The Role of Salicylic Acid and Jasmonic Acid in Pathogen Defence

V. A. Halim; A. Vess; D. Scheel; S. Rosahl

doi:10.1055/s-2006-924025

Plant Biology, Inhaltsverzeichnis

Plant Biol (Stuttg) 2006; 8(3): 307-313
DOI: 10.1055/s-2006-924025

Review Article

Georg Thieme Verlag Stuttgart KG · New York

The Role of Salicylic Acid and Jasmonic Acid in Pathogen Defence

V. A. Halim¹ , A. Vess¹ , D. Scheel¹ , S. Rosahl¹

¹Department of Stress and Developmental Biology, Leibniz Institute of Plant Biochemistry, Weinberg 3, 06120 Halle/Saale, Germany

Abstract

Phytohormones are not only instrumental in regulating developmental processes in plants but also play important roles for the plant's responses to biotic and abiotic stresses. In particular, abscisic acid, ethylene, jasmonic acid, and salicylic acid have been shown to possess crucial functions in mediating or orchestrating stress responses in plants. Here, we review the role of salicylic acid and jasmonic acid in pathogen defence responses with special emphasis on their function in the solanaceous plant potato.

Key words

Plant-pathogen interaction - pathogen-associated molecular patterns - systemic acquired resistance - Phytophthora infestans - Solanum tuberosum.

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References

1 Abad M. S., Hakimi S. M., Kaniewski W. K., Rommens C. M., Shulaev V., Lam E., Shah D. M.. Characterization of acquired resistance in lesion-mimic transgenic potato expressing bacterio-opsin. Molecular Plant-Microbe Interactions. (1997); 10 635-645
2 Abramovitch R. B., Martin G. B.. Strategies used by bacterial pathogens to suppress plant defences. Current Opinion in Plant Biology. (2004); 7 356-364
3 Afitlhile M. M., Fukushige H., Nishimura M., Hildebrand D. F.. A defect in glyoxysomal fatty acid beta-oxidation reduces jasmonic acid accumulation in Arabidopsis. . Plant Physiology and Biochemistry. (2005); 43 603-609
4 Alvarez M. E.. Salicylic acid in the machinery of hypersensitive cell death and disease resistance. Plant Molecular Biology. (2000); 44 429-442
5 Anderson J., Badruzsaufari E., Schenk P., Manners J., Desmond O., Ehlert C., Maclean D., Ebert P., Kazan K.. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell. (2004); 16 3460-3479
6 Asai T., Tena G., Plotnikova J., Willmann M. R., Chiu W. L., Gomez-Gomez L., Boller T., Ausubel F. M., Sheen J.. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature. (2002); 415 977-983
7 Berger S., Bell E., Mullet J. E.. Two methyl jasmonate-insensitive mutants show altered expression of AtVsp in response to methyl jasmonate and wounding. Plant Physiology. (1996); 111 525-531
8 Bokshi A. I., Morris S. C., Deverall B. J.. Effects of benzothiadiazole and acetylsalicylic acid on beta-1,3-glucanase activity and disease resistance in potato. Plant Pathology. (2003); 52 22-27
9 Brunner F., Rosahl S., Lee J., Rudd J. J., Geiler C., Kauppinen S., Rasmussen G., Scheel D., Nürnberger T.. Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases. EMBO Journal. (2002); 21 6681-6688
10 Cao H., Bowling S. A., Gordon S., Dong X.. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell. (1994); 6 1583-1592
11 Cohen Y., Gisi U., Mosinger E.. Systemic resistance of potato plants against Phytophthora infestans induced by unsaturated fatty acids. Physiological and Molecular Plant Pathology. (1991); 38 255-263
12 Cohen Y., Gisi U., Niderman T.. Local and systemic protection against Phytophthora infestans induced in potato and tomato plants by jasmonic acid and jasmonic-methylester. Phytopathology. (1993); 83 1054-1062
13 Coquoz J.-L., Buchala A., Meuwly P., Métraux J.-P.. Arachidonic acid induces local but not systemic synthesis of salicylic acid and confers systemic resistance in potato plants to Phytophthora infestans and Alternaria solani. Phytopathology. (1995); 85 1219-1224
14 Coquoz J. L., Buchala A., Métraux J. P.. The biosynthesis of salicylic acid in potato plants. Plant Physiology. (1998); 117 1095-1101
15 Cruz Castillo M., Martinez C., Buchala A., Métraux J. P., Leon J.. Gene-specific involvement of beta-oxidation in wound-activated responses in Arabidopsis. . Plant Physiology. (2004); 135 85-94
16 Delaney T., Uknes S., Vernooij B., Friedrich L., Weymann K., Negrotto D., Gaffney T., Gut-Rella M., Kessmann H., Ward E., Ryals J.. A central role of salicylic acid in plant disease resistance. Science. (1994); 266 1247-1250
17 Delaney T. P., Friedrich L., Ryals J. A.. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proceedings of the National Academy of Sciences of the USA. (1995); 92 6602-6606
18 Despres C., DeLong C., Glaze S., Liu E., Fobert P. R.. The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell. (2000); 12 279-290
19 Devoto A., Nieto-Rostro M., Xie D., Ellis C., Harmston R., Patrick E., Davis J., Sherratt L., Coleman M., Turner J. G.. COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis. . The Plant Journal. (2002); 32 457-466
20 Dong X.. NPR1, all things considered. Current Opinion in Plant Biology. (2004); 7 547-552
21 Durrant W. E., Dong X.. Systemic acquired resistance. Annual Review of Phytopathology. (2004); 42 185-209
22 Farmer E. E., Johnson R. R., Ryan C. A.. Regulation of proteinase inhibitor gene expression by methyl jasmonate and jasmonic acid. Plant Physiology. (1992); 98 995-1002
23 Feussner I., Wasternack C.. The lipoxygenase pathway. Annual Review of Plant Biology. (2002); 53 275-297
24 Feys B., Benedetti C. E., Penfold C. N., Turner J. G.. Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell. (1994); 6 751-759
25 Flor H. H.. Current status of the gene-for-gene concept. Annual Review of Phytopathology. (1971); 9 275-296
26 Fobert P. R., Despres C.. Redox control of systemic acquired resistance. Current Opinion in Plant Biology. (2005); 8 378-382
27 Glazebrook J.. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology. (2005); 43 205-227
28 Göbel C., Feussner I., Hamberg M., Rosahl S.. Oxylipin profiling in pathogen-infected potato leaves. Biochimica et Biophysica Acta. (2002); 1584 55-64
29 Gomez-Gomez L., Boller T.. Flagellin perception: a paradigm for innate immunity. Trends in Plant Science. (2002); 7 251-256
30 Green T. R., Ryan C. A.. Wound-induced proteinase inhibitors in plant leaves: a possible defense mechanism against insects. Science. (1972); 175 776-777
31 Halim V. A., Hunger A., Macioszek V., Landgraf P., Nürnberger T., Scheel D., Rosahl S.. The oligopeptide elicitor Pep-13 induces salicylic acid-dependent and ‐independent defense reactions in potato. Physiological and Molecular Plant Pathology. (2004); 64 311-318
32 Howe G. A., Lightner J., Browse J., Ryan C. A.. An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell. (1996); 8 2067-2077
33 Judelson H. S., Tooley P. W.. Enhanced polymerase chain reaction methods for detecting and quantifying Phytophthora infestans in plants. Phytopathology. (2000); 90 1112-1119
34 Kim M. G., da Cunha L., McFall A. J., Belkhadir Y., DebRoy S., Dangl J. L., Mackey D.. Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defence in Arabidopsis. . Cell. (2005); 121 749-759
80 Kombrink E., Büchter R., Wegener S., Scheel D.. Systemic acquired resistance in potato. Lyr, H., Russell, P. E., and Sisler, H. D., eds. Modern Fungicides and Antifungal Compounds. Andover; Intercept Ltd. (1996): 483-491
35 Landgraf P., Feussner I., Hunger A., Scheel D., Rosahl S.. Systemic accumulation of 12-oxo-phytodienoic acid in SAR-induced potato plants. European Journal of Plant Pathology. (2002); 108 279-283
36 Li C., Schilmiller A. L., Liu G., Lee G. I., Jayanty S., Sageman C., Vrebalov J., Giovannoni J. J., Yagi K., Kobayashi Y., Howe G. A.. Role of β-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell. (2005); 17 971-986
37 Li L., Zhao Y., McCaig B. C., Wingerd B. A., Wang J., Whalon M. E., Pichersky E., Howe G. A.. The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defence responses, and glandular trichome development. Plant Cell. (2004); 16 126-143
38 Ligterink W., Kroj T., zur Nieden U., Hirt H., Scheel D.. Receptor-mediated activation of a MAP kinase in pathogen defense of plants. Science. (1997); 276 2054-2057
39 Lorenzo O., Chico J. M., Sanchez-Serrano J. J., Solano R.. JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defence responses in Arabidopsis. . Plant Cell. (2004); 16 1938-1950
40 Lorenzo O., Solano R.. Molecular players regulating the jasmonate signalling network. Current Opinion in Plant Biology. (2005); 8 532-540
41 McConn M., Browse J.. The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell. (1996); 8 403-416
42 McDowell J. M., Dangl J. L.. Signal transduction in the plant immune response. Trends in Biochemical Science. (2000); 25 79-82
43 Menke F. L., van Pelt J. A., Pieterse C. M., Klessig D. F.. Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis. Plant Cell. (2004); 16 897-907
44 Navarro L., Zipfel C., Rowland O., Keller I., Robatzek S., Boller T., Jones J.. The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiology. (2004); 135 1113-1128
45 Nickstadt A., Thomma B., Feussner I., Kangasjarvi J., Zeier J., Loeffler C., Scheel D., Berger S.. The jasmonate-insensitive mutant jin1 shows increased resistance to biotrophic as well as necrotrophic pathogens. Molecular Plant Pathology. (2004); 5 425-434
46 Niggeweg R., Thurow C., Weigel R., Pfitzner U., Gatz C.. Tobacco TGA factors differ with respect to interaction with NPR1, activation potential and DNA-binding properties. Plant Molecular Biology. (2000); 42 775-788
47 Nomura K., Melotto M., He S. Y.. Suppression of host defense in compatible plant - Pseudomonas syringae interactions. Current Opinion in Plant Biology. (2005); 8 361-368
48 Nürnberger T., Brunner F.. Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Current Opinion in Plant Biology. (2002); 5 318-324
49 Nürnberger T., Lipka V.. Non-host resistance in plants: new insights into an old phenomenon. Molecular Plant Pathology. (2005); 6 335-345
50 Nürnberger T., Nennstiel D., Jabs T., Sacks W. R., Hahlbrock K., Scheel D.. High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell. (1994); 78 449-460
51 Nürnberger T., Scheel D.. Signal transmission in the plant immune response. Trends in Plant Science. (2001); 6 372-379
52 Park J. H., Halitschke R., Kim H. B., Baldwin I. T., Feldmann K. A., Feyereisen R.. A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. The Plant Journal. (2002); 31 1-12
53 Petersen M., Brodersen P., Naested H., Andreasson E., Lindhart U., Johansen B., Nielsen H. B., Lacy M., Austin M. J., Parker J. E., Sharma S. B., Klessig D. F., Martienssen R., Mattsson O., Jensen A. B., Mundy J.. Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell. (2000); 103 1111-1120
54 Rairdan G. J., Delaney T. P.. Role of salicylic acid and NIM1/NPR1 in race-specific resistance in Arabidopsis. Genetics. (2002); 161 803-811
55 Ribnicky D. M., Shulaev V. V., Raskin I. I.. Intermediates of salicylic acid biosynthesis in tobacco. Plant Physiology. (1998); 118 565-572
81 Rosahl S., Feussner I.. Oxylipins. Murphy, D. J., ed. Plant Lipids: Biology, Utilisation and Manipulation. Oxford; Blackwell (2004): 329-454
56 Royo J., Leon J., Vancanneyt G., Albar J. P., Rosahl S., Ortego F., Castanera P., Sanchez-Serrano J. J.. Antisense-mediated depletion of a potato lipoxygenase reduces wound induction of proteinase inhibitors and increases weight gain of insect pests. Proceedings of the National Academy of Sciences of the USA. (1999); 96 1146-1151
57 Royo J., Vancanneyt G., Perez A. G., Sanz C., Störmann K., Rosahl S., Sanchez-Serrano J. J.. Characterization of three potato lipoxygenases with distinct enzymatic activities and different organ-specific and wound-regulated expression patterns. Journal of Biological Chemistry. (1996); 271 21012-21019
58 Sacks W., Nürnberger T., Hahlbrock K., Scheel D.. Molecular characterization of nucleotide sequences encoding the extracellular glycoprotein elicitor from Phytophthora megasperma. Molecular and General Genetics. (1995); 246 45-55
59 Sanchez-Serrano J., Schmidt R., Schell J., Willmitzer L.. Nucleotide sequence of proteinase inhibitor II encoding cDNA of potato (Solanum tuberosum) and its mode of expression. Molecular and General Genetics. (1986); 203 15-20
60 Schneider K., Kienow L., Schmelzer E., Colby T., Bartsch M., Miersch O., Wasternack C., Kombrink E., Stuible H. P.. A new type of peroxisomal acyl-coenzyme A synthetase from Arabidopsis thaliana has the catalytic capacity to activate biosynthetic precursors of jasmonic acid. Journal of Biological Chemistry. (2005); 280 13962-13972
61 Shah J., Tsui F., Klessig D. F.. Characterization of a Salicylic Acid-Insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Molecular Plant-Microbe Interactions. (1997); 10 69-78
62 Staswick P. E., Su W., Howell S. H.. Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proceedings of the National Academy of Sciences of the USA. (1992); 89 6837-6840
63 Staswick P. E., Tiryaki I.. The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. . Plant Cell. (2004); 16 2117-2127
64 Stelmach B. A., Muller A., Hennig P., Gebhardt S., Schubert-Zsilavecz M., Weiler E. W.. A novel class of oxylipins, sn1-O-(12-oxophytodienoyl)-sn2-O-(hexadecatrienoyl)-monogalactosyl diglyceride, from Arabidopsis thaliana. Journal of Biological Chemistry. (2001); 276 12832-12838
65 Stintzi A., Weber H., Reymond P., Browse J., Farmer E. E.. Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proceedings of the National Academy of Sciences of the USA. (2001); 98 12837-12842
66 Subramaniam R., Desveaux D., Spickler C., Michnick S. W., Brisson N.. Direct visualization of protein interactions in plant cells. Nature Biotechnology. (2001); 19 769-772
67 Tiryaki I., Staswick P. E.. An Arabidopsis mutant defective in jasmonate response is allelic to the auxin-signaling mutant axr1. Plant Physiology. (2002); 130 887-894
68 Vijayan P., Shockey J., Levesque C. A., Cook R. J., Browse J.. A role for jasmonate in pathogen defense of Arabidopsis. Proceedings of the National Academy of Sciences of the USA. (1998); 95 7209-7214
69 Vleeshouwers V., Van Dooijeweert W., Govers F., Kamoun S., Colon L. T.. Does basal PR gene expression in Solanum species contribute to non-specific resistance to Phytophthora infestans?. Physiological and Molecular Plant Pathology. (2000); 57 35-42
70 von Malek B., van der Graaff E., Schneitz K., Keller B.. The Arabidopsis male-sterile mutant dde2-2 is defective in the ALLENE OXIDE SYNTHASE gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway. Planta. (2002); 216 187-192
71 Weber H., Chetelat A., Caldelari D., Farmer E. E.. Divinyl ether fatty acid synthesis in late blight-diseased potato leaves. Plant Cell. (1999); 11 485-493
72 Weigel R. R., Pfitzner U. M., Gatz C.. Interaction of NIMIN1 with NPR1 modulates PR gene expression in Arabidopsis. . Plant Cell. (2005); 17 1279-1291
73 Wildermuth M. C., Dewdney J., Wu G., Ausubel F. M.. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature. (2001); 414 562-565
74 Xiao S., Dai L., Liu F., Wang Z., Peng W., Xie D.. COS1: an Arabidopsis coronatine insensitive1 suppressor essential for regulation of jasmonate-mediated plant defense and senescence. Plant Cell. (2004); 16 1132-1142
75 Xu L., Liu F., Lechner E., Genschik P., Crosby W. L., Ma H., Peng W., Huang D., Xie D.. The SCF(COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell. (2002); 14 1919-1935
76 Yu D., Liu Y., Fan B., Klessig D. F., Chen Z.. Is the high basal level of salicylic acid important for disease resistance in potato?. Plant Physiology. (1997); 115 343-349
77 Zhang Y., Fan W., Kinkema M., Li X., Dong X.. Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR‐1 gene. Proceedings of the National Academy of Sciences of the USA. (1999); 96 6523-6528
78 Zhou J. M., Trifa Y., Silva H., Pontier D., Lam E., Shah J., Klessig D. F.. NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR‐1 gene required for induction by salicylic acid. Molecular Plant-Microbe Interactions. (2000); 13 191-202
79 Zipfel C., Robatzek S., Navarro L., Oakeley E., Jones J., Felix G., Boller T.. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature. (2004); 428 764-767

S. Rosahl

Department of Stress and Developmental Biology
Leibniz Institute of Plant Biochemistry

Weinberg 3

06120 Halle/Saale

Germany

eMail: srosahl@ipb-halle.de

Guest Editor: R. Reski