Karrikins Discovered in Smoke Trigger Arabidopsis Seed Germination by a Mechanism Requiring Gibberellic Acid Synthesis and Light

Discovery of the primary seed germination stimulant in smoke, 3-methyl-2H-furo[2,3-c]pyran-2-one (KAR1), has resulted inidentification of a family of structurally related plant growth regulators, karrikins. KAR1 acts as a key germination trigger formany species from fire-prone, Mediterranean climates, but a molecular mechanism for this response remains unknown. Wedemonstrate that Arabidopsis (Arabidopsis thaliana), an ephemeral of the temperate northern hemisphere that has never, to ourknowledge, been reported to be responsive to fire or smoke, rapidly and sensitively perceives karrikins. Thus, these signalingmolecules may have greater significance among angiosperms than previously realized. Karrikins can trigger germination ofprimary dormant Arabidopsis seeds far more effectively than known phytohormones or the structurally related strigolactoneGR-24. Natural variation and depth of seed dormancy affect the degree of KAR1 stimulation. Analysis of phytohormonemutant germination reveals suppression of KAR1 responses by abscisic acid and a requirement for gibberellin (GA) synthesis.The reduced germination of sleepy1 mutants is partially recovered by KAR1, which suggests that germination enhancement bykarrikin is only partly DELLA dependent. While KAR1 has little effect on sensitivity to exogenous GA, it enhances expressionof the GA biosynthetic genes GA3ox1 and GA3ox2 during seed imbibition. Neither abscisic acid nor GA levels in seed areappreciably affected by KAR1 treatment prior to radicle emergence, despite marked differences in germination outcome. KAR1stimulation of Arabidopsis germination is light-dependent and reversible by far-red exposure, although limited induction ofGA3ox1 still occurs in the dark. The observed requirements for light and GA biosynthesis provide the first insights into thekarrikin mode of action.