Song_2026_Int.J.Mol.Sci_27_

De-S-acylation enzymes mediate the reversible S-acylation cycle and play critical roles in plant development and stress responses. However, the precise origin and evolutionary dynamics of this gene family in plants remain poorly understood. In this study, a total of 718 ABAPT genes were identified across 73 plant genomes, including 622 ABHD17 and 96 ABHD13 homologs, which share only a 20-30% conserved sequence identity between them. We further performed comprehensive analyses of gene duplication and structure, protein properties, synteny networks, and expression profiles to establish a systematic framework by classifying ABAPT genes in land plants. Our results revealed that ABHD13 genes have been retained as a single copy in most angiosperm genomes, whereas ABHD17 genes have undergone extensive expansion. ABAPT genes formed three major evolutionary clades: Clade 1 contained ABHD13 homologs, while Clades 2 and 3 harbored ABHD17 homologs. The three clades showed distinct disparities in intron-exon structural patterns and IDR properties. Phylogenomic synteny network analyses revealed the deeply conserved genomic syntenies within each of the six ABAPT subclades among the three clades, while Cluster4-Monocot was more dynamic and showed distinct lineage-specific duplication patterns restricted to Poaceae. ABHD13s exhibited constitutive expression patterns, while the tissue-specific expression genes were predominantly found within the ABHD17s subfamily. Notably, the ABAPT8/9 subgroups were specifically expressed in reproductive organs, and the weighted gene co-expression network identified specific groups to find ABAPT-specific regulatory features, implying the presence of potential modules for the protein S-acylation cycle during pollen development. Additionally, our results suggested that C-terminal Cys-rich region was required for ABAPT10 localization. Altogether, this study sheds light on the evolutionary divergence of the ABAPT subclades across major green plant lineages and emphasizes the need for future functional characterizations.