Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-23T19:34:15.507Z Has data issue: false hasContentIssue false
  • English
  • Français

Smoke exposure alters endogenous gibberellin and abscisic acid pools and gibberellin sensitivity while eliciting germination in the post-fire annual, Nicotiana attenuata

Published online by Cambridge University Press:  22 February 2007

Jens Schwachtje  and
Ian T. Baldwin
Jens Schwachtje
Affiliation:
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, Jena, D-07745, Germany
Ian T. Baldwin*
Affiliation:
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, Jena, D-07745, Germany
*
*Correspondence Fax: +49 3641 571 102 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Exposure to smoke is required for the germination of seeds from dormant genotypes of Nicotiana attenuata, a post-fire annual of the Great Basin Desert. Germination can be elicited by GA1,3,4,7 treatments and inhibited by the GA biosynthesis inhibitor, paclobutrazol (PAC), abscisic acid (ABA) and terpenes leached from unburned litter of the plant’s natural habitat. We analysed the endogenous GA and ABA dynamics during the 22 h after imbibition, when smoke-treated dormant seeds commit to germination. Extractable GA1+3 pools decreased in all seeds, but the decrease was more dramatic within 2 h of smoke exposure, which was followed by an increase between hours 2 and 4. Extractable ABA pools increased shortly after imbibition and remained stable in control, water-treated seeds, but decreased sharply in smoke-treated seeds. PAC completely inhibited smoke-induced germination when seeds were treated for 12 h after smoke exposure, consistent with the requirement of de novo GA synthesis for germination. Smoke treatment in the dark did not result in germination, whereas GA3 treatment did, a result consistent with phytochrome-mediated GA biosynthesis. Smoke exposure dramatically increased the sensitivity of seeds to exogenous GA3 treatments in both the light and dark, and light exposure increased this sensitivity an additional tenfold. Taken together, these results suggest that while germination requires endogenous GA synthesis, the effects of smoke treatment increase GA sensitivity, which is correlated with a decrease in endogenous ABA pools.

Keywords

abscisic aciddormancygibberellic acidgerminationNicotiana attenuatapaclobutrazolsmoke
Type
Research Article
Information
Seed Science Research , Volume 14 , Issue 1 , March 2004 , pp. 51 - 60
Copyright
Copyright © Cambridge University Press 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baldwin, I.T., Staszakkozinski, L. and Davidson, R. (1994) Up in smoke. 1. Smoke-derived germination cues for the post-fire annual, Nicotiana attenuata Torr Ex Watson. Journal of Chemical Ecology 20, 2345–2371.CrossRefGoogle Scholar
Bewley, J. D. (1997) Seed germination and dormancy. Plant Cell 9, 1055–1066.CrossRefGoogle ScholarPubMed
Brown, N.A.C. and van Staden, J. (1997) Smoke as a germination cue: A review. Plant Growth Regulation 22, 115–124.CrossRefGoogle Scholar
Casal, J.J. and Sánchez, R.A. (1998) Phytochromes and seed germination. Seed Science Research 8, 317–329.CrossRefGoogle Scholar
Chen, F. and Bradford, K.J. (2000) Expression of an expansin is associated with endosperm weakening during tomato seed germination. Plant Physiology 124, 1265–1274.CrossRefGoogle ScholarPubMed
Dahal, P., Nevins, D.J. and Bradford, K.J. (1997) Relationship of endo-β-D-mannanase activity and cell wall hydrolysis in tomato endosperm to germination rates. Plant Physiology 113, 1243–1252.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Derkx, M.P.M., Vermeer, E. and Karssen, C.M. (1994) Gibberellins in seeds of Arabidopsis thaliana. Biological activities, identification and effects of light and chilling on endogenous levels. Plant Growth Regulation 15, 223–234.CrossRefGoogle Scholar
Doherty, L.C. and Cohn, M.A. (2000) Seed dormancy in red rice (Oryza sativa). XI. Commercial liquid smoke elicits germination. Seed Science Research 10, 415–421.CrossRefGoogle Scholar
Egerton-Warburton, L.M. (1998) A smoke-induced alteration of the sub-testa cuticle in seeds of the post-fire recruiter, Emmenanthe penduliflora Benth. (Hydrophyllaceae). Journal of Experimental Botany 49, 1317–1327.CrossRefGoogle 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
García-Martínez, J.L. and Gil, J. (2001) Light regulation of gibberellin biosynthesis and mode of action. Journal of Plant Growth Regulation 20, 354–368.CrossRefGoogle ScholarPubMed
Gardner, M.J., Dalling, K.J., Light, M.E., Jäger, A.K. and van Staden, J. (2001) Does smoke substitute for red light in the germination of light-sensitive lettuce seeds by affecting gibberellin metabolism? South African Journal of Botany 67, 636–640.CrossRefGoogle Scholar
Grappin, P., Bouinot, D., Sotta, B., Miginiac, E. and Jullien, M. (2000) Control of seed dormancy in Nicotiana plumbaginifolia: post-imbibition abscisic acid synthesis imposes dormancy maintenance. Planta 210, 279–285.CrossRefGoogle ScholarPubMed
Hashimoto, T. and Yamaki, T. (1959) On the physiological effects of gibberellins A1, A2, A3, and A4. Botanical Magazine 72, 178–181.CrossRefGoogle Scholar
Hays, D.B., Yeung, E.C. and Pharis, R.P. (2002) The role of gibberellins in embryo axis development. Journal of Experimental Botany 53, 1747–1751.CrossRefGoogle ScholarPubMed
Hedden, P. and Phillips, A.L. (2000) Gibberellin metabolism: new insights revealed by the genes. Trends in Plant Science 5, 523–530.CrossRefGoogle ScholarPubMed
Hilhorst, H.W.M. (1995) A critical update on seed dormancy. I. Primary dormancy. Seed Science Research 5, 61–73.CrossRefGoogle Scholar
Hilhorst, H.W.M. and Karssen, C.M. (1992) Seed dormancy and germination – the role of abscisic-acid and gibberellins and the importance of hormone mutants. Plant Growth Regulation 11, 225–238.CrossRefGoogle Scholar
Kamiya, Y. and García-Martínez, J.L. (1999) Regulation of gibberellin biosynthesis by light. Current Opinion in Plant Biology 2, 398–403.CrossRefGoogle ScholarPubMed
Karssen, C.M., Laçka, E. (1986) 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.CrossRefGoogle Scholar
Karssen, C.M., Zagorski, S., Kepczynski, J. and Groot, S.P.C. (1989) Key role for endogenous gibberellins in the control of seed germination. Annals of Botany 63, 71–80.CrossRefGoogle Scholar
Koornneef, M., Bentsink, L. and Hilhorst, H. (2002) Seed dormancy and germination. Current Opinion in Plant Biology 5, 33–36.CrossRefGoogle ScholarPubMed
Krock, B., Schmidt, S., Hertweck, C. and Baldwin, I.T. (2002) Vegetation-derived abscisic acid and four terpenes enforce dormancy in seeds of the post-fire annual Nicotiana attenuata. Seed Science Research 12, 239–252.CrossRefGoogle Scholar
Lee, S., Cheng, H., King, K.E., Wang, W., He, Y., Hussain, A., Lo, J., Harberd, N.P. and Peng, J. (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes and Development 16, 646–658.CrossRefGoogle ScholarPubMed
Le Page-Degivry, M.T., Garello, G. and Barthe, P. (1997) Changes in abscisic acid biosynthesis and catabolism during dormancy breaking in Fagus sylvatica embryo. Journal of Plant Growth Regulation 16, 57–61.CrossRefGoogle Scholar
Leubner-Metzger, G. (2002) Seed after-ripening and over-expression of class I β-1,3-glucanase confer maternal effects on tobacco testa rupture and dormancy release. Planta 215, 959–968.CrossRefGoogle Scholar
Leubner-Metzger, G. and Meins, F. (2000) Sense transformation reveals a novel role for class I beta-1,3-glucanase in tobacco seed germination. Plant Journal 23, 215–221.CrossRefGoogle 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 induction in tobacco seed germination. Planta 199, 282–288.CrossRefGoogle Scholar
Li, B.L. and Foley, M.E. (1997) Genetic and molecular control of seed dormancy. Trends in Plant Science 2, 384–389.CrossRefGoogle Scholar
Min, X.J. and Bartholomew, D.P. (1996) Effect of plant growth regulators on ethylene production, 1-aminocyclopropane-1-carboxylic acid oxidase activity, and initiation of inflorescence development of pineapple. Journal of Plant Growth Regulation 15, 121–128.CrossRefGoogle Scholar
Minorsky, P.V. (2002) Smoke-induced germination. Plant Physiology 128, 1167–1168.CrossRefGoogle Scholar
Nonogaki, H., Gee, O.H. and Bradford, K.J. (2000) A germination-specific endo-β-mannanase gene is expressed in the micropylar endosperm cap of tomato seeds. Plant Physiology 123, 1235–1245.CrossRefGoogle ScholarPubMed
Olszewski, N., Sun, T. and Gubler, F. (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14, S61–S80CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Rademacher, W. (2000) Growth retardants: Effects on gibberellin biosynthesis and other metabolic pathways. Annual Review of Plant Physiology and Plant Molecular Biology 51, 501–531.CrossRefGoogle ScholarPubMed
Sanchez, R.A., de Miguel, L., Lima, C. and de Lederkremer, R.M. (2002) Effect of low water potential on phytochrome-induced germination, endosperm softening and cell-wall mannan degradation in Datura ferox seeds. Seed Science Research 12, 155–163.CrossRefGoogle Scholar
Schmitz, N., Abrams, S.R. and Kermode, A.R. (2000) Changes in abscisic acid content and embryo sensitivity to (+)-abscisic acid during the termination of dormancy of yellow cedar seeds. Journal of Experimental Botany 51, 1159–1162.CrossRefGoogle ScholarPubMed
Swain, S.M., Reid, J.B. and Kamiya, Y. (1997) Gibberellins are required for embryo growth and seed development in pea. Plant Journal 12, 1329–1338.CrossRefGoogle Scholar
Thomas, T.H. and van Staden, J. (1995) Dormancy break of celery (Apium graveolens L.) seeds by plant derived smoke extract. Plant Growth Regulation 17, 195–198.CrossRefGoogle Scholar
Toorop, P.E., van Aelst, A.C. and Hilhorst, H.W.M. (2000) The second step of the biphasic endosperm cap weakening that mediates tomato (Lycopersicon esculentum) seed germination is under control of ABA. Journal of Experimental Botany 51, 1371–1379.Google ScholarPubMed
Toyomasu, T., Kawaide, H., Mitsuhashi, W., Inoue, Y. and Kamiya, Y. (1998) Phytochrome regulates gibberellin biosynthesis during germination of photoblastic lettuce seeds. Plant Physiology 118, 1517–1523.CrossRefGoogle ScholarPubMed
van Staden, J., Jager, A.K. and Strydom, A. (1995) Interaction between a plant-derived smoke extract, light and phytohormones on the germination of light-sensitive lettuce seeds. Plant Growth Regulation 17, 213–218.CrossRefGoogle Scholar
Vidal, A.M., Gisbert, C., Talon, M., Primo-Millo, E., Lopez-Diaz, I. and Garcia-Martinez, J.L. (2001) The ectopic overexpression of a citrus gibberellin 20-oxidase enhances the non-13-hydroxylation pathway of gibberellin biosynthesis and induces an extremely elongated phenotype in tobacco. Physiologia Plantarum 112, 251–260.CrossRefGoogle ScholarPubMed
Welbaum, G.E., Bradford, K.J., Yim, K.O., Booth, D.T. and Oluoch, M.O. (1998) Biophysical, physiological and biochemical processes regulating seed germination. Seed Science Research 8, 161–172.CrossRefGoogle Scholar
Wu, C.T., Leubner-Metzger, G., Meins, F. and Bradford, K.J. (2001) Class I β-1,3-glucanase and chitinase are expressed in the micropylar endosperm of tomato seeds prior to radicle emergence. Plant Physiology 126, 1299–1313.CrossRefGoogle Scholar
Yamaguchi, S. and Kamiya, Y. (2002) Gibberellins and light-stimulated seed germination. Journal of Plant Growth Regulation 20, 369–376.CrossRefGoogle Scholar
Yamaguchi, S., Smith, M.W., Brown, R.G.S., Kamiya, Y. and Sun, T.P. (1998) Phytochrome regulation and differential expression of gibberellin 3 β-hydroxylase genes in germinating Arabidopsis seeds. Plant Cell 10, 2115–2126.Google Scholar