Comprehensive Characterization of B-Box Zinc Finger Genes in Citrullus lanatus and Their Response to Hormone and Abiotic Stresses

Plant B-BOX (BBX) zinc finger transcription factors play crucial roles in growth and development and the stress response. Although the BBX family has been characterized in various plants, systematic analysis in watermelon is still lacking. In this study, 25 watermelon ClBBX genes were identified. ClBBXs were grouped into five clades (Clade I, II, III, IV, and V) based on their conserved domains and phylogenetic relationships. Most of the ClBBXs (84%) might be localized in the nuclei or cytoplasm. The classification of ClBBXs was consistent with their gene structures. They were unevenly distributed in nine chromosomes except for Chr4 and Chr10, with the largest number of six members in Chr2. Segmental duplications were the major factor in ClBBX family expansion. Some BBXs of watermelon and Arabidopsis evolved from a common ancestor. In total, 254 hormonal and stress-responsive cis elements were discovered in ClBBX promoters. ClBBXs were differentially expressed in tissues, and the expression levels of ClBBX15 and 16 were higher in aboveground tissues than in roots, while the patterns of ClBBX21a, 21b, 21c, 28 and 30b were the opposite. With salicylic acid, methyl jasmonate and salt stress conditions, 17, 18 and 18 ClBBXs exhibited significant expression changes, respectively. In addition, many ClBBXs, including ClBBX29b, 30a and 30b, were also responsive to cold and osmotic stress. In summary, the simultaneous response of multiple ClBBXs to hormonal or abiotic stress suggests that they may have functional interactions in the stress hormone network. Clarifying the roles of key ClBBXs in transcriptional regulation and mediating protein interactions will be an important task. Our comprehensive characterization of the watermelon ClBBX family provides vital clues for the in-depth analysis of their biological functions in stress and hormone signaling pathways.