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Cell signalling and gene regulation
Plant signal transduction pathways: greying of the black boxes
Editorial overview
Jerome Giraudat* and Julian I Schroeder‡
Addresses
*Institut des Sciences du Vegetal, CNRS UPR2355–Bat 23,
1 Avenue de la Terrasse, 91190 Gif-sur-Yvette, France
‡ Division of Biology, Cell and Developmental Biology Section, and
Center for Molecular Genetics, University of California San Diego,
La Jolla, California 92093-0116, USA
Current Opinion in Plant Biology 2001, 4:379–381
1369-5266/01/$ — see front matter
© 2001 Elsevier Science Ltd. All rights reserved.
Abbreviation
MAPK mitogen-activated protein kinase
Signal transduction networks are essential to plant growth
and development, allowing cells and tissues to perceive
and respond to continuous changes in their environment.
Multiple signalling pathways exist in plant cells, controlling important processes including hormone and light
perception, pathogen defence, stress survival, cell division
and circadian rhythms. Until 10 years ago, the plant signal
transduction pathways that transmit well-known stimuli
were viewed as black boxes. Through advances in
Arabidopsis genetics and numerous other important
approaches, individual elements and short signalling
segments and complexes have been discovered, resulting
in a greying of the black boxes. Furthermore, the molecular
mechanisms by which signalling pathways crosstalk with
each other or by which specificity is conferred within a
complex signalling network are currently areas of intensive
research in plant biology and eukaryotic biology in general.
It has long been recognised that most aspects of plant
growth and physiology are regulated by networks of
signalling mechanisms rather than by linear signal
transduction pathways, rendering plants particularly
attractive for dissecting crosstalk and specificity mechanisms.
In this issue of Current Opinion in Plant Biology, recent
advances in rapidly moving areas of plant signalling
research are reviewed and important newly arising open
questions are formulated.
The review by Leyser (pp 382–386) illustrates that the
analysis of the auxin signalling pathway has reached an
exciting period during which results from both genetic and
biochemical studies are merging into a coherent working
model for the ‘middle’ of the pathway. The molecular
analysis of auxin response mutants of Arabidopsis has
indicated that auxin signalling is mediated by regulated
protein degradation via a protein ubiquitin ligase complex
of the SCF (SKP1, cullin/CDC53, F-box protein) type.
Recent studies suggest that targets for this degradative
pathway include the auxin efflux carriers of the PIN family,
as well as nuclear auxin/IAA (indole acetic acid) proteins
that regulate gene transcription through interactions with
members of the auxin response factor (ARF) family.
As discussed above, in the case of auxin, the identification
of genes through targeted Arabidopsis mutant screens has
provided invaluable insights into the structure of several
plant signalling pathways. More and more frequently,
however, known hormone-response genes are also being
recovered in genetic screens that were not designed to find
them. For instance, several recent reports described genetic
crosstalk among abscisic acid (ABA), ethylene and sugar
responses. Gazzarrini and McCourt (pp 387–391) review
these intriguing findings and discuss the extent to which
these genetic interactions might reflect the in vivo situation.
Mitogen-activated protein kinase (MAPK) cascades are
evolutionarily conserved signalling modules with essential
regulatory functions in plants as in other eukaryotes. Tena
et al. (pp 392–400) provide a detailed analysis of the
MAPK cascade genes present in the recently completed
Arabidopsis genome. They also review exciting recent
developments in our understanding of the role of plant
MAPK cascades in hormonal responses, cell cycle regulation,
abiotic stress signalling (see also Zhu, pp 401–406) and
pathogen defence (see also Romeis, pp 407–414). In many
instances, an emerging feature of MAPK signalling is that
their physiological outcome appears to be dictated by the
interactions of multiple and antagonistic MAPK cascades.
Plants have to endure environmental challenges such as
drought, soil salinity, and cold temperatures. The article by
Zhu highlights recent progress in understanding the
signalling pathways that are either specific or common to
these stresses. In particular, characterisation of the sos (salt
overly sensitive) mutants of Arabidopsis has revealed a novel
calcium-regulated kinase pathway that is specifically
dedicated to signalling the ionic aspects of salt stress. This
ion homeostasis pathway appears to be unique to plants.
Molecular studies have identified additional (SOS-independent) protein kinases that are activated either specifically by
osmotic stress or by multiple abiotic and biotic stresses.
The plant’s surveillance system for pathogen attack is
based on early recognition of the invading organism and
the activation of defence mechanisms that result in the
arrest of further invasion and resistance of the plant. As
reviewed by Romeis, numerous recent studies indicate
that members of different kinase subfamilies are involved
at each step of this process: recognition of pathogenderived molecules, induction of defence mechanisms, and
desensitisation of defence responses. Over the past few
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Cell signalling and gene regulation
years, biochemical and genetic studies have been instrumental in characterising these protein kinases. Recent
advances in the large-scale analysis of phosphoproteins by
mass spectrometry (or phosphoproteomics) should now
help to build the links between the single components of
plant defence signalling pathways.
The calcium ion acts as an intracellular second messenger
in a variety of signalling pathways. An immediate question,
therefore, is how do calcium-based signalling cascades
achieve their specificity? As reviewed by Evans et al.
(pp 415–420), recent results demonstrate that, in plants,
stimulus-induced oscillations in cytosolic free calcium
encode information that is used to specify the outcome of
the final response. In particular, substantial evidence
indicates that calcium oscillations are involved in the control
of guard cell turgor (see also Assmann and Wang, pp 421–428),
Nod factor signalling, and pollen-tube growth. Some new
challenges in this exciting field will be to understand how
calcium oscillations are generated and decoded.
Stomata open and close because of turgor changes that are
driven by ion fluxes across the guard-cell plasma membrane
and tonoplast. Stomatal guard cells respond rapidly to
multiple environmental and internal stimuli, and they are a
well-developed model system for the analysis of early
signalling mechanisms. Assmann and Wang review the latest
advances in deciphering the signalling events that mediate
ABA-induced stomatal closing (see also Evans et al.) or bluelight-induced stomatal opening. Environmental factors,
including atmospheric CO2 levels, also control stomatal
density. These regulations occur over developmental and
even evolutionary time scales; a first set of genes involved in
this response has been identified recently.
Yanovsky and Kay (pp 429–435) review the recent progress
made in the genetic and molecular dissection of the plant
circadian system. Arabidopsis does not contain true homologues of the clock genes found in Drosophila, Neurospora,
or mice. However, as in these organisms, the plant clock
appears to be based on a transcriptional feedback loop.
Indeed, recent studies show that reciprocal regulation
among TIMING OF CAB EXPRESSION 1 (TOC1),
CIRCADIAN-CLOCK-ASSOCIATED 1 (CCA1), and
LATE ELONGATED HYPOCOTYL (LHY) forms a
negative feedback loop that may be central to clock
function in Arabidopsis. Significant progress has also been
made in identifying components of the signalling pathways
through which light resets the clock or by which the clock
modulates its own resetting. Finally, microarray analyses
have expanded the number of physiological processes
known to be under clock control, and will help to identify
additional components of the circadian system.
Inhibition of hypocotyl elongation by light has been of
great value to the study of photomorphogenesis. In particular,
this response has been used to isolate numerous mutants
lacking specific photoreceptors or downstream signalling
components. An important challenge now is to arrange all
of these elements into testable signalling networks. Parks
et al. (pp 436–440) describe how significant advances
towards this goal are being made by time-resolved kinetic
analysis of hypocotyl growth in wild-type plants and
photomorphogenic mutants of Arabidopsis. Such studies
indicate that the instantaneous rate of hypocotyl growth in
light results from the integration of opposing forces, both
inhibition and promotion, and that each stage of the
response is regulated by different light receptors.
In the shoot apical meristem, the central zone harbours the
stem cells, which continually produce new cells, whereas
initiation of lateral organs occurs in the surrounding
peripheral zone. Haecker and Laux (pp 441–446) review
recent studies that provide exciting molecular insights into
the cell–cell signalling mechanisms that are involved in
stem cell homeostasis and organ initiation. Stem cell population is maintained by a feedback loop between the stem
cells and the underlying organising centre, this feedback
mechanism is based on a regulatory loop between the
CLAVATA and WUSCHEL genes. Polar auxin transport is
required for the organisation of the peripheral zone into
primordium and non-primordium cells, and auxin is also
necessary for organ outgrowth.
One of the largest families of transcription factors in plants
is the so-called R2R3-MYB protein family. Whereas the
vertebrate c-MYB contains three repeats (R1, R2 and R3)
in its MYB DNA-binding domain, MYB proteins of the
R2R3-type contain only two repeats and are present exclusively in plants. After exhaustive mining of the Arabidopsis
genome sequence, Stracke et al. (pp 447–456) identified
125 R2R3-MYB genes, for which they present a detailed
classification and nomenclature. Available genetic studies
indicate that R2R3-MYB genes control several aspects of
plant secondary metabolism, as well as the identity and
fate of plant cells.
Meyer (pp 457–462) reviews the latest advances in our
understanding of chromatin remodelling in plants. Recent
studies indicate that, in addition to its important role in
transcription, chromatin remodelling regulates mechanisms
in plants that include replication, repair and recombination.
A number of well-characterised chromatin remodelling
factors has been identified. These factors have been
allocated defined molecular functions that are, in most
cases, associated with the modification of histone proteins.
Most chromatin remodelling processes, however, involve
the combined effects of multiple factors in higher order
complexes. Thus, an important challenge is to understand
the interactions among the components of these chromatin
remodelling complexes.
Substantial progress in understanding plant signal transduction pathways is being made through interdisciplinary
studies. These studies are showing that many of the central
signalling mechanisms in plants deviate from animal cell
Editorial overview Giraudat and Schroeder
paradigms. Nevertheless, an understanding of all of the
elements linked from ‘beginning to end’ within a single plant
signalling pathway has not been achieved to date, although
relatively densely populated backbones are being assembled
for ethylene, guard cell and phytochrome signalling. Recent
advances suggest that signal transduction is far too complex
to be carried out by a linear backbone. These findings point
to signaling branches, to complex crosstalk among signalling
pathways, and to positive and negative regulators at various
stages in the pathway. Importantly, individual ‘islands’ (i.e.
genes and proteins) have been identified that affect each of
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the classically known plant signalling pathways. Combined
genetic, genomic, biochemical, proteomic and cell-biological
research is making use of these islands to identify neighbouring proteins and complete signalling branches.
Future advances will ultimately decipher the mechanisms
that produce crosstalk among different pathways. The
pace of discovery is accelerating and the greying black
boxes will dramatically become more transparent, giving
rise to the next generations of important and exciting
questions in plant biology.