Photosynthetica 2019, 57(2):668-679 | DOI: 10.32615/ps.2019.069

Discovering trends in photosynthesis using modern analytical tools:More than 100 reasons to use chlorophyll fluorescence

W. BĄBA1, A. KOMPAŁA-BĄBA2, M. ZABOCHNICKA-ŚWIĄTEK3, J. LUŹNIAK1, R. HANCZARUK2, A. ADAMSKI5, H.M. KALAJI5,6
1 Department of Plant Ecology, Institute of Botany, Jagiellonian University, Gronostajowa 3, 30-387 Kraków, Poland
2 Department of Botany and Nature Protection, University of Silesia in Katowice, Jagiellońska 28, 40-032 Katowice, Poland
3 Częstochowa University of Technology, Institute of Environmental Engineering, Brzez&5x301;nicka 60a, 42-200 Częstochowa, Poland
5 White Hill Company, Żurawia 71/3, 15-540 Białystok, Poland
6 Department of Plant Physiology, Faculty of Agriculture and Biology, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776 Warsaw, Poland

In this review, using the network analysis, based on the bibliometric data, collected from Web of Science Core Collection database, we followed the development of chlorophyll fluorescence research (CFR) during 1947-2018. We confirmed dramatic increase in diversity of CFR from late 90-ties and vigorous development of this discipline in the last ten years. They are parallel to an increase in number of research areas and institutions involved and were triggered by the accumulation of knowledge and methodological, technological, and communication advances, especially modern fluorimeters and fluorescence techniques. The network analysis of keywords and research areas confirmed CFR changed into modern, multidisciplinary, highly collaborative discipline, in which in spite of many 'core' disciplines as plant science, environmental sciences, agronomy/food science and technology, the promising, modern areas developed: biochemistry and molecular biology, remote sensing, and big data artificial intelligence method.

Keywords: collaboration; globalization; plant physiological status; trends in chlorophyll fluorescence research.

Received: October 5, 2018; Accepted: April 8, 2019; Prepublished online: May 6, 2019; Published: May 16, 2019Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
BĄBA, W., KOMPAŁA-BĄBA, A., ZABOCHNICKA-ŚWIĄTEK, M., LUŹNIAK, J., HANCZARUK, R., ADAMSKI, A., & KALAJI, H.M. (2019). Discovering trends in photosynthesis using modern analytical tools:More than 100 reasons to use chlorophyll fluorescence. Photosynthetica57(2), 668-679. doi: 10.32615/ps.2019.069.
Download citation

Supplementary files

Download fileBaba 2052 Table 3S.docx

File size: 34.54 kB

Download fileBaba 2052 Table 7S.pdf

File size: 113.44 kB

Download fileBaba 2052 Table 6S.docx

File size: 28.82 kB

Download fileBaba 2052 Table 4S.docx

File size: 52.61 kB

Download fileBaba 2052 Table 5S.docx

File size: 74.24 kB

Download fileBaba 2052 Table 2S.docx

File size: 71.2 kB

Download fileBaba 2052 Table 1S.docx

File size: 41.67 kB

References

  1. Abid G., M'hamdi M., Mingeot D. et al.: Effect of drought stress on chlorophyll fluorescence, antioxidant enzyme activities and gene expression patterns in faba bean (Vicia faba L.). - Arch. Agron. Soil Sci. 63: 536-552, 2017. Go to original source...
  2. Alam B., Nair D., Jacob J.: Low temperature stress modifies the photochemical efficiency of a tropical tree species Hevea brasiliensis: effects of varying concentration of CO2 and photon flux density. - Photosynthetica 43: 247-252, 2005. Go to original source...
  3. Allel D., Ben-Amar A., Abdelly C.: Leaf photosynthesis, chlorophyll fluorescence and ion content of barley (Hordeum vulgare) in response to salinity. - J. Plant Nutr. 41: 497-508, 2018. Go to original source...
  4. Azevedo H., Pinto C.G.G., Fernandes J. et al.: Cadmium effects on sunflower growth and photosynthesis. - J. Plant Nutr. 28: 2211-2220, 2005. Go to original source...
  5. Bąba W., Kalaji HM., Kompała-Bąba A., Goltsev V.: Acclimatization of photosynthetic apparatus of tor grass (Brachypodium pinnatum) during expansion. - PLoS ONE 11: e0156201, 2016. Go to original source...
  6. Bąba W., Kurowska M., Kompała-Bąba A. et al.: Genetic diversity of populations of Brachypodium pinnatum (L.) P. Beauv.: expansive grass in a fragmented landscape. - Pol. J. Ecol. 60: 31-40, 2012.
  7. Baker N., Rosenqvist E.: Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. - J. Exp. Bot. 55: 1607-1621, 2004. Go to original source...
  8. Bałazy K., Trudnowska E., Wichorowski M., Błachowiak-Samołyk K.: Large versus small zooplankton in relation to temperature in the Arctic shelf region. - Polar Res. 37: 1427409, 2018. Go to original source...
  9. Baycu G., Gevrek-Kürüm N., Moustaka J. et al.: Cadmium-zinc accumulation and photosystem II responses of Noccaea caerulescens to Cd and Zn exposure. - Environ. Sci. Pollut. R. 24: 2840-2850, 2017.
  10. Blankenship R.E.: Molecular Mechanisms of Photosynthesis. Pp. 312. Wiley-Blackwell, Chichester 2014.
  11. Brestič M., Živčák M., Kalaji H.M. et al.: Photosystem II thermostability in situ: Environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L. - Plant Physiol. Bioch. 57: 93-105, 2012.
  12. Bussotti F.: Assessment of stress conditions in Quercus ilex L. leaves by O-J-I-P chlorophyll alpha fluorescence analysis. - Plant Biosyst. 138: 101-109, 2004. Go to original source...
  13. Cai S., Xu D.: Light intensity-dependent reversible down-regulation and irreversible damage of PSII in soybean leaves. - Plant Sci. 163: 847-853, 2002. Go to original source...
  14. Cetner M.D., Kalaji H.M., Goltsev V. et al.: Effects of nitrogen-deficiency on efficiency of light-harvesting apparatus in radish. - Plant Physiol. Bioch. 119: 81-92, 2017. Go to original source...
  15. Dąbrowski P., Baczewska A.H., Pawluskiewicz 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...
  16. Drusch M., Moreno J., Del Bello U. et al.: The FLuorescence EXplorer mission concept - ESA's Earth Explorer 8. - IEEE T. Geosci. Remote 55: 1273-1284, 2017. Go to original source...
  17. Ferrell J., Earl H., Vencill W.: The effect of selected herbicides on CO2 assimilation, chlorophyll fluorescence, and stomatal conductance in johnsongrass (Sorghum halepense L.). - Weed Sci. 51: 28-31, 2003. Go to original source...
  18. Goltsev V., Zaharieva I., Chernev P. et al.: Drought-induced modifications of photosynthetic electron transport in intact leaves: Analysis and use of neural networks as a tool for a rapid non-invasive estimation. - BBA-Bioenergetics 1817: 1490-1498, 2012.
  19. Goltsev V., Zaharieva I., Chernev P., Strasser R.J.: Delayed fluorescence in photosynthesis. - Photosynth. Res. 101: 217-232, 2009. Go to original source...
  20. Goltsev V.N., Kalaji H.M., Paunov M. et al.: Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. - Russ. J. Plant Physl+ 63: 869-893, 2016.
  21. Govindjee: Sixty-three years since Kautsky: Chlorophyll a fluorescence. - Aust. J. Plant Physiol. 22: 131-160, 1995. Go to original source...
  22. Govindjee, Beatty T., Gest H., Allen J.F.: Discoveries in Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 1304. Springer, Dordrecht 2005.
  23. Govindjee, Šesták, Z., Peters, W.R.: The early history of "Photosynthetica", "Photosynthesis Research" and their publishers. - Photosynthetica 40: 1-11, 2002. Go to original source...
  24. Holub O., Seufferheld M., Gohlke C. et al.: Fluorescence lifetime imaging (FLI) in real-time - a new technique in photosynthesis research. - Photosynthetica 38: 581-599, 2000. Go to original source...
  25. Jabłoński A.: Efficiency of anti-stokes fluorescence in dyes. - Nature 131: 839-40, 1933. Go to original source...
  26. Joiner J., Yoshida Y., Vasilkov A.P. et al.: The seasonal cycle of satellite chlorophyll fluorescence observations and its relationship to vegetation phenology and ecosystem atmosphere carbon exchange. - Remote Sens. Environ. 152: 375-391, 2014. Go to original source...
  27. 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, 2017a.
  28. Kalaji H.M., Goltsev V.N., Żuk-Golaszewska K. et al.: Chlorophyll Fluorescence. Understanding Crop Performance: Basics and Applications. Pp. 222. CRC Press, Boca Raton 2017c. Go to original source...
  29. Kalaji H.M., Jajoo A., Oukarroum A. et al.: Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. - Acta Physiol. Plant. 38: 102-114, 2016. Go to original source...
  30. Kalaji H.M., Schansker G., Brestič M. et al.: Frequently asked questions about chlorophyll fluorescence, the sequel. - Photosynth. Res. 132: 13-66, 2017b. Go to original source...
  31. 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, 2014. Go to original source...
  32. Kautsky H., Hirsch A.: Neue Versuche zur Kohlensäureassimilation. - Naturwissenschaften 19: 964, 1931. Go to original source...
  33. Kučerová J., Konôpková A., Pšidová E. et al.: Adaptive variation in physiological traits of beech provenances in Central Europe. - iForest 11: 24-31, 2018. Go to original source...
  34. Ladle R.J., Todd P.A., Malhado A.C.M.: Assessing insularity in global science. - Scientometrics 93: 745-750, 2012. Go to original source...
  35. Laisk A., Eichelmann H., Oja V. et al.: Photosystem II cycle and alternative electron flow in leaves. - Plant Cell Physiol. 47: 972-983, 2006. Go to original source...
  36. Lapa G., Morandini F., Ferrat L.: Sap flow and photosynthetic response to climate and drought of Pinus nigra in a Mediterranean natural forest. - Trees-Struct. Funct. 31: 1711-1721, 2017.
  37. Lazár D.: Chlorophyll a fluorescence induction. - BBA-Bioenergetics 1412: 1-28, 1999. Go to original source...
  38. Lazár D.: Chlorophyll a fluorescence rise induced by high light illumination of dark-adapted plant tissue studied by means of a model of photosystem II and considering photosystem II heterogeneity. - J. Theor. Biol. 220: 469-503, 2003. Go to original source...
  39. Lazár D.: The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. - Funct. Plant Biol. 33: 9-30, 2006. Go to original source...
  40. Lazár D.: Modelling of light-induced chlorophyll a fluorescence rise (O-J-I-P transient) and changes in 820 nm-transmittance signal of photosynthesis. - Photosynthetica 47: 483-498, 2009. Go to original source...
  41. 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...
  42. Lazár D., Schansker G.: Models of chlorophyll a fluorescence transients. - In: Laisk A., Nedbal L., Govindjee (ed.): Photosynthesis in silico: Understanding Complexity from Molecules to Ecosystems. Advances in Photosynthesis and Respiration. Pp. 85-123. Springer, Dordrecht 2009.
  43. Lazár D., Tomek P., Ilík P., Nauš J.: Determination of the antenna heterogeneity of Photosystem II by direct simultaneous fitting of several fluorescence rise curves measured with DCMU at different light intensities. - Photosynth. Res. 68: 247-57, 2001. Go to original source...
  44. Lebedeva G.V., Belyaeva N.E., Demin O.V. et al.: Kinetic model of primary photosynthetic processes in chloroplasts. Description of the fast phase of chlorophyll fluorescence induction under different light intensities. - Biophysics 47: 968-980, 2002.
  45. Li S.-H., Ge Z.-M., Xie L.-N. et al.: Ecophysiological response of native and exotic salt marsh vegetation to waterlogging and salinity: Implications for the effects of sea-level rise. - Sci. Rep.-UK 8: 2441-2453, 2018. Go to original source...
  46. Massacci A., Nabiev S.M., Pietrosanti L. et al.: Response of the photosynthetic apparatus of cotton (Gossypium hirsutum) to the onset of drought stress under field conditions studied by gas-exchange analysis and chlorophyll fluorescence imaging. - Plant Physiol. Bioch. 46: 189-195, 2008. Go to original source...
  47. Munday J.G., Govindjee: Light-induced changes in the fluorescence yield of chlorophyll a in vivo. III. The dip and the peak of the fluorescence transient in Chlorella pyrenoidosa. - Biophys. J. 9: 1-29, 1969. Go to original source...
  48. 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...
  49. Papageorgiou G.C., Govindjee: Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 818. Springer, Dordrecht 2004. Go to original source...
  50. Persson O., Danell R., Schneider J.: How to use Bibexcel for various types of bibliometric analysis. - In: Åström F., Danell R., Larsen B., Schneider J. (ed.): Celebrating Scholarly Communication Studies: A Festschrift for Olle Persson at His 60th Birthday. Pp. 9-24. International Society for Scientometrics and Informetrics, Leuven 2009.
  51. Pflug E.E., Buchmann N., Siegwolf R.T.W. et al.: Resilient leaf physiological response of European beech (Fagus sylvatica L.) to summer drought and drought release. - Front. Plant Sci. 9: 187, 2018. Go to original source...
  52. 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...
  53. Schreiber U.: Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. - In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 279-319. Springer, Dordrecht 2004. Go to original source...
  54. Schreiber U., Schliwa U., Bilger W.: Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. - Photosynth. Res. 10: 51-62, 1986. Go to original source...
  55. Stirbet A., Govindjee: On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: Basis and applications of the OJIP fluorescence transient. - J. Photoch. Photobio. B 104: 236-257, 2011. Go to original source...
  56. 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...
  57. 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 56: 86-104, 2018. Go to original source...
  58. Stirbet A., Riznichenko G.Y., Rubin A.B., Govindjee: Modeling chlorophyll a fluorescence transient: relation to photosynthesis. - Biochemistry-Moscow+ 79: 291-323, 2014. Go to original source...
  59. 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...
  60. Strasser R.J., Govindjee: The Fo and the O-J-I-P fluorescence rise in higher plants and algae. - In: Argyroudi-Akoyunoglou J.H. (ed.): Regulation of Chloroplast Biogenesis. Pp. 423-26. Springer, Boston 1992. Go to original source...
  61. 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...
  62. 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...
  63. van Eck N.J., Waltman L.: VOS: A new method for visualizing similarities between objects. - In: Decker R., Lenz H.-J. (ed.): Advanced Data Analysis. Pp. 299-306. Springer, Berlin-Heidelberg 2007. Go to original source...
  64. van Eck N.J., Waltman L.: How to normalize cooccurrence data? An analysis of some well-known similarity measures. - J. Assoc. Inf. Sci. Tech. 60: 1635-1651, 2009.
  65. van Eck N.J., Waltman L.: Visualizing bibliometric networks. - In: Ding Y., Rousseau R., Wolfram D. (ed.): Measuring Scholarly Impact. Pp. 285-320. Springer, Cham 2014. Go to original source...
  66. Vialet-Chabrand S., Matthews J.S.A., Simkin A.J. et al.: Importance of fluctuations in light on plant photosynthetic acclimation. - Plant Physiol. 173: 2163-2179, 2017. Go to original source...
  67. Vredenberg W.J.: A three-state model for energy trapping and chlorophyll fluorescence in photosystem II incorporating radical pair recombination. - Biophys. J. 79: 26-38, 2000. Go to original source...
  68. Vredenberg W.J.: On the quantitative relation between dark kinetics of NPQ-induced changes in variable fluorescence and the activation state of the CF0.CF1.ATPase in leaves. - Photosynthetica 56: 139-149, 2018. Go to original source...
  69. Walther S., Voigt M., Thum T. et al.: Satellite chlorophyll fluorescence measurements reveal large-scale decoupling of photosynthesis and greenness dynamics in boreal evergreen forests. - Glob. Change Biol. 22: 2979-2996, 2016. Go to original source...
  70. Zhu X.G., Govindjee, Baker N.R. et al.: Chlorophyll a fluorescence induction kinetics in leaves predicted from a model describing each discrete step of excitation energy and electron transfer associated with Photosystem II. - Planta 223: 114-133, 2005. Go to original source...
  71. 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.
  72. Żurek G., Rybka K., Pogrzeba M. et al.: Chlorophyll a fluorescence in evaluation of the effect of heavy metal soil contamination on perennial grasses. - PLoS ONE 9: e91475, 2014.