Suppressors of Systemin Signaling Identify Genes in the Tomato Wound Response Pathway

Corresponding author: Gregg A. Howe, DOE-Plant Research Laboratory, Michigan State University, S-206 Plant Biology Bldg., East Lansing, MI 48824., howeg{at}pilot.msu.edu (E-mail)

Communicating editor: V. L. CHANDLER

In tomato plants, systemic induction of defense genes in response to herbivory or mechanical wounding is regulated by an 18-amino-acid peptide signal called systemin. Transgenic plants that overexpress prosystemin, the systemin precursor, from a 35S::prosystemin (35S::prosys) transgene exhibit constitutive expression of wound-inducible defense proteins including proteinase inhibitors and polyphenol oxidase. To study further the role of (pro)systemin in the wound response pathway, we isolated and characterized mutations that suppress 35S::prosys-mediated phenotypes. Ten recessive, extragenic suppressors were identified. Two of these define new alleles of def-1, a previously identified mutation that blocks both wound- and systemin-induced gene expression and renders plants susceptible to herbivory. The remaining mutants defined four loci designated Spr-1, Spr-2, Spr-3, and Spr-4 (for Suppressed in 35S::prosystemin-mediated responses). spr-3 and spr-4 mutants were not significantly affected in their response to either systemin or mechanical wounding. In contrast, spr-1 and spr-2 plants lacked systemic wound responses and were insensitive to systemin. These results confirm the function of (pro)systemin in the transduction of systemic wound signals and further establish that wounding, systemin, and 35S::prosys induce defensive gene expression through a common signaling pathway defined by at least three genes (Def-1, Spr-1, and Spr-2).

This article has been cited by other articles:

				Z. Deng, X. Zhang, W. Tang, J. A. Oses-Prieto, N. Suzuki, J. M. Gendron, H. Chen, S. Guan, R. J. Chalkley, T. K. Peterman, et al. A Proteomics Study of Brassinosteroid Response in Arabidopsis Mol. Cell. Proteomics, December 1, 2007; 6(12): 2058 - 2071. [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]

				G. Pearce, W. F. Siems, R. Bhattacharya, Y.-C. Chen, and C. A. Ryan Three Hydroxyproline-rich Glycopeptides Derived from a Single Petunia Polyprotein Precursor Activate defensin I, a Pathogen Defense Response Gene J. Biol. Chem., June 15, 2007; 282(24): 17777 - 17784. [Abstract] [Full Text] [PDF]

				N. Holton, A. Cano-Delgado, K. Harrison, T. Montoya, J. Chory, and G. J. Bishop Tomato BRASSINOSTEROID INSENSITIVE1 Is Required for Systemin-Induced Root Elongation in Solanum pimpinellifolium but Is Not Essential for Wound Signaling PLANT CELL, May 1, 2007; 19(5): 1709 - 1717. [Abstract] [Full Text] [PDF]

				C. Li, J. Zhao, H. Jiang, X. Wu, J. Sun, C. Zhang, X. Wang, Y. Lou, and C. Li The Wound Response Mutant suppressor of prosystemin-mediated responses6 (spr6) is a Weak Allele of the Tomato Homolog of CORONATINE-INSENSITIVE1 (COI1) Plant Cell Physiol., May 1, 2006; 47(5): 653 - 663. [Abstract] [Full Text] [PDF]

				K. Ament, M. R. Kant, M. W. Sabelis, M. A. Haring, and R. C. Schuurink Jasmonic Acid Is a Key Regulator of Spider Mite-Induced Volatile Terpenoid and Methyl Salicylate Emission in Tomato Plant Physiology, August 1, 2004; 135(4): 2025 - 2037. [Abstract] [Full Text] [PDF]

				M. Boter, O. Ruiz-Rivero, A. Abdeen, and S. Prat Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis Genes & Dev., July 1, 2004; 18(13): 1577 - 1591. [Abstract] [Full Text] [PDF]

				L. Li, Y. Zhao, B. C. McCaig, B. A. Wingerd, J. Wang, M. E. Whalon, E. Pichersky, and G. A. Howe The Tomato Homolog of CORONATINE-INSENSITIVE1 Is Required for the Maternal Control of Seed Maturation, Jasmonate-Signaled Defense Responses, and Glandular Trichome Development PLANT CELL, January 1, 2004; 16(1): 126 - 143. [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]

				C. Li, M. M. Williams, Y.-T. Loh, G. I. Lee, and G. A. Howe Resistance of Cultivated Tomato to Cell Content-Feeding Herbivores Is Regulated by the Octadecanoid-Signaling Pathway Plant Physiology, September 1, 2002; 130(1): 494 - 503. [Abstract] [Full Text] [PDF]

				J. C. Schultz Shared Signals and the Potential for Phylogenetic Espionage Between Plants and Animals Integr. Comp. Biol., July 1, 2002; 42(3): 454 - 462. [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]

				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]

				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]

				J. Leon, E. Rojo, and J. J. Sanchez-Serrano Wound signalling in plants J. Exp. Bot., January 1, 2001; 52(354): 1 - 9. [Abstract] [Full Text] [PDF]

				G. A. Howe, G. I. Lee, A. Itoh, L. Li, and A. E. DeRocher Cytochrome P450-Dependent Metabolism of Oxylipins in Tomato. Cloning and Expression of Allene Oxide Synthase and Fatty Acid Hydroperoxide Lyase Plant Physiology, June 1, 2000; 123(2): 711 - 724. [Abstract] [Full Text]

				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]