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First published online December 12, 2008; 10.1104/pp.108.131516

Plant Physiology 149:863-873 (2009)
© 2009 American Society of Plant Biologists

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DEVELOPMENT AND HORMONE ACTION

Karrikins Discovered in Smoke Trigger Arabidopsis Seed Germination by a Mechanism Requiring Gibberellic Acid Synthesis and Light1,[W],[OA]

David C. Nelson, Julie-Anne Riseborough, Gavin R. Flematti, Jason Stevens, Emilio L. Ghisalberti, Kingsley W. Dixon and Steven M. Smith*

Plant Energy Biology (D.C.N., J.-A.R., S.M.S.), Plant Biology (J.-A.R., K.W.D.), and Biomedical, Biomolecular, and Chemical Sciences (G.R.F., E.L.G., S.M.S.), University of Western Australia, Crawley, Western Australia 6009, Australia; and Kings Park and Botanic Garden, West Perth, Western Australia 6005, Australia (J.S., K.W.D.)

Discovery of the primary seed germination stimulant in smoke, 3-methyl-2H-furo[2,3-c]pyran-2-one (KAR1), has resulted in identification of a family of structurally related plant growth regulators, karrikins. KAR1 acts as a key germination trigger for many species from fire-prone, Mediterranean climates, but a molecular mechanism for this response remains unknown. We demonstrate that Arabidopsis (Arabidopsis thaliana), an ephemeral of the temperate northern hemisphere that has never, to our knowledge, been reported to be responsive to fire or smoke, rapidly and sensitively perceives karrikins. Thus, these signaling molecules may have greater significance among angiosperms than previously realized. Karrikins can trigger germination of primary dormant Arabidopsis seeds far more effectively than known phytohormones or the structurally related strigolactone GR-24. Natural variation and depth of seed dormancy affect the degree of KAR1 stimulation. Analysis of phytohormone mutant 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 by karrikin is only partly DELLA dependent. While KAR1 has little effect on sensitivity to exogenous GA, it enhances expression of the GA biosynthetic genes GA3ox1 and GA3ox2 during seed imbibition. Neither abscisic acid nor GA levels in seed are appreciably affected by KAR1 treatment prior to radicle emergence, despite marked differences in germination outcome. KAR1 stimulation of Arabidopsis germination is light-dependent and reversible by far-red exposure, although limited induction of GA3ox1 still occurs in the dark. The observed requirements for light and GA biosynthesis provide the first insights into the karrikin mode of action.


1 This work was supported by the Australian Research Council (grant nos. FF0457721, DP0667197, DP0880484, and DP0559058) and the Centres of Excellence Program of the Government of Western Australia.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Steven M. Smith (ssmith{at}cyllene.uwa.edu.au).

[W] The online version of this article contains Web-only data.

[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.131516

* Corresponding author; e-mail ssmith{at}cyllene.uwa.edu.au.

Received October 21, 2008; accepted December 5, 2008; published December 12, 2008.


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