Independent horizontal transfer of genes encoding α/β-hydrolases with strigolactone binding and hydrolytic activities from bacteria to fungi and plants.

Abstract

Strigolactones (SLs) are not only phytohormones that influence multiple aspects of plant growth and development, but also signaling molecules for interactions between plants and certain fungi or bacteria. In plants, the SL receptor is an α/β-hydrolase (ABH) encoded by the D14/KAI2 gene family, which is known to be derived from proteobacterial RsbQ through horizontal gene transfer (HGT). In the phytopathogenic fungus Cryphonectria parasitica, another ABH named CpD14 was found to possess SL binding and hydrolytic activities and mediate SL responses, exhibiting potential SL perception functions. Here, we demonstrate that CpD14 and its homologs in Leotiomyceta fungi were derived from actinobacteria through an independent HGT event, forming a distinct CpD14-like (CDL) family across fungi and bacteria. X-ray crystallography and structural analyses reveal that actinobacterial and fungal CDL proteins share a conserved core 'α/β fold' domain with D14/KAI2/RsbQ but possess a unique lid domain. Biochemical assays show that both actinobacterial CDL and proteobacterial RsbQ can recognize and hydrolyze SLs, suggesting that they are pre-adapted for SL responses and potential perception. Plant D14/KAI2 and fungal CDL proteins retained these functional activities while evolving distinct ligand specificities for SL structural variants. This work reveals that independent HGT events from two bacterial groups apparently provided plants and their interacting fungi with pre-adapted ABH proteins which were deployed for SL perception or responses.