The differentiation of water-conducting tracheary elements (TEs) is the result of the orchestrated construction of secondary wall structure, including lignification, and programmed cell death (PCD), including cellular autolysis. To understand the orchestrated regulation of differentiation of TEs, we investigated the regulatory mechanism of gene expression directing TE differentiation. Detailed loss-of-function and gain-of-function analyses of the ZCP4 (Zinniacysteine protease 4) promoter, which confers TE-specific expression, demonstrated that a novel 11-bp cis-element is necessary and sufficient for the immature TE-specific promoter activity. The 11-bp cis-element-like sequences were found in promoters of many Arabidopsis TE differentiation-related genes. A gain-of-function analysis with similar putative cis-elements from secondary wall formation or modification-related genes as well as PCD-related genes indicated that the cis-elements are also sufficient for TE-specific expression of genes. These results demonstrate that a common sequence, designated as the tracheary-element-regulating cis-element, confers TE-specific expression to both genes related to secondary wall formation or modification and PCD.