Networking by small-molecule hormones in plant immunity

Buchanan, B.B., Gruissem, W. & Jones, R.L. Biochemistry & Molecular Biology of Plants 1367 (American Society of Plant Physiologists, Rockville, Maryland, USA, 2000).

Pozo, M.J., Van Loon, L.C. & Pieterse, C.M.J. Jasmonates—signals in plant-microbe interactions. J. Plant Growth Regul. 23, 211–222 (2004).

Van Loon, L.C., Geraats, B.P.J. & Linthorst, H.J.M. Ethylene as a modulator of disease resistance in plants. Trends Plant Sci. 11, 184–191 (2006).

Loake, G. & Grant, M. Salicylic acid in plant defence—the players and protagonists. Curr. Opin. Plant Biol. 10, 466–472 (2007).

Howe, G.A. Jasmonates as signals in the wound response. J. Plant Growth Regul. 23, 223–237 (2004).

Von Dahl, C.C. & Baldwin, I.T. Deciphering the role of ethylene in plant-herbivore interactions. J. Plant Growth Regul. 26, 201–209 (2007).

Asselbergh, B., De Vleesschauwer, D. & Höfte, M. Global switches and fine-tuning—ABA modulates plant pathogen defense. Mol. Plant Microbe Interact. 21, 709–719 (2008).

Mauch-Mani, B. & Mauch, F. The role of abscisic acid in plant-pathogen interactions. Curr. Opin. Plant Biol. 8, 409–414 (2005).

Navarro, L. et al. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436–439 (2006).

Wang, D., Pajerowska-Mukhtar, K., Hendrickson Culler, A. & Dong, X. Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr. Biol. 17, 1784–1790 (2007).

Navarro, L. et al. DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr. Biol. 18, 650–655 (2008).

Walters, D.R. & McRoberts, N. Plants and biotrophs: a pivotal role for cytokinins? Trends Plant Sci. 11, 581–586 (2006).

Siemens, J. et al. Transcriptome analysis of Arabidopsis clubroots indicate a key role for cytokinins in disease development. Mol. Plant Microbe Interact. 19, 480–494 (2006).

Nakashita, H. et al. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J. 33, 887–898 (2003).

Shan, L.B. et al. 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 (2008).

Walters, D. & Heil, M. Costs and trade-offs associated with induced resistance. Physiol. Mol. Plant Pathol. 71, 3–17 (2007).

De Vos, M. et al. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant Microbe Interact. 18, 923–937 (2005).

Glazebrook, J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205–227 (2005).

Jones, J.D.G. & Dangl, J.L. The plant immune system. Nature 444, 323–329 (2006).

Göhre, V. & Robatzek, S. Breaking the barriers: microbial effector molecules subvert plant immunity. Annu. Rev. Phytopathol. 46, 189–215 (2008).

Nürnberger, T. & Kemmerling, B. Pathogen-associated molecular patterns (PAMP) and PAMP-triggered immunity. Annu. Plant Rev. 34, 16–47 (2009).

Chisholm, S.T., Coaker, G., Day, B. & Staskawicz, B.J. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803–814 (2006).

Schwessinger, B. & Zipfel, C. News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr. Opin. Plant Biol. 11, 389–395 (2008).

Tsuda, K., Sato, M., Glazebrook, J., Cohen, J.D. & Katagiri, F. Interplay between MAMP-triggered and SA-mediated defense responses. Plant J. 53, 763–775 (2008).

De Wit, P.J.G.M. Pathogen avirulence and plant resistance: a key role for recognition. Trends Plant Sci. 2, 452–458 (1997).

Thomma, B.P.H.J., Penninckx, I.A.M.A., Broekaert, W.F. & Cammue, B.P.A. The complexity of disease signaling in Arabidopsis. Curr. Opin. Immunol. 13, 63–68 (2001).

Durrant, W.E. & Dong, X. Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185–209 (2004).

Van Loon, L.C., Rep, M. & Pieterse, C.M.J. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44, 135–162 (2006).

Mishina, T.E. & Zeier, J. Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J. 50, 500–513 (2007).

Dong, X. NPR1, all things considered. Curr. Opin. Plant Biol. 7, 547–552 (2004).

Vlot, A.C., Klessig, D.F. & Park, S.-W. Systemic acquired resistance: the elusive signal(s). Curr. Opin. Plant Biol. 11, 436–442 (2008).

Van Loon, L.C., Bakker, P.A.H.M. & Pieterse, C.M.J. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36, 453–483 (1998).

Pozo, M.J. & Azcon-Aguilar, C. Unraveling mycorrhiza-induced resistance. Curr. Opin. Plant Biol. 10, 393–398 (2007).

Van Wees, S.C.M., Van der Ent, S. & Pieterse, C.M.J. Plant immune responses triggered by beneficial microbes. Curr. Opin. Plant Biol. 11, 443–448 (2008).

Bakker, P.A.H.M., Pieterse, C.M.J. & Van Loon, L.C. Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97, 239–243 (2007).

Van der Ent, S. et al. MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol. 146, 1293–1304 (2008).

Conrath, U. et al. Priming: getting ready for battle. Mol. Plant Microbe Interact. 19, 1062–1071 (2006).

Pozo, M.J., Van der Ent, S., Van Loon, L.C. & Pieterse, C.M.J. Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria-induced systemic resistance in Arabidopsis thaliana. New Phytol. 180, 511–523 (2008).

Ton, J., Van Pelt, J.A., Van Loon, L.C. & Pieterse, C.M.J. Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Mol. Plant Microbe Interact. 15, 27–34 (2002).

Van Oosten, V.R. et al. Differential effectiveness of microbially induced resistance against herbivorous insects in Arabidopsis. Mol. Plant Microbe Interact. 21, 919–930 (2008).

Stout, M.J., Thaler, J.S. & Thomma, B.P.H.J. Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu. Rev. Entomol. 51, 663–689 (2006).

Poelman, E.H., van Loon, J.J.A. & Dicke, M. Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends Plant Sci. 13, 534–541 (2008).

Van der Putten, W.H., Vet, L.E.M., Harvey, J.A. & Wäckers, F.L. Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol. Evol. 16, 547–554 (2001).

Reymond, P. & Farmer, E.E. Jasmonate and salicylate as global signals for defense gene expression. Curr. Opin. Plant Biol. 1, 404–411 (1998).

Pieterse, C.M.J. & Dicke, M. Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci. 12, 564–569 (2007).

Kunkel, B.N. & Brooks, D.M. Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5, 325–331 (2002).

Bostock, R.M. Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu. Rev. Phytopathol. 43, 545–580 (2005).

Kendrick, M.D. & Chang, C. Ethylene signaling: new levels of complexity and regulation. Curr. Opin. Plant Biol. 11, 479–485 (2008).

Katsir, L., Chung, H.S., Koo, A.J.K. & Howe, G.A. Jasmonate signaling: a conserved mechanism of hormone sensing. Curr. Opin. Plant Biol. 11, 428–435 (2008).

Doherty, H.M., Selvendran, R.R. & Bowles, D.J. The wound response of tomato plants can be inhibited by aspirin and related hydroxy-benzoic acids. Physiol. Mol. Plant Pathol. 33, 377–384 (1988).

Penninckx, I.A.M.A., Thomma, B.P.H.J., Buchala, A., Métraux, J.-P. & Broekaert, W.F. Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10, 2103–2113 (1998).

Katagiri, F. A global view of defense gene expression regulation—a highly interconnected signaling network. Curr. Opin. Plant Biol. 7, 506–511 (2004).

Glazebrook, J. et al. Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J. 34, 217–228 (2003).

Koornneef, A. et al. Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol. 147, 1358–1368 (2008).

Spoel, S.H., Johnson, J.S. & Dong, X. Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc. Natl. Acad. Sci. USA 104, 18842–18847 (2007).

Spoel, S.H. et al. NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15, 760–770 (2003).

Schenk, P.M. et al. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl. Acad. Sci. USA 97, 11655–11660 (2000).

Mur, L.A.J., Kenton, P., Atzorn, R., Miersch, O. & Wasternack, C. The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol. 140, 249–262 (2006).

Van Wees, S.C.M., De Swart, E.A.M., Van Pelt, J.A., Van Loon, L.C. & Pieterse, C.M.J. Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 97, 8711–8716 (2000).

Koornneef, A. & Pieterse, C.M.J. Cross-talk in defense signaling. Plant Physiol. 146, 839–844 (2008).

Spoel, S.H. & Dong, X. Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 3, 348–351 (2008).

Kazan, K. & Manners, J.M. Jasmonate signaling: toward an integrated view. Plant Physiol. 146, 1459–1468 (2008).

Lorenzo, O. & Solano, R. Molecular players regulating the jasmonate signalling network. Curr. Opin. Plant Biol. 8, 532–540 (2005).

López, M.A., Bannenberg, G. & Castresana, C. Controlling hormone signaling is a plant and pathogen challenge for growth and survival. Curr. Opin. Plant Biol. 11, 420–427 (2008).

Robert-Seilaniantz, A., Navarro, L., Bari, R. & Jones, J.D.G. Pathological hormone imbalances. Curr. Opin. Plant Biol. 10, 372–379 (2007).

Petersen, M. et al. Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell 103, 1111–1120 (2000).

Brodersen, P. et al. Arabidopsis MAP kinase 4 regulates salicylic acid- and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. Plant J. 47, 532–546 (2006).

Kachroo, P., Shanklin, J., Shah, J., Whittle, E.J. & Klessig, D.F. A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proc. Natl. Acad. Sci. USA 98, 9448–9453 (2001).

Ndamukong, I. et al. SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. Plant J. 50, 128–139 (2007).

Li, J., Brader, G. & Palva, E.T. The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16, 319–331 (2004).

Kachroo, P., Kachroo, A., Lapchyk, L., Hildebrand, D. & Klessig, D.F. Restoration of defective cross talk in ssi2 mutants: Role of salicylic acid, jasmonic acid, and fatty acids in SSI2-mediated signaling. Mol. Plant Microbe Interact. 16, 1022–1029 (2003).

Mou, Z., Fan, W.H. & Dong, X.N. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935–944 (2003).

Pieterse, C.M.J. & Van Loon, L.C. NPR1: the spider in the web of induced resistance signaling pathways. Curr. Opin. Plant Biol. 7, 456–464 (2004).

Yuan, Y. et al. Functional analysis of rice NPR1-like genes reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnol. J. 5, 313–324 (2007).

Leon-Reyes, A. et al. Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiol. 149, 1797–1809 (2009).

Johansson, A., Staal, J. & Dixelius, C. Early responses in the Arabidopsis-Verticillium longisporum pathosystem are dependent on NDR1, JA- and ET-associated signals via cytosolic NPR1 and RFO1. Mol. Plant Microbe Interact. 19, 958–969 (2006).

Pré, M. et al. The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol. 147, 1347–1357 (2008).

Lorenzo, O., Piqueras, R., Sánchez-Serrano, J.J. & Solano, R. ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15, 165–178 (2003).

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 defense responses in Arabidopsis. Plant Cell 16, 1938–1950 (2004).

Anderson, J.P. et al. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16, 3460–3479 (2004).

Nickstadt, A. et al. The jasmonate-insensitive mutant jin1 shows increased resistance to biotrophic as well as necrotrophic pathogens. Mol. Plant Pathol. 5, 425–434 (2004).

Truman, W., Bennett, M.H., Kubigsteltig, I., Turnbull, C. & Grant, M. Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc. Natl. Acad. Sci. USA 104, 1075–1080 (2007).

Laurie-Berry, N., Joardar, V., Street, I.H. & Kunkel, B.N. The Arabidopsis thaliana JASMONATE INSENSITIVE 1 gene is required for suppression of salicylic acid-dependent defenses during infection by Pseudomonas syringae. Mol. Plant Microbe Interact. 19, 789–800 (2006).

Verberne, M.C., Hoekstra, J., Bol, J.F. & Linthorst, H.J.M. Signaling of systemic acquired resistance in tobacco depends on ethylene perception. Plant J. 35, 27–32 (2003).

Lawton, K.A., Potter, S.L., Uknes, S. & Ryals, J. Acquired resistance signal transduction in Arabidopsis is ethylene independent. Plant Cell 6, 581–588 (1994).

De Vos, M. et al. Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiol. 142, 352–363 (2006).

Adie, B.A.T. et al. ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19, 1665–1681 (2007).

Flors, V. et al. Interplay between JA, SA and ABA signalling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. Plant J. 54, 81–92 (2008).

Yasuda, M. et al. Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell 20, 1678–1692 (2008).

Mohr, P.G. & Cahill, D.M. Suppression by ABA of salicylic acid and lignin accumulation and the expression of multiple genes, in Arabidopsis infected with Pseudomonas syringae pv. tomato. Funct. Integr. Genomics 7, 181–191 (2007).

Nagpal, P. et al. Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132, 4107–4118 (2005).

Liu, J. & Wang, X.-J. An integrative analysis of the effects of auxin on jasmonic acid biosynthesis in Arabidopsis thaliana. J. Integr. Plant Biol. 48, 99–103 (2006).

Chen, Z.Y. et al. Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc. Natl. Acad. Sci. USA 104, 20131–20136 (2007).

Belkhadir, Y. & Chory, J. Brassinosteroid signaling: a paradigm for steroid hormone signaling from the cell surface. Science 314, 1410–1411 (2006).

Chinchilla, D. et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497–500 (2007).

Heese, A. et al. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl. Acad. Sci. USA 104, 12217–12222 (2007).

Kemmerling, B. et al. The BRI1-associated kinase 1, BAK1, has a brassinolide-independent role in plant cell-death control. Curr. Biol. 17, 1116–1122 (2007).

Tzfira, T. & Citovsky, V. Agrobacterium-mediated genetic transformation of plants: biology and biotechnology. Curr. Opin. Biotechnol. 17, 147–154 (2006).

Cristescu, S.M., De Martinis, D., Hekkert, S.T., Parker, D.H. & Harren, F.J.M. Ethylene production by Botrytis cinerea in vitro and in tomatoes. Appl. Environ. Microbiol. 68, 5342–5350 (2002).

Spaepen, S., Vanderleyden, J. & Remans, R. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev. 31, 425–448 (2007).

Nomura, K., Melotto, M. & He, S.-Y. Suppression of host defense in compatible plant-Pseudomonas syringae interactions. Curr. Opin. Plant Biol. 8, 361–368 (2005).

de Torres-Zabala, M. et al. Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J. 26, 1434–1443 (2007).

Jelenska, J. et al. A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr. Biol. 17, 499–508 (2007).

Brooks, D.M., Bender, C.L. & Kunkel, B.N. The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defences in Arabidopsis thaliana. Mol. Plant Pathol. 6, 629–639 (2005).

Uppalapati, S.R. et al. The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv. tomato DC3000. Mol. Plant Microbe Interact. 20, 955–965 (2007).

Traw, M.B., Kim, J., Enright, S., Cipollini, D.F. & Bergelson, J. Negative cross-talk between salicylate- and jasmonate-mediated pathways in the Wassilewskija ecotype of Arabidopsis thaliana. Mol. Ecol. 12, 1125–1135 (2003).

Scheres, B. & Lipka, V. Plant cell biology—get your networks together. Curr. Opin. Plant Biol. 10, 546–548 (2007).

Long, T.A., Rady, S.M. & Benfey, P.N. Systems approaches to identifying gene regulatory networks in plants. Annu. Rev. Cell Dev. Biol. 24, 81–103 (2008).