Derivative-based time-adjusted analysis of diurnal and within-tree variation in the OJIP fluorescence transient of silver birch

. 2023 Sep ; 157 (2-3) : 133-146. [epub] 20230629

Jazyk angličtina Země Nizozemsko Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37382782

Grantová podpora
C-NEUT, project number 347862 Academy of Finland

Odkazy

PubMed 37382782
PubMed Central PMC10485093
DOI 10.1007/s11120-023-01033-x
PII: 10.1007/s11120-023-01033-x
Knihovny.cz E-zdroje

The JIP test, based on fast chlorophyll fluorescence (ChlF) kinetics and derived parameters, is a dependable tool for studying photosynthetic efficiency under varying environmental conditions. We extracted additional information from the whole OJIP and the normalized variable fluorescence (Vt) transient curve using first and second-order derivatives to visualize and localize points of landmark events. To account for light-induced variations in the fluorescence transient, we present a time-adjusted JIP test approach in which the derivatives of the transient curve are used to determine the exact timing of the J and I steps instead of fixed time points. We compared the traditional JIP test method with the time-adjusted method in analyzing fast ChlF measurements of silver birch (Betula pendula) in field conditions studying diurnal and within-crown variation. The time-adjusted JIP test method showed potential for studying ChlF dynamics, as it takes into account potential time shifts in the occurrence of J and I steps. The exact occurrence times of J and I steps and other landmark events coincided with the times of significant differences in fluorescence intensity. Chlorophyll fluorescence parameters were linearly related to photosynthetic photon flux density (PPFD) at different times of day, and the values obtained by the time-adjusted JIP test showed a stronger linear regression than the traditional JIP test. For fluorescence parameters having significant differences among different times of day and crown layers, the time-adjusted JIP test resulted in more clear differences than the traditional JIP test. Diurnal ChlF intensity data indicated that differences between the southern and northern provenance were only evident under low light conditions. Taken together, our results emphasize the potential relevance of considering the time domain in the analysis of the fast ChlF induction.

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Adams WW, Demmig-Adams B (2004) Chlorophyll fluorescence as a tool to monitor plant response to the environment. In: Papageorgiou GC, Govindjee G (Eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 583–604. 10.1007/978-1-4020-3218-9_22

Baker NR, Rosenqvist E. Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot. 2004;55:1607–1621. doi: 10.1093/jxb/erh196. PubMed DOI

Bantis F, FRUCHTENICHT E, GRAAP J, Ströll S, Reininger N, SCHAFER L, Pollastrini M, Holland V, Bussotti F, Radoglou K, Brüggemann W (2020) Special issue in honour of Prof. Reto J. Strasser - The JIP-test as a tool for forestry in times of climate change. Photosynthetica 58

Bednaříková M, Folgar-Cameán Y, Kučerová Z, Lazár D, Špundová M, Hájek J, Barták M. Special issue in honour of Prof. Reto J. Strasser—analysis of K- and L-band appearance in OJIPs in Antarctic lichens in low and high temperature. Photosynthetica. 2020;58:646–656. doi: 10.32615/ps.2019.180. DOI

Boardman NK. Comparative photosynthesis of sun and shade plants. Annu Rev Plant Physiol. 1977;28:355–377. doi: 10.1146/annurev.pp.28.060177.002035. DOI

Boisvert S, Joly D, Carpentier R. Quantitative analysis of the experimental O–J–I–P chlorophyll fluorescence induction kinetics. FEBS J. 2006;273:4770–4777. doi: 10.1111/j.1742-4658.2006.05475.x. PubMed DOI

Bussotti F, Desotgiu R, Pollastrini M, Cascio C. The JIP test: a tool to screen the capacity of plant adaptation to climate change. Scand J for Res. 2010;25:43–50. doi: 10.1080/02827581.2010.485777. DOI

Bussotti F, Desotgiu R, Cascio C, Pollastrini M, Gravano E, Gerosa G, Marzuoli R, Nali C, Lorenzini G, Salvatori E, Manes F, Schaub M, Strasser RJ (2011) Ozone stress in woody plants assessed with chlorophyll a fluorescence. A critical reassessment of existing data. Environ Exp Bot 73:19–30

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

Cascio C, Schaub M, Novak K, Desotgiu R, Bussotti F, Strasser RJ. Foliar responses to ozone of Fagus sylvatica L. seedlings grown in shaded and in full sunlight conditions. Environ Exp Bot. 2010;68:188–197. doi: 10.1016/j.envexpbot.2009.10.003. DOI

Chen S, Strasser RJ, Qiang S. In vivo assessment of effect of phytotoxin tenuazonic acid on PSII reaction centers. Plant Physiol Biochem. 2014;84:10–21. doi: 10.1016/j.plaphy.2014.09.004. PubMed DOI

Demmig B, Björkman O. Comparison of the effect of excessive light on chlorophyll fluorescence (77 K) and photon yield of O 2 evolution in leaves of higher plants. Planta. 1987;171:171–184. doi: 10.1007/BF00391092. PubMed DOI

Deepak M, Keski-Saari S, Fauch L, Granlund L, Oksanen E, Keinänen M (2019) Leaf canopy layers affect spectral reflectance in silver birch. Remote Sens 11:2884

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

Desotgiu R, Cascio C, Pollastrini M, Gerosa G, Marzuoli R, Bussotti F. Short and long term photosynthetic adjustments in sun and shade leaves of Fagus sylvatica L., investigated by fluorescence transient (FT) analysis. Plant Biosyst. 2012;146:206–216. doi: 10.1080/11263504.2012.705350. DOI

Digrado A, de la Motte LG, Bachy A, Mozaffar A, Schoon N, Bussotti F, Amelynck C, Dalcq A-C, Fauconnier M-L, Aubinet M, Heinesch B, du Jardin P, Delaplace P. Decrease in the photosynthetic performance of temperate grassland species does not lead to a decline in the gross primary production of the ecosystem. Front Plant Sci. 2018 doi: 10.3389/fpls.2018.00067. PubMed DOI PMC

Evans JR. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia. 1989;78:9–19. doi: 10.1007/BF00377192. PubMed DOI

Force L, Critchley C, van Rensen JJS. New fluorescence parameters for monitoring photosynthesis in plants. Photosynth Res. 2003;78:17. doi: 10.1023/A:1026012116709. PubMed DOI

Guo Y, Lu Y, Goltsev V, Strasser RJ, Kalaji HM, Wang H, Wang X, Chen S, Qiang S. Comparative effect of tenuazonic acid, diuron, bentazone, dibromothymoquinone and methyl viologen on the kinetics of Chl a fluorescence rise OJIP and the MR820 signal. Plant Physiol Biochem. 2020;156:39–48. doi: 10.1016/j.plaphy.2020.08.044. PubMed DOI

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;124:1013–1022. doi: 10.1111/oik.01986. DOI

Johkan M, Shoji K, Goto F, Hahida S, Yoshihara T. Effect of green light wavelength and intensity on photomorphogenesis and photosynthesis in Lactuca sativa. Environ Exp Bot. 2012;75:128–133. doi: 10.1016/j.envexpbot.2011.08.010. DOI

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. doi: 10.1016/j.envexpbot.2010.10.009. DOI

Kalaji HM, Oukarroum A, Alexandrov V, Kouzmanova M, Brestic M, Zivcak M, Samborska IA, Cetner MD, Allakhverdiev SI, Goltsev V. Identification of nutrient deficiency in maize and tomato plants by in vivo chlorophyll a fluorescence measurements. Plant Physiol Biochem. 2014;81:16–25. doi: 10.1016/j.plaphy.2014.03.029. PubMed DOI

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;122:121–158. doi: 10.1007/s11120-014-0024-6. PubMed DOI PMC

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. Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynth Res. 2017;132:13–66. doi: 10.1007/s11120-016-0318-y. PubMed DOI PMC

Kalaji HM, Bąba W, Gediga K, Goltsev V, Samborska IA, Cetner MD, Dimitrova S, Piszcz U, Bielecki K, Karmowska K, Dankov K, Kompała-Bąba A. Chlorophyll fluorescence as a tool for nutrient status identification in rapeseed plants. Photosynth Res. 2018;136:329–343. doi: 10.1007/s11120-017-0467-7. PubMed DOI PMC

Khan N, Jemaa E, Hamdani S, Qu M, Lv M, Perveen S, Stirbet A, Govindjee G, Cn Z (2020) Natural variation in the fast phase of chlorophyll a fluorescence induction curve (OJIP) in a global rice minicore panel. Photosynth Res 150:137–158 PubMed

Kohonen T. Self-organizing maps. Berlin: Springer; 2012.

Koutra E, Chondrogiannis C, Grammatikopoulos G. Variability of the photosynthetic machinery tolerance when imposed to rapidly or slowly imposed dehydration in native Mediterranean plants. Photosynthetica. 2022;60:88–101. doi: 10.32615/ps.2022.003. DOI

Lichtenthaler H, Buschmann C, Doell M, Fietz HJ, Bach T, Kozel U, Meier D, Rahmsdorf U. Photosynthetic activity, chloroplast ultrastructure, and leaf characteristics of high-light and low-light plants and of sun and shade leaves. Photosynth Res. 1981;2:115–141. doi: 10.1007/BF00028752. PubMed DOI

Lichtenthaler HK, Ač A, Marek MV, Kalina J, Urban O. Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree species. Plant Physiol Biochem. 2007;45:577–588. doi: 10.1016/j.plaphy.2007.04.006. PubMed DOI

Maillette L. Structural dynamics of silver birch. I. The fates of buds. J Appl Ecol. 1982;19:203–218. doi: 10.2307/2403005. DOI

Mathur S, Jain L, Jajoo A. Photosynthetic efficiency in sun and shade plants. Photosynthetica. 2018;56:354–365. doi: 10.1007/s11099-018-0767-y. DOI

Mattila H, Sotoudehnia P, Kuuslampi T, Stracke R, Mishra KB, Tyystjärvi E. Singlet oxygen, flavonols and photoinhibition in green and senescing silver birch leaves. Trees. 2021 doi: 10.1007/s00468-021-02114-x(8July2021,datelastaccessed). DOI

Maxwell K, Johnson G (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51(345): 659–668 PubMed

Noguchi K, Gel YR, Brunner E, Konietschke F. nparLD: an R software package for the nonparametric analysis of longitudinal data in factorial experiments. J Stat Softw. 2012;50:1–23. doi: 10.18637/jss.v050.i12. PubMed DOI

Pellegrini E, Campanella A, Paolocci M, Trivellini A, Gennai C, Muganu M, Nali C, Lorenzini G. Functional leaf traits and diurnal dynamics of photosynthetic parameters predict the behavior of grapevine varieties towards ozone. PLoS ONE. 2015;10:e0135056. doi: 10.1371/journal.pone.0135056. PubMed DOI PMC

Pollastrini M, Holland V, Brüggemann W, Bruelheide H, Dănilă I, Jaroszewicz B, Valladares F, Bussotti F. Taxonomic and ecological relevance of the chlorophyll a fluorescence signature of tree species in mixed European forests. New Phytol. 2016;212:51–65. doi: 10.1111/nph.14026. PubMed DOI

Pollastrini M, Nogales AG, Benavides R, Bonal D, Finer L, Fotelli M, Gessler A, Grossiord C, Radoglou K, Strasser RJ, Bussotti F. Tree diversity affects chlorophyll a fluorescence and other leaf traits of tree species in a boreal forest. Tree Physiol. 2017;37:199–208. PubMed

Pons T, Pearcy RW (1994) Nitrogen reallocation and photosynthetic acclimation in response to partial shading in soybean plants. 10.1111/j.1399-3054.1994.tb03034.x

Qiang H, Richmond A. Productivity and photosynthetic efficiency ofSpirulina platensis as affected by light intensity, algal density and rate of mixing in a flat plate photobioreactor. J Appl Phycol. 1996;8:139–145. doi: 10.1007/BF02186317. DOI

Rijkers T, Pons TL, Bongers F. The effect of tree height and light availability on photosynthetic leaf traits of four neotropical species differing in shade tolerance. Funct Ecol. 2000;14:77–86. doi: 10.1046/j.1365-2435.2000.00395.x. DOI

Rohart F, Gautier B, Singh A, Lê Cao K-A. mixOmics: An R package for ’omics feature selection and multiple data integration. PLoS Comput Biol. 2017;13:e1005752. doi: 10.1371/journal.pcbi.1005752. PubMed DOI PMC

Sperdouli I, Moustakas M (2012) Spatio-temporal heterogeneity in Arabidopsis thaliana leaves under drought stress. Plant Biol 14:118–128 PubMed

Srivastava A, Strasser RJ. Stress and stress management of land plants during a regular day. J Plant Physiol. 1996;148:445–455. doi: 10.1016/S0176-1617(96)80278-1. DOI

Stirbet A, Govindjee N. Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise. Photosynth Res. 2012;113:15–61. doi: 10.1007/s11120-012-9754-5. PubMed DOI

Stirbet A, Govindjee, On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B. 2011;104:236–257. doi: 10.1016/j.jphotobiol.2010.12.010. PubMed DOI

Stirbet A, Lazár D, Kromdijk J, Govindjee, Chlorophyll a fluorescence induction: can just a one-second measurement be used to quantify abiotic stress responses? Photosynthetica. 2018;56:86–104. doi: 10.1007/s11099-018-0770-3. DOI

Strasser R, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. Probing Photosynth Mech Regul Adapt

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

Strasser R, Tsimilli-Michael M, Dangre D, Rai M (2007) Biophysical phenomics reveals functional building blocks of plants systems biology: a case study for the evaluation of the impact of mycorrhization with Piriformospora indica. In: Advanced techniques in soil microbiology, pp 319–341

Swoczyna T, Kalaji H, Bussotti F, Mojski J, Pollastrini M. Environmental stress -what can we learn from chlorophyll a fluorescence analysis in woody plants? A review. Front Plant Sci. 2022;13:1–19. doi: 10.3389/fpls.2022.1048582. PubMed DOI PMC

Tenkanen A, Keski-Saari S, Salojärvi J, Oksanen E, Keinänen M, Kontunen-Soppela S (2020) Differences in growth and gas exchange between southern and northern provenances of silver birch (Betula pendula Roth) in northern Europe Thomas S (ed). Tree Physiol 40:198–214 PubMed

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

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;43:16–30. doi: 10.1093/treephys/tpac104. PubMed DOI PMC

Tomek P, Lazár D, Ilík P, Naus J. Research note: On the intermediate steps between the O and P steps in chlorophyll a fluorescence rise measured at different intensities of exciting light. Funct Plant Biol. 2001;28:1151–1160. doi: 10.1071/PP01065. DOI

Tsimilli-Michael M. Revisiting JIP-test: An educative review on concepts, assumptions, approximations, definitions and terminology. Photosynthetica. 2019;57:90–107.

Tsimilli-Michael M, Pêcheux M, Strasser RJ. Light and heat stress adaptation of the symbionts of temperate and coral reef foraminifers probed in hospite by the chlorophyll a fluorescence kinetics. Z Für Naturforschung C. 1999;54:671. doi: 10.1515/znc-1999-9-1009. DOI

Tsimilli-Michael M, Strasser R (2001) Fingerprints of climate changes on the photosynthetic apparatus’ behaviour, monitored by the JIP-test, pp 229–247

Tyystjärvi E, Koski A, Keränen M, Nevalainen O. The Kautsky curve is a built-in barcode. Biophys J. 1999;77:1159–1167. doi: 10.1016/S0006-3495(99)76967-5. PubMed DOI PMC

Urban O, Kosvancová M, Marek M, Lichtenthaler H. Induction of photosynthesis and importance of limitations during the induction phase in sun and shade leaves of five ecologically contrasting tree species from the temperate zone. Tree Physiol. 2007;27:1207–1215. doi: 10.1093/treephys/27.8.1207. PubMed DOI

Way D, Pearcy R (2012) Sunflecks in trees and forests: from photosynthetic physiology to global change biology. Tree Physiol 32:1066–1081 PubMed

Xia Q, Tan J, Cheng S, Jiang Y, Guo Y. Sensing plant physiology and environmental stress by automatically tracking Fj and Fi features in PSII chlorophyll fluorescence induction. Photochem Photobiol. 2019;95:1495–1503. doi: 10.1111/php.13141. PubMed DOI

Zivcak M, Brestic M, Kunderlikova K, Olsovska K, Allakhverdiev SI. Effect of photosystem I inactivation on chlorophyll a fluorescence induction in wheat leaves: Does activity of photosystem I play any role in OJIP rise? J Photochem Photobiol B. 2015;152:318–324. doi: 10.1016/j.jphotobiol.2015.08.024. PubMed DOI

Zivcak M, Olsaovska K, Slamka P, Galambosova J, Rataj V, Shao H-B, Kalaji HM, Brestic M, Zivcak M (reprint author) (2014) Measurements of chlorophyll fluorescence in different leaf positions may detect nitrogen deficiency in wheat. YIC-IR 101. http://ir.yic.ac.cn/handle/133337/8566. Accessed 11 Oct, 2022

Zushi K, Matsuzoe N. Using of chlorophyll a fluorescence OJIP transients for sensing salt stress in the leaves and fruits of tomato. Sci Hortic. 2017;219:216–221. doi: 10.1016/j.scienta.2017.03.016. DOI

Zushi K, Kajiwara S, Matsuzoe N. Chlorophyll a fluorescence OJIP transient as a tool to characterize and evaluate response to heat and chilling stress in tomato leaf and fruit. Sci Hortic. 2012;148:39–46. doi: 10.1016/j.scienta.2012.09.022. DOI

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