Signal Transduction in Plants

183 Pages·1996·12.794 MB·English

by  J. M. Ward, J. I. Schroeder (auth.), Prof. P. Aducci (eds.)

MCBU
Molecular and Cell Biology Updates
Series Editors:
Prof. Dr. Angelo Azzi
Institut fur Biochemie
und Molekularbiologie
BOhlstr.28
CH-3012 Bern
Switzerland
Prof. Dr. Lester Packer
Dept. of Molecular
and Cell Biology
251 Life Science Addition
Membrane Bioenergetics Group
Berkeley, CA 94720
USA
Signal Transduction in Plants
~dited by P. Aducci
Birkhauser Verlag
Basel· Boston· Berlin
Volume editors' address:
Prof. P. Aducci
University of Rome "Tor Vergata"
Department of Biology
Via della Ricerca Scientifica
1-00133 Rome
Italy
A CI P catalogue record for this book is available
from the Library of Congress, Washington D.C., USA
Deutsche Bibliothek Cataloging-in-Publication Data
Signal transduction in plants / ed. by P. Aducci.
-Basel; Boston; Berlin:
Birkhiiuser, 1997
(Molecular and cell biology updates)
ISBN-13: 978-3-0348-9938-3
NE: Aducci, Patrizia IHrsg.1
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© 1997 Birkhiiuser Verlag, PO Box 133, CH-4010 Basel, Switzerland
SofIcover reprint of the hardcover 1s t edition 1997
Printed on acid-free paper produced from chlorine-free pulp.
ISBN-13: 978-3-0348-9938-3 e-ISBN-13: 978-3-0348-9183-7
001: 10,1007/978-3-0348-9183-7
987654321
Table of Contents
Preface ................................................... VII
Chemical signals: Hormones, Phytotoxins
Roles of ion channels in initiation of signal transduction in higher plants
I.M. Ward and 1.1. Schroeder . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
ABA signaling in plant development and growth
T.L. Thomas, H.-I. Chung and A. N. Nunberg .......................... 23
Auxin perception and signal transduction
M.A. Venis and R.M. Napier ..................................... 45
Transduction of ethylene responses
M.A. Hall and A.R. Smith . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65
Phytotoxins as molecular signals
P. Aducci, A. Ballio and M. Marra . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83
Physical signals: Blue and red light
Blue light-activated signal transduction in higher plants
W.R. Briggs and E. Liscum ...................................... 107
The transduction of light signals by phytochrome
C. Bowler ................................................. 137
Biotic signals: Host-pathogen interactions
Perception of fungal elicitors and signal transduction
F. Cervone, R. Castoria, F. Leckie and G. De Lorenzo 153
Subject index ...... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 179
Preface
Increasing interest has been emerging in the last decade in the field of signal recognition and
transduction. This is particularly true for animal systems where an impressive amount of literature
is appearing and where many important pathways have been clarified at a molecular level. In the
elucidation of the functions of single components of a given pathway, gene cloning has played a
major role and opened the field to the genetic engineering of these complex systems. At variance
with this situation, plant systems are less well elucidated, even if in recent years exciting research
developments have been initiated especially with the view toward the most promising role of
plants in biotechnology.
Recent studies have elucidated some of the events involved in the perception of the plant
hormone signals and some steps concerning its transduction. Only for three of the five hormones
in plants, namely auxin, ethylene and cytokinins, have specific receptors been isolated. The use of
classical molecular approaches, together with the more recently isolated mutants, have produced
crucial information on receptors and shed light on possible transduction pathways. As in the case
of red light, more than one pathway can be triggered by one specific signal.
Many systems involved in animal signaling are now shown to be present also in plants, and in
view of the fast progress in this area, it will be possible in the near future to fully describe the
content of the "black boxes" in the reaction chain specifically triggered by a signal.
These have been some of the reasons that prompted us to prepare the present book. It reflects
the current "state of the art" in the field of signal transduction in plants. The contributing authors
are experts in different areas of plant physiology and plant molecular biology and have used
different approaches to study the recognition and transduction of different signals specific for
plant organisms. These can be chemical or physical in nature and some examples will be presen
ted on the molecular mechanisms by which hormones, toxins or light can regulate plant growth,
differentiation and morphogenesis. Moreover, plant-pathogen interactions are now beginning to
be clarified and some progress on their molecular basis is being described.
This book, for its multidisciplinary approach, for the different technologies used and for the
emerging interesting peculiarities of the plant world should be of interest both to experts in the
field and to a wider audience.
I would like to thank my coworkers Vincenzo Fogliano, Maria Rosaria Fullone, Mauro Marra
and Silvia Bacocco for their help in organizing the material for the book and the staff of
Birkhauser for their collaboration.
Patrizia Aducci
Signal Transduction in Plants
P. Aducci (ed.)
© 1997 Birkhiiuser Verlag BaseVSwitzerland
Roles of ion channels in initiation of signal transduction in higher plants
I.M. Ward and 1.1. Schroeder
Department of Biology and Center for Molecular Genetics, University of California San Diego, La Joila,
CA 92093-0116, USA
Introduction
Recently, progress has been made in identifying initial signal reception mechanisms and early
events in signaling cascades in higher plants. Ion channels, along with intracellular signaling pro
teins and second messengers, are critical components mediating early events in higher plant signal
transduction. Ion channel-mediated signal transduction in higher plants has notable differences
from signaling mechanisms in animal systems. Of the many types of ion channels found in
higher plants, there are indications that anion channels, along with Ca2+ channels, play critical and
rate-limiting roles in the mediation of early events of signal transduction. We have now begun to
obtain the first insights into the modes of regulation, the membrane localization, and in the case of
K+ channels, the molecular structure of higher plant ion channels.
In this chapter we focus mainly on novel findings concerning the function and regulation of
anion and Ca2+ channels and outline testable models of their involvement in signal transduction.
Our objective is to summarize these findings and to point out the many open questions involving
early events in plant signal transduction. To illustrate the functions of higher plant ion channels in
the initiation of signaling cascades, in the first section we discuss the relatively better understood
molecular mechanisms of abscisic acid (ABA)-induced stomatal closing with a special focus on
new and emerging concepts. In the second section, we address Ca2+-dependent and Ca2+-inde
pendent signaling processes in plants and analyze certain putative parallels between initial guard
cell signaling and both the initiation of defense responses and phytochrome-induced signaling.
Abscisic acid-initiated signal transduction in guard cells
Since the initial patch-clamp studies of guard cells showed a role for K+ channels in mediating
stomatal movements (Schroeder et aI., 1984), guard cells have become a model system for under-
2 J. M. Ward and J. 1. Schroeder
standing early signal transduction events in plants. A variety of signals, including hormones, light,
humidity, and water status, influence stomatal aperture, allowing plants to balance CO2 uptake and
water loss under diverse environmental conditions. The hormone ABA is synthesized in response
to drought and induces a cascade of signaling events in guard cells reSUlting in stomatal closing
(Mansfield et a!., 1990). Recent research has led to the identification of several early events in
ABA signaling, providing a potent system to analyze the intermediate steps in this transduction
cascade.
The events that directly follow ABA receptor activation have proven difficult to identify, primar
ily because of a general lack of information concerning the cellular location and structure of the
ABA receptor. Experiments involving microinjection of ABA have indicated a requirement for
extracellular ABA receptors (Anderson et aI., 1994; Gilroy and Jones, 1994). However, the pH
dependence of ABA inhibition of stomatal opening (Anderson et a!., 1994, and references
therein), as well as the effects of the release of caged ABA within guard cells (Allan et a!., 1994)
and the effects of microinjected ABA on stomatal closing in the presence of 1 ~M extracellular
ABA (Schwartz et a!., 1994) argues for a role of cytosolic ABA in guard cell signaling. In addi
tion, ABA-induced 86Rb+ efflux from guard cells appears to depend on the concentrations of
A
B
c
channel
D
K + channel
Figure 1. Simplified model for the coordinated regulation of plasma membrane ion channels required for ABA-in
duced stomatal closing. (A) Activation of abscisic acid receptors leads to Ca2+-dependent and Ca2+-independent
signaling events that regulate ion channel activity. (B) The rapid activation of nonselective ion channels causes
membrane depolarization and allows Ca2+ influx from the extracellular space. The increase in cytosolic Ca2+ and
the production of other signaling intermediates trigger further Ca2+ release from intracellular stores. (C) Membrane
depolarization, elevated cytosolic Ca2+, and protein phosphorylation events activate anion channels, which mediate
anion release and long-term membrane depolarization. (D) K+ efflux through voltage dependent outward K+ chan
nels is driven by membrane depolarization and enhanced by ABA-induced cytosolic alkalinization.
Roles of ion channels in initiation of signal transduction in higher plants 3
both intracellular and extracellular ABA (MacRobbie, 1995). A model that may account for these
circumstantial observations has been proposed in which both extracellular and intracellular sites
for ABA reception exist (Anderson et al., 1994; MacRobbie, 1995). A better understanding of the
mechanism of ABA perception and the initial targets of activated receptors requires further cellu
lar and molecular identification of the ABA receptors.
One of the earliest known responses of guard cells to ABA is an increase in cytosolic Ca2+
(McAinsh et aI., 1990; Schroeder and Hagiwara, 1990). Increases in cytosolic Ca2+ have been
demonstrated to be sufficient to induce stomatal closure (Gilroy et aI., 1990). The activation of
non-selective, Ca2+ permeable ion channels in the plasma membrane that allow Ca2+ influx
occurs within 2 seconds of ABA exposure (Schroeder and Hagiwara, 1990), indicating a close
coupling between ABA receptors and these ion channels. The oscillatory activity of Ca2+ -perme
able ion channels indicates a close but not direct coupling as depicted in Figure 1 (Schroeder and
Hagiwara, 1990). Although it has been suggested that Ca2+ influx from the extracellular space is
required for stomatal closing (DeSilva et aI., 1985; Schwartz et al., 1988), recent work has indi
cated that Ca2+ is released in parallel from intracellular stores: injection of inositol 1,4,5-trisphos
phate (InsP3), which is thought to trigger Ca2+ release from internal stores in guard cells, produ
ces stomatal closing (Gilroy et aI., 1990). In fact, evidence indicates a possible increase in InsP3
levels in guard cells in response to ABA (MacRobbie, 1992; Cote and Crain, 1994). Cytosolic
Ca2+ (Schroeder and Hagiwara, 1989) and InsP3 (Blatt et al., 1990) also reversibly inhibit inward
K+ channels. Furthermore, the inhibition of inward-rectifying K+ channels in guard cells
following ABA application is not dependent on extracellular Ca2+ but is abolished by intracellular
application of Ca2+ buffers. These data suggest that ABA-induced Ca2+ release from intracellular
stores can mediate K+ channel inhibition, while not excluding the occurrence of Ca2+ influx at the
plasma membrane (Lemtiri-Chlieh and MacRobbie, 1994). In support of these findings sugges
ting multiple cellular sources of Ca2+ influx into the cytosol, imaging studies have shown that
ABA induces transient cytosolic Ca2+ increases in the vicinity of both the plasma membrane and
the vacuole in guard cells (McAinsh et al., 1992). More recently, oscillations in cytoplasmic free
Ca2+ in guard cells, which result in stomatal closure, have been directly demonstrated to depend
on both Ca2+ influx and intracellular Ca2+ release (McAinsh et al., 1995). These data, as well as
other findings on Ca2+- independent signaling (Allan et aI., 1994, discussed later in this chapter),
indicate that guard cells provide a good system to analyze parallel signaling mechanisms. It is
becoming evident that multiple Ca2+ channels exist in guard cells and the immediate questions of
signal specificity and coupling mechanisms require further analysis. For example, it has not yet
been directly demonstrated whether InsP3 induces Ca2+ influx from intracellular stores in guard
cells or from the extracellular space.
4 J. M. Ward and J. 1. Schroeder
Regulation of K+ channels and H+ pumps during guard cell signaling
Increases in cytosolic Ca2+ inhibit cellular components that are important in controlling stomatal
opening. Plasma membrane H+-ATPase activity that drives stomatal opening is inhibited almost
completely when cytosolic Ca2+ is elevated to 111M (Kinoshita et al., 1995). The inhibition of H+
pumping would inhibit stomatal opening, but alone is unlikely sufficient to induce stomatal clo
sure, as described below. Proton pump inhibition is not sufficient to generate the membrane
depolarization positive of the K+ eqUilibrium potential required for stomatal closing. Inward-recti
fying K+ channels in the guard cell plasma membrane are also inhibited by elevated cytosolic
Ca2+ (Schroeder and Hagiwara, 1989; Blatt et aI., 1990; Fairley-Grenot and Assmann, 1991;
Lemtiri-Chlieh and MacRobbie, 1994; Kelly et aI., 1995). Recent work demonstrated that strong
ly elevated cytosolic Ca2+ levels in the range of I to 1.3 11M are required to significantly inhibit
inward-rectifying K+ channels in guard cells (Kelly et aI., 1995). This regulation of K+ influx is
considered to be of secondary importance for the stomatal closing mechanisms discussed here
because K+ uptake channels provide a major pathway for K+ accumulation during stomatal
opening (Schroeder et a!., 1987; Schroeder, 1988; Schroeder and Hagiwara, 1989; Thiel et al.,
1992) and have not been proposed to contribute to stomatal closing. Recent findings on second
messenger regulation of these K+ uptake channels are reviewed elsewhere (Assmann, 1993).
Potassium channel currents in guard cells are much larger than required for physiological K+
fluxes during stomatal movements. Thus, inward K+ channels in guard cells were initially char
acterized as sufficient but not rate limiting for stomatal opening. It was stated that "residual K+
currents measured after reduction by 10 mM Ba2+ (90% block) were estimated still to be suffi
cient to allow stomatal movements in physiologically observed periods" (Schroeder et a!., 1987
p. 4112). Recent data have shown that the rate of stomatal opening is only decreased when inward
K+ channels are blocked by 90% (Kelly et a!., 1995). Therefore, stomatal opening is likely to be
controlled by the rate-limiting plasma membrane H+ pumps which are tightly regulated in guard
cells (Kinoshita et a!., 1995).
Stomatal closing is driven by the reduction in guard cell turgor, which requires the efflux of
large amounts of K+ and anions and a parallel conversion of malate to starch (Raschke, 1979;
MacRobbie, 1981; Outlaw, 1983). Outward-rectifying K+ channels were identified and character
ized as a pathway for K+ efflux during stomatal closing (Schroeder et al., 1984; Schroeder et a!.,
1987; Schroeder, 1988; Blatt, 1990; Blatt and Armstrong, 1993). Detailed studies have shown that
K+ efflux can be mediated by outward-rectifying K+ channels in the plasma membrane that are
activated by membrane depolarization (Fig. 1) (Schroeder et aI., 1987; Schroeder, 1988; Blatt and
Armstrong, 1993). ABA enhances outward K+ channel currents (Blatt, 1990) via an ABA-