Identification of genes regulated by a jasmonate- and salt-inducible transcription factor JRE3 in tomato

In Solanum lycoperisicum (tomato), a transcription factor of APETALA2/ETHYLENE RESPONSE FACTOR (AP2/ERF) family, JASMONATE-RESPONSIVE ERF 3 (JRE3), is a closest homolog of JRE4, a master transcriptional regulator of steroidal glycoalkaloid (SGA) biosynthesis. In tomato genome, JRE3 resides in a gene cluster with JRE4 and related JRE1, JRE2, and JRE5, while JRE6 exists as a singleton on a different chromosome. All of the JREs are induced by jasmonates (JAs), whereas sodium chloride (NaCl) treatment drastically increases the expression of the JREs except for JRE4 and JRE6. In this study, to get insights into the regulatory function of the JA- and NaCl-inducible JRE3, a series of genes upregulated by beta-estradiol-induced overexpression of JRE3 are identified with microarray analysis in transgenic tomato hairy roots. No gene involved in the SGA pathway has been identified through the screening, confirming the functional distinction between JRE3 and JRE4. Among the JRE3-regulated genes, we characterize the stress-induced expression of genes encoding malate synthase and tonoplast dicarboxylate transporter both involved in malate accumulation. In transient transactivation assay, we reveal that both terminal regions of JRE4, but not a central DNA-binding domain, are indispensable for the induction of a gene involved in the JRE4 regulon. Functional differentiation of the JREs is discussed.