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PLIP lipases can initiate jasmonic acid (JA) biosynthesis. However, little is known about the transcriptional regulation of this process. In this study, an ERF transcription factor (CsESE3) was found to be co-expressed with all necessary genes for JA biosynthesis and several key genes for wax biosynthesis in transcriptomes of ‘Newhall’ navel orange. CsESE3shows partial sequence similarity to the well-known wax regulator SHINEs (SHNs), but lacks a complete MM protein domain. Ectopic overexpression of CsESE3in tomato (OE) resulted in reduction of fruit surface brightness and dwarf phenotype compared to the wild type. The OE tomato lines also showed significant increases in the content of wax and JA and the expression of key genes related to their biosynthesis. Overexpression of CsESE3in citrus callus and fruit enhanced the JA content and the expression of JA biosynthetic genes. Furthermore, CsESE3could bind to and activate the promoters of two phospholipases from the PLIP gene family to initiate JA biosynthesis. Overall, this study indicated that CsESE3could mediate JA biosynthesis by activating PLIPgenes and positively modulate wax biosynthesis. The findings provide important insights into the coordinated control of two defense strategies of plants represented by wax and JA biosynthesis.