European Journal of Forest Research

, Volume 138, Issue 1, pp 79–92 | Cite as

Variation in the performance and thermostability of photosystem II in European beech (Fagus sylvatica L.) provenances is influenced more by acclimation than by adaptation

  • Daniel KurjakEmail author
  • Alena Konôpková
  • Jaroslav Kmeť
  • Miroslava Macková
  • Josef Frýdl
  • Marek Živčák
  • Sari Palmroth
  • Ľubica Ditmarová
  • Dušan Gömöry
Original Paper


The assisted migration of resistant seeds and seedlings may be a key to mitigating the effects of climate change on the productivity and composition of forest ecosystems. These efforts require an understanding of the intraspecific variability in the response of trees to extreme weather events such as heat waves. In this study, we assessed the geographical patterns of photosystem II (PSII) performance and thermostability in European beech (Fagus sylvatica L.) and whether intraspecific differences are associated with climate of origin. Two provenance trials with starkly contrasting climates were used for this study. Leaves were sampled both before and after natural heat stress exposure. Rapid chlorophyll fluorescence kinetics was used to evaluate PSII performance and PSII thermostability after simulated heat stress. The performance of PSII at 30 °C, which is still considered a non-damaging temperature, was generally slightly better at the warmer location than at the colder location. The populations originating closer to the Slovenian refugium, as well as those growing closer to their site of origin, showed better performance of PSII but not greater thermostability. The effect of simulated heat stress was much stronger in the colder plots compared to the warmer plots, but only for previously stressed trees. Likewise, we found indicators of geographical patterns of thermotolerance as well as relationships between thermotolerance and climate of origin mostly for trees exposed to natural heat. While the origin of provenances partly explained the variation among provenances, acclimation driven by climate played a major role in the response to heat stress. In beech, PSII seems to have a potential for coping with high temperature.


Heat stress Thermotolerance Fagus sylvatica L. Chlorophyll a fluorescence JIP test Provenance trial Intraspecific variability 



Basal fluorescence


Maximum quantum yield of PSII photochemistry


Photosynthetic performance index


Severity of thermal stress, the ratio between the Fv/Fm measured after simulated heat stress and the value of Fv/Fm measured under non-stressing temperature


The temperature at which Fv/Fm declines 15% from the maximum value


The critical temperature inducing abrupt changes in F0



The provenance experiment has been established through the realization of the project European Network for the Evaluation of the Genetic Resources of Beech for Appropriate Use in Sustainable Forestry Management (AIR3-CT94-2091) under the coordination of H.-J. Muhs and G. von Wühlisch. The experimental plots Tále and Zbraslav were established by L. Paule and V. Hynek, respectively. The study was supported by research grants of the Slovak Research and Development Agency APVV-0135-12, by the project of the Ministry of Agriculture of the Czech Republic—institutional support MZE-RO0118 and by the Research Agency of the MESRS of the SR, Project No. ITMS 26220220066 (20%). International cooperation in the study of physiological variability of beech provenances was established within the COST action FP1202 Strengthening conservation: a key issue for adaptation of marginal/peripheral populations of forest trees to climate change in Europe (MaP-FGR).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10342_2018_1155_MOESM1_ESM.xlsx (27 kb)
Supplementary material 1 (XLSX 27 kb)
10342_2018_1155_MOESM2_ESM.docx (1.2 mb)
Supplementary material 2 (DOCX 1197 kb)


  1. Alía R, Moro-Serrano J, Notivol E (2001) Genetic variability of Scots pine (Pinus sylvestris) provenances in Spain: growth traits and survival. Silva Fenn 35:27–38CrossRefGoogle Scholar
  2. Aranda I, Cano FJ, Gasco A, Cochard H, Nardini A, Mancha JA, Lopez R, Sanchez-Gomez D (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 35:34–46CrossRefGoogle Scholar
  3. Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Ann Rev Plant Physio 31:491–543CrossRefGoogle Scholar
  4. Bigras FJ (2000) Selection of white spruce families in the context of climate change: heat tolerance. Tree Physiol 20:1227–1234CrossRefGoogle Scholar
  5. Brestic M, Zivcak M (2013) PSII fluorescence techniques for measurement of drought and high temperature stress signal in crop plants: protocols and applications. In: Rout GR, Das AB (eds) Molecular stress physiology of plants. Springer India, India, pp 87–131CrossRefGoogle Scholar
  6. Brestic M, Zivcak M, Kalaji HM, Carpentier R, Allakhverdiev SI (2012) Photosystem II thermostability in situ: environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L. Plant Physiol Biochem 57:93–105CrossRefGoogle Scholar
  7. Buiteveld J, Vendramin GG, Leonardi S, Kamer K, Geburek T (2007) Genetic diversity and differentiation in European beech (Fagus sylvatica L.) stands varying in management history. Forest Ecol Manag 247:98–106CrossRefGoogle Scholar
  8. Bussotti F, Pollastrini M (2017) Observing climate change impacts on European forests: what works and what does not in ongoing long-term monitoring networks. Front Plant Sci 8:629CrossRefGoogle Scholar
  9. Bussotti F, Desotgiu R, Pollastrini M, Cascio C (2010) The JIP test: a tool to screen the capacity of plant adaptation to climate change. Scand J For Res 25:43–50CrossRefGoogle Scholar
  10. Bussotti F, Pollastrini M, Holland V, Brüggemann W (2015) Functional traits and adaptive capacity of European forests to climate change. Environ Exp Bot 111:91–113CrossRefGoogle Scholar
  11. Carsjens C, Nguyen Ngoc Q, Guzy J, Knutzen F, Meier IC, Muller M, Finkeldey R, Leuschner C, Polle A (2014) Intra-specific variations in expression of stress-related genes in beech progenies are stronger than drought-induced responses. Tree Physiol 34:1348–1361CrossRefGoogle Scholar
  12. Comps B, Gömöry D, Letouzey J, Thiébaut B, Petit RJ (2001) Diverging trends between heterozygosity and allelic richness during postglacial colonization in the European beech. Genetics 157:389–397Google Scholar
  13. Digrado A, Bachy A, Mozaffar A, Schoon N, Bussotti F, Amelynck C, Dalcq AC, Fauconnier ML, Aubinet M, Heinesch B, du Jardin P, Delaplace P (2017) Long-term measurements of chlorophyll a fluorescence using the JIP-test show that combined abiotic stresses influence the photosynthetic performance of the perennial ryegrass (Lolium perenne) in a managed temperate grassland. Physiol Plant 161:355–371CrossRefGoogle Scholar
  14. Dreyer E, Le Roux X, Montpied P, Daudet FA, Masson F (2001) Temperature response of leaf photosynthetic capacity in seedlings from seven temperate tree species. Tree Physiol 21:223–232CrossRefGoogle Scholar
  15. Fijarczyk A, Babik W (2015) Detecting balancing selection in genomes: limits and prospects. Mol Ecol 24:3529–3545CrossRefGoogle Scholar
  16. Froux F, Ducrey M, Epron D, Dreyer E (2004) Seasonal variations and acclimation potential of the thermostability of photochemistry in four Mediterranean conifers. Ann For Sci 61:235–241CrossRefGoogle Scholar
  17. Georgieva K, Tsonev T, Velikova V, Yordanov I (2000) Photosynthetic activity during high temperature treatment of pea plants. J Plant Physiol 157:169–176CrossRefGoogle Scholar
  18. Ghouil H, Montpied P, Epron D, Ksontini M, Hanchi B, Dreyer E (2003) Thermal optima of photosynthetic functions and thermostability of photochemistry in cork oak seedlings. Tree Physiol 23:1031–1039CrossRefGoogle Scholar
  19. Gömöry D, Paule L, Vyšný J (2007) Patterns of allozyme variation in western Eurasian Fagus. Bot J Linn Soc 154:165–174CrossRefGoogle Scholar
  20. Gömöry D, Ditmarová Ľ, Hrivnák M, Jamnická G, Kmeť J, Krajmerová D, Kurjak D (2015) Differentiation in phenological and physiological traits in European beech (Fagus sylvatica L.). Eur J For Res 134:1075–1085CrossRefGoogle Scholar
  21. Guissé B, Srivastava A, Strasser RJ (1995) The polyphasic rise of the chlorophyll a fluorescence (O–K–J–I–P) in heat stressed leaves. Arch Sci Genève 48:147–160Google Scholar
  22. Hajek P, Kurjak D, von Wühlisch G, Delzon S, Schuldt B (2016) Intraspecific variation in wood anatomical, hydraulic, and foliar traits in ten European beech provenances differing in growth yield. Front Plant Sci 7:791CrossRefGoogle Scholar
  23. Havaux M (1993) Rapid photosynthetic adaptation to heat stress triggered in potato leaves by moderately elevated temperatures. Plant Cell Environ 16:461–467CrossRefGoogle Scholar
  24. Havaux M, Gruszecki WI, Dupont I, Leblanc RM (1991) Increased heat emission and its relationship to the xanthophyll cycle in pea leaves exposed to strong light stress. J Photochem Photobiol B Biol 8:361–370CrossRefGoogle Scholar
  25. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  26. Ilík P, Špundová M, Šicner M, Melkovičová H, Kučerová Z, Krchňák P, Fürst T, Večeřová K, Panzarová K, Benediktyová Z, Trtílek M (2018) Estimating heat tolerance of plants by ion leakage: a new method based on gradual heating. New Phytol 218:1278–1287CrossRefGoogle Scholar
  27. Ježík M, Blaženec M, Střelcová K, Ditmarová Ľ (2011) The impact of the 2003–2008 weather variability on intra-annual stem diameter changes of beech trees at a submontane site in central Slovakia. Dendrochronologia 29:227–235CrossRefGoogle Scholar
  28. Jump AS, Hunt JM, Peñuelas J (2006) Rapid climate change-related growth decline at the southern range edge of Fagus sylvatica. Glob Change Biol 12:2163–2174CrossRefGoogle Scholar
  29. Kalaji HM, Schansker G, Brestic M, Bussotti F, Calatayud A, Ferroni L, Goltsev V, Guidi L, Jajoo A, Li P, Losciale P, Mishra VK, Misra AN, Nebauer SG, Pancaldi S, Penella C, Pollastrini M, Suresh K, Tambussi E, Yanniccari M, Zivcak M, Cetner MD, Samborska IA, Stirbet A, Olsovska K, Kunderlikova K, Shelonzek H, Rusinowski S, Bąba W (2017) Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynth Res 132:13–66CrossRefGoogle Scholar
  30. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241CrossRefGoogle Scholar
  31. Konôpková A, Kurjak D, Kmeť J, Klumpp R, Longauer R, Ditmarová Ľ, Gömöry D (2018) Differences in photochemistry and response to heat stress between silver fir (Abies alba Mill.) provenances. Trees 32:73–86CrossRefGoogle Scholar
  32. Kouřil R, Lazár D, Ilík P, Skotnica J, Krchnák P, Naus J (2004) High-temperature induced chlorophyll fluorescence rise in plants at 40–50 degrees C: experimental and theoretical approach. Photosynt Res 81:49–66CrossRefGoogle Scholar
  33. Kučerová J, Konôpková A, Pšidová E, Kurjak D, Jamnická G, Slugenová K, Gömöry D, Ditmarová L (2018) Adaptive variation in physiological traits of beech provenances in Central Europe. iForest 11:24–31CrossRefGoogle Scholar
  34. Ladjal M, Epron D, Ducrey M (2000) Effects of drought preconditioning on thermotolerance of photosystem II and susceptibility of photosynthesis to heat stress in cedar seedlings. Tree Physiol 20:1235–1241CrossRefGoogle Scholar
  35. Lazár D, Ilík P (1997) High-temperature induced chlorophyll fluorescence changes in barley leaves. Comparison of the critical temperatures determined from fluorescence induction and from fluorescence temperature curve. Plant Sci 124:159–164CrossRefGoogle Scholar
  36. Lazár D, Ilík P, Nauš J (1997) An appearance of K-peak in fluorescence induction depends on the acclimation of barley leaves to higher temperatures. J Lumin 72–74:595–596CrossRefGoogle Scholar
  37. Li J, Li H, Jakobsson M, Li S, Sjödin P, Lascoux M (2012) Joint analysis of demography and selection in population genetics: where do we stand and where could we go? Mol Ecol 21:28–44CrossRefGoogle Scholar
  38. Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gomory D, Latalowa M, Litt T, Paule L, Roure JM, Tantau I, van der Knaap WO, Petit RJ, de Beaulieu JL (2006) A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol 171:199–221CrossRefGoogle Scholar
  39. Mátyás C (1994) Modeling climate change effects with provenance test data. Tree Physiol 14:797–804CrossRefGoogle Scholar
  40. Mátyás C, Berki I, Czúcz B, Gálos B, Móricz N, Rasztovits E (2010) Future of beech in Southeast Europe from the perspective of evolutionary ecology. Acta Silv Lignaria Hung 6:91–110Google Scholar
  41. Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. BBA Bioenerg 1767:414–421CrossRefGoogle Scholar
  42. Pachauri RK, Mayer L et al (2014) Climate change 2014: synthesis report. In: Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. IPCC, Geneva, SwitzerlandGoogle Scholar
  43. Paludan-Müller G, Saxe H, Leverenz JW (1999) Responses to ozone in 12 provenances of European beech (Fagus sylvatica): genotypic variation and chamber effects on photosynthesis and dry-matter partitioning. New Phytol 144:261–273CrossRefGoogle Scholar
  44. Pšidová E, Živčák M, Stojnić S, Orlović S, Gömöry D, Kučerová J, Ditmarová Ľ, Střelcová K, Brestič M, Kalaji HM (2018) Altitude of origin influences the responses of PSII photochemistry to heat waves in European beech (Fagus sylvatica L.). Environ Exp Bot 152:97–106CrossRefGoogle Scholar
  45. 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 8:1111–1121CrossRefGoogle Scholar
  46. Robson TM, Garzón MB, BeechCOSTe52 database consortium (2018) Phenotypic trait variation measured on European genetic trials of Fagus sylvatica L. Sci Data 5:180149CrossRefGoogle Scholar
  47. Rose L, Leuschner C, Köckemann B, Buschmann H (2009) Are marginal beech (Fagus sylvatica L.) provenances a source for drought tolerant ecotypes? Eur J For Res 128:335–343CrossRefGoogle Scholar
  48. Schuldt B, Knutzen F, Delzon S, Jansen S, Müller-Haubold H, Burlett R, Clough Y, Leuschner C (2016) How adaptable is the hydraulic system of European beech in the face of climate change-related precipitation reduction? New Phytol 210:443–458CrossRefGoogle Scholar
  49. Snider JL, Oosterhuis DM, Collins GD, Pilon C, FitzSimons TR (2013) Field-acclimated Gossypium hirsutum cultivars exhibit genotypic and seasonal differences in photosystem II thermostability. J Plant Physiol 170:489–496CrossRefGoogle Scholar
  50. Stirbet A, Lazár D, Kromdijk J (2018) Chlorophyll a fluorescence induction: can just a one-second measurement be used to quantify abiotic stress responses? Photosynthetica 56:86–104CrossRefGoogle Scholar
  51. Stojnić S, Orlović S, Pilipović A, Vilotic D, Sijacic-Nikolic M, Miljkovic D (2012) Variation in leaf physiology among three provenances of European beech (Fagus sylvatica L.) in provenance trial in Serbia. Genetika 44:341–353CrossRefGoogle Scholar
  52. Stojnić S, Orlović S, Trudić B, Živković U, von Wuehlisch G, Miljković D (2015) Phenotypic plasticity of European beech (Fagus sylvatica L.) stomatal features under water deficit assessed in provenance trial. Dendrobiology 73:163–173CrossRefGoogle Scholar
  53. Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Probing photosynthesis: mechanisms, regulation and adaptation, pp 445–483Google Scholar
  54. Weng JH, Lai MF (2005) Estimating heat tolerance among plant species by two chlorophyll fluorescence parameters. Photosynthetica 43:439–444CrossRefGoogle Scholar
  55. Williams MI, Dumroese RK (2013) Preparing for climate change: forestry and assisted migration. J For 111:287–297Google Scholar
  56. Wu Q, Zheng P, Hu Y, Wei F (2014) Genome-scale analysis of demographic history and adaptive selection. Protein Cell 5:99–112CrossRefGoogle Scholar
  57. Yamane Y, Kashino Y, Koike H, Satoh K (1997) Increases in the fluorescence Fo level and reversible inhibition of Photosystem II reaction center by high-temperature treatments in higher plants. Photosynth Res 52:57–64CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Faculty of ForestryTechnical University in ZvolenZvolenSlovakia
  2. 2.Forestry and Game Management Research InstituteJílovištěCzech Republic
  3. 3.Faculty of Agrobiology and Food ResourcesSlovak University of Agriculture in NitraNitraSlovakia
  4. 4.Division of Environmental Science and Policy, Nicholas School of the EnvironmentDuke UniversityDurhamUSA
  5. 5.Institute of Forest EcologySlovak Academy of SciencesZvolenSlovakia

Personalised recommendations