Modification of the plant cell wall components is crucial during plant development and stress response. The polysaccharide pectin and its derivative pectate acid are targets of various cell wall remodelling enzymes. Here, we characterise the PECTATE LYASE-LIKE 21 (PLL21) gene in Arabidopsis thaliana, identified from a screen for downstream targets of karrikin signalling. PLL21 transcripts are negatively regulated by karrikins in a KAI2- and SMAX1-dependent manner. Knockout mutants of PLL21 exhibit elongated hypocotyls, reduced secondary branching, and an early flowering phenotype. Among the 26 PLL genes of Arabidopsis, we find that AtPLL1 and AtPLL2 form a distinct clade with microbial homologues, while AtPLL3 through AtPLL26 belong to a plant-specific clade. The monophyletic nesting of plant PLL genes within microbial PLLs suggests a horizontal gene transfer event in the ancestor of land plants and Zygnematophyceae. We identified a structural motif unique to plant-specific PLLs consistent with post-transfer functional diversification. Interestingly, this set of PLLs is completely absent in hornworts, which are known for their unique pectin side chains. This result may shed light on the substrate specificity of these PLLs, suggesting that their evolution is linked to specific pectin modifications found in higher plants. The plant-specific PLLs are implicated in diverse functions, including pollen germination, vascular development and responses to biotic stress. Our study reveals that the AtPLL21 clade plays a role in KAI2-dependent photomorphogenesis, contributing to our understanding of hormonal signalling, cell wall remodelling and the evolutionary history of PLL genes.