Chemical warfare or modulators of defence responses - the function of secondary metabolites in plant immunity

Current Opinion in Plant Biology

Volumn 15, Issue 4, 2012, Pages 407-414

  Bednarek, Paweł ^a  

^a INSTITUTE OF BIOORGANIC CHEMISTRY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

3 INDOLECARBOXYLIC ACID; ABC TRANSPORTER; ANTIINFECTIVE AGENT; BENZOXAZINE DERIVATIVE; CAMALEXIN; CHEMICAL WARFARE AGENT; GLUCOSINOLATE; INDOLE DERIVATIVE; INDOLE-3-CARBOXYLIC ACID; ISOTHIOCYANIC ACID DERIVATIVE; THIAZOLE DERIVATIVE;

BACTERIUM; CELL WALL; FUNGUS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PLANT; PLANT IMMUNITY; REVIEW;

ANTI-INFECTIVE AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIA; BENZOXAZINES; CELL WALL; CHEMICAL WARFARE AGENTS; FUNGI; GLUCOSINOLATES; HOST-PATHOGEN INTERACTIONS; INDOLES; ISOTHIOCYANATES; PLANT IMMUNITY; PLANTS; THIAZOLES;

EID: 84864515421     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2012.03.002     Document Type: Review

References (59)

1. Panstruga R., Parker J.E., Schulze-Lefert P. SnapShot: plant immune response pathways. Cell 2009, 136. 978-U976.
2. Dodds P.N., Rathjen J.P. Plant immunity: towards an integrated view of plant-pathogen interactions. Nature Reviews Genetics 2010, 11:539-548.
3. Bednarek P., Osbourn A. Plant-microbe interactions: chemical diversity in plant defense. Science 2009, 324:746-748.
4. Dixon R.A. Natural products and plant disease resistance. Nature 2001, 411:843-847.
5. Frey M., Chomet P., Glawischnig E., Stettner C., Grun S., Winklmair A., Eisenreich W., Bacher A., Meeley R.B., Briggs S.P., et al. Analysis of a chemical plant defense mechanism in grasses. Science 1997, 277:696-699.
6. Frey M., Schullehner K., Dick R., Fiesselmann A., Gierl A. Benzoxazinoid biosynthesis, a model for evolution of secondary metabolic pathways in plants. Phytochemistry 2009, 70:1645-1651.
7. Bednarek P., Pislewska-Bednarek M., Svatos A., Schneider B., Doubsky J., Mansurova M., Humphry M., Consonni C., Panstruga R., Sanchez-Vallet A., et al. A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 2009, 323:101-106.
8. Fan J., Crooks C., Creissen G., Hill L., Fairhurst S., Doerner P., Lamb C. Pseudomonas sax genes overcome aliphatic isothiocyanate-mediated non-host resistance in Arabidopsis. Science 2011, 331:1185-1188.
9. Thomma B.P.H.J., Nelissen I., Eggermont K., Broekaert W.F. Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. Plant Journal 1999, 19:163-171.
10. Djamei A., Schipper K., Rabe F., Ghosh A., Vincon V., Kahnt J., Osorio S., Tohge T., Fernie A.R., Feussner I., et al. Metabolic priming by a secreted fungal effector. Nature 2011, 478:395-398.
11. Zhou H., Lin J., Johnson A., Morgan Robyn L., Zhong W., Ma W. Pseudomonas syringae type III effector HopZ1 targets a host enzyme to suppress isoflavone biosynthesis and promote infection in soybean. Cell Host & Microbe 2011, 9:177-186.
12. Amborabé B.-E., Fleurat-Lessard P., Chollet J.-F., Roblin G. Antifungal effects of salicylic acid and other benzoic acid derivatives towards Eutypa lata: structure-activity relationship. Plant Physiology and Biochemistry 2002, 40:1051-1060.
13. Vlot A.C., Dempsey D.M.A., Klessig D.F. Salicylic acid, a multifaceted hormone to combat disease. Annual Review of Phytopathology 2009, 47:177-206.
14. Brown P.D., Tokuhisa J.G., Reichelt M., Gershenzon J. Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 2003, 62:471-481.
15. Sonderby I.E., Geu-Flores F., Halkier B.A. Biosynthesis of glucosinolates - gene discovery and beyond. Trends in Plant Science 2010, 15:283-290.
16. Barth C., Jander G. Arabidopsis myrosinases TGG1 and TGG2 have redundant function in glucosinolate breakdown and insect defense. Plant Journal 2006, 46:549-562.
17. Wittstock U., Burow M. Glucosinolate breakdown in Arabidopsis: mechanism, regulation and biological significance. The Arabidopsis Book 2010, e0134.
18. Brown K.K., Hampton M.B. Biological targets of isothiocyanates. Biochimica Et Biophysica Acta-General Subjects 2011, 1810:888-894.
19. Tierens K.F.M.J., Thomma B.P.H.J., Brouwer M., Schmidt J., Kistner K., Porzel A., Mauch-Mani B., Cammue B.P.A., Broekaert W.F. Study of the role of antimicrobial glucosinolate-derived isothiocyanates in resistance of Arabidopsis to microbial pathogens. Plant Physiology 2001, 125:1688-1699.
20. Sonderby I.E., Hansen B.G., Bjarnholt N., Ticconi C., Halkier B.A., Kliebenstein D.J. A systems biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates. PLoS ONE 2007, 2:e1322.
21. Zhao Z., Zhang W., Stanley B.A., Assmann S.M. Functional proteomics of Arabidopsis thaliana guard cells uncovers new stomatal signaling pathways. The Plant Cell 2008, 20:3210-3226.
22. Islam M.M., Tani C., Watanabe-Sugimoto M., Uraji M., Jahan M.S., Masuda C., Nakamura Y., Mori I.C., Murata Y. Myrosinases, TGG1 and TGG2, redundantly function in ABA and MeJA signaling in Arabidopsis guard cells. Plant and Cell Physiology 2009, 50:1171-1175.
23. Khokon M.A.R., Jahan M.S., Rahman T., Hossain M.A., Muroyama D., Minami I., Munemasa S., Mori I.C., Nakamura Y., Murata Y. Allyl isothiocyanate (AITC) induces stomatal closure in Arabidopsis. Plant, Cell & Environment 2011, 34:1900-1906.
24. Melotto M., Underwood W., Koczan J., Nomura K., He S.Y. Plant stomata function in innate immunity against bacterial invasion. Cell 2006, 126:969-980.
25. Freeman B.C., Beattie G.A. Bacterial growth restriction during host resistance to Pseudomonas syringae is associated with leaf water loss and localized cessation of vascular activity in Arabidopsis thaliana. Molecular Plant-Microbe Interactions 2009, 22:857-867.
26. +-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biology 2009, 7:1-16.
27. Zeng W., Melotto M., He S.Y. Plant stomata: a checkpoint of host immunity and pathogen virulence. Current Opinion in Biotechnology 2010, 21:599-603.
28. Jammes F., Yang X., Xiao S., Kwak J.M. Two Arabidopsis guard cell-preferential MAPK genes, MPK9 and MPK12, function in biotic stress response. Plant Signaling & Behavior 2011, 6:1875-1877.
29. Stotz H.U., Sawada Y., Shimada Y., Hirai M.Y., Sasaki E., Krischke M., Brown P.D., Saito K., Kamiya Y. Role of camalexin, indole glucosinolates, and side chain modification of glucosinolate-derived isothiocyanates in defense of Arabidopsis against Sclerotinia sclerotiorum. Plant Journal 2011, 67:81-93.
30. Guimarães R.L., Stotz H.U. Oxalate production by Sclerotinia sclerotiorum deregulates guard cells during infection. Plant Physiology 2004, 136:3703-3711.
31. Lipka V., Dittgen J., Bednarek P., Bhat R., Wiermer M., Stein M., Landtag J., Brandt W., Rosahl S., Scheel D., et al. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 2005, 310:1180-1183.
32. Bednarek P., Piślewska-Bednarek M., Ver Loren van Themaat E., Maddula R.K., Svatoš A., Schulze-Lefert P. Conservation and clade-specific diversification of pathogen-inducible tryptophan and indole glucosinolate metabolism in Arabidopsis thaliana relatives. New Phytologist 2011, 192:713-726.
33. Sanchez-Vallet A., Ramos B., Bednarek P., Lopez G., Pislewska-Bednarek M., Schulze-Lefert P., Molina A. Tryptophan-derived secondary metabolites in Arabidopsis thaliana confer non-host resistance to necrotrophic Plectosphaerella cucumerina fungi. Plant Journal 2010, 63:115-127.
34. Clay N.K., Adio A.M., Denoux C., Jander G., Ausubel F.M. Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 2009, 323:95-101.
35. Pfalz M., Mikkelsen M.D., Bednarek P., Olsen C.E., Halkier B.A., Kroymann J. Metabolic engineering in Nicotiana benthamiana reveals key enzyme functions in Arabidopsis indole glucosinolate modification. Plant Cell 2011, 23:716-729.
36. Pfalz M., Vogel H., Kroymann J. The gene controlling the indole glucosinolate modifier1 quantitative trait locus alters indole glucosinolate structures and aphid resistance in Arabidopsis. Plant Cell 2009, 21:985-999.
37. Consonni C., Bednarek P., Humphry M., Francocci F., Ferrari S., Harzen A., van Themaat E.V.L., Panstruga R. Tryptophan-derived metabolites are required for antifungal defense in the Arabidopsis mlo2 mutant. Plant Physiology 2010, 152:1544-1561.
38. Schlaeppi K., Abou-Mansour E., Buchala A., Mauch F. Disease resistance of Arabidopsis to Phytophthora brassicae is established by the sequential action of indole glucosinolates and camalexin. Plant Journal 2010, 62:840-851.
39. Hiruma K., Onozawa-Komori M., Takahashi F., Asakura M., Bednarek P., Okuno T., Schulze-Lefert P., Takano Y. Entry mode-dependent function of an indole glucosinolate pathway in Arabidopsis for nonhost resistance against anthracnose pathogens. Plant Cell 2010, 22:2429-2443.
40. Adie B.A.T., Perez-Perez J., Perez-Perez M.M., Godoy M., Sanchez-Serrano J.J., Schmelz E.A., Solano R. ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 2007, 19:1665-1681.
41. Maeda K., Houjyou Y., Komatsu T., Hori H., Kodaira T., Ishikawa A. AGB1 and PMR5 contribute to PEN2-mediated preinvasion resistance to Magnaporthe oryzae in Arabidopsis thaliana. Molecular Plant-Microbe Interactions 2009, 22:1331-1340.
42. Elliott C.E., Harjono, Howlett B.J. Mutation of a gene in the Fungus Leptosphaeria maculans allows increased frequency of penetration of stomatal apertures of Arabidopsis thaliana. Molecular Plant 2008, 1:471-481.
43. Jacobs S., Zechmann B., Molitor A., Trujillo M., Petutschnig E., Likpa V., Kogel K.H., Schafer P. Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica. Plant Physiology 2011, 156:726-740.
44. Stein M., Dittgen J., Sanchez-Rodriguez C., Hou B.H., Molina A., Schulze-Lefert P., Lipka V., Somerville S. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 2006, 18:731-746.
45. Luna E., Pastor V., Robert J., Flors V., Mauch-Mani B., Ton J. Callose deposition: a multifaceted plant defense response. Molecular Plant-Microbe Interactions 2010, 24:183-193.
46. Millet Y.A., Danna C.H., Clay N.K., Songnuan W., Simon M.D., Werck-Reichhart D., Ausubel F.M. Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. The Plant Cell 2010, 22:973-990.
47. Ahmad S., Veyrat N., Gordon-Weeks R., Zhang Y., Martin J., Smart L., Glauser G., Erb M., Flors V., Frey M., et al. Benzoxazinoid metabolites regulate innate immunity against aphids and fungi in maize. Plant Physiology 2011, 157:317-327.
48. Kim J.H., Lee B.W., Schroeder F.C., Jander G. Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid). The Plant Journal 2008, 54:1015-1026.
49. Humphry M., Bednarek P., Kemmerling B., Koh S., Stein M., Göbel U., Stüber K., Piślewska-Bednarek M., Loraine A., Schulze-Lefert P., et al. A regulon conserved in monocot and dicot plants defines a functional module in antifungal plant immunity. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:21896-21901.
50. Pedras M.S.C., Yaya E.E., Glawischnig E. The phytoalexins from cultivated and wild crucifers: chemistry and biology. Natural Product Reports 2011, 28:1381-1405.
51. Stefanato F.L., Abou-Mansour E., Buchala A., Kretschmer M., Mosbach A., Hahn M., Bochet C.G., Métraux J.-P., Schoonbeek H.-j. The ABC transporter BcatrB from Botrytis cinerea exports camalexin and is a virulence factor on Arabidopsis thaliana. The Plant Journal 2009, 58:499-510.
52. Bottcher C., Westphal L., Schmotz C., Prade E., Scheel D., Glawischnig E. The multifunctional enzyme CYP71B15 (PHYTOALEXIN DEFICIENT3) converts cysteine-indole-3-acetonitrile to camalexin in the indole-3-acetonitrile metabolic network of Arabidopsis thaliana. Plant Cell 2009, 21:1830-1845.
53. Møller B.L. Functional diversifications of cyanogenic glucosides. Current Opinion in Plant Biology 2010, 13:338-347.
54. McLusky S.R., Bennett M.H., Beale M.H., Lewis M.J., Gaskin P., Mansfield J.W. Cell wall alterations and localized accumulation of feruloyl-3'-methoxytyramine in onion epidermis at sites of attempted penetration by Botrytis allii are associated with actin polarisation, peroxidase activity and suppression of flavonoid biosynthesis. Plant Journal 1999, 17:523-534.
55. Forcat S., Bennett M., Grant M., Mansfield J.W. Rapid linkage of indole carboxylic acid to the plant cell wall identified as a component of basal defence in Arabidopsis against hrp mutant bacteria. Phytochemistry 2010, 71:870-876.
56. Tan J.W., Bednarek P., Liu H.K., Schneider B., Svatos A., Hahlbrock K. Universally occurring phenylpropanoid and species-specific indolic metabolites in infected and uninfected Arabidopsis thaliana roots and leaves. Phytochemistry 2004, 65:691-699.
57. Zhao Y.D., Hull A.K., Gupta N.R., Goss K.A., Alonso J., Ecker J.R., Normanly J., Chory J., Celenza J.L. Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes & Development 2002, 16:3100-3112.
58. Kliebenstein D.J., Rowe H.C., Denby K.J. Secondary metabolites influence Arabidopsis/Botrytis interactions: variation in host production and pathogen sensitivity. Plant Journal 2005, 44:25-36.
59. Bressan M., Roncato M.A., Bellvert F., Comte G., Haichar F.E., Achouak W., Berge O. Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots. ISME Journal 2009, 3:1243-1257.