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Secondary dormancy dynamics depends on primary dormancy status in Arabidopsis thaliana

Published online by Cambridge University Press:  12 January 2015

Gabriela A. Auge ,
Logan K. Blair ,
Liana T. Burghardt ,
Jennifer Coughlan ,
Brianne Edwards ,
Lindsay D. Leverett  and
Kathleen Donohue
Gabriela A. Auge*
Affiliation:
Duke University, Department of Biology, Box 90338, Durham, NC27708, USA
Logan K. Blair
Affiliation:
Duke University, Department of Biology, Box 90338, Durham, NC27708, USA
Liana T. Burghardt
Affiliation:
Duke University, Department of Biology, Box 90338, Durham, NC27708, USA
Jennifer Coughlan
Affiliation:
Duke University, Department of Biology, Box 90338, Durham, NC27708, USA
Brianne Edwards
Affiliation:
Duke University, Department of Biology, Box 90338, Durham, NC27708, USA
Lindsay D. Leverett
Affiliation:
Duke University, Department of Biology, Box 90338, Durham, NC27708, USA Duke University, University Program in Ecology, Box 90328, Durham, NC27708, USA
Kathleen Donohue
Affiliation:
Duke University, Department of Biology, Box 90338, Durham, NC27708, USA
*
*Correspondence: E-mail: gabriela.auge@duke.edu
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Abstract

Seed dormancy can prevent germination under unfavourable conditions that reduce the chances of seedling survival. Freshly harvested seeds often have strong primary dormancy that depends on the temperature experienced by the maternal plant and which is gradually released through afterripening. However, seeds can be induced into secondary dormancy if they experience conditions or cues of future unfavourable conditions. Whether this secondary dormancy induction is influenced by seed-maturation conditions and primary dormancy has not been explored in depth. In this study, we examined secondary dormancy induction in seeds of Arabidopsis thaliana matured under different temperatures and with different levels of afterripening. We found that low water potential and a range of temperatures, from 8°C to 35°C, induced secondary dormancy. Secondary dormancy induction was affected by the state of primary dormancy of the seeds. Specifically, afterripening had a non-monotonic effect on the ability to be induced into secondary dormancy by stratification; first increasing in sensitivity as afterripening proceeded, then declining in sensitivity after 5 months of afterripening, finally increasing again by 18 months of afterripening. Seed-maturation temperature sometimes had effects that were independent of expressed primary dormancy, such that seeds that had matured at low temperature, but which had comparable germination proportions as seeds matured at warmer temperatures, were more easily induced into secondary dormancy. Because seed-maturation temperature is a cue of when seeds were matured and dispersed, these results suggest that the interaction of seed-maturation temperature, afterripening and post-dispersal conditions all combine to regulate the time of year of seed germination.

Keywords

dormancy cyclinggerminationmaternal effectsphenologystratificationwater potential
Type
Research Papers
Information
Seed Science Research , Volume 25 , Special Issue 2: Seed Dormancy , June 2015 , pp. 230 - 246
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Copyright
Copyright © Cambridge University Press 2015 

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References

Argyris, J., Dahal, P., Hayashi, E., Still, D. and Bradford, K. (2008) Genetic variation for lettuce seed thermoinhibition is associated with temperature-sensitive expression of abscisic acid, gibberellin, and ethylene biosynthesis, metabolism, and response genes. Plant Physiology 148, 926–947.Google Scholar
Baskin, C. and Baskin, J. (1998) Seeds: Ecology, biogeography and evolution of dormancy and germination. San Diego, Academic Press.Google Scholar
Baskin, J. and Baskin, C. (1972) Ecological life cycle and physiological ecology of seed germination of Arabidopsis thaliana . Canadian Journal of Botany 50, 353–360.Google Scholar
Baskin, J. and Baskin, C. (1983) Seasonal changes in the germination responses of buried seeds of Arabidopsis thaliana and ecological interpretation. Botanical Gazette 144, 540–543.Google Scholar
Batlla, D. and Benech-Arnold, R. (2006) The role of fluctuations in soil water content on the regulation of dormancy changes in buried seeds of Polygonum aviculare L. Seed Science Research 16, 47–59.CrossRefGoogle Scholar
Batlla, D., Nicoletta, M. and Benech-Arnold, R. (2007) Sensitivity of Polygonum aviculare seeds to light as affected by soil moisture conditions. Annals of Botany 5, 915–924.CrossRefGoogle Scholar
Bentsink, L. and Koornneef, M. (2008) Seed dormancy and germination. The Arabidopsis Book. The American Society of Plant Biology. Available at http://dx.doi.org/10.1199/tab.0119 (accessed accessed 11 December 2014).Google Scholar
Bewley, J. (1997) Seed germination and dormancy. The Plant Cell 9, 1055–1066.Google Scholar
Bewley, J. and Black, M. (1994) Seeds; physiology of development and germination. New York, Plenum Press.Google Scholar
Cadman, C., Toorop, P., Hilhorst, H. and Finch-Savage, W. (2006) Gene expression profiles of Arabidopsis Cvi seeds during cycling through dormant and non-dormant states indicate a common underlying dormancy control mechanism. The Plant Journal 46, 805–822.Google Scholar
Carrera, E., Holman, T., Medhurst, A., Dietrich, D., Footitt, S., Theodoulou, F. and Holdsworth, M. (2008) Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis . The Plant Journal 53, 214–224.CrossRefGoogle ScholarPubMed
Chiang, G., Bartsch, M., Barua, D., Nakabayashi, K., Debieu, M., Kronholm, I., Koornneef, M., Soppe, W., Donohue, K. and de Meaux, J. (2011) DOG1 expression predicts maternal effects and geographic variation in germination in Arabidopsis thaliana . Molecular Ecology 20, 3336–3349.Google Scholar
Debieu, M., Tang, C., Stich, B., Sikosek, T., Effgen, S., Josephs, E., Schmitt, J., Nordborg, M., Koornneef, M. and de Meaux, J. (2013) Co-variation between seed dormancy, growth rate and flowering time changes with latitude in Arabidopsis thaliana . PLoS ONE 8, e61075.Google Scholar
Donohue, K. (2009) Completing the cycle: maternal effects as the missing link in plant life cycles. Philosophical Transactions of the Royal Society of London B, Biological Sciences 364, 1059–1074.Google Scholar
Donohue, K. and Schmitt, J. (1998) Maternal environmental effects: Adaptive plasticity? pp. 137–158 in Mousseau, T.A.; Fox, C.W. (Eds) Maternal effects as adaptations. Oxford, Oxford University Press.Google Scholar
Donohue, K., Dorn, L., Griffith, C., Kim, E.-S., Aguilera, J. and Schmitt, J. (2005a) Niche construction through germination cueing: life history responses to timing of germination in Arabidopsis thaliana . Evolution 59, 771–785.Google ScholarPubMed
Donohue, K., Dorn, L., Griffith, C., Schmitt, J., Kim, E.-S. and Aguilera, A. (2005b) The evolutionary ecology of seed germination of Arabidopsis thaliana: variable natural selection on germination timing. Evolution 59, 758–770.Google Scholar
Donohue, K., Heschel, M., Chiang, G., Butler, C. and Barua, D. (2007) Phytochrome mediates germination responses to multiple seasonal cues. Plant, Cell and Environment 30, 202–212.Google Scholar
Donohue, K., Rubio de Casas, R., Burghardt, L., Kovach, K. and Willis, C. (2010) Germination, post-germination adaptation, and species ecological ranges. Annual Review of Evolution, Ecology and Systematics 41, 293–319.Google Scholar
Finch-Savage, W. and Leubner-Metzger, G. (2006) Seed dormancy and the control of germination. New Phytologist 171, 501–523.Google Scholar
Finch-Savage, W., Cadman, C., Toorop, P., Lynn, J. and Hilhorst, H. (2007) Seed dormancy release in Arabidopsis Cvi by dry afterripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directed by environmentally specific sensing. The Plant Journal 51, 60–78.Google Scholar
Footitt, S., Douterelo-Soler, I., Clay, H. and Finch-Savage, W. (2011) Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways. Proceedings of the National Academy of Sciences, USA 108, 20236–20241.Google Scholar
Footitt, S., Huang, Z., Clay, H., Mead, A. and Finch-Savage, W. (2013) Temperature, light and nitrate sensing coordinate Arabidopsis seed dormancy cycling, resulting in winter and summer annual phenotypes. The Plant Journal 74, 1003–1015.Google Scholar
Fox, J. and Weisberg, H.S. (2011) An R companion to applied regression. Los Angeles, Sage Publications.Google Scholar
Griffith, C., Kim, E.-S. and Donohue, K. (2004) Life-history variation and adaptation in the historically mobile plant, Arabidopsis thaliana (Brassicaceae), in North America. American Journal of Botany 91, 837–849.Google Scholar
Gutterman, Y. (1992) Maternal effects on seeds during development. pp. 27–60 in Fenner, M. (Ed.) Seeds: The ecology of regeneration in plant communities. Wallingford, UK, CAB International.Google Scholar
Hoffman, M. (2002) Biogeography of Arabidopsis thaliana (L.) Heynh. (Brassicaceae). Journal of Biogeography 21, 125–134.Google Scholar
Holdsworth, M., Bentsink, L. and Soppe, W. (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy, and germination. New Phytologist 179, 33–54.Google Scholar
Huang, X., Schmitt, J., Dorn, L., Griffith, C., Effgen, S., Takao, S., Koorneef, M. and Donohue, K. (2010) The earliest stages of adaptation in an experimental plant population: strong selection to QTLS for seed dormancy. Molecular Ecology 19, 1335–1351.Google Scholar
Huo, H., Dahal, P., Kunusoth, K., McCallum, C. and Bradford, K. (2013) Expression of 9-cis-EPOXYCAROTENOID DIOXYGENASE 4 is essential for thermoinhibition of lettuce seed germination but not for seed development or stress tolerance. The Plant Cell 25, 884–900.Google Scholar
Iglesias-Fernandez, R., Rodrıguez-Gacio, M. and Matilla, A. (2011) Progress in research on dry afterripening. Seed Science Research 21, 69–80.Google Scholar
Kendall, S. and Penfield, S. (2012) Maternal and zygotic temperature signalling in the control of seed dormancy and germination. Seed Science Research 22, S23–S29.Google Scholar
Kronholm, I., Xavier Pico, F., Alonso-Blanco, C., Goudet, J. and de Meaux, J. (2012) Genetic basis of adaptation in Arabidopsis thaliana: Local adaptation at the seed dormancy QTL DOG1. Evolution 66, 2287–2302.Google Scholar
Leubner-Metzger, G. (2005) Beta-1,3-glucanase gene expression in low-hydrated seeds as a mechanism for dormancy release during tobacco after-ripening. The Plant Journal 41, 133–145.Google Scholar
Meimoun, P., Mordret, E., Langlade, N., Balzergue, S., Arribat, S., Bailly, C. and El-Maarouf-Bouteau, H. (2014) Is gene transcription involved in seed dry after-ripening? PLoS ONE 9, e86442.Google Scholar
Montesinos-Navarro, A., Xavier Picó, F. and Tonsor, S. (2012) Clinal variation in seed traits influencing life cycle timing in Arabidopsis thaliana . Evolution 66, 3417–3431.CrossRefGoogle ScholarPubMed
Murphey, M., Kovach, K., Elnaccash, T., He, H., Bentskink, L. and Donohue, K. (2014) DOG1-imposed dormancy mediates germination responses to temperature cues. Environmental and Experimental Botany 112, 33–43.Google Scholar
Penfield, S. and Springthorpe, V. (2012) Understanding chilling responses in Arabidopsis seeds and their contribution to life history. Philosophical Transactions of the Royal Society B, Biological Sciences 367, 291–297.Google Scholar
Ratcliffe, D. (1965) Germination characteristics and their inter- and intra-population variability in Arabidopsis . Arabidopsis Information Service 13, .Google Scholar
R Core Team (2009) R: a language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing.Google Scholar
Rubio de Casas, R., Kovach, K., Dittmar, E., Barua, D., Barco, B. and Donohue, K. (2012) Seed after-ripening and dormancy determine adult life history independently of germination timing. New Phytologist 194, 868–879.Google Scholar
Sharbel, T., Haubold, B. and Mitchell-Olds, T. (2000) Genetic isolation by distance in Arabidopsis thaliana: biogeography and postglacial colonization of Europe. Molecular Ecology 9, 2109–2118.Google Scholar
Taylor, N., Hills, P., Gold, J., Stirk, W. and van Staden, J. (2005) Factors contributing to the regulation of thermoinhibition in Tagetes minuta L. Journal of Plant Physiology 162, 1270–1279.Google Scholar
Thompson, L. (1994) The spatiotemporal effects of nitrogen and litter on the population dynamics of Arabidopsis thaliana . Journal of Ecology 82, 63–68.Google Scholar
Toh, S., Kamiya, Y., Kawakami, N., Nambara, E., McCourt, P. and Tsuchiya, Y. (2012) Thermoinhibition uncovers a role for strigolactones in Arabidopsis seed germination. Plant and Cell Physiology 53, 107–117.Google Scholar
Tozer, M. and Ooi, M. (2014) Humidity-regulated dormancy onset in the Fabaceae: a conceptual model and its ecological implications for the Australian wattle Acacia saligna . Annals of Botany 114, 579–590.Google Scholar
Watt, M., Bloomberg, M. and Finch-Savage, W. (2011) Development of a hydrothermal time model that accurately characterises how thermoinhibition regulates seed germination. Plant, Cell and Environment 34, 870–876.Google Scholar
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