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Vegetation-derived abscisic acid and four terpenes enforce dormancy in seeds of the post-fire annual, Nicotiana attenuata

Published online by Cambridge University Press:  22 February 2007

Bernd Krock ,
Sybille Schmidt ,
Christian Hertweck  and
Ian T. Baldwin
Bernd Krock
Affiliation:
Max-Planck-Institut für Chemische Ökologie, Carl-Zeiss-Promenade 10, D-07745 Jena, Germany
Sybille Schmidt
Affiliation:
Max-Planck-Institut für Chemische Ökologie, Carl-Zeiss-Promenade 10, D-07745 Jena, Germany
Christian Hertweck
Affiliation:
Max-Planck-Institut für Chemische Ökologie, Carl-Zeiss-Promenade 10, D-07745 Jena, Germany Hans-Knöll-Institut für Naturstofforschung, Beutenbergstr. 11a, D-07745 Jena, Germany
Ian T. Baldwin*
Affiliation:
Max-Planck-Institut für Chemische Ökologie, Carl-Zeiss-Promenade 10, D-07745 Jena, Germany
*
*Correspondence Fax: +49-(0)-3641-643653 Email: [email protected]
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Abstract

The native tobacco, Nicotiana attenuata, synchronizes its germination with the immediate post-fire environment with a combination of germination stimulants found in wood smoke and inhibitors from the unburned litter of the dominant vegetation. The inhibitors override the stimulants and prevent seeds from germinating maladaptively in unburned habitats adjacent to burns. To understand the physiological basis of this environmental control of germination, we tested several previously isolated signals, phytohormones and their respective biosynthesis inhibitors. The germination inhibitors methyl jasmonate (MeJA, a constituent of sagebrush litter), bornane-2,5-dione (BD, a constituent of juniper litter extract, JLE) and JLE did not alter abscisic acid (ABA) content of imbibed seeds. Treatment with the ABA biosynthesis inhibitor, fluridone, inhibited the dormancy-inducing effects of BD, JLE and MeJA, but surprisingly did not affect endogenous ABA levels in treated seeds. However, ABA leached from litter of the species, which dominate the plant community before fires, plays an important role in germination control. We conclude that N. attenuata seeds, which can lie dormant in the soil for 150 years between fires, time their germination with the post-fire environment by responding to smoke, ABA and four terpenes (BD, 1,8-cineole, β-thujaplicin and camphor) leaching from the litter of the dominant vegetation.

Keywords

Nicotiana attenuatasecondary dormancysmokeabscisic acidgibberellic acidfluridonemethyl jasmonatebornane-25-dione
Type
Research Article
Information
Seed Science Research , Volume 12 , Issue 4 , December 2002 , pp. 239 - 252
Copyright
Copyright © Cambridge University Press 2002

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References

Baldwin, I.T. 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, 2373–2391.CrossRefGoogle ScholarPubMed
Baldwin, I.T., 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, 2345–2371.Google Scholar
Barney, M.A. and Frischknecht, N.C. (1974) Vegetation changes following fire in the pinyon-juniper type of west-central Utah. Journal of Range Management 27, 91–96.Google Scholar
Baskin, C.C. and Baskin, J.M. (1998) Seeds: Ecology, biogeography and evolution of dormancy and germination. San Diego, Academic Press.Google Scholar
Baxter, B.J.M. and van Staden, J. (1994) Plant-derived smoke: an effective seed pre-treatment. Plant Growth Regulation 14, 279–282.CrossRefGoogle Scholar
Bewley, J.D. (1997) Seed germination and dormancy. Plant Cell 9, 1055–1066.CrossRefGoogle ScholarPubMed
Bewley, J.D. and Black, M. (1994) Seeds. Physiology of development and germination (2nd edition). New York, Plenum Press.Google Scholar
Bredt, J. (1923) Über die Bildung von Diketocamphan (Ketocampher) und von Diketofenchan (Ketofenchon) bei der Oxydation des Camphers bzw. des Fenchons mit Chromsäure. Journal für Praktische Chemie 106, 336–343.CrossRefGoogle Scholar
Brotherson, J.D., Szyska, L.A. and Evenson, W.E. (1980) Poisonous plants of Utah. Great Basin Naturalist 40, 229–253.Google Scholar
Brown, J.S. and Venable, D.L. (1986) Evolutionary ecology of seed-bank annuals in temporally varying environments. American Naturalist 127, 31–47.Google Scholar
Brown, N.A.C. (1993) Promotion of germination of fynbos seeds by plant-derived smoke. New Phytologist 123, 575–583.Google Scholar
Christensen, N.L. and Muller, C.H. (1975a) Effects of fire on factors controlling plant growth in Adenostoma chaparral. Ecological Monographs 45, 29–55.CrossRefGoogle Scholar
Christensen, N.L. and Muller, C.H. (1975b) Relative importance of factors controlling germination and seedling survival in Adenostoma chaparral. American Midland Naturalist 93, 71–78.CrossRefGoogle Scholar
Cutler, A.J. and Krochko, J.E. (1999) Formation and breakdown of ABA. Trends in Plant Science 4, 472–478.Google Scholar
Debeaujon, I. and Koornneef, M. (2000) Gibberellin requirement for Arabidopsis seed germination is determined both by testa characteristics and embryonic abscisic acid. Plant Physiology 122, 415–424.Google Scholar
Egerton-Warburton, L.M. and Ghisalberti, E.L. (2001) Isolation and structural identification of a germination inhibitor in fire-recruiters from the California chaparral. Journal of Chemical Ecology 27, 371–382.Google Scholar
Emery, D.E. (1992) Seed propagation of native California plants. Santa Barbara, CA, Santa Barbara Botanic Garden.Google Scholar
Frey, A., Audran, C., Marin, E., Sotta, B. and Marion-Poll, A. (1999) Engineering seed dormancy by the modification of zeaxanthin epoxidase gene expression. Plant Molecular Biology 39, 1267–1274.CrossRefGoogle ScholarPubMed
Garello, G., Barthe, P., Bonelli, M., Bianco-Trinchant, J., Bianco, J. and Le Page-Degivry, M.-T. (2000) Abscisic acid-regulated responses of dormant and non-dormant embryos of Helianthus annuus: Role of ABA-inducible proteins. Plant Physiology and Biochemistry 38, 473–482.Google Scholar
Goodspeed, T.H. (1954) The genus Nicotiana. Waltham, MA, Chronica Botanica Co.Google Scholar
Grappin, P., Bouinot, D., Sotta, B., Miginiac, E. and Jullien, M. (2000) Control of seed dormancy in Nicotiana plumbaginafolia: a post-imbibition abscisic acid synthesis imposes dormancy maintenance. Planta 210, 279–285.Google Scholar
Grossmann, K. (1990) Plant growth retardants as tools in physiological research. Physiologia Plantarum 78, 640–648.Google Scholar
Harper, J.L. (1994) Population biology of plants. San Diego, Academic Press.Google Scholar
Hedden, P. and Kamiya, Y. (1997) Gibberellin biosynthesis: enzymes, genes and their regulation. Annual Review of Plant Physiology and Plant Molecular Biology 48, 431–460.Google Scholar
Hegenauer, R. (1973) Chemotaxonomie der Pflanzen. Vol. 1. Stuttgart, Birkhäuser Verlag.CrossRefGoogle Scholar
Hilhorst, H.W.M., Smitt, A.I. and Karssen, C.M. (1986) Gibberellin-biosynthesis and sensitivity-mediated stimulation of seed germination of Sisymbrium officinale by red light and nitrate. Physiologia Plantarum 67, 285–290.CrossRefGoogle Scholar
Iglesias, R.G. and Babiano, M.J. (1997) Endogenous abscisic acid during the germination of chick-pea seeds. Physiologia Plantarum 100, 500–504.Google Scholar
Jullien, M. and Bouinot, D. (1997) Seed dormancy and responses of seeds to phytohormones in Nicotiana plumbaginifolia. pp.203–214 in Ellis, R.H.; Black, M.; Murdoch, A.J.; Hong, T.D. (Eds) Basic and applied aspects of seed biology. Dordrecht, Kluwer Academic.Google Scholar
Karssen, C.M. (1976) Two sites of hormonal action during germination of Chenopodium album seeds. Physiologia Plantarum 36, 264–270.Google Scholar
Karssen, C.M. and Laçka, E. (1985) A revision of the hormone balance theory of seed dormancy: studies on gibberellin and/or abscisic acid-deficient mutants of Arabidopsis thaliana. pp.315–323 in Bopp, M. (Ed.) Plant growth substances 1985. Berlin, Springer-Verlag.Google Scholar
Keeley, J.E. and Fotheringham, C.J. (1997) Trace gas emissions and smoke-induced seed germination. Science 276, 1248–1250.Google Scholar
Keeley, J.E., Morton, B.A., Pedrosa, A. and Trotter, P. (1985) Role of allelopathy, heat and charred wood in the germination of chaparral herbs and suffrutescents. Journal of Ecology 73, 445–458.Google Scholar
Keeley, S.C. and 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, 1289–1297.Google Scholar
Koniak, S. (1985) Succession in pinyon-juniper woodlands following wildfire in the Great Basin. Great Basin Naturalist 45, 556–566.Google Scholar
Koornneef, M., Leon-Kloosterziel, K.M., Schwartz, S.H. and Zeevaart, J.A.D. (1998) The genetic and molecular dissection of abscisic acid biosynthesis and signal transduction in Arabidopsis. Plant Physiology and Biochemistry 36, 83–89.CrossRefGoogle Scholar
Le Page-Degivry, M.-T. and Garello, G. (1992) In situ abscisic acid synthesis - a requirement for induction of dormancy in Helianthus annuus. Plant Physiology 98, 1386–1390.CrossRefGoogle ScholarPubMed
Leubner-Metzger, G. and Meins, F. (2000) Sense transformation reveals a novel role for class I β-1,3-glucanase in tobacco seed germination. Plant Journal 23, 215–221.CrossRefGoogle Scholar
Leubner-Metzger, G., Fründt, C., Vögeli-Lange, R. and Meins, F. (1995) Class I β-1,3-glucanases in the endosperm of tobacco during germination. Plant Physiology 109, 751–759.Google Scholar
Leubner-Metzger, G., Fründt, C. and Meins, F. (1996) Effects of gibberellins, darkness and osmotica on endosperm rupture and class I β-1,3-glucanase inductionin tobacco seed germination. Planta 199, 282–288.CrossRefGoogle Scholar
Lynds, G.Y. and Baldwin, I.T. (1998) Fire, nitrogen, and defensive plasticity in Nicotiana attenuata. Oecologia 115, 531–540.Google ScholarPubMed
Mirov, N.T. (1936) Germination behavior of some California plants. Ecology 17, 667–672.Google Scholar
Ni, B.R. and Bradford, K.J. (1993) Germination and dormancy of abscisic acid- and gibberellin-deficient mutant tomato (Lycopersicon esculentum) seeds - sensitivity of germination to abscisic acid, gibberellin and water potential. Plant Physiology 101, 607–617.Google Scholar
Philippi, T. (1993a) Bet-hedging germination of desert annuals: Beyond the first year. American Naturalist 142, 474–487.CrossRefGoogle ScholarPubMed
Philippi, T. (1993b) Bet-hedging germination of desert annuals: Variation among populations and maternal effects in Lepidium lasiocarpum. American Naturalist 142, 488–507.Google Scholar
Pierce, S.M., Esler, K. and Cowling, R.M. (1995) Smoke-induced germination of succulents (Mesembryanthemaceae) from fire-prone and fire-free habitats in South Africa. Oecologia 102, 520–522.Google Scholar
Preston, C.A. and Baldwin, I.T. (1999) Positive and negative signals regulate germination in the post-fire annual, Nicotiana attenuata. Ecology 80, 481–494.Google Scholar
Quick, C.R. and Quick, A.S. (1961) Germination of ceanothus seeds. Madroño 16, 23–30.Google Scholar
Ritchie, S. and Gilroy, S. (1998) Gibberellins: regulation genes and germination. New Phytologist 140, 363–383.CrossRefGoogle ScholarPubMed
Romagni, J.G., Allen, S.N. and Dayan, F.E. (2000) Allelopathic effects of volatile cineoles on two weedy plant species. Journal of Chemical Ecology 26, 303–313.Google Scholar
Stone, E.C. and Juhren, G. (1953) Fire stimulated germination: effect of burning on germination of brush seed investigated in physiological study of chamise. California Agriculture 7, 13–14.Google Scholar
Toyomasu, T., Yamane, H., Murofushi, N. and Inoue, Y. (1994) Effects of exogenously applied gibberellins and red light on the endogenous levels of abscisic acid in photoblastic lettuce seeds. Plant and Cell Physiology 35, 127–129.Google Scholar
van de Venter, H.A. and Esterhuizen, A.D. (1988) The effect of factors associated with fire on seed germination of Erica sessiliflora and E. hebecalyx (Ericaceae). South African Journal of Botany 54, 301–304.CrossRefGoogle Scholar
Vleeshouwers, L.M., Bouwmeester, H.J. and Karssen, C.M. (1995) Redefining seed dormancy - an attempt to integrate physiology and ecology. Journal of Ecology 83, 1031–1037.Google Scholar
Wareing, P.F. and Saunders, P.F. (1971) Hormones and dormancy. Annual Review of Plant Physiology 22, 261–288.Google Scholar
Wells, P.V. (1959) An ecological investigation on two desert tobaccos. Ecology 40, 626–644.Google Scholar
Went, F.W., Juhren, G. and Juhren, M.C. (1952) Fire and biotic factors affecting germination. Ecology 33, 351–364.CrossRefGoogle Scholar
White, C.N. and Rivin, C.J. (2000) Gibberellins and seed development in maize. II. Gibberellin biosynthesis inhibition enhances abscisic acid signaling in cultured embryos. Plant Physiology 122, 1089–1097.Google Scholar
Wright, H.A. and Bailey, A.W. (1982) Fire ecology, United States and southern Canada. New York, John Wiley.Google Scholar
Yoshioka, T., Endo, T. and Satoh, S. (1998) Restoration of seed germination at supraoptimal temperatures by fluridone, an inhibitor of abscisic acid biosynthesis. Plant and Cell Physiology 39, 307–312.CrossRefGoogle Scholar
Young, J.A. and Evans, R.A. (1978) Population dynamics after wildfires in sagebrush grasslands. Journal of Range Management 31, 283–289.Google Scholar