Rhythms in Plants: Phenomenology, Mechanisms, and Adaptive Significance

365 Pages·2007·8.768 MB·English

by  Nava Moran (auth.), Prof. Dr. Stefano Mancuso, Dr. Sergey Shabala (eds.)

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
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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, 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