Skip to main content
Log in

Seasonality of PSII thermostability and water use efficiency of in situ mountainous Norway spruce (Picea abies)

  • Original Paper
  • Published:
Journal of Forestry Research Aims and scope Submit manuscript

Abstract

The stability of monocultural, even-aged spruce forests at lower altitudes in Central Europe is seriously threatened by the prospects of global climate change. The thermostability and water use efficiency of their photosynthetic apparatus might play a vital role in their successful acclimation. In this study, photosystem II (PSII) performance (OJIP transient, rapid light curves) and thermostability were analyzed in Norway spruce (Picea abies (L.) Karst.) throughout the growing season of the exceptionally warm year 2018 (May–September) in the Western Carpathians, Slovakia. These measurements were accompanied by analysis of pigment concentrations in the needles. In addition, gas-exchange temperature curves were produced weekly from June until September to obtain intrinsic water use efficiencies. At the beginning of the growing season, needles exposed to heat stress showed significantly higher basal fluorescence and lower quantum yield, performance index, critical temperature thresholds of PSII inactivation and non-photochemical yield in comparison to other months. The overall thermostability (heat-resistance) of PSII peaked in July and August, reflected in the lowest basal fluorescence and the highest quantum yield of PSII, critical temperature thresholds and yield of non-photochemical quenching under heat stress. Additionally, the ratio between chlorophyll and carotenoids was the highest in August and had a positive impact on PSII thermostability. Moreover, the high-temperature intrinsic water use efficiency was significantly higher during July and August than in June. Results show that 15-year-old trees of Picea abies at 840 m a.s.l. exhibited acclimative seasonal responses of PSII thermostability and intrinsic water use efficiency during an exceptionally warm year. Our results suggest that mountainous P. abies at lower altitudes can acclimate their photosynthetic apparatus to higher temperatures during summer.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Agrawal D, Jajoo A (2015) Investigating primary sites of damage in photosystem II in response to high temperature. Indian J Plant Physiol 20:304–309

    Article  Google Scholar 

  • Altman J, Fibich P, Santruckova H, Dolezal J, Stepanek P, Kopacek J, Hunova I, Oulehle F, Tumajer J, Cienciala E (2017) Environmental factors exert strong control over the climate-growth relationships of Picea abies in Central Europe. Sci Total Environ 609:506–516

    Article  CAS  Google Scholar 

  • Augé RM, Green CD, Stodola AJW, Saxton AM, Olinick JB, Evans RM (2000) Correlations of stomatal conductance with hydraulic and chemical factors in several deciduous tree species in a natural habitat. New Phytol 145:483–500

    Article  Google Scholar 

  • Barnes JD, Pfirrmann T, Steiner K, Lutz C, Busch U, Kuchenhoff H, Payer HD (1995) Effects of elevated CO2, elevated O3 and potassium deficiency on Norway spruce (Picea abies (L) Karst.): seasonal changes in photosynthesis and non-structural carbohydrate content. Plant Cell Environ 18:1345–1457

    Article  CAS  Google Scholar 

  • Bigras FJ (2000) Selection of white spruce families in the context of climate change: heat tolerance. Tree Physiol 20:1227–1234

    Article  CAS  Google Scholar 

  • Blattný T, Šťastný T (1959) Prirodzené rozšírenie lesných drevín na Slovensku. Natural distribution of woody species in Slovakia, SVTL, Bratislava, Slovakia4

    Google Scholar 

  • 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 87–131. https://doi.org/10.1007/978-81-322-0807-5_4

    Chapter  Google Scholar 

  • Busch F, Hüner NPA, Ensminger I (2007) Increased air temperature during simulated autumn conditions does not increase photosynthetic carbon gain but affects the dissipation of excess energy in seedlings of the evergreen conifer Jack pine. Plant Physiol 143:1242–1251

    Article  CAS  Google Scholar 

  • Cannell MGR (1989) Physiological basis of wood production: a review. Scand J for Res 4:459–490

    Article  Google Scholar 

  • D’Odorico P, Besik A, Wong CYS, Isabel N, Ensminger I (2020) High-throughput drone-based remote sensing reliably tracks phenology in thousands of conifer seedlings. New Phytol 226:1667–1681

    Article  Google Scholar 

  • Day TA, Heckathorn SA, DeLucia EH (1991) Limitations of photosynthesis in Pinus taeda L. (loblolly pine) at low soil temperatures. Plant Physiol 96:1246–1254

    Article  CAS  Google Scholar 

  • Deligöz A, Bayar E, Genç M, Karatepe Y, Kirdar E, Cankara F (2018) Seasonal and needle age-related variations in the biochemical characteristics of Pinus nigra subsp. pallasiana (Lamb.) Holmboe. J for Sci 64:379–386

    Article  Google Scholar 

  • Ensminger I, Schmidt L, Lloyd J (2008) Soil temperature and intermittent frost modulate the rate of recovery of photosynthesis in Scots pine under simulated spring conditions. New Phytol 177:428–442

    Article  CAS  Google Scholar 

  • Faseela P, Sinisha AK, Brestič M, Puthur JT (2020) Special issue in honour of Prof. Reto J. Strasser-Chlorophyll a fluorescence parameters as indicators of a particular abiotic stress in rice. Photosynthetica 58:293–300

    Article  CAS  Google Scholar 

  • Fleischer P, Pichler V, Fleischer JP, Holko L, Máliš F, Gömöryová E, Cudlín P, Holeksa J, Michalová Z, Homolová Z, Škvarenina J, Střelcová K, Hlaváč P (2017) Forest ecosystem services affected by natural disturbances, climate and land-use changes in the Tatra Mountains. Clim Res 73:57–71

    Article  Google Scholar 

  • 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 61:235–241

    Article  CAS  Google Scholar 

  • Gagne M, Minocha R, Long S, McCulloh K (2020) Species-specific combined effects of heatwaves, drought, and elevated (CO2) on cellular metabolism in the foliage. Picea abies and Betula papyrifera (preprint). https://doi.org/10.22541/au.159714926.65470087

  • Gimenez C, Fereres E, Ruz C, Orgaz F (1997) Water relations and gas exchange of olive trees: diurnal and seasonal patterns of leaf water potential, photosynthesis and stomatal conductance. Acta Hortic. https://doi.org/10.17660/ActaHortic.1997.449.57

    Article  Google Scholar 

  • González de Andrés E, Blanco JA, Imbert JB, Guan BT, Lo Y, Castillo FJ (2019) ENSO and NAO affect long-term leaf litter dynamics and stoichiometry of Scots pine and European beech mixedwoods. Glob Change Biol 25:3070–3090

    Article  Google Scholar 

  • Guerrieri R, Belmecheri S, Ollinger SV, Asbjornsen H, Jennings K, Xiao J, Stocker BD, Martin M, Hollinger DY, Bracho-Garrillo R, Clark K, Dore S, Kolb T, Munger JW, Novick K, Richardson AD (2019) Disentangling the role of photosynthesis and stomatal conductance on rising forest water-use efficiency. Proc NatL Acad Sci 116:16909–16914

    Article  CAS  Google Scholar 

  • Guissé B, Srivastava A, Strasser RJ (1995) The polyphasic rise of the chlorophyll a fluorescence (O-K-J-I-P) in heat-stressed leaves. Archs Sci Geneve 48(2):147–160

    Google Scholar 

  • Hartl-Meier C, Zang C, Dittmar C, Esper J, Göttlein A, Rothe A (2014) Vulnerability of Norway spruce to climate change in mountain forests of the European Alps. Clim Res 60:119–132

    Article  Google Scholar 

  • Hatfield JL, Dold C (2019) Water-use efficiency: advances and challenges in a changing climate. Front Plant Sci 10:103. https://doi.org/10.3389/fpls.2019.00103

    Article  Google Scholar 

  • Havaux M, Dall’Osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145:1506–1520

    Article  CAS  Google Scholar 

  • Hikosaka K (2021) Photosynthesis, chlorophyll fluorescence and photochemical reflectance index in photoinhibited leaves. Funct Plant Biol 48:815. https://doi.org/10.1071/FP20365

    Article  CAS  Google Scholar 

  • Huang W, Yang YJ, Hu H, Zhang SB (2016) Seasonal variations in photosystem I compared with photosystem II of three alpine evergreen broad-leaf tree species. J Photochem Photobiol B 165:71–79

    Article  CAS  Google Scholar 

  • Húdoková H, Petrik P, Petek-Petrik A, Konôpková A, Leštianska A, Střelcová K, Kmeť J, Kurjak D (2022) Heat-stress response of photosystem II in five ecologically important tree species of European temperate forests. Biologia. https://doi.org/10.1007/s11756-021-00958-9

    Article  Google Scholar 

  • Jamnická G, Fleischer P, Konôpková A, Pšidová E, Kučerová J, Kurjak D, Živčák M, Ditmarová L (2019) Norway spruce (Picea abies L.) provenances use different physiological strategies to cope with water deficit. Forests 10:651. https://doi.org/10.3390/f10080651

    Article  Google Scholar 

  • Jamnická G, Konôpková A, Petrík P, Petek A, Húdoková H, Fleischer P, Homolová Z, Ježík M, Ditmarová Ľ (2020) Physiological vitality of Norway spruce (Picea abies L.) stands along an altitudinal gradient in Tatra National Park. Cent Eur for J 66:227–242. https://doi.org/10.2478/forj-2020-0019

    Article  Google Scholar 

  • Janka E, Körner O, Rosenqvist E, Ottosen CO (2013) High temperature stress monitoring and detection using chlorophyll a fluorescence and infrared thermography in chrysanthemum (Dendranthema grandiflora). Plant Physiol Biochem 67:87–94

    Article  CAS  Google Scholar 

  • Jensen AM, Warren JM, Hanson PJ, Childs J, Wullschleger SD (2015) Needle age and season influence photosynthetic temperature response and total annual carbon uptake in mature Picea mariana trees. Ann Bot 116:821–832

    Article  CAS  Google Scholar 

  • Karlický V, Kurasová I, Ptáčková B, Večeřová K, Urban O, Špunda V (2016) Enhanced thermal stability of the thylakoid membranes from spruce. a comparison with selected angiosperms. Photosynth Res 130:357–371

    Article  Google Scholar 

  • Katanić Z, Atić L, Dž F, Cesar V, Lepeduš H (2012) PSII photochemistry in vegetative buds and needles of Norway spruce (Picea abies L. Karst.) probed by OJIP chlorophyll a fluorescence measurement. Acta Biol Hung 63:218–230

    Article  Google Scholar 

  • Klughammer C, Schreiber U (2008) Complementary PSII quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. PAM Appl Notes 1:27–35

    Google Scholar 

  • Koller S, Holland V, Brüggemann W (2020) Special issue in honour of Prof. Reto J. Strasser-Seasonal monitoring of PSII functionality and relative chlorophyll content on a field site in two consecutive years: a case study of different oak species. Photosynthetica 58:379–390

    Article  CAS  Google Scholar 

  • 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 32:73–86

    Article  Google Scholar 

  • Korshykov I, Shevchuk N, Guseynova E (2019) The changes of colouring and content of photosynthetic pigments in unevenaged needles of Picea pungens Engelm. in conditions of urban plantings. Plant Introduction 81:82–89

    Google Scholar 

  • Kotakis C, Akhtar P, Zsiros O, Garab G, Lambrev PH (2018) Increased thermal stability of photosystem II and the macro-organization of thylakoid membranes, induced by co-solutes, associated with changes in the lipid-phase behaviour of thylakoid membranes. Photosynthetica 56:254–264

    Article  CAS  Google Scholar 

  • Kovač Ž, Platt T, Ninčević Gladan Ž, Morović M, Sathyendranath S, Raitsos D, Grbec B, Matić F, Veža J (2018) A 55-year time series station for primary production in the Adriatic Sea: data correction, extraction of photosynthesis parameters and regime shifts. Remote Sens 10:1460. https://doi.org/10.3390/rs10091460

    Article  Google Scholar 

  • Krejza J, Cienciala E, Světlík J, Bellan M, Noyer E, Horáček P, Štěpánek P, Marek MV (2021) Evidence of climate-induced stress of Norway spruce along elevation gradient preceding the current dieback in Central Europe. Trees 35:103–119

    Article  Google Scholar 

  • Kunert N, Hajek P, Hietz P, Morris H, Rosner S, Tholen D (2021) Summer temperatures reach the thermal tolerance threshold of photosynthetic decline in temperate conifers. Plant Biol. https://doi.org/10.1111/plb.13349

    Article  Google Scholar 

  • Kurjak D, Konôpková A, Kmeť J, Macková M, Frýdl J, Živčák M, Palmroth S, Ditmarová Ľ, Gömöry D (2019) Variation in the performance and thermostability of photosystem II in European beech (Fagus sylvatica L.) provenances is influenced more by acclimation than by adaptation. Eur J for Res 138:79–92

    Article  CAS  Google Scholar 

  • 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 124:159–164

    Article  Google Scholar 

  • Lazár D, Pospíšil P (1999) Mathematical simulation of chlorophyll a fluorescence rise measured with 3-(3′,4′-dichlorophenyl)-1,1-dimethylurea-treated barley leaves at room and high temperatures. Eur Biophys J 28:468–477

    Article  Google Scholar 

  • Lazár D, Pospíšil P, Nauš J (1999) Decrease of fluorescence intensity after the K Step in chlorophyll a fluorescence induction is suppressed by electron acceptors and donors to photosystem II. Photosynthetica 37:255–265

    Article  Google Scholar 

  • Lévesque M, Siegwolf R, Saurer M, Eilmann B, Rigling A (2014) Increased water-use efficiency does not lead to enhanced tree growth under xeric and mesic conditions. New Phytol 203:94–109

    Article  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In: Methods in enzymology (Vol. 148, pp. 350-382). Academic Press

  • Linares JC, Camarero JJ (2012) From pattern to process: linking intrinsic water-use efficiency to drought-induced forest decline. Glob Change Biol 18:1000–1015

    Article  Google Scholar 

  • Mafakheri A, Siosemardeh A, Bahramnejad B, Struik PC, Sohrabi Y (2010) Effect of drought stress on yield, proline and chlorophyll contents in three chickpea cultivars. Australian J Crop Sci 8:580–585

  • Magney TS, Bowling DR, Logan BA, Grossmann K, Stutz J, Blanken PD, Burns SP, Cheng R, Garcia MA, Kӧhler P, Lopez S, Parazoo NC, Raczka B, Schimel D, Frankenberg C (2019) Mechanistic evidence for tracking the seasonality of photosynthesis with solar-induced fluorescence. Proc Natl Acad Sci 116:11640–11645

    Article  CAS  Google Scholar 

  • Maslova TG, Mamushina NS, Sherstneva OA, Bubolo LS, Zubkova EK (2009) Seasonal structural and functional changes in the photosynthetic apparatus of evergreen conifers. Russ J Plant Physiol 56:607–615

    Article  CAS  Google Scholar 

  • Mathias JM, Thomas RB (2021) Global tree intrinsic water use efficiency is enhanced by increased atmospheric CO2 and modulated by climate and plant functional types. Proc Natl Acad Sci 118:e2014286118. https://doi.org/10.1073/pnas.2014286118

    Article  CAS  Google Scholar 

  • Mathur S, Allakhverdiev SI, Jajoo A (2011) Analysis of high temperature stress on the dynamics of antenna size and reducing side heterogeneity of Photosystem II in wheat leaves (Triticum aestivum). Biochim Biophys Acta BBA-Bioenerg 1807:22–29

    Article  CAS  Google Scholar 

  • Mathur S, Agrawal D, Jajoo A (2014) Photosynthesis: Response to high temperature stress. J Photochem Photobiol b, Biol 137:116–126

    Article  CAS  Google Scholar 

  • Mehne-Jakobs B (1995) Seasonal development of the photosynthetic performance of Norway spruce (Picea abies [L.] Karst.) under magnesium deficiency. Plant Soil 168–169:255–261. https://doi.org/10.1007/BF00029336

    Article  Google Scholar 

  • Mohammed GH, Colombo R, Middleton EM, Rascher U, van der Tol C, Nedbal L, Goulas Y, Pérez-Priego O, Damm A, Meroni M, Joiner J, Cogliati S, Verhoef W, Malenovský Z, Gastellu-Etchegorry JP, Miller JR, Guanter L, Moreno J, Moya I, Berry JA, Frankenberg C, Zarco-Tejada PJ (2019) Remote sensing of solar-induced chlorophyll fluorescence (SIF) in vegetation: 50 years of progress. Remote Sens Environ 231:111177. https://doi.org/10.1016/j.rse.2019.04.030

    Article  Google Scholar 

  • Mukherjee S, Mishra A, Trenberth KE (2018) Climate change and drought: a perspective on drought indices. Curr Clim Change Rep 4:145–163

    Article  Google Scholar 

  • Murthy R, Zarnoch SJ, Dougherty PM (1997) Seasonal trends of light-saturated net photosynthesis and stomatal conductance of loblolly pine trees grown in contrasting environments of nutrition, water and carbon dioxide. Plant Cell Environ 20:558–568

    Article  Google Scholar 

  • Navarro-Cerrillo RM, Sánchez-Salguero R, Herrera R, Ceacero Ruiz CJ, Moreno-Rojas JM, Manzanedo RD, López-Quintanilla J (2016) Contrasting growth and water use efficiency after thinning in mixed Abies pinsapoPinus pinasterPinus sylvestris forests. J for Sci 62:53–64

    Article  Google Scholar 

  • Neuwirth B, Rabbel I, Bendix J, Bogena HR, Thies B (2021) The European heat wave 2018: the dendroecological response of oak and spruce in Western Germany. Forests 12:283. https://doi.org/10.3390/f12030283

    Article  Google Scholar 

  • Orlowsky B, Seneviratne SI (2012) Global changes in extreme events: regional and seasonal dimension. Clim Change 110:669–696

    Article  Google Scholar 

  • Petrova S, Todorova K, Dakova M, Mehmed E, Nikolov B, Denev I, Stratiev M, Georgiev G, Delchev A, Stamenov S, Firkova L, Gesheva N, Kadirova D, Velcheva I (2017) Photosynthetic pigments as parameters/indicators of tree tolerance to urban environment (Plovdiv, Bulgaria). Ecol Balc 9:53–62

    Google Scholar 

  • Pietrzykowski M, Woś B (2021) The impact of climate change on forest tree species dieback and changes in their distribution. In: Choudhary DK, Mishra A, Varma A (eds) Climate change and the microbiome soil biology. Springer International Publishing, Cham, pp 447–460. https://doi.org/10.1007/978-3-030-76863-8_23

    Chapter  Google Scholar 

  • Pokhrel Y, Felfelani F, Satoh Y, Boulange J, Burek P, Gädeke A, Gerten D, Gosling SN, Grillakis M, Gudmundsson L, Hanasaki N, Kim H, Koutroulis A, Liu J, Papadimitriou L, Schewe J, Müller Schmied H, Stacke T, Telteu CE, Thiery W, Veldkamp T, Zhao F, Wada Y (2021) Global terrestrial water storage and drought severity under climate change. Nat Clim Change 11:226–233

    Article  Google Scholar 

  • Pollastri S, Tsonev T, Loreto F (2014) Isoprene improves photochemical efficiency and enhances heat dissipation in plants at physiological temperatures. J Exp Bot 65:1565–1570

    Article  CAS  Google Scholar 

  • Porcar-Castell A (2011) A high-resolution portrait of the annual dynamics of photochemical and non-photochemical quenching in needles of Pinus sylvestris. Physiol Plant 143:139–153

    Article  CAS  Google Scholar 

  • Raczka B, Porcar-Castell A, Magney T, Lee JE, Köhler P, Frankenberg C, Grossmann K, Logan BA, Stutz J, Blanken PD, Burns SP, Duarte H, Yang X, Lin JC, Bowling DR (2019) Sustained nonphotochemical quenching shapes the seasonal pattern of solar-induced fluorescence at a high-elevation evergreen forest. J Geophys Res Biogeosciences 124:2005–2020

    Article  Google Scholar 

  • Robinson DC, Wellburn AR (1991) Seasonal changes in the pigments of Norway spruce, Picea abies (L.) Karst, and the influence of summer ozone exposures. New Phytol 119:251–259. https://doi.org/10.1111/j.1469-8137.1991.tb01028.x

    Article  CAS  Google Scholar 

  • Saurer M, Siegwolf RTW, Schweingruber FH (2004) Carbon isotope discrimination indicates improving water-use efficiency of trees in northern Eurasia over the last 100 years: isotope discrimination in Northern Eurasia. Glob Change Biol 10:2109–2120

    Article  Google Scholar 

  • Schuldt B, Buras A, Arend M, Vitasse Y, Beierkuhnlein C, Damm A, Gharun M, Grams TEE, Hauck M, Hajek P, Hartmann H, Hiltbrunner E, Hoch G, Holloway-Phillips M, Körner C, Larysch E, Lübbe T, Nelson DB, Rammig A, Rigling A, Rose L, Ruehr NK, Schumann K, Weiser F, Werner C, Wohlgemuth T, Zang CS, Kahmen A (2020) A first assessment of the impact of the extreme 2018 summer drought on Central European forests. Basic Appl Ecol 45:86–103

    Article  Google Scholar 

  • Schurman JS, Trotsiuk V, Bače R, Čada V, Fraver S, Janda P, Kulakowski D, Labusova J, Mikoláš M, Nagel TA, Seidl R, Synek M, Svobodová K, Chaskovskyy O, Teodosiu M, Svoboda M (2018) Large-scale disturbance legacies and the climate sensitivity of primary Picea abies forests. Glob Change Biol 24:2169–2181

    Article  Google Scholar 

  • Shabala S (2017) Plant stress physiology. CAB International, Wallingford, UK

    Book  Google Scholar 

  • Silkina OV, Vinokurova RI (2009) Seasonal dynamics of chlorophyll and microelement content in developing conifer needles of Abies sibirica and Picea abies. Russ J Plant Physiol 56:780–786

    Article  CAS  Google Scholar 

  • Spiecker H (2000) Growth of Norway spruce (Picea abies [L.] Karst.) under changing environmental conditions in Europe. In: Klimo E, Hager H, Kulhavý J (Ed) Spruce monocultures in Central Europe—problems and prospects. EFI Proceedings. European Forest Institute, Joensuu, Finland, pp 11–26

  • 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 56:86–104

    Article  CAS  Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (Ed) Chlorophyll a fluorescence: a signature of photosynthesis. Springer Netherlands, Dordrecht, pp.321–362. https://doi.org/10.1007/978-1-4020-3218-9_12

  • Szőllősi E, Oláh V, Kanalas P, Kis J, Fenyvesi A, Mészáros I (2010) Seasonal variation of leaf ecophysiological traits within the canopy of Quercus petraea (Matt.) Liebl. trees. Acta Biol Hung 61:172–188

    Article  Google Scholar 

  • Tomášková I, Pastierovič F, Krejzková A, Čepl J, Hradecký J (2021) Norway spruce ecotypes distinguished by chlorophyll a fluorescence kinetics. Acta Physiol Plant 43:24. https://doi.org/10.1007/s11738-020-03190-1

    Article  CAS  Google Scholar 

  • Valadares J, Figueiredo de Paula N, Cesar de Paula R (2014) Physiological changes in eucalyptus hybrids under different irrigation regimes. Revista Ciencia Agronomica 45:805–814

  • Verhoeven A, Osmolak A, Morales P, Crow J (2009) Seasonal changes in abundance and phosphorylation status of photosynthetic proteins in eastern white pine and balsam fir. Tree Physiol 29:361–374

    Article  CAS  Google Scholar 

  • Vodnik D, Gogala N (1994) Seasonal fluctuations of photosynthesis and its pigments in 1-year mycorrhized spruce seedlings. Mycorrhiza 4:277–281

    Article  Google Scholar 

  • Voltas J, Aguilera M, Gutiérrez E, Shestakova TA (2020) Shared drought responses among conifer species in the middle Siberian taiga are uncoupled from their contrasting water-use efficiency trajectories. Sci Total Environ 720:137590. https://doi.org/10.1016/j.scitotenv.2020.137590

    Article  CAS  Google Scholar 

  • Waterhouse JS, Switsur VR, Barker AC, Carter AHC, Hemming DL, Loader NJ, Robertson I (2004) Northern European trees show a progressively diminishing response to increasing atmospheric carbon dioxide concentrations. Quat Sci Rev 23:803–810

    Article  Google Scholar 

  • Waters ER, Vierling E (2020) Plant small heat shock proteins—evolutionary and functional diversity. New Phytol 227:24–37

    Article  CAS  Google Scholar 

  • Wu G, Liu X, Chen T, Xu G, Wang B, Kang H, Li C, Zeng X (2020) The positive contribution of iWUE to the resilience of Schrenk spruce (Picea schrenkiana) to extreme drought in the western Tianshan Mountains, China. Acta Physiol Plant 42:168. https://doi.org/10.1007/s11738-020-03158-1

    Article  CAS  Google Scholar 

  • 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 52:57–64

    Article  CAS  Google Scholar 

  • Zarter CR, Demmig-Adams B, Ebbert V, Adamska I, Adams WW (2006) Photosynthetic capacity and light harvesting efficiency during the winter-to-spring transition in subalpine conifers. New Phytol 172:283–292

    Article  Google Scholar 

  • Zeltiņš P, Katrevičs J, Gailis A, Maaten T, Desaine I, Jansons A (2019) Adaptation capacity of Norway spruce provenances in western Latvia. Forests 10:840. https://doi.org/10.3390/f10100840

    Article  Google Scholar 

  • Zhang Q, Ficklin DL, Manzoni S, Wang L, Way D, Phillips RP, Novick KA (2019) Response of ecosystem intrinsic water use efficiency and gross primary productivity to rising vapor pressure deficit. Environ Res Lett 14:074023. https://doi.org/10.1088/1748-9326/ab2603

    Article  CAS  Google Scholar 

  • Zhou L, Wang S, Chi Y, Li Q, Huang K, Yu Q (2015) Responses of photosynthetic parameters to drought in subtropical forest ecosystem of China. Sci Rep 5:18254. https://doi.org/10.1038/srep18254

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

D.K. and P.F. conceived the study design and coordinated the experiment. P.P., A.P.P., A.K., and D.K. conducted the fluorescence measurements. P.P., A.P.P. and P.F. conducted the gas-exchange measurements. A.P.P., A.K. and S.S. conducted the assimilation pigments measurements. P.P., P.F. and I.K. performed the statistical analysis. P.P. and A.P.P. wrote the first version of the manuscript, which was discussed and approved by all the co-authors. All authors have read and agreed to the submitted version of the manuscript.

Corresponding author

Correspondence to Anja Petek-Petrik.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Project funding: This work was supported by the Ministry of Education, Youth and Sports of CR within the CzeCOS program (grant number LM2018123), the Slovak Grant Agency for Science (no. VEGA 1/0535/20) and Slovak Research and Development Agency (APVV-17-0644) and project FORRES, ITMS: 313011T678 (20%) supported by the Operational Programme Integrated Infrastructure (OPII) funded by the ERDF.

The online version is available at http://www.springerlink.com.

Guest editor: Yanbo Hu.

Corresponding editor: Yanbo Hu.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Petrik, P., Petek-Petrik, A., Konôpková, A. et al. Seasonality of PSII thermostability and water use efficiency of in situ mountainous Norway spruce (Picea abies). J. For. Res. 34, 197–208 (2023). https://doi.org/10.1007/s11676-022-01476-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11676-022-01476-3

Keywords

Navigation