sorry forgot to paste the txt file
here:
Full text provided by www.sciencedirect.com
Plant neurobiology: an integrated
view of plant signaling
Eric D. Brenner1, Rainer Stahlberg2, Stefano Mancuso3,4, Jorge Vivanco5,
Frantis ˇek Balus ˇka4,6,7and Elizabeth Van Volkenburgh2
1Genomics, New York Botanical Garden, NY 10458, USA
2Department of Biology, University of Washington, Seattle, WA 98195, USA
3Department of Horticulture, University of Florence, Viale delle Idee 30, 50019 Sesto Fiorentino (FI), Italy
4International Plant Neurobiology Laboratory, Viale delle idee 30, 50019 Florence, Italy; Kirschallee 1, 53115 Bonn, Germany
5Center for Rhizosphere Biology and Department of Horticulture, Colorado State University, 217 Shepardson, Fort Collins,
CO 80523-1173, USA
6Institite of Cellular and Molecular Botany, Rheinische Friedrich-Wilhelms-University of Bonn, Kirschallee 1, 53115 Bonn, Germany
7Institute of Botany, Slovak Academy of Sciences, Dubravska cesta 14, SK-84223, Bratislava, Slovak Republic
Plant neurobiology is a newly focused field of plant
biology research that aims to understand how plantsprocess the information they obtain from their environ-
ment to develop, prosper and reproduce optimally. The
behavior plants exhibit is coordinated across the wholeorganism by some form of integrated signaling, com-munication and response system. This system includeslong-distance electrical signals, vesicle-mediated trans-port of auxin in specialized vascular tissues, and produc-tion of chemicals known to be neuronal in animals. Herewe review how plant neurobiology is being directedtoward discovering the mechanisms of signaling inwhole plants, as well as among plants and theirneighbors.
The concept of plant neurobiology
To contend with environmental variability, plants oftenshow considerable plasticity in their developmental and
physiological behaviors. Some of their apparent choices
include: when and where to forage for nutrients and whereto allocate those nutrients and derived organic moleculeswithin the organism; when and what organs to generate orsenesce; when to reproduce and the number of progeny tocreate; how to mount a defense against attack and in whattissues or organs; and when and where to transmit che-mical signals to surrounding organisms. All theseresponses must occur within the context of a changingenvironment, including periodic and meteorological varia-tion regarding light, nutrients, water, wind, temperature
and attack. They must be made within the multicellular
confines of the complex biological unit of the plant bodyand, thus, require coordinated cell-to-cell signaling, whichrequires a sophisticated information storage and acquisi-tion system.
Plant neurobiology ( Box 1 ) is a newly initiated field of
research [1]aimed at understanding how plants perceive
their circumstances and respond to environmental inputin an integrated fashion, taking into account the combinedmolecular, chemical and electrical components of
intercellular plant signaling. Plant neurobiology is distinctfrom 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 directedtowards discovering and understanding the action ofunknown and known systemic signals. These signals areboth fast and slow, and are derived from electrical, hydrau-lic and chemical sources. They include recent discoveries ofintercellularly transported macromolecules that regulatedevelopment and/or defense pathways, including tran-scriptional 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 behaviorwith emphasis on the symplastic and apoplastic infrastruc-ture that supports long-distance signaling as well as thedownstream gene networks that synthesize this informa-tion. New advances in genomics and bioinformatics from asystems-biology approach should further help sift throughthe complexity of cellular and intracellular informationcircuitry.
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 communitiesof organisms or communities of genes. At the level ofunicellular bacteria, special gene circuits coordinate thebehavior of inter- and intra-specific bacterial communities;this system has been termed quorum sensing [6].
Therefore, it might not be surprising that multicellularorganisms such as plants have developed gene circuits thatcould regulate the behavior of the community. The field ofplant neurobiology will ultimately have to account for howindividual plant gene circuits and signals are able to
coordinate community interactions. It is becoming
accepted that plants in natural environments can regulatethe microbial community in their rhizosphere and thatfunctional groups of plants are linked in naturallandscapes [7,8]. In the past, pathways and gene circuits
Review TRENDS in Plant Science Vol.11 No.8
Corresponding author: Brenner, E.D. ( ebrenner@nybg.org ); Balus ˇka, F.
(baluska@uni-bonn.de ); Van Volkenburgh, E. ( lizvanv@u.washington.edu )
Available online 13 July 2006.
www.sciencedirect.com 1360-1385/$ – see front matter /C2232006 Elsevier Ltd. All rights reserved. doi: 10.1016/j.tplants.2006.06.009have been studied at the single plant level, usually at the
cellular or subcellular level. However, the ecological sig-nificance of these gene responses – in terms of competitionand interaction between plants of the same species andother 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 JagadisChandra Bose (1858–1937): ‘he was the first to recognizethe ubiquitous importance of electrical signaling betweenplant cells in coordinating responses to the environment.’Bose provided direct evidence that long-distance, rapidelectrical signaling stimulated leaf movements in Mimosa
and Desmodium and also showed that plants produce
continuous, systemic electrical pulses.
Bose’s overall conclusion that plants have an electro-
mechanical pulse, a nervous system, a form of intelligence,and are capable of remembering and learning, was not wellreceived in its time. A hundred years later, concepts ofplant intelligence, learning, and long-distance electricalsignaling in plants have entered the mainstreamliterature.
Recently, plant neurobiological aspects have regained
an audience, both among the lay press [10–12] and the
general scientific community [1,13–15] . Nevertheless,
the concept of plant intelligence generates a considerable
amount of controversy. Some scientists do not view plantsas intelligent organisms and so restrict the concept ofintelligence only to animals or even to a specific subsetof animals such as chordates or humans. One recent,rather broad definition of plant intelligence is ‘adaptivelyvariable growth over the lifetime of a plant’ [16].A nalternative definition of plant intelligence is an intrinsic
ability to process information from both abiotic and bioticstimuli that allows optimal decisions about future activ-ities in a given environment.
This Review article touches on several aspects of plant
neurobiology to present some examples of emergent topics
in the field. One is the cryptic function of long-distanceelectrical signals and their poorly understood role in reg-ulating plant responses. The second examines the role ofhomologous molecules from plants that are similar toneuroreceptors and neurotransmitters in the nervous sys-tem of animals. The final aspect discussed is the neuro-transmitter-like characteristics of the phytohormoneauxin. These examples are intended to show how differenttopics have overlapping themes within the field of plantneurobiology. Moreover, they also document how informa-
tion generated in other areas of plant biological research,
from molecular and cellular aspects of signal transductionto physiology and even community ecology of plants, mighteventually be brought together toward understandinghow plants acquire and integrate information so as tocoordinate responses affecting the whole plant body.
Early evidence of electrical signals in plants
In 1791, Luigi Galvani provided the first evidence of anelectrical signal being behind the ‘mysterious fluid’ thatwas previously believed to mediate muscle contraction
[17]. Stimulated by this discovery, Alexander von Hum-
boldt carried out /C244000 experiments with both animals
(including himself) and plants [18]. He concluded that the
bioelectrical nature of animals and plants is based on thesame principles [19]. Later, Emile du Bois-Reymond [20]
used a galvanometer to measure the electrical potentialbetween the intact surface and the cut end of nerve fibers(the first crude recording of a membrane potential). Hefound that mechanical and electrical stimuli caused a rapidnegative signal (‘negative Schwankung’). These experi-ments represent the first instrumental recording of what
he then called an ‘action potential’. Within the next 30
years, action potentials were also measured in two sensi-tive plants: Dionaea muscipula (Venus fly trap) [21] and
Mimosa pudica [22–24] .
These discoveries suggested that the excitability of
plant cells could be a means of intercellular communicationin plants [24–28] . Despite the repeated demonstrations of
electrical long-distance signals in plants, the concept of aplant nervous-analog system lost popularity in the scien-tific community in favor of a chemical diffusion mechanismof signaling coinciding with the discovery and effects of
plant hormones. Moreover, the early anatomical studies
revealed particularities of plant cells, such as turgidity andthick cell walls, which were considered incompatible withelectrical transmissions. This turn of events was so com-plete that electrical signals themselves were thought to becaused and mediated by chemicals [29]. Most biologists
began to view plants as passive organisms without a needfor rapid electrical signals. Later, publicity from pop cul-ture 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), stig-matized any possible similarities between plant signaling414 Review TRENDS in Plant Science Vol.11 No.8
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 ‘ States-
man ’: he wrote ‘ …and we removed the entire manufacture of cloth
made from flax and broom-cords and all that we just now calledvegetable 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 avegetal fiber and for analogy anything of fibrous nature such as atendon as in Homer’s Iliad: ‘ …and he drew the bow, clutching at
once the notched arrow and the string of ox’s sinew ( neyron)’[111] .
Indeed, this is the meaning of the word ‘neuron’ as given in the
classical Greek–English 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 andequipped with voltage-gated channels and a vesicular traffickingapparatus that is sensitive to calcium signals, mediated viasynaptotagmins, induced by electrical signals. This transfer ofsignals occurs at electro-chemical synapses, allowing direct cell-cell coupling. At the molecular level, plants have many, if not all thecomponents found in the animal neuronal system. There are actionpotentials (see Box 2 ), voltage-gated channels, a vesicular trafficking
apparatus sensitive to calcium signals, including synaptotagminsand other components of the neuronal cell infrastructure. Plants useplasmodesmata for direct cell-cell transport; these cytoplasmicconnections have a poorly described role in electrical couplingbetween adjacent polarized plant cells [112] . It is also hypothesized
that plant cells can become specialized for vesicle trafficking-mediated, polarized hormonal transport.
www.sciencedirect.comand animal neurobiology. Many plant biologists, wittingly
or unwittingly, practiced a form of self-censorship inthought, discussion and research that inhibited askingrelevant questions of possible homologies between neuro-biology and phytobiology. The prohibition against anthro-
pomorphosizing plant function, perpetuated ignorance of
the work of outstanding researchers such as Sir JohnBurdon-Sanderson, Charles Darwin, Wilhelm Pfeffer,Georg Haberlandt and Erwin Bu ¨nning, and so prevented
the investigation of the roles of electrical long-distancesignals. Not surprisingly, the importance of I.I. Gunar’sand A.M. Sinykhin’s [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 Pick-ard summarized the knowledge of plant action potentials
in 1973 [30].
A modern view of the long-distance electrical
signals of plantsSince Burdon-Sanderson first measured electrical signals[21], considerable data have been collected measuring and
characterizing electrical signaling in plants. Notably, thestudy of the electrical activity of characean cells, and morerecent experiments on guard cells using patch clampmethods have created a strong base for understandingplant electrophysiology at the cellular level. Information
about ion channels and transporters is available both from
genomic investigations and electrophysiological character-izations of their activities. A big challenge facing plantneurobiologists is connecting this molecular informationobtained at the cellular level to understanding long-dis-tance electrical signaling and systemic responses in plants.Plants can propagate two principal types of electricalsignals ( Box 2 ). Traps of Dionaea flytraps and Aldrovanda
vesiculosa , as well as of some lower plants, possess omni-
directional action potentials (APs) similar to cardiac myo-cytes [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-distancesignals is slow wave potentials (SWPs) also known asvariation potentials (VPs) [32]. SWPs are unique to plants;they follow hydraulic pressure changes that use the vas-
cular bundles (xylem) for propagation over long distancesalong the plant axis. Studies suggest that both APs andSWPs can be triggered by natural factors (in particularlight and shade) [31,33,34] . Aside from affecting cytoplas-
mic calcium levels, peroxidation, respiration, photosynth-
esis[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] ,
flower induction [39] and recognition of herbivore attack.
Electrical signals have been linked with changes in ratesof respiration and photosynthesis [30,35] , observed
in response to pollination [40,41] , phloem transport
[42–44] , and the rapid, systemic deployment of plant
defenses [45–50] .
A thorough understanding of how electrical signals are
related to these diverse responses is still in its infancy.
Novel approaches are necessary to understand themechanistic particularities of propagating action poten-tials in plants over much longer distances than the lengthof an axon in animal nerve cells. Such approaches must bedirected towards explaining the role of sieve tubes, com-panion cells, forisomes and plasmodesmata [51] in propa-
gating these signals. To understand these plant electricalresponses fully, such as the photoelectric response ofphotosynthetic cells, [52], APs [31]and SWPs [32], we will
also need to define 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 plantsA minor sensation was caused in the plant biologycommunity when the first ligand-peptide hormonesystemin was identified [53]. Systemin can activate
defense responses throughout a damaged leaf within anhour of wounding and throughout the entire plant after acouple 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 developmentalsystems that rely on a variety of ligands that activate anancient 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-distancesignals has not been determined [45,50,57] . Among
the metabolic neurotransmitters, acetylcholine, catechola-mines, 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 develop-ment. It has long been noted by scientists that each ofthese compounds are present in plants, often at relativelyhigh concentrations [13]. However, it is unclear whether
these compounds play a metabolic or a signaling role inplants 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 gluta-mate in plants – the glutamate receptors [60]. GlutamateReview TRENDS in Plant Science Vol.11 No.8 415
Box 2. Electrical long-distance signals of plants
Electrical long-distance signaling in plants is well established
[31–36,38,39,45,51] . 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, whereasAPs are induced after the membrane potential of a cell dropsbeyond a certain threshold value (implying a crucial role of voltage-gated ion channels), SWPs (VPs) are induced by rapid turgorincrease. APs follow an all-or-nothing principle in producingconstant, full amplitudes, whereas SWPs (VPs) are graded signalsof variable size. While calcium, chloride and potassium channels areinvolved in the ionic mechanism of plant APs, VPs are thought toinvolve the transient shut down of the P-type H
+ATPase in addition
to the possible involvement of unidentified ion channels [31,32] .I n
general, the depolarization reverts more slowly in SWPs than in theshort-lived APs and, hence, the term slow in SWPs (VPs).
www.sciencedirect.comcauses rapid membrane depolarization in roots coupled
with calcium flux in Arabidopsis [61], which acts synergis-
tically with glycine to control ligand-mediated gating ofcalcium 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 Arabi-
dopsis 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]. Glu-
tamate receptor agonists found in plants include kainatefrom 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 signal-
ing roles. BMAA has served as a useful compound to
understand plant glutamate receptors because it altersmorphogenesis in plants by enhancing hypocotyl elonga-tion [64]. Direct genetic evidence has shown that a gluta-
mate receptor in rice is necessary for meristematic functionand organization [70], indicating a fundamental role for
glutamate signaling in plant growth and development.Plant glutamate receptors are phylogenetically relatedto GABA receptors in animals [71]. Like glutamate, the
role of GABA is undefined. GABA, which is readily pro-duced from glutamate via glutamate decarboxylase and
detoxified via GABA deaminase has also been implicated
in long-distance sensing as a signal for nitrogen availabil-ity[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 acet-ylcholine has also gained strong support as a signal inplants recently [75]. Acetylcholine is the only neurotrans-
mitter that is inactivated by enzymatic cleavage via acet-ylcholinesterase activity. This enzyme is specificallyinhibited by neostigmine bromide. Interestingly, neostig-
mine bromide inhibits the graviresponse of maize roots;
this enzyme was cloned in maize recently [75].In silico
screening has shown that homologs of maize acetylcholi-nesterase are widely distributed in plants [75].
Several tryptophan derivatives have been investigated
for their role in signaling, including serotonin, which hasbeen the subject of numerous studies in plant developmentbut whose role remains elusive [13]. Melatonin has also
been detected in plants and has been shown to have a rolein a variety of complex processes such as flowering [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 character-istics reminiscent of neurotransmitters as described below.
Neurotransmitter-like cell-cell transport of auxin
Polar transport of auxin is inherently linked to signaling-based regulation of growth and polarity of plants. Forinstance, the plant body is shaped in response to environ-mental gradients, particularly of light and gravity [78,79] ;
these factors influence auxin transport such that the hor-mone is delivered to tissues induced to grow. Auxin istransported across the whole plant body via effective
cell-cell transport mechanisms involving both the symplastand the apoplast. However, it is not clear why auxinbypasses the cytoplasmic channels of the plasmodesmatacrossing through the apoplast, whose diameter could easily
accommodate several auxin molecules. This suggests the
presence of an active mechanism that prevents auxinentering the plasmodesmata [80]and implies a functional
benefit for including an apoplastic step in the polar trans-
port of auxin.
Transcellular auxin transport is accomplished via a
poorly understood vesicle-based process that involves theputative auxin transporters, or transport facilitators, recy-cling 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 traffickingbecause classical inhibitors of exocytosis, such as BrefeldinA and monensin, inhibit the polar transport of auxin withinminutes 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 thetranscellular transport of auxin takes place [88]. Impor-
tantly, mutated PIN2 (pin2Gly97) expressed in buddingyeast cells localized exclusively to intracellular compart-ments but was still functional in auxin transport. This
particular finding 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[91–93] , 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 auxin-enriched vesicles [88], elicit electrical responses in adjacent
cells within a few seconds [93]. Such electrical activation
would be reminiscent of signaling molecules with neuro-
transmitter-like properties [81]. These fast electrical
responses at the plasma membranes encountering extra-cellular 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 bedistinct from the auxin-induced responses with a lag-timeof many minutes to hours, which are based on auxinreceptors and generally involve changes in gene expression[95] via auxin-mediated activation of transcriptional reg-
ulators known as auxin response factors [96]. Further-
more, secreted auxin molecules interact with cell wall
peroxidases, inducing the formation of reactive oxygenspecies 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 sig-
naling properties of intercellularly transported auxin is animportant topic that falls well within the realm of plantneurobiology.
Last but not least, Arabidopsis cells express and use
large batteries of neuronal molecules supporting416 Review TRENDS in Plant Science Vol.11 No.8
www.sciencedirect.comendocytosis, vesicle trafficking and regulated secretion
[102–108] , driving the cell-cell communication at chemical
neuronal synapses. This robust vesicle trafficking appara-tus of Arabidopsis fits well with the predictions made by
plant neurobiology.
Outlook
Recent advances in plant biology, including moleculargenomics and cell biology, as well as in chemical andbiochemical ecology, will now allow us to study plants asbehavioral organisms with a capacity to receive, store,share, process and use information from the abiotic andbiotic environments. How plants acquire information fromtheir environment, both abiotic and biotic, and integratethis information into responsive behavior is the focus of theemerging field of plant neurobiology. Understanding this
complex plant behavior within the field of plant neurobiol-
ogy will require the combined efforts of plant scientistsfrom 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 experienceregarding 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 DiFirenze related to their activities in the field of plant neurobiology.
References
1 Balus ˇka, 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, 600–605
3 Yoo, B.C. et al. (2004) A systemic small RNA signaling system in
plants. Plant Cell 16, 1979–2000
4 Kim, J.Y. (2005) Regulation of short-distance transport of RNA and
protein. Curr. Opin. Plant Biol. 8, 45–52
5 Ryan,C.A. et al. (2002)Polypeptide hormones. PlantCell 14,S251–S264
6 Camilli, A. and Bassler, B.L. (2006) Bacterial small-molecule
signaling pathways. Science 311, 1113–1116
7 Bais, H.P. et al. (2004) How plants communicate using the
underground information superhighway. Trends Plant Sci. 9, 26–32
8 Weir, T.L. et al. (2006) Oxalate contributes to the resistance of
Gaillardia grandiflora and Lupinus sericeus to a phytotoxin
produced by Centaurea maculosa .Planta 223, 785–795
9 Shepherd, V.A. (2005) From semi-conductors to the rhythms of
sensitive plants: the research of J.C. Bose. Cell. Mol. Biol. 51, 607–619
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, 413–419
15 Stahlberg, R. (2006) Historical overview on plant neurobiology. Plant.
Signal. Behav. 1, 6–8
16 Trewavas, A. (2003) Aspects of plant intelligence. Ann. Bot. (Lond.) 92,
1–20
17 Galvani, L. (1791) De viribus Electricitatis in Motu Musculari
Commentarius. Bon. Sci. Art. Inst. Acad. Comm. 7, 363–418
18 von Humboldt, A. (1797) Versuche u ¨ber die gereizte Muskel- und
Nervenfaser nebst Vermuthungen u ¨ber den chemischen Process des
Lebens in der Thier und Pflanzenwelt , Posen
19 Botting, D. (1973) Humboldt and the Cosmos, Georg Rainbird
20 Du Bois-Reymond, E. (1848) Untersuchungen u ¨ber tierische
Elektrizita ¨t(Vol. I), Reimer21 Burdon-Sanderson, J. (1873) Note on the electrical phenomena which
accompany stimulation of the leaf of Dionea muscipula .Proc. Roy.
Soc. London 21, 495–496
22 Kunkel, K.A.J. (1878) U ¨ber elektromotorische Wirkungen an
unverletzten lebenden Pflanzenteilen. Arb. Bot. Inst. Wu ¨rzburg 2, 1–17
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 Sinnpflanze,
Engelmann-Verlag
28 Bunning, E. (1959). Die seismonastischen Reaktionen. In Encyclopedia
of Plant Physiology (Vol. XVII) ( Physiology of Movements ) (Ruhland, W.,
ed.), pp. 184–238, Springer Verlag
29 Gunar, I.I. and Sinykhin, A.M. (1963) Functional significance of action
currents affecting the gas exchange of higher plants. Sov. Plant.
Physiol. 10, 219–226
30 Pickard, B.G. (1973) Action potentials in higher plants. Bot. Rev. 39,
172–201
31 Trebacz, K. et al. (2006) Electrical signals in long-distance
communication in plants. In Communications in Plants. Neuronal
Aspects of Plant Life (Balus ˇka, F. et al. , eds), pp. 277–290, 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 (Balus ˇka, F. et al. , eds), pp.
291–308, 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, 15–22
34 Volkov, A.G. (2006) Electrophysiology and phototropism. In
Communication in Plants: Neuronal Aspects of Plant Life (Balus ˇka,
F.et al. , eds), pp. 351–368, Springer Verlag
35 Koziolek, C. et al. (2003) Transient knockout of photosynthesis
mediated by electrical signals. New Phytol. 161, 715–722
36 Lautner, S. et al. (2005) Characteristics of electrical signals in poplar
and responses in photosynthesis. Plant Physiol. 138, 2200–2209
37 Knoblauch, M. et al. (2004) ATP-independent contractile proteins
from plants. Nat. Mater. 2, 600–603
38 Volkov, A.G. (2000) Green plants: electrochemical interfaces. J.
Electroanal. Chem. 483, 150–156
39 Wagner, E. et al. (2006) Hydro-electrochemical integration of the
higher plant – basis for electrogenic flower initiation. In
Communication in Plants: Neuronal Aspects of Plant Life (Balus ˇka,
F.et al. , eds), pp. 369–389, Springer Verlag
40 Sinyukhin, A.M. and Britikov, E.A. (1967) Action potentials in the
reproductive system of plants. Nature 215, 1278–1280
41 Spanjers, A.W. (1981) Biolelectric potential changes in the style of
Lilium longiflorum Thunb. After self- and cross-pollination of the
stigma. Planta 153, 1–5
42 Fromm, J. and Eschrich, W. (1988) Transportprocesses in stimulated
a n dn o n - s t i m u l a t e dl e a v e so fM i m o s ap u d i c a . Trees (Berl.) 2, 7–24
43 Fromm, J. and Bauer, T. (1994) Action potentials in maize sieve tubes
change phloem translocation. J. Exp. Bot. 273, 463–469
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 PINIIgene expression. Plant Cell Physiol. 45, 456–459
45 Wildon, D.C. et al. (1992) Electrical signaling and systemic proteinase
inhibitor induction in the wounded plant. Nature 360, 62–65
46 Malone, M. et al. (1994) The relationship between wound-induced
proteinase inhibitors and hydraulic signals in tomato seedlings. Plant
Cell Environ. 17, 81–87
47 Herde, O. et al. (1995) Proteinase inhibitor II gene expression induced
by electrical stimulation and control of photosynthetic activity intomato plants. Plant Cell Physiol. 36, 737–742
48 Herde, O. et al. (1996) Localized wounding by heat initiates the
accumulation of proteinase inhibitor II in abscisic acid deficienttomato plants by triggering jasmonic acid biosynthesis. Plant
Physiol. 112, 853–860Review TRENDS in Plant Science Vol.11 No.8 417
www.sciencedirect.com49 Stankovic, B. and Davies, E. (1996) Both action potentials and
variation potentials induce proteinase inhibitor gene expression intomato. FEBS Lett. 390, 275–279
50 Stankovic, B. and Davies, E. (1998) The wound response in tomato
involves rapid growth and electric responses, systemically up-regulated transcription of proteinase inhibitor and calmodulin.Plant Cell Physiol. 39, 268–274
51 van Bel, A.J.E. and Ehlers, K. (2003) Electrical signalling via
plasmodesmata. In Plasmodesmata (Oparka, K., ed.), pp. 263–278,
Blackwell Publishing
52 Spalding, E.P. et al. (1992) Ion channels in Arabidopsis plasma
membrane: transport characteristics and involvement in light-induced voltage changes. Plant Physiol. 99, 96–102
53 Pearce, G. et al. (1991) A polypeptide from tomato leaves induces
wound-inducible inhibitor proteins. Science 253, 895–898
54 Narvaez-Vasquez, J. et al. (1995) Autoradiographic and biochemical
evidence for the systemic translocation of systemin in tomato plants.Planta 195, 593–600
55 Wang, Z.Y. and He, J.X. (2004) Brassinosteroid signal transduction –
choices of signals and receptors. Trends Plant Sci. 9, 91–96
56 Moyen, C. and Johannes, E. (1996) Systemin transiently depolarizes
the tomato mesophyll cell membrane and antagonizes fusicoccin-induced extracellular acidification of mesophyll tissue. Plant Cell
Environ. 19, 464–470
57 Pena-Cortes, H. et al. (1995) Signals involved in wound-induced
proteinase inhibitor II gene expression in tomato and potatoplants. Proc. Natl. Acad. Sci. U. S. A. 92, 4106–4113
58 Balus ˇka, F. et al. (2004) Root apices as plant command centres: the
unique ‘brain-like’ status of the root apex transition zone. Biologia
(Bratisl.) 59, 9–17
59 Brenner, E.D. (2002) Drugs in the plant. Cell 109, 680–681
60 Lam, H.M. et al. (1998) Glutamate-receptor genes in plants. Nature
396, 125–126
61 Dennison, K.L. and Spalding, E.P. (2000) Glutamate-gated calcium
fluxes in Arabidopsis .Plant Physiol. 124, 1511–1514
62 Dubos, C. et al. (2003) A role for glycine in the gating of plant NMDA-
like receptors. Plant J. 35, 800–810
63 Lacombe, B. et al. (2001) The identity of plant glutamate receptors.
Science 292, 1486–1487
64 Brenner, E.D. et al. (2000) Arabidopsis mutants resistant to S(+)-beta-
methyl-alpha, beta-diaminopropionic acid, a cycad-derived glutamatereceptor agonist. Plant Physiol. 124, 1615–1624
65 Kim, S.A. et al. (2001) Overexpression of the AtGluR2 gene encoding
anArabidopsis homolog of mammalian glutamate receptors impairs
calcium utilization and sensitivity to ionic stress in transgenic plants.
Plant Cell Physiol. 42, 74–84
66 Kang, J. and Turano, F.J. (2003) The putative glutamate receptor 1.1
(AtGLR1.1) functions as a regulator of carbon and nitrogenmetabolism in Arabidopsis thaliana .
Proc. Natl. Acad. Sci. U. S. A.
100, 6872–6877
67 Filleur, S. et al. (2005) Nitrate and glutamate sensing by plant roots.
Biochem. Soc. Trans. 33, 283–286
68 Sivaguru, M. et al. (2003) Aluminum rapidly depolymerizes cortical
microtubules and depolarizes the plasma membrane: evidence thatthese responses are mediated by a glutamate receptor. Plant Cell
Physiol. 44, 667–675
69 Spencer, P.S. (1999) Food toxins, ampa receptors, and motor neuron
diseases. Drug Metab. Rev. 31, 561–587
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, 340–349
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,
1417–1420
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, 1035–1046
73 Palanivelu, R. et al. (2003) Pollen tube growth and guidance is
regulated by POP2, an Arabidopsis gene that controls GABA
levels. Cell 114, 47–59
74 Bouche, N. and Fromm, H. (2004) GABA in plants: just a metabolite?
Trends Plant Sci. 9, 110–11575 Sagane, Y. et al. (2005) Molecular characterization of maize
acetylcholinesterase. A novel enzyme family in the plant kingdom.Plant Physiol. 138, 1359–1371
76 Kolar, J. and Machackova, I. (2005) Melatonin in higher plants:
occurrence and possible functions. J. Pineal Res. 39, 333–341
77 Arnao, M.B. and Herna ´ndez-Ruiz, J. (2006) The physiological function
of melatonin in plants. Plant Signal. Behav. 1, 88–95
78 Muday, G.K. et al. (2003) Vesicular cycling mechanisms that control
auxin transport polarity. Trends Plant Sci. 8, 301–304
79 Friml, J. (2003) Auxin transport – shaping the plant. Curr. Opin.
Plant Biol. 6, 7–12
80 Sˇamaj, 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 Balus ˇka, F. et al. (2003) Polar transport of auxin: carrier-mediated
flux across the plasma membrane or neurotransmitter-like secretion?Trends Cell Biol. 13, 282–285
82 Friml, J. and Wis ´niewska, J. (2005). Auxin as an intercellular signal.
InIntercellular Communication in Plants (Flemming A., ed.),
Annual
Plant Reviews 16, pp. 1–26, Blackwell Publishing
83 Wisniewska, J. et al. (2006) Polar PIN localization directs auxin flow
in plants. Science 312, 883
84 Petrasek, J. et al. (2006) PIN proteins perform a rate-limiting function
in cellular auxin efflux. Science 312, 914–918
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 efflux, but not to influx, of auxin insuspension-cultured tobacco cells. Plant Physiol. 116, 833–844
87 Mancuso, S. et al. (2005) Non-invasive and continuous recordings of
auxin fluxes in intact root apex with a carbon-nanotube-modified andself-referencing microelectrode. Anal. Biochem. 341, 344–351
88 Schlicht, M. et al. (2006) Auxin immunolocalization implicates a
vesicular neurotransmitter-like mode of polar auxin transport inroot apices. Plant Signal. Behav. 1, 122–133
89 Balus ˇka, F. et al. (2005) Plant synapses: actin-based adhesion domains
for cell-to-cell communication. Trends Plant Sci. 10, 106–111
90 Barlow, P.W. et al. (2004) Polarity in roots. In Polarity in Plants
(Lindsey, K., ed.), pp. 192–241, Blackwell Publishing
91 Felle, H. et al. (1991) The electrical response of maize to auxin.
Biochim. Biophys. Acta 1064, 199–204
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
/C0conductance. Planta 198, 404–412
93 Steffens, B. et al. (2001) The auxin signal for protoplast swelling is
perceived by extracellular ABP1. Plant J. 27, 591–599
94 Bauly, J.M. et al. (2000) Overexpression of auxin-binding protein
enhances the sensitivity of guard cells to auxin. Plant Physiol. 124,
1229–1238
95 Yamagami, M. et al. (2004) Two distinct signaling pathways
participate in auxin-induced swelling of pea epidermal protoplasts.Plant Physiol. 134, 735–747
96 Parry, G. and Estelle, M. (2006) Auxin receptors: a new role for F-box
proteins. Curr. Opin. Cell Biol. 18, 152–156
97 Kawano, T. et al. (2001) Fungal auxin antagonist hypaphorine
competitively inhibits indole-3-acetic acid-dependent superoxidegeneration by horseradish peroxidase. Biochem. Biophys. Res.
Commun. 288, 546–551
98 Laloi, C. et al. (2004) Reactive oxygen signalling: the latest news.
Curr. Opin. Plant Biol. 7, 323–328
99 Apel, K. and Hirt, H. (2004) Reactive oxygen species: metabolism,
oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55,
373–399
100 Pagnussat, G.C. et al. (2004) Nitric oxide mediates the indole acetic
acid induction activation of a mitogen-activated protein kinasecascade involved in adventitious root development. Plant Physiol.
135, 279–286
101 Huang, E.P. (1997) Synaptic plasticity: a role for nitric oxide in LTP.
Curr. Biol. 7, R141–R143
102 Sanderoot, A.A. et al. (2000) The Arabidopsis genome. An abundance
of soluble N-ethylmaleimide-sensitive factor adaptor protein
receptors. Plant Physiol. 124, 1558–1569418 Review TRENDS in Plant Science Vol.11 No.8
www.sciencedirect.com103 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, 49–65
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, 935–954
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, 221–251108 S ˇamaj, J. et al. (2005) The endocytic network in plants. Trends Cell
Biol. 15, 425–433
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 Greek–English 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, 215–227
113 Tomkins, P. and Bird, C. (1973) The Secret Life of Plants, Harper & RowReview TRENDS in Plant Science Vol.11 No.8 419
Elsevier celebrates two anniversaries with
a gift to university libraries in the developing world
In 1580, the Elzevir family began their printing and bookselling business in the Netherlands, publishing
works by scholars such as John Locke, Galileo Galilei and Hugo Grotius. On 4 March 1880, Jacobus
George Robbers founded the modern Elsevier company intending, just like the original Elzevir family, to
reproduce fine editions of literary classics for the edification of others who shared his passion, other
‘Elzevirians’. Robbers co-opted the Elzevir family printer’s mark, stamping the new Elsevier products
with a classic symbol of the symbiotic relationship between publisher and scholar. Elsevier has since
become a leader in the dissemination of scientific, technical and medical (STM) information, building a
reputation for excellence in publishing, new product innovation and commitment to its STM
communities.
In celebration of the House of Elzevir’s 425th anniversary and the 125th anniversary of the modern
Elsevier company, Elsevier donated books to ten university libraries in the developing world. Entitled
‘A Book in Your Name’, each of the 6700 Elsevier employees worldwide was invited to select one of
the chosen libraries to receive a book donated by Elsevier. The core gift collection contains the
company’s most important and widely used STM publications, including Gray’s Anatomy, Dorland’s
Illustrated Medical Dictionary, Essential Medical Physiology, Cecil Essentials of Medicine, Mosby’s
Medical, Nursing and Allied Health Dictionary, The Vaccine Book, Fundamentals of Neuroscience, and
Myles Textbook for Midwives.
The ten beneficiary libraries are located in Africa, South America and Asia. They include the Library of
the Sciences of the University of Sierra Leone; the library of the Muhimbili University College of Health
Sciences of the University of Dar es Salaam, Tanzania; the library of the College of Medicine of the
University of Malawi; and the University of Zambia; Universite du Mali; Universidade Eduardo
Mondlane, Mozambique; Makerere University, Uganda; Universidad San Francisco de Quito, Ecuador;
Universidad Francisco Marroquin, Guatemala; and the National Centre for Scientific and Technological
Information (NACESTI), Vietnam.
Through ‘A Book in Your Name’, these libraries received books with a total retail value of
approximately one million US dollars.
For more information, visit www.elsevier.com
www.sciencedirect.com