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Kępczyński, J.; Kępczyńska, E. Plant-Derived Smoke and Karrikin 1  Activity in Seed. Encyclopedia. Available online: https://encyclopedia.pub/entry/46387 (accessed on 12 April 2024).
Kępczyński J, Kępczyńska E. Plant-Derived Smoke and Karrikin 1  Activity in Seed. Encyclopedia. Available at: https://encyclopedia.pub/entry/46387. Accessed April 12, 2024.
Kępczyński, Jan, Ewa Kępczyńska. "Plant-Derived Smoke and Karrikin 1  Activity in Seed" Encyclopedia, https://encyclopedia.pub/entry/46387 (accessed April 12, 2024).
Kępczyński, J., & Kępczyńska, E. (2023, July 04). Plant-Derived Smoke and Karrikin 1  Activity in Seed. In Encyclopedia. https://encyclopedia.pub/entry/46387
Kępczyński, Jan and Ewa Kępczyńska. "Plant-Derived Smoke and Karrikin 1  Activity in Seed." Encyclopedia. Web. 04 July, 2023.
Plant-Derived Smoke and Karrikin 1  Activity in Seed
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Plant-derived smoke and smoke water (SW) can stimulate seed germination in numerous plants from fire-prone and fire-free areas, including cultivated plants and agricultural weeds. Smoke contains thousands of compounds; only several stimulants and inhibitors have been isolated from smoke. Among the six karrikins present in smoke, karrikin 1 (KAR1) seems to be key for the stimulating effect of smoke. The discovery and activity of highly diluted SW and KAR1 at extremely low concentrations (even at ca. 10−9 M) inducing seed germination of a wide array of horticultural and agricultural plants have created tremendous opportunities for the use of these factors in pre-sowing seed treatment through smoke- or KAR1-priming.

smoke-priming somatic embryogenesis smoke water karrikin KAR1-priming

1. Introduction

After they have been sown, seeds are exposed to various environmental factors influencing seed germination and seedling establishment. These processes seldom take place under optimal conditions. Adverse environmental factors, e.g., extreme temperatures, drought, or high salinity, may slow down germination, prevent uniform germination, and/or cause a low percentage of germination, poor seedling emergence, and irregular plant development, which consequently leads to a reduction in the quality and size of the yield [1][2]. Seed priming technology is an economically successful, viable key strategy to increase crop production under non-stressful and stressful environmental conditions. Conventional seed priming, e.g., hydropriming, osmopriming and matriconditioning, involves seed hydration, allowing metabolism to proceed but preventing radicle protrusion. So far, various priming methods, e.g., hormopriming, gas priming, physical priming, biopriming etc., responsible for the induction of various physio-biochemical traits improving seed vigor, have been developed [2][3] (Figure 1).
Figure 1. Methods of seed priming.
Since crop cultivation under adverse environmental conditions may reduce yields by up to 50% [4], various cost-effective and easily applicable types of priming should be more widely used, and the search for new pre-sowing techniques should be developed. Demonstrating the ability to stimulate seed germination and seedling growth in many plant crops by plant-derived smoke and smoke-derived KAR1 has generated new opportunities for their use in the pre-sowing treatment of seeds by SW- and KAR1-priming.

2. The Importance of Discovering the Biological Activity of Smoke and Compounds Isolated from It

Having observed that vegetation regenerates after a fire, farmers began to use smoke to treat seeds. In many areas, farmers have used fire and plant-derived smoke to treat seeds to stimulate their germination [5]. Initial data on the effect of smoke on seed germination were published by De Lange and Boucher in 1990 [6]. To those scientists, the discovery of smoke-saturated water (SW) being as effective as smoke alone are owed. This information generated great interest, followed by a large number of publications on the influence of smoke and SW on seed germination in several plant species. The role of smoke in seed germination was also described in reviews [5][7][8][9][10][11][12]. It has been reported that seeds or seedlings of over 1300 plant species respond to smoke or SW [7][12]. Smoke/SW stimulate seed germination in plants derived from areas where fires can occur and crops, vegetables, and weeds [5][9]. Very interesting was the demonstration that SW can be prepared by bubbling, through water, when burning leaves of monocotyledons, dicotyledons and gymnosperms leaves of plants originating not only from fire-prone areas, and also that SW does not lose its activity even after several years of storage [13]. Results of experiments on the beneficial effect of smoke on seed germination and seedling growth were very quickly put into practice by the development of various commercial preparations [14].
It took many years to search, among thousands of compounds in smoke, for the compound responsible for stimulating smoke-driven germination. The search proved successful only in 2004 when two independent teams isolated butenolide, currently called karrikinolide or karrikin 1 (KAR1), from plant-derived smoke [15] and from burnt cellulose [16] (Figure 2).
Figure 2. The structure of some bioactive karrikins and strigolactones. KAR1 - 3 methyl-2H-furo[2,3-c]pyran-2-one, most often the most active of the karrikins and found in smoke at the highest concentration; KAR2-karrikin with activity towards Arabidopsis seeds higher than that of KAR1; strigol-natural strigolactone; GR24-synthetic strigolactone. Both karrikins and strigolactones have a butenolide ring. Karrikins and GR24 have similar effects on seed germination, e.g., Arabidopsis and Brassica tournefortii, seedling photomorphogenesis and expression of genes [17][18]. KAR1, in contrast to GR24, could not stimulate the germination of parasitic weed seeds.
Smoke is now known to contain also other karrikins, numbered from KAR1 to KAR6 [8]. KAR1 is usually the most active of all known karrikins; it is present in the highest concentration of smoke, 5.5 to 38 times higher than other karrikins [8]. The KAR1 concentration of 6.7 × 10−7 M was found to correspond to a SW dilution of 1:100 [7]. The compound has been found to stimulate seed germination of plants from fire-prone areas and fire-free regions; the germination of crops and weeds is also stimulated. KAR1 was shown to be very active at extremely low concentrations such as 10−10–10−7 M. Various times of imbibition in a KAR1 solution, e.g., from 1 min for Emmenanthe penduliflora seeds [7] to 6 h for Avena fatua caryopses [19] was sufficient to stimulate germination. KAR1 can be synthesized using different substrates and is commercially available (Table 1).
Table 1. Substrates used for KAR1 synthesis.
Glyceronitrile was reported to appear after fire; in addition to karrikins, ethylene and nitric oxide (NO) are also present in smoke and induce dormancy release in many seeds. They all are recognized as signals in upper soil layers, characteristic of fire and smoke, for dormant seeds to germinate [25] (Table 2).
Table 2. Effects of some compounds present in plant-derived smoke on seed germination. ↑stimulation; ↓ inhibition.
Seed germination is stimulated by hydroquinone, and seedling growth is improved by catechol, both compounds being detected in smoke as well [30]. Further research has shown that there are seeds which respond to KAR1, but their germination is neither affected nor stimulated by smoke [9]. Moreover, weak—as opposed to strong—SW dilutions inhibit seed germination. Such an effect of SW has been suspected to be related to the presence in the smoke of certain inhibitors antagonistic to karrikins and/or other stimulants. Other experiments revealed the presence of three compounds: 3,4,5-trimethyl furan-2 (5H)-one (TMB), 5,5-dimethylfuran-2(5H)-one and (5RS)-5-ethylfuran-2(5H)-one that inhibited seed germination and exerted an antagonistic effect towards that of KAR1 [28][31]. Thus, the effect of smoke should be considered as a comprehensive biological response to the interacting compounds present in the smoke. Some studies showed TMB to be present in the soil in concentrations higher than those of KAR1 and to be more water-soluble than KAR1 [12]. It has been proposed that TMB accumulated in the soil is diluted and washed away by heavy rainfall, which makes it possible for the stimulatory effect of KAR1 to be expressed. This agrees with a previous suggestion that smoke plays a dual function in regulating seed germination in soil [32].

3. Seed Priming with SW or KAR1 Solution

Since the high effectiveness of SW at high dilutions and KAR1 at low concentrations as stimulants of seed germination and/or seedling development have been demonstrated [8][9][11][33], the agents have become a focus of research on seed priming, a pre-sowing technique. For priming, seeds were imbibed in Petri dishes on filter paper moistened with appropriate solutions of SW or KAR1 or were soaked in solutions of these agents (Table 3).
Table 3. Examples of beneficial effects of SW- or KAR1-priming.
Then, the SW- or KAR1-primed seeds were surface dried or dried to air dry level and sown immediately or after storage in Petri dishes or soil. Subsequently, germination, seedling emergence, seedling growth and/or certain indicators of metabolism were determined. SW- or KAR1-priming were applied to seeds of natural plants in the revegetation strategy and to improve seedling emergence and the development of cultivated plants. Early experiments with Themeda triandra, a dominant fire-climax grass, showed seeds imbibed in an SW solution and then dried and stored at 25 °C to germinate better than untreated seeds [45]. The cited authors rightly concluded that such seed pre-treatment could be used to revegetate the plant. Later, other promising results were obtained from research on SW application to prime seeds of cultivated plants. Germination of Solanum centrale, S. dioicum and S. orbiculatum seeds, vigor index and 18-d old seedling length were found to increase when the seeds were imbibed in SW and immediately transferred to Petri dishes with agar [44]. However, it is not known whether the stimulating effect of SW-priming would also persist after seed drying and storage. In another experiment, soaking of Silybum marianum seeds, a plant native to Europe, Asia, and Africa, at present cultivated for the pharmaceutical industry [43] in SW, despite drying, enhanced the germination speed at 25 °C, vigor index and 14-days old seedling length. Soaking Dactylis glomerata seeds in SW solution and drying them before sowing in the field increased germination, seedling emergence under field conditions and biomass after ten weeks of crop cultivation [48]. That beneficial effects can also appear under environmental conditions was an important information. In another experiment, soaking of Zea mays seeds in SW increased the rate of seed germination and fresh weight of shoots and roots in 8-day-old seedlings [46]. Moreover, chlorophyll and carotenoid contents were higher in seedlings obtained from the primed seeds.
Because SW-priming positively affected seed germination, seedling emergence and/or seedling development, experiments were carried out to explore the effects of KAR1-priming or both SW- and KAR1-priming, in one of the experiments, the sowing of Zea mays kernels soaked in an SW or KAR1 solution, followed by surface drying, increased the plant height, root and shoot weight and dry weight after 30 days of greenhouse cultivation [47], indicating the advantages of both SW- and KAR1-priming. However, whether this positive effect persisted until the end of plant development and whether it was reflected in the yield is unknown. Doubtless, the use of primed seeds in commercial practice would be enhanced if positive effects were not reduced due to the post-treatment seed drying and drying and storage. Therefore, it was essential to find out if seeds subjected to KAR1-priming could be stored for some time without losing the beneficial priming effect. In one experiment, the effect of priming on the development of plants after cultivation under environmental conditions was addressed using Daucus carota. SW and KAR1 were applied during the soaking of D. carota seeds, air-dried before sowing, increased germination in soil and seedling growth after 120 days of growth under natural conditions [39]. Moreover, both priming techniques increased the photosynthesis rate and the contents of carotene and ascorbic acid. Capsicum annuum seeds, primed with KAR1 by soaking, showed improved germination of both immature and mature seeds. The technique worked better in immature prime than hydropriming [35]. Likewise, an advantageous effect of KAR1-priming was observed in 20-day-old C. annuum seedlings when the fresh weight of the seedlings grown on a peat moss medium was determined. The stimulatory effect of KAR1 also included an increase in catalase (CAT), ascorbate peroxidase (APX) and superoxide dismutase (SOD) activities in both immature and mature seeds.
So far, various priming technologies have been successfully used to enhance resistance to abiotic stresses, consistently improving overall plant growth [1]. SW and KAR1 have been demonstrated to have a positive effect not only on seed germination and seedling development under optimal conditions but also under stress [11], so it was logical to conduct research aimed at finding out whether SW- and/or KAR1-priming can be used to increase plant tolerance to various abiotic stresses. However, only limited, albeit important, information has been obtained so far through experiments focusing on using both above-priming techniques to improve seed germination, seedling emergence and establishment under various stress conditions. Extreme temperatures, too low or too high, are known to have an adverse impact on seed germination and plant development by disrupting metabolism, damaging structures, and ultimately leading to the death of cells, organ tissues and even the entire organism. Priming Lycopersicon esculentum by soaking the seeds in a KAR1 solution increased the seedling vigor after 7-day incubation at various temperatures, including sub- and supraoptimal [41].
Moreover, KAR1-priming enhanced seedling vigor under salt and osmotic stress—the cultivation of Brassica napus cv. English giant, an annual herbaceous leafy vegetable, can be limited due to the high temperature and water stress. SW-priming and, to a larger extent, KAR1-priming increased seed germination at heat stress (40 °C) [34].
Likewise, SW- and KAR1-priming by imbibing seeds of Eragrostis tef, a major cereal crop in the Horn of Africa countries, were used to test germination and vigor of 7-day-old seedlings at various temperatures, including 40 °C, and at osmotic stress [40]. The treatment improved both germination and seedling vigor. Similarly, SW-priming of Oryza sativa seeds increased seed germination and seedling vigor under salt stress simulated by NaCl solutions [42]. Effects of priming included an increase in the chlorophyll and carotenoid contents. In addition, priming increased the contents of K+ and Ca+, but decreased that of Na+. In Ceratotheca triloba, SW- and KAR1-priming increased seed germination after 25 days under osmotic stress caused by PEG 6000 solutions [36]. Both priming techniques also improved the growth of 25-day-old seedlings under stress. The effect of KAR1-priming on the alleviation of stress caused by cadmium, a pollutant prevalent in arable lands, was studied on seeds of Coriandrum sativum, an important herbaceous plant cultivated in various regions of the world and used in pharmacy, cosmetology, and various cuisines as a spice [37]. Cadmium was found to inhibit seed germination and to reduce the fresh and dry weight of 15-day-old seedlings. The inhibitory effect declined when primed seeds were used. The beneficial effect of priming on cadmium stress tolerance was associated with increased leaf osmotic potential, membrane stability, photosynthesis rate and proline content. Moreover, KAR1-priming resulted in decreased contents of malondialdehyde (MDA) and hydrogen peroxide (H2O2) and electrolyte leakage. In contrast, antioxidant enzymes: superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT) in seedlings were found to enhance their activity. The effect of KAR1-priming of Cucumis melo seeds sown, after surface drying, in peat moss at two depths and kept at 20 and 25 °C in the controlled climatic room for 24 days, on seedling emergence and seedling fresh and dry weight was also examined [38]. The KAR1-priming advantage was particularly evident if the seeds were of poorer quality and were sown too deep at a sub-optimal temperature of 20 °C. KAR1-priming was observed to increase seedling emergence, speed, and final percentage, and seedling fresh weight at 20 °C more effectively than at 25 °C when the seeds were sown deeper.
It is probably still long before SW and/or KAR1 will be commercially applied in priming technology. One can only consider the potential use of SW- and KAR1-priming in increasing seed tolerance to adverse environmental factors. So far, research has been limited to assessing the effects on germination and seedling development, often on Petri dishes. The impact of both types of priming on plant development and yield under environmental conditions in most cases has not been determined. In the experiments, SW- or KAR1-primed seeds were most often used immediately after the treatment or only after surface drying, and it is known that other priming techniques and KAR1-priming diminish the seed priming benefit as a result of drying. Perhaps a solution would be to dry the seeds gradually, similarly to the drying manner recommended for somatic embryos.
Considering the practical application of SW or KAR1 in priming, if the seeds are sensitive to SW, SW-priming seems more valuable because the SW preparation is easy and cost-free. Although KAR1 is expensive due to its effectiveness at very low concentrations, its use is also promising. Knowledge of KAR1-primed seed metabolism is still scant. Application of SW and/or KAR1 in combination with other conditioning methods, e.g., osmopriming or matripriming, to seeds of economically important plants requires further research.

4. SW and KAR1 in Seed Biotechnology

The use of both SW and KAR1 in vitro cultures of various plant materials has been a focus of several studies. As fire and smoke were found to be capable of inducing flowering in some plants, e.g., Cyrtanthus ventricosus and Watsonia borbonica [49][50], experiments were conducted to follow the response of pollen of various plants from fire-prone areas. SW or KAR1 were demonstrated to stimulate pollen germination and tube growth of various plant species; therefore, it was correctly concluded that both agents could increase flower pollination, leading to increased fertilization and seed yield [51][52]. However, no data are showing the effect on the seed yield. It was very interesting and extremely important to discover that, under natural conditions and in vitro, it is possible to generate embryos from somatic cells without fertilization. Somatic embryogenesis, which makes it possible to produce artificial seeds, is of great interest to both the researchers striving to explain the process and the practitioners who could use the process for the mass multiplication of plants. Application of somatic embryogenesis in practice requires optimalisation of the process for the sake of high efficiency, particularly with respect to cotyledonary embryos, the most advanced stage of embryo development. Experiments were carried out to examine the suitability of SW and KAR1 in improving somatic embryogenesis (Table 4).
Table 4. Effect of SW and KAR1 in tissue cultures. + stimulation; − no effect; ND- no data.
However, only a few examples of SW or KAR1 are being applied to improve somatic embryogenesis. SW was shown to increase embryogenesis efficiency in Pelargonium hortorum [54] markedly. Important insights were gained, including the observation that SW increased the formation of cotyledonary embryos. When SW was applied to the hypocotyl explant or during the induction phase, the number of cotyledonary embryos increased fivefold. In Pinus wallichiana, SW used in the induction medium increased the number of cotyledonary embryos by about 3.5 [55]. SW was also found to increase the occurrence of secondary embryogenesis in Brassica napus [57]. These data may suggest that karrikin in the smoke was likely responsible for its stimulatory effect. It is important to note that KAR1 accelerated the development of torpedo embryos in Baloskion tetraphyllum [53]. Knowledge of the effect of SW and KAR1 on somatic embryo germination and conversion to plantlets is incomplete. An experiment with P. wallichiana showed SW to stimulate the germination of cotyledonary somatic embryos and to increase the number of surviving seedlings [55]. Likewise, KAR1 improved both somatic embryo germination and plantlet development in B. tetraphyllum [53]. Since SW and KAR1 were initially known as inducers of in vivo seed germination, it is understandable that they were applied to find out if they would be useful in inducing the in vitro seed germination. One of the methods of orchid production involves the sowing of seeds. Therefore, using agents that improve in vitro orchid seed germination is appropriate. SW stimulated the germination of asymbiotic seeds, protocorm differentiation and plant regeneration in Vanda parviflora, an epiphytic orchid [59]. Also, seed germination and plant recovery of the epiphytic orchid Xenikophyton smeeanum and Tulbaghia ludwigiana, a popular garden plant, was increased by SW [60].
Similarly, SW stimulated seed germination and the formation of protocorms in the epiphytic orchid Ansellia africana [58]. However, KAR1 could not induce germination or protocorm formation, which indicates that the SW activity can be associated with compounds other than karrikin(s) or other stimulant(s) present in SW. Seeds of different plant species, e.g., Aloe arborescens, were stimulated to germinate by SW [61]. Therefore, it has been demonstrated that SW could be used in orchid and aloe propagation. An in vitro experiment involving Balsamorhiza deltoidea and B. sagittata, plants from fire-prone areas of America, showed that, like in seeds of some plant species, KAR2—in contrast to—KAR1 was active in vivo as a stimulant [62].
Data on using both SW and KAR1 in seed biotechnology are promising, although too scant. There are no examples of KAR1 interaction with plant hormones in the regulation of somatic embryogenesis. The effects of the compound on the level of phytohormones are unknown, and the mechanism of in vitro treatments that considers the molecular level requires research.

5. Mechanism of Karrikin Signalling

Recently, great progress in elucidating the karrikin signaling mechanism has been observed (Figure 3).
Figure 3. A proposed mechanism of KAR1 signalling. KAI2 (KARRIKIN INSENSITIVE2)-α,β hydrolases performing enzyme and receptor functions; K -a putative karrikin-derived molecule; F-box –recognizes substrate; Skp1 –substrate adaptor; Cullin –regulates complex activity; Rbx –facilitates transfer ubiquitin (Ub); E2 –transfers the ubiquitin to the substrate.
Several studies indicate that KAR1 must be metabolized for an answer to this compound to emerge (63). KAR1 is metabolized to K (a putative karrikin-derived molecule). Activation of KAI2 (KARRIKIN INSENSITIVE2)-α,β hydrolases by K enables interaction with MAX2, an F-box protein part of Skp1-Cullin-F-box (SCF) E3 ubiquitin ligase complex. MAX2 recognizes SMAX1 (SUPPRESSOR OF MAX2), and SMXL2 (SMAX1-LIKE2), proteins that prevent the appearance of a response to KAR1. SMAX1 and SMXL2 proteins undergo polyubiquitination, followed by proteosomal degradation leading to the emergence of a response characteristic of KAR1 [63]. Fascinating is the great similarity in the signalling mechanism of both butenolide molecules, karrikins, unidentified in plants, and plant hormones, strigolactones [63][64]. MAX2 also mediates responses to strigolactones, which activate D14 (DWARF14)- α,β hydrolases structurally similar to KAI2 [18][65]. D14 acts with MAX2 to target SMXL6, SMXL7 and SMXL8 for ubiquitination and degradation. D14 can also target SMAX1 and SMXL2 when an adequate agonist is present. Moreover, there are also similarities in the signaling mechanism of karrikins and plant hormones such as auxins, jasmonates and gibberellins. All response systems involve the Skp1/Cullin/F-box-E3 ubiquitin ligase complex and the ubiquitination of the regulatory protein and its degradation by the 26S proteosome. Studies that involve karrikin and plant hormones pathways will not be referred to here; an extensive review of Blázquez and coworkers provides ample and adequate information [66].

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