13 Ethylene: Multi-Tasker in Plant–Attacker Interactions
Sjoerd Van der Ent
Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University, PO Box 800.56, Utrecht, TB, 3508 The Netherlands
Centre for BioSystems Genomics, PO Box 98, Wageningen, AB, 6700 The Netherlands
Search for more papers by this authorCorné M.J. Pieterse
Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University, PO Box 800.56, Utrecht, TB, 3508 The Netherlands
Centre for BioSystems Genomics, PO Box 98, Wageningen, AB, 6700 The Netherlands
Search for more papers by this authorSjoerd Van der Ent
Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University, PO Box 800.56, Utrecht, TB, 3508 The Netherlands
Centre for BioSystems Genomics, PO Box 98, Wageningen, AB, 6700 The Netherlands
Search for more papers by this authorCorné M.J. Pieterse
Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University, PO Box 800.56, Utrecht, TB, 3508 The Netherlands
Centre for BioSystems Genomics, PO Box 98, Wageningen, AB, 6700 The Netherlands
Search for more papers by this authorAbstract
In the past decades, the role of ethylene in the regulation of plant responses to biotic stress has been intensively studied. Analyses of plant genotypes that are impaired in ethylene biosynthesis, perception or signalling revealed an important role for ethylene in the primary response to pathogen attack. In addition, ethylene has been demonstrated to fulfil a key function in the control of systemic immune responses that are induced by beneficial micro-organisms. Although the importance of ethylene in the regulation of plant immune responses is evident, its role in stimulating disease resistance or susceptibility appears to depend greatly on the plant–attacker combination. Whereas in many studies ethylene was demonstrated to facilitate disease resistance or tolerance, in other studies ethylene was shown to support pathogen infection. Recent advances in defence-signalling research have revealed that ethylene plays an important role in modulating interactions between defence-signalling pathways that are regulated by either salicylic acid (SA) or jasmonic acid (JA). By functioning as a modulator of these important defence-regulatory pathways, ethylene may play a decisive positive or negative role in the final outcome of the immune response of a plant.
References
- Adie, B., Chico, J.M., Rubio-Somoza, I., et al. (2007) Modulation of plant defenses by ethylene. Journal of Plant Growth Regulation 26, 160–177.
- Ahn, I.-P., Lee, S.-W. and Suh, S.-C. (2007) Rhizobacteria-induced priming in Arabidopsis is dependent on ethylene, jasmonic acid, and NPR1. Molecular Plant-Microbe Interactions 20, 759–768.
- Arshad, M. and Frankenberger, W.T. (1992) Ethylene, Agricultural Sources and Applications. Kluwer Academic/Plenum, New York.
- Asselbergh, B., De Vleesschauwer, D. and Höfte, M. (2008) Global switches and fine-tuning - ABA modulates plant pathogen defense. Molecular Plant-Microbe Interactions 21, 709–719.
- Attaran, E., Zeier, T.E., Griebel, T., et al. (2009) Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. The Plant Cell 21, 954–971.
- Barry, C.S., Fox, E.A., Yen, H.C., et al. (2001) Analysis of the ethylene response in the epinastic mutant of tomato. Plant Physiology 127, 58–66.
- Beckers, G.J.M. and Spoel, S.H. (2006) Fine-tuning plant defence signalling: salicylate versus jasmonate. Plant Biology 8, 1–10.
- Beckers, G.J.M., Jaskiewicz, M., Liu, Y., et al. (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana . The Plant Cell 21, 944–953.
- Bent, A.F., Innes, R.W., Ecker, J.R., et al. (1992) Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens. Molecular Plant-Microbe Interactions 5, 372–378.
- Bent, A.F., Hoffman, T.K., Schmidt, J.S., et al. (2006) Disease- and performance-related traits of ethylene-insensitive soybean. Crop Science 46, 893–901.
- Berrocal-Lobo, M. and Molina, A. (2004) Ethylene response factor 1 mediates Arabidopsis resistance to the soilborne fungus Fusarium oxysporum . Molecular Plant-Microbe Interactions 17, 763–770.
- Berrocal-Lobo, M., Molina, A. and Solano, R. (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. The Plant Journal 29, 23–32.
- Bezemer, T.M. and Van Dam, N.M. (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends in Ecology and Evolution 20, 617–624.
- Block, A., Schmelz, E., O'Donnell, P.J., et al. (2005) Systemic acquired tolerance to virulent bacterial pathogens in tomato. Plant Physiology 138, 1481–1490.
- Bodenhausen, N. and Reymond, P. (2007) Signaling pathways controlling induced resistance to insect herbivores in Arabidopsis. Molecular Plant-Microbe Interactions 20, 1406–1420.
- Boller, T. (1991) Ethylene in pathogenesis and disease resistance. In: A.K. Mattoo and J.C. Suttle (eds) The Plant Hormone Ethylene. CRC Press, Boca Raton, pp. 293–314.
- Bostock, R.M. (1999) Signal conflicts and synergies in induced resistance to multiple attackers. Physiological and Molecular Plant Pathology 55, 99–109.
- Bostock, R.M. (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annual Review of Phytopathology 43, 545–580.
- Broekaert, W.F., Delaure, S.L., De Bolle, M.F.C., et al. (2006) The role of ethylene in host-pathogen interactions. Annual Review of Phytopathology 44, 393–416.
- Bruce, T.J.A., Matthes, M.C., Napier, J.A., et al. (2007) Stressful “memories” of plants: evidence and possible mechanisms. Plant Science 173, 603–608.
- Bruessow, F., Gouhier-Darimont, C., Buchala, A., et al. (2010) Insect eggs suppress plant defence against chewing herbivores. The Plant Journal 62, 876–885.
- Cartieaux, F., Contesto, C., Gallou, A., et al. (2008) Simultaneous interaction of Arabidopsis thaliana with Bradyrhizobium sp strain ORS278 and Pseudomonas syriugae pv. tomato DC3000 leads to complex transcriptome changes. Molecular Plant-Microbe Interactions 21, 244–259.
- Chagué, V., Elad, Y., Barakat, R., et al. (2002) Ethylene biosynthesis in Botrytis cinerea . FEMS Microbiology Ecology 40, 143–149.
- Chagué, V., Danit, L.V., Siewers, V., et al. (2006) Ethylene sensing and gene activation in Botrytis cinerea: a missing link in ethylene regulation of fungus-plant interactions? Molecular Plant-Microbe Interactions 19, 33–42.
- Chang, C., Kwok, S.F., Bleecker, A.B., et al. (1993) Arabidopsis ethylene-response gene Etr1 -- similarity of product to 2-component regulators. Science 262, 539–544.
- Chen, N., Goodwin, P.H. and Hsiang, T. (2003) The role of ethylene during the infection of Nicotiana tabacum by Colletotrichum destructivum . Journal of Experimental Botany 54, 2449–2456.
- Chen, X., Steed, A., Travella, S., et al. (2009) Fusarium graminearum exploits ethylene signalling to colonize dicotyledonous and monocotyledonous plants. New Phytologist 182, 975–983.
- Chisholm, S.T., Coaker, G., Day, B., et al. (2006) Host--microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803–814.
- Ciardi, J.A., Tieman, D.M., Lund, S.T., et al. (2000) Response to Xanthomonas campestris pv. vesicatoria in tomato involves regulation of ethylene receptor gene expression. Plant Physiology 123, 81–92.
- Conn, V.M., Walker, A.R. and Franco, C.M.M. (2008) Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana . Molecular Plant-Microbe Interactions 21, 208–218.
- Conrath, U., Beckers, G.J.M., Flors, V., et al. (2006) Priming: getting ready for battle. Molecular Plant-Microbe Interactions 19, 1062–1071.
- Cooper, W., Bouzayen, M., Hamilton, A., et al. (1998) Use of transgenic plants to study the role of ethylene and polygalacturonase during infection of tomato fruit by Colletotrichum gloeosporioides . Plant Pathology 47, 308–316.
- Cui, J., Bahrami, A.K., Pringle, E.G., et al. (2005) Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proceedings of the National Academy of Sciences of the United States of America 102, 1791–1796.
- Czechowski, T., Bari, R.P., Stitt, M., et al. (2004) Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. The Plant Journal 38, 366–379.
- De Vleesschauwer, D., Djavaheri, M., Bakker, P.A.H.M., et al. (2008) Pseudomonas fluorescens WCS374r-induced systemic resistance in rice against Magnaporthe oryzae is based on pseudobactin-mediated priming for a salicylic acid-repressible multifaceted defense response. Plant Physiology 148, 1996–2012.
- De Vos, M., Van Oosten, V.R., Jander, G., et al. (2007) Plants under attack: multiple interactions with insects. Plant Signaling & Behavior 2, 527–529.
- De Vos, M., Van Zaanen, W., Koornneef, A., et al. (2006) Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiology 142, 352–363.
- De Vos, M., Van Oosten, V.R., Van Poecke, R.M.P., et al. (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Molecular Plant-Microbe Interactions 18, 923–937.
- Delaney, T.P., Uknes, S., Vernooij, B., et al. (1994) A central role of salicylic acid in plant disease resistance. Science 266, 1247–1250.
- Diaz, J., Ten Have, A. and Van Kan, J.A.L. (2002) The role of ethylene and wound signaling in resistance of tomato to Botrytis cinerea . Plant Physiology 129, 1341–1351.
- Dicke, M., Van Loon, J.J.A. and Soler, R. (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nature Chemical Biology 5, 317–324.
- Dong, X. (1998) SA, JA, ethylene, and disease resistance in plants. Current Opinion in Plant Biology 1, 316–323.
- Dong, X. (2004) NPR1, all things considered. Current Opinion in Plant Biology 7, 547–552.
- Duff, B., Schouten, A. and Raaijmakers, J.M. (2003) Pathogen self-defense: mechanisms to counteract microbial antagonism. Annual Review of Phytopathology 41, 501–538.
- Durrant, W.E. and Dong, X. (2004) Systemic acquired resistance. Annual Review of Phytopathology 42, 185–209.
- Ellis, C. and Turner, J.G. (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. The Plant Cell 13, 1025–1033.
- Ellis, C., Karafyllidis, L. and Turner, J.G. (2002a) Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae . Molecular Plant-Microbe Interactions 15, 1025–1030.
- Ellis, C., Karafyllidis, I., Wasternack, C., et al. (2002b) The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. The Plant Cell 14, 1557–1566.
- Felton, G.W. and Korth, K.L. (2000) Trade-offs between pathogen and herbivore resistance. Current Opinion in Plant Biology 3, 309–314.
- Frost, C.J., Mescher, M.C., Carlson, J.E., et al. (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiology 146, 818–824.
- Fujino, D.W., Burger, D.W., Yang, S.F., et al. (1988) Characterization of an ethylene overproducing mutant of tomato (Lycopersicon esculentum Mill. cultivar VFN8). Plant Physiology 88, 774–779.
- Gaffney, T., Friedrich, L., Vernooij, B., et al. (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261, 754–756.
- Geraats, B.P.J., Bakker, P.A.H.M. and Van Loon, L.C. (2002) Ethylene insensitivity impairs resistance to soilborne pathogens in tobacco and Arabidopsis thaliana . Molecular Plant-Microbe Interactions 15, 1078–1085.
- Geraats, B.P.J., Bakker, P.A.H.M., Lawrence, C.B., et al. (2003) Ethylene-insensitive tobacco shows differentially altered susceptibility to different pathogens. Phytopathology 93, 813–821.
- Glazebrook, J. (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43, 205–227.
- Glazebrook, J., Chen, W., Estes, B., et al. (2003) Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. The Plant Journal 34, 217–228.
- Grant, M. and Lamb, C. (2006) Systemic immunity. Current Opinion in Plant Biology 9, 414–420.
- Haines, N.M., Shiel, P.J., Fellman, J.K., et al. (2003) Abnormalities in growth, development and physiological responses to biotic and abiotic stress in potato (Solanum tuberosum) transformed with Arabidopsis ETR1 . Journal of Agricultural Science 141, 333–347.
- Hammerschmidt, R. (2009) Systemic acquired resistance. In: L.C. Van Loon (ed.) Plant Innate Immunity. Academic Press Ltd-Elsevier Science Ltd, London, pp. 173–222.
- Hase, S., Van Pelt, J.A., Van Loon, L.C., et al. (2003) Colonization of Arabidopsis roots by Pseudomonas fluorescens primes the plant to produce higher levels of ethylene upon pathogen infection. Physiological and Molecular Plant Pathology 62, 219–226.
- Hase, S., Takahashi, S., Takenaka, S., et al. (2008) Involvement of jasmonic acid signalling in bacterial wilt disease resistance induced by biocontrol agent Pythium oligandrum in tomato. Plant Pathology 57, 870–876.
- Heil, M. and Baldwin, I.T. (2002) Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends in Plant Science 7, 61–67.
- Hirsch, J., Deslandes, L., Feng, D.X., et al. (2002) Delayed symptom development in ein2–1, an Arabidopsis ethylene-insensitive mutant, in response to bacterial wilt caused by Ralstonia solanacearum . Phytopathology 92, 1142–1148.
- Hoffman, T., Schmidt, J.S., Zheng, X., et al. (1999) Isolation of ethylene-insensitive soybean mutants that are altered in pathogen susceptibility and gene-for-gene disease resistance. Plant Physiology 119, 935–949.
- Hossain, M.M., Sultana, F., Kubota, M., et al. (2008) Differential inducible defense mechanisms against bacterial speck pathogen in Arabidopsis thaliana by plant-growth-promoting-fungus Penicillium sp. GP16–2 and its cell free filtrate. Plant and Soil 304, 227–239.
- Howe, G.A. and Jander, G. (2008) Plant immunity to insect herbivores. Annual Review of Plant Biology 59, 41–66.
- Huang, Y., Li, H., Hutchison, C.E., et al. (2003) Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis . The Plant Journal 33, 221–233.
- Iavicoli, A., Boutet, E., Buchala, A., et al. (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Molecular Plant-Microbe Interactions 16, 851–858.
- Johansson, A., Staal, J. and Dixelius, C. (2006) Early responses in the Arabidopsis-Verticillium longisporum pathosystem are dependent on NDR1, JA- and ET-associated signals via cytosolic NPR1 and RFO1. Molecular Plant-Microbe Interactions 19, 958–969.
- Jones, J.D.G. and Dangl, J.L. (2006) The plant immune system. Nature 444, 323–329.
- Kachroo, P., Yoshioka, K., Shah, J., et al. (2000) Resistance to turnip crinkle virus in Arabidopsis is regulated by two host genes and is salicylic acid dependent but NPR1, ethylene, and jasmonate independent. The Plant Cell 12, 677–690.
- Kazan, K. and Manners, J.M. (2008) Jasmonate signaling: toward an integrated view. Plant Physiology 146, 1459–1468.
- Kloepper, J.W., Ryu, C.-M. and Zhang, S.A. (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94, 1259–1266.
- Kloepper, J.W., Leong, J., Teintze, M., et al. (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286, 885–886.
- Knoester, M., Pieterse, C.M.J., Bol, J.F., et al. (1999) Systemic resistance in Arabidopsis induced by rhizobacteria requires ethylene-dependent signaling at the site of application. Molecular Plant-Microbe Interactions 12, 720–727.
- Knoester, M., Van Loon, L.C., Van den Heuvel, J., et al. (1998) Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi. Proceedings of the National Academy of Sciences of the United States of America 95, 1933–1937.
- Koornneef, A. and Pieterse, C.M.J. (2008) Cross-talk in defense signaling. Plant Physiology 146, 839–844.
- Koornneef, A., Verhage, A., Leon-Reyes, A., et al. (2008a) Towards a reporter system to identify regulators of cross-talk between salicylate and jasmonate signaling pathways in Arabidopsis. Plant Signaling & Behavior 3, 543–546.
- Koornneef, A., Leon-Reyes, A., Ritsema, T., et al. (2008b) Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiology 147, 1358–1368.
- Korolev, N., David, D.R. and Elad, Y. (2008) The role of phytohormones in basal resistance and Trichoderma-induced systemic resistance to Botrytis cinerea in Arabidopsis thaliana . Biocontrol 53, 667–683.
- Kunkel, B.N. and Brooks, D.M. (2002) Cross talk between signaling pathways in pathogen defense. Current Opinion in Plant Biology 5, 325–331.
- Lanahan, M.B., Yen, H.C., Giovannoni, J.J., et al. (1994) The Never Ripe mutation blocks ethylene perception in tomato. The Plant Cell 6, 521–530.
- Lawton, K., Weymann, K., Friedrich, L., et al. (1995) Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Molecular Plant-Microbe Interactions 8, 863–870.
- Lawton, K.A., Potter, S.L., Uknes, S., et al. (1994) Acquired resistance signal transduction in Arabidopsis is ethylene independent. The Plant Cell 6, 581–588.
- Léon-Kloosterziel, K.M., Verhagen, B.W.M., Keurentjes, J.J.B., et al. (2005) Colonization of the Arabidopsis rhizosphere by fluorescent Pseudomonas spp. activates a root-specific, ethylene-responsive PR-5 gene in the vascular bundle. Plant Molecular Biology 57, 731–748.
- Leon-Reyes, A., Du, Y., Koornneef, A., et al. (2010) Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Molecular Plant-Microbe Interactions 23, 187–197.
- Leon-Reyes, A., Spoel, S.H., De Lange, E.S., et al. (2009) Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiology 149, 1797–1809.
- Lin, Z.F., Alexander, L., Hackett, R., et al. (2008) LeCTR2, a CTR1-like protein kinase from tomato, plays a role in ethylene signalling, development and defence. The Plant Journal 54, 1083–1093.
- Loake, G. and Grant, M. (2007) Salicylic acid in plant defence--the players and protagonists. Current Opinion in Plant Biology 10, 466–472.
- Lorenzo, O. and Solano, R. (2005) Molecular players regulating the jasmonate signalling network. Current Opinion in Plant Biology 8, 532–540.
- Lorenzo, O., Piqueras, R., Sánchez-Serrano, J.J., et al. (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. The Plant Cell 15, 165–178.
- Lund, S.T., Stall, R.E. and Klee, H.J. (1998) Ethylene regulates the susceptible response to pathogen infection in tomato. The Plant Cell 10, 371–382.
- Mauch-Mani, B. and Mauch, F. (2005) The role of abscisic acid in plant--pathogen interactions. Current Opinion in Plant Biology 8, 409–414.
- McConn, J., Creelman, R.A., Bell, E., et al. (1997) Jasmonate is essential for insect defense in Arabidopsis. Proceedings of the National Academy of Science of the United States of America 94, 5473–5477.
- Mur, L.A.J., Kenton, P., Atzorn, R., et al. (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiology 140, 249–262.
- Nakashita, H., Yasuda, M., Nitta, T., et al. (2003) Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. The Plant Journal 33, 887–898.
- Navarro, L., Bari, R., Achard, P., et al. (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Current Biology 18, 650–655.
- Navarro, L., Dunoyer, P., Jay, F., et al. (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436–439.
- Nawrath, C. and Métraux, J.-P. (1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. The Plant Cell 11, 1393–1404.
- Norman-Setterblad, C., Vidal, S. and Palva, T.E. (2000) Interacting signal pathways control defense gene expression in Arabidopsis in response to cell wall-degrading enzymes from Erwinia carotovora. Molecular Plant-Microbe Interactions 13, 430–438.
- O'Donnell, P.J., Schmelz, E.A., Moussatche, P., et al. (2003) Susceptible to intolerance – a range of hormonal actions in a susceptible Arabidopsis pathogen response. The Plant Journal 33, 245–257.
- Ortuño, A., Nemsa, I., Alvarez, N., et al. (2008) Correlation of ethylene synthesis in Citrus fruits and their susceptibility to Alternaria alternata pv. citri . Physiological and Molecular Plant Pathology 72, 162–166.
- Osbourn, A. (1996) Saponins and plant defence – a soap story. Trends in Plant Science 1, 4–9.
- Penmetsa, R.V., Uribe, P., Anderson, J., et al. (2008) The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. The Plant Journal 55, 580–595.
- Penninckx, I.A.M.A., Thomma, B.P.H.J., Buchala, A., et al. (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. The Plant Cell 10, 2103–2113.
- Pieterse, C.M.J. and Van Loon, L.C. (2004) NPR1: the spider in the web of induced resistance signaling pathways. Current Opinion in Plant Biology 7, 456–464.
- Pieterse, C.M.J. and Dicke, M. (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends in Plant Science 12, 564–569.
- Pieterse, C.M.J., Leon-Reyes, A., Van der Ent, S., et al. (2009) Networking by small-molecule hormones in plant immunity. Nature Chemical Biology 5, 308–316.
- Pieterse, C.M.J., Van Wees, S.C.M., Hoffland, E., et al. (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. The Plant Cell 8, 1225–1237.
- Pieterse, C.M.J., Van Wees, S.C.M., Ton, J., et al. (2002) Signalling in rhizobacteria--induced systemic resistance in Arabidopsis thaliana . Plant Biology 4, 535–544.
- Pieterse, C.M.J., Van Wees, S.C.M., Van Pelt, J.A., et al. (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. The Plant Cell 10, 1571–1580.
- Pieterse, C.M.J., Van Pelt, J.A., Ton, J., et al. (2000) Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis requires sensitivity to jasmonate and ethylene but is not accompanied by an increase in their production. Physiological and Molecular Plant Pathology 57, 123–134.
- Poelman, E.H., Broekgaarden, C., Van Loon, J.J.A., et al. (2008) Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Molecular Ecology 17, 3352–3365.
- Pozo, M.J. and Azcon-Aguilar, C. (2007) Unraveling mycorrhiza-induced resistance. Current Opinion in Plant Biology 10, 393–398.
- Pozo, M.J., Van der Ent, S., Van Loon, L.C., et al. (2008) Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria-induced systemic resistance in Arabidopsis thaliana . New Phytologist 180, 511–523.
- Pré, M., Atallah, M., Champion, A., et al. (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiology 147, 1347–1357.
- Raaijmakers, J.M. and Weller, D.M. (1998) Natural plant protection by 2,4-diacetylphloroglucinol-producing Pseudomonas spp. in take-all decline soils. Molecular Plant-Microbe Interactions 11, 144–152.
- Reymond, P. and Farmer, E.E. (1998) Jasmonate and salicylate as global signals for defense gene expression. Current Opinion in Plant Biology 1, 404–411.
- Robert-Seilaniantz, A., Navarro, L., Bari, R., et al. (2007) Pathological hormone imbalances. Current Opion in Plant Biology 10, 372–379.
- Robison, M.M., Shah, S., Tamot, B., et al. (2001) Reduced symptoms of Verticillium wilt in transgenic tomato expressing a bacterial ACC deaminase. Molecular Plant Pathology 2, 135–145.
- Rojo, E., Solano, R. and Sanchez-Serrano, J.J. (2003) Interactions between signaling compounds involved in plant defense. Journal of Plant Growth Regulation 22, 82–98.
- Ryu, C.-M., Murphy, J.F., Mysore, K.S., et al. (2004) Plant growth-promoting rhizobacteria systemically protect Arabidopsis thaliana against Cucumber mosaic virus by a salicylic acid and NPR1-independent and jasmonic acid-dependent signaling pathway. The Plant Journal 39, 381–392.
- Schenk, P.M., Kazan, K., Wilson, I., et al. (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proceedings of the National Academy of Sciences of the United States of America 97, 11655–11660.
- Schippers, B., Bakker, A.W. and Bakker, P.A.H.M. (1987) Interactions of deleterious and beneficial rhizosphere micoorganisms and the effect of cropping practices. Annual Review of Phytopathology 115, 339–358.
- Segarra, G., Van der Ent, S., Trillas, I., et al. (2009) MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biology 11, 90–96.
- Seo, H.S., Song, J.T., Cheong, J.-J., et al. (2001) Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proceedings of the National Acacemy of Sciences of the United States of America 98, 4788–4793.
- Shan, L.B., He, P., Li, J.M., et al. (2008) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host & Microbe 4, 17–27.
- Shoresh, M., Yedidia, I. and Chet, I. (2005) Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 95, 76–84.
- Siemens, J., Keller, I., Sarx, J., et al. (2006) Transcriptome analysis of Arabidopsis clubroots indicate a key role for cytokinins in disease development. Molecular Plant-Microbe Interactions 19, 480–494.
- Spoel, S.H. and Dong, X. (2008) Making sense of hormone crosstalk during plant immune responses. Cell Host & Microbe 3, 348–351.
- Spoel, S.H., Johnson, J.S. and Dong, X. (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proceedings of the National Academy of Sciences of the United States of America 104, 18842–18847.
- Spoel, S.H., Koornneef, A., Claessens, S.M.C., et al. (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. The Plant Cell 15, 760–770.
- Staswick, P.E., Yuen, G.Y. and Lehman, C.C. (1998) Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare . The Plant Journal 15, 747–754.
- Stein, E., Molitor, A., Kogel, K.H., et al. (2008) Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires fasmonic acid signaling and the cytoplasmic function of NPR1. Plant and Cell Physiology 49, 1747–1751.
- Stout, M.J., Thaler, J.S. and Thomma, B.P.H.J. (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annual Review of Entomology 51, 663–689.
- Thaler, J.S., Owen, B. and Higgins, V.J. (2004) The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiology 135, 530–538.
- Thaler, J.S., Karban, R., Ullman, D.E., et al. (2002) Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites. Oecologia 131, 227–235.
- Thomma, B.P.H.J., Eggermont, K., Tierens, K.F.M., et al. (1999) Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea . Plant Physiology 121, 1093–1102.
- Thomma, B.P.H.J., Penninckx, I.A.M.A., Broekaert, W.F., et al. (2001) The complexity of disease signaling in Arabidopsis . Current Opinion in Immunology 13, 63–68.
- Thomma, B.P.H.J., Eggermont, K., Penninckx, I.A.M.A., et al. (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proceedings of the National Academy of Sciences of the United States of America 95, 15107–15111.
- Tierens, K.F.M., Thomma, B.P.H.J., Brouwer, M., et al. (2001) Study of the role of antimicrobial glucosinolate-derived isothiocyanates in resistance of Arabidopsis to microbial pathogens. Plant Physiology 125, 1688–1699.
- Tjamos, S.E., Flemetakis, E., Paplomatas, E.J., et al. (2005) Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Molecular Plant-Microbe Interactions 18, 555–561.
- Ton, J., Pieterse, C.M.J. and Van Loon, L.C. (1999) Identification of a locus in Arabidopsis controlling both the expression of rhizobacteria-mediated induced systemic resistance (ISR) and basal resistance against Pseudomonas syringae pv. tomato . Molecular Plant-Microbe Interactions 12, 911–918.
- Ton, J., Flors, V. and Mauch-Mani, B. (2009) The multifaceted role of ABA in disease resistance. Trends in Plant Science 14, 310–317.
- Ton, J., Van Pelt, J.A., Van Loon, L.C., et al. (2002a) The Arabidopsis ISR1 locus is required for rhizobacteria-mediated induced systemic resistance against different pathogens. Plant Biology 4, 224–227.
- Ton, J., Van Pelt, J.A., Van Loon, L.C., et al. (2002b) Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis . Molecular Plant-Microbe Interactions 15, 27–34.
- Ton, J., Davison, S., Van Wees, S.C.M., et al. (2001) The Arabidopsis ISR1 locus controlling rhizobacteria-mediated induced systemic resistance is involved in ethylene signaling. Plant Physiology 125, 652–661.
- Ton, J., De Vos, M., Robben, C., et al. (2002c) Characterization of Arabidopsis enhanced disease susceptibility mutants that are affected in systemically induced resistance. Plant Journal 29, 11–21.
- Van der Ent, S., Van Wees, S.C.M. and Pieterse, C.M.J. (2009a) Jasmonate signals in plant interactions with beneficial microbes. Phytochemistry 70, 1581–1588.
- Van der Ent, S., Van Hulten, M.H.A., Pozo, M.J., et al. (2009b) Priming of plant innate immunity by rhizobacteria and ß-aminobutyric acid: differences and similarities in regulation. New Phytologist 183, 419–431.
- Van der Ent, S., Verhagen, B.W.M., Van Doorn, R., et al. (2008) MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiology 146, 1293–1304.
- Van der Putten, W.H., Vet, L.E.M., Harvey, J.A., et al. (2001) Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends in Ecology and Evolution 16, 547–554.
- Van Hulten, M., Pelser, M., Van Loon, L.C., et al. (2006) Costs and benefits of priming for defense in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 103, 5602–5607.
-
Van Loon, L.C.
(2000)
Systemic induced resistance. In:
A.J. Slusarenko,
R.S.S. Fraser and
L.C. Van Loon (eds)
Mechanisms of Resistance to Plant Diseases.
Kluwer Academic,
Dordrecht, pp.
521–574.
10.1007/978-94-011-3937-3_13 Google Scholar
-
Van Loon, L.C. and
Bakker, P.A.H.M.
(2003)
Signalling in rhizobacteria--plant interactions. In:
J. De Kroon and
E. J. W. Visser (eds)
Root Ecology.
Springer-Verlag,
Berlin Heidelberg, pp.
287–330.
10.1007/978-3-662-09784-7_12 Google Scholar
- Van Loon, L.C. and Bakker, P.A.H.M. (2006) Induced systemic resistance as a mechanism of disease suppression by rhizobacteria. In: Z.A. Siddiqui (ed.) PGPR: Biocontrol and Biofertilization. Springer, Dordrecht, pp. 39–66.
- Van Loon, L.C., Bakker, P.A.H.M. and Pieterse, C.M.J. (1998) Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology 36, 453–483.
- Van Loon, L.C., Geraats, B.P.J. and Linthorst, H.J.M. (2006a) Ethylene as a modulator of disease resistance in plants. Trends in Plant Science 11, 184–191.
- Van Loon, L.C., Rep, M. and Pieterse, C.M.J. (2006b) Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology 44, 135–162.
- Van Oosten, V.R., Bodenhausen, N., Reymond, P., et al. (2008) Differential effectiveness of microbially induced resistance against herbivorous insects in Arabidopsis. Molecular Plant-Microbe Interactions 21, 919–930.
- Van Peer, R., Niemann, G.J. and Schippers, B. (1991) Induced resistance and phytoalexin accumulation in biological control of fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 81, 728–734.
- Van Wees, S.C.M., Van der Ent, S. and Pieterse, C.M.J. (2008) Plant immune responses triggered by beneficial microbes. Current Opinion in Plant Biology 11, 443–448.
- Van Wees, S.C.M., Luijendijk, M., Smoorenburg, I., et al. (1999) Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonate-inducible gene Atvsp upon challenge. Plant Molecular Biology 41, 537–549.
- Van Wees, S.C.M., De Swart, E.A.M., Van Pelt, J.A., et al. (2000) Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana . Proceedings of the National Academy of Sciences of the United States of America 97, 8711–8716.
- Van Wees, S.C.M., Pieterse, C.M.J., Trijssenaar, A., et al. (1997) Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Molecular Plant-Microbe Interactions 10, 716–724.
- Verberne, M.C., Hoekstra, J., Bol, J.F., et al. (2003) Signaling of systemic acquired resistance in tobacco depends on ethylene perception. The Plant Journal 35, 27–32.
- Verhage, A., van Wees, S.C.M. and Pieterse, C.M.J. (2010) Plant immunity: it's the hormones talking, but what do they say? Plant Physiology 154, 536–540.
- Verhagen, B.W.M., Glazebrook, J., Zhu, T., et al. (2004) The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis . Molecular Plant-Microbe Interactions 17, 895–908.
- Veronese, P., Ruiz, M.T., Coca, M.A., et al. (2003) In defense against pathogens. Both plant sentinels and foot soldiers need to know the enemy. Plant Physiology 131, 1580–1590.
- Vijayan, P., Shockey, J., Lévesque, C.A., et al. (1998) A role for jasmonate in pathogen defense of Arabidopsis . Proceedings of the National Academy of Sciences of the United States of America 95, 7209–7214.
- Vlot, A.C., Klessig, D.F. and Park, S.-W. (2008) Systemic acquired resistance: the elusive signal(s). Current Opinion in Plant Biology 11, 436–442.
- Vlot, A.C., Dempsey, D.A. and Klessig, D.F. (2009) Salicylic acid, a multifaceted hormone to combat disease. Annual Review of Phytopathology 47, 177–206.
- Von Dahl, C.C. and Baldwin, I.T. (2007) Deciphering the role of ethylene in plant--herbivore interactions. Journal of Plant Growth Regulation 26, 201–209.
- Walker, T.S., Bais, H.P., Halligan, K.M., et al. (2003) Metabolic profiling of root exudates of Arabidopsis thaliana . Journal of Agricultural and Food Chemistry 51, 2548–2554.
- Waller, F., Achatz, B., Baltruschat, H., et al. (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proceedings of the National Academy of Sciences of the United States of America 102, 13386–13391.
- Walling, L.L. (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiology 146, 859–866.
- Walters, D. and Heil, M. (2007) Costs and trade-offs associated with induced resistance. Physiological and Molecular Plant Pathology 71, 3–17.
- Walters, D.R. (2009) Are plants in the field already induced? Implications for practical disease control. Crop Protection 28, 459–465.
- Walters, D.R. and Boyle, C. (2005) Induced resistance and allocation costs: what is the impact of pathogen challenge? Physiological and Molecular Plant Pathology 66, 40–44.
- Walters, D.R. and McRoberts, N. (2006) Plants and biotrophs: a pivotal role for cytokinins? Trends in Plant Science 11, 581–586.
- Wang, D., Pajerowska-Mukhtar, K., Hendrickson Culler, A., et al. (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Current Biology 17, 1784–1790.
- Wang, K.L.C., Yoshida, H., Lurin, C., et al. (2004) Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 428, 945–950.
- Wei, G., Kloepper, J.W. and Tuzun, S. (1991) Induction of systemic resistance of cucumber to Colletrotichum orbiculare by select strains of plant-growth promoting rhizobacteria. Phytopathology 81, 1508–1512.
- Weller, D.M., Raaijmakers, J.M., McSpadden Gardener, B.B., et al. (2002) Microbial populations responsible for specific soil suppressiveness to pathogens. Annual Review of Phytopathology 40, 309–348.
- Wildermuth, M.C., Dewdney, J., Wu, G., et al. (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414, 562–565.
- Wilkinson, J.Q., Lanahan, M.B., Yen, H.C., et al. (1995) An ethylene-inducible component of signal-transduction encoded by Never-Ripe . Science 270, 1807–1809.
- Wilkinson, J.Q., Lanahan, M.B., Clark, D.G., et al. (1997) A dominant mutant receptor from Arabidopsis confers ethylene insensitivity in heterologous plants. Nature Biotechnology 15, 444–447.
- Wrather, J.A. and Koenning, S.R. (2006) Estimates of disease effects on soybean yields in the United States 2003 to 2005. Journal of Nematology 38, 173–180.
- Wubben, M.J.E., Su, H., Rodermel, S.R., et al. (2001) Susceptibility to the sugar beet cyst nematode is modulated by ethylene signal transduction in Arabidopsis thaliana . Molecular Plant-Microbe Interactions 14, 1206–1212.
- Xu, X., Chen, C., Fan, B., et al. (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. The Plant Cell 18, 1310–1326.
- Yan, Z., Reddy, M.S., Ryu, C.-M., et al. (2002) Induced systemic protection against tomato late blight elicited by plant growth-promoting rhizobacteria. Phytopathology 92, 1329–1333.
- Yuan, Y., Zhong, S., Li, Q., et al. (2007) Functional analysis of rice NPR1-like genes reveals that OsNPR1 /NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnology Journal 5, 313–324.
- Zhou, N., Tootle, T.L., Tsui, F., et al. (1998) PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. The Plant Cell 10, 1021–1030.
Citing Literature
Browse other articles of this reference work: