The complex origins of strigolactone signalling in land plants

Strigolactones (SLs) are a class of plant hormones that control many aspects of plant growth. The SL signaling mechanism is homologous to that of karrikins (KARs), a smoke-derived compounds that stimulate seed germination. In angiosperms, the SL receptor is an α/β hydrolase known as DWARF14 (D14); its close homologue, KARRIKIN INSENSITIVE2 (KAI2), functions as a KAR receptor, and likely recognizes an uncharacterized, endogenous signal. Previous phylogenetic analyses have suggested that the KAI2 lineage is ancestral in land plants, and that canonical D14-type SL receptors only arose in seed plants; this is paradoxical, however, as non-vascular plants synthesize and respond to SLs. Here, we have used a combination of phylogenetic and structural approaches to understand the evolution of the D14/KAI2 family in land plants. We analyzed 339 members of the D14/KAI2 family from land plants and charophyte algae. Our phylogenetic analyses show that the divergence between the eu-KAI2 clade and the DDK (D14/DLK2/KAI2) clade occurred very early in land plant evolution. We identify characteristic structural features of D14 and KAI2 proteins, and show that the earliest members of the DDK lineage structurally resemble KAI2, and not D14 proteins. We also show that proteins in the KAI2 lineage have exceptional sequence conservation across land plants. Our results suggest that SL perception has relatively relaxed structural requirements, and that the evolution from KAI2-like to D14-like protein structure in the DDK lineage may have been driven by interactions with protein partners, rather than being required for SL perception itself.