Preparation of Plant-derived Smoke for Stimulating Seed Germination and Quantification of Karrikins Using High Performance Liquid Chromatography
Yıl 2023,
Cilt: 29 Sayı: 3, 800 - 810, 25.09.2023
Yasemin Kemeç Hürkan
,
Cüneyt Akı
Öz
Smoke water (SW) is produced naturally or artificially from burning plant material. It provides the germination of the seeds of many plants and accelerates the growth and development of the plant and is also used in many fields of plant science. SW preparation is a relatively easy and inexpensive method, but a standard method for its preparation has not been developed yet. Therefore, the aim of this research is to develop a low-cost efficient method to produce SW, to standardize it and to measure the amount of the main active biomolecule karrikin (KAR1) by HPLC. We also aimed to test and compare the best working concentration of SW and commercially available KAR1 on apricot (Prunus armeniaca L.) seeds. The SWs were diluted to 1:100, 1:500, 1:1000, 1:5000 and 1:10000 ratios, and KAR1 to 0.01 μM, 0.1 μM, 1 μM, 5 μM and 10 μM concentrations. In terms of germination, it was determined that the use of 1:1000 (60%) concentration in the SW group and 1 μM (72%) concentration in the KAR1 group was appropriate. This is the first research in which a standard method was developed for obtaining SW. We think this study will be a guide to researchers who plan to study with smoke water, since we obtained the most concentrated KAR1 according to the literature.
Destekleyen Kurum
Çanakkale Onsekiz Mart Üniversitesi Bilimsel Araştırma Projeleri Koordinasyon Birimi
Proje Numarası
FDK-2020-3345
Teşekkür
This research was supported by Council of Higher Education 100/2000 Fellowship Program, TÜBİTAK-BİDEB 2211/A National PhD Scholarship Program and the project FDK-2020-3345 by Çanakkale Onsekiz Mart University Scientific Research Projects Coordination Unit. I would like to thank Assist. Prof. Dr. Kaan HURKAN for his help throughout the study. This research is a part of a Mrs. Yasemin KEMEÇ HÜRKAN’s Doctoral thesis.
Kaynakça
- Artık N, Velioğlu S & Kavalcı B (1993). Şeker alkollerden ksilitol; özellikleri üretimi ve gıdalarda kullanımı. Gıda 18:101-109
- Baldwin I T, Staszak K L & Davidson R (1994). Up in smoke: I. Smoke-derived germination cues for postfire annual, Nicotiana attenuata torr. Ex. Watson. Journal of Chemical Ecology 20(9): 2345-2371. https://doi.org/10.1007/BF02033207
- Baxter B J M & Van Staden J (1994). Plant-derived smoke: an effective seed pre-treatment. Plant Growth Regulation 14(3): 279-282. https://doi.org/10.1007/BF00024804
- Baxter B J M, Van Staden J, Granger J E & Brown N A C (1994). Plant-derived smoke and smoke extracts stimulate seed germination of the fire-climax grass Themeda triandra. Environmental and Experimental Botany 34(2): 217-223. https://doi.org/10.1016/0098-8472(94)90042-6
- Beeby A & Brennan A M (1997). First Ecology. Chapman & Hall, London
- Bewley J (1997). Seed germination and dormancy. Plant Cell 9: 1055-1066.
- Brown N A C & Van Staden J (1997). Smoke as a germination cue: A review. Plant Growth Regulation 22(2): 115-124. https://doi.org/10.1023/A:1005852018644
- Çatav Ş S, Bekar I, Ateş B S, Ergan G, Oymak F, Ülker E D & Tavşanoǧlu Ç (2012). Germination response of five eastern Mediterranean woody species to smoke solutions derived from various plants. Turkish Journal of Botany 36(5): 480-487. https://doi.org/10.3906/bot-1111-12
- Çatav Ş S, Elgin E S, Dağ Ç, Stark J L & Küçükakyüz K (2018). NMR-based metabolomics reveals that plant-derived smoke stimulates root growth via affecting carbohydrate and energy metabolism in maize. Metabolomics 14(11): 1-11. https://doi.org/10.1007/s11306-018-1440-y
- Çatav Ş S, Küçükakyüz K, Akbaş K & Tavşanoǧlu Ç (2014). Smoke-enhanced seed germination in Mediterranean Lamiaceae. Seed Science Research 24(3): 257-264. https://doi.org/10.1017/S0960258514000142
- Çatav Ş S, Küçükakyüz K, Tavşanoğlu Ç & Pausas J G (2018). Effect of fire-derived chemicals on germination and seedling growth in Mediterranean plant species. Basic and Applied Ecology 30: 65-75. https://doi.org/10.1016/j.baae.2018.05.005
- Chiwocha S D S, Dixon K W, Flematti G R, Ghisalberti E L, Merritt D J, Nelson D C, … Stevens J C (2009). Karrikins: A new family of plant growth regulators in smoke. Plant Science 177(4): 252-256. https://doi.org/10.1016/j.plantsci.2009.06.007
- Christensen N L (1985). Shrubland fire regimes and their evolutionary consequences. In P. S. T. A & P. S. White (Eds.), The Ecology of Natural Disturbance and Patch Dynamics, Academic Press, London, pp. 85-100
- Chumpookam J, Lin H L & Shiesh C C (2012). Effect of smoke-water on seed germination and seedling growth of papaya (Carica papaya cv.Tainung No.2). HortScience 47(6): 741-744. https://doi.org/10.37855/jah.2012.v14i02.23
- Commander L, Merritt D, Rokich D & Dixon K (2009). Seed biology of Australian arid zone species: germination of 18 species used for rehabilitation. Journal of Arid Environments 73: 617-625.
- Daws M, Davies J, Pritchard H, NAC B & Van Staden J (2007). Butenolide from plant-derived smoke enhances germination and seedling growth of arable weeds species. Plant Growth Regul 51: 73-82.
- De Cuyper C, Struk S, Braem L, Gevaert K, De Jaeger G & Goormachtig S (2017). Strigolactones, karrikins and beyond. Plant Cell and Environment 40(9): 1691-1703. https://doi.org/10.1111/pce.12996
- De Lange J H & Boucher C (1990). Autecological studies on Audouinia capitata (Bruniaceae). I. Plant-derived smoke as a seed germination cue. South African Journal of Botany 56(6): 700-703. https://doi.org/10.1016/s0254-6299(16)31009-2
- Downes K S, Light M E, Pošta M, Kohout L & Van Staden J (2013). 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. Annals of Botany 111(3): 489-497. https://doi.org/10.1093/aob/mcs300
- Flematti G R, Dixon K W & Smith S M (2015). What are karrikins and how were they “discovered” by plants? BMC Biology 13(1): 1-7. https://doi.org/10.1186/s12915-015-0219-0
- Flematti G R, Ghisalberti E L, Dixon K W & Trengove R D (2004). A compound from smoke that promotes seed germination. Science 305: 977. https://doi.org/10.1126/science.1099944
- Flematti G R, Ghisalberti E L, Dixon K W & Trengove R D (2009). Identification of alkyl substituted 2H-furo[2,3-c]pyran-2-ones as germination stimulants present in smoke. Journal of Agricultural and Food Chemistry 57(20): 9475-9480. https://doi.org/10.1021/jf9028128
- Flematti G R, Scaffidi A, Dixon K W, Smith S M & Ghisalberti E L (2011). Production of the seed germination stimulant karrikinolide from combustion of simple carbohydrates. Journal of Agricultural and Food Chemistry 59(4): 1195-1198. https://doi.org/10.1021/jf1041728
- Grossmann K (1990). Plant growth retardants as tools in physiological research. Physiologia Plantarum 78: 640-648.
- Gupta S, Hrdlicka J, Ngoroyemoto N, Nemahunguni N K, Gucky T, Novak O, … Van Staden J (2019). Preparation and standardisation of smoke‑water for seed germination and plant growth stimulation. Journal of Plant Growth Regulation 1-8.
- Hrdlička J, Gucký T, Novák O, Kulkarni M, Gupta S, Van Staden J & Doležal K (2019). Quantification of karrikins in smoke water using ultra-high performance liquid chromatography-tandem mass spectrometry. Plant Methods 15(1): 1-12. https://doi.org/10.1186/s13007-019-0467-z
- Kazancı D D (2014). Akdeniz Bitkilerinin Yangın Sonrası Çimlenme Özelliklerinin Belirlenmesi. Hacettepe Üniversitesi.
- Keeley J E, Morton B A, Pedrosa A & Trotter P (1985). Role of allelopathy , heat and charred wood in the germination of chaparral herbs and suffrutescents. Journal of Ecology 73(2): 445-458.
- Keeley J E & Fotheringham C J (1997). Trace gas emissions and smoke-induced seed germination. Science 276: 1248-1250.
- Keeley Jon E & Fotheringham C J (1998). Smoke-induced seed germination in California chaparral. Ecology 79(7): 2320-2336. https://doi.org/10.1890/0012-9658(1998)079[2320:SISGIC]2.0.CO;2
- Keeley J E (1995). Seed-Germination patterns in fire-prone mediterranean-climate regions. In M T K Arroyo, P H Zedler & M D Fox (Eds.), Ecology and Biogeography of Mediterranean Ecosystems in Chile, California and Australia, Springer-Verlag, New York, pp. 239-273
- Keeley S C & Pizzorno M (1986). Charred Wood stimulated germination of two fire-following herbs of the california chaparral and the role of hemicellulose. American Journal of Botany 73(9): 1289-1297. https://doi.org/10.1002/j.1537-2197.1986.tb10870.x
- Kemeç Hürkan Y & Akı C (2022). Surface sterilization optimization in seeds of şalak apricot variety (Prunus armeniaca L. cv. Şalak). Journal of the Institute of Science and Technology 12(3): 1358-1363. https://doi.org/10.21597/jist
- Kochanek J, Long R L, Lisle A T & Flematti G R (2016). Karrikins identified in biochars indicate post-fire chemical cues can influence community diversity and plant development. PLoS ONE 11(8): 1-19. https://doi.org/10.1371/journal.pone.0161234
- Kucera B, Cohn M & Leubner Metzger G (2005). Plant hormone interactions during seed dormancy release and germination. Seed Science Research 15: 281-307.
- Light M E, Daws M I & Van Staden J (2009). Smoke-derived butenolide: Towards understanding its biological effects. South African Journal of Botany 75(1): 1-7. https://doi.org/10.1016/j.sajb.2008.10.004
- Light M E, Gardner M J, Jäger A K & Van Staden J (2002). Dual regulation of seed germination by smoke solutions. Plant Growth Regulation 37(2): 135-141. https://doi.org/10.1023/A:1020536711989
- Light Marnie E, Burger B V, Staerk D, Kohout L & Van Staden J (2010). Butenolides from plant-derived smoke: natural plant-growth regulators with antagonistic actions on seed germination. Journal of Natural Products 73(2): 267-269. https://doi.org/10.1021/np900630w
- Merritt D, Kristiansen M, Flematti G R, Turner S & EL G (2006). Effects of a butenolide present in smoke on light-mediated germination of Australian Asteraceae. Seed Science Research 16: 29-35.
- Nelson D C, Flematti G R, Ghisalberti E L, Dixon K W & Smith S M (2012). Regulation of seed germination and seedling growth by chemical signals from burning vegetation. Annual Review of Plant Biology 63: 107-130. https://doi.org/10.1146/annurev-arplant-042811-105545
- Nelson D C, Riseborough J A, Flematti G R, Stevens J, Ghisalberti E L, Dixon K W & Smith S M (2009). Karrikins discovered in smoke trigger arabidopsis seed germination by a mechanism requiring gibberellic acid synthesis and light. Plant Physiology 149(2): 863-873. https://doi.org/10.1104/pp.108.131516
- Shabir S, Ilyas N, Asif S, Iqbal M, Kanwal S & Ali Z (2021). Deciphering the role of plant-derived smoke solution in ameliorating saline stress and improving physiological, biochemical, and growth responses of wheat. Journal of Plant Growth Regulation 41(7): 2769-2786. https://doi.org/10.1007/s00344-021-10473-5
- Stevens J, Merritt D, Flematti G, Ghisalberti E & Dixon K (2007). 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 298: 113-24.
- Tavşanoğlu Ç, Gürkan B (2004). Akdeniz havzasında bitkilerin kuraklık ve yangına uyumları. OT Sistematik Tanik Dergisi 11(1): 119-132.
- Tavşanoğlu Ç (2011). Fire-related cues (heat shock and smoke) and seed germination in a Cistus creticus population in Southwestern Turkey. Ekoloji 20(79): 99-104. https://doi.org/10.5053/ekoloji.2011.7913
- Tavsanoǧlu C, Ergan G, Çatav S S, Zare G, Küçükakyüz K & Özüdoǧru B (2017). Multiple fire-related cues stimulate germination in Chaenorhinum rubrifolium (Plantaginaceae), a rare annual in the Mediterranean Basin. Seed Science Research 27(1): 26-38. https://doi.org/10.1017/S0960258516000283
- Türkan İ, Tokur S & Öztürk M (1985). Akdeniz ekosistemleri. Akdeniz Ekosistemleri, Doğa Bilim Dergisi A, 2, 9.
- Van Staden J, Jäger A K, Light M E & Burger B V (2004). Isolation of the major germination cue from plant-derived smoke. South African Journal of Botany 70(4): 654-659. https://doi.org/10.1016/S0254-6299(15)30206-4
- Van Staden J, Jager A & Strydom A (1995). Interaction between a plant-derived smoke extract, light and phytohormones on the germination of light-sensitive lettuce seeds. Plant Growth Regul 17: 213-218.
- Van Staden J, Brown N A C, Jäger A K & Johnson T A (2000). Smoke as a germination cue. Plant Species Biology 15(2): 167-178. https://doi.org/10.1046/j.1442-1984.2000.00037.x
- Yüksel F (2017). Fungal inokulasyon yoluyla buğday samanı lignoselülozik içeriğinin parçalanması ve in situ naylon torbatekniği ile yem değerinin belirlenmesi. Atatürk Üniversitesi.
Yıl 2023,
Cilt: 29 Sayı: 3, 800 - 810, 25.09.2023
Yasemin Kemeç Hürkan
,
Cüneyt Akı
Proje Numarası
FDK-2020-3345
Kaynakça
- Artık N, Velioğlu S & Kavalcı B (1993). Şeker alkollerden ksilitol; özellikleri üretimi ve gıdalarda kullanımı. Gıda 18:101-109
- Baldwin I T, Staszak K L & Davidson R (1994). Up in smoke: I. Smoke-derived germination cues for postfire annual, Nicotiana attenuata torr. Ex. Watson. Journal of Chemical Ecology 20(9): 2345-2371. https://doi.org/10.1007/BF02033207
- Baxter B J M & Van Staden J (1994). Plant-derived smoke: an effective seed pre-treatment. Plant Growth Regulation 14(3): 279-282. https://doi.org/10.1007/BF00024804
- Baxter B J M, Van Staden J, Granger J E & Brown N A C (1994). Plant-derived smoke and smoke extracts stimulate seed germination of the fire-climax grass Themeda triandra. Environmental and Experimental Botany 34(2): 217-223. https://doi.org/10.1016/0098-8472(94)90042-6
- Beeby A & Brennan A M (1997). First Ecology. Chapman & Hall, London
- Bewley J (1997). Seed germination and dormancy. Plant Cell 9: 1055-1066.
- Brown N A C & Van Staden J (1997). Smoke as a germination cue: A review. Plant Growth Regulation 22(2): 115-124. https://doi.org/10.1023/A:1005852018644
- Çatav Ş S, Bekar I, Ateş B S, Ergan G, Oymak F, Ülker E D & Tavşanoǧlu Ç (2012). Germination response of five eastern Mediterranean woody species to smoke solutions derived from various plants. Turkish Journal of Botany 36(5): 480-487. https://doi.org/10.3906/bot-1111-12
- Çatav Ş S, Elgin E S, Dağ Ç, Stark J L & Küçükakyüz K (2018). NMR-based metabolomics reveals that plant-derived smoke stimulates root growth via affecting carbohydrate and energy metabolism in maize. Metabolomics 14(11): 1-11. https://doi.org/10.1007/s11306-018-1440-y
- Çatav Ş S, Küçükakyüz K, Akbaş K & Tavşanoǧlu Ç (2014). Smoke-enhanced seed germination in Mediterranean Lamiaceae. Seed Science Research 24(3): 257-264. https://doi.org/10.1017/S0960258514000142
- Çatav Ş S, Küçükakyüz K, Tavşanoğlu Ç & Pausas J G (2018). Effect of fire-derived chemicals on germination and seedling growth in Mediterranean plant species. Basic and Applied Ecology 30: 65-75. https://doi.org/10.1016/j.baae.2018.05.005
- Chiwocha S D S, Dixon K W, Flematti G R, Ghisalberti E L, Merritt D J, Nelson D C, … Stevens J C (2009). Karrikins: A new family of plant growth regulators in smoke. Plant Science 177(4): 252-256. https://doi.org/10.1016/j.plantsci.2009.06.007
- Christensen N L (1985). Shrubland fire regimes and their evolutionary consequences. In P. S. T. A & P. S. White (Eds.), The Ecology of Natural Disturbance and Patch Dynamics, Academic Press, London, pp. 85-100
- Chumpookam J, Lin H L & Shiesh C C (2012). Effect of smoke-water on seed germination and seedling growth of papaya (Carica papaya cv.Tainung No.2). HortScience 47(6): 741-744. https://doi.org/10.37855/jah.2012.v14i02.23
- Commander L, Merritt D, Rokich D & Dixon K (2009). Seed biology of Australian arid zone species: germination of 18 species used for rehabilitation. Journal of Arid Environments 73: 617-625.
- Daws M, Davies J, Pritchard H, NAC B & Van Staden J (2007). Butenolide from plant-derived smoke enhances germination and seedling growth of arable weeds species. Plant Growth Regul 51: 73-82.
- De Cuyper C, Struk S, Braem L, Gevaert K, De Jaeger G & Goormachtig S (2017). Strigolactones, karrikins and beyond. Plant Cell and Environment 40(9): 1691-1703. https://doi.org/10.1111/pce.12996
- De Lange J H & Boucher C (1990). Autecological studies on Audouinia capitata (Bruniaceae). I. Plant-derived smoke as a seed germination cue. South African Journal of Botany 56(6): 700-703. https://doi.org/10.1016/s0254-6299(16)31009-2
- Downes K S, Light M E, Pošta M, Kohout L & Van Staden J (2013). 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. Annals of Botany 111(3): 489-497. https://doi.org/10.1093/aob/mcs300
- Flematti G R, Dixon K W & Smith S M (2015). What are karrikins and how were they “discovered” by plants? BMC Biology 13(1): 1-7. https://doi.org/10.1186/s12915-015-0219-0
- Flematti G R, Ghisalberti E L, Dixon K W & Trengove R D (2004). A compound from smoke that promotes seed germination. Science 305: 977. https://doi.org/10.1126/science.1099944
- Flematti G R, Ghisalberti E L, Dixon K W & Trengove R D (2009). Identification of alkyl substituted 2H-furo[2,3-c]pyran-2-ones as germination stimulants present in smoke. Journal of Agricultural and Food Chemistry 57(20): 9475-9480. https://doi.org/10.1021/jf9028128
- Flematti G R, Scaffidi A, Dixon K W, Smith S M & Ghisalberti E L (2011). Production of the seed germination stimulant karrikinolide from combustion of simple carbohydrates. Journal of Agricultural and Food Chemistry 59(4): 1195-1198. https://doi.org/10.1021/jf1041728
- Grossmann K (1990). Plant growth retardants as tools in physiological research. Physiologia Plantarum 78: 640-648.
- Gupta S, Hrdlicka J, Ngoroyemoto N, Nemahunguni N K, Gucky T, Novak O, … Van Staden J (2019). Preparation and standardisation of smoke‑water for seed germination and plant growth stimulation. Journal of Plant Growth Regulation 1-8.
- Hrdlička J, Gucký T, Novák O, Kulkarni M, Gupta S, Van Staden J & Doležal K (2019). Quantification of karrikins in smoke water using ultra-high performance liquid chromatography-tandem mass spectrometry. Plant Methods 15(1): 1-12. https://doi.org/10.1186/s13007-019-0467-z
- Kazancı D D (2014). Akdeniz Bitkilerinin Yangın Sonrası Çimlenme Özelliklerinin Belirlenmesi. Hacettepe Üniversitesi.
- Keeley J E, Morton B A, Pedrosa A & Trotter P (1985). Role of allelopathy , heat and charred wood in the germination of chaparral herbs and suffrutescents. Journal of Ecology 73(2): 445-458.
- Keeley J E & Fotheringham C J (1997). Trace gas emissions and smoke-induced seed germination. Science 276: 1248-1250.
- Keeley Jon E & Fotheringham C J (1998). Smoke-induced seed germination in California chaparral. Ecology 79(7): 2320-2336. https://doi.org/10.1890/0012-9658(1998)079[2320:SISGIC]2.0.CO;2
- Keeley J E (1995). Seed-Germination patterns in fire-prone mediterranean-climate regions. In M T K Arroyo, P H Zedler & M D Fox (Eds.), Ecology and Biogeography of Mediterranean Ecosystems in Chile, California and Australia, Springer-Verlag, New York, pp. 239-273
- Keeley S C & Pizzorno M (1986). Charred Wood stimulated germination of two fire-following herbs of the california chaparral and the role of hemicellulose. American Journal of Botany 73(9): 1289-1297. https://doi.org/10.1002/j.1537-2197.1986.tb10870.x
- Kemeç Hürkan Y & Akı C (2022). Surface sterilization optimization in seeds of şalak apricot variety (Prunus armeniaca L. cv. Şalak). Journal of the Institute of Science and Technology 12(3): 1358-1363. https://doi.org/10.21597/jist
- Kochanek J, Long R L, Lisle A T & Flematti G R (2016). Karrikins identified in biochars indicate post-fire chemical cues can influence community diversity and plant development. PLoS ONE 11(8): 1-19. https://doi.org/10.1371/journal.pone.0161234
- Kucera B, Cohn M & Leubner Metzger G (2005). Plant hormone interactions during seed dormancy release and germination. Seed Science Research 15: 281-307.
- Light M E, Daws M I & Van Staden J (2009). Smoke-derived butenolide: Towards understanding its biological effects. South African Journal of Botany 75(1): 1-7. https://doi.org/10.1016/j.sajb.2008.10.004
- Light M E, Gardner M J, Jäger A K & Van Staden J (2002). Dual regulation of seed germination by smoke solutions. Plant Growth Regulation 37(2): 135-141. https://doi.org/10.1023/A:1020536711989
- Light Marnie E, Burger B V, Staerk D, Kohout L & Van Staden J (2010). Butenolides from plant-derived smoke: natural plant-growth regulators with antagonistic actions on seed germination. Journal of Natural Products 73(2): 267-269. https://doi.org/10.1021/np900630w
- Merritt D, Kristiansen M, Flematti G R, Turner S & EL G (2006). Effects of a butenolide present in smoke on light-mediated germination of Australian Asteraceae. Seed Science Research 16: 29-35.
- Nelson D C, Flematti G R, Ghisalberti E L, Dixon K W & Smith S M (2012). Regulation of seed germination and seedling growth by chemical signals from burning vegetation. Annual Review of Plant Biology 63: 107-130. https://doi.org/10.1146/annurev-arplant-042811-105545
- Nelson D C, Riseborough J A, Flematti G R, Stevens J, Ghisalberti E L, Dixon K W & Smith S M (2009). Karrikins discovered in smoke trigger arabidopsis seed germination by a mechanism requiring gibberellic acid synthesis and light. Plant Physiology 149(2): 863-873. https://doi.org/10.1104/pp.108.131516
- Shabir S, Ilyas N, Asif S, Iqbal M, Kanwal S & Ali Z (2021). Deciphering the role of plant-derived smoke solution in ameliorating saline stress and improving physiological, biochemical, and growth responses of wheat. Journal of Plant Growth Regulation 41(7): 2769-2786. https://doi.org/10.1007/s00344-021-10473-5
- Stevens J, Merritt D, Flematti G, Ghisalberti E & Dixon K (2007). 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 298: 113-24.
- Tavşanoğlu Ç, Gürkan B (2004). Akdeniz havzasında bitkilerin kuraklık ve yangına uyumları. OT Sistematik Tanik Dergisi 11(1): 119-132.
- Tavşanoğlu Ç (2011). Fire-related cues (heat shock and smoke) and seed germination in a Cistus creticus population in Southwestern Turkey. Ekoloji 20(79): 99-104. https://doi.org/10.5053/ekoloji.2011.7913
- Tavsanoǧlu C, Ergan G, Çatav S S, Zare G, Küçükakyüz K & Özüdoǧru B (2017). Multiple fire-related cues stimulate germination in Chaenorhinum rubrifolium (Plantaginaceae), a rare annual in the Mediterranean Basin. Seed Science Research 27(1): 26-38. https://doi.org/10.1017/S0960258516000283
- Türkan İ, Tokur S & Öztürk M (1985). Akdeniz ekosistemleri. Akdeniz Ekosistemleri, Doğa Bilim Dergisi A, 2, 9.
- Van Staden J, Jäger A K, Light M E & Burger B V (2004). Isolation of the major germination cue from plant-derived smoke. South African Journal of Botany 70(4): 654-659. https://doi.org/10.1016/S0254-6299(15)30206-4
- Van Staden J, Jager A & Strydom A (1995). Interaction between a plant-derived smoke extract, light and phytohormones on the germination of light-sensitive lettuce seeds. Plant Growth Regul 17: 213-218.
- Van Staden J, Brown N A C, Jäger A K & Johnson T A (2000). Smoke as a germination cue. Plant Species Biology 15(2): 167-178. https://doi.org/10.1046/j.1442-1984.2000.00037.x
- Yüksel F (2017). Fungal inokulasyon yoluyla buğday samanı lignoselülozik içeriğinin parçalanması ve in situ naylon torbatekniği ile yem değerinin belirlenmesi. Atatürk Üniversitesi.