Photosynthetica, 2020 (vol. 58), SPECIAL ISSUE

Photosynthetica 2020, 58(2):657-670 | DOI: 10.32615/ps.2020.012

Special issue in honour of Prof. Reto J. Strasser – Photosynthetic efficiency of two Platanus orientalis L. ecotypes exposed to moderately high temperature - JIP-test analysis

S. DIMITROVA1, M. PAUNOV1, B. PAVLOVA1, K. DANKOV1, M. KOUZMANOVA1, V. VELIKOVA2, T. TSONEV2, H.M. KALAJI3, V. GOLTSEV1
1 Department of Biophysics and Radiobiology, Faculty of Biology, Sofia University 'St. Kliment Ohridski', 8 Dragan Tsankov Blvd., 1164 Sofia, Bulgaria
2 Institute of Plant Physiology and Genetics, Bulgarian Academy of Sciences, Acad. G. Bontchev Str. 21, 1113 Sofia, Bulgaria
3 Department of Plant Physiology, Institute of Biology, Faculty of Agriculture and Biology, Warsaw University of Life Sciences - SGGW, Warsaw, Poland

Plane (Platanus orientalis) is a popular park tree in Europe but is almost extinct in natural ecosystems, because of climate changes. In our study, two ecotypes of plane tree (Bulgarian and Italian) were submitted to moderately elevated temperature that occurs in summer. Our aim was to compare stress reactions, tolerance, and adaptability of these plants. Leaf age had a significant impact on the stress effects. For correct interpretation of the results, we investigated leaves at different positions from the apical bud, i.e., leaves of different age. We assessed their photosynthetic efficiency at room temperature and after treatment at moderately high temperature by simultaneous measurement of prompt and delayed chlorophyll fluorescence, as well as light reflection at 820 nm. For more precise interpretation of the obtained results we did principal component analysis. The two studied plane ecotypes showed different tolerance to the elevated temperature. Plants of Italian ecotype showed better adaptivity and developed advantageous photosynthetic characteristics, while Bulgarian ecotype was more affected. Plants of both ecotypes recovered from the heat stress.

Keywords: difference curves; electron transport chain; JIP-test; photosynthesis; photosystem I; photosystem II.

Received: October 4, 2019; Revised: January 9, 2020; Accepted: January 22, 2020; Prepublished online: April 4, 2020; Published: April 7, 2020Show citation

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DIMITROVA, S., PAUNOV, M., PAVLOVA, B., DANKOV, K., KOUZMANOVA, M., VELIKOVA, V., ... GOLTSEV, V. (2020). Special issue in honour of Prof. Reto J. Strasser – Photosynthetic efficiency of two Platanus orientalis L. ecotypes exposed to moderately high temperature - JIP-test analysis. Photosynthetica, 58(SPECIAL ISSUE), 657-670. doi: 10.32615/ps.2020.012.
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    References

    1. Allakhverdiev S.I., Kreslavski V.D., Klimov V.V. et al.: Heat stress: An overview of molecular responses in photosyn-thesis. - Photosynth. Res. 98: 541-550, 2008. Go to original source...
    2. Benz J.P., Lintala M., Soll J. et al.: A new concept for ferredoxin-NADP(H) oxidoreductase binding to plant thylakoids. - Trends Plant Sci. 15: 608-613, 2010. Go to original source...
    3. Black R., Bennett S.R.G., Thomas S.M. et al.: Migration as adaptation. - Nature 478: 447-449, 2011. Go to original source...
    4. Blankenship R.E.: - Molecular Mechanisms of Photosynthesis. 2nd Edition. Pp. 312. John Wiley & Sons, Chichester 2014.
    5. Bolhàr-Nordenkampf H., Long S., Baker N. et al.: Chlorophyll fluorescence as a probe of the photosynthetic competence of leaves in the field: a review of current instrumentation. - Funct. Ecol. 3: 497-514, 1989. Go to original source...
    6. Bucharova A., Durka W., Hermann J.-M. et al.: Plants adapted to warmer climate do not outperform regional plants during a natural heat wave. - Ecol. Evol. 6: 4160-4165, 2016. Go to original source...
    7. Bukhov N., Wiese C., Neimanis S. et al.: Heat sensitivity of chloroplasts and leaves: leakage of protons from thylakoids and reversible activation of cyclic electron transport. - Photosynth. Res. 59: 81-93, 1999. Go to original source...
    8. Cao J., Govindjee: Chlorophyll a fluorescence transient as an indicator of active and inactive Photosystem II in thylakoid membranes. - BBA-Bioenergetics 1015: 180-188, 1990. Go to original source...
    9. Ceppi M.G., Oukarroum A., Çiçek N. et al.: 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. Plantarum 144: 277-288, 2012. Go to original source...
    10. Chernev P., Goltsev V., Strasser R.: Mathematical modelling of stress effects in plants monitored by luminescent methods. - Bulg. J. Plant Physiol. XXIX: 387-387, 2003.
    11. Dąbrowski P., Baczewska A., Pawluśkiewicz B. et al.: Prompt chlorophyll a fluorescence as a rapid tool for diagnostic changes in PSII structure inhibited by salt stress in Perennial ryegrass. - J. Photoch. Photobio. B 157: 22-31, 2016. Go to original source...
    12. Ducruet J.M.: Relation between the heat-induced increase of F0 fluorescence and a shift in the electronic equilibrium at the acceptor side of photosystem 2. - Photosynthetica 37: 335-338, 1999. Go to original source...
    13. Goltsev V., Chernev P., Zaharieva I. et al.: Kinetics of delayed chlorophyll a fluorescence registered in milliseconds time range. - Photosynth. Res. 84: 209-215, 2005. Go to original source...
    14. Goltsev V., Venediktov P.S., Janumov D.A.: Temperature dependence of the delayed fluorescence from wheat leaves treated with DCMU. - BBA-Bioenergetics 593: 133-135, 1980. Go to original source...
    15. Goltsev V., Yordanov I., Gurmanova M. et al.: [Temperature-induced transitions in photosynthetic apparatus of bean plants probed by JIP-test.] - Agr. Sci. 2: 7-14, 2010. [In Bulgarian] Go to original source...
    16. Goltsev V., Zaharieva I.: Temperature effects on characteristics of dark relaxation of delayed fluorescence in Zea mays leaves. -Bulg. J. Plant Physiol. XXIX: 391-392, 2003.
    17. Goltsev V., Zaharieva I., Chernev P. et al.: Origin of kinetic components of millisecond delayed chlorophyll fluorescence. XIII International Congress on Photosynthesis. Pp. 211-213. The International Society of Photosynthesis Research, 2004.
    18. Goltsev V., Zaharieva I., Chernev P., Strasser R.: Delayed chlorophyll fluorescence as a monitor for physiological state of photosynthetic apparatus. - Biotechnol. Biotec. Eq. 23: 452-457, 2009a. Go to original source...
    19. Goltsev V., Zaharieva I., Chernev P., Strasser R.J.: Delayed fluorescence in photosynthesis. - Photosynth. Res. 101: 217-232, 2009b. Go to original source...
    20. Guissé B., Srivastava A., Strasser R.J.: The polyphasic rise of the chlorophyll a fluorescence (O-K-J-I-P) in heat-stressed leaves. - Arch. Sci. Geneve 48: 147-160, 1995.
    21. Harbinson J., Woodward F.: The use of light-induced absorbance changes at 820 nm to monitor the oxidation state of P-700 in leaves. - Plant Cell Environ. 10: 131-140, 1987.
    22. Havaux M.: Characterization of thermal damage to the photo-synthetic electron transport system in potato leaves. - Plant Sci. 94: 19-33, 1993. Go to original source...
    23. Havaux M.: Probing electron transport through and around photosystem II in vivo by the combined use of photoacoustic spectroscopy and chlorophyll fluorometry. - Israel J. Chem. 38: 247-256, 1998. Go to original source...
    24. Havaux M., Greppin H., Strasser R.J.: Functioning of photo-systems I and II in pea leaves exposed to heat stress in the presence or absence of light: Analysis using in vivo fluorescence, absorbance and photoacoustic measurements. - Planta 186: 88-98, 1991. Go to original source...
    25. Haveman J., Lavorel J.: Identification of the 120 µs phase in the decay of delayed fluoerscence in spinach chloroplasts and subchloroplast particles as the intrinsic back reaction. The dependence of the level of this phase on the thylakoids internal pH. - BBA-Bioenergetics 408: 269-283, 1975. Go to original source...
    26. Hewitt N., Klenk N., Smith A.L. et al.: Taking stock of the assisted migration debate. - Biol. Conserv. 144: 2560-2572, 2011. Go to original source...
    27. Huang S., Lv L., Zhu J. et al.: Extending growing period is limited to offsetting negative effects of climate changes on maize yield in the North China Plain. - Field Crop. Res. 215: 66-73, 2018. Go to original source...
    28. Jursinic P.: Delayed fluorescence: current concepts and status. - In: Govindjee, Amesz J., Fork D.J. (ed.): Light Emission by Plants and Bacteria. Pp. 291-328. Academic Press, Orlando 1986. Go to original source...
    29. Kalaji H.M., Bąba W., Gediga K. et al.: Chlorophyll fluorescence as a tool for nutrient status identification in rapeseed plants. - Photosynth. Res. 136: 329-343, 2018. Go to original source...
    30. Kalaji H.M., Goltsev V., Brestič M. et al.: In vivo measurements of light emission in plants. - In: Allakhverdiev S., Rubin A., Shuvalov V. (ed.): Photosynthesis: Open Questions and What We Know Today. Pp. 1-40. Institute of Computer Science, Izhevsk-Moscow 2014c.
    31. Kalaji H.M., Goltsev V.N., Żuk-Gołaszewska K. et al.: Chloro-phyll Fluorescence: Understanding Crop Performance - Basics and Applications. Pp. 222. CRC Press, Boca Raton-London-New York 2017. Go to original source...
    32. Kalaji H.M., Jajoo A., Oukarroum A. et al.: The use of chlorophyll fluorescence kinetics analysis to study the performance of photosynthetic machinery in plants. - In: Ahmad P., Rasool S. (ed.): Emerging Technologies and Management of Crop Stress Tolerance. Pp. 347-384. Academic Press, San Diego 2014a. Go to original source...
    33. Kalaji H.M., Jajoo A., Oukarroum A. et al.: Chlorophyll a fluores-cence as a tool to monitor physiological status of plants under abiotic stress conditions. - Acta Physiol. Plant. 38: 102, 2016. Go to original source...
    34. Kalaji H.M., Schansker G., Ladle R.J. et al.: Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. - Photosynth. Res. 122: 121-158, 2014b. Go to original source...
    35. Kautsky H., Hirsch A.: Neue Versuche zur Kohlensäureassimila-tion. - Naturwissenschaften 19: 964-964, 1931. Go to original source...
    36. Kouřil R., Lazár D., Ilík P. et al.: High-temperature induced chlorophyll fluorescence rise in plants at 40-50°C: experi-mental and theoretical approach. - Photosynth. Res. 81: 49-66, 2004. Go to original source...
    37. Lavorel J.: Luminescence. - In: Govindjee (ed.): Bioenergetics of Photosynthesis. Pp. 223-317. Academic Press, London 1975. Go to original source...
    38. Lawlor D.W., Paul M.J.: Source/sink interactions underpin crop yield: the case for trehalose 6-phosphate/SnRK1 in improvement of wheat. - Front. Plant Sci. 5: 418, 2014. Go to original source...
    39. Lazár D.: Chlorophyll a fluorescence induction. - BBA-Bioenergetics 1412: 1-28, 1999. Go to original source...
    40. Lazár D., Nauš J., Matoušková M., Flašarová M.: Mathematical modeling of changes in chlorophyll fluorescence induction caused by herbicides. - Pestic. Biochem. Phys. 57: 200-210, 1997. Go to original source...
    41. Li L., Aro E.-M., Millar A.H.: Mechanisms of photodamage and protein turnover in photoinhibition. - Trends Plant Sci. 23: 667-676, 2018. Go to original source...
    42. Lichtenthaler H.K., Babani F.: Light adaptation and senescence of the photosynthetic apparatus. Changes in pigment composi-tion, chlorophyll fluorescence parameters and photosynthetic activity. - In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Pp. 713-736. Springer, Dordrecht 2004. Go to original source...
    43. Marković D.Z., Kalauzi A., Radenović C.N.: Delayed fluores-cence induction transients: Mathematical modelling based on the chosen kinetic models. - Gen. Physiol. Biophys. 20: 303-313, 2001.
    44. Mathur S., Allakhverdiev S.I., Jajoo A.: Analysis of high temperature stress on the dynamics of antenna size and reducing side heterogeneity of Photosystem II in wheat leaves (Triticum aestivum). - BBA-Bioenergetics 1807: 22-29, 2011.
    45. Oja V., Eichelmann H., Peterson R.B. et al.: Deciphering the 820 nm signal: redox state of donor side and quantum yield of Photosystem I in leaves. - Photosynth. Res. 78: 1, 2003. Go to original source...
    46. Oukarroum A., Goltsev V., Strasser R.J.: Temperature effects on pea plants probed by simultaneous measurements of the kinetics of prompt fluorescence, delayed fluorescence and modulated 820 nm reflection. - PLoS ONE 8: e59433, 2013. Go to original source...
    47. Pospíšil P., Tyystjärvi E.: Molecular mechanism of high-temperature-induced inhibition of acceptor side of Photo-system II. - Photosynth. Res. 62: 55-66, 1999. Go to original source...
    48. Samborska I.A., Kalaji H.M., Sieczko L. et al.: Structural and functional disorder in the photosynthetic apparatus of radish plants under magnesium deficiency. - Funct. Plant Biol. 45: 668-679, 2018. Go to original source...
    49. Samborska I.A., Kalaji H.M., Sieczko L. et al.: Can just one-second measurement of chlorophyll a fluorescence be used to predict sulphur deficiency in radish (Raphanus sativus L. sativus) plants? - Curr. Plant Biol. 19: 100096, 2019. Go to original source...
    50. Sane P.V., Desai T.S., Tatake V.G., Govindjee: Heat induced reversible increase in photosystem I emission in algae, leaves and chloroplasts: Spectra, activities, and relation to state changes. - Photosynthetica 18: 439-444, 1984.
    51. Scheibe R., Backhausen J.E., Emmerlich V. et al.: Strategies to maintain redox homeostasis during photosynthesis under changing conditions. - J. Exp. Bot. 56: 1481-1489, 2005. Go to original source...
    52. Schreiber U., Bilger W., Neubauer C.: Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. - In: Schulze E.-D., Caldwell M. (ed.): Ecophysiology of Photosynthesis. Springer Study Edition. Pp. 49-70. Springer, Berlin-Heidelberg 1995. Go to original source...
    53. Schreiber U., Neubauer C.: O2-dependent electron flow, mem-brane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. - Photosynth. Res. 25: 279-293, 1990. Go to original source...
    54. Shuvalov V.A., Litvin F.F.: Mechanism of delayed light emission of plans leaves and enersy storage in photosynthetic centers. -Mol. Biol.-Moscow+ 3: 45-56, 1969.
    55. Srivastava A., Guissé B., Greppin H., Strasser R.J.: Regulation of antenna structure and electron transport in Photosystem II of Pisum sativum under elevated temperature probed by the fast polyphasic chlorophyll a fluorescence transient: OKJIP. - BBA-Bioenergetics 1320: 95-106, 1997. Go to original source...
    56. Srivastava A., Strasser R.J.: Stress and stress management of land plants during a regular day. - J. Plant Physiol. 148: 445-455, 1996. Go to original source...
    57. Srivastava A., Strasser R.J., Govindjee: Polyphasic rise of chloro- phyll a fluorescence in herbicide-resistant D1 mutants of Chlamydomonas reinardtii. - Photosynth. Res. 43: 131-141, 1995. Go to original source...
    58. Stirbet A.: Excitonic connectivity between photosystem II units: What is it, and how to measure it? - Photosynth. Res. 116: 189-214, 2013. Go to original source...
    59. 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. Photoch. Photobio. B 104: 236-257, 2011. Go to original source...
    60. Stirbet A., Govindjee: Chlorophyll a fluorescence induction: A personal perspective of the thermal phase, the J-I-P rise. - Photosynth. Res. 113: 15-61, 2012. Go to original source...
    61. Strasser B.J., Strasser R.J.: Measuring fast fluorescence transients to address environmental questions: The JIP test. - In: Mathis P. (ed.): Photosynthesis: From Light to Biosphere. Vol. 5. Pp. 977-980. Kluwer Academic Publishers, Dordrecht 1995. Go to original source...
    62. Strasser R.J., Eggenberg P., Strasser B.J.: How to work without stress but with fluorescence. - Bull. Royal Soc. Liege 65: 330-349, 1996.
    63. Strasser R.J., Govindjee: On the O-J-I-P fluorescence transient in leaves and D1 mutants of Chlamidomonas reinhardtii. - In: Murata N. (ed.): Research in Photosynthesis. Pp. 29-32. Kluwer Academic Publishers, Dordrecht 1992.
    64. Strasser R.J., Srivastava A., Tsimilli-Michael M.: Screening the vitality and photosynthetic activity of plants by the fluo-rescence transient. - In: Behl R.K., Punia M.S., Lather B.P.S. (ed.): Crop Improvement for Food Security. Pp. 72-115. SSARM, Hisar 1999.
    65. Strasser R.J., Stirbet A.D.: Estimation of the energetic connectivity of PS II centres in plants using the fluorescence rise O-J-I-P: Fitting of experimental data to three different PS II models. - Math. Comput. Simulat. 56: 451-462, 2001.
    66. Strasser R.J., Tsimilli-Michael M.: Activity and heterogeneity of PSII probed in vitro by the chlorophyll a fluorescence rise O-(K)-JIP. - In: Garab G. (ed): Photosynthesis: Mechanisms and Effects. Pp. 2321-2324. Springer, Dordrecht 1998.
    67. Strasser R.J., Tsimilli-Michael M.: Stress in plants, from daily rhythm to global changes, detected and quantified by the JIP-test. - Chimie Nouvelle (SRC) 75: 3321-3326, 2001.
    68. Strasser R.J., 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. - BBA-Bioenergetics 1797: 1313-1326, 2010. Go to original source...
    69. Strasser R.J., Tsimilli-Michael M., Srivastava A.: Analysis of the chlorophyll a fluorescence transient. - In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 321-362. Springer, Dordrecht 2004. Go to original source...
    70. Tsimilli-Michael M., Strasser R.J.: The energy flux theory 35 years later: formulations and applications. - Photosynth. Res. 117: 289-320, 2013. Go to original source...
    71. Velikova V., Tsonev T., Tattini M. et al.: Physiological and structural adjustments of two ecotypes of Platanus orientalis L. from different habitats in response to drought and re-watering. - Conserv. Physiol. 6: coy073, 2018.
    72. Velitchkova M., Ivanov A.G., Christov A.M.: Ultrastructural and fluorescence properties of granal and stromal membranes of pea chloroplasts exposed to heat stress. - Photosynthetica 23: 360-363, 1989.
    73. White A.C., Rogers A., Rees M., Osborne C.P.: How can we make plants grow faster? A source-sink perspective on growth rate. - J. Exp. Bot. 67: 31-45, 2016. Go to original source...
    74. Woolhouse H.W.: Leaf senescence. - In: Smith H., Grierson D. (ed.): The Biology of Plant Development. Pp. 256-284. Blackwell Scientific Publications, Oxford 1987.
    75. Yamane Y., Kashino Y., Koike H., Satoh K.: 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, 1997. Go to original source...
    76. Yamane Y., Kashino Y., Koike H., Satoh K.: Effects of high temperatures on the photosynthetic systems in spinach: Oxygen-evolving activities, fluorescence characteristics and the denaturation process. - Photosynth. Res. 57: 51-59, 1998. Go to original source...
    77. Yordanov I., Goltsev V., Chernev P. et al.: Modulated sink-source interactions preserve the PSII electron transport from senescence-induced inactivation in model system with expanded life span induced by decapitation of bean plants. -In: Allen J.F., Gantt E., Golbeck J.H., Osmond B. (ed.): Photosynthesis: Energy from the Sun. Pp. 675-679. Springer, Dordrecht 2007. Go to original source...
    78. Zaharieva I., Dau H.: Energetics and kinetics of S-state transitions monitored by delayed chlorophyll fluorescence. - Front. Plant Sci. 10: 386, 2019. Go to original source...
    79. Zaharieva I., Goltsev V.: Advances on Photosystem II investiga-tion by measurement of delayed chlorophyll fluorescence by a phosphoroscopic method. - Photochem. Photobiol. 77: 292-298, 2003. Go to original source...
    80. Zaharieva I., Goltsev V., Chernev P., Strasser R.J.: Temperature effects on parameters of millisecond delayed chlorophyll fluorescence - A mathematical model. - In: Berden Zrimec M., Zrimec A., Drobne D., Milani M. (ed.): Weak Photon Emission from Living Tissues: Delayed Luminescence - Facts & Perspectives. Pp. 24-28. Institute of Physical Biology, Grosuplje 2004.
    81. Zhang R., Sharkey T.D.: Photosynthetic electron transport and proton flux under moderate heat stress. - Photosynth. Res. 100: 29-43, 2009. Go to original source...
    82. Zhou L., Cheng S., Yu H.: Detection of chlorophyll content of rice leaves by chlorophyll fluorescence spectrum based on PCA-ANN. Proceedings of the 2016 7th International Conference on Mechatronics, Control and Materials (ICMCM 2016). Pp. 52-56. Atlantis Press, Paris 2016. Go to original source...
    83. Živčák M., Brestič M., Kalaji H.M., Govindjee: Photosynthetic responses of sun- and shade-grown barley leaves to high light: Is the lower PSII connectivity in shade leaves associated with protection against excess of light? - Photosynth. Res. 119: 339-354, 2014. Go to original source...
    84. Živčák M., Brestič M., Olšovská K., Slamka P.: Performance index as a sensitive indicator of water stress in Triticum aestivum L. - Plant Soil Environ. 54: 133-139, 2008.

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