Abstract
Watermelon is an economically important horticultural crop cultivated worldwide. The ERF family is one of the largest transcription factor families in plants and plays an extensive role in regulating growth, development, hormone signaling, and stress responses. Although the ERF family has been characterized in various plant species, it remains unexplored in watermelon. In this study, we identified 118 ClERF family members in Citrullus lanatus and classified them into ten subgroups. We conducted comprehensive analyses of their physicochemical properties, evolutionary relationships, chromosomal locations, collinearity, gene structures, conserved motifs, and promoter cis-regulatory elements. Furthermore, we comprehensively analyzed the expression patterns of subgroup VIII genes and transcriptional responses to abiotic stresses (cold, salt), a biotic stress (Fusarium wilt), and hormone treatments (ABA, MeJA, SA, BR and ETH). Crucially, functional analysis demonstrated that overexpression of ClERF054 significantly enhanced plant susceptibility to cold and salt stresses. This research establishes a theoretical foundation for understanding the ClERF gene family in watermelon and provides important insights into the functional divergence of subgroup VIII members in hormone signaling and biotic/abiotic stress responses, while also facilitating investigations into the regulatory mechanisms of ClERF054 under cold and salt stresses. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-025-07867-y.