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  Eur.J.Hortic.Sci. 81 (1) 13-21 | DOI: 10.17660/eJHS.2016/81.1.2
ISSN 1611-4426 print and 1611-4434 online | © ISHS 2016 | European Journal of Horticultural Science | Original article

Early frost reactions of different populations of Quercus robur L. and Tilia cordata Mill. in Germany

M. Selig and H. Bohne
Institute for Horticultural Production Systems, Section Woody Plant and Propagation Physiology, Leibniz Universität Hannover, Hannover, Germany

Local adapted tree populations underlie the risk of losing their adaptive traits by hybridization with trees of non-local populations. To prevent this hybridization the German government amended the Federal Nature Conservation Act (BNatschG) in 2010 and six defined areas of origin were arranged (BMU, 2012) for the use of plants in free nature. The transfer of propagation material between them is forbidden from March 1st, 2020. However, the grade of local adaptation in populations of woody species in Germany is not clearly demonstrated. The aim of this study was to investigate differences in early frost reactions among German populations of Quercus robur and Tilia cordata by artificial freezing of shoots at -15°C and -25°C in November 2011. The process of bud set was rated prior and frost damage, sugar, starch and proline concentration were measured after the freezing experiments. To estimate long term survival whole plants were frozen simultaneously and then cultivated to investigate their regeneration. We did not find differences in bud set and early frost hardiness of shoots between German populations of the target species. Differences in these traits only occurred for the included Hungarian population of Quercus robur with lower grade of bud set and higher frost damage while having the highest proline concentration. Physiological differences occurred among German populations of Tilia cordata with higher soluble sugar concentration of the most southern population (47.51°N). However, these physiological differences did not improve frost hardiness indicating phenology as the main factor for early frost hardiness in the current experiment. The ecological differences at the sites of origin of the used populations do not seem to be big enough to generate different early frost reactions in our experiment, counteracting ecological factors affecting the same biological parameter substitute each other or high phenotypic plasticity covers local adaptation.

Keywords adaptation, bud set, carbohydrates, index of injury, proline, provenances

Significance of this study

What is already known on this subject?

  • The adaptation of woody plant populations to local ecological conditions can lead to different abiotic stress reactions, e.g., early frost. These adaptive traits can be lost by hybridization with non-local populations. However, the magnitude of local adaptation in German populations of Quercus robur and Tilia cordata is not fully clear. Nevertheless from March 1st, 2020 the Federal Nature Conservation Act forbids the planting of populations outside their newly arranged defined areas of origin in free nature.
What are the new findings?
  • After transfer to the experimental site in Hannover and growth for seven months, we did not find differences in bud set between German populations of the target species. Also after artificial freezing at -15°C and -25°C in November 2011 no interpopulation differences in frost damage occurred. Differences in sugar, starch and proline concentration were marginal.
What is the expected impact on horticulture?
  • Based on the results for possible risks due to early frost, the partitioning of six defined areas of origin for the use of woody plants in free nature of Germany has to be reconsidered. An exchange of plant material between adjacent defined areas of origin should be possible in case of a lack of suitable plant material. This would alleviate the expenditure for the acquisition of seed for tree nurseries and improve the supply of planting stock.

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  • Abod, S., and Webster, A. (1991). Carbohydrates and their effects on growth and establishment of Tilia and Betula: I. Seasonal changes in soluble and insoluble carbohydrates. J. of Hortic. Sci. 66(2), 235–246.

  • Aitken, S.N., Yeaman, S., Holliday, J.A., Wang, T., and Curtis-McLane, S. (2008). Adaptation, migration or extirpation: climate change outcomes for tree populations. Evolutionary Applications 1(1), 95–111.

  • Ashraf, M., and Foolad, M.R. (2007). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany 59(2), 206–216.

  • Aslamarz, A.A., Vahdati, K., Hassani, D., Rahemi, M., Mohammadi, N., and Leslie, C. (2011). Cold Hardiness and its Relationship with Proline Content in Persian Walnut. Eur. J. of Hortic. Sci. 76(3), 84–90.

  • Bano, A., Rehman, A., and Winiger, M. (2009). Altitudinal variation in the content of protein, proline, sugar and abscisic acid (ABA) in the alpine herbs from Hunza valley, Pakistan. Pak. J. Bot. 41(4), 1593–1602.

  • Bates, L., Waldren, R., and Teare, I. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil 39(1), 205–207.

  • Biere, A., and Verhoeven, K. (2008). Local adaptation and the consequences of being dislocated from coevolved enemies. New Phytologist 180(2), 265–268.

  • BMU (Bundesministerium für Umwelt, Naturschutz und Reaktorsicherheit). (2012). Leitfaden zur Verwendung gebietseigener Gehölze. BMU Refer. 13, 1–32.

  • BNatschG. 2009. [Bundesnaturschutzgesetz vom 29. Juli 2009 (BGBl. I S. 2542), das durch Artikel 421 der Verordnung vom 31. August 2015 (BGBl. I S. 1474) geändert worden ist].

  • Boehringer S.A. (1984). Methods of enzymatic food analysis using single reagents. Boehringer Mannheim GmbH, Mannheim.

  • Campbell, R.K., and Sorensen, F.C. (1973). Cold-Acclimation in Seedling Douglas-Fir Related to Phenology and Provenance. Ecology 54(5), 1148–1151.

  • Christersson, L. (1978). The Influence of Photoperiod and Temperature on the Development of Frost Hardiness in Seedlings of Pinus silvestris and Picea abies. Physiologia Plantarum 44(3), 288–294.

  • Dauwe, R., Holliday, J., Aitken, S.N., and Mansfield, S.D. (2012). Metabolic dynamics during autumn cold acclimation within and among populations of Sitka spruce (Picea sitchensis). The New Phytologist 194(1), 192–205.

  • Deans, J., and Harvey, F. (1995). Phenologies of sixteen European provenances of sessile oak growing in Scotland. Forestry 68(3), 265–274.

  • Flint, H.L., Boyce, B.R., and Beattie, D.J. (1967). Index of injury – A useful expression of freezing injury to plant tissues as determined by the electrolytic method. Canadian Journal of Plant Science 47(2), 229–230.

  • FoVG. 2002. [Forstvermehrungsgutgesetz vom 22. Mai 2002 (BGBl. I S. 1658), das durch Artikel 414 der Verordnung vom 31. August 2015 (BGBl. I S. 1474) geändert worden ist].

  • Hamrick, J.L., Godt, M.J.W., and Sherman-Broyles, S.L. (1992). Factors influencing levels of genetic diversity in woody plant species. New Forests 6(1–4), 95–124.

  • Hamrick, J. (2004). Response of forest trees to global environmental changes. Forest Ecology and Management 197(1-3), 323–335.

  • Heide, O.M. (1974). Growth and Dormancy in Norway Spruce Ecotypes (Picea abies) I. Interaction of Photoperiod and Temperature. Physiologia Plantarum 30(1), 1–12.

  • Hothorn, T., Bretz, F., and Westfall, P.H. (2008). Simultaneous inference in general parametric models. Biometrical Journal 50(3), 346–363.

  • Howe, G.T., Aitken, S.N., Neale, D.B., Jermstad, K.D., Wheeler, N.C., and Chen, T.H.H. (2003). From genotype to phenotype : unraveling the complexities of cold adaptation in forest trees. Canadian Journal of Botany 81(12), 1247–1266.

  • Hufford, K.M., and Mazer, S.J. (2003). Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends in Ecology and Evolution 18(3), 147–155.

  • Hurme, P., Repo, T., Savolainen, O., and Pääkkönen, T. (1997). Climatic adaptation of bud set and frost hardiness in Scots pine (Pinus sylvestris). Canadian J. of Forest Res. 27(5), 716–723.

  • Ingvarsson, P.K., García, M.V., Hall, D., Luquez, V., and Jansson, S. (2006). Clinal variation in phyB2, a candidate gene for day-length-induced growth cessation and bud set, across a latitudinal gradient in European aspen (Populus tremula). Genetics 172(3), 1845–1853.

  • Jensen, J.S., and Deans, J.D. (2004). Late Autumn Frost Resistance of Twelve North European Provenances of Quercus Species. Scandinavian Journal of Forest Research 19(5), 390–399.

  • Junttila, O. (1980). Effect of photoperiod and temperature on apical growth cessation in two ecotypes of Salix and Betula. Physiologia Plantarum 48(3), 347–352.

  • Kawecki, T.J. (2008). Adaptation to Marginal Habitats. Annual Review of Ecology, Evolution, and Systematics 39(1), 321–342.

  • Kempa, S., Krasensky, J., Dal Santo, S., Kopka, J., and Jonak, C. (2008). A central role of abscisic acid in stress-regulated carbohydrate metabolism. PloS One 3(12), e3935.

  • Kim, Y.T., and Glerum, C. (1995). Seasonal free amino acid fluctuations in red pine and white spruce needles. Canadian Journal of Forest Research 25(5), 697–703.

  • Kleinschmit, J. (1993). Intraspecific variation of growth and adaptive traits in European oak species. Annals of Forest Science 50, 166–185.

  • Kosová, K., Vítámvás, P., and Prášil, I.T. (2007). The role of dehydrins in plant response to cold. Biologia Plantarum 51(4), 601–617.

  • Kozlowski, T.T., and Pallardy, S.G. (2002). Acclimation and Adaptive Responses of Woody Plants to Environmental Stresses. The Botanical Review 68 (2), 270–334.[0270:AAAROW]2.0.CO;2.

  • Kreyling, J., Thiel, D., Nagy, L., Jentsch, A., Huber, G., Konnert, M., and Beierkuhnlein, C. (2011). Late frost sensitivity of juvenileFagus sylvatica L. differs between southern Germany and Bulgaria and depends on preceding air temperature. European Journal of Forest Research 131(3), 717–725.

  • Kreyling, J., Buhk, C., Backhaus, S., Hallinger, M., Huber, G., Huber, L., Jentsch, A., Konnert, M., Thiel, D., Wilmking, M., and Beierkuhnlein, C. (2014). Local adaptations to frost in marginal and central populations of the dominant forest tree Fagus sylvatica L. as affected by temperature and extreme drought in common garden experiments. Ecology and Evolution 4(5), 594–605.

  • Li, C., Puhakainen, T., Welling, A., Vihera-Aarnio, A., Ernstsen, A., Junttila, O., Heino, P., and Palva, E.T. (2002). Cold acclimation in silver birch (Betula pendula). Development of freezing tolerance in different tissues and climatic ecotypes. Physiologia Plantarum 116(4), 478–488.

  • Li, C., Welling, A., Puhakainen, T., Viherä-Aarnio, A., Ernstsen, A., Junttila, O., Heino, P., and Palva, E.T. (2005). Differential responses of silver birch (Betula pendula) ecotypes to short-day photoperiod and low temperature. Tree Physiology 25(12), 1563–1569.

  • McKay, H.M. (1992). Electrolyte leakage from fine roots of conifer seedlings: a rapid index of plant vitality following cold storage. Canadian Journal of Forest Research 22(9), 1371–1377.

  • Morin, X., Améglio, T., Ahas, R., Kurz-Besson, C., Lanta, V., Lebourgeois, F., Miglietta, F., and Chuine, I. (2007). Variation in cold hardiness and carbohydrate concentration from dormancy induction to bud burst among provenances of three European oak species. Tree Physiology 27(6), 817–825.

  • Murelli, C., Rizza, F., Albini, F.M., Dulio, A., Terzi, V., and Cattivelli, L. (1995). Metabolic changes associated with cold-acclimation in contrasting cultivars of barley. Physiologia Plantarum 94(1), 87–93.

  • Northwest German Forest Research Station (NW-FVA) (without year).

  • Oleksyn, J., Zytkowiak, R., Karolewski, P., Reich, P.B., and Tjoelker, M.G. (2000). Genetic and environmental control of seasonal carbohydrate dynamics in trees of diverse Pinus sylvestris populations. Tree Physiology 20(12), 837–847.

  • Palonen, P. (1999). Relationship of seasonal changes in carbohydrates and cold hardiness in canes and buds of three red raspberry cultivars. J. Am. Soc. Hortic. Sci. 124(5), 507–513.

  • R Core Team (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL

  • Rohde, A., Bastien, C., and Boerjan, W. (2011). Temperature signals contribute to the timing of photoperiodic growth cessation and bud set in poplar. Tree Physiology 31(5), 472–482.

  • Savolainen, O., Pyhäjärvi, T., and Knürr, T. (2007). Gene Flow and Local Adaptation in Trees. Ann. Rev. of Ecology, Evolution, and Systematics 38 (1), 595–619.

  • Schmidt, P.A., and Krause, A. (1997). Zur Abgrenzung von Herkunftsgebieten bei Baumschulgehölzen für die freie Landschaft. Natur & Landschaft 72, 92–95.

  • Strimbeck, G.R., Kjellsen, T.D., Schaberg, P.G., and Murakami, P.F. (2008). Dynamics of low-temperature acclimation in temperate and boreal conifer foliage in a mild winter climate. Tree Physiology 28(9), 1365–1374.

  • Vaartaja, O. (1954). Photoperiodic ecotypes of trees. Canadian Journal of Botany 32(3), 392–399.

  • Viherä-Aarnio, A., Häkkinen, R., and Junttila, O. (2006). Critical night length for bud set and its variation in two photoperiodic ecotypes of Betula pendula. Tree Physiology 26(8), 1013–1018.

  • Vitasse, Y., Porté, A.J., Kremer, A., Michalet, R., and Delzon, S. (2009a). Responses of canopy duration to temperature changes in four temperate tree species: relative contributions of spring and autumn leaf phenology. Oecologia 161(1), 187–198.

  • Vitasse, Y., Delzon, S., Bresson, C.C., Michalet, R., and Kremer, A. (2009b). Altitudinal differentiation in growth and phenology among populations of temperate-zone tree species growing in a common garden. Canadian Journal of Forest Research 39(7), 1259–1269.

  • Vitasse, Y., Bresson, C.C., Kremer, A., Michalet, R., and Delzon, S. (2010). Quantifying phenological plasticity to temperature in two temperate tree species. Functional Ecology 24(6), 1211–1218.

  • Wanner, L., and Junttila, O. (1999). Cold-induced freezing tolerance in Arabidopsis. Plant Physiology 120(2), 391–399.

  • Whiteleyl, R., Black-Samuelsson, S., and Jansson, G. (2003). Within and between population variation in adaptive traits in Ulmus laevis, the European white elm. Forest Genetics 10(4), 306–319.

  • Zhao, D., MacKown, C.T., Starks, P.J., and Kindiger, B.K. (2010). Rapid Analysis of Nonstructural Carbohydrate Components in Grass Forage Using Microplate Enzymatic Assays. Crop Science 50(4), 1537–1545.

Received: 4 June 2015 | Revised: 24 August 2015 | Accepted: 17 November 2015 | Published: 22 February 2016 | Available online: 22 February 2016

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