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379 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 380 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 381 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.