Download Resistance response physiology and signal transduction

305
Resistance response physiology and signal transduction
Dierk Scheel
Plants defend themselves against pathogen attack by
activating a multicomponent defense response. The activation
of this response requires recognition of the pathogen and
initiation of signal transduction processes that finally result
in a spatially and temporally regulated expression of individual
defense reactions. Several components involved in signaling
resistance reactions have recently been identified and
characterized.
Addresses
Institut für Pflanzenbiochemie, Weinberg 3, D-06120 Halle (Saale),
Germany; e-mail: [email protected]
Current Opinion in Plant Biology 1998, 1:305–310
http://biomednet.com/elecref/1369526600100305
 Current Biology Ltd ISSN 1369-5266
Abbreviations
HR
hypersensitive response
MAP
mitogen-activated protein
NOS
nitric oxide synthase
ROS
reactive oxygen species
SAR
systemic acquired resistance
Introduction
Plants are resistant to most potential pathogens in their
environment, as they are either not host plants for a
particular pathogen species or are host plants, but harbor
resistance genes allowing them to specifically recognize
distinct pathogen races that carry the corresponding
avirulence gene [1•,2•]. In both cases similar, if not
identical multicomponent defense responses are initiated
most probably by the interaction of elicitors that act as
ligands for receptors in the plant plasma membrane or
cytosol [1•,3•]. Although several resistance genes have
been isolated, receptor function of the corresponding
proteins remains to be demonstrated [2•]. In contrast,
several putative non-host receptors have been detected,
but with one possible exception [4•] the corresponding
genes have not been isolated [1•]. Only fragments of the
signal networks linking such receptors to defense response
elements are known [1•,5•].
Resistance response physiology
Pathogen recognition at the site of infection initiates
cellular and systemic signaling processes that activate
multicomponent defense responses at local and systemic
levels, and these responses result in rapid establishment
of local resistance and delayed development of systemic
acquired resistance [1•,6•,7]. In a generalizing view that
ignores species- and interaction-specific features, the
earliest components of the cellular response include
directed movements of organelles and the nucleus towards
the site of pathogen attack [8–10], extracellular generation
of reactive oxygen species (ROS) [11,12•,13•], formation
of cell wall appositions mostly consisting of callose at
the site of attempted penetration [12•], often followed
by cellular collapse which is one type of programmed
cell death called the hypersensitive response (HR) [14•].
These processes are frequently accompanied by release
of phenolics from disintegrating cellular compartments,
which upon contact with cytosolic enzymes are chemically
modified or polymerized [15]. Accumulation of defense
gene transcripts follows these initial events sometimes
in the attacked cells, but mostly in surrounding tissue
[16]. These genes encode pathogenesis-related proteins,
such as glucanases, chitinases, defensins etc., and enzymes
involved in the biosynthesis of phytoalexins and other,
often phenylpropanoid- or fatty acid-derived secondary
metabolites. Some of these products act directly as defense
factors, for example some pathogenesis-related proteins
and phytoalexins, whereas others apparently represent
signaling elements, such as jasmonate and salicylate, some
of which participate in the induction of systemic acquired
resistance [6•,7]. This latter type of broad resistance is
accompanied by systemic development of microlesions
and gene activation [17••]. In summary, plants are able to
activate an efficient multicomponent defense machinery,
if potential pathogens are timely recognized and the
resulting signals are appropriately processed.
Signal transduction
Apparently, pathogens are recognized by perception of
elicitors through receptors that are either located on the
plasma membrane or in the cytosol [1•–3•]. Binding of the
elicitor ligand to its receptor initiates a signal transduction
chain, whose components have been most frequently
studied with pharmacological methods in cultured plant
cells treated with various elicitors. Many elicitors do
not stimulate hypersensitive cell death, even when this
reaction occurs during the corresponding plant–pathogen
interaction [1•].
Calcium and ion channels
The earliest reactions of plant cells to elicitors are
changes in plasma membrane permeability leading to
calcium and proton influx and potassium and chloride
efflux [1•]. These ion fluxes appear to be necessary and
sufficient for induction of the oxidative burst, defense
gene activation and phytoalexin production [18••,19•]. In
parsley, a novel elicitor-responsive calcium inward channel
has been detected and characterized [20••]. By binding
to its receptor, the elicitor increases the open probability
of this plasma membrane-located ion channel and may
thereby stimulate elevated cytosolic calcium levels, as well
as activate additional ion channels and pumps that cause
the other ion fluxes observed. Another calcium-permeable
channel was found to be activated in tomato protoplasts
306
Plant–microbe interactions
in response to a race-specific elicitor from Cladosporium
fulvum [21]. As in parsley, open probability was increased
by elicitor treatment, whereas single channel conductivity
was unaffected. Transient increases in cytosolic calcium
concentrations have been detected in tobacco cells in
response to various elicitors [22•]. The inhibitory effects
of different calcium channel inhibitors, calcium chelators
and ommission of extracellular calcium on these elicitorstimulated transient changes in cytosolic calcium levels
suggest that they are at least partially caused by calcium
influx. The experimental evidence currently available,
however, is also consistent with receptor-mediated release
of calcium from internal stores as an immediate elicitor
response, which then triggers calcium influx. Elevation of
cytosolic calcium levels was also observed in epidermal
cowpea cells of resistant plants, but not susceptible plants
upon infection with appropriate races of the cowpea
rust fungus [23••]. Calcium channel inhibitors preventing
increases of cytosolic calcium concentrations also delayed
the development of the hypersensitive response.
G proteins
Several lines of pharmacological evidence suggest that
heterotrimeric GTP-binding proteins and protein phosphorylation/dephosphorylation are involved in transfering
elicitor signals from the receptor to calcium channels that
activate downstream reactions, such as the oxidative burst
and phytoalexin accumulation [21,24,25•]. In cultured soybean cells, mastoparan, a G protein-activating peptide, was
found to stimulate calcium influx, increases in cytosolic
calcium levels and production of reactive oxygen species
in the absence of elicitor [22•]. Mastoparan treatment
of parsley cells activates ion fluxes, oxidative burst and
phytoalexin accumulation in a manner comparable to
that of the elicitor response (H Zinecker, D Scheel,
unpublished data). Ectopic expression of the cholera toxin
A1 subunit inhibiting GTPase activity of G proteins
in tobacco plants resulted in high salicylate levels,
constitutive expression of PR proteins and enhanced
pathogen resistance [26]. Similar effects were reported for
tobacco plants expressing a small GTP-binding protein
[27].
Reactive oxygen species
Elicitor-mediated calcium influx, as well as transient
elevation of cytosolic calcium levels were found to be
necessary for elicitor stimulation of the oxidative burst
[18••,22•]. This extracellular generation of ROS, such as
superoxide, hydrogen peroxide and hydroxyl free radical,
is a central component of the plants defense machinery
[11,28]. ROS act as direct toxicants to pathogens [29],
catalyze early reinforcement of physical barriers [30] and
are involved in signaling later defense reactions, such
as phytoalexin synthesis and defense gene activation
[18••,31], programmed cell death [31,32] and protective
reactions in healthy tissue against ROS damage [33].
Several lines of evidence suggest that ROS production
during the oxidative burst is catalyzed by a plasma
membrane-located NAD(P)H oxidase that might show
some homologies to the mammalian respiratory burst
oxidase [19•,25•,34,35,36•,37•]. As in mammalian phagocytosing cells, superoxide radicals are the first ROS
generated and are then rapidly converted to hydrogen
peroxide and oxygen, probably by extracellular superoxide
dismutase [18••]. Furthermore, the occurrence of hydroxyl
radicals has recently been described in elicitor-treated rice
cells [38].
In several plant species, including parsley, the oxidative
burst was found to be necessary for phytoalexin production [18••,39,40], whereas inhibition of elicitor-stimulated
ROS production did not affect phytoalexin synthesis
in soybean and tobacco [33,41,42]. Loss-of-function and
gain-of-function experiments with cultured parsley cells
demonstrated that superoxide radicals generated during
the oxidative burst are involved in receptor-mediated
induction of phytoalexin accumulation by an oligopeptide
elicitor [18••]. Since superoxide radicals cannot cross the
plasma membrane, they probably generate novel signals
by interacting with plasma membrane components, such
as fatty acids and proteins.
Superoxide radicals were also found to be necessary
and sufficient to trigger programmed cell death and PR
protein expression in Arabidopsis lsd1 mutants (lesion
simulating disease resistance response) which are unable
to control lesion spreading once it is initiated [31]. The
corresponding gene encodes a zinc finger protein that
monitors an superoxidase-dependent signal and negatively
regulates plant cell death and defense gene activation
[43••].
Infection of wild-type Arabidopsis plants with an avirulent
strain of Pseudomonas syringae stimulates the formation
of local and small-sized systemic lesions, as well as
systemic acquired resistance (SAR) [17••]. Systemic lesion
formation and SAR depend on hydrogen peroxide from
the oxidative burst and on secondary systemic microbursts
[17••], but the local reaction requires both, hydrogen
peroxide and nitric oxide (M Delledonne, Y Xia, RA
Dixon C Lamb, personal communication). Avirulent
bacteria stimulate simultaneous formation of hydrogen
peroxide and nitric oxide, whereas inoculation with
virulent bacterial strains induces only a minor response.
In cultured soybean cells, hydrogen peroxide and nitric
oxide in combination are necessary and sufficient for
defense gene activation and induction of programmed cell
death. The authors propose the existence of a binary
signal transduction system with separate pathways for ROS
and nitric oxide generation that synergistically activate
defense genes and programmed cell death (M Delledonne,
Y Xia, RA Dixon, C Lamb, personal communication). In
tobacco infected with tobacco mosaic virus, nitric oxide
synthase (NOS) activity is increased and nitric oxide, as
well as NOS application, induce PR protein synthesis
and phenylalanine ammonia lyase expression (J Durner,
Resistance response physiology and signal transduction Scheel
D Wendehenne, DF Klessig, personal communication).
Pharmacological evidence from this experimental system
suggests that, as in mammals, nitric oxide-mediated gene
activation is signaled through cyclic GMP and cyclic ADP
ribose. Cyclic ADP ribose, therefore, may represent a very
upstream player in both hormone and defense signaling,
since it activates abscisic acid- and pathogen-responsive
genes through calcium release mechanisms (Jörg Durner,
David Wendehenne and Daniel F Klessig, personal
communication) [44••]. It remains to be elucidated,
however, whether this calcium release is at all related
to the calcium influx and transient increases in cytosolic
calcium that are rapidly stimulated by elicitor treament
and infection [18••,20••,21,22•,23••].
Protein kinases
Pharmacological evidence and in vivo phosphorylation data
suggest that phosphorylation cascades are involved in defense signaling at many different levels [32,45–51]. Some
plant resistance genes encode receptor-like protein kinases
themselves that may activate downstream signaling elements by phosphorylation [2•,52,53]. The Pto gene of
tomato, which confers resistance to bacterial speck disease,
encodes a cytosolic serine/threonine kinase that interacts
with other proteins, probably by phosphorylating them;
some of these target proteins are putative transcription
factors thought to activate PR protein-encoding genes
[54•].
Recently, a class of protein kinases with strong homology
to mitogen-activated protein kinases (MAP kinases) of
yeast and mammals was found to be involved in signaling
cascades of plants as well [55•]. Receptor-mediated rapid
and transient activation of the elicitor-responsive MAP
kinase, ERM kinase, was demonstrated in cultured parsley
cells treated with an oligopeptide elicitor [56••]. Within the
corresponding signal transduction chain, activation of this
MAP kinase is located downstream of elicitor-responsive
ion channels, but upstream or independent of the
oxidative burst. Upon activation, ERM kinase was found
to be translocated to the nucleus, where it may be involved
in defense gene activation. Several putative transcription
factors of plant defense genes indeed appear to be
regulated by phosphorylation [57,58•,59].
A salicylate-responsive MAP kinase, SIP kinase, has been
purified from tobacco [60••]. Salicylic acid, which is
known to be an important signal molecule in local and
systemic defense responses in many plants [5•], as well
as its biologically active analogs, activate SIP kinase,
induce PR protein expression and enhance pathogen
resistance in tobacco [60••]. Furthermore, SIP kinase is
activated in tobacco mosaic virus-infected resistant tobacco
plants [61••] by two well-defined elicitins, parasiticein and
cryptogein, and a crude cell wall elicitor which all derived
from Phytophthora spp. [62••]. Most interestingly, the
elicitins which activate defense genes, induce phytoalexin
production and stimulate an oxidative burst and proton
307
influx in tobacco, also cause hypersensitive cell death and
prolonged SIP kinase activation. In contrast, the crude cell
wall elicitor does not cause cell death and only activates
SIP kinase very transiently. Furthermore, the elicitins
activate at least two more unknown putative MAP kinases
that do not respond to the cell wall elicitor preparation
[62••].
A wound-responsive MAP kinase from tobacco, WIP
kinase, is activated locally and systemically in response to
tobacco mosaic virus infection in an resistance-gene dependent manner [61••]. In this case, the post-translational
activation of WIP kinase is preceded by, and requires
accumulation of, the corresponding transcript and protein.
Since these processes are independent of salicylate, WIP
kinase is considered to be a signal component located
upstream of salicylate in local and systemic resistance of
tobacco to tobacco mosaic virus. Differential activation
of distinct MAP kinases at transcriptional, post-transcriptional and/or post-translational levels with elicitor-specific
kinetics may, therefore, be important for the generation of
signal-specific reactions. The importance of signal duration
has also been observed for elicitor-stimulated ion fluxes
in parsley, where quality and kinetics were found to be
important for the resulting gene activation pattern [18••]
and for the oxidative burst, which occurs with different
kinetics in compatible and incompatible plant pathogen
interactions [11]. Most interestingly, transcription factors
were found to be differentially activated in animal cells
by calcium response amplitude and duration [63••]. As
elicitor-mediated ion fluxes appear to be located upstream
of MAP kinase activation within defense signal cascades
[56••], these regulation phenomena may be causally
related.
Jasmonate
The rapid accumulation of jasmonate has been observed
in many cultured plant cells in response to various elicitor
treatments [1•,64]. In suspension-cultured rice cells, an
N-acetylchitoheptaose elicitor induces the synthesis of
the phytoalexin, momilactone A, which is preceded by
transient accumulation of jasmonate [65]. Avoidance of
elicitor-stimulated jasmonate accumulation by the lipoxygenase inhibitor, ibuprofen, also prevented phytoalexin
accumulation which could still be induced by exogenous
jasmonate application. Contrasting results were recently
obtained with cultured parsley cells, where jasmonate
accumulation is stimulated through the oligopeptide
receptor downstream of ion fluxes and oxidative burst
(T Kroj, D Scheel, unpublished data). In this experimental system, however, complete suppression of elicitorstimulated jasmonate accumulation by the lipoxygenase
inhibitors phenidone, indoprofen or ibuprofen does not
at all affect elicitor-induced defense gene activation and
phytoalexin accumulation. In accordance with this result,
jasmonate or its derivatives are poor elicitors in parsley
cells. It may be concluded, therefore, that jasmonate
appears to be necessary and sufficient for triggering
308
Plant–microbe interactions
the defense response in rice, whereas it is at least not
necessary in parsley.
This review clearly describes the differences between systemic acquired and
induced resistance in plants.
7.
Sticher L, Mauch-Mani B, Métraux JP: Systemic acquired
resistance. Annu Rev Phytopath 1997, 35:235-270.
8.
Heath MC, Nimchuk ZL, Xu H: Plant nuclear migrations
as indicators of critical interactions between resistant or
susceptible cowpea epidermal cells and invasion hyphae of
the cowpea rust fungus. New Phytol 1997, 35:689-700.
9.
Gross P, Julius C, Schmelzer E, Hahlbrock K: Translocation
of cytoplasm and nucleus to fungal penetration sites is
associated with depolymerization of microtubules and defense
gene activation in infected, cultured parsley cells. EMBO J
1993, 12:1735-1744.
10.
Freytag S, Arabatzis N, Hahlbrock K, Schmelzer E: Reversible
cytoplasmic rearrangements precede wall apposition,
hypersensitive cell death and defense-related gene activation
in potato/Phytophthora infestans interactions. Planta 1994,
194:123-135.
11.
Lamb C, Dixon RA: The oxidative burst in plant disease
resistance. Annu Rev Plant Physiol Plant Mol Biol 1997, 48:251275.
Conclusions
The multicomponent defense response of plants to
pathogens appears to be activated by ligand/receptor
interactions, in which avr gene- and pathogen or plant
surface-derived elicitors serve as ligands for plasma
membrane-located or cytosolic receptors. Most elicitors
activate defense genes and induce phytoalexin synthesis,
whereas only a subset also stimulates programmed cell
death. It is not clear yet, at which level of signal
transduction both signaling pathways separate. Amplitude
and duration, however, of individual signal elements may
be important for the quality of the final reaction.
Highly conserved signaling elements appear to be employed in elicitor signal transduction, such as ion channels,
calcium transients, protein kinases and phosphatases,
G-proteins, ROS, NO, cyclic GMP, cyclic ADP ribose and
fatty acid derivatives. The way how, and if at all, a distinct
signal element is integrated into a given plants signaling
network, however, appears to be rather variable.
Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB: Subcellular
localization of hydrogen peroxide in plants, hydrogen peroxide
accumulation in papillae and hypersensitive response during
the barley-powdery mildew interaction. Plant J 1997, 11:11871194.
The authors describe the light microscopical localization of reactive oxygen
species in infected barley plants in relation to other early defense responses
and programmed cell death.
Note added in proof
13.
•
The papers referred to in the text as (M Delledonne, Y
Xia, RA Dixon and C Lamb, personal communication)
and (J Durner, D Wendehenne, DF Klessig, personal
communication) have now been accepted for publication
as [66••] and [67••] respectively.
12.
•
Bestwick CS, Brown IR, Bennett MHR, Mansfield JW:
Localization of hydrogen peroxide accumulation during the
hypersensitive reaction of lettuce cells to Pseudomonas
syringae pv. phaseolicola. Plant Cell 1997, 9:209-221.
The localization of reactive oxygen species in plant tissue infected with phytopathogenic bacteria is analyzed by electron microscopy and its appearance is correlated with programmed cell death.
14.
Heath MC: Apoptosis, programmed cell death and the
•
hypersensitive response. Eur J Plant Pathol 1998, 104:117-124.
A critical review on cell death in animals, fungi and plants.
References and recommended reading
15.
Papers of particular interest, published within the annual period of review,
have been highlighted as:
Osbourn AE: Preformed antimicrobial compounds and plant
defense against fungal attack. Plant Cell 1996, 8:1821-1831.
16.
Somssich IE, Hahlbrock K: Pathogen defense in plants — a
paradigm of biological complexity. Trends Plant Sci 1998, 3:8690.
• of special interest
•• of outstanding interest
1.
•
Ebel J, Scheel D: Signals in host–parasite interactions. In The
Mycota; Vol V, Plant Relationships, Part A. Edited by Carroll GC,
Tudzynski P. Berlin: Springer-Verlag; 1997:85-105.
The structure of known elicitors, their mode of recognition and signal transduction mechanisms are reviewed.
2.
Hammond-Kosack KE, Jones JDG: Plant disease resistance
•
genes. Annu Rev Plant Physiol Plant Mol Biol 1997, 48:575-607.
This review describes structure and function of plant disease resistance
genes.
3.
•
Bonas U, Van den Ackerveken G: Recognition of bacterial
avirulence proteins occurs inside the plant cell: a general
phenomenon in resistance to bacterial diseases? Plant J 1997,
12:1-7.
The recognition of bacterial avirulence gene products by the corresponding
cytosolic plant resistance gene products is updated.
4.
•
Umemoto N, Kakitani M, Iwamatsu A, Yoshikawa M, Yamaoka N,
Ishida I: The structure and function of a soybean β-glucanelicitor-binding protein. Proc Natl Acad Sci USA 1997, 94:10291034.
The manuscript describes the isolation and characterization of a soybean
gene encoding one component of a binding site for a glucan elicitor from
Phytophthora sojae.
5.
Yang Y, Shah J, Klessig DF: Signal perception and transduction
•
in plant defense responses. Genes Dev 1997, 11:1621-1639.
The authors provide an excellent detailed summary of local and systemic
plant defense signaling.
6.
•
Van Loon LC: Induced resistance in plants and the role
of pathogenesis-related proteins. Eur J Plant Pathol 1997,
103:753-765.
17.
••
Alvarez ME, Pennell RI, Meijer P-J, Ishikawa A, Dixon RA, Lamb C:
Reactive oxygen intermediates mediate a systemic network in
the establishment of plant immunity. Cell 1998, 92:773-784.
The authors provide experimental evidence for a causal role of reactive oxygen species generated during the local oxidative burst in systemic development of microlesions, defense gene activation and resistance.
18.
••
Jabs T, Tschöpe M, Colling C, Hahlbrock K, Scheel D: Elicitorstimulated ion fluxes and O2− from the oxidative burst are
essential components in triggering defense gene activation
and phytoalexin synthesis in parsley. Proc Natl Acad Sci USA
1997, 94:4800-4805.
Evidence is provided that links receptor-mediated ion fluxes via the oxidative
burst with defense gene activation and phytoalexin production.
19.
•
Pugin A, Frachisse J-M, Tavernier E, Bligny R, Gout E, Douce R,
Guern J: Early events induced by the elicitor cryptogein
in tobacco cells: involvement of a plasma membrane
NADPH oxidase and activation of glycolysis and the pentose
phosphate pathway. Plant Cell 1997, 9:2077-2091.
An early response of tobacco cells to the elicitin cryptogein, is NADPH
oxidation without changes in NAD+ and ATP levels.
20.
••
Zimmermann S, Nürnberger T, Frachisse J-M, Wirtz W, Guern J,
Hedrich R, Scheel D: Receptor-mediated activation of a plant
Ca2+-permeable ion channel involved in pathogen defense.
Proc Natl Acad Sci USA 1997, 94:2751-2755.
Patch-clamp analysis of an elicitor-responsive plasma membrane-located ion
channel, whose open probability is altered through a receptor-mediated signal chain.
21.
Gelli A, Higgins VJ, Blumwald E: Activation of plant plasma
membrane Ca2+-permeable channels by race-specific fungal
elicitors. Plant Physiol 1997, 113:269-279.
Resistance response physiology and signal transduction Scheel
Chandra S, Low PS: Measurement of Ca2+ fluxes during
elicitation of the oxidative burst in aequorin-transformed
tobacco cells. J Biol Chem 1997, 272:28274-28280.
Changes in cytosolic Ca2+ levels are determined in aequorin-expressing
soybean cells in response to various elicitors
22.
•
309
39.
Apostol I, Heinstein PF, Low PS: Rapid stimulation of an
oxidative burst during elicitation of cultured plant cells: role
in defense and signal transduction. Plant Physiol 1989, 90:109116.
40.
Doke N: Generation of superoxide anion by potato tuber
protoplasts during the hypersensitive response to hyphal
cell wall components of Phytophthora infestans and specific
inhibition of the reaction by suppressors of hypersensitivity.
Physiol Plant Pathol 1983, 23:359-367.
41.
Legendre L, Heinstein PF, Low PS: Evidence for participation of
GTP-binding proteins in elicitation of the rapid oxidative burst
in cultured soybean cells. J Biol Chem 1992, 267:20140-20147.
Mithöfer A, Daxberger A, Fromhold-Treu D, Ebel J: Involvement of
an NAD(P)H oxidase in the elicitor-inducible oxidative burst of
soybean. Phytochem 1997, 45:1101-1107.
42.
Xing T, Higgins VJ, Blumwald E: Race-specific elicitors of
Cladosporium fulvum promote translocation of cytosolic
components of NADPH oxidase to the plasma membrane of
tomato cells. Plant Cell 1997, 9:249-259.
Heterologous antisera raised against subunits of the human respiratory burst
oxidase are employed to detect assembly of cross-reacting plant proteins.
Rustérucci C, Stallaert V, Milat M-L, Pugin A, Ricci P, Blein JP: Relationship between active oxygen species, lipid
peroxydation, necrosis, and phytoalexin production induced
by elicitins in Nicotiana. Plant Physiol 1996, 111:885-891.
43.
••
23.
••
Xu H, Heath MC: Role of calcium in signal transduction during
the hypersensitive response caused by basidiospore-derived
infection of the cowpea rust fungus. Plant Cell 1998, 10:585597.
Changes in cytosolic Ca2+ levels are measured in epidermal cells of cowpea
during compatible and incompatible interactions with rust fungi.
24.
25.
•
26.
27.
Beffa R, Szell M, Meuwly P, Pay A, Vögeli-Lange R, Métraux JP,
Neuhaus G, Meins F, Nagy J, Nagy F: Cholera toxin elevates
pathogen resistance and induces pathogenesis-related gene
expression in tobacco. EMBO J 1995, 14:5753-5761.
Sano H, Seo S, Orudgev E, Youssefian S, Ishizuka K, Ohashi Y:
Expression of the gene for a small GTP-binding protein in
transgenic tobacco elevates endogenous cytokinin levels,
abnormally induces salicylic acid in response to wounding, and
increases resistance to tobacco mosaic virus infection. Proc
Natl Acad Sci USA 1994, 91:10556-10560.
Dietrich RA, Richberg MH, Schmidt R, Dean C, Dangl JL: A novel
zinc finger protein is encoded by the Arabidopsis LSD1 gene
and functions as a negative regulator of plant cell death. Cell
1997, 88:685-694.
The gene encodes a protein that monitors a superoxide-dependent signal
and negatively regulates plant cell death and defense gene activation.
44.
••
Wu Y, Kuzma J, Maréchal E, Graeff R, Lee HC, Foster R, Chua NH: Abscisic acid signaling through cyclic ADP-ribose in plants.
Science 1997, 278:2126-2130.
The functional involvement of cyclic ADP ribose, a well-known signal compound in animal cells, in plant hormone signaling is described.
45.
Dietrich A, Mayer JE, Hahlbrock K: Fungal elicitor triggers rapid,
transient, and specific protein phosphorylation in parsley cell
suspension cultures. J Biol Chem 1990, 265:6360-6368.
46.
Felix G, Grosskopf DG, Regenass M, Boller T: Rapid changes
in protein phosphorylation are involved in transduction of the
elicitor signal in plant cells. Proc Natl Acad Sci USA 1991,
88:8831-8834.
47.
Felix G, Regenass M, Spanu P, Boller T: The protein
phosphatase inhibitor calyculin A mimics elicitor action in
plant cells and induces rapid hyperphosphorylation of specific
proteins as revealed by pulse labeling with [33P] phosphate.
Proc Natl Acad Sci USA 1994, 91:952-956.
28.
Doke N: The oxidative burst: roles in signal transduction and
plant stress. In Oxidative Stress and the Molecular Biology of
Antioxidant Defenses. Edited by Scandalios JG. New York: Cold
Spring Harbor Laboratory Press; 1997:785-813.
29.
Baker CJ, Orlandi EW: Active oxygen in plant pathogenesis.
Annu Rev Phytopath 1995, 33:299-321.
30.
Tenhaken R, Levine A, Brisson LF, Dixon RA, Lamb C: Function of
the oxidative burst in hypersensitive disease resistance. Proc
Natl Acad Sci USA 1995, 92:4158-4163.
48.
31.
Jabs T, Dietrich RA, Dangl JL: Initiation of runaway cell death
in an Arabidopsis mutant by extracellular superoxide. Science
1996, 273:1853-1856.
Viard M-P, Martin F, Pugin A, Ricci P, Blein J-P: Protein
phosphorylation is induced in tobacco cells by the elicitor
cryptogein. Plant Physiol 1994, 104:1245-1249.
49.
32.
Levine A, Pennell RI, Alvarez ME, Palmer R, Lamb C: Calciummediated apoptosis in a plant hypersensitive disease
resistance response. Curr Biol 1996, 6:427-437.
Kauss H, Jeblick W, Conrath U: Protein kinase inhibitor K-252a
and fusicoccin induce similar initial changes in ion transport of
parsley suspension cells. Physiol Plant 1992, 85:483-488.
50.
33.
Levine A, Tenhaken R, Dixon R: hydrogen peroxide from the
oxidative burst orchestrates the plant hypersensitive disease
resistance response. Cell 1994, 79:583-593.
Kauss H, Jeblick W: Pretreatment of parsley suspension
cultures with salicylic acid enhances spontaneous and
elicited production of hydrogen peroxide. Plant Physiol 1995,
108:1171-1178.
51.
34.
Kieffer F, Simon-Plas F, Maume BF, Blein JP: Tobacco cells
contain a protein, immunologically related to the neutrophil
small G protein Rac2 and involved in elicitor-induced oxidative
burst. FEBS Lett 1997, 403:149-153.
Suzuki K, Shinshi H: Transient activation and tyrosine
phosphorylation of a protein kinase in tobacco cells treated
with a fungal elicitor. Plant Cell 1995, 7:639-647.
52.
Song WY, Wang GL, Chen LL, Kim HX, Pi LY, Holsten T,
Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P:
A receptor kinase-like protein encoded by the rice disease
resistance gene Xa21. Science 1995, 270:1804-1806.
53.
Feuillet C, Schachermayr G, Keller B: Molecular cloning of a
new receptor-like kinase gene encoded at the Lr10 disease
resistance locus of wheat. Plant J 1997, 11:45-52.
35.
Groom QJ, Torres MA, Fordham-Skelton AP, Hammond-Kosack KE,
Robinson NJ, Jones JDG: rbohA, a rice homologue of the
mammalian gp91phox respiratory burst oxidase. Plant J 1996,
10:515-522.
36.
•
Keller T, Damude HG, Werner D, Doerner P, Dixon RA, Lamb C:
A plant homolog of the neutrophil NADPH oxidase gp91phox
subunit gene encodes a plasma membrane protein with
calcium binding motifs. Plant Cell 1998, 10:255-266.
The plant homolog of a subunit of the human respiratory burst oxidase has
been isolated, characterized and its localization in the plasma membrane
determined using homologous antisera.
37.
•
Torres MA, Onouchi H, Hamada S, Machida C, HammondKosack KE, Jones JDG: Six Arabidopsis thaliana homologues of
the human respiratory burst oxidase (gp91phox). Plant J 1998,
14:365-370.
Structure and expression of six Arabidopsis genes with significant homology
to a subunit of the human respiratory burst oxidase are described.
38.
Kuchitsu K, Kosaka H, Shiga T, Shibuya N: EPR evidence
for generation of hydroxyl radical triggered by Nacetylchitooligosaccharide elicitor and a protein phosphatase
inhibitor in suspension-cultured rice cells. Protoplasma 1995,
188:138-142.
54.
•
Zhou J, Tang X, Martin GB: The Pto kinase conferring resistance
to tomato bacterial speck disease interacts with proteins that
bind a cis-element of pathogenesis-related genes. EMBO J
1997, 16:3207-3218.
Genes encoding putative transcription factors for defense genes interact
with the cytoplasmic receptor for a bacterial avirulence gene product.
55.
Hirt H: Multiple roles of MAP kinases in plant signal
•
transduction. Trend Plant Sci 1997, 2:11-15.
The author reviews evidence for functional involvement of MAP kinases in
plant signal transduction pathways.
56.
••
Ligterink W, Kroj T, zur Nieden U, Hirt H, Scheel D: Receptormediated activation of a MAP kinase in pathogen defense of
plants. Science 1997, 276:2054-2057.
A MAP kinase is activated through an elicitor receptor and integrated into
the corresponding signal transduction chain.
57.
Yu LM, Lamb CJ, Dixon RA: Purification and biochemical
characterization of proteins which bind to the H-box cis-
310
Plant–microbe interactions
element implicated in transcriptional activation of plant
defense genes. Plant J 1993, 3:805-816.
58.
•
Dröge-Laser W, Kaiser A, Lindsay WP, Halkier BA, Loake GJ,
Doerner P, Dixon RA, Lamb C: Rapid stimulation of a soybean
protein-serine kinase which phosphorylates a novel bZIP
DNA-binding protein, G/HBF-1, during the induction of early
transcription-dependent defenses. EMBO J 1997, 16:726-738.
Elicitor treatment of soybean cells activates a protein kinase that phosphorylates and thereby activates a transcription factor of defense genes.
59.
Després C, Subramaniam R, Matton DP, Brisson N: The activation
of the potato PR-10a gene requires the phosphorylation of the
nuclear factor PBF-1. Plant Cell 1995, 7:589-598.
MAP kinases are differentially activated by various elicitors and the duration
of their activation is correlated with response specificity.
63.
••
Dolmetsch RE, Lewis RS, Goodnow CC, JIH: Differential
activation of transcription factors induced by calcium response
amplitude and duration. Nature 1997, 386:855-858.
The differential activation of transcription factors in animal cells appears to
be regulated through response amplitude and duration of Ca2+ transients,
a regulatory mechanism that is probably also important in plants.
64.
Gundlach H, Müller MJ, Kutchan TM, Zenk MH: Jasmonic acid is
a signal transducer in elicitor-induced plant cell cultures. Proc
Natl Acad Sci USA 1992, 89:2389-2393.
65.
Nojiri H, Sugimori M, Yamane H, Nishimura Y, Yamada A,
Shibuya N, Kodama O, Murofushi N, Omori T: Involvement of
jasmonic acid in elicitor-induced phytoalexin production in
suspension-cultured rice cells. Plant Physiol 1996, 110:387392.
60.
Zhang S, Klessig DF: Salicylic acid activates a 48 kD MAP
••
kinase in tobacco. Plant Cell 1997, 9:809-824.
The authors have purified and characterized a salicylate-responsive MAP
kinase and isolated the corresponding gene.
61.
••
Zhang S, Klessig DF: Resistance gene N-mediated de novo
synthesis and activation of a tobacco mitogen-activated
protein kinase by tobacco mosaic virus infection. Proc Natl
Acad Sci USA 1998, 95:7433-7438.
The rather unusual case is described that a MAP kinase involved in resistance gene-mediated signal transduction is activated at the transcriptional
level.
62.
••
Zhang S, Du H, Klessig DF: Activation of the tobacco SIP kinase
by both a cell wall-derived carbohydrate elicitor and purified
proteinaceous elicitins from Phytophthora spp. Plant Cell 1998,
10:435-449.
66.
Delledonne M, Xia Y, Dixon RA, Lamb C: Nitric oxide signal
••
functions in plant disease resistance. Nature 1998, in press.
Direct evidence is provided for the involvement of both hydrogen peroxide
and nitric oxide in signaling defense gene activation and programmed cell
death in plant disease resistance.
67.
••
Durner J, Wendehenne D, Klessig DF: Defense gene induction in
tobacco by nitric oxide, cyclic GMP and cyclic ADP ribose. Proc
Natl Acad Sci 1998, in press.
Results are presented that suggest the involvement of a signal transduction
chain consisting of nitric oxide, cyclic GMP and cyclic ADP ribose in elicitormediated gene activation.