Skip to main content

Advertisement

SpringerLink
Log in

Intraspecific variations in drought response and fitness traits of beech (Fagus sylvatica L.) seedlings from three provenances differing in annual precipitation

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

European beech presents intraspecific variations in drought resistance strategies that are mediated by the amount of precipitation in the habitat.

Abstract

Climate change predictions forecast extended drought periods, which are expected to pose an enhanced risk to forest trees. Here, we investigated the drought response and fitness traits in European beech (Fagus sylvatica L.) in response to a severe progressive drought. The capability of three beech provenances from habitats differing in annual precipitation (544, 665, and 766 mm year−1) to cope with drought was compared in a common garden experiment using beech seedlings. Soil and plant water status, maximum quantum yield of PSII, growth and biomass partitioning, stomatal conductance, and transcript abundance pattern of the kinase, Open Stomata 1 (OST1), of control (well-watered) and drought-treated (water withheld) plants from each provenance were repeatedly measured during a 60-day drought experiment. The lowest precipitation provenance displayed a more isohydric phenotype with a prompt stomatal closure, increased OST1 levels, high water potential and leaf water content, and a decrement in the maximum quantum yield of PSII. The other two provenances showed a more anisohydric stomatal regulation with a slow and delayed stomatal closure and a decrease in the water status. These findings suggest that intraspecific variations in beech for diverging drought resistance strategies exist and might be mediated by differences in the abscisic acid signaling pathway. The higher precipitation provenance maintained high quantum yield of PSII, and water potentials above −2.0 MPa for a longer period of time than the other two provenances, and consequently, mortality was delayed in this provenance. We concluded that lower precipitation adapted plants employ a drought resistance strategy suitable for the moderate drought, whereas the higher precipitation habitat plants revealed mechanisms, which could be better suited to cope with more severe drought events.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ambrose AR, Baxter WL, Wong CS et al (2015) Contrasting drought-response strategies in California redwoods. Tree Physiol 35:453–469. doi:10.1093/treephys/tpv016

    Article  PubMed  Google Scholar 

  • Aranda I, Cano FJ, Gascó A et al (2015) Variation in photosynthetic performance and hydraulic architecture across European beech (Fagus sylvatica L.) populations supports the case for local adaptation to water stress. Tree Physiol 35:34–46. doi:10.1093/treephys/tpu101

    Article  CAS  PubMed  Google Scholar 

  • Baudis M, Ellerbrock RH, Felsmann K et al (2014) Intraspecific differences in responses to rainshelter-induced drought and competition of Fagus sylvatica L. across Germany. Forest Ecol Manag 330:283–293. doi:10.1016/j.foreco.2014.07.012

    Article  Google Scholar 

  • Bréda N, Huc R, Granier A, Dreyer E (2006) Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann Forest Sci 63:20. doi:10.1051/forest:2006042

    Article  Google Scholar 

  • Brodribb TJ, McAdam SAM (2013) Abscisic acid mediates a divergence in the drought response of two conifers. Plant Physiol 162:1370–1377. doi:10.1104/pp.113.217877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brodribb TJ, McAdam SAM, Jordan GJ, Martins SCV (2014) Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proc Natl Acad Sci USA 111:14489–14493. doi:10.1073/pnas.1407930111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cano FJ, Sánchez-Gómez D, Rodríguez-Calcerrada J et al (2013) Effects of drought on mesophyll conductance and photosynthetic limitations at different tree canopy layers. Plant Cell Environ 36:1961–1980. doi:10.1111/pce.12103

    PubMed  Google Scholar 

  • Carsjens C, Nguyen QN, Guzy J et al (2014) Intra-specific variations in expression of stress-related genes in beech progenies are stronger than drought-induced responses. Tree Physiol 34:1348–1361. doi:10.1093/treephys/tpu093

    Article  CAS  PubMed  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116. doi:10.1007/BF02670468

    Article  CAS  Google Scholar 

  • Ciais P, Reichstein M, Viovy N et al (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437:529–533. doi:10.1038/nature03972

    Article  CAS  PubMed  Google Scholar 

  • Cochard H, Lemoine D, Dreyer E (1999) The effects of acclimation to sunlight on the xylem vulnerability to embolism in Fagus sylvatica L. Plant Cell Environ 22:101–108. doi:10.1046/j.1365-3040.1999.00367.x

    Article  Google Scholar 

  • Ellenberg H (1988) Vegetation ecology of Central Europe. Cambridge University Press, Cambridge

    Google Scholar 

  • Ellenberg H (1996) Vegetation Mitteleuropas mit den Alpen, 5th edn. Ulmer, Stuttgart

    Google Scholar 

  • Fang J, Lechowicz MJ (2006) Climatic limits for the present distribution of beech (Fagus L.) species in the world. J Biogeogr 33:1804–1819. doi:10.1111/j.1365-2699.2006.01533.x

    Article  Google Scholar 

  • Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. Sage, Thousand Oaks. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion

  • García-Plazaola JI, Becerril JM (2000) Effects of drought on photoprotective mechanisms in European beech (Fagus sylvatica) seedlings from different provenances. Trees 14:485–490. doi:10.1007/s004680000068

    Article  Google Scholar 

  • Geßler A, Keitel C, Kreuzwieser J et al (2006) Potential risks for European beech (Fagus sylvatica) in a changing climate. Trees 21:1–11. doi:10.1007/s00468-006-0107-x

    Article  Google Scholar 

  • Granier A, Reichstein M, Bréda N et al (2007) Evidence for soil water control on carbon and water dynamics in European forests during the extremely dry year: 2003. Agric Forest Meteorol 143:123–145. doi:10.1016/j.agrformet.2006.12.004

    Article  Google Scholar 

  • Hacke U, Sauter JJ (1995) Vulnerability of xylem to embolism in relation to leaf water potential and stomatal conductance in Fagus sylvatica F. purpurea and Populus balsamifera. J Exp Bot 46:1177–1183. doi:10.1093/jxb/46.9.1177

    Article  CAS  Google Scholar 

  • Heilmann-Clausen J, Bradshaw RHW, Emborg J, Hannon G (2007) The history and present conditions of Suserup Skov: a nemoral, deciduous forest reserve in a cultural landscape. Ecol Bull 52:7–17

    Google Scholar 

  • IPCC (2014) Climate Change 2014: synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change

  • Jones HG (1993) Drought tolerance and water-use efficiency. In: Smith JAC, Griffiths H (eds) Water deficits: plant responses from cell to community. BIOS Scientific Publishers, Oxford, pp 193–203

    Google Scholar 

  • Jump AS, Hunt JM, Peñuelas J (2006) Rapid climate change-related growth decline at the southern range edge of Fagus sylvatica. Global Change Biol 12:2163–2174. doi:10.1111/j.1365-2486.2006.01250.x

    Article  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. doi:10.1111/j.1461-0248.2004.00684.x

    Article  Google Scholar 

  • Klein T (2014) The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours. Funct Ecol 28:1313–1320. doi:10.1111/1365-2435.12289

    Article  Google Scholar 

  • Knutzen F, Meier IC, Leuschner C (2015) Does reduced precipitation trigger physiological and morphological drought adaptations in European beech (Fagus sylvatica L.)? Comparing provenances across a precipitation gradient. Tree Physiol 35:949–963. doi:10.1093/treephys/tpv057

    Article  PubMed  Google Scholar 

  • Leuzinger S, Zotz G, Asshoff R, Körner C (2005) Responses of deciduous forest trees to severe drought in Central Europe. Tree Physiol 25:641–650

    Article  PubMed  Google Scholar 

  • Levitt J (1972) Responses of plants to environmental stresses. Academic Press, New York

    Google Scholar 

  • Lindner M, Maroschek M, Netherer S et al (2010) Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. Forest Ecol Manag 259:698–709. doi:10.1016/j.foreco.2009.09.023

    Article  Google Scholar 

  • Martínez-Ferri E, Balaguer L, Valladares F et al (2000) Energy dissipation in drought-avoiding and drought-tolerant tree species at midday during the Mediterranean summer. Tree Physiol 20:131–138

    Article  PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668. doi:10.1093/jexbot/51.345.659

    Article  CAS  PubMed  Google Scholar 

  • McDowell N, Pockman WT, Allen CD et al (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739. doi:10.1111/j.1469-8137.2008.02436.x

    Article  PubMed  Google Scholar 

  • Meier IC, Leuschner C (2008) Belowground drought response of European beech: fine root biomass and carbon partitioning in 14 mature stands across a precipitation gradient. Global Change Biol 14:2081–2095. doi:10.1111/j.1365-2486.2008.01634.x

    Article  Google Scholar 

  • Müller M, Seifert S, Finkeldey R (2015) A candidate gene-based association study reveals SNPs significantly associated with bud burst in European beech (Fagus sylvatica L.). Tree Genet Genomes 11:116. doi:10.1007/s11295-015-0943-1

    Article  Google Scholar 

  • Müller-Haubold H, Hertel D, Seidel D et al (2013) Climate responses of aboveground productivity and allocation in Fagus sylvatica: a transect study in mature forests. Ecosystems 16:1498–1516. doi:10.1007/s10021-013-9698-4

    Article  Google Scholar 

  • Mustilli A-C, Merlot S, Vavasseur A et al (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089–3099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olbrich M, Gerstner E, Welzl G et al (2008) Quantification of mRNAs and housekeeping gene selection for quantitative real-time RT-PCR normalization in European beech (Fagus sylvatica L.) during abiotic and biotic stress. Z Für Naturforschung C J Biosci 63:574. doi:10.1007/s11104-009-0129-4

    Article  CAS  Google Scholar 

  • Peuke AD, Schraml C, Hartung W, Rennenberg H (2002) Identification of drought-sensitive beech ecotypes by physiological parameters. New Phytol 154:373–387. doi:10.1046/j.1469-8137.2002.00400.x

    Article  CAS  Google Scholar 

  • Pfaffl MW (2004) Quantification strategies in real-time PCR. AZ Quant PCR 1:89–113

    Google Scholar 

  • Picon C, Guehl JM, Ferhi A (1996) Leaf gas exchange and carbon isotope composition responses to drought in a drought-avoiding (Pinus pinaster) and a drought-tolerant (Quercus petraea) species under present and elevated atmospheric CO2 concentrations. Plant Cell Environ 19:182–190. doi:10.1111/j.1365-3040.1996.tb00239.x

    Article  Google Scholar 

  • Pluess AR, Weber P (2012) Drought-adaptation potential in Fagus sylvatica: linking moisture availability with genetic diversity and dendrochronology. PLoS One 7:e33636. doi:10.1371/journal.pone.0033636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rennenberg H, Loreto F, Polle A et al (2006) Physiological responses of forest trees to heat and drought. Plant Biol 8:556–571. doi:10.1055/s-2006-924084

    Article  CAS  PubMed  Google Scholar 

  • Robson TM, Sánchez-Gómez D, Cano FJ, Aranda I (2012) Variation in functional leaf traits among beech provenances during a Spanish summer reflects the differences in their origin. Tree Genet Genomes 8:1111–1121. doi:10.1007/s11295-012-0496-5

    Article  Google Scholar 

  • Sánchez-Gómez D, Robson TM, Gascó A et al (2013) Differences in the leaf functional traits of six beech (Fagus sylvatica L.) populations are reflected in their response to water limitation. Environ Exp Bot 87:110–119. doi:10.1016/j.envexpbot.2012.09.011

    Article  Google Scholar 

  • Schall P, Lödige C, Beck M, Ammer C (2012) Biomass allocation to roots and shoots is more sensitive to shade and drought in European beech than in Norway spruce seedlings. Forest Ecol Manag 266:246–253. doi:10.1016/j.foreco.2011.11.017

    Article  Google Scholar 

  • Scholander P, Hammel H, Bradstreet E, Hemmingsen E (1965) Sap pressure in vascular plants. Science 148:339–346

    Article  CAS  PubMed  Google Scholar 

  • Schroeder JI, Allen GJ, Hugouvieux V et al (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658. doi:10.1146/annurev.arplant.52.1.627

    Article  CAS  PubMed  Google Scholar 

  • Schwanz P, Häberle K-H, Polle A (1996) Interactive effects of elevated CO2, ozone and drought stress on the activities of antioxidative enzymes in needles of Norway spruce trees (Picea abies, [L] Karsten) grown with luxurious N-supply. J Plant Physiol 148:351–355. doi:10.1016/S0176-1617(96)80264-1

    Article  CAS  Google Scholar 

  • Seifert S (2012) Variation of candidate genes related to climate change in European beech (Fagus sylvatica L.). Dissertation. Georg-August-University, Göttingen

    Google Scholar 

  • Sirichandra C, Davanture M, Turk BE et al (2010) The Arabidopsis ABA-activated kinase OST1 phosphorylates the bZIP transcription factor ABF3 and creates a 14-3-3 binding site involved in its turnover. PLoS One 5:e13935. doi:10.1371/journal.pone.0013935

    Article  PubMed  PubMed Central  Google Scholar 

  • Skelton RP, West AG, Dawson TE (2015) Predicting plant vulnerability to drought in biodiverse regions using functional traits. Proc Natl Acad Sci USA 112:5744–5749. doi:10.1073/pnas.1503376112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stojanović DB, Kržič A, Matović B et al (2013) Prediction of the European beech (Fagus sylvatica L.) xeric limit using a regional climate model: an example from southeast Europe. Agric Forest Meteorol 176:94–103. doi:10.1016/j.agrformet.2013.03.009

    Article  Google Scholar 

  • Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. J Exp Bot 49:419–432. doi:10.1093/jxb/49.Special_Issue.419

    Article  Google Scholar 

  • Thiel D, Kreyling J, Backhaus S et al (2014) Different reactions of central and marginal provenances of Fagus sylvatica to experimental drought. Eur J Forest Res 133:247–260. doi:10.1007/s10342-013-0750-x

    Article  Google Scholar 

  • Tognetti R, Johnson JD, Michelozzi M (1995) The response of European beech (Fagus sylvatica) seedlings from two Italian populations to drought and recovery. Trees 9:348–354. doi:10.1007/BF00202499

    Article  Google Scholar 

  • Urli M, Porté AJ, Cochard H et al (2013) Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiol 33:672–683. doi:10.1093/treephys/tpt030

    Article  CAS  PubMed  Google Scholar 

  • Valladares F, Skillman JB, Pearcy RW (2002) Convergence in light capture efficiencies among tropical forest understory plants with contrasting crown architectures: a case of morphological compensation. Am J Bot 89:1275–1284. doi:10.3732/ajb.89.8.1275

    Article  PubMed  Google Scholar 

  • Weber P, Bugmann H, Pluess AR et al (2012) Drought response and changing mean sensitivity of European beech close to the dry distribution limit. Trees 27:171–181. doi:10.1007/s00468-012-0786-4

    Article  Google Scholar 

  • Yang N, Zavišić A, Pena R, Polle A (2016) Phenology, photosynthesis, and phosphorus in European beech (Fagus sylvatica L.) in two forest soils with contrasting P contents. J Plant Nutr Soil Sci 179:151–158. doi:10.1002/jpln.201500539

    Article  CAS  Google Scholar 

  • Yue B, Xue W, Xiong L et al (2006) Genetic basis of drought resistance at reproductive stage in rice: separation of drought tolerance from drought avoidance. Genetics 172:1213–1228. doi:10.1534/genetics.105.045062

    Article  PubMed  PubMed Central  Google Scholar 

  • Zang C, Hartl-Meier C, Dittmar C et al (2014) Patterns of drought tolerance in major European temperate forest trees: climatic drivers and levels of variability. Global Chang Biol 20:3767–3779. doi:10.1111/gcb.12637

    Article  Google Scholar 

Download references

Acknowledgements

We thank Dr. Caroline Carsjens and Dr. Dennis Janz for helpful discussions, and Viktoria Pfander and Thomas Klein (Laboratory for Radio-Isotopes University of Göttingen) for excellent technical support. Funding of this work by the Ministry for Science and Culture of Lower Saxony (Germany) as part of the program “Klimafolgenforschung in Niedersachsen” (KLIFF) and German Science Foundation (DFG, Grant PE 2256/1-1) is gratefully acknowledged. Ngoc Quynh Nguyen is grateful to the Ministry of Education and Training of Vietnam for a Ph.D. student scholarship.

Author information

Author notes

  1. Quynh Ngoc Nguyen

    Present address: Hung Vuong University, Nong Trang, Viet Tri, Phu Tho, Vietnam

Authors and Affiliations

  1. Forest Botany and Tree Physiology, University of Goettingen, Buesgenweg 2, 37077, Goettingen, Germany

    Quynh Ngoc Nguyen, Andrea Polle & Rodica Pena

Authors
  1. Quynh Ngoc Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea Polle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rodica Pena
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rodica Pena.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by M. Zwieniecki.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nguyen, Q.N., Polle, A. & Pena, R. Intraspecific variations in drought response and fitness traits of beech (Fagus sylvatica L.) seedlings from three provenances differing in annual precipitation. Trees 31, 1215–1225 (2017). https://doi.org/10.1007/s00468-017-1539-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-017-1539-1

Keywords

Search

Navigation