Butenolides from Plant-Derived Smoke: Natural Plant-Growth Regulators with Antagonistic Actions on Seed Germination

Abstract

Smoke plays an intriguing role in promoting the germination of seeds of many species following a fire. Recently, a bicyclic compound containing a condensed butenolide moiety, 3-methyl-2H-furo [2,3-c]pyran-2-one (1), was reported as a potent germination promoter from plant-derived smoke. In this study, a related butenolide, 3,4,5-trimethylfuran-2(5H)-one (2), which inhibits germination and significantly reduces the effect of 1 when applied simultaneously, was also isolated from plant-derived smoke. The interaction of these compounds with opposing actions on seed germination may have important ecological implications in a post-fire environment and could be useful molecules for understanding the events involved in breaking seed dormancy and promoting seed germination.Smoke from burning vegetation is recognized as an important environmental cue and promoter of germination for seeds of many species from both fire-prone and non-fire-prone environments.(1) Smoke-water, prepared by bubbling smoke through a container of water, is also highly effective in promoting seed germination of the responsive species and is a more convenient method of treatment. The major germination compound responsible for the observed germination increase was isolated and identified as 3-methyl-2H-furo[2,3-c]pyran-2-one (1, karrikinolide),(2, 3) a discovery that has revealed a class of plant bioactive compounds that are referred to as karrikins(4) and are proposed to be a new and important family of naturally occurring plant growth regulators.(5, 6) Subsequently, 1 has been shown to improve germination and improve seedling vigor of several species, including those from fire-prone environments, arable and parasitic weeds, several Australian Solanum species, and crop plants.(5) Due to the fact that it has an effect at extremely low concentrations (as low as 1 nM), it has potential as an important agronomic and horticultural chemical.(5, 7) Although the mode of action of smoke and 1 (and related karrikins) in promoting germination and vigor is currently unknown, research is progressing in this field. (4,8,9) Previous investigations of smoke-stimulated seed germination demonstrated that dilute solutions of smoke-water were highly effective in promoting the germination of light-sensitive seeds of Lactuca sativa L. cv. Grand Rapids.Thus, Grand Rapids lettuce was used as an effective model species for bioactivity-guided fractionation of smoke-water.(3, 10) Although, in general, smoke provides a positive stimulus for germination, a negative effect of high concentrations of smoke-water on germination is well demonstrated.(10-13) This effect can most likely be attributed to inhibitory compounds (i.e., compounds other than the promotory karrikins) that are present in the smoke-water. Smoke (from cigarettes or other products) is known to contain numerous compounds (estimated to be well over 4000),(14) some of which are toxic or carcinogenic. In another study, it was reported that smoke could possibly play a dual regulatory role during germination,(1...

Smoke and heat: influence on seedling emergence from the germinable soil seed bank of mesic grassland in South Africa

“…This elevated plant mass production in response to the fire-related treatments has been repeatedly shown for a range of agricultural and horticultural crops (Kulkarni et al 2010). Although the mechanisms responsible for the elevated growth rate are not fully understood, there is a general suggestion that the active compound(s) present in plant-derived smoke perhaps influence enzyme systems which control growth rate (Light et al 2010). Findings of this greenhouse experiment suggest that not only are smoke-responsive species more likely to germinate following a fire in the field, but also that a faster growth rate of some smoke-responsive species will increase their competitive ability for limiting resources (Tilman 1988).…”

Effects of smoke water and karrikin on seed germination of 13 species growing in China

“…It is a heat-stable, long-lasting and water-soluble compound that can stimulate seed germination and seedling growth at very low concentrations (1-100 nM) [25,[27][28][29][30]. At present, butenolide can be artificially synthesized and has wide applicability as a germination and growth stimulant with potential implications for both weed management and improving crop seedling growth [31][32][33].…”

Interaction of karrikinolide and ethylene in controlling germination of dormant Avena fatua L. caryopses

“…There are also examples showing that KAR 1 and smoke are not equally effective in all species. Smoke contains many compounds besides the KAR 1 , some of which may inhibit germination (Light et al 2010). Both smoke and the KAR 1 stimulate germination of partially dormant caryopses (seeds) of Avena fatua, an important widespread, persistent weed, which infests agricultural soils for several years (Adkins and Peters 2001;Kępczyński et al 2006b;Daws et al 2007;Stevens et al 2007).…”