SYSTEMIC ACQUIRED RESISTANCE
Abstract
▪ Abstract Systemic acquired resistance (SAR) is a mechanism of induced defense that confers long-lasting protection against a broad spectrum of microorganisms. SAR requires the signal molecule salicylic acid (SA) and is associated with accumulation of pathogenesis-related proteins, which are thought to contribute to resistance. Much progress has been made recently in elucidating the mechanism of SAR. Using the model plant Arabidopsis, it was discovered that the isochorismate pathway is the major source of SA during SAR. In response to SA, the positive regulator protein NPR1 moves to the nucleus where it interacts with TGA transcription factors to induce defense gene expression, thus activating SAR. Exciting new data suggest that the mobile signal for SAR might be a lipid molecule. We discuss the molecular and genetic data that have contributed to our understanding of SAR and present a model describing the sequence of events leading from initial infection to the induction of defense genes.
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Plant infection with many microbes can often lead to activation of the systemic-acquired resistant pathway, which decreases susceptibility to insect herbivores.
“Plant infection with many microbes can often lead to activation of the systemic-acquired resistant pathway (13) which, in turn, decreases susceptibility to insect herbivores (39).”
Many tripartite interactions report a positive effect, where a challenging microorganism alters the plant to become more resistant to herbivory.
“Many tripartite interactions also report a positive effect, where a challenging microorganism alters the plant to become more resistant to herbivory.”
Cites
MYB transcription factors in Arabidopsis
Dubos, C., Stracke, R., Erich Grotewold, A., Weißhaar, B., Martin, C. R., & Lepiniec, L. (2010) · Trends in Plant Science · doi:10.1016/j.tplants.2010.06.005 · Cited by 4,885 · see citing works
SYSTEMIC RESISTANCE INDUCED BY RHIZOSPHERE BACTERIA
van Loon, L. C., Bakker, P. A. H. M., & Pieterse, C. M. J. (1998) · Annual Review of Phytopathology · doi:10.1146/annurev.phyto.36.1.453 · Cited by 2,366 · see citing works
Isochorismate synthase is required to synthesize salicylic acid for plant defence
Wildermuth, M. C., Dewdney, J., Wu, G., & Ausubel, F. M. (2001) · Nature · doi:10.1038/35107108 · Cited by 2,333 · see citing works
Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H., & Hunt, D. M. (1996) · The Plant Cell · doi:10.1105/tpc.8.10.1809 · Cited by 2,060 · see citing works
van Loon, L. C., & van Strien, E. A. (1999) · Physiological and Molecular Plant Pathology · doi:10.1006/pmpp.1999.0213 · Cited by 1,943 · see citing works
bZIP transcription factors in Arabidopsis
Jakoby, M. J., Weißhaar, B., Dröge‐Laser, W., Vicente‐Carbajosa, J., Tiedemann, J., Kroj, T., & Parcy, F. (2002) · Trends in Plant Science · doi:10.1016/s1360-1385(01)02223-3 · Cited by 1,862 · see citing works
Requirement of Salicylic Acid for the Induction of Systemic Acquired Resistance
Gaffney, T. D., Friedrich, L., Vernooij, B., Negrotto, D. V., Nye, G., Uknes, S. J., Ward, E. R., Keßmann, H., & Ryals, J. A. (1993) · Science · doi:10.1126/science.261.5122.754 · Cited by 1,855 · see citing works
A Central Role of Salicylic Acid in Plant Disease Resistance
Delaney, T. P., Uknes, S. J., Vernooij, B., Friedrich, L., Weymann, K. B., Negrotto, D. V., Gaffney, T. D., Gut-Rella, M., Keßmann, H., Ward, E. R., et al. (1994) · Science · doi:10.1126/science.266.5188.1247 · Cited by 1,754 · see citing works
Resistance gene-dependent plant defense responses.
Hammond-Kosack, K. E., & Jones, J. D. G. (1996) · The Plant Cell · doi:10.1105/tpc.8.10.1773 · Cited by 1,703 · see citing works
Inducers of Plant Systemic Acquired Resistance Regulate NPR1 Function through Redox Changes
Mou, Z., Fan, W., & Dong, X. (2003) · Cell · doi:10.1016/s0092-8674(03)00429-x · Cited by 1,588 · see citing works
Self-citationCao, H., Glazebrook, J., Clarke, J. D., Volko, S. M., & Dong, X. (1997) · Cell · doi:10.1016/s0092-8674(00)81858-9 · Cited by 1,572 · see citing works
Self-citationCao, H., Bowling, S. A., Gordon, A., & Dong, X. (1994) · The Plant Cell · doi:10.1105/tpc.6.11.1583 · Cited by 1,495 · see citing works
Self-citationCross talk between signaling pathways in pathogen defense
Kunkel, B. N., & Brooks, D. M. (2002) · Current Opinion in Plant Biology · doi:10.1016/s1369-5266(02)00275-3 · Cited by 1,455 · see citing works
Sticher, L., Mauch‐Mani, B., & Métraux, A. J. (1997) · Annual Review of Phytopathology · doi:10.1146/annurev.phyto.35.1.235 · Cited by 1,436 · see citing works
Salicylic Acid: A Likely Endogenous Signal in the Resistance Response of Tobacco to Viral Infection
Malamy, J. E., Carr, J. P., Klessig, D. F., & Raskin, I. (1990) · Science · doi:10.1126/science.250.4983.1002 · Cited by 1,371 · see citing works
Coordinated plant defense responses in Arabidopsis revealed by microarray analysis
Schenk, P. M., Kazan, K., Wilson, I. W., Anderson, J. P., Richmond, T., Somerville, S. C., & Manners, J. M. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.21.11655 · Cited by 1,370 · see citing works
Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance.
Ward, E. R., Uknes, S. J., Williams, S. C., Dincher, S. S., Wiederhold, D. L., Alexander, D. C., Goy, P. A., Métraux, J., & Ryals, J. A. (1991) · The Plant Cell · doi:10.1105/tpc.3.10.1085 · Cited by 1,274 · see citing works
Spoel, S. H., Koornneef, A., Claessens, S. M. C., Korzelius, J., van Pelt, J. A., Mueller, M. J., Buchala, A. J., Métraux, J., Brown, R., Kazan, K., et al. (2003) · The Plant Cell · doi:10.1105/tpc.009159 · Cited by 1,219 · see citing works
Self-citationA Novel Signaling Pathway Controlling Induced Systemic Resistance in Arabidopsis
Pieterse, C. M. J., Wees, S. C. M. V., van Pelt, J. A., Knoester, M., Laan, R., Gerrits, H., Weisbeek, P. J., & van Loon, L. C. (1998) · The Plant Cell · doi:10.1105/tpc.10.9.1571 · Cited by 1,207 · see citing works
Active Oxygen Species in the Induction of Plant Systemic Acquired Resistance by Salicylic Acid
Chen, Z., Silva, H., & Klessig, D. F. (1993) · Science · doi:10.1126/science.8266079 · Cited by 1,184 · see citing works
Álvarez, M. E., Pennell, R. I., Meijer, P., Ishikawa, A., Dixon, R. A., & Lamb, C. (1998) · Cell · doi:10.1016/s0092-8674(00)81405-1 · Cited by 1,154 · see citing works
Görlach, J., Volrath, S., Knauf-Beiter, G., Hengy, G., Beckhove, U., Kogel, K.-H., Oostendorp, M., Staub, T. H., Ward, E., Keßmann, H., et al. (1996) · The Plant Cell · doi:10.1105/tpc.8.4.629 · Cited by 1,066 · see citing works
Liu, Y., Schiff, M., MARATHE, R. P., & Dinesh‐Kumar, S. P. (2002) · The Plant Journal · doi:10.1046/j.1365-313x.2002.01297.x · Cited by 1,043 · see citing works
The transcriptome of Arabidopsis thaliana during systemic acquired resistance
Maleck, K., Levine, A., Eulgem, T., Morgan, A., Schmid, J., Lawton, K. A., Dangl, J. L., & Dietrich, R. A. (2000) · Nature Genetics · doi:10.1038/82521 · Cited by 1,021 · see citing works
Increase in Salicylic Acid at the Onset of Systemic Acquired Resistance in Cucumber
Métraux, J., Signer, H., Ryals, J. A., Ward, E. R., Wyss‐Benz, M., Gaudin, J., Raschdorf, K., Schmid, E., Blum, W., & Inverardi, B. (1990) · Science · doi:10.1126/science.250.4983.1004 · Cited by 984 · see citing works
Systemic acquired resistance induced by localized virus infections in plants
Ross, A. F. (1961) · Virology · doi:10.1016/0042-6822(61)90319-1 · Cited by 876 · see citing works
Nawrath, C., & Métraux, J. (1999) · The Plant Cell · doi:10.1105/tpc.11.8.1393 · Cited by 834 · see citing works
Airborne signalling by methyl salicylate in plant pathogen resistance
Shulaev, V., Silverman, P., & Raskin, I. (1997) · Nature · doi:10.1038/385718a0 · Cited by 823 · see citing works
Milligan, S. B., Bodeau, J. P., Yaghoobi, J., Kaloshian, I., Zabel, P., & Williamson, V. M. (1998) · The Plant Cell · doi:10.1105/tpc.10.8.1307 · Cited by 804 · see citing works
Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco
White, R. F. (1979) · Virology · doi:10.1016/0042-6822(79)90019-9 · Cited by 797 · see citing works
A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis
Maldonado-Alconada, A. M., Doerner, P. W., Dixon, R. A., Lamb, C. J., & Cameron, R. K. (2002) · Nature · doi:10.1038/nature00962 · Cited by 787 · see citing works
Aarts, N., Metz, M., Holub, E. B., Staskawicz, B. J., Daniels, M. J., & Parker, J. E. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.17.10306 · Cited by 780 · see citing works
Pieterse, C. M. J., Wees, S. C. M. V., Hoffland, E., van Pelt, J. A., & van Loon, L. C. (1996) · The Plant Cell · doi:10.1105/tpc.8.8.1225 · Cited by 777 · see citing works
Delaney, T. P., Friedrich, L., & Ryals, J. A. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.14.6602 · Cited by 772 · see citing works
Lawton, K. A., Friedrich, L., Hunt, M. D., et al. (1996) · The Plant Journal · doi:10.1046/j.1365-313x.1996.10010071.x · Cited by 766 · see citing works
The nematode resistance gene Mi of tomato confers resistance against the potato aphid
Rossi, M., Goggin, F. L., Milligan, S. B., Kaloshian, I., Ullman, D. E., & Williamson, V. M. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.17.9750 · Cited by 759 · see citing works
Nuclear Localization of NPR1 Is Required for Activation of PR Gene Expression
Kinkema, M., Fan, W., & Dong, X. (2000) · The Plant Cell · doi:10.1105/tpc.12.12.2339 · Cited by 718 · see citing works
Self-citationZhang, Y., Fan, W., Kinkema, M., Li, X., & Dong, X. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.11.6523 · Cited by 717 · see citing works
Self-citationArabidopsis mutants simulating disease resistance response
Dietrich, R. A., Delaney, T. P., Uknes, S. J., et al. (1994) · Cell · doi:10.1016/0092-8674(94)90218-6 · Cited by 715 · see citing works
A benzothiadiazole derivative induces systemic acquired resistance in tobacco
Friedrich, L., Lawton, K. A., Ruess, W., et al. (1996) · The Plant Journal · doi:10.1046/j.1365-313x.1996.10010061.x · Cited by 702 · see citing works
Vernooij, B., Friedrich, L., Morse, A. M., Reist, R., Kolditz-Jawhar, R., Ward, E. R., Uknes, S. J., Keßmann, H., & Ryals, J. A. (1994) · The Plant Cell · doi:10.1105/tpc.6.7.959 · Cited by 642 · see citing works
Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4
Feys, B. J., Moisan, L. J., Newman, M., & Parker, J. E. (2001) · The EMBO Journal · doi:10.1093/emboj/20.19.5400 · Cited by 629 · see citing works
Falk, A. B., Feys, B. J., Frost, L. N., Jones, J. D. G., Daniels, M. J., & Parker, J. E. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.6.3292 · Cited by 629 · see citing works
Induced Systemic Resistance (ISR) Against Pathogens in the Context of Induced Plant Defences
Heil, M. (2002) · Annals of Botany · doi:10.1093/aob/mcf076 · Cited by 623 · see citing works
Wees, S. C. M. V., Swart, E., van Pelt, J. A., et al. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.130425197 · Cited by 618 · see citing works
Fitness costs of induced resistance: emerging experimental support for a slippery concept
Heil, M. (2002) · Trends in Plant Science · doi:10.1016/s1360-1385(01)02186-0 · Cited by 612 · see citing works
Isolation of Arabidopsis Mutants With Enhanced Disease Susceptibility by Direct Screening
Glazebrook, J., Rogers, E. E., & Ausubel, F. M. (1996) · Genetics · doi:10.1093/genetics/143.2.973 · Cited by 608 · see citing works
Nawrath, C., Heck, S., Parinthawong, N., & Métraux, J. (2002) · The Plant Cell · doi:10.1105/tpc.010376 · Cited by 605 · see citing works
Després, C., DeLong, C. M. O., Glaze, S., Liu, E., & Fobert, P. R. (2000) · The Plant Cell · doi:10.1105/tpc.12.2.279 · Cited by 599 · see citing works
van Loon, L. C., & van Kammen, A. (1970) · Virology · doi:10.1016/0042-6822(70)90395-8 · Cited by 593 · see citing works
Després, C., Chubak, C., Rochon, A., Clark, R., Bethune, T. D., Desveaux, D., & Fobert, P. R. (2003) · The Plant Cell · doi:10.1105/tpc.012849 · Cited by 592 · see citing works
Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling
Jirage, D., Tootle, T. L., Reuber, T. L., Frost, L. N., Feys, B. J., Parker, J. E., Ausubel, F. M., & Glazebrook, J. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.23.13583 · Cited by 585 · see citing works
Yu, D., Chen, C., & Chen, Z. (2001) · The Plant Cell · doi:10.1105/tpc.010115 · Cited by 585 · see citing works
Shirasu, K., Nakajima, H., Rajasekhar, V. K., Dixon, R. A., & Lamb, C. J. (1997) · The Plant Cell · doi:10.1105/tpc.9.2.261 · Cited by 585 · see citing works
Cao, H., Li, X., & Dong, X. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.11.6531 · Cited by 575 · see citing works
Self-citationZhou, J., Trifa, Y., Silva, H., Pontier, D., Lam, E., Shah, J., & Klessig, D. F. (2000) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi.2000.13.2.191 · Cited by 541 · see citing works
Shah, J., Tsui, F., & Klessig, D. F. (1997) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi.1997.10.1.69 · Cited by 524 · see citing works
Parker, J. E., Holub, E. B., Frost, L. N., et al. (1996) · The Plant Cell · doi:10.1105/tpc.8.11.2033 · Cited by 521 · see citing works
Zhang, Y., Tessaro, M. J., Lassner, M., & Li, X. (2003) · The Plant Cell · doi:10.1105/tpc.014894 · Cited by 518 · see citing works
Salicylic Acid and Disease Resistance in Plants
Dempsey, D. A., Shah, J., & Klessig, D. F. (1999) · Critical Reviews in Plant Sciences · doi:10.1080/07352689991309397 · Cited by 508 · see citing works
Rasmussen, J. B., Hammerschmidt, R., & Zook, M. N. (1991) · PLANT PHYSIOLOGY · doi:10.1104/pp.97.4.1342 · Cited by 503 · see citing works
Glazebrook, J., Chen, W., Estes, B., Chang, H., Nawrath, C., Métraux, J., Zhu, T., & Katagiri, F. (2003) · The Plant Journal · doi:10.1046/j.1365-313x.2003.01717.x · Cited by 499 · see citing works
Ryals, J. A., Weymann, K. B., Lawton, K. A., Friedrich, L., Ellis, D., Steiner, H., Johnson, J. R., Delaney, T. P., Jesse, T., Vos, P., et al. (1997) · The Plant Cell · doi:10.1105/tpc.9.3.425 · Cited by 480 · see citing works
Fan, W., & Dong, X. (2002) · The Plant Cell · doi:10.1105/tpc.001628 · Cited by 479 · see citing works
Self-citationZhang, Y., Goritschnig, S., Dong, X., & Li, X. (2003) · The Plant Cell · doi:10.1105/tpc.015842 · Cited by 472 · see citing works
Self-citationTwo tobacco DNA-binding proteins with homology to the nuclear factor CREB
Katagiri, F., Lam, E., & Chua, N. (1989) · Nature · doi:10.1038/340727a0 · Cited by 468 · see citing works
PAD4 Functions Upstream from Salicylic Acid to Control Defense Responses in Arabidopsis
Zhou, N., Tootle, T. L., Tsui, F., Klessig, D. F., & Glazebrook, J. (1998) · The Plant Cell · doi:10.1105/tpc.10.6.1021 · Cited by 445 · see citing works
Salicylic Acid in Rice (Biosynthesis, Conjugation, and Possible Role)
Silverman, P., Seskar, M., Kanter, D., Schweizer, P., Métraux, J., & Raskin, I. (1995) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.2.633 · Cited by 442 · see citing works
Hydrogen Peroxide Stimulates Salicylic Acid Biosynthesis in Tobacco
León, J., Lawton, M. A., & Raskin, I. (1995) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.4.1673 · Cited by 437 · see citing works
Durner, J., & Klessig, D. F. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.24.11312 · Cited by 425 · see citing works
Ton, J., van Pelt, J. A., van Loon, L. C., et al. (2002) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi.2002.15.1.27 · Cited by 404 · see citing works
Johnson, C., Boden, E., & Arias, J. (2003) · The Plant Cell · doi:10.1105/tpc.012211 · Cited by 377 · see citing works
Beisson, F., Koo, A. J., Ruuska, S. A., et al. (2003) · PLANT PHYSIOLOGY · doi:10.1104/pp.103.022988 · Cited by 375 · see citing works
Functional analysis of regulatory sequences controlling PR‐1 gene expression in Arabidopsis
Lebel, E. G., Heifetz, P. B., Thorne, L. B., Uknes, S. J., Ryals, J. A., & Ward, E. R. (1998) · The Plant Journal · doi:10.1046/j.1365-313x.1998.00288.x · Cited by 357 · see citing works
Chern, M., Fitzgerald, H. A., Yadav, R. C., Canlas, P. E., Dong, X., & Ronald, P. C. (2001) · The Plant Journal · doi:10.1046/j.1365-313x.2001.01070.x · Cited by 353 · see citing works
Self-citationBiosynthesis and metabolism of salicylic acid.
Lee, H. I., León, J., & Raskin, I. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.10.4076 · Cited by 339 · see citing works
Yield penalties of disease resistance in crops
Brown, J. K. M. (2002) · Current Opinion in Plant Biology · doi:10.1016/s1369-5266(02)00270-4 · Cited by 332 · see citing works
Sugar import and metabolism during seed development
WEBER, H., Borisjuk, L., & Wobus, U. (1997) · Trends in Plant Science · doi:10.1016/s1360-1385(97)85222-3 · Cited by 326 · see citing works
Kumar, D., & Klessig, D. F. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307162100 · Cited by 322 · see citing works
Blein, J., Coutos‐Thévenot, P., Marion, D., et al. (2002) · Trends in Plant Science · doi:10.1016/s1360-1385(02)02284-7 · Cited by 310 · see citing works
Heil, M., Hilpert, A., Kaiser, W. M., et al. (2000) · Journal of Ecology · doi:10.1046/j.1365-2745.2000.00479.x · Cited by 308 · see citing works
Shirano, Y., Kachroo, P., Shah, J., & Klessig, D. F. (2002) · The Plant Cell · doi:10.1105/tpc.005348 · Cited by 302 · see citing works
Overproduction of salicylic acid in plants by bacterial transgenes enhances pathogen resistance
Verberne, M. C., Verpoorte, R., Bol, J. F., Mercado‐Blanco, J., & Linthorst, H. J. M. (2000) · Nature Biotechnology · doi:10.1038/77347 · Cited by 288 · see citing works
Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory
Felton, G. W., Korth, K. L., Bi, J. L., Wesley, S. V., Huhman, D. V., Mathews, M. C., Murphy, J. B., Lamb, C. J., & Dixon, R. A. (1999) · Current Biology · doi:10.1016/s0960-9822(99)80140-7 · Cited by 271 · see citing works
Li, X., Zhang, Y., Clarke, J. D., Li, Y., & Dong, X. (1999) · Cell · doi:10.1016/s0092-8674(00)81962-5 · Cited by 262 · see citing works
Self-citationYu, D. (2001) · The Plant Cell · doi:10.1105/tpc.13.7.1527 · Cited by 251 · see citing works
Dewdney, J., Reuber, T. L., Wildermuth, M. C., et al. (2000) · The Plant Journal · doi:10.1046/j.1365-313x.2000.00870.x · Cited by 246 · see citing works
Is Salicylic Acid a Translocated Signal of Systemic Acquired Resistance in Tobacco?
Shulaev, V., León, J., & Raskin, I. (1995) · The Plant Cell · doi:10.1105/tpc.7.10.1691 · Cited by 233 · see citing works
A fast neutron deletion mutagenesis‐based reverse genetics system for plants
Li, X., Song, Y., Century, K. S., Straight, S., Ronald, P. C., Dong, X., Lassner, M., & Zhang, Y. (2001) · The Plant Journal · doi:10.1046/j.1365-313x.2001.01084.x · Cited by 232 · see citing works
Self-citationIs hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance?
Neuenschwander, U. H., Vernooij, B., Friedrich, L., et al. (1995) · The Plant Journal · doi:10.1046/j.1365-313x.1995.08020227.x · Cited by 231 · see citing works
Salicylate, superoxide synthesis and cell suicide in plant defence
DRAPER, J. (1997) · Trends in Plant Science · doi:10.1016/s1360-1385(97)01030-3 · Cited by 229 · see citing works
Ecological costs of induced resistance
Heil, M. (2002) · Current Opinion in Plant Biology · doi:10.1016/s1369-5266(02)00267-4 · Cited by 224 · see citing works
Desveaux, D., Subramaniam, R., Després, C., Mess, J., Lévesque, C., Fobert, P. R., Dangl, J. L., & Brisson, N. (2004) · Developmental Cell · doi:10.1016/s1534-5807(04)00028-0 · Cited by 210 · see citing works
Nandi, A. K., Welti, R., & Shah, J. (2004) · The Plant Cell · doi:10.1105/tpc.016907 · Cited by 209 · see citing works
Characterizing the stress/defense transcriptome of Arabidopsis
Mahalingam, R., Gomez-Buitrago, A., Eckardt, N. A., et al. (2003) · Genome biology · doi:10.1186/gb-2003-4-3-r20 · Cited by 206 · see citing works
Fitzgerald, H. A., Chern, M., Navarre, R., et al. (2004) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi.2004.17.2.140 · Cited by 204 · see citing works
Genetic dissection of systemic acquired resistance
Dong, X. (2001) · Current Opinion in Plant Biology · doi:10.1016/s1369-5266(00)00178-3 · Cited by 200 · see citing works
Self-citationInduced Systemic Resistance in Cucumber in Response to 2,6-Dichloro-Isonicotinic Acid and Pathogens
Métraux, J., Ahl-Goy, P., Staub, T. H., et al. (1991) · Current plant science and biotechnology in agriculture · doi:10.1007/978-94-015-7934-6_66 · Cited by 189 · see citing works
Recent breakthroughs in the study of salicylic acid biosynthesis
Métraux, J. (2002) · Trends in Plant Science · doi:10.1016/s1360-1385(02)02313-0 · Cited by 189 · see citing works
A role for salicylic acid and NPR1 in regulating cell growth in Arabidopsis
Vanacker, H., Lu, H., Rate, D. N., & Greenberg, J. T. (2001) · The Plant Journal · doi:10.1046/j.1365-313x.2001.01158.x · Cited by 186 · see citing works
Signal transduction in systemic acquired resistance.
Ryals, J. A., Lawton, K. A., Delaney, T. P., et al. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.10.4202 · Cited by 162 · see citing works
A lipid transfer protein binds to a receptor involved in the control of plant defence responses
Buhot, N., Douliez, J., Jacquemard, A., Marion, D., Tran, V., Maume, B. F., Milat, M.-L., Ponchet, M., Mikès, V., Kader, J. C., et al. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)03116-7 · Cited by 161 · see citing works
An, L., Oon, L. L. E., & Trien, E. A. V. A. S. (1999) · Cited by 156 · see citing works
Signal conflicts and synergies in induced resistance to multiple attackers
Bostock, R. M. (1999) · Physiological and Molecular Plant Pathology · doi:10.1006/pmpp.1999.0218 · Cited by 155 · see citing works
Kim, H. S., & Delaney, T. P. (2002) · The Plant Journal · doi:10.1046/j.1365-313x.2001.01411.x · Cited by 153 · see citing works
Friedrich, L., Lawton, K. A., Dietrich, R. A., et al. (2001) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi.2001.14.9.1114 · Cited by 152 · see citing works
Niggeweg, R., Thurow, C., Kegler, C., et al. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m909267199 · Cited by 142 · see citing works
Identification of a Soluble, High-Affinity Salicylic Acid-Binding Protein in Tobacco
Du, H., & Klessig, D. F. (1997) · PLANT PHYSIOLOGY · doi:10.1104/pp.113.4.1319 · Cited by 138 · see citing works
Transport of Salicylic Acid in Tobacco Necrosis Virus-Infected Cucumber Plants
Mölders, W., Buchala, A. J., & Métraux, J. (1996) · PLANT PHYSIOLOGY · doi:10.1104/pp.112.2.787 · Cited by 134 · see citing works
Weigel, R. R., Bäuscher, C., Pfitzner, A. J. P., & Pfitzner, U. M. (2001) · Plant Molecular Biology · doi:10.1023/a:1010652620115 · Cited by 132 · see citing works
Local and Systemic Biosynthesis of Salicylic Acid in Infected Cucumber Plants
Meuwly, P., Mölders, W., Buchala, A. J., et al. (1995) · PLANT PHYSIOLOGY · doi:10.1104/pp.109.3.1107 · Cited by 132 · see citing works
Mauch, F., Mauch‐Mani, B., Gaille, C., et al. (2001) · The Plant Journal · doi:10.1046/j.1365-313x.2001.00940.x · Cited by 132 · see citing works
Coquoz, J.-L. (1995) · Phytopathology · doi:10.1094/phyto-85-1219 · Cited by 121 · see citing works
Xiang, C., Miao, Z., & Lam, E. (1997) · Plant Molecular Biology · doi:10.1023/a:1005873500238 · Cited by 113 · see citing works
Cipollini, D. F. (2002) · Oecologia · doi:10.1007/s00442-002-0909-5 · Cited by 110 · see citing works
Niggeweg, R., Thurow, C., Weigel, R. R., et al. (2000) · Plant Molecular Biology · doi:10.1023/a:1006319113205 · Cited by 109 · see citing works
Ton, J., Davison, S., Wees, S. C. M. V., van Loon, L. C., & Pieterse, C. M. J. (2001) · PLANT PHYSIOLOGY · doi:10.1104/pp.125.2.652 · Cited by 108 · see citing works
Ton, J., de Vos, M., Robben, C., et al. (2002) · The Plant Journal · doi:10.1046/j.1365-313x.2002.01190.x · Cited by 107 · see citing works
A new family of plant transcription factors displays a novel ssDNA-binding surface
Desveaux, D., Allard, J., Brisson, N., et al. (2002) · Nature Structural Biology · doi:10.1038/nsb814 · Cited by 106 · see citing works
Is the High Basal Level of Salicylic Acid Important for Disease Resistance in Potato?
Yu, D., Liu, Y., Fan, B., et al. (1997) · PLANT PHYSIOLOGY · doi:10.1104/pp.115.2.343 · Cited by 97 · see citing works
Guedes, M., Richmond, S., & Kuć, J. A. (1980) · Physiological Plant Pathology · doi:10.1016/0048-4059(80)90056-9 · Cited by 96 · see citing works
Tenhaken, R., & Rubel, C. J. (1997) · PLANT PHYSIOLOGY · doi:10.1104/pp.115.1.291 · Cited by 96 · see citing works
Kiefer, I., & Slusarenko, A. J. (2003) · PLANT PHYSIOLOGY · doi:10.1104/pp.103.021709 · Cited by 90 · see citing works
Pontier, D., Miao, Z., & Lam, E. (2001) · The Plant Journal · doi:10.1046/j.1365-313x.2001.01086.x · Cited by 89 · see citing works
Salicylic acid: signal perception and transduction
Shah, J., & Klessig, D. F. (1999) · New comprehensive biochemistry · doi:10.1016/s0167-7306(08)60503-7 · Cited by 85 · see citing works
Jenns, A. E. (1979) · Phytopathology · doi:10.1094/phyto-69-753 · Cited by 76 · see citing works
Salicylic Acid and Disease Resistance in Plants
Dempsey, D. A. (1999) · Critical Reviews in Plant Sciences · doi:10.1016/s0735-2689(99)00391-3 · Cited by 64 · see citing works
Characterization of a New Arabidopsis Mutant Exhibiting Enhanced Disease Resistance
Silva, H., Yoshioka, K., Dooner, H. K., et al. (1999) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi.1999.12.12.1053 · Cited by 60 · see citing works
Induced systemic protection in cucumbers: the source of the “signal”
Dean, R. A., & Kuć, J. A. (1986) · Physiological and Molecular Plant Pathology · doi:10.1016/s0048-4059(86)80066-2 · Cited by 57 · see citing works
Mayda, E., Mauch‐Mani, B., & Vera, P. (2000) · The Plant Cell · doi:10.1105/tpc.12.11.2119 · Cited by 43 · see citing works
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Salicylic acid, a multifaceted hormone to combat disease
Vlot, A. C., Dempsey, D. A., & Klessig, D. F. (2009) · Annual Review of Phytopathology · doi:10.1146/annurev.phyto.050908.135202 · Cited by 2,568 · see citing works
Kleinnijenhuis, J., Quintin, J., Preijers, F., Joosten, L. A. B., Ifrim, D. C., Saeed, S., Jacobs, C., van Loenhout, J., de Jong, D., Stunnenberg, H. G., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1202870109 · Cited by 1,728 · see citing works
Quintin, J., Saeed, S., Martens, J. H. A., Giamarellos-Bourboulis, E. J., Ifrim, D. C., Logie, C., Jacobs, L., Jansen, T., Kullberg, B.-J., Wijmenga, C., et al. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.06.006 · Cited by 1,289 · see citing works
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Stout, M. J., Thaler, J. S., & Thomma, B. P. H. J. (2006) · Annual Review of Entomology · doi:10.1146/annurev.ento.51.110104.151117 · Cited by 463 · see citing works
Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes
Van der Ent, S., Van Wees, S. C. M., & Pieterse, C. M. J. (2009) · Phytochemistry · doi:10.1016/j.phytochem.2009.06.009 · Cited by 443 · see citing works
Stress-activated Genomic Expression Changes Serve a Preparative Role for Impending Stress in Yeast
Berry, D. B., & Gasch, A. P. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-07-0680 · Cited by 326 · see citing works
Franceschi, C., Salvioli, S., Garagnani, P., de Eguileor, M., Monti, D., & Capri, M. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00982 · Cited by 290 · see citing works
Signaling by small metabolites in systemic acquired resistance
Shah, J., Chaturvedi, R., Chowdhury, Z., Venables, B., & Petros, R. A. (2014) · The Plant Journal · doi:10.1111/tpj.12464 · Cited by 151 · see citing works
Aydi Ben Abdallah, R., Stedel, C., Garagounis, C., Nefzi, A., Jabnoun-Khiareddine, H., Papadopoulou, K. K., & Daami-Remadi, M. (2017) · Crop Protection · doi:10.1016/j.cropro.2017.05.008 · Cited by 87 · see citing works
De Vleesschauwer, D., Chernin, L., & Höfte, M. M. (2009) · BMC Plant Biology · doi:10.1186/1471-2229-9-9 · Cited by 77 · see citing works
Asari, S., Ongena, M., Debois, D., De Pauw, E., Chen, K., Bejai, S., & Meijer, J. (2017) · Annals of Botany · doi:10.1093/aob/mcx089 · Cited by 30 · see citing works
Elmer, W. H. (2014) · Phytopathology · doi:10.1094/phyto-08-13-0219-r · Cited by 19 · see citing works
Ncube, E. N., Steenkamp, P. A., Madala, N. E., & Dubery, I. A. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.01469 · Cited by 8 · see citing works
- Authors
- Durrant, W. E., & Dong, X.
- Affiliations
- Duke University (US)
- ORCID
- Dong, X.
- Venue
- Annual Review of Phytopathology
- Publisher
- Annual Reviews
- Published
- 2004-09-01
- Volume
- 42
- Issue
- 1
- Pages
- 185-209
- ISSN
- 0066-4286 (ISSN-L)
- 1545-2107
- OpenAlex
- W2129742189
- Cited by
- 3,184
- References
- 130
- Citations by year
- 2026: 81 · 2025: 124 · 2024: 102 · 2023: 137 · 2022: 131 · 2021: 171 · 2020: 176 · 2019: 132 · 2018: 113 · 2017: 161 · 2016: 134 · 2015: 177 · 2014: 207 · 2013: 217 · 2012: 186
- FWCI
- 8.74
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annual Review of Phytopathology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- U.S. Department of Agriculture
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- systemic acquired resistance, salicylic acid, NPR1, TGA transcription factors, pathogenesis-related proteins, induced plant defense, defense gene expression, lipid signaling, Arabidopsis thaliana, plant immunity
- MeSH terms
- DNA-Binding Proteins, Immunity, Innate, Nuclear Proteins, Transcription Factors, Signal Transduction, Arabidopsis, Models, Immunological, Gene Expression Regulation, Plant, Salicylic Acid, Arabidopsis Proteins
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