Abstract
Karrikins (KARs), smoke-derived butenolides, are perceived by the α/β-fold hydrolase KARRIKIN INSENSITIVE2 (KAI2) and thought to mimic endogenous, yet elusive plant hormones tentatively called KAI2-ligands (KLs). The sensitivity to different karrikin types as well as the number of KAI2 paralogs varies among plant species, suggesting diversification and co-evolution of ligand-receptor relationships. We found that the genomes of legumes, comprising a number of important crops with protein-rich, nutritious seed, contain two or more KAI2 copies. We uncover sub-functionalization of the two KAI2 versions in the model legume Lotus japonicus and demonstrate differences in their ability to bind the synthetic ligand GR24ent-5DS in vitro and in genetic assays with Lotus japonicus and the heterologous Arabidopsis thaliana background. These differences can be explained by the exchange of a widely conserved phenylalanine in the binding pocket of KAI2a with a tryptophan in KAI2b, which arose independently in KAI2 proteins of several unrelated angiosperms. Furthermore, two polymorphic residues in the binding pocket are conserved across a number of legumes and may contribute to ligand binding preferences. The diversification of KAI2 binding pockets suggests the occurrence of several different KLs acting in non-fire following plants, or an escape from possible antagonistic exogenous molecules. Unexpectedly, L. japonicus responds to diverse synthetic KAI2-ligands in an organ-specific manner. Hypocotyl growth responds to KAR1, KAR2 and rac-GR24, while root system development responds only to KAR1. This differential responsiveness cannot be explained by receptor-ligand preferences alone, because LjKAI2a is sufficient for karrikin responses in the hypocotyl, while LjKAI2a and LjKAI2b operate redundantly in roots. Instead, it likely reflects differences between plant organs in their ability to transport or metabolise the synthetic KLs. Our findings provide new insights into the evolution and diversity of butenolide ligand-receptor relationships, and open novel research avenues into their ecological significance and the mechanisms controlling developmental responses to divergent KLs.
Highlights
Karrikins (KARs) are small butenolide compounds derived from smoke of burning vegetation that were identified as germination stimulants of fire-following plants [1]
The most recently discovered plant hormone receptor KARRIKIN INSENSITVE 2 (KAI2), binds a small butenolide called karrikin that was discovered in smoke and induces germination of fire-following plants
We report that genomes of species in the legume hologalegina clade encode two KARRIKIN INSENSITIVE2 (KAI2) versions
Summary
Karrikins (KARs) are small butenolide compounds derived from smoke of burning vegetation that were identified as germination stimulants of fire-following plants [1]. There are six known KARs, of which KAR1 is most abundant in smoke-water and most active on seed germination of fire-following plants [1,10,11], but Arabidopsis responds more strongly to KAR2, which lacks the methyl group at the butenolide ring that is characteristic for KAR1 [2,3,11]. The rice orthologs of KAI2 (D14-LIKE) and MAX2 (D3) are essential for root colonization by arbuscular mycorrhiza (AM) fungi, and are involved in regulating mesocotyl elongation [7,16,17] These roles of KAI2, unrelated to smoke and seed germination, suggest that karrikins mimic yet-unknown endogenous (and possibly AM fungus-derived) signaling molecules that bind to KAI2 to regulate plant development or AM symbiosis, and are provisionally called KAI2-ligands (KLs) [12,18]
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