What are karrikins and how were they ‘discovered’ by plants?
© Flematti et al. 2015
Published: 21 December 2015
Karrikins are a family of compounds produced by wildfires that can stimulate the germination of dormant seeds of plants from numerous families. Seed plants could have ‘discovered’ karrikins during fire-prone times in the Cretaceous period when flowering plants were evolving rapidly. Recent research suggests that karrikins mimic an unidentified endogenous compound that has roles in seed germination and early plant development. The endogenous signalling compound is presumably not only similar to karrikins, but also to the related strigolactone hormones.
What are karrikins?
How were karrikins discovered?
Where does the karrikin name come from?
The formal names of the compounds are too complex for common usage and there are many butenolides in nature, so a more recognisable common name was required. To reflect their discovery in smoke, the family of compounds was named ‘karrikins’ from the word ‘karrik’, which is an Aboriginal term for smoke from the Western Australian Noongar people [4, 5]. It is common practice in biology to add the ‘-in’ suffix to denote a group of related molecules, such as ‘cytokinins’ in plants or ‘endorphins’ in animals. Fire and smoke play important roles in Aboriginal culture in Australia, and the karrikin name acknowledges that fact. The original compound identified is often referred to as ‘karrikinolide’: the ‘-olide’ suffix indicates that it is a lactone. The karrikins are abbreviated to KAR and numbered in order of their identification in smoke (Fig. 2).
What are the properties of karrikins?
Karrikins comprise only C, H and O, and contain two ring structures, one of which is a pyran and the other a lactone comprising a five-membered ring known as a butenolide. The pure compound is a crystalline substance with a melting point of 118–119 °C that readily dissolves in organic solvents and sparingly in water. All the karrikins are closely related in structure. The first of the compounds to be identified, KAR1, is usually the most abundant in smoke and the most active in seed germination. Seeds of some fire-followers can respond to as little as 10−10 M KAR1, which is similar in effectiveness to plant hormones .
How are karrikins produced by fire?
It was found that burning many different plant materials, including straw, cellulose filter paper and even sugars, could generate karrikins. Their production from polysaccharides and sugars explains the pyran ring of karrikins, which is proposed to be derived directly from pyranose sugars in plant material (Fig. 2). The precise chemical reaction is unknown but it requires oxygen, and it is even possible to generate seed-germination activity by heating plant material at 180 °C for 30 minutes. So karrikins are probably produced around the home by toasting and roasting certain plant foods. The smoke from cigarettes stimulates seed germination, probably due to the presence of karrikins. Further research has shown that karrikins are unstable at very high temperatures . It is likely, therefore, that they are produced in the less-intense parts of wildfires, vaporise, and collect in the smoke and condensation and become bound to soil particles in the same way that cooled smoke can be deposited onto seeds to stimulate their germination. Karrikins may be ‘carried’ in smoke by a process of steam distillation but are not carried for long distances in smoke, and largely remain close to the source of the fire .
How long do karrikins remain in the soil?
Measurements of karrikins in soil are technically very challenging but seed-germination bioassays can be used to detect activity, one study suggesting that active compound(s) can persist in the soil for over seven years after a fire . Karrikins are unstable in ultraviolet light  so they might be expected to decay rapidly in natural sunlight; however, smoke contains many aromatic compounds that can absorb ultraviolet light and could protect karrikins by acting as organic ‘sunscreens’. On the other hand, karrikins can be washed away by rain and elute through sandy soils relatively quickly, so their concentration will steadily decline.
Why do karrikins not stimulate new seed to germinate?
It might be expected that seeds falling from a new plant in a burnt landscape would immediately encounter karrikins in the soil, and so germinate. While this happens for just a few species, most species need their seeds to be buried in soil for a year or more, a process known as after-ripening, before they become karrikin-responsive. There is also evidence that some seeds may need to undergo a series of wetting and drying cycles in the soil before they become responsive, which means that they depend on a future fire for germination .
What types of plants respond to karrikins?
Seeds from many different families of flowering plants and conifers representing many plant life forms (trees, shrubs, herbs, annuals) will respond to karrikins, and many more respond to smoke, implying that the karrikin response is widespread and may have evolved independently in different groups . Plants with smoke-responsive seed are found in both fire-prone and non-fire-prone environments. Most are dicotyledonous plants but many grasses also respond to smoke. Surprisingly, not only fire-followers respond but also many weedy species, including agricultural weeds . Even seeds of horticultural plants such as lettuce and tomato will have improved germination in response to karrikins under some circumstances. This implies that the ability or potential for a response to karrikins is something fundamental to plants, but the fire-followers have fine-tuned this response to their advantage in post-fire landscapes.
Do fires produce any other chemicals that stimulate germination?
Do karrikins have any other effects on plants?
Are karrikins of commercial or practical use?
Smoke water is sometimes used to promote germination of garden and horticultural seeds, and can be purchased commercially or easily made. However, many commercial smoke germination products are made from combusting wood that, because of its high lignin content, produces germination inhibitors. Aerosol smoke is also used, and some nurseries or landscape restoration operations use this approach to treat seeds directly or to smoke seedling trays . There has been much interest in the possible use of chemically synthesised karrikins to treat soil to bring about wide-scale and vigorous germination of the resident weed soil seed bank — a process known as ‘suicidal germination’. This could be used for re-vegetation of degraded land, or to promote germination of dormant weed seeds in farmer’s fields so that the weeds can be eliminated. Further research is needed to develop more cost-effective synthesis and improve delivery methods for large-scale commercial application of karrikins.
How do karrikins work?
The realisation that many plant species respond to karrikins led to the discovery that seeds of Arabidopsis thaliana can respond . Arabidopsis is the geneticist’s dream because of the resources and knowledge that are available. Arabidopsis seeds with a small amount of dormancy will respond to KAR1 or KAR2, provided that there is no nitrate present, which causes seeds to germinate regardless of the karrikin. Selection of Arabidopsis mutants that fail to respond to karrikins led to the discovery of two genes that are essential for karrikin action. One gene, named MORE AXILARY GROWTH2 (MAX2), was already known for its role in responses to strigolactone hormones , while the other, KARRIKIN-INSENSITIVE2 (KAI2), was similar to the gene coding for the strigolactone receptor, known as DWARF14 . These discoveries led to the idea that karrikins simply mimic strigolactones, because they both have a butenolide ring (Fig. 2). We now know that this is not the case in Arabidopsis. Karrikins and strigolactones are perceived separately and the plant responds differently to the two classes of compound, but the two systems are obviously very closely related . Formally we still do not know if the mode of action of karrikins in fire-followers is the same as that in Arabidopsis, but all plants apparently contain a KAI2 gene, so it seems likely.
What is the normal function of the karrikin response system?
Are karrikins metabolised by plants?
Since evidence for the direct interaction of KAR1 with KAI2 is equivocal, there remains the possibility that the karrikin compounds found in smoke require uptake and conversion by the seed into an active compound before interaction with KAI2. This could explain why some seeds are less responsive than others, if they lack the processes and enzymes for uptake or metabolism. Although there are reports that KAR1 can interact directly with KAI2 protein, other studies do not support this. A further complication is that while strigolactones are destroyed by the hydrolase activity of their receptor protein DWARF14, such evidence is lacking for karrikins and KAI2. It is possible, therefore, that plants take up karrikins and convert them to active compounds that then interact directly with the KAI2 protein.
How does the karrikin response system influence plant growth and development?
Treatment of plants with karrikins or analysis of mutants that do not respond to karrikins reveals that signalling though the KAI2 pathway leads to changes in gene expression. A search for mutants that suppress the karrikin-insensitive mutant phenotype led to the discovery of a gene named SUPPRESSOR OF MAX2-1 (SMAX1), which is required for the KAI2 signalling system. At the same time a closely related gene named DWARF53 was found to be required for strigolactone signalling in rice. These genes encode proteins that are repressors of gene transcription, and DWARF53 is degraded when strigolactones are present, leading to activation of target genes. It is likely that karrikin signalling works in the same way, but targets different genes for activation, with different growth responses (Fig. 6) .
How did plants ‘discover’ karrikins?
Where can I go for more information?
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- Nelson DC, Flematti GR, Ghisalberti EL, Dixon KW, Smith SM. Regulation of seed germination and seedling growth by chemical signals from burning vegetation. Annu Rev Plant Biol. 2012;63:107–30.PubMedView ArticleGoogle Scholar
- De Lange JH, Boucher C. Autecological studies on Audouinia capitata (Bruniaceae). I. Plant-derived smoke as a seed germination cue. S Afr J Bot. 1990;56:700–3.Google Scholar
- Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD. A compound from smoke that promotes seed germination. Science. 2004;305:977.PubMedView ArticleGoogle Scholar
- Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD. Identification of alkyl substituted 2H-furo[2,3-c]pyran-2-ones as germination stimulants present in smoke. J Agric Food Chem. 2009;57:9475–80.PubMedView ArticleGoogle Scholar
- Nelson DC, Riseborough JA, Flematti GR, Stevens J, Ghisalberti EL, Dixon KW, et al. Karrikins discovered in smoke trigger Arabidopsis seed germination by a mechanism requiring gibberellic acid synthesis and light. Plant Physiol. 2009;149:863–73.PubMedPubMed CentralView ArticleGoogle Scholar
- Scaffidi A, Waters MT, Skelton BW, Bond CS, Sobolev AN, Bythell-Douglas R, et al. Solar irradiation of the seed germination stimulant karrikinolide produces two novel head-to-head cage dimers. Org Biomol Chem. 2012;10:4069–73.PubMedView ArticleGoogle Scholar
- Preston CA, Baldwin IT. Positive and negative signals regulate germination in the post-fire annual, Nicotiana attenuata. Ecology. 1999;80:481–94.View ArticleGoogle Scholar
- Stevens JC, Merritt DJ, Flematti GR, Ghisalberti EL, Dixon KW. Seed germination of agricultural weeds is promoted by the butenolide 3-methyl-2H-furo[2,3-c]pyran-2-one under laboratory and field conditions. Plant Soil. 2007;298:113–24.View ArticleGoogle Scholar
- Flematti GR, Merritt DJ, Piggott MJ, Trengove RD, Smith SM, Dixon KW, et al. Burning vegetation produces cyanohydrins that liberate cyanide and promote seed germination. Nat Commun. 2011;2:360.PubMedView ArticleGoogle Scholar
- Downes KS, Light ME, Pošta M, Kohout L, van Staden J. Comparison of germination responses of Anigozanthos flavidus (Haemodoraceae), Gyrostemon racemiger and Gyrostemon ramulosus (Gyrostemonaceae) to smoke-water and the smoke-derived compounds karrikinolide (KAR1) and glyceronitrile. Ann Bot. 2013;111:489–97.PubMedPubMed CentralView ArticleGoogle Scholar
- Waters MT, Scaffidi A, Sun YK, Flematti GR, Smith SM. The karrikin response system of Arabidopsis. Plant J. 2014;79:623–31.PubMedView ArticleGoogle Scholar
- Dixon KW, Merritt DJ, Flematti GR, Ghisalberti EL. Karrikinolide—a phytoreactive compound derived from smoke with applications in horticulture, ecological restoration and agriculture. Acta Hortic. 2009;813:155–70.View ArticleGoogle Scholar
- Smith SM. Q&A: What are strigolactones and why are they important to plants and soil microbes? BMC Biol. 2013;12:19.View ArticleGoogle Scholar
- Smith SM, Li JY. Signaling and responses to strigolactones and karrikins. Curr Opin Plant Biol. 2014;21:23–9.PubMedView ArticleGoogle Scholar
- He T, Pausas JG, Belcher CM, Schwilk DW, Lamont BB. Fire-adapted traits of Pinus arose in the fiery Cretaceous. New Phytol. 2012;194:751–9.PubMedView ArticleGoogle Scholar
- Waters MT, Scaffidi A, Moulin ALY, Sun YK, Flematti GR, Smith SM. A Selaginella moellendorfii ortholog of KARRIKIN INSENSITIVE2 functions in Arabidopsis development but cannot mediate responses to karrikins or strigolactones. Plant Cell. 2015;27:1925–44.PubMedPubMed CentralView ArticleGoogle Scholar
- Conn CE, Bythell-Douglas R, Neumann D, Yoshida S, Whittington B, Westwood JH, et al. Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science. 2015;349:540–3.PubMedView ArticleGoogle Scholar