Hydrogen Peroxide Acts as a Second Messenger for the Induction of Defense Genes in Tomato Plants in Response to Wounding, Systemin, and Methyl Jasmonate

Correspondence to: Clarence A. Ryan, tamura{at}wsu.edu (E-mail), 509-335-7643 (fax)

The systemic accumulation of both hydrogen peroxide (H₂O₂) and proteinase inhibitor proteins in tomato leaves in response to wounding was inhibited by the NADPH oxidase inhibitors diphenylene iodonium (DPI), imidazole, and pyridine. The expression of several defense genes in response to wounding, systemin, oligosaccharides, and methyl jasmonate also was inhibited by DPI. These genes, including those of four proteinase inhibitors and polyphenol oxidase, are expressed within 4 to 12 hr after wounding. However, DPI did not inhibit the wound-inducible expression of genes encoding prosystemin, lipoxygenase, and allene oxide synthase, which are associated with the octadecanoid signaling pathway and are expressed 0.5 to 2 hr after wounding. Accordingly, treatment of plants with the H₂O₂-generating enzyme glucose oxidase plus glucose resulted in the induction of only the later-expressed defensive genes and not the early-expressed signaling-related genes. H₂O₂ was cytochemically detected in the cell walls of vascular parenchyma cells and spongy mesophyll cells within 4 hr after wounding of wild-type tomato leaves, but not earlier. The cumulative results suggest that active oxygen species are generated near cell walls of vascular bundle cells by oligogalacturonide fragments produced by wound-inducible polygalacturonase and that the resulting H₂O₂ acts as a second messenger for the activation of defense genes in mesophyll cells. These data provide a rationale for the sequential, coordinated, and functional roles of systemin, jasmonic acid, oligogalacturonides, and H₂O₂ signals for systemic signaling in tomato plants in response to wounding.

This article has been cited by other articles:

				M. M. Islam, S. Munemasa, M. A. Hossain, Y. Nakamura, I. C. Mori, and Y. Murata Roles of AtTPC1, Vacuolar Two Pore Channel 1, in Arabidopsis Stomatal Closure Plant Cell Physiol., February 1, 2010; 51(2): 302 - 311. [Abstract] [Full Text] [PDF]

				H. L. Wong and K. Shimamoto Sending ROS on a Bullet Train Sci. Signal., September 29, 2009; 2(90): pe60 - pe60. [Abstract] [Full Text] [PDF]

				G. Miller, K. Schlauch, R. Tam, D. Cortes, M. A. Torres, V. Shulaev, J. L. Dangl, and R. Mittler The Plant NADPH Oxidase RBOHD Mediates Rapid Systemic Signaling in Response to Diverse Stimuli Sci. Signal., August 18, 2009; 2(84): ra45 - ra45. [Abstract] [Full Text] [PDF]

				F. C. Kupper, E. Gaquerel, A. Cosse, F. Adas, A. F. Peters, D. G. Muller, B. Kloareg, J.-P. Salaun, and P. Potin Free Fatty Acids and Methyl Jasmonate Trigger Defense Reactions in Laminaria digitata Plant Cell Physiol., April 1, 2009; 50(4): 789 - 800. [Abstract] [Full Text] [PDF]

				N. S. Coll, A. Danon, J. Meurer, W. K. Cho, and K. Apel Characterization of soldat8, a Suppressor of Singlet Oxygen-Induced Cell Death in Arabidopsis Seedlings Plant Cell Physiol., April 1, 2009; 50(4): 707 - 718. [Abstract] [Full Text] [PDF]

				J. H. Fowler, J. Narvaez-Vasquez, D. N. Aromdee, V. Pautot, F. M. Holzer, and L. L. Walling Leucine Aminopeptidase Regulates Defense and Wound Signaling in Tomato Downstream of Jasmonic Acid PLANT CELL, April 1, 2009; 21(4): 1239 - 1251. [Abstract] [Full Text] [PDF]

				W. Van den Ende and R. Valluru Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging? J. Exp. Bot., January 1, 2009; 60(1): 9 - 18. [Abstract] [Full Text] [PDF]

				H. Fahnenstich, T. E. Scarpeci, E. M. Valle, U.-I. Flugge, and V. G. Maurino Generation of Hydrogen Peroxide in Chloroplasts of Arabidopsis Overexpressing Glycolate Oxidase as an Inducible System to Study Oxidative Stress Plant Physiology, October 1, 2008; 148(2): 719 - 729. [Abstract] [Full Text] [PDF]

				M. Marina, S. J. Maiale, F. R. Rossi, M. F. Romero, E. I. Rivas, A. Garriz, O. A. Ruiz, and F. L. Pieckenstain Apoplastic Polyamine Oxidation Plays Different Roles in Local Responses of Tobacco to Infection by the Necrotrophic Fungus Sclerotinia sclerotiorum and the Biotrophic Bacterium Pseudomonas viridiflava Plant Physiology, August 1, 2008; 147(4): 2164 - 2178. [Abstract] [Full Text] [PDF]

				P. N. Moschou, M. Sanmartin, A. H. Andriopoulou, E. Rojo, J. J. Sanchez-Serrano, and K. A. Roubelakis-Angelakis Bridging the Gap between Plant and Mammalian Polyamine Catabolism: A Novel Peroxisomal Polyamine Oxidase Responsible for a Full Back-Conversion Pathway in Arabidopsis Plant Physiology, August 1, 2008; 147(4): 1845 - 1857. [Abstract] [Full Text] [PDF]

				C. Tretner, U. Huth, and B. Hause Mechanostimulation of Medicago truncatula leads to enhanced levels of jasmonic acid J. Exp. Bot., July 1, 2008; 59(10): 2847 - 2856. [Abstract] [Full Text] [PDF]

				F. Wen, D. Xing, and L. Zhang Hydrogen peroxide is involved in high blue light-induced chloroplast avoidance movements in Arabidopsis J. Exp. Bot., July 1, 2008; 59(10): 2891 - 2901. [Abstract] [Full Text] [PDF]

				S. Wang, S. M. Assmann, and N. V. Fedoroff Characterization of the Arabidopsis Heterotrimeric G Protein J. Biol. Chem., May 16, 2008; 283(20): 13913 - 13922. [Abstract] [Full Text] [PDF]

				R. C. Leegood Roles of the bundle sheath cells in leaves of C3 plants J. Exp. Bot., May 1, 2008; 59(7): 1663 - 1673. [Abstract] [Full Text] [PDF]

				L. Pauwels, K. Morreel, E. De Witte, F. Lammertyn, M. Van Montagu, W. Boerjan, D. Inze, and A. Goossens Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells PNAS, January 29, 2008; 105(4): 1380 - 1385. [Abstract] [Full Text] [PDF]

				I.-P. Ahn Glufosinate Ammonium-Induced Pathogen Inhibition and Defense Responses Culminate in Disease Protection in bar-Transgenic Rice Plant Physiology, January 1, 2008; 146(1): 213 - 227. [Abstract] [Full Text] [PDF]

				R. Angelini, A. Tisi, G. Rea, M. M. Chen, M. Botta, R. Federico, and A. Cona Involvement of Polyamine Oxidase in Wound Healing Plant Physiology, January 1, 2008; 146(1): 162 - 177. [Abstract] [Full Text] [PDF]

				F. C. Lanfermeijer, M. Staal, R. Malinowski, J. W. Stratmann, and J. T. M. Elzenga Micro-Electrode Flux Estimation Confirms That the Solanum pimpinellifolium cu3 Mutant Still Responds to Systemin Plant Physiology, January 1, 2008; 146(1): 129 - 139. [Abstract] [Full Text] [PDF]

				N. Beffagna and I. Lutzu Inhibition of catalase activity as an early response of Arabidopsis thaliana cultured cells to the phytotoxin fusicoccin J. Exp. Bot., December 1, 2007; 58(15-16): 4183 - 4194. [Abstract] [Full Text] [PDF]

				C. Liu and M. C. Mehdy A Nonclassical Arabinogalactan Protein Gene Highly Expressed in Vascular Tissues, AGP31, Is Transcriptionally Repressed by Methyl Jasmonic Acid in Arabidopsis Plant Physiology, November 1, 2007; 145(3): 863 - 874. [Abstract] [Full Text] [PDF]

				H. W. Choi, Y. J. Kim, S. C. Lee, J. K. Hong, and B. K. Hwang Hydrogen Peroxide Generation by the Pepper Extracellular Peroxidase CaPO2 Activates Local and Systemic Cell Death and Defense Response to Bacterial Pathogens Plant Physiology, November 1, 2007; 145(3): 890 - 904. [Abstract] [Full Text] [PDF]

				C.-Y. Hong, Y. T. Hsu, Y.-C. Tsai, and C. H. Kao Expression of ASCORBATE PEROXIDASE 8 in roots of rice (Oryza sativa L.) seedlings in response to NaCl J. Exp. Bot., October 4, 2007; (2007) erm174v1. [Abstract] [Full Text] [PDF]

				J. Hirayama, S. Cho, and P. Sassone-Corsi Circadian control by the reduction/oxidation pathway: Catalase represses light-dependent clock gene expression in the zebrafish PNAS, October 2, 2007; 104(40): 15747 - 15752. [Abstract] [Full Text] [PDF]

				R. Doczi, G. Brader, A. Pettko-Szandtner, I. Rajh, A. Djamei, A. Pitzschke, M. Teige, and H. Hirt The Arabidopsis Mitogen-Activated Protein Kinase Kinase MKK3 Is Upstream of Group C Mitogen-Activated Protein Kinases and Participates in Pathogen Signaling PLANT CELL, October 1, 2007; 19(10): 3266 - 3279. [Abstract] [Full Text] [PDF]

				Y. Yan, S. Stolz, A. Chetelat, P. Reymond, M. Pagni, L. Dubugnon, and E. E. Farmer A Downstream Mediator in the Growth Repression Limb of the Jasmonate Pathway PLANT CELL, August 1, 2007; 19(8): 2470 - 2483. [Abstract] [Full Text] [PDF]

				P. K. Kandoth, S. Ranf, S. S. Pancholi, S. Jayanty, M. D. Walla, W. Miller, G. A. Howe, D. E. Lincoln, and J. W. Stratmann Tomato MAPKs LeMPK1, LeMPK2, and LeMPK3 function in the systemin-mediated defense response against herbivorous insects PNAS, July 17, 2007; 104(29): 12205 - 12210. [Abstract] [Full Text] [PDF]

				A. Huffaker and C. A. Ryan Endogenous peptide defense signals in Arabidopsis differentially amplify signaling for the innate immune response PNAS, June 19, 2007; 104(25): 10732 - 10736. [Abstract] [Full Text] [PDF]

				S. Munemasa, K. Oda, M. Watanabe-Sugimoto, Y. Nakamura, Y. Shimoishi, and Y. Murata The coronatine-insensitive 1 Mutation Reveals the Hormonal Signaling Interaction between Abscisic Acid and Methyl Jasmonate in Arabidopsis Guard Cells. Specific Impairment of Ion Channel Activation and Second Messenger Production Plant Physiology, March 1, 2007; 143(3): 1398 - 1407. [Abstract] [Full Text] [PDF]

				I.-P. Ahn, S. Kim, Y.-H. Lee, and S.-C. Suh Vitamin B1-Induced Priming Is Dependent on Hydrogen Peroxide and the NPR1 Gene in Arabidopsis Plant Physiology, February 1, 2007; 143(2): 838 - 848. [Abstract] [Full Text] [PDF]

				J. Collen, C. Herve, I. Guisle-Marsollier, J. J. Leger, and C. Boyen Expression profiling of Chondrus crispus (Rhodophyta) after exposure to methyl jasmonate J. Exp. Bot., November 1, 2006; 57(14): 3869 - 3881. [Abstract] [Full Text] [PDF]

				X. Hu, A. Zhang, J. Zhang, and M. Jiang Abscisic Acid is a Key Inducer of Hydrogen Peroxide Production in Leaves of Maize Plants Exposed to Water Stress Plant Cell Physiol., November 1, 2006; 47(11): 1484 - 1495. [Abstract] [Full Text] [PDF]

				H. Maeda, W. Song, T. L. Sage, and D. DellaPenna Tocopherols Play a Crucial Role in Low-Temperature Adaptation and Phloem Loading in Arabidopsis PLANT CELL, October 1, 2006; 18(10): 2710 - 2732. [Abstract] [Full Text] [PDF]

				M. d. l. M. Dana, J. A. Pintor-Toro, and B. Cubero Transgenic Tobacco Plants Overexpressing Chitinases of Fungal Origin Show Enhanced Resistance to Biotic and Abiotic Stress Agents Plant Physiology, October 1, 2006; 142(2): 722 - 730. [Abstract] [Full Text] [PDF]

				K. Kojo, T. Yaeno, K. Kusumi, H. Matsumura, S. Fujisawa, R. Terauchi, and K. Iba Regulatory Mechanisms of ROI Generation are Affected by Rice spl Mutations Plant Cell Physiol., August 1, 2006; 47(8): 1035 - 1044. [Abstract] [Full Text] [PDF]

				A. Cona, G. Rea, M. Botta, F. Corelli, R. Federico, and R. Angelini Flavin-containing polyamine oxidase is a hydrogen peroxide source in the oxidative response to the protein phosphatase inhibitor cantharidin in Zea mays L. J. Exp. Bot., July 1, 2006; 57(10): 2277 - 2289. [Abstract] [Full Text] [PDF]

				J. M. Cheeseman Hydrogen peroxide concentrations in leaves under natural conditions J. Exp. Bot., July 1, 2006; 57(10): 2435 - 2444. [Abstract] [Full Text] [PDF]

				J. HIDEMA and T. KUMAGAI Sensitivity of Rice to Ultraviolet-B Radiation Ann. Bot., June 1, 2006; 97(6): 933 - 942. [Abstract] [Full Text] [PDF]

				M. Sagi and R. Fluhr Production of Reactive Oxygen Species by Plant NADPH Oxidases Plant Physiology, June 1, 2006; 141(2): 336 - 340. [Full Text] [PDF]

				P. M. Mullineaux, S. Karpinski, and N. R. Baker Spatial Dependence for Hydrogen Peroxide-Directed Signaling in Light-Stressed Plants Plant Physiology, June 1, 2006; 141(2): 346 - 350. [Full Text] [PDF]

				C. J. Song, I. Steinebrunner, X. Wang, S. C. Stout, and S. J. Roux Extracellular ATP Induces the Accumulation of Superoxide via NADPH Oxidases in Arabidopsis Plant Physiology, April 1, 2006; 140(4): 1222 - 1232. [Abstract] [Full Text] [PDF]

				T. Yaeno, B. Saito, T. Katsuki, and K. Iba Ozone-induced Expression of the Arabidopsis FAD7 Gene Requires Salicylic Acid, but not NPR1 and SID2 Plant Cell Physiol., March 1, 2006; 47(3): 355 - 362. [Abstract] [Full Text] [PDF]

				M. E. Maffei, A. Mithofer, G.-I. Arimura, H. Uchtenhagen, S. Bossi, C. M. Bertea, L. S. Cucuzza, M. Novero, V. Volpe, S. Quadro, et al. Effects of Feeding Spodoptera littoralis on Lima Bean Leaves. III. Membrane Depolarization and Involvement of Hydrogen Peroxide Plant Physiology, March 1, 2006; 140(3): 1022 - 1035. [Abstract] [Full Text] [PDF]

				Y. Lou and I. T. Baldwin Silencing of a Germin-Like Gene in Nicotiana attenuata Improves Performance of Native Herbivores Plant Physiology, March 1, 2006; 140(3): 1126 - 1136. [Abstract] [Full Text] [PDF]

				C. Yamamizo, K. Kuchimura, A. Kobayashi, S. Katou, K. Kawakita, J. D.G. Jones, N. Doke, and H. Yoshioka Rewiring Mitogen-Activated Protein Kinase Cascade by Positive Feedback Confers Potato Blight Resistance Plant Physiology, February 1, 2006; 140(2): 681 - 692. [Abstract] [Full Text] [PDF]

				T. RUUHOLA and S. YANG Wound-induced Oxidative Responses in Mountain Birch Leaves Ann. Bot., January 1, 2006; 97(1): 29 - 37. [Abstract] [Full Text] [PDF]

				R. S. Quilliam, P. J. Swarbrick, J. D. Scholes, and S. A. Rolfe Imaging photosynthesis in wounded leaves of Arabidopsis thaliana J. Exp. Bot., January 1, 2006; 57(1): 55 - 69. [Abstract] [Full Text] [PDF]

				L. A.J. Mur, P. Kenton, R. Atzorn, O. Miersch, and C. Wasternack The Outcomes of Concentration-Specific Interactions between Salicylate and Jasmonate Signaling Include Synergy, Antagonism, and Oxidative Stress Leading to Cell Death Plant Physiology, January 1, 2006; 140(1): 249 - 262. [Abstract] [Full Text] [PDF]

				S. Davletova, K. Schlauch, J. Coutu, and R. Mittler The Zinc-Finger Protein Zat12 Plays a Central Role in Reactive Oxygen and Abiotic Stress Signaling in Arabidopsis Plant Physiology, October 1, 2005; 139(2): 847 - 856. [Abstract] [Full Text] [PDF]

				B. A. Wolucka, A. Goossens, and D. Inze Methyl jasmonate stimulates the de novo biosynthesis of vitamin C in plant cell suspensions J. Exp. Bot., September 1, 2005; 56(419): 2527 - 2538. [Abstract] [Full Text] [PDF]

				N. Beffagna, B. Buffoli, and C. Busi Modulation of Reactive Oxygen Species Production During Osmotic Stress in Arabidopsis thaliana Cultured Cells: Involvement of the Plasma Membrane Ca2+-ATPase and H+-ATPase Plant Cell Physiol., August 1, 2005; 46(8): 1326 - 1339. [Abstract] [Full Text] [PDF]

				R. Shin, R. H. Berg, and D. P. Schachtman Reactive Oxygen Species and Root Hairs in Arabidopsis Root Response to Nitrogen, Phosphorus and Potassium Deficiency Plant Cell Physiol., August 1, 2005; 46(8): 1350 - 1357. [Abstract] [Full Text] [PDF]

				J. W. Wang and J. Y. Wu Nitric Oxide is Involved in Methyl Jasmonate-induced Defense Responses and Secondary Metabolism Activities of Taxus Cells Plant Cell Physiol., June 1, 2005; 46(6): 923 - 930. [Abstract] [Full Text] [PDF]

				J. H. Joo, S. Wang, J.G. Chen, A.M. Jones, and N. V. Fedoroff Different Signaling and Cell Death Roles of Heterotrimeric G Protein {alpha} and {beta} Subunits in the Arabidopsis Oxidative Stress Response to Ozone PLANT CELL, March 1, 2005; 17(3): 957 - 970. [Abstract] [Full Text] [PDF]

				C. Li, A. L. Schilmiller, G. Liu, G. I. Lee, S. Jayanty, C. Sageman, J. Vrebalov, J. J. Giovannoni, K. Yagi, Y. Kobayashi, et al. Role of {beta}-Oxidation in Jasmonate Biosynthesis and Systemic Wound Signaling in Tomato PLANT CELL, March 1, 2005; 17(3): 971 - 986. [Abstract] [Full Text] [PDF]

				O. Avsian-Kretchmer, Y. Gueta-Dahan, S. Lev-Yadun, R. Gollop, and G. Ben-Hayyim The Salt-Stress Signal Transduction Pathway That Activates the gpx1 Promoter Is Mediated by Intracellular H2O2, Different from the Pathway Induced by Extracellular H2O2 Plant Physiology, July 1, 2004; 135(3): 1685 - 1696. [Abstract] [Full Text] [PDF]

				R. Shin and D. P. Schachtman Hydrogen peroxide mediates plant root cell response to nutrient deprivation PNAS, June 8, 2004; 101(23): 8827 - 8832. [Abstract] [Full Text] [PDF]

				A. A. Rodriguez, A. R. Cordoba, L. Ortega, and E. Taleisnik Decreased reactive oxygen species concentration in the elongation zone contributes to the reduction in maize leaf growth under salinity J. Exp. Bot., June 1, 2004; 55(401): 1383 - 1390. [Abstract] [Full Text] [PDF]

				R. Shin, J.-M. An, C.-J. Park, Y. J. Kim, S. Joo, W. T. Kim, and K.-H. Paek Capsicum annuum Tobacco Mosaic Virus-Induced Clone 1 Expression Perturbation Alters the Plant's Response to Ethylene and Interferes with the Redox Homeostasis Plant Physiology, May 1, 2004; 135(1): 561 - 573. [Abstract] [Full Text] [PDF]

				M. Maffei, S. Bossi, D. Spiteller, A. Mithofer, and W. Boland Effects of Feeding Spodoptera littoralis on Lima Bean Leaves. I. Membrane Potentials, Intracellular Calcium Variations, Oral Secretions, and Regurgitate Components Plant Physiology, April 1, 2004; 134(4): 1752 - 1762. [Abstract] [Full Text] [PDF]

				M. Sagi, O. Davydov, S. Orazova, Z. Yesbergenova, R. Ophir, J. W. Stratmann, and R. Fluhr Plant Respiratory Burst Oxidase Homologs Impinge on Wound Responsiveness and Development in Lycopersicon esculentum PLANT CELL, March 1, 2004; 16(3): 616 - 628. [Abstract] [Full Text] [PDF]

				K. Zhu-Salzman, R. A. Salzman, J.-E. Ahn, and H. Koiwa Transcriptional Regulation of Sorghum Defense Determinants against a Phloem-Feeding Aphid Plant Physiology, January 1, 2004; 134(1): 420 - 431. [Abstract] [Full Text] [PDF]

				T. S. Babu, T. A. Akhtar, M. A. Lampi, S. Tripuranthakam, D. G. Dixon, and B. M. Greenberg Similar Stress Responses are Elicited by Copper and Ultraviolet Radiation in the Aquatic Plant Lemna gibba: Implication of Reactive Oxygen Species as Common Signals Plant Cell Physiol., December 15, 2003; 44(12): 1320 - 1329. [Abstract] [Full Text] [PDF]

				M. L. Orozco-Cardenas and C. A. Ryan Polygalacturonase {beta}-Subunit Antisense Gene Expression in Tomato Plants Leads to a Progressive Enhanced Wound Response and Necrosis in Leaves and Abscission of Developing Flowers Plant Physiology, October 1, 2003; 133(2): 693 - 701. [Abstract] [Full Text] [PDF]

				A. DEVOTO and J. G. TURNER Regulation of Jasmonate-mediated Plant Responses in Arabidopsis Ann. Bot., September 1, 2003; 92(3): 329 - 337. [Abstract] [Full Text] [PDF]

				G. Bloomfield and C. Pears Superoxide signalling required for multicellular development of Dictyostelium J. Cell Sci., August 15, 2003; 116(16): 3387 - 3397. [Abstract] [Full Text] [PDF]

				C. L. Ballare Stress Under the Sun: Spotlight on Ultraviolet-B Responses Plant Physiology, August 1, 2003; 132(4): 1725 - 1727. [Full Text] [PDF]

				M. M. Izaguirre, A. L. Scopel, I. T. Baldwin, and C. L. Ballare Convergent Responses to Stress. Solar Ultraviolet-B Radiation and Manduca sexta Herbivory Elicit Overlapping Transcriptional Responses in Field-Grown Plants of Nicotiana longiflora Plant Physiology, August 1, 2003; 132(4): 1755 - 1767. [Abstract] [Full Text] [PDF]

				C. Brehelin, E. H. Meyer, J.-P. de Souris, G. Bonnard, and Y. Meyer Resemblance and Dissemblance of Arabidopsis Type II Peroxiredoxins: Similar Sequences for Divergent Gene Expression, Protein Localization, and Activity Plant Physiology, August 1, 2003; 132(4): 2045 - 2057. [Abstract] [Full Text] [PDF]

				S. R. Holley, R. D. Yalamanchili, D. S. Moura, C. A. Ryan, and J. W. Stratmann Convergence of Signaling Pathways Induced by Systemin, Oligosaccharide Elicitors, and Ultraviolet-B Radiation at the Level of Mitogen-Activated Protein Kinases in Lycopersicon peruvianum Suspension-Cultured Cells Plant Physiology, August 1, 2003; 132(4): 1728 - 1738. [Abstract] [Full Text] [PDF]

				J. E. Dombrowski Salt Stress Activation of Wound-Related Genes in Tomato Plants Plant Physiology, August 1, 2003; 132(4): 2098 - 2107. [Abstract] [Full Text] [PDF]

				C. Li, G. Liu, C. Xu, G. I. Lee, P. Bauer, H.-Q. Ling, M. W. Ganal, and G. A. Howe The Tomato Suppressor of prosystemin-mediated responses2 Gene Encodes a Fatty Acid Desaturase Required for the Biosynthesis of Jasmonic Acid and the Production of a Systemic Wound Signal for Defense Gene Expression PLANT CELL, July 1, 2003; 15(7): 1646 - 1661. [Abstract] [Full Text] [PDF]

				P.-J. Jih, Y.-C. Chen, and S.-T. Jeng Involvement of Hydrogen Peroxide and Nitric Oxide in Expression of the Ipomoelin Gene from Sweet Potato Plant Physiology, May 1, 2003; 132(1): 381 - 389. [Abstract] [Full Text] [PDF]

				H. R. Lascano, L. M. Casano, M. Martin, and B. Sabater The Activity of the Chloroplastic Ndh Complex Is Regulated by Phosphorylation of the NDH-F Subunit Plant Physiology, May 1, 2003; 132(1): 256 - 262. [Abstract] [Full Text] [PDF]

				R. Halitschke, K. Gase, D. Hui, D. D. Schmidt, and I. T. Baldwin Molecular Interactions between the Specialist Herbivore Manduca sexta (Lepidoptera, Sphingidae) and Its Natural Host Nicotiana attenuata. VI. Microarray Analysis Reveals That Most Herbivore-Specific Transcriptional Changes Are Mediated by Fatty Acid-Amino Acid Conjugates Plant Physiology, April 1, 2003; 131(4): 1894 - 1902. [Abstract] [Full Text] [PDF]

				M. Jiang and J. Zhang Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves J. Exp. Bot., December 1, 2002; 53(379): 2401 - 2410. [Abstract] [Full Text] [PDF]

				M. Mino, K. Maekawa, K.'i. Ogawa, H. Yamagishi, and M. Inoue Cell Death Processes during Expression of Hybrid Lethality in Interspecific F1 Hybrid between Nicotiana gossei Domin and Nicotiana tabacum Plant Physiology, December 1, 2002; 130(4): 1776 - 1787. [Abstract] [Full Text] [PDF]

				J. Narvaez-Vasquez and C. A. Ryan Jr. The systemin precursor gene regulates both defensive and developmental genes in Solanum tuberosum PNAS, November 26, 2002; 99(24): 15818 - 15821. [Abstract] [Full Text] [PDF]

				M. A. Samuel and B. E. Ellis Double Jeopardy: Both Overexpression and Suppression of a Redox-Activated Plant Mitogen-Activated Protein Kinase Render Tobacco Plants Ozone Sensitive PLANT CELL, September 1, 2002; 14(9): 2059 - 2069. [Abstract] [Full Text] [PDF]

				M. L. Orozco-Cardenas and C. A. Ryan Nitric Oxide Negatively Modulates Wound Signaling in Tomato Plants Plant Physiology, September 1, 2002; 130(1): 487 - 493. [Abstract] [Full Text] [PDF]

				R. D. Yalamanchili and J. W. Stratmann Ultraviolet-B Activates Components of the Systemin Signaling Pathway in Lycopersicon peruvianum Suspension-cultured Cells J. Biol. Chem., August 2, 2002; 277(32): 28424 - 28430. [Abstract] [Full Text] [PDF]

				A. A. Rodriguez, K. A. Grunberg, and E. L. Taleisnik Reactive Oxygen Species in the Elongation Zone of Maize Leaves Are Necessary for Leaf Extension Plant Physiology, August 1, 2002; 129(4): 1627 - 1632. [Abstract] [Full Text] [PDF]

				J. Diaz, A. ten Have, and J. A.L. van Kan The Role of Ethylene and Wound Signaling in Resistance of Tomato to Botrytis cinerea Plant Physiology, July 1, 2002; 129(3): 1341 - 1351. [Abstract] [Full Text] [PDF]

				G. NOCTOR, S. VELJOVIC-JOVANOVIC, S. DRISCOLL, L. NOVITSKAYA, and C. H. FOYER Drought and Oxidative Load in the Leaves of C3 Plants: a Predominant Role for Photorespiration? Ann. Bot., June 15, 2002; 89(7): 841 - 850. [Abstract] [Full Text] [PDF]

				Y. H. Cheong, H.-S. Chang, R. Gupta, X. Wang, T. Zhu, and S. Luan Transcriptional Profiling Reveals Novel Interactions between Wounding, Pathogen, Abiotic Stress, and Hormonal Responses in Arabidopsis Plant Physiology, June 1, 2002; 129(2): 661 - 677. [Abstract] [Full Text] [PDF]

				E. Vranova, D. Inze, and F. Van Breusegem Signal transduction during oxidative stress J. Exp. Bot., May 15, 2002; 53(372): 1227 - 1236. [Abstract] [Full Text] [PDF]

				C. A. Ryan and D. S. Moura Systemic wound signaling in plants: A new perception PNAS, May 14, 2002; 99(10): 6519 - 6520. [Full Text] [PDF]

				J. G. Turner, C. Ellis, and A. Devoto The Jasmonate Signal Pathway PLANT CELL, May 1, 2002; 14(90001): S153 - 164. [Full Text] [PDF]

				L. Li, C. Li, G. I. Lee, and G. A. Howe Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato PNAS, April 30, 2002; 99(9): 6416 - 6421. [Abstract] [Full Text] [PDF]

				T. Yang and B. W. Poovaiah Hydrogen peroxide homeostasis: Activation of plant catalase by calcium/calmodulin PNAS, March 19, 2002; 99(6): 4097 - 4102. [Abstract] [Full Text] [PDF]

				J. Leon, J. Royo, G. Vancanneyt, C. Sanz, H. Silkowski, G. Griffiths, and J. J. Sanchez-Serrano Lipoxygenase H1 Gene Silencing Reveals a Specific Role in Supplying Fatty Acid Hydroperoxides for Aliphatic Aldehyde Production J. Biol. Chem., January 4, 2002; 277(1): 416 - 423. [Abstract] [Full Text]

				J. M. Chico, M. Raices, M. T. Tellez-Inon, and R. M. Ulloa A Calcium-Dependent Protein Kinase Is Systemically Induced upon Wounding in Tomato Plants Plant Physiology, January 1, 2002; 128(1): 256 - 270. [Abstract] [Full Text] [PDF]

				L. Li, C. Li, and G. A. Howe Genetic Analysis of Wound Signaling in Tomato. Evidence for a Dual Role of Jasmonic Acid in Defense and Female Fertility Plant Physiology, December 1, 2001; 127(4): 1414 - 1417. [Full Text] [PDF]

				M. Jiang and J. Zhang Effect of Abscisic Acid on Active Oxygen Species, Antioxidative Defence System and Oxidative Damage in Leaves of Maize Seedlings Plant Cell Physiol., November 1, 2001; 42(11): 1265 - 1273. [Abstract] [Full Text] [PDF]