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 f ¨ur Pflanzenbiochemie, Weinberg 3, D-06120 Halle (Saale), Germany; e-mail: dscheel@ipb.uni-halle.de
Current Opinion in Plant Biology1998,1:305–310 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
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 elicitor-stimulated 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 phos-phorylation/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 soy-bean 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 phago-cytosing 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 produc-tion [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••].
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 (J ¨org 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 andin vivophosphorylation data suggest that phosphorylation cascades are involved in de-fense signaling at many different levels [32,45–51]. Some plant resistance genes encode receptor-like protein kinases themselves that may activate downstream signaling el-ements 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
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 de-pendent 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-transcrip-tional and/or post-translapost-transcrip-tional 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
the defense response in rice, whereas it is at least not necessary in parsley.
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 em-ployed 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.
Note added in proof
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.
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
•
1. Ebel J, Scheel D:Signals in host–parasite interactions.InThe 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 trans-duction mechanisms are reviewed.
•
2. Hammond-Kosack KE, Jones JDG:Plant disease resistance genes.Annu Rev Plant Physiol Plant Mol Biol1997,48:575-607. 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 J1997, 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 soybeanβ -glucan-elicitor-binding protein.Proc Natl Acad Sci USA1997,94 :1029-1034.
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 Dev1997,11:1621-1639. 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 Pathol1997, 103:753-765.
This review clearly describes the differences between systemic acquired and induced resistance in plants.
7. Sticher L, Mauch-Mani B, M ´etraux JP:Systemic acquired resistance.Annu Rev Phytopath1997,35:235-270. 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 Phytol1997,35:689-700. 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 infestansinteractions.Planta1994, 194:123-135.
11. Lamb C, Dixon RA:The oxidative burst in plant disease resistance.Annu Rev Plant Physiol Plant Mol Biol1997,48 :251-275.
•
12. 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 J1997,11 :1187-1194.
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.
•
13. Bestwick CS, Brown IR, Bennett MHR, Mansfield JW: Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells toPseudomonas syringaepv.phaseolicola.Plant Cell1997,9:209-221.
The localization of reactive oxygen species in plant tissue infected with phy-topathogenic bacteria is analyzed by electron microscopy and its appear-ance is correlated with programmed cell death.
•
14. Heath MC:Apoptosis, programmed cell death and the hypersensitive response.Eur J Plant Pathol1998,104:117-124. A critical review on cell death in animals, fungi and plants.
15. Osbourn AE:Preformed antimicrobial compounds and plant defense against fungal attack.Plant Cell1996,8:1821-1831. 16. Somssich IE, Hahlbrock K:Pathogen defense in plants — a
paradigm of biological complexity.Trends Plant Sci1998,3 :86-90.
••
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.Cell1998,92:773-784. The authors provide experimental evidence for a causal role of reactive oxy-gen species oxy-generated during the local oxidative burst in systemic develop-ment of microlesions, defense gene activation and resistance.
••
18. Jabs T, Tsch ¨ope M, Colling C, Hahlbrock K, Scheel D: Elicitor-stimulated 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 Cell1997,9:2077-2091.
An early response of tobacco cells to the elicitin cryptogein, is NADPH oxidation without changes in NAD+and ATP levels.
••
20. Zimmermann S, N ¨urnberger 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 USA1997,94:2751-2755.
Patch-clamp analysis of an elicitor-responsive plasma membrane-located ion channel, whose open probability is altered through a receptor-mediated sig-nal chain.
21. Gelli A, Higgins VJ, Blumwald E:Activation of plant plasma membrane Ca2+-permeable channels by race-specific fungal
•
22. Chandra S, Low PS:Measurement of Ca2+fluxes during
elicitation of the oxidative burst in aequorin-transformed tobacco cells.J Biol Chem1997,272:28274-28280.
Changes in cytosolic Ca2+ levels are determined in aequorin-expressing
soybean cells in response to various elicitors
••
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 Cell1998,10 :585-597.
Changes in cytosolic Ca2+levels are measured in epidermal cells of cowpea
during compatible and incompatible interactions with rust fungi. 24. 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 Chem1992,267:20140-20147.
•
25. Xing T, Higgins VJ, Blumwald E:Race-specific elicitors of
Cladosporium fulvumpromote translocation of cytosolic components of NADPH oxidase to the plasma membrane of tomato cells.Plant Cell1997,9:249-259.
Heterologous antisera raised against subunits of the human respiratory burst oxidase are employed to detect assembly of cross-reacting plant proteins. 26. Beffa R, Szell M, Meuwly P, Pay A, V ¨ogeli-Lange R, M ´etraux JP,
Neuhaus G, Meins F, Nagy J, Nagy F:Cholera toxin elevates pathogen resistance and induces pathogenesis-related gene expression in tobacco.EMBO J1995,14:5753-5761. 27. 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 USA1994,91:10556-10560.
28. Doke N:The oxidative burst: roles in signal transduction and plant stress.InOxidative 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 Phytopath1995,33:299-321.
30. Tenhaken R, Levine A, Brisson LF, Dixon RA, Lamb C:Function of the oxidative burst in hypersensitive disease resistance.Proc Natl Acad Sci USA1995,92:4158-4163.
31. Jabs T, Dietrich RA, Dangl JL:Initiation of runaway cell death in anArabidopsismutant by extracellular superoxide.Science
1996,273:1853-1856.
32. Levine A, Pennell RI, Alvarez ME, Palmer R, Lamb C: Calcium-mediated apoptosis in a plant hypersensitive disease resistance response.Curr Biol1996,6:427-437.
33. Levine A, Tenhaken R, Dixon R:hydrogen peroxide from the oxidative burst orchestrates the plant hypersensitive disease resistance response.Cell1994,79:583-593.
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 Lett1997,403:149-153.
35. Groom QJ, Torres MA, Fordham-Skelton AP, Hammond-Kosack KE, Robinson NJ, Jones JDG:rbohA, a rice homologue of the mammaliangp91phoxrespiratory burst oxidase.Plant J1996, 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 Cell1998,10:255-266.
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, Hammond-Kosack KE, Jones JDG:SixArabidopsis thalianahomologues of the human respiratory burst oxidase (gp91phox).Plant J1998,
14:365-370.
Structure and expression of sixArabidopsisgenes 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
N-acetylchitooligosaccharide elicitor and a protein phosphatase inhibitor in suspension-cultured rice cells.Protoplasma1995, 188:138-142.
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 Physiol1989,90 :109-116.
40. Doke N:Generation of superoxide anion by potato tuber protoplasts during the hypersensitive response to hyphal cell wall components ofPhytophthora infestansand specific inhibition of the reaction by suppressors of hypersensitivity.
Physiol Plant Pathol1983,23:359-367.
41. Mith ¨ofer A, Daxberger A, Fromhold-Treu D, Ebel J:Involvement of an NAD(P)H oxidase in the elicitor-inducible oxidative burst of soybean.Phytochem1997,45:1101-1107.
42. Rust ´erucci C, Stallaert V, Milat M-L, Pugin A, Ricci P, Blein J-P:Relationship between active oxygen species, lipid peroxydation, necrosis, and phytoalexin production induced by elicitins inNicotiana.Plant Physiol1996,111:885-891.
••
43. Dietrich RA, Richberg MH, Schmidt R, Dean C, Dangl JL:A novel zinc finger protein is encoded by the ArabidopsisLSD1gene 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, Mar ´echal E, Graeff R, Lee HC, Foster R, Chua N-H:Abscisic acid signaling through cyclic ADP-ribose in plants.
Science1997,278:2126-2130.
The functional involvement of cyclic ADP ribose, a well-known signal com-pound 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 Chem1990,265:6360-6368. 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 USA1991, 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 USA1994,91:952-956.
48. Viard M-P, Martin F, Pugin A, Ricci P, Blein J-P:Protein phosphorylation is induced in tobacco cells by the elicitor cryptogein.Plant Physiol1994,104:1245-1249.
49. 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 Plant1992,85:483-488. 50. Kauss H, Jeblick W:Pretreatment of parsley suspension
cultures with salicylic acid enhances spontaneous and elicited production of hydrogen peroxide.Plant Physiol1995, 108:1171-1178.
51. Suzuki K, Shinshi H:Transient activation and tyrosine phosphorylation of a protein kinase in tobacco cells treated with a fungal elicitor.Plant Cell1995,7:639-647.
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 geneXa21.Science1995,270:1804-1806. 53. Feuillet C, Schachermayr G, Keller B:Molecular cloning of a
new receptor-like kinase gene encoded at theLr10disease resistance locus of wheat.Plant J1997,11:45-52.
•
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 Sci1997,2:11-15.
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: Receptor-mediated activation of a MAP kinase in pathogen defense of plants.Science1997,276:2054-2057.
A MAP kinase is activated through an elicitor receptor and integrated into the corresponding signal transduction chain.
-element implicated in transcriptional activation of plant defense genes.Plant J1993,3:805-816.
•
58. Dr ¨oge-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 J1997,16:726-738. Elicitor treatment of soybean cells activates a protein kinase that phospho-rylates and thereby activates a transcription factor of defense genes. 59. Despr ´es C, Subramaniam R, Matton DP, Brisson N:The activation
of the potatoPR-10agene requires the phosphorylation of the nuclear factor PBF-1.Plant Cell1995,7:589-598.
••
60. Zhang S, Klessig DF:Salicylic acid activates a 48 kD MAP kinase in tobacco.Plant Cell1997,9:809-824.
The authors have purified and characterized a salicylate-responsive MAP kinase and isolated the corresponding gene.
••
61. Zhang S, Klessig DF:Resistance geneN-mediatedde novo
synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection.Proc Natl Acad Sci USA1998,95:7433-7438.
The rather unusual case is described that a MAP kinase involved in resis-tance 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 fromPhytophthoraspp.Plant Cell1998, 10:435-449.
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.Nature1997,386:855-858.
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, M ¨uller MJ, Kutchan TM, Zenk MH:Jasmonic acid is
a signal transducer in elicitor-induced plant cell cultures.Proc Natl Acad Sci USA1992,89:2389-2393.
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 Physiol1996,110 :387-392.
••
66. Delledonne M, Xia Y, Dixon RA, Lamb C:Nitric oxide signal functions in plant disease resistance.Nature1998, 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 Sci1998, in press.
