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Regulation of a Virus-Induced Lethal Disease in Tomato Revealed by LongSAGE Analysis

Infection of Cucumber mosaic virus (CMV) and D satellite RNA (satRNA) in tomato plants induces rapid plant death, which has caused catastrophic crop losses. We conducted long serial analysis of gene expression (LongSAGE) in control and virus-infected plants to identify the genes that may be involved in the development of this lethal tomato disease. The transcriptomes were compared between mock-inoculated plants and plants infected with CMV, CMV/D satRNA, or CMV/Dm satRNA (a nonnecrogenic mutant of D satRNA with three mutated nucleotides). The analysis revealed both general and specific changes in the tomato transcriptome after infection with these viruses. A massive transcriptional difference of approximately 400 genes was found between the transcriptomes of CMV/D and CMV/Dm satRNA-infected plants. Particularly, the Long-SAGE data indicated the activation of ethylene synthesis and signaling by CMV/D satRNA infection. Results from inoculation tests with an ethylene-insensitive mutant and treatments with an ethylene action inhibitor further confirmed the role of ethylene in mediating the epinastic leaf symptoms and the secondary cell death in the stem. Results from Northern blot analysis demonstrated the partial contribution of ethylene in the induced defense responses in CMV/D satRNA-infected plants.