Day-to-day variation in chlorophyll fluorescence parameters of northern and southern silver birch in a common garden

Olusegun Olaitan Akinyemi , Jaroslav Čepl , Sarita Keski-Saari , Jan Stejskal , Ivana Tomášková , Markku Keinänen , Sari Kontunen-Soppela

Journal of Forestry Research ›› 2025, Vol. 36 ›› Issue (1) : 16

PDF
Journal of Forestry Research ›› 2025, Vol. 36 ›› Issue (1) :16 DOI: 10.1007/s11676-024-01814-7
Original Paper
research-article

Day-to-day variation in chlorophyll fluorescence parameters of northern and southern silver birch in a common garden

Author information +
History +
PDF

Abstract

We used fast chlorophyll fluorescence transients (OJIP) to study provenance-related differences in photosynthetic performance and the magnitude of day-to-day chlorophyll fluorescence (ChlF) variation in northern (67° N) and southern (62° N) silver birches in a common garden at 62° N. ChlF transients were measured five times during two weeks in the middle of summer to avoid seasonal variation. Differences in growth and leaf morphological traits between the provenances were also examined. The northern trees had higher chlorophyll content, larger leaf areas, and higher leaf fresh and dry mass than the southern trees, but the leaf mass per area did not differ between the provenances. The southern trees were taller and showed higher annual shoot growth than the northern trees. For all the ChlF parameters, day-to-day variation was significant and followed the same pattern for both provenances with no significant provenance × day interaction, suggesting a similar response to environmental variation. The northern provenance had higher values in parameters related to the reduction of end electron acceptors at the Photosystem I (PSI) acceptor side as probed by ChlF. This and higher values for performance indices PIabs and PItot in northern than in southern trees suggest higher photosynthetic performance of northern trees in line with the latitudinal compensation strategy. Provenance differences in these parameters increased towards the end of the measurement period, suggesting preparation for earlier growth cessation in northern trees triggered by the shortening day length. The study shows that provenance differences in ChlF can be relatively stable regardless of environmental variation but might be influenced by physiological alterations in preparation for future changes in environmental conditions.

Keywords

JIP test / Betula pendula / Provenances / Intra-annual variation / Chlorophyll / Leaf mass per area / LMA / Growth

Cite this article

Download citation ▾
Olusegun Olaitan Akinyemi, Jaroslav Čepl, Sarita Keski-Saari, Jan Stejskal, Ivana Tomášková, Markku Keinänen, Sari Kontunen-Soppela. Day-to-day variation in chlorophyll fluorescence parameters of northern and southern silver birch in a common garden. Journal of Forestry Research, 2025, 36(1): 16 DOI:10.1007/s11676-024-01814-7

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Akinyemi OO, Čepl J, Keski-Saari S, Tomášková I, Stejskal J, Kontunen-Soppela S, Keinänen M. Derivative-based time-adjusted analysis of diurnal and within-tree variation in the OJIP fluorescence transient of silver birch. Photosynth Res, 2023, 157(2): 133-146

[2]

Baker NR, Rosenqvist E. Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot, 2004, 55(403): 1607-1621

[3]

Benowicz A, Guy RD, El-Kassaby YA. Geographic pattern of genetic variation in photosynthetic capacity and growth in two hardwood species from British Columbia. Oecologia, 2000, 123(2): 168-174

[4]

Björkman O, Demmig B. Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta, 1987, 170(4): 489-504

[5]

Brien CJ (2021) asremlPlus: Augments ASReml-R in fitting mixed models and packages generally in exploring prediction differences. R package version 1–4.

[6]

Bussotti F, Gerosa G, Digrado A, Pollastrini M. Selection of chlorophyll fluorescence parameters as indicators of photosynthetic efficiency in large scale plant ecological studies. Ecol Indic, 2020, 108: 105686

[7]

Butler DG, Cullis BR, Gilmour AR, Gogel BJ, Thompson R (2017) ASReml-R reference manual version 4. VSN International Ltd, Hemel Hempstead, HP1 1ES, UK.

[8]

Bylesjö M, Segura V, Soolanayakanahally RY, Rae AM, Trygg J, Gustafsson P, Jansson S, Street NR (2008) LAMINA: a tool for rapid quantification of leaf size and shape parameters. BMC Plant Biol 8:82. https://doi.org/10.1186/1471-2229-8-82

[9]

Ceppi MG, Oukarroum A, Çiçek N, Strasser RJ, Schansker G. The IP amplitude of the fluorescence rise OJIP is sensitive to changes in the photosystem I content of leaves: a study on plants exposed to magnesium and sulfate deficiencies, drought stress and salt stress. Physiol Plant, 2012, 144(3): 277-288

[10]

Colautti RI, Maron JL, Barrett SCH. Common garden comparisons of native and introduced plant populations: latitudinal clines can obscure evolutionary inferences. Evol Appl, 2009, 2(2187-199

[11]

Crous KY, Uddling J, De Kauwe MG. Temperature responses of photosynthesis and respiration in evergreen trees from boreal to tropical latitudes. New Phytol, 2022, 234(2): 353-374

[12]

Dąbrowski P, Keutgen AJ, Keutgen N, Sierka E, Baczewska-Dąbrowska AH, Mojski J, Pawluśkiewicz B, Sieczko L, Kalaji HM. Photosynthetic efficiency of perennial ryegrass (Lolium perenne L.) seedlings in response to Ni and Cd stress. Sci Rep, 2023, 13(1): 5357

[13]

De Frenne P, Graae BJ, Rodríguez-Sánchez F, Kolb A, Chabrerie O, Decocq G, De Kort H, De Schrijver A, Diekmann M, Eriksson O, Gruwez R, Hermy M, Lenoir J, Plue J, Coomes DA, Verheyen K. Latitudinal gradients as natural laboratories to infer species’ responses to temperature. J Ecol, 2013, 101(3784-795

[14]

Deepak M, Keski-Saari S, Fauch L, Granlund L, Oksanen E, Keinänen M. Spectral reflectance in silver birch genotypes from three provenances in Finland. Remote Sens, 2020, 12(17): 2677

[15]

Deepak M, Lihavainen J, Keski-Saari S, Kontunen-Soppela S, Salojärvi J, Tenkanen A, Heimonen K, Oksanen E, Keinänen M. Genotype- and provenance-related variation in the leaf surface secondary metabolites of silver birch. Can J for Res, 2018, 48(5494-505

[16]

Färkkilä SMA, Valtonen A, Saravesi K, Anslan S, Markkola A, Kontunen-Soppela S. The effects of geographic origin and genotype on fungal diversity of silver birch (Betula pendula). Fungal Ecol, 2023, 63: 101241

[17]

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

[18]

Fracheboud Y, Luquez V, Björkén L, Sjödin A, Tuominen H, Jansson S. The control of autumn senescence in European aspen. Plant Physiol, 2009, 149(4): 1982-1991

[19]

Gill AL, Gallinat AS, Sanders-DeMott R, Rigden AJ, Gianotti DJS, Mantooth JA, Templer PH. Changes in autumn senescence in northern hemisphere deciduous trees: a meta-analysis of autumn phenology studies. Ann Bot, 2015, 116(6): 875-888

[20]

Gilmour AR, Gogel BJ, Cullis BR, Welham S, Thompson R. ASREML user guide. Struct Specif Release, 2015, 4: 1

[21]

Gornall J, Guy R. Geographic variation in ecophysiological traits of black cottonwood (Populus trichocarpa). Can J Bot, 2007, 85: 1202-1213

[22]

Heimonen K, Valtonen A, Kontunen-Soppela S, Keski-Saari S, Rousi M, Oksanen E, Roininen H. Colonization of a host tree by herbivorous insects under a changing climate. Oikos, 2015, 124(8): 1013-1022

[23]

Heimonen K, Valtonen A, Kontunen-Soppela S, Keski-Saari S, Rousi M, Oksanen E, Roininen H. Insect herbivore damage on latitudinally translocated silver birch (Betula pendula)–predicting the effects of climate change. Clim Change, 2015, 131(2): 245-257

[24]

Húdoková H, Petrik P, Petek-Petrik A, Konôpková A, Leštianska A, Střelcová K, Kme J, Kurjak D. Heat-stress response of photosystem II in five ecologically important tree species of European temperate forests. Biologia, 2022, 77(3): 671-680

[25]

Hynynen J, Niemistö P, Viherä-Aarnio A, Brunner A, Hein S, Velling P. Silviculture of birch (Betula pendula Roth and Betula pubescens Ehrh.) in northern Europe. Forestry (Lond), 2010, 83(1): 103-119

[26]

Inoue S, Dang QL, Man RZ, Tedla B. Northward migration of trembling aspen will increase growth but reduce resistance to drought-induced xylem cavitation. Botany, 2019, 97(11): 627-638

[27]

Jalink H, van der Schoor R (2015) Role of fluorescence approaches to understand functional traits of photosynthesis. In: Phenomics in crop plants: trends, options and limitations. Springer India, pp 181–194. https://doi.org/10.1007/978-81-322-2226-2_12

[28]

Jansen M, Gilmer F, Biskup B, Nagel KA, Rascher U, Fischbach A, Briem S, Dreissen G, Tittmann S, Braun S, De Jaeger I, Metzlaff M, Schurr U, Scharr H, Walter A. Simultaneous phenotyping of leaf growth and chlorophyll fluorescence via GROWSCREEN FLUORO allows detection of stress tolerance in Arabidopsis thaliana and other rosette plants. Funct Plant Biol, 2009, 36(11): 902-914

[29]

Järvinen P, Lemmetyinen J, Savolainen O, Sopanen T. DNA sequence variation in BpMADS2 gene in two populations of Betula pendula. Mol Ecol, 2003, 12(2): 369-384

[30]

Kalaji HM, Govindjee BK, Kościelniak J, Żuk-Gołaszewska K. Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environ Exp Bot, 2011, 73: 64-72

[31]

Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, Brestic M, Bussotti F, Calatayud A, Dąbrowski P, Elsheery NI, Ferroni L, Guidi L, Hogewoning SW, Jajoo A, Misra AN, Nebauer SG, Pancaldi S, Penella C, Poli D, Pollastrini M, Romanowska-Duda ZB, Rutkowska B, Serôdio J, Suresh K, Szulc W, Tambussi E, Yanniccari M, Zivcak M. Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res, 2014, 122(2): 121-158

[32]

Kaluthota S, Pearce DW, Evans LM, Letts MG, Whitham TG, Rood SB. Higher photosynthetic capacity from higher latitude: foliar characteristics and gas exchange of southern, central and northern populations of Populus angustifolia. Tree Physiol, 2015, 35(9): 936-948

[33]

Kaluthota S, Pearce DW, Evans LM, Whitham TG, Rood SB. Greener leaves from northern trees: latitudinal compensation in riparian cottonwoods. For Ecol Manag, 2024, 562: 121919

[34]

Khan N, Essemine J, Hamdani S, Qu MN, Lyu MJA, Perveen S, Stirbet A, Govindjee G, Zhu XG. Natural variation in the fast phase of chlorophyll a fluorescence induction curve (OJIP) in a global rice minicore panel. Photosynth Res, 2021, 150(1–3): 137-158

[35]

Körner C. The use of ‘altitude’ in ecological research. Trends Ecol Evol, 2007, 22(11569-574

[36]

Lazár D. The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct Plant Biol, 2006, 33(1): 9-30

[37]

Matloobi M (2012) Light harvesting and photosynthesis by the canopy. In: Advances in Photosynthesis, Fundamental Aspects. https://doi.org/10.5772/27592

[38]

Mattila H, Khorobrykh S, Hakala-Yatkin M, Havurinne V, Kuusisto I, Antal T, Tyystjärvi T, Tyystjärvi E. Action spectrum of the redox state of the plastoquinone pool defines its function in plant acclimation. Plant J, 2020, 104(4): 1088-1104

[39]

Maurya JP, Bhalerao RP. Photoperiod- and temperature-mediated control of growth cessation and dormancy in trees: a molecular perspective. Ann Bot, 2017, 120(3): 351-360

[40]

McKown AD, Guy RD, Klápště J, Geraldes A, Friedmann M, Cronk QCB, El-Kassaby YA, Mansfield SD, Douglas CJ. Geographical and environmental gradients shape phenotypic trait variation and genetic structure in Populus trichocarpa. New Phytol, 2014, 201(4): 1263-1276

[41]

Murchie EH, Lawson T. Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot, 2013, 64(13): 3983-3998

[42]

Oukarroum A, Bussotti F, Goltsev V, Kalaji HM. Correlation between reactive oxygen species production and photochemistry of photosystems I and II in Lemna gibba L. plants under salt stress. Environ Exp Bot, 2015, 109: 80-88

[43]

Oukarroum A, Schansker G, Strasser RJ. Drought stress effects on photosystem I content and photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance. Physiol Plant, 2009, 137(2): 188-199

[44]

Palmé AE, Su Q, Rautenberg A, Manni F, Lascoux M. Postglacial recolonization and cpDNA variation of silver birch. Betula Pendula Mol Ecol, 2003, 12(1): 201-212

[45]

Petrik P, Petek-Petrik A, Kurjak D, Mukarram M, Klein T, Gömöry D, Střelcová K, Frýdl J, Konôpková A. Interannual adjustments in stomatal and leaf morphological traits of European beech (Fagus sylvatica L.) demonstrate its climate change acclimation potential. Plant Biol, 2022, 24(7): 1287-1296

[46]

Pollastrini M, Brüggeman W, Fotelli M, Bussotti F (2022) Downregulation of PSI regulates photosynthesis in early successional tree species. Evidence from a field survey across European forests. J Photochem Photobiol 12: 100145 https://doi.org/10.1016/j.jpap.2022.100145

[47]

Pollastrini M, Salvatori E, Fusaro L, Manes F, Marzuoli R, Gerosa G, Brüggemann W, Strasser RJ, Bussotti F. Selection of tree species for forests under climate change: is PSI functioning a better predictor for net photosynthesis and growth than PSII?. Tree Physiol, 2020, 40(11): 1561-1571

[48]

Possen BJHM, Rousi M, Keski-Saari S, Silfver T, Kontunen-Soppela S, Oksanen E, Mikola J. New evidence for the importance of soil nitrogen on the survival and adaptation of silver birch to climate warming. Ecosphere, 2021, 12(5): e03520

[49]

Provazník D, Stejskal J, Hansen OK, Čepl J, Erichsen ER, Hansen JK, Zádrapová D, Tomášková I. Addressing the altitudinal and geographical gradient in European beech via photosynthetic parameters: a case study on Calabrian beech transplanted to Denmark. Front for Glob Change, 2024, 7: 1369464

[50]

R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/

[51]

Rochaix JD. Regulation and dynamics of the light-harvesting system. Annu Rev Plant Biol, 2014, 65: 287-309

[52]

Salojärvi J, Smolander OP, Nieminen K, Rajaraman S, Safronov O, Safdari P, Lamminmäki A, Immanen J, Lan TY, Tanskanen J, Rastas P, Amiryousefi A, Jayaprakash B, Kammonen JI, Hagqvist R, Eswaran G, Ahonen VH, Serra JA, Asiegbu FO, de Dios B-L, Blande D, Blokhina O, Blomster T, Broholm S, Brosché M, Cui FQ, Dardick C, Ehonen SE, Elomaa P, Escamez S, Fagerstedt KV, Fujii H, Gauthier A, Gollan PJ, Halimaa P, Heino PI, Himanen K, Hollender C, Kangasjärvi S, Kauppinen L, Kelleher CT, Kontunen-Soppela S, Koskinen JP, Kovalchuk A, Kärenlampi SO, Kärkönen AK, Lim KJ, Leppälä J, MacPherson L, Mikola J, Mouhu K, Mähönen AP, Niinemets Ü, Oksanen E, Overmyer K, Palva ET, Pazouki L, Pennanen V, Puhakainen T, Poczai P, Possen BJHM, Punkkinen M, Rahikainen MM, Rousi M, Ruonala R, van der Schoot C, Shapiguzov A, Sierla M, Sipilä TP, Sutela S, Teeri TH, Tervahauta AI, Vaattovaara A, Vahala J, Vetchinnikova L, Welling A, Wrzaczek M, Xu EJ, Paulin LG, Schulman AH, Lascoux M, Albert VA, Auvinen P, Helariutta Y, Kangasjärvi J. Genome sequencing and population genomic analyses provide insights into the adaptive landscape of silver birch. Nat Genet, 2017, 49(6904-912

[53]

Savolainen O, Pyhäjärvi T, Knürr T. Gene flow and local adaptation in trees. Annu Rev Ecol Evol Syst, 2007, 38: 595-619

[54]

Schansker G, Srivastava A, Strasser RJ. Characterization of the 820 nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct Plant Biol, 2003, 30(7): 785-796

[55]

Schansker G, Tóth SZ, Strasser RJ. Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim Biophys Acta, 2005, 1706(3): 250-261

[56]

Sipka GB, Magyar M, Mezzetti A, Akhtar P, Zhu QJ, Xiao YN, Han GY, Santabarbara S, Shen JR, Lambrev PH, Garab G. Light-adapted charge-separated state of photosystem II: structural and functional dynamics of the closed reaction center. Plant Cell, 2021, 33(4): 1286-1302

[57]

Soolanayakanahally RY, Guy RD, Silim SN, Drewes EC, Schroeder WR. Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar (Populus balsamifera L.). Plant Cell Environ, 2009, 32(12): 1821-1832

[58]

Soolanayakanahally RY, Guy RD, Street NR, Robinson KM, Silim SN, Albrectsen BR, Jansson S. Comparative physiology of allopatric Populus species: geographic clines in photosynthesis, height growth, and carbon isotope discrimination in common gardens. Front Plant Sci, 2015, 6: 528

[59]

Stejskal J, Čepl J, Neuwirthová E, Akinyemi OO, Chuchlík J, Provazník D, Keinänen M, Campbell P, Albrechtová J, Lstibůrek M, et al.. Making the genotypic variation visible: hyperspectral phenotyping in scotspine seedlings. Plant Phenomics, 2023, 5: 0111

[60]

Stirbet A, Lazár D, KromdijkGovindjee J. Chlorophyll a fluorescence induction: can just a one-second measurement be used to quantify abiotic stress responses?. Photosynthetica, 2018, 56(1): 86-104

[61]

Strasser R, Srivastava A, Tsimilli-Michael M. Yunus M. The fluorescence transient as a tool to characterize and screen photosynthetic samples. Probing Photosynthesis: Mechanisms, 2000, London, Regulation and Adaptation, Taylor and Francis445-483

[62]

Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V. Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta, 2010, 1797(6–7): 1313-1326

[63]

Tedla B, Dang QL, Inoue S. White birch has limited phenotypic plasticity to take advantage of increased photoperiods at higher latitudes north of the seed origin. For Ecol Manag, 2019, 451: 117565

[64]

Tenkanen A (2023) Latitude-related variation in silver birch provenances in a changing climate: Growth, biomass allocation and photosynthesis-associated leaf-traits in the field and in growth chamber trials. Itä-Suomen yliopisto. https://erepo.uef.fi/handle/123456789/29468

[65]

Tenkanen A, Keinänen M, Oksanen E, Keski-Saari S, Kontunen-Soppela S. Polar day syndrome: differences in growth, photosynthetic traits and sink-size patterns between northern and southern Finnish silver birch (Betula pendula Roth) provenances in native and non-native photoperiods. Tree Physiol, 2023, 43(1): 16-30

[66]

Tenkanen A, Keski-Saari S, Salojärvi J, Oksanen E, Keinänen M, Kontunen-Soppela S. Differences in growth and gas exchange between southern and northern provenances of silver birch (Betula pendula Roth) in northern Europe. Tree Physiol, 2020, 40(2198-214

[67]

Tenkanen A, Suprun S, Oksanen E, Keinänen M, Keski-Saari S, Kontunen-Soppela S. Strategy by latitude? Higher photosynthetic capacity and root mass fraction in northern than southern silver birch (Betula pendula Roth) in uniform growing conditions. Tree Physiol, 2021, 41(6): 974-991

[68]

Tsimilli-Michael M, Strasser RJ (2008) In vivo assessment of stress impact on plant’s vitality: applications in detecting and evaluating the beneficial role of mycorrhization on host plants. In: Varma A (ed) Mycorrhiza. Springer Berlin Heidelberg, pp 679–703. https://doi.org/10.1007/978-3-540-78826-3_32

[69]

Tyystjärvi E, Koski A, Keränen M, Nevalainen O. The Kautsky curve is a built-in barcode. Biophys J, 1999, 77(2): 1159-1167

[70]

Vakkari P (2009) Silver birch (Betula pendula). https://cgspace.cgiar.org/handle/10568/104741

[71]

Viherä-Aarnio A, Velling P (2017) Growth, wood density and bark thickness of silver birch originating from the Baltic countries and Finland in two Finnish provenance trials. Silva Fennica 51(4): 7731. https://doi.org/10.14214/sf.7731

[72]

Virtanen O (2023) Light-acclimation and regulation of photosynthesis in autotrophic Chlamydomonas reinhardtii. https://www.utupub.fi/handle/10024/175564

[73]

Way DA, Montgomery RA. Photoperiod constraints on tree phenology, performance and migration in a warming world. Plant Cell Environ, 2015, 38(9): 1725-1736

[74]

Way DA, Pearcy RW. Sunflecks in trees and forests: from photosynthetic physiology to global change biology. Tree Physiol, 2012, 32(9): 1066-1081

Funding

University of Eastern Finland (including Kuopio University Hospital)

RIGHTS & PERMISSIONS

The Author(s)

PDF

24

Accesses

0

Citation

Detail

Sections
Recommended

/