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Plant neurobiology: an integrated view of plant signaling

Eric D. Brenner1, Rainer Stahlberg2, Stefano Mancuso3,4, Jorge Vivanco5, Frantisek Baluska4,6,7 and Elizabeth Van Volkenburgh2
1 2

Genomics, New York Botanical Garden, NY 10458, USA Department of Biology, University of Washington, Seattle, WA 98195, USA 3 Department of Horticulture, University of Florence, Viale delle Idee 30, 50019 Sesto Fiorentino (FI), Italy 4 International Plant Neurobiology Laboratory, Viale delle idee 30, 50019 Florence, Italy; Kirschallee 1, 53115 Bonn, Germany 5 Center for Rhizosphere Biology and Department of Horticulture, Colorado State University, 217 Shepardson, Fort Collins, CO 80523-1173, USA 6 Institite of Cellular and Molecular Botany, Rheinische Friedrich-Wilhelms-University of Bonn, Kirschallee 1, 53115 Bonn, Germany 7 Institute of Botany, Slovak Academy of Sciences, Dubravska cesta 14, SK-84223, Bratislava, Slovak Republic

Plant neurobiology is a newly focused eld of plant biology research that aims to understand how plants process the information they obtain from their environment to develop, prosper and reproduce optimally. The behavior plants exhibit is coordinated across the whole organism by some form of integrated signaling, communication and response system. This system includes long-distance electrical signals, vesicle-mediated transport of auxin in specialized vascular tissues, and production of chemicals known to be neuronal in animals. Here we review how plant neurobiology is being directed toward discovering the mechanisms of signaling in whole plants, as well as among plants and their neighbors. The concept of plant neurobiology To contend with environmental variability, plants often show considerable plasticity in their developmental and physiological behaviors. Some of their apparent choices include: when and where to forage for nutrients and where to allocate those nutrients and derived organic molecules within the organism; when and what organs to generate or senesce; when to reproduce and the number of progeny to create; how to mount a defense against attack and in what tissues or organs; and when and where to transmit chemical signals to surrounding organisms. All these responses must occur within the context of a changing environment, including periodic and meteorological variation regarding light, nutrients, water, wind, temperature and attack. They must be made within the multicellular connes of the complex biological unit of the plant body and, thus, require coordinated cell-to-cell signaling, which requires a sophisticated information storage and acquisition system. Plant neurobiology (Box 1) is a newly initiated eld of research [1] aimed at understanding how plants perceive their circumstances and respond to environmental input in an integrated fashion, taking into account the combined
Corresponding author: Brenner, E.D. (ebrenner@nybg.org); Baluska, F. (baluska@uni-bonn.de); Van Volkenburgh, E. (lizvanv@u.washington.edu) Available online 13 July 2006.
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molecular, chemical and electrical components of intercellular plant signaling. Plant neurobiology is distinct from the various disciplines within plant biology in that the goal of plant neurobiology is to illuminate the structure of the information network that exists within plants. Hence, much of the emphasis in plant neurobiology is directed towards discovering and understanding the action of unknown and known systemic signals. These signals are both fast and slow, and are derived from electrical, hydraulic and chemical sources. They include recent discoveries of intercellularly transported macromolecules that regulate development and/or defense pathways, including transcriptional activators [2], RNA molecules [3,4] and peptide hormones [5], as well as decades-worth of information on phytohormones. These and yet to be discovered signals will be brought into a composite view of complex plant behavior with emphasis on the symplastic and apoplastic infrastructure that supports long-distance signaling as well as the downstream gene networks that synthesize this information. New advances in genomics and bioinformatics from a systems-biology approach should further help sift through the complexity of cellular and intracellular information circuitry. In animals, and particularly in humans, the concept of neurobiology is tightly coordinated with behavior. However, neurobiology also covers the coordinated behavior of communities, whether these be communities of organisms or communities of genes. At the level of unicellular bacteria, special gene circuits coordinate the behavior of inter- and intra-specic bacterial communities; this system has been termed quorum sensing [6]. Therefore, it might not be surprising that multicellular organisms such as plants have developed gene circuits that could regulate the behavior of the community. The eld of plant neurobiology will ultimately have to account for how individual plant gene circuits and signals are able to coordinate community interactions. It is becoming accepted that plants in natural environments can regulate the microbial community in their rhizosphere and that functional groups of plants are linked in natural landscapes [7,8]. In the past, pathways and gene circuits

1360-1385/$ see front matter 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2006.06.009

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Box 1. The etymological origin of the word neuron

In Plato, the word neuron is used with the connotation of vegetal fibre. In the dialogs Cratylus, Theaetetus, Sophist and Statesman: he wrote . . .and we removed the entire manufacture of cloth made from flax and broom-cords and all that we just now called vegetable fibres (neyron). . . [109]. In Athens, a cobbler was a neurorrhaphos or one who sews with vegetal fibers [110]. Thus, in the ancient Greek language, neuron is normally used to indicate a vegetal fiber and for analogy anything of fibrous nature such as a tendon as in Homers Iliad: . . .and he drew the bow, clutching at once the notched arrow and the string of oxs sinew (neyron) [111]. Indeed, this is the meaning of the word neuron as given in the classical GreekEnglish Lexicon by Henry Liddell and Robert Scott [110]. Neuron means anything of a fibrous nature. In animal cell biology, neurons are excitable animal cells that propagate electrical action potentials. Neurons are polarized and equipped with voltage-gated channels and a vesicular trafficking apparatus that is sensitive to calcium signals, mediated via synaptotagmins, induced by electrical signals. This transfer of signals occurs at electro-chemical synapses, allowing direct cellcell coupling. At the molecular level, plants have many, if not all the components found in the animal neuronal system. There are action potentials (see Box 2), voltage-gated channels, a vesicular trafficking apparatus sensitive to calcium signals, including synaptotagmins and other components of the neuronal cell infrastructure. Plants use plasmodesmata for direct cell-cell transport; these cytoplasmic connections have a poorly described role in electrical coupling between adjacent polarized plant cells [112]. It is also hypothesized that plant cells can become specialized for vesicle traffickingmediated, polarized hormonal transport.

alternative denition of plant intelligence is an intrinsic ability to process information from both abiotic and biotic stimuli that allows optimal decisions about future activities in a given environment. This Review article touches on several aspects of plant neurobiology to present some examples of emergent topics in the eld. One is the cryptic function of long-distance electrical signals and their poorly understood role in regulating plant responses. The second examines the role of homologous molecules from plants that are similar to neuroreceptors and neurotransmitters in the nervous system of animals. The nal aspect discussed is the neurotransmitter-like characteristics of the phytohormone auxin. These examples are intended to show how different topics have overlapping themes within the eld of plant neurobiology. Moreover, they also document how information generated in other areas of plant biological research, from molecular and cellular aspects of signal transduction to physiology and even community ecology of plants, might eventually be brought together toward understanding how plants acquire and integrate information so as to coordinate responses affecting the whole plant body. Early evidence of electrical signals in plants In 1791, Luigi Galvani provided the rst evidence of an electrical signal being behind the mysterious uid that was previously believed to mediate muscle contraction [17]. Stimulated by this discovery, Alexander von Humboldt carried out $4000 experiments with both animals (including himself) and plants [18]. He concluded that the bioelectrical nature of animals and plants is based on the same principles [19]. Later, Emile du Bois-Reymond [20] used a galvanometer to measure the electrical potential between the intact surface and the cut end of nerve bers (the rst crude recording of a membrane potential). He found that mechanical and electrical stimuli caused a rapid negative signal (negative Schwankung). These experiments represent the rst instrumental recording of what he then called an action potential. Within the next 30 years, action potentials were also measured in two sensitive plants: Dionaea muscipula (Venus y trap) [21] and Mimosa pudica [2224]. These discoveries suggested that the excitability of plant cells could be a means of intercellular communication in plants [2428]. Despite the repeated demonstrations of electrical long-distance signals in plants, the concept of a plant nervous-analog system lost popularity in the scientic community in favor of a chemical diffusion mechanism of signaling coinciding with the discovery and effects of plant hormones. Moreover, the early anatomical studies revealed particularities of plant cells, such as turgidity and thick cell walls, which were considered incompatible with electrical transmissions. This turn of events was so complete that electrical signals themselves were thought to be caused and mediated by chemicals [29]. Most biologists began to view plants as passive organisms without a need for rapid electrical signals. Later, publicity from pop culture in the 1970s, generated by the controversial book The Secret Life of Plants [113] (including paranormal claims that plants are attuned to human emotional states), stigmatized any possible similarities between plant signaling

have been studied at the single plant level, usually at the cellular or subcellular level. However, the ecological signicance of these gene responses in terms of competition and interaction between plants of the same species and other species and with the natural community at large have been overlooked and should be reconsidered. Plant neurobiology is as new as it is old for it touches upon the controversial question of plant intelligence. Consider what Virginia A. Shepherd [9] wrote about the work of the eminent plant electrophysiologist Jagadis Chandra Bose (18581937): he was the rst to recognize the ubiquitous importance of electrical signaling between plant cells in coordinating responses to the environment. Bose provided direct evidence that long-distance, rapid electrical signaling stimulated leaf movements in Mimosa and Desmodium and also showed that plants produce continuous, systemic electrical pulses. Boses overall conclusion that plants have an electromechanical pulse, a nervous system, a form of intelligence, and are capable of remembering and learning, was not well received in its time. A hundred years later, concepts of plant intelligence, learning, and long-distance electrical signaling in plants have entered the mainstream literature. Recently, plant neurobiological aspects have regained an audience, both among the lay press [1012] and the general scientic community [1,1315]. Nevertheless, the concept of plant intelligence generates a considerable amount of controversy. Some scientists do not view plants as intelligent organisms and so restrict the concept of intelligence only to animals or even to a specic subset of animals such as chordates or humans. One recent, rather broad denition of plant intelligence is adaptively variable growth over the lifetime of a plant [16]. An
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and animal neurobiology. Many plant biologists, wittingly or unwittingly, practiced a form of self-censorship in thought, discussion and research that inhibited asking relevant questions of possible homologies between neurobiology and phytobiology. The prohibition against anthropomorphosizing plant function, perpetuated ignorance of the work of outstanding researchers such as Sir John Burdon-Sanderson, Charles Darwin, Wilhelm Pfeffer, Georg Haberlandt and Erwin Bunning, and so prevented the investigation of the roles of electrical long-distance signals. Not surprisingly, the importance of I.I. Gunars and A.M. Sinykhins [29] discovery that action potentials exist not only in a few specialized plants such as Dionaea and Mimosa, but also in cucurbits and other normal plants, escaped mainstream plant science. Barbara Pickard summarized the knowledge of plant action potentials in 1973 [30]. A modern view of the long-distance electrical signals of plants Since Burdon-Sanderson rst measured electrical signals [21], considerable data have been collected measuring and characterizing electrical signaling in plants. Notably, the study of the electrical activity of characean cells, and more recent experiments on guard cells using patch clamp methods have created a strong base for understanding plant electrophysiology at the cellular level. Information about ion channels and transporters is available both from genomic investigations and electrophysiological characterizations of their activities. A big challenge facing plant neurobiologists is connecting this molecular information obtained at the cellular level to understanding long-distance electrical signaling and systemic responses in plants. Plants can propagate two principal types of electrical signals (Box 2). Traps of Dionaea ytraps and Aldrovanda vesiculosa, as well as of some lower plants, possess omnidirectional action potentials (APs) similar to cardiac myocytes [31]. More common among higher plants are APs that are directionally propagated in vascular bundles along the plant axis. The second type of electrical long-distance signals is slow wave potentials (SWPs) also known as variation potentials (VPs) [32]. SWPs are unique to plants;

they follow hydraulic pressure changes that use the vascular bundles (xylem) for propagation over long distances along the plant axis. Studies suggest that both APs and SWPs can be triggered by natural factors (in particular light and shade) [31,33,34]. Aside from affecting cytoplasmic calcium levels, peroxidation, respiration, photosynthesis [31,35,36] and plugging phloem transport by forisomes [37], APs have also been associated with such signaling processes as blue light-induced phototropism [34,38], ower induction [39] and recognition of herbivore attack. Electrical signals have been linked with changes in rates of respiration and photosynthesis [30,35], observed in response to pollination [40,41], phloem transport [4244], and the rapid, systemic deployment of plant defenses [4550]. A thorough understanding of how electrical signals are related to these diverse responses is still in its infancy. Novel approaches are necessary to understand the mechanistic particularities of propagating action potentials in plants over much longer distances than the length of an axon in animal nerve cells. Such approaches must be directed towards explaining the role of sieve tubes, companion cells, forisomes and plasmodesmata [51] in propagating these signals. To understand these plant electrical responses fully, such as the photoelectric response of photosynthetic cells, [52], APs [31] and SWPs [32], we will also need to dene the molecular basis behind ion-channel function involved in these processes, as well as the many different ligands that trigger these responses. Animal neurotransmitters and receptor homologs found in plants A minor sensation was caused in the plant biology community when the rst ligand-peptide hormone systemin was identied [53]. Systemin can activate defense responses throughout a damaged leaf within an hour of wounding and throughout the entire plant after a couple of hours [54]. Since then, several peptide hormones have been isolated in plants with roles involving not only defense but also development [5]. Plant peptide hormones are conserved with animal defense or developmental systems that rely on a variety of ligands that activate an ancient system of leucine-rich repeat-containing receptors [55]. Systemin-induced pathways induce depolarization of leaf cells [56]. Whether this action is the direct effect of systemin or mediated through electrical long-distance signals has not been determined [45,50,57]. Among the metabolic neurotransmitters, acetylcholine, catecholamines, histamines, serotonin, dopamine, melatonin, GABA (g-aminobutyric acid) and glutamate are the most common in the animal nervous system, playing roles in sensing, locomotion, vision, information processing and development. It has long been noted by scientists that each of these compounds are present in plants, often at relatively high concentrations [13]. However, it is unclear whether these compounds play a metabolic or a signaling role in plants despite numerous studies [1,58,59]. Among all these neurotransmitters, strong evidence now supports glutamate as a signaling molecule in plants, particularly with the discovery of a likely target of glutamate in plants the glutamate receptors [60]. Glutamate

Box 2. Electrical long-distance signals of plants

Electrical long-distance signaling in plants is well established [3136,38,39,45,51]. There are two types of electrical long-distance signals in plants: action potentials (APs) and slow wave potentials (SWPs) or variation potentials (VPs) [31,32]. Both appear as transient depolarizations in the membrane potential of affected cells, both signals share a refractory period, a time interval necessary before another signal can be induced or propagated. However, whereas APs are induced after the membrane potential of a cell drops beyond a certain threshold value (implying a crucial role of voltagegated ion channels), SWPs (VPs) are induced by rapid turgor increase. APs follow an all-or-nothing principle in producing constant, full amplitudes, whereas SWPs (VPs) are graded signals of variable size. While calcium, chloride and potassium channels are involved in the ionic mechanism of plant APs, VPs are thought to involve the transient shut down of the P-type H+ ATPase in addition to the possible involvement of unidentified ion channels [31,32]. In general, the depolarization reverts more slowly in SWPs than in the short-lived APs and, hence, the term slow in SWPs (VPs).
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causes rapid membrane depolarization in roots coupled with calcium ux in Arabidopsis [61], which acts synergistically with glycine to control ligand-mediated gating of calcium channels [62]. Genes that are similar to genes for glutamate receptors in the animal nervous system have been found in plants, including 20 such genes in Arabidopsis alone [63]. Physiological evidence indicates a role in growth potentially as a response to light [60,64], calcium sensitivity [65], nitrogen sensing [66], root growth [67], and aluminum-sensitivity mediated via microtubules [68]. Glutamate receptor agonists found in plants include kainate from seaweed, b-N-oxalylamino-L-alanine (BOAA) in grass pea (Lathyrus sativus), quisqualic acid from Quisqualis, and S(+)-b-methyl-a, b-diaminopropionic acid (BMAA) from cycads (reviewed in Ref. [69]). It is not known if these native plant agonists have protective, metabolic or signaling roles. BMAA has served as a useful compound to understand plant glutamate receptors because it alters morphogenesis in plants by enhancing hypocotyl elongation [64]. Direct genetic evidence has shown that a glutamate receptor in rice is necessary for meristematic function and organization [70], indicating a fundamental role for glutamate signaling in plant growth and development. Plant glutamate receptors are phylogenetically related to GABA receptors in animals [71]. Like glutamate, the role of GABA is undened. GABA, which is readily produced from glutamate via glutamate decarboxylase and detoxied via GABA deaminase has also been implicated in long-distance sensing as a signal for nitrogen availability [72]. GABA has also been implicated as a maternal signal in the directional growth of pollen tubes to the ovule [73] (the role of GABA in plants is reviewed in Ref. [74]). Besides glutamate and GABA, the neurotransmitter acetylcholine has also gained strong support as a signal in plants recently [75]. Acetylcholine is the only neurotransmitter that is inactivated by enzymatic cleavage via acetylcholinesterase activity. This enzyme is specically inhibited by neostigmine bromide. Interestingly, neostigmine bromide inhibits the graviresponse of maize roots; this enzyme was cloned in maize recently [75]. In silico screening has shown that homologs of maize acetylcholinesterase are widely distributed in plants [75]. Several tryptophan derivatives have been investigated for their role in signaling, including serotonin, which has been the subject of numerous studies in plant development but whose role remains elusive [13]. Melatonin has also been detected in plants and has been shown to have a role in a variety of complex processes such as owering [76,77]. Interestingly, in this respect, the most important signaling tryptophan derivative in plants is auxin, which has a basic regulatory role in plant growth and development. Auxin, which is transported cell-to-cell, also has some characteristics reminiscent of neurotransmitters as described below. Neurotransmitter-like cell-cell transport of auxin Polar transport of auxin is inherently linked to signalingbased regulation of growth and polarity of plants. For instance, the plant body is shaped in response to environmental gradients, particularly of light and gravity [78,79]; these factors inuence auxin transport such that the hormone is delivered to tissues induced to grow. Auxin is
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transported across the whole plant body via effective cell-cell transport mechanisms involving both the symplast and the apoplast. However, it is not clear why auxin bypasses the cytoplasmic channels of the plasmodesmata crossing through the apoplast, whose diameter could easily accommodate several auxin molecules. This suggests the presence of an active mechanism that prevents auxin entering the plasmodesmata [80] and implies a functional benet for including an apoplastic step in the polar transport of auxin. Transcellular auxin transport is accomplished via a poorly understood vesicle-based process that involves the putative auxin transporters, or transport facilitators, recycling between the plasma membrane and the endosomes [58,81,82]. Both PIN proteins [83,84] and certain ABC transporters have been shown to function in the polar transport of auxin [85]. Importantly, cell-cell transport of auxin is based on continuous vesicular trafcking because classical inhibitors of exocytosis, such as Brefeldin A and monensin, inhibit the polar transport of auxin within minutes in treated suspension cells [86] and intact root apices [87]. Moreover, auxin is enriched within endosomes and the cell wall region between cells across which the transcellular transport of auxin takes place [88]. Importantly, mutated PIN2 (pin2Gly97) expressed in budding yeast cells localized exclusively to intracellular compartments but was still functional in auxin transport. This particular nding strongly suggests that PIN2 can act as a vesicular transporter [84]. All these features suggest a similarity between auxin and neurotransmitter release from neuronal cells [58,81,89,90]. Considering that auxin is known to induce fast electrical responses when applied extracellularly [9193], the role of auxin can be seen in a new light when viewed from the plant neurobiology perspective [58]. One hypothesis is that auxin molecules, secreted via auxinenriched vesicles [88], elicit electrical responses in adjacent cells within a few seconds [93]. Such electrical activation would be reminiscent of signaling molecules with neurotransmitter-like properties [81]. These fast electrical responses at the plasma membranes encountering extracellular auxin molecules might be mediated via the ABP1 (auxin binding protein)-based signaling cascade [93,94] or some other receptors. This signaling cascade is likely to be distinct from the auxin-induced responses with a lag-time of many minutes to hours, which are based on auxin receptors and generally involve changes in gene expression [95] via auxin-mediated activation of transcriptional regulators known as auxin response factors [96]. Furthermore, secreted auxin molecules interact with cell wall peroxidases, inducing the formation of reactive oxygen species within the cell wall [97]. These highly reactive molecules act as potent signaling molecules in plants [98,99]. Moreover, auxin signaling is also closely linked to nitric oxide [100], which has numerous roles at neuronal synapses [101]. Further examination of the dynamic signaling properties of intercellularly transported auxin is an important topic that falls well within the realm of plant neurobiology. Last but not least, Arabidopsis cells express and use large batteries of neuronal molecules supporting

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endocytosis, vesicle trafcking and regulated secretion [102108], driving the cell-cell communication at chemical neuronal synapses. This robust vesicle trafcking apparatus of Arabidopsis ts well with the predictions made by plant neurobiology. Outlook Recent advances in plant biology, including molecular genomics and cell biology, as well as in chemical and biochemical ecology, will now allow us to study plants as behavioral organisms with a capacity to receive, store, share, process and use information from the abiotic and biotic environments. How plants acquire information from their environment, both abiotic and biotic, and integrate this information into responsive behavior is the focus of the emerging eld of plant neurobiology. Understanding this complex plant behavior within the eld of plant neurobiology will require the combined efforts of plant scientists from diverse backgrounds and from all disciplines.
Acknowledgements
We thank Robert Cleland and Tsvi Sachs for their insightful and helpful critique of this work. Their valuable ideas and in-depth experience regarding the nature of signaling in plants have been most valuable toward integrating the various concepts in this manuscript. S.M. and F.B. receive support from the Florence bank Ente Cassa Di Risparmio Di Firenze related to their activities in the eld of plant neurobiology.

References
1 Baluska, F. et al. (2006) Communication in Plants: Neuronal Aspects of Plant Life, Springer Verlag 2 Kurata, T. et al. (2005) Intercellular movement of transcription factors. Curr. Opin. Plant Biol. 8, 600605 3 Yoo, B.C. et al. (2004) A systemic small RNA signaling system in plants. Plant Cell 16, 19792000 4 Kim, J.Y. (2005) Regulation of short-distance transport of RNA and protein. Curr. Opin. Plant Biol. 8, 4552 5 Ryan, C.A. et al. (2002) Polypeptide hormones. Plant Cell 14, S251S264 6 Camilli, A. and Bassler, B.L. (2006) Bacterial small-molecule signaling pathways. Science 311, 11131116 7 Bais, H.P. et al. (2004) How plants communicate using the underground information superhighway. Trends Plant Sci. 9, 2632 8 Weir, T.L. et al. (2006) Oxalate contributes to the resistance of Gaillardia grandiora and Lupinus sericeus to a phytotoxin produced by Centaurea maculosa. Planta 223, 785795 9 Shepherd, V.A. (2005) From semi-conductors to the rhythms of sensitive plants: the research of J.C. Bose. Cell. Mol. Biol. 51, 607619 10 Simons, P. (1992) The Action Plant: Movement and Nervous Behavior in Plants, Oxford Press 11 Attenborough, D. (1995) The Private Life of Plants: A Natural History of Plant Behavior, Princeton University Press 12 Narby, J. (2005) Intelligence in Nature, J.P. Tarcher Press 13 Roshchina, V.V. (2001) Neurotransmitters in Plant Life, Science Publishers 14 Trewavas, A. (2005) Green plants as intelligent organisms. Trends Plant Sci. 10, 413419 15 Stahlberg, R. (2006) Historical overview on plant neurobiology. Plant. Signal. Behav. 1, 68 16 Trewavas, A. (2003) Aspects of plant intelligence. Ann. Bot. (Lond.) 92, 120 17 Galvani, L. (1791) De viribus Electricitatis in Motu Musculari Commentarius. Bon. Sci. Art. Inst. Acad. Comm. 7, 363418 18 von Humboldt, A. (1797) Versuche uber die gereizte Muskel- und Nervenfaser nebst Vermuthungen uber den chemischen Process des Lebens in der Thier und Panzenwelt, Posen 19 Botting, D. (1973) Humboldt and the Cosmos, Georg Rainbird 20 Du Bois-Reymond, E. (1848) Untersuchungen uber tierische Elektrizitat (Vol. I), Reimer
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21 Burdon-Sanderson, J. (1873) Note on the electrical phenomena which accompany stimulation of the leaf of Dionea muscipula. Proc. Roy. Soc. London 21, 495496 22 Kunkel, K.A.J. (1878) Uber elektromotorische Wirkungen an unverletzten lebenden Panzenteilen. Arb. Bot. Inst. Wurzburg 2, 117 23 Bose, J.Ch. (1907) Plant Response as a Means of Physiological Investigation, Longman, Green & Co 24 Bose, J.Ch. (1926) The Nervous Mechanism of Plants, Longman, Green & Co 25 Pfeffer, W. (1873) Physiologische Untersuchungen, Engelmann-Verlag 26 Pfeffer, W. (1906) The Physiology of Plants: a Treatise upon the Metabolism and Sources of Energy in Plants, Clarendon Press 27 Haberlandt, G. (1890) Das reizleitende Gewebesystem der Sinnpanze, Engelmann-Verlag 28 Bunning, E. (1959). Die seismonastischen Reaktionen. In Encyclopedia of Plant Physiology (Vol. XVII) (Physiology of Movements) (Ruhland, W., ed.), pp. 184238, Springer Verlag 29 Gunar, I.I. and Sinykhin, A.M. (1963) Functional signicance of action currents affecting the gas exchange of higher plants. Sov. Plant. Physiol. 10, 219226 30 Pickard, B.G. (1973) Action potentials in higher plants. Bot. Rev. 39, 172201 31 Trebacz, K. et al. (2006) Electrical signals in long-distance communication in plants. In Communications in Plants. Neuronal Aspects of Plant Life (Baluska, F. et al., eds), pp. 277290, Springer Verlag 32 Stahlberg, R. et al. (2006) Slow wave potentials a propagating electrical signal unique to higher plants. In Communication in Plants: Neuronal Aspects of Plant Life (Baluska, F. et al., eds), pp. 291308, Springer Verlag 33 Stahlberg, R. et al. (2006) Shade-induced action potentials in Helianthus anuus L. originate primarily from the epicotyl. Plant Signal. Behav. 1, 1522 34 Volkov, A.G. (2006) Electrophysiology and phototropism. In Communication in Plants: Neuronal Aspects of Plant Life (Baluska, F. et al., eds), pp. 351368, Springer Verlag 35 Koziolek, C. et al. (2003) Transient knockout of photosynthesis mediated by electrical signals. New Phytol. 161, 715722 36 Lautner, S. et al. (2005) Characteristics of electrical signals in poplar and responses in photosynthesis. Plant Physiol. 138, 22002209 37 Knoblauch, M. et al. (2004) ATP-independent contractile proteins from plants. Nat. Mater. 2, 600603 38 Volkov, A.G. (2000) Green plants: electrochemical interfaces. J. Electroanal. Chem. 483, 150156 39 Wagner, E. et al. (2006) Hydro-electrochemical integration of the higher plant basis for electrogenic ower initiation. In Communication in Plants: Neuronal Aspects of Plant Life (Baluska, F. et al., eds), pp. 369389, Springer Verlag 40 Sinyukhin, A.M. and Britikov, E.A. (1967) Action potentials in the reproductive system of plants. Nature 215, 12781280 41 Spanjers, A.W. (1981) Biolelectric potential changes in the style of Lilium longiorum Thunb. After self- and cross-pollination of the stigma. Planta 153, 15 42 Fromm, J. and Eschrich, W. (1988) Transport processes in stimulated and non-stimulated leaves of Mimosa pudica. Trees (Berl.) 2, 724 43 Fromm, J. and Bauer, T. (1994) Action potentials in maize sieve tubes change phloem translocation. J. Exp. Bot. 273, 463469 44 Fisahn, J. et al. (2004) Analysis of the transient increase in cytosolic Ca2+ during the action potential of higher plants with high temporal resolution: requirement of Ca2+ transients for induction of jasmonic acid biosynthesis and PINII gene expression. Plant Cell Physiol. 45, 456459 45 Wildon, D.C. et al. (1992) Electrical signaling and systemic proteinase inhibitor induction in the wounded plant. Nature 360, 6265 46 Malone, M. et al. (1994) The relationship between wound-induced proteinase inhibitors and hydraulic signals in tomato seedlings. Plant Cell Environ. 17, 8187 47 Herde, O. et al. (1995) Proteinase inhibitor II gene expression induced by electrical stimulation and control of photosynthetic activity in tomato plants. Plant Cell Physiol. 36, 737742 48 Herde, O. et al. (1996) Localized wounding by heat initiates the accumulation of proteinase inhibitor II in abscisic acid decient tomato plants by triggering jasmonic acid biosynthesis. Plant Physiol. 112, 853860

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49 Stankovic, B. and Davies, E. (1996) Both action potentials and variation potentials induce proteinase inhibitor gene expression in tomato. FEBS Lett. 390, 275279 50 Stankovic, B. and Davies, E. (1998) The wound response in tomato involves rapid growth and electric responses, systemically upregulated transcription of proteinase inhibitor and calmodulin. Plant Cell Physiol. 39, 268274 51 van Bel, A.J.E. and Ehlers, K. (2003) Electrical signalling via plasmodesmata. In Plasmodesmata (Oparka, K., ed.), pp. 263278, Blackwell Publishing 52 Spalding, E.P. et al. (1992) Ion channels in Arabidopsis plasma membrane: transport characteristics and involvement in lightinduced voltage changes. Plant Physiol. 99, 96102 53 Pearce, G. et al. (1991) A polypeptide from tomato leaves induces wound-inducible inhibitor proteins. Science 253, 895898 54 Narvaez-Vasquez, J. et al. (1995) Autoradiographic and biochemical evidence for the systemic translocation of systemin in tomato plants. Planta 195, 593600 55 Wang, Z.Y. and He, J.X. (2004) Brassinosteroid signal transduction choices of signals and receptors. Trends Plant Sci. 9, 9196 56 Moyen, C. and Johannes, E. (1996) Systemin transiently depolarizes the tomato mesophyll cell membrane and antagonizes fusicoccininduced extracellular acidication of mesophyll tissue. Plant Cell Environ. 19, 464470 57 Pena-Cortes, H. et al. (1995) Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. Proc. Natl. Acad. Sci. U. S. A. 92, 41064113 58 Baluska, F. et al. (2004) Root apices as plant command centres: the unique brain-like status of the root apex transition zone. Biologia (Bratisl.) 59, 917 59 Brenner, E.D. (2002) Drugs in the plant. Cell 109, 680681 60 Lam, H.M. et al. (1998) Glutamate-receptor genes in plants. Nature 396, 125126 61 Dennison, K.L. and Spalding, E.P. (2000) Glutamate-gated calcium uxes in Arabidopsis. Plant Physiol. 124, 15111514 62 Dubos, C. et al. (2003) A role for glycine in the gating of plant NMDAlike receptors. Plant J. 35, 800810 63 Lacombe, B. et al. (2001) The identity of plant glutamate receptors. Science 292, 14861487 64 Brenner, E.D. et al. (2000) Arabidopsis mutants resistant to S(+)-betamethyl-alpha, beta-diaminopropionic acid, a cycad-derived glutamate receptor agonist. Plant Physiol. 124, 16151624 65 Kim, S.A. et al. (2001) Overexpression of the AtGluR2 gene encoding an Arabidopsis homolog of mammalian glutamate receptors impairs calcium utilization and sensitivity to ionic stress in transgenic plants. Plant Cell Physiol. 42, 7484 66 Kang, J. and Turano, F.J. (2003) The putative glutamate receptor 1.1 (AtGLR1.1) functions as a regulator of carbon and nitrogen metabolism in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 100, 68726877 67 Filleur, S. et al. (2005) Nitrate and glutamate sensing by plant roots. Biochem. Soc. Trans. 33, 283286 68 Sivaguru, M. et al. (2003) Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. Plant Cell Physiol. 44, 667675 69 Spencer, P.S. (1999) Food toxins, ampa receptors, and motor neuron diseases. Drug Metab. Rev. 31, 561587 70 Li, J. et al. (2006) A rice glutamate receptor-like gene is critical for the division and survival of individual cells in the root apical meristem. Plant Cell 18, 340349 71 Turano, F.J. et al. (2001) The putative glutamate receptors from plants are related to two superfamilies of animal neurotransmitter receptors via distinct evolutionary mechanisms. Mol. Biol. Evol. 18, 14171420 72 Beuve, N. et al. (2004) Putative role of g-aminobutyric acid (GABA) as a long distance signal in up-regulation of nitrate uptake in Brassica napus L. Plant Cell Environ. 27, 10351046 73 Palanivelu, R. et al. (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114, 4759 74 Bouche, N. and Fromm, H. (2004) GABA in plants: just a metabolite? Trends Plant Sci. 9, 110115
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75 Sagane, Y. et al. (2005) Molecular characterization of maize acetylcholinesterase. A novel enzyme family in the plant kingdom. Plant Physiol. 138, 13591371 76 Kolar, J. and Machackova, I. (2005) Melatonin in higher plants: occurrence and possible functions. J. Pineal Res. 39, 333341 77 Arnao, M.B. and Hernandez-Ruiz, J. (2006) The physiological function of melatonin in plants. Plant Signal. Behav. 1, 8895 78 Muday, G.K. et al. (2003) Vesicular cycling mechanisms that control auxin transport polarity. Trends Plant Sci. 8, 301304 79 Friml, J. (2003) Auxin transport shaping the plant. Curr. Opin. Plant Biol. 6, 712 80 Samaj, J. et al. (2002) Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip growth. EMBO J. 21, 3296 3306 81 Baluska, F. et al. (2003) Polar transport of auxin: carrier-mediated ux across the plasma membrane or neurotransmitter-like secretion? Trends Cell Biol. 13, 282285 82 Friml, J. and Wisniewska, J. (2005). Auxin as an intercellular signal. In Intercellular Communication in Plants (Flemming A., ed.), Annual Plant Reviews 16, pp. 126, Blackwell Publishing 83 Wisniewska, J. et al. (2006) Polar PIN localization directs auxin ow in plants. Science 312, 883 84 Petrasek, J. et al. (2006) PIN proteins perform a rate-limiting function in cellular auxin efux. Science 312, 914918 85 Geisler, M. and Murphy, A. (2006) The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Lett. 580, 1094 1102 86 Delbarre, A. et al. (1998) Short-lived and phosphorylated proteins contribute to carrier-mediated efux, but not to inux, of auxin in suspension-cultured tobacco cells. Plant Physiol. 116, 833844 87 Mancuso, S. et al. (2005) Non-invasive and continuous recordings of auxin uxes in intact root apex with a carbon-nanotube-modied and self-referencing microelectrode. Anal. Biochem. 341, 344351 88 Schlicht, M. et al. (2006) Auxin immunolocalization implicates a vesicular neurotransmitter-like mode of polar auxin transport in root apices. Plant Signal. Behav. 1, 122133 89 Baluska, F. et al. (2005) Plant synapses: actin-based adhesion domains for cell-to-cell communication. Trends Plant Sci. 10, 106111 90 Barlow, P.W. et al. (2004) Polarity in roots. In Polarity in Plants (Lindsey, K., ed.), pp. 192241, Blackwell Publishing 91 Felle, H. et al. (1991) The electrical response of maize to auxin. Biochim. Biophys. Acta 1064, 199204 92 Keller, C.P. and Van Volkenburgh, E. (1996) The electrical response of Avena coleoptile cortex to auxins: evidence in vivo for activation of a Cl conductance. Planta 198, 404412 93 Steffens, B. et al. (2001) The auxin signal for protoplast swelling is perceived by extracellular ABP1. Plant J. 27, 591599 94 Bauly, J.M. et al. (2000) Overexpression of auxin-binding protein enhances the sensitivity of guard cells to auxin. Plant Physiol. 124, 12291238 95 Yamagami, M. et al. (2004) Two distinct signaling pathways participate in auxin-induced swelling of pea epidermal protoplasts. Plant Physiol. 134, 735747 96 Parry, G. and Estelle, M. (2006) Auxin receptors: a new role for F-box proteins. Curr. Opin. Cell Biol. 18, 152156 97 Kawano, T. et al. (2001) Fungal auxin antagonist hypaphorine competitively inhibits indole-3-acetic acid-dependent superoxide generation by horseradish peroxidase. Biochem. Biophys. Res. Commun. 288, 546551 98 Laloi, C. et al. (2004) Reactive oxygen signalling: the latest news. Curr. Opin. Plant Biol. 7, 323328 99 Apel, K. and Hirt, H. (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373399 100 Pagnussat, G.C. et al. (2004) Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol. 135, 279286 101 Huang, E.P. (1997) Synaptic plasticity: a role for nitric oxide in LTP. Curr. Biol. 7, R141R143 102 Sanderoot, A.A. et al. (2000) The Arabidopsis genome. An abundance of soluble N-ethylmaleimide-sensitive factor adaptor protein receptors. Plant Physiol. 124, 15581569

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103 Uemura, T. et al. (2004) Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct. Funct. 29, 4965 104 Sutter, J.-U. et al. (2006) Selective mobility and sensitivity to SNAREs is exhibited by the Arabidopsis KAT1 K+ channel at the plasma membrane. Plant Cell 18, 935954 105 Craxton, M. (2004) Synaptotagmin gene content of the sequenced genomes. BMC Genomics 5, 43 106 Rutherford, S. and Moore, I. (2002) The Arabidopsis Rab GTPase family: another enigma variation. Curr. Opin. Plant Biol. 5, 518 528 107 Murphy, A.S. et al. (2005) Endocytotic cycling of PM proteins. Annu. Rev. Plant Biol. 56, 221251

108 Samaj, J. et al. (2005) The endocytic network in plants. Trends Cell Biol. 15, 425433 109 Plato (Vol. 12, translated by H.N. Fowler), Harvard University Press, William Heinemann published 1921 110 Liddell, H.G. and Scott, R. (1940) A GreekEnglish Lexicon (revised and augmented throughout by H.S. Jones with the assistance of R. McKenzie), Clarendon Press 111 Homer The Iliad (with an English Translation by A.T. Murray 1924. Vols 1 and 2) 112 Spanswick, R.M. (1972) Electrical coupling between cells of higher plants: a direct demonstration of intercellular communication. Planta 102, 215227 113 Tomkins, P. and Bird, C. (1973) The Secret Life of Plants, Harper & Row

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