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .7 1.2.2 The Ionic Basis for the Osmotic Motor . . . . . . . . . . . . . . . . . . . . . . .8 1.2.3 Plasma Membrane Transporters . . . . . . . . . . . . . . . . . . . . . . . . . . . .10 1.2.4 Tonoplast Transporters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .16 1.3 Mechanisms of Regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .17 1.3.1 Regulation by Protein Modification – Phosphorylation . . . . . . . . .17 1.3.2 The Perception of Light . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .21 1.3.3 Intermediate Steps . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .23 1.3.4 Regulation by Other Effectors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .28 1.4 Unanswered Questions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .30 1.4.1 Acute, Fast Signalling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .31 1.4.2 The Clock Input and Output . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .31 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .32 2 The Pollen Tube Oscillator: Integrating Biophysics and Biochemistry into Cellular Growth and Morphogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .39 NUNOMORENO, RENATOCOLAÇOANDJOSÉA. FEIJÓ Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .39 2.1 Finding Stability in Instability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .39 2.2 Why Pollen Tubes? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .42 2.3 Growth Oscillations: Trembling with Anticipation? . . . . . . . . . . . . . . . . . .42 2.4 Under Pressure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .45 2.5 Another Brick in the Cell Wall . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .46 2.6 Cytosolic Approaches to Oscillations: the Ions Within . . . . . . . . . . . . . . . .47 2.7 On the Outside: Ions and Fluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .51 2.8 Actin Cytoskeleton: Pushing it to the Limit . . . . . . . . . . . . . . . . . . . . . . . . .54 xii Contents 2.9 Membrane Trafficking and Signalling on the Road . . . . . . . . . . . . . . . . . .55 2.10 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .57 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .58 3 Ultradian Growth Oscillations in Organs: Physiological Signal or Noise? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .63 TOBIASI. BASKIN Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .63 3.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .63 3.1.1 Oscillations as Window into Growth . . . . . . . . . . . . . . . . . . . . . . .63 3.1.2 Growth Versus Movement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .65 3.2 Circumnutation: Growing Around in Circles? . . . . . . . . . . . . . . . . . . . . . .65 3.3 In Search of Ultradian Growth Oscillations . . . . . . . . . . . . . . . . . . . . . . . .68 3.4 The Power of Bending in Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .70 3.5 Conclusion and Perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .73 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .73 4 Nutation in Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .77 SERGIOMUGNAI, ELISAAZZARELLO, ELISAMASI, CAMILLAPANDOLFI ANDSTEFANOMANCUSO Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .77 4.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .77 4.2 Theories and Models for Circumnutation . . . . . . . . . . . . . . . . . . . . . . . . . .81 4.2.1 ‘Internal Oscillator’ Model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .83 4.2.2 ‘Gravitropic Overshoot’ Model . . . . . . . . . . . . . . . . . . . . . . . . . . . .84 4.2.3 The ‘Mediating’ Model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .85 4.3 Root Circumnutation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .86 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .88 Part 2 Stomata Oscillations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .91 5 Oscillations in Plant Transpiration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .93 ANDERSJOHNSSON Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .93 5.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .93 5.2 Models for Rhythmic Water Transpiration . . . . . . . . . . . . . . . . . . . . . . . .95 5.2.1 Overall Description – “Lumped” Model . . . . . . . . . . . . . . . . . . . . .95 5.2.2 Overall Description – “Composed” Models . . . . . . . . . . . . . . . . . .97 5.2.3 Self-Sustained Guard Cell Oscillations – (Ca2+) Oscillations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .98 cyt 5.2.4 Water Channels . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .98 5.2.5 Comments on Modelling Transpiration Rhythms . . . . . . . . . . . . .99 5.3 Basic Experimental Methods Used . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .99 5.4 Experimental Findings on Transpiration Oscillations . . . . . . . . . . . . . .100 5.4.1 Occurrence of Transpiration Rhythms: Period of Rhythms . . . .101 5.4.2 Some Environmental Parameters Influencing Oscillations . . . .101 5.4.3 Singularities of Transpiration Rhythms: Test of Models . . . . . . .104