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Syringaldehyde is a novel smoke-derived germination cue for the native fire-chasing tobacco, Nicotiana attenuata

Published online by Cambridge University Press:  31 January 2022

Dechang Cao
Affiliation:
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena,, Thüringen07745, Germany
Matthias Schöttner
Affiliation:
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena,, Thüringen07745, Germany
Rayko Halitschke
Affiliation:
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena,, Thüringen07745, Germany
Dapeng Li
Affiliation:
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena,, Thüringen07745, Germany
Gundega Baldwin
Affiliation:
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena,, Thüringen07745, Germany
Catarina Rocha
Affiliation:
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena,, Thüringen07745, Germany
Ian T. Baldwin*
Affiliation:
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena,, Thüringen07745, Germany
*
*Author for Correspondence: Ian T. Baldwin, E-mail: baldwin@ice.mpg.de

Abstract

Smoke-derived seed germination is an important trait for plants to colonize postfire habitats. The well-characterized smoke-derived chemicals of karrikins germinate seeds of species not known to occur after fires in nature. Hence, the ecologically relevant germination cues in smoke remain to be explored for native postfire plants. With the fire-chaser, Nicotiana attenuata, we revisit a bioassay-driven fractionation of liquid smoke to identify ecologically relevant germination cues. By combining bioassay-guided fractionation and comparative unbiased metabolomics, we developed a robust and efficient method to identify germination cues in smoke. Syringaldehyde (SAL) was re-identified as a germination cue in fractions of liquid smoke that promote seed germination. SAL was found to be produced during wildfires in the plant's native habitat, efficiently adsorbed to N. attenuata seeds from aqueous solutions and not readily leached from soil and accurately predicted the boundaries of natural fire events that reflect the occurrence of native postfire N. attenuata populations. We propose that SAL is an ecologically relevant germination cue in smoke for this species.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Bahulikar, RA, Stanculescu, D, Preston, CA and Baldwin, IT (2004) ISSR and AFLP analysis of the temporal and spatial population structure of the post-fire annual, Nicotiana attenuata, in SW Utah. BMC Ecology 4, 12.CrossRefGoogle Scholar
Baldwin, IT and Morse, L (1994) Up in smoke: II. Germination of Nicotiana attenuata in response to smoke-derived cues and nutrients in burned and unburned soils. Journal of Chemical Ecology 20, 23732391.CrossRefGoogle ScholarPubMed
Baldwin, IT, Staszak-Kozinski, L and Davidson, R (1994) Up in smoke: I. Smoke-derived germination cues for postfire annual, Nicotiana attenuata torr. Ex. Watson. Journal of Chemical Ecology 20, 23452371.CrossRefGoogle ScholarPubMed
Baskin, CC and Baskin, JM (2014) Seeds: ecology, biogeography, and evolution of dormancy and germination (2nd edn). San Diego, USA, Academic Press/Elsevier.Google Scholar
Berridge, MV, Herst, PM and Tan, AS (2005) Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnology Annual Review 11, 127152.CrossRefGoogle ScholarPubMed
Bhattacharya, S and Baldwin, IT (2012) The post-pollination ethylene burst and the continuation of floral advertisement are harbingers of non-random mate selection in Nicotiana attenuata. Plant Journal 71, 587601.CrossRefGoogle ScholarPubMed
Bond, WJ and Keeley, JE (2005) Fire as a global ‘herbivore’: the ecology and evolution of flammable ecosystems. Trends in Ecology and Evolution 20, 387394.CrossRefGoogle ScholarPubMed
Bowman, DMJS, Balch, JK, Artaxo, P, WJ, Bond, JM, Carlson, MA, Cochrane, CM, D'antonio, RS, Defries, JC, Doyle, SP, Harrison, FH, Johnston, JE, Keeley, MA, Krawchuk, CA, Kull, JB, Marston, MA, Moritz, IC, Prentice, CI, Roos, AC, Scott, TW, Swetnam, GR, Van Der Werf and SJ, Pyne (2009) Fire in the earth system. Science 324, 481484.CrossRefGoogle ScholarPubMed
Bytebier, B, Antonelli, A, Bellstedt, DU and Linder, HP (2011) Estimating the age of fire in the Cape flora of South Africa from an orchid phylogeny. Proceedings of the Royal Society B: Biological Sciences 278, 188195.CrossRefGoogle ScholarPubMed
Collette, JC and Ooi, MKJ (2017) Germination ecology of the endangered species Asterolasia buxifolia (Rutaceae): smoke response depends on season and light. Australian Journal of Botany 65, 283291.CrossRefGoogle Scholar
Downes, KS, Lamont, BB, Light, ME and van Staden, J (2010) The fire ephemeral Tersonia cyathiflora (Gyrostemonaceae) germinates in response to smoke but not the butenolide 3-methyl-2H-furo[2,3-c]pyran-2-one. Annals of Botany 106, 381384.CrossRefGoogle Scholar
Downes, KS, Light, ME, Posta, M, Kohout, L and van Staden, J (2014) Do fire-related cues, including smoke-water, karrikinolide, glyceronitrile and nitrate, stimulate the germination of 17 Anigozanthos taxa and Blancoa canescens (Haemodoraceae)? Australian Journal of Botany 62, 347358.CrossRefGoogle Scholar
Flematti, GR, Ghisalberti, EL, Dixon, KW and Trengove, RD (2004) A compound from smoke that promotes seed germination. Science 305, 977.CrossRefGoogle ScholarPubMed
Flematti, GR, Merritt, DJ, Piggott, MJ, RD, Trengove, SM, Smith, KW, Dixon and EL, Ghisalberti (2011) Burning vegetation produces cyanohydrins that liberate cyanide and stimulate seed germination. Nature Communications 2, 360.CrossRefGoogle ScholarPubMed
He, T, Pausas, JG, Belcher, CM, Schwilk, DW and Lamont, BB (2012) Fire-adapted traits of Pinus arose in the fiery Cretaceous. New Phytologist 194, 751759.CrossRefGoogle ScholarPubMed
Heidke, I, Hartland, A, Scholz, D, Pearson, A, Hellstrom, J, SFM, Breitenbach and Hoffmann, T (2021) Lignin oxidation products in soil, dripwater and speleothems from four different sites in New Zealand. Biogeosciences 18, 22892300.CrossRefGoogle Scholar
Keeley, JE and Fotheringham, CJ (1997) Trace gas emissions and smoke-induced seed germination. Science 276, 12481250.CrossRefGoogle Scholar
Keeley, JE and Fotheringham, CJ (1998) Smoke-induced seed germination in California chaparral. Ecology 79, 23202336.CrossRefGoogle Scholar
Keeley, JE and Pausas, JG (2018) Evolution of ‘smoke’ induced seed germination in pyroendemic plants. South African Journal of Botany 115, 251255.CrossRefGoogle Scholar
Keeley, JE, Pausas, JG, Rundel, PW, Bond, WJ and Bradstock, RA (2011) Fire as an evolutionary pressure shaping plant traits. Trends in Plant Science 16, 406411.CrossRefGoogle ScholarPubMed
Krock, B, Schmidt, S, Hertweck, C and Baldwin, IT (2002) Vegetation-derived abscisic acid and four terpenes enforce dormancy in seeds of the post-fire annual, Nicotiana attenuata. Seed Science Research 12, 239252.CrossRefGoogle Scholar
Krügel, T, Lim, M, Gase, K, Halitschke, R and Baldwin, IT (2002) Agrobacterium-mediated transformation of Nicotiana attenuata, a model ecological expression system. Chemoecology 12, 177183.CrossRefGoogle Scholar
Lamont, BB and He, T (2017) Fire-proneness as a prerequisite for the evolution of fire-adapted traits. Trends in Plant Science 22, 278288.CrossRefGoogle ScholarPubMed
Li, F, Bond-Lamberty, B and Levis, S (2014) Quantifying the role of fire in the Earth system. Biogeosciences 11, 1345.CrossRefGoogle Scholar
Light, ME, Gardner, MJ, Jäger, AK and van Staden, J (2002) Dual regulation of seed germination by smoke solutions. Plant Growth Regulation 37, 135141.CrossRefGoogle Scholar
Lynds, GY and Baldwin, IT (1998) Fire, nitrogen, and defensive plasticity in Nicotiana attenuata. Oecologia 115, 531540.Google ScholarPubMed
Manela, N, Dagon, E, Semesh, H and Ovadia, O (2019) Smoke interacts with fire history to stimulate soil seed bank germination in Mediterranean woodlands. Journal of Plant Ecology 12, 419427.CrossRefGoogle Scholar
Morffy, N, Faure, L and Nelson, DC (2016) Smoke and hormone mirrors: action and evolution of karrikin and strigolactone signaling. Trends in Genetics 32, 176188.CrossRefGoogle ScholarPubMed
Nelson, DC, Riseborough, J-A, Flematti, GR, Stevens, J, EL, Ghisalberti, KW, Dixon and SM, Smith (2009) Karrikins discovered in smoke trigger Arabidopsis seed germination by a mechanism requiring gibberellic acid synthesis and light. Plant Physiology 149, 863873.CrossRefGoogle ScholarPubMed
Nelson, DC, Flematti, GR, Riseborough, J-A, Ghisalberti, EL, Dixon, KW and Smith, SM (2010) Karrikins enhance light responses during germination and seedling development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 107, 70957100.CrossRefGoogle ScholarPubMed
Ooi, MKJ (2019) The importance of fire season when managing threatened plant species: a long-term case-study of a rare Leucopogon species (Ericaceae). Journal of Environmental Management 236, 1724.CrossRefGoogle Scholar
Ooi, MKJ, Auld, TD and Whelan, RJ (2004) Delayed post-fire seedling emergence linked to season: a case study with Leucopogon species (Epacridaceae). Plant Ecology 174, 183196.CrossRefGoogle Scholar
Papenfus, HB, Naidoo, D, Pošta, M, Finnie, JF and Staden, JV (2015) The effects of smoke derivatives on in vitro seed germination and development of the leopard orchid Ansellia africanan. Plant Biology 18, 289294.CrossRefGoogle Scholar
Preston, CA and Baldwin, IT (1999) Positive and negative signals regulate germination in the post-fire annual, Nicotiana attenuata. Ecology 80, 481494.CrossRefGoogle Scholar
Preston, C, Betts, H and Baldwin, I (2002) Methyl jasmonate as an allelopathic agent: sagebrush inhibits germination of a neighboring tobacco, Nicotiana attenuata. Journal of Chemical Ecology 28, 23432369.CrossRefGoogle ScholarPubMed
Preston, CA, Becker, R and Baldwin, IT (2004) Is ‘NO’ news good news? Nitrogen oxides are not components of smoke that elicits germination in two smoke-stimulated species, Nicotiana attenuata and Emmenanthe penduliflora. Seed Science Research 14, 7379.CrossRefGoogle Scholar
Scaffidi, A, Waters, MT, Sun, YK, BW, Skelton, KW, Dixon, EL, Ghisalberti, GR, Flematti and SM, Smith (2014) Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiology 165, 12211232.CrossRefGoogle ScholarPubMed
Schuman, MC, Heinzel, N, Gaquerel, E, Svatos, A and Baldwin, IT (2009) Polymorphism in jasmonate signaling partially accounts for the variety of volatiles produced by Nicotiana attenuata plants in a native population. New Phytologist 183, 11341148.CrossRefGoogle Scholar
Schwachtje, J and Baldwin, IT (2004) Smoke exposure alters endogenous gibberellin and abscisic acid pools and gibberellin sensitivity while eliciting germination in the post-fire annual, Nicotiana attenuata. Seed Science Research 14, 5160.CrossRefGoogle Scholar
Sun, YK, Yao, J, Scaffidi, A, KT, Melville, SF, Davies, CS, Bond, SM, Smith, GR, Flematti and MT, Waters (2020) Divergent receptor proteins confer responses to different karrikins in two ephemeral weeds. Nature Communications 11, 1264.CrossRefGoogle ScholarPubMed
Tonnabel, J, Mignot, A, Douzery, EJP, AG, Rebelo, FM, Schurr, Midgley, J, Illing, N, Justy, F, Orcel, D and Olivieri, I (2014) Convergent and correlated evolution of major life-history traits in the angiosperm genus Leucadendron (Proteaceae). Evolution 68, 27752792.CrossRefGoogle Scholar
van Staden, J, Jäger, AK, Light, ME, Burger, BV, Brown, NAC and Thomas, TH (2004) Isolation of the major germination cue from plant-derived smoke. South African Journal of Botany 70, 654659.CrossRefGoogle Scholar
Wang, M, Carver, JJ, Phelan, VV, LM, Sanchez, Garg, N, Peng, Y, DD, Nguyen, Watrous, J, CA, Kapono, Luzzatto-Knaan, T, Porto, C, Bouslimani, A, AV, Melnik, MJ, Meehan, W-T, Liu, Crüsemann, M, PD, Boudreau, Esquenazi, E, Sandoval-Calderón, M, RD, Kersten, LA, Pace, RA, Quinn, KR, Duncan, C-C, Hsu, DJ, Floros, RG, Gavilan, Kleigrewe, K, Northen, T, RJ, Dutton, Parrot, D, EE, Carlson, Aigle, B, CF, Michelsen, Jelsbak, L, Sohlenkamp, C, Pevzner, P, Edlund, A, Mclean, J, Piel, J, BT, Murphy, Gerwick, L, C-C, Liaw, Y-L, Yang, H-U, Humpf, Maansson, M, RA, Keyzers, AC, Sims, AR, Johnson, AM, Sidebottom, BE, Sedio, Klitgaard, A, CB, Larson, PCA, Boya, Torres-Mendoza, D, DJ, Gonzalez, DB, Silva, LM, Marques, DP, Demarque, Pociute, E, EC, O'neill, Briand, E, EJN, Helfrich, EA, Granatosky, Glukhov, E, Ryffel, F, Houson, H, Mohimani, H, JJ, Kharbush, Zeng, Y, JA, Vorholt, KL, Kurita, Charusanti, P, KL, Mcphail, KF, Nielsen, Vuong, L, Elfeki, M, MF, Traxler, Engene, N, Koyama, N, OB, Vining, Baric, R, RR, Silva, SJ, Mascuch, Tomasi, S, Jenkins, S, Macherla, V, Hoffman, T, Agarwal, V, PG, Williams, Dai, J, Neupane, R, Gurr, J, AM, Rodríguez, CLamsa, A, Zhang, C, Dorrestein, K, BM, Duggan, Almaliti, J, P-M, Allard, Phapale, P, L-F, Nothias, Alexandrov, T, Litaudon, M, J-L, Wolfender, JE, Kyle, TO, Metz, Peryea, T, D-T, Nguyen, Vanleer, D, Shinn, P, Jadhav, A, Müller, R, KM, Waters, Shi, W, Liu, X, Zhang, L, Knight, R, PR, Jensen, , Palsson, Pogliano, K, RG, Linington, Gutiérrez, M, NP, Lopes, WH, Gerwick, BS, Moore, PC, Dorrestein and Bandeira, N (2016) Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nature Biotechnology 34, 828837.CrossRefGoogle ScholarPubMed
Zimmerman, GT and Laven, RD (1987) Effects of forest fuel smoke on dwarf mistletoe seed-germination. Great Basin Naturalist 47, 652659.Google Scholar
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Syringaldehyde is a novel smoke-derived germination cue for the native fire-chasing tobacco, Nicotiana attenuata
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