Hostname: page-component-7f64f4797f-m2b9p Total loading time: 0 Render date: 2025-11-04T08:02:25.216Z Has data issue: false hasContentIssue false
  • English
  • Français

Timing of seed germination correlated with temperature-based environmental conditions during seed development in conifers

Published online by Cambridge University Press:  09 December 2014

Yang Liu  and
Yousry A. El-Kassaby
Yang Liu
Affiliation:
Department of Forest and Conservation Sciences, Faculty of Forestry, The University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada
Yousry A. El-Kassaby*
Affiliation:
Department of Forest and Conservation Sciences, Faculty of Forestry, The University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada
*
*Correspondence E-mail: y.el-kassaby@ubc.ca
Get access Rights & Permissions [Opens in a new window]

Abstract

Ecological (climatic and geographic) variation in early life-history transitions is a vital determinant of the adaptive evolution of timing of seed germination. This study aimed to investigate the correlation between timing of seed germination and environmental conditions during seed development. We examined seed germination timing of 15 coniferous seed lots of lodgepole pine, ‘interior’ spruce and western hemlock collected from natural stands in British Columbia (BC), Canada, under manipulated [stratification, thermo-priming (15 or 20°C) and their combinations] and non-manipulated (control) conditions. Timing of seed germination showed strong and positive correlation with the temperature-based environmental condition during seed development. This pattern persisted across species and seed lots within species, substantiating the historic importance of environmental conditions during seed development and maturation to life-history traits. Moreover, the strategy of phenotypic plasticity affecting timing of seed germination was observed across the applied germination treatments. These results provide insight into the germination niche as affected by global warming, indicating that conifers' seed dormancy in BC (north of 54°N) tends to increase and the changes associated with early spring warm-up are expected to accelerate seedling emergence, as shortened winters would have a minimal effect on dormancy decay.

Keywords

climate changegermination manipulationgermination nicheinterior and coastal conifer speciesphenotypic plasticityseed developmental environmenttiming of seed germination

Information

Type
Research Papers
Information
Seed Science Research , Volume 25 , Issue 1 , March 2015 , pp. 29 - 45
Check for updates
Copyright
Copyright © Cambridge University Press 2014 

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.)

Article purchase

Temporarily unavailable

References

Alberto, F.J., Aitken, S.N., Alía, R., González-Martínez, S.C., Hänninen, H., Kremer, A., Lefèvre, F., Lenormand, T., Yeaman, S., Whetten, R. and Savolainen, O. (2013) Potential for evolutionary responses to climate change evidence from tree populations. Global Change Biology 19, 1645–1661.Google Scholar
Andersson, S. and Shaw, R.G. (1994) Phenotypic plasticity in Crepis tectorum (Asteraceae): genetic correlations across light regimens. Heredity 72, 113–125.Google Scholar
Baskin, C.C. and Baskin, M.J. (1998) Seeds: ecology, biogeography, and evolution of dormancy and germination. San Diego, California, Academic Press.Google Scholar
Behera, N. and Nanjundiah, V. (1995) An investigation into the role of phenotypic plasticity in evolution. Journal of Theoretical Biology 172, 225–234.CrossRefGoogle ScholarPubMed
Bell, G. (2008) Selection: the mechanism of evolution (2nd edition). New York, USA, Oxford University Press.Google Scholar
Bewley, J.D., Bradford, K.J., Hilhorst, H.W.M. and Nonogaki, H. (2012) Seeds: Physiology of development, germination, and dormancy (3rd edition). eBook, Springer. doi:10.1007/978-1-4614-4693-4 .Google Scholar
Black, M., Bewley, J.D. and Halmer, P. (2006) The encyclopedia of seeds. Wallingford, UK, CABI Publishing.Google Scholar
Bradshaw, A.D. (1965) Evolutionary significance of phenotypic plasticity in plants. Advances in Genetics Incorporating Molecular Genetic Medicine 13, 115–155.Google Scholar
Bull, J.J. (1987) Evolution of phenotypic variance. Evolution 41, 303–315.Google Scholar
Bulmer, M. (1994) Theoretical evolutionary ecology. Sunderland, Massachusetts, Sinauer Associates.Google Scholar
Caron, G.E., Wang, B.S.P. and Schooley, H.O. (1993) Variation in Picea glauca seed germination associated with the year of cone collection. Canadian Journal of Forest Research 23, 1306–1313.Google Scholar
Carta, A., Probert, R., Moretti, M., Peruzzi, L. and Bedini, G. (2014) Seed dormancy and germination in three Crocus ser. Verni species (Iridaceae): implications for evolution of dormancy within the genus. Plant Biology 16, 1065–1074.Google Scholar
Chiang, G.C.K., Bartsch, M., Barua, D., Nakabayashi, K., Debieu, M., Kronholm, I., Koornneef, M., Soppe, W.J.J., Donohue, K. and de Meaux, J. (2011) DOG1 expression is predicted by the seed-maturation environment and contributes to geographical variation in germination in Arabidopsis thaliana . Molecular Ecology 20, 3336–3349.Google Scholar
Clausen, J. and Hiesey, W.M. (1960) The balance between coherence and variation in evolution. Proceedings of the National Academy of Sciences of the United States of America 46, 494–506.Google Scholar
Cohen, D. (1966) Optimizing reproduction in a randomly varying environment. Journal of Theoretical Biology 12, 119–129.CrossRefGoogle Scholar
Dale, V.H., Joyce, L.A., McNulty, S., Neilson, R.P., Ayres, M.P., Flannigan, M.D., Hanson, P.J., Irland, L.C., Lugo, A.E., Peterson, C.J., Simberloff, D., Swanson, F.J., Stocks, B.J. and Wotton, B.M. (2001) Climate change and forest disturbances. Bioscience 51, 723–734.CrossRefGoogle Scholar
Debat, V. and David, P. (2001) Mapping phenotypes: canalization, plasticity and developmental stability. Trends in Ecology & Evolution 16, 555–561.CrossRefGoogle Scholar
de Jong, G. (2005) Evolution of phenotypic plasticity: patterns of plasticity and the emergence of ecotypes. New Phytologist 166, 101–117.CrossRefGoogle ScholarPubMed
Donohue, K., de Casas, R.R., Burghardt, L., Kovach, K. and Willis, C.G. (2010) Germination, postgermination adaptation, and species ecological ranges. Annual Review of Ecology, Evolution, and Systematics 41, 293–319.CrossRefGoogle Scholar
El-Kassaby, Y.A., Moss, I., Kolotelo, D. and Stoehr, M. (2008) Seed germination: mathematical representation and parameters extraction. Forest Science 54, 220–227.Google Scholar
Fenner, M. and Thompson, K. (2005) The ecology of seeds. Cambridge, UK, Cambridge University Press.CrossRefGoogle Scholar
Fernández-Pascual, E., Jiménez-Alfaro, B., Caujapé-Castells, J., Jaén-Molina, R. and Díaz, T.E. (2013) A local dormancy cline is related to the seed maturation environment, population genetic composition and climate. Annals of Botany 112, 937–945.Google Scholar
Fierst, J.L. (2011) A history of phenotypic plasticity accelerates adaptation to a new environment. Journal of Evolutionary Biology 24, 1992–2001.Google Scholar
Finch-Savage, W.E. and Leubner-Metzger, G. (2006) Seed dormancy and the control of germination. New Phytologist 171, 501–523.Google Scholar
Forrest, J. and Miller-Rushing, A.J. (2010) Toward a synthetic understanding of the role of phenology in ecology and evolution. Philosophical Transactions of the Royal Society B – Biological Sciences 365, 3101–3112.Google Scholar
Franks, S.J., Avise, J.C., Bradshaw, W.E., Conner, J.K., Etterson, J.R., Mazer, S.J., Shaw, R.G. and Weis, A.E. (2008) The resurrection initiative: storing ancestral genotypes to capture evolution in action. Bioscience 58, 870–873.Google Scholar
Franks, S.J., Weber, J.J. and Aitken, S.N. (2014) Evolutionary and plastic responses to climate change in terrestrial plant populations. Evolutionary Applications 7, 123–139.CrossRefGoogle ScholarPubMed
Gauch, H.G. (1992) Statistical analysis of regional yield trials: AMMI analysis of factorial designs. Amsterdam, Elsevier.Google Scholar
Granhus, A., Fløistad, I.S. and Søgaard, G. (2009) Bud burst timing in Picea abies seedlings as affected by temperature during dormancy induction and mild spells during chilling. Tree Physiology 29, 497–503.Google Scholar
Grubb, P.J. (1977) The maintenance of species-richness in plant communities: the importance of the regeneration niche. Biological Reviews 52, 107–145.CrossRefGoogle Scholar
Hänninen, H., Häkkinen, R., Hari, P. and Koski, V. (1990) Timing of growth cessation in relation to climatic adaptation of northern woody plants. Tree Physiology 6, 29–39.Google Scholar
Hermisson, J. and Wagner, G.P. (2004) The population genetic theory of hidden variation and genetic robustness. Genetics 168, 2271–2284.CrossRefGoogle ScholarPubMed
Horvath, D.P., Sung, S., Kim, D., Chao, W. and Anderson, J. (2010) Characterization, expression and function of DORMANCY ASSOCIATED MADS-BOX genes from leafy spurge. Plant Molecular Biology 73, 169–179.Google Scholar
Hoyle, G.L., Steadman, K.J., Daws, M.I. and Adkins, S.W. (2008) Pre- and post-harvest influences on seed dormancy status of an Australian Goodeniaceae species, Goodenia fascicularis . Annals of Botany 102, 93–101.Google Scholar
Huang, X.Q., Schmitt, J., Dorn, L., Griffith, C., Effgen, S., Takao, S., Koornneef, M. and Donohue, K. (2010) The earliest stages of adaptation in an experimental plant population: strong selection on QTLs for seed dormancy. Molecular Ecology 19, 1335–1351.Google Scholar
IPCC (2007) Climate change 2007: the physical science basis. pp. 1–996 in Solomon, S.; Qin, D.; Manning, M.; Chen, Z.; Marquis, M.; Averyt, K.B.; Tignor, M.; Miller, H.L. (Eds) Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK, Cambridge University Press.Google Scholar
ISTA (1999) International rules for seed testing. Seed Science and Technology 27, 50–52.Google Scholar
Jablonka, E. and Lamb, M.J. (1998) Epigenetic inheritance in evolution. Journal of Evolutionary Biology 11, 159–183.Google Scholar
Johnsen, Ø., Fossdal, C.G., Nagy, N., Molmann, J., Daehlen, O.G. and Skrøppa, T. (2005) Climatic adaptation in Picea abies progenies is affected by the temperature during zygotic embryogenesis and seed maturation. Plant Cell and Environment 28, 1090–1102.Google Scholar
Kalcsits, L., Silim, S. and Tanino, K. (2009a) The influence of temperature on dormancy induction and plant survival in woody plants. London, CABI International.Google Scholar
Kalcsits, L.A., Silim, S. and Tanino, K. (2009b) Warm temperature accelerates short photoperiod-induced growth cessation and dormancy induction in hybrid poplar (Populus× spp.). Trees – Structure and Function 23, 971–979.CrossRefGoogle Scholar
Kang, M.S. (2003) Handbook of formulas and software for plant geneticists and breeders. Binghamton, New York, Food Products Press.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
Kendall, S.L., Hellwege, A., Marriot, P., Whalley, C., Graham, I.A. and Penfield, S. (2011) Induction of dormancy in Arabidopsis summer annuals requires parallel regulation of DOG1 and hormone metabolism by low temperature and CBF transcription factors. Plant Cell 23, 2568–2580.CrossRefGoogle ScholarPubMed
Koller, D. (1962) Preconditioning of germination in lettuce at time of fruit ripening. American Journal of Botany 49, 841–844.Google Scholar
Kremer, A., Ronce, O., Robledo-Arnuncio, J.J., Guillaume, F., Bohrer, G., Nathan, R., Bridle, J.R., Gomulkiewicz, R., Klein, E.K., Ritland, K., Kuparinen, A., Gerber, S. and Schueler, S. (2012) Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecology Letters 15, 378–392.Google Scholar
Kvaalen, H. and Johnsen, Ø. (2008) Timing of bud set in Picea abies is regulated by a memory of temperature during zygotic and somatic embryogenesis. New Phytologist 177, 49–59.Google Scholar
Liu, Y., Kermode, A.R. and El-Kassaby, Y.A. (2013) The role of moist-chilling and thermo-priming on the germination characteristics of white spruce (Picea glauca) seed. Seed Science and Technology 41, 321–335.Google Scholar
Manly, B.F.J. (2005) Multivariate statistical methods: A primer (3rd edition). Boca Raton, Florida, Chapman & Hall/CRC.Google Scholar
Matesanz, S., Gianoli, E. and Valladares, F. (2010) Global change and the evolution of phenotypic plasticity in plants. The Year in Evolutionary Biology 1206, 35–55.Google Scholar
Meyers, L.A. and Bull, J.J. (2002) Fighting change with change: adaptive variation in an uncertain world. Trends in Ecology & Evolution 17, 551–557.Google Scholar
Montesinos-Navarro, A., Picó, F.X. and Tonsor, S.J. (2012) Clinal variation in seed traits influencing life cycle timing in Arabidopsis thaliana . Evolution 66, 3417–3431.Google Scholar
Morley, F. (1958) The inheritance and ecological significance of seed dormancy in subterranean clover (Trifolium subterraneum L.). Australian Journal of Biological Sciences 11, 261–274.Google Scholar
Müller, K., Bouyer, D., Schnittger, A. and Kermode, A.R. (2012) Evolutionarily conserved histone methylation dynamics during seed life-cycle transitions. PLoS ONE 7, e51532.Google Scholar
Nicotra, A.B., Atkin, O.K., Bonser, S.P., Davidson, A.M., Finnegan, E.J., Mathesius, U., Poot, P., Purugganan, M.D., Richards, C.L., Valladares, F. and van Kleunen, M. (2010) Plant phenotypic plasticity in a changing climate. Trends in Plant Science 15, 684–692.Google Scholar
Pigliucci, M. (2001) Phenotypic plasticity: Beyond nature and nurture. Maryland, Johns Hopkins University Press.Google Scholar
Pigliucci, M. and Murren, C.J. (2003) Perspective: Genetic assimilation and a possible evolutionary paradox: can macroevolution sometimes be so fast as to pass us by? Evolution 57, 1455–1464.Google Scholar
Price, T.D., Qvarnstrom, A. and Irwin, D.E. (2003) The role of phenotypic plasticity in driving genetic evolution. Proceedings of the Royal Society B–Biological Sciences 270, 1433–1440.Google Scholar
Rehfeldt, G.E., Tchebakova, N.M., Parfenova, Y.I., Wykoff, W.R., Kuzmina, N.A. and Milyutin, L.I. (2002) Intraspecific responses to climate in Pinus sylvestris . Global Change Biology 8, 912–929.Google Scholar
Reich, P.B. and Oleksyn, J. (2008) Climate warming will reduce growth and survival of Scots pine except in the far north. Ecology Letters 11, 588–597.CrossRefGoogle ScholarPubMed
Richardson, A.D., Black, T.A., Ciais, P., Delbart, N., Friedl, M.A., Gobron, N., Hollinger, D.Y., Kutsch, W.L., Longdoz, B., Luyssaert, S., Migliavacca, M., Montagnani, L., Munger, J.W., Moors, E., Piao, S.L., Rebmann, C., Reichstein, M., Saigusa, N., Tomelleri, E., Vargas, R. and Varlagin, A. (2010) Influence of spring and autumn phenological transitions on forest ecosystem productivity. Philosophical Transactions of the Royal Society B–Biological Sciences 365, 3227–3246.Google Scholar
Robeson, S.M. (2004) Trends in time-varying percentiles of daily minimum and maximum temperature over North America. Geophysical Research Letters 31, 1–4.Google Scholar
Rowe, J.S. (1964) Environmental preconditioning with special reference to forestry. Ecology 45, 399–403.Google Scholar
Schlichting, C.D. and Pigliucci, M. (1998) Phenotypic evolution: A reaction norm perspective. Sunderland, Massachusetts, Sinauer Associates.Google Scholar
Schmitt, J. and Wulff, R.D. (1993) Light spectral quality, phytochrome and plant competition. Trends in Ecology & Evolution 8, 47–51.Google Scholar
Schwartz, M.D., Ahas, R. and Aasa, A. (2006) Onset of spring starting earlier across the Northern Hemisphere. Global Change Biology 12, 343–351.Google Scholar
Skordilis, A. and Thanos, C.A. (1995) Seed stratification and germination strategy in the Mediterranean pines Pinus brutia and Pinus halepensis . Seed Science Research 5, 151–160.Google Scholar
Skrøppa, T., Kohmann, K., Johnsen, Ø., Steffenrem, A. and Edvardsen, Ø.M. (2007) Field performance and early test results of offspring from two Norway spruce seed orchards containing clones transferred to warmer climates. Canadian Journal of Forest Research–Revue Canadienne de Recherche Forestiere 37, 515–522.Google Scholar
Smith, H. (1995) Physiological and ecological function within the phytochrome family. Annual Review of Plant Physiology and Plant Molecular Biology 46, 289–315.Google Scholar
Steadman, K.J., Ellery, A.J., Chapman, R., Moore, A. and Turner, N.C. (2004) Maturation temperature and rainfall influence seed dormancy characteristics of annual ryegrass (Lolium rigidum). Australian Journal of Agricultural Research 55, 1047–1057.Google Scholar
Stearns, S.C. and Hoekstra, R.F. (2000) Evolution: an introduction. Oxford, UK, Oxford University Press.Google Scholar
Svendsen, E., Wilen, R., Stevenson, R., Liu, R.S. and Tanino, K.K. (2007) A molecular marker associated with low-temperature induction of dormancy in red osier dogwood (Cornus sericea). Tree Physiology 27, 385–397.Google Scholar
Tabachnick, B.G. and Fidell, L.S. (2012) Using multivariate statistics (6th edition). Boston, Pearson Education.Google Scholar
Tanino, K.K., Kalcsits, L., Silim, S., Kendall, E. and Gray, G.R. (2010) Temperature-driven plasticity in growth cessation and dormancy development in deciduous woody plants: a working hypothesis suggesting how molecular and cellular function is affected by temperature during dormancy induction. Plant Molecular Biology 73, 49–65.Google Scholar
Toh, S., Imamura, A., Watanabe, A., Nakabayashi, K., Okamoto, M., Jikumaru, Y., Hanada, A., Aso, Y., Ishiyama, K., Tamura, N., Iuchi, S., Kobayashi, M., Yamaguchi, S., Kamiya, Y., Nambara, E. and Kawakami, N. (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiology 146, 1368–1385.Google Scholar
Van Dijk, H. and Hautekèete, N. (2007) Long day plants and the response to global warming: rapid evolutionary change in day length sensitivity is possible in wild beet. Journal of Evolutionary Biology 20, 349–357.Google Scholar
Visser, M.E., Caro, S.P., van Oers, K., Schaper, S.V. and Helm, B. (2010) Phenology, seasonal timing and circannual rhythms: towards a unified framework. Philosophical Transactions of the Royal Society B–Biological Sciences 365, 3113–3127.Google Scholar
Vranckx, G. and Vandelook, F. (2012) A season- and gap-detection mechanism regulates seed germination of two temperate forest pioneers. Plant Biology 14, 481–490.Google Scholar
Waddington, C.H. (1942) Canalization of development and the inheritance of acquired characters. Nature 150, 563–565.Google Scholar
Waddington, C.H. (1957) The strategy of the genes: A discussion of some aspects of theoretical biology. London, Allen & Unwin.Google Scholar
Waddington, C.H. (1961) Genetic assimilation. Advances in Genetics Incorporating Molecular Genetic Medicine 10, 257–293.Google Scholar
Walck, J.L., Baskin, J.M. and Baskin, C.C. (1997) A comparative study of the seed germination biology of a narrow endemic and two geographically-widespread species of Solidago (Asteraceae). 1. Germination phenology and effect of cold stratification on germination. Seed Science Research 7, 47–58.Google Scholar
Wang, T., Hamann, A., Spittlehouse, D.L. and Aitken, S.N. (2006) Development of scale-free climate data for western Canada for use in resource management. International Journal of Climatology 26, 383–397.Google Scholar
Wang, T.L., Hamann, A., Spittlehouse, D.L. and Murdock, T.Q. (2012) ClimateWNA – high resolution spatial climate data for western North America. Journal of Applied Meteorology and Climatology 51, 16–29.Google Scholar
West-Eberhard, M.J. (2003) Developmental plasticity and evolution. New York, Oxford University Press.Google Scholar
Yan, W.K. (2001) GGEbiplot – A windows application for graphical analysis of multienvironment trial data and other types of two-way data. Agronomy Journal 93, 1111–1118.Google Scholar
Yan, W. and Kang, M.S. (2003) GGE biplot analysis: A graphical tool for breeders, geneticists, and agronomists. Boca Raton, Florida, CRC Press.Google Scholar
Yan, W. and Tinker, N.A. (2006) Biplot analysis of multi-environment trial data: principles and applications. Canadian Journal of Plant Science 86, 623–645.Google Scholar
Zhang, X.Y., Tarpley, D. and Sullivan, J.T. (2007) Diverse responses of vegetation phenology to a warming climate. Geophysical Research Letters 34, L19405.Google Scholar
Supplementary material: File

Liu and El-Kassaby Supplementary Material

Table S1 and Figure S1

Download Liu and El-Kassaby Supplementary Material(File)
File 998.5 KB