Bao Wang, Qingzhe Zhai, Chuanyou Li, Jiaqiang Sun, Le Kang, Tingting Huang, Jianing Wei, Chang Bao Li, Shuyu Li, Liuhua Yan, and Minmin Du
In response to insect attack and mechanical wounding, plants activate the expression of genes involved in various defense-related processes. A fascinating feature of these inducible defenses is their occurrence both locally at the wounding site and systemically in undamaged leaves throughout the plant. Wound-inducible proteinase inhibitors (PIs) in tomato (Solanum lycopersicum) provide an attractive model to understand the signal transduction events leading from localized injury to the systemic expression of defense-related genes. Among the identified intercellular molecules in regulating systemic wound response of tomato are the peptide signal systemin and the oxylipin signal jasmonic acid (JA). The systemin/JA signaling pathway provides a unique opportunity to investigate, in a single experimental system, the mechanism by which peptide and oxylipin signals interact to coordinate plant systemic immunity. Here we describe the characterization of the tomato suppressor of prosystemin-mediated responses8 (spr8) mutant, which was isolated as a suppressor of (pro)systemin-mediated signaling. spr8 plants exhibit a series of JA-dependent immune deficiencies, including the inability to express wound-responsive genes, abnormal development of glandular trichomes, and severely compromised resistance to cotton bollworm (Helicoverpa armigera) and Botrytis cinerea. Map-based cloning studies demonstrate that the spr8 mutant phenotype results from a point mutation in the catalytic domain of TomLoxD, a chloroplast-localized lipoxygenase involved in JA biosynthesis. We present evidence that overexpression of TomLoxD leads to elevated wound-induced JA biosynthesis, increased expression of wound-responsive genes and, therefore, enhanced resistance to insect herbivory attack and necrotrophic pathogen infection. These results indicate that TomLoxD is involved in wound-induced JA biosynthesis and highlight the application potential of this gene for crop protection against insects and pathogens., Author Summary Plants have evolved sophisticated strategies to defend themselves against insect attack. Wound-inducible proteinase inhibitors (PIs) in tomato (Solanum lycopersicum) provide an attractive model to understand the signal transduction events leading from localized injury to the systemic expression of defense-related genes. A wealth of evidence indicates that the peptide signal systemin and the phytohormone jasmonic acid (JA) work together in the same signaling pathway to activate the expression of PIs and other defense-related genes. We have been using a genetic approach to dissect the systemin/JA signaling pathway and to discover important genes that can be used for crop protection. Here we report the characterization of the suppressor of prosystemin-mediated responses8 (spr8) mutant, which is defective in wound-induced defense gene expression and therefore is more susceptible to insect attack. We demonstrate that spr8 defines the TomLoxD gene, which encodes a chloroplast-localized lipoxygenase involved in wound-induced JA biosynthesis. Further, we demonstrate that genetic manipulation of Spr8/TomLoxD leads to increased plant resistance against insect attack and pathogen infection.