, Volume 56, Issue 1, pp 86–104 | Cite as

Chlorophyll a fluorescence induction: Can just a one-second measurement be used to quantify abiotic stress responses?

  • A. StirbetEmail author
  • D. LazárEmail author
  • J. Kromdijk
  • Govindjee


Chlorophyll (Chl) a fluorescence induction (transient), measured by exposing dark-adapted samples to high light, shows a polyphasic rise, which has been the subject of extensive research over several decades. Several Chl fluorescence parameters based on this transient have been defined, the most widely used being the FV [= (FM–F0)]/FM ratio as a proxy for the maximum quantum yield of PSII photochemistry. However, considerable additional information may be derived from analysis of the shape of the fluorescence transient. In fact, several performance indices (PIs) have been defined, which are suggested to provide information on the structure and function of PSII, as well as on the efficiencies of specific electron transport reactions in the thylakoid membrane. Further, these PIs have been proposed to quantify plant tolerance to stress, such as by high light, drought, high (or low) temperature, or N-deficiency. This is an interesting idea, since the speed of the Chl a fluorescence transient measurement (<1 s) is very suitable for high-throughput phenotyping. In this review, we describe how PIs have been used in the assessment of photosynthetic tolerance to various abiotic stress factors. We synthesize these findings and draw conclusions on the suitability of several PIs in assessing stress responses. Finally, we highlight an alternative method to extract information from fluorescence transients, the Integrated Biomarker Response. This method has been developed to define multi-parametric indices in other scientific fields (e.g., ecology), and may be used to combine Chl a fluorescence data with other proxies characterizing CO2 assimilation, or even growth or grain yield, allowing a more holistic assessment of plant performance.

Additional key words

JIP-test Kautsky effect performance index tolerance to stress 



photon flux absorbed by the antenna of PSII units


area above the OJIP transient


chill factor index




cross section




driving force


drought factor index


flux of energy dissipation (through processes other than trapping) in the antenna of PSII units


rate of electron transport from the reduced QA to the intersystem electron acceptors


minimum Chl a fluorescence




fluorescence induction


maximum Chl a fluorescence


terminal steady state of Chl a fluorescence


heat sensitivity index

I step

Chl a fluorescence at ~ 30 ms


integrated biomarker response

J step

Chl a fluorescence at ~ 2 ms

K step

Chl a fluorescence at ~ 0.3 ms


initial slope (first 0.3 ms) of the O-J fluorescence rise


nonphotochemical quenching of the excited states of Chl


oxygen-evolving complex


reaction center Chls of PSII






photochemical stress index


performance index


performance index leaf ratio




rate of electron transport from the reduced QA to the final electron acceptors of PSI


ratio of fluorescence decrease to steady state fluorescence


reactive oxygen species


relative water content


structure-function index


normalized area above the OJIP transient


flux of exciton trapping by active PSII reaction centers leading to QA reduction


relative amplitude of the I–P phase of Chl a fluorescence


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Acosta-Motos J.R., Ortuño M.F., Bernal-Vicente A. et al.: Responses to salt stress: Adaptive mechanisms.–Agronomy 7: 18, 2017.CrossRefGoogle Scholar
  2. Adams III W.W., Zarter C.R., Mueh K.E. et al.: Energy dissipation and photoinhibition: A continuum of photoprotection.–In: Demmig-Adams B., Adams III W.W., Mattoo A.K. (ed.): Photoprotection, Photoinhibition, Gene Regulation, and Environment. Pp. 49–64. Springer Science+Business Media B.V., Dordrecht 2008.Google Scholar
  3. Adamski J.M., Cargnelutti D., Sperotto R.A. et al.: Identification and physiological characterization of two sister lines of indica rice (Oryza sativa L.) with contrasting levels of cold tolerance.–Can. J. Plant Sci. 96: 197–214, 2016.CrossRefGoogle Scholar
  4. Ainsworth E.A., Yendrek C.R., Sitch S. et al.: The effects of ozone on net primary productivity and implications for climate change.–Annu. Rev. Plant Biol. 63: 637–661, 2012.PubMedCrossRefGoogle Scholar
  5. Allakhverdiev S.I., Murata N.: Salt stress inhibits photosystem II and I in cynobacteria.–Photosynth. Res. 98: 529–539, 2008.PubMedCrossRefGoogle Scholar
  6. Alloway B.J.: Sources of heavy metals and metalloids in soils.–In: Alloway B. (ed.): Heavy Metals in Soils. Environmental Pollution, Vol. 22. Springer, Dordrecht 2013.CrossRefGoogle Scholar
  7. Appenroth K.J., Stöckel J., Srivastava A. et al.: Multiple effects of chromate on the photosynthetic apparatus of Spirodela polyrhiza as probed by OJIP chlorophyll a fluorescence measurements.–Environ. Pollut. 115: 49–64, 2001.PubMedCrossRefGoogle Scholar
  8. Baker N.R.: Chlorophyll fluorescence: A probe of photosynthesis in vivo.–Annu. Rev. Plant Biol. 59: 89–113, 2008.PubMedCrossRefGoogle Scholar
  9. Baldassarre V., Cabassi G., Ferrante A.: Use of chlorophyll a fluorescence for evaluating the quality of leafy vegetables.–Aust. J. Crop Sci. 5: 735–741, 2011.Google Scholar
  10. Bazzaz M.B., Govindjee: Effects of cadmium nitrate on spectral characteristics and light reactions of chloroplasts.–Environ. Lett. 6: 1–12, 1974a.PubMedCrossRefGoogle Scholar
  11. Bazzaz M.B., Govindjee: Effects of lead chloride on chloroplast reactions.–Environ. Lett. 6: 175–191, 1974b.PubMedCrossRefGoogle Scholar
  12. Beliaeff B., Burgeot T.: Integrated biomarker response: a useful tool for ecological risk assessment.–Environ. Toxicol. Chem. 21: 1316–1322, 2002.PubMedCrossRefGoogle Scholar
  13. Björkman O., Demmig B.: Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins.–Planta 170: 489–504, 1987.PubMedCrossRefGoogle Scholar
  14. Blankenship R.E.: Molecular Mechanisms of Photosynthesis, 2nd ed. Pp. 312. Blackwell-John Wiley, Oxford 2014.Google Scholar
  15. Blevins D.G., Lukaszewski K.M.: Boron in plant structure and function.–Annu. Rev. Plant Phys. 49: 481–500, 1998.CrossRefGoogle Scholar
  16. Bohnert H.J., Nelson D.E., Jensen R.G.: Adaptations to environmental stresses.–Plant Cell 7: 1099–1111, 1995.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Boureima S. Oukarroum A., Diouf M. et al.: Screening for drought tolerance in mutant germplasm of sesame (Sesamum indicum) probing by chlorophyll a fluorescence.–Environ. Exp. Bot. 81: 37–43, 2012.CrossRefGoogle Scholar
  18. Broeg K., Lehtonen K.K.: Indices for the assessment of environmental pollution of the Baltic Sea coasts: Integrated assessment of a multi-biomarker approach.–Mar. Pollut. Bull. 53: 508–522, 2006.PubMedCrossRefGoogle Scholar
  19. Bussotti F., Agati G., Desotgiu R. et al.: Ozone foliar symptoms in woody plants assessed with ultrastructural and fluorescence analysis.–New Phytol. 166: 941–955, 2005.PubMedCrossRefGoogle Scholar
  20. Bussotti F., Strasser R.J., Schaub M.: Photosynthetic behavior of woody species under high ozone exposure probed with the JIPtest: A review.–Environ. Pollut. 147: 430–437, 2007.PubMedCrossRefGoogle Scholar
  21. Butler W.L., Kitajima M.: Fluorescence quenching in photosystem II of chloroplasts.–Biochim. Biophys. Acta 376: 116–125, 1975.PubMedCrossRefGoogle Scholar
  22. Chaves M.M., Flexas J., Pinheiro C.: Photosynthesis under drought and salt stress: Regulation mechanisms from whole plant to cell.–Ann. Bot.-London 103: 551–560, 2009.CrossRefGoogle Scholar
  23. Chen S., Yang J., Zhang M. et al.: Classification and characteristics of heat tolerance in Ageratina adenophora populations using fast chlorophyll a fluorescence rise O-J-I-P.–Environ. Exp. Bot. 122: 126–140, 2016.CrossRefGoogle Scholar
  24. Clijsters H., Cuypers A., Vangronsveld J.: Physiological responses to heavy metals in higher plants; Defence against oxidative stress.–Z. Naturforsch. 54c: 720–734, 1999.Google Scholar
  25. D’Agostino I.B., Kieber J.J.: Molecular mechanisms of cytokinin action.–Curr. Opin. Plant Biol. 2: 359–364, 1999.PubMedCrossRefGoogle Scholar
  26. Demmig-Adams B., Adams W.W., Heber U. et al.: Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts.–Plant Physiol. 92: 293–301, 1990.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Dinis L.-T., Ferreira H., Pinto G. et al.: Kaolin-based, foliar reflective film protects photosystem II structure and function in grapevine leaves exposed to heat and high solar radiation.–Photosynthetica 54: 47–55, 2016.CrossRefGoogle Scholar
  28. Duarte B., Pedro S., Marques J.C. et al.: Zostera noltii development probing using chlorophyll a transient analysis (JIP-test) under field conditions: Integrating physiological insights into a photochemical stress index.–Ecol. Indic. 76: 219–229, 2017.CrossRefGoogle Scholar
  29. Edwards G.E., Baker N.R.: Can CO2 assimilation in maize leaves be predicted accurately from chlorophyll fluorescence analysis?–Photosynth. Res. 37: 89–102, 1993.PubMedCrossRefGoogle Scholar
  30. Fahlgren N., Gehan M.A., Baxter I.: Lights, camera, action: highthroughput plant phenotyping is ready for a close up.–Curr. Opin. Plant Biol. 24: 93–99, 2015.PubMedCrossRefGoogle Scholar
  31. Fan J., Hu Z., Xie Y. et al.: Alleviation of cold damage to photosystem II and metabolisms by melatonin in Bermudagrass.–Front. Plant Sci. 6: 925, 2015.PubMedPubMedCentralCrossRefGoogle Scholar
  32. Feller U., Crafts-Brandner S.J., Salvucci M.E.: Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/ oxygenase (Rubisco) activase-mediated activation of Rubisco.–Plant Physiol. 116: 539–546, 1998.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Ferrante A., Maggiore T.: Chlorophyll a fluorescence measurements to evaluate storage time and temperature of Valeriana leafy vegetables.–Postharvest Biol. Tec. 45: 73–80, 2007.CrossRefGoogle Scholar
  34. Ferreira N.G.C., Cardoso D.N., Morgado R. et al.: Long-term exposure of the isopod Porcellionides pruinosus to nickel: costs in the energy budget and detoxification enzymes.–Chemosphere 135: 354–362, 2015b.PubMedCrossRefGoogle Scholar
  35. Ferreira N.G.C., Morgado R., Santos M.J.G. et al.: Biomarkers and energy reserves in the isopod Porcellionides pruinosus: The effects of long-term exposure to dimethoate.–Sci. Total Environ. 502: 91–102, 2015a.PubMedCrossRefGoogle Scholar
  36. Flexas J., Bota J., Loreto F. et al.: Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants.–Plant Biol. 6: 269–279, 2004.PubMedCrossRefGoogle Scholar
  37. Frolec J., Řebiček J., Lazár D. et al.: Impact of two different types of heat stress on chloroplast movement and fluorescence signal of tobacco leaves.–Plant Cell Rep. 29: 705–714, 2010.PubMedCrossRefGoogle Scholar
  38. Genty B., Briantais J.-M., Baker N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.–Biochim. Biophys. Acta 990: 87–92, 1989.CrossRefGoogle Scholar
  39. Genty B., Briantais J.-M., Da Silva J.B.V.: Effect of drought on primary photosynthetic processes of cotton leaves.–Plant Physiol. 83: 360–364, 1987.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 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.–Biochim. Biophys. Acta 1817: 1490–1498, 2012.PubMedCrossRefGoogle Scholar
  41. Govindjee, Amesz J., Fork D.C. (ed.): Light Emission by Plants and Bacteria. Pp. 660. Academic Press, Orlando 1986.Google Scholar
  42. Govindjee, Papageorgiou G.C.: Chlorophyll fluorescence and photosynthesis: fluorescence transients.–In: Giese A.C. (ed.): Photophysiology, Vol. 6. Pp. 1–46. Academic Press, New York 1971.Google Scholar
  43. Govindjee, Shevela D., Björn L.-O.: Evolution of the Z-scheme of photosynthesis: a perspective.–Photosynth. Res. 133: 5–15, 2017.PubMedCrossRefGoogle Scholar
  44. Govindjee: Chlorophyll a fluorescence: a bit of basics and history.–In: Papageorgiou G.C., {ieGovindjee (ed.): Chlorophyll a fluorescence: A signature of Photosynthesis, Advances in Photosynthesis and Respiration. Vol. 19. Pp. 1–41. Springer, Dordrecht 2004.Google Scholar
  45. Govindjee: Sixty-three years since Kautsky: chlorophyll a fluorescence.–Aust. J. Plant Physiol. 22: 131–160, 1995.CrossRefGoogle Scholar
  46. Gravano E., Bussotti F., Strasser R.J. et al.: Ozone symptoms in leaves of woody plants in open-top chambers: ultrastructural and physiological characteristics.–Physiol. Plantarum 121: 620–633, 2004.CrossRefGoogle Scholar
  47. Greenbaum N.L., Ley A.C., Mauzerall D.C.: Use of a lightinduced respiratory transient to measure the optical cross section of photosystem I in Chlorella.–Plant Physiol. 84: 879–882, 1987.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Guanter L., Zhang Y., Jung M. et al.: Global and time-resolved monitoring of crop photosynthesis with chlorophyll fluorescence.–Proc. Natl. Acad. Sci. USA 111: E1327–E1333, 2014.PubMedCrossRefGoogle Scholar
  49. 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. Genève 48: 147–160, 1995.Google Scholar
  50. Hakala M., Tuominen I., Keränen M.: Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of Photosystem II.–Biochim. Biophys. Acta 1706: 68–80, 2005.PubMedCrossRefGoogle Scholar
  51. Hamdani S., Qu M., Xin C.-P. et al.: Variations between the photosynthetic properties of elite and landrace Chinese rice cultivars revealed by simultaneous measurements of 820 nm transmission signal and chlorophyll a fluorescence induction.–J. Plant Physiol. 177: 128–138, 2015.PubMedCrossRefGoogle Scholar
  52. Hasegawa P.M., Bressan R.A., Zhu J. et al.: Plant cellular and molecular responses to high salinity.–Annu. Rev. Plant Phys. 51: 463–499, 2000.CrossRefGoogle Scholar
  53. Hendrickson L., Förster B., Pogson B.J. et al: A simple chlorophyll fluorescence parameter that correlates with the rate coefficient of photoinactivation of photosystem II.–Photosynth. Res. 84: 43–49, 2005.PubMedCrossRefGoogle Scholar
  54. Hermans C., Smeyers M., Rodriguez R.M. et al.: Quality assessment of urban trees: A comparative study of physiological characterisation, airborne imaging and on site fluorescence monitoring by the OJIP-test.–J. Plant Physiol. 160: 81–90, 2003.PubMedCrossRefGoogle Scholar
  55. Hoagland D.R., Arnon D.I.: The water-culture method for growing plants without soil.–In: Agricultural Experiment Station, Circular 347. Pp. 1–39. College of Agriculture, University of California, Berkeley 1938.Google Scholar
  56. Humplík J.F., Lazár L., Husičková A. et al.: Automated phenotyping of plant shoots using imaging methods for analysis of plant stress responses–a review.–Plant Methods 11: 29, 2015.PubMedPubMedCentralCrossRefGoogle Scholar
  57. Jedmowski C., Ashoub A., Momtaz O. et al.: Impact of drought, heat, and their combination on chlorophyll fluorescence and yield of wild barley (Hordeum spontaneum).–J. Bot. 2015: 120868, 2015.Google Scholar
  58. Jedmowski C., Bayramov S., Brüggemann W.: Comparative analysis of drought stress effects on photosynthesis of Eurasian and North African genotypes of wild barley.–Photosynthetica 52: 564–573, 2014.CrossRefGoogle Scholar
  59. Jedmowski C., Brüggemann W.: Imaging of fast chlorophyll fluorescence induction curve (OJIP) parameters, applied in a screening study with wild barley (Hordeum spontaneum) genotypes under heat stress.–J. Photoch. Photobio. B 151: 153–160, 2015.CrossRefGoogle Scholar
  60. Jiang C.-D., Shi L., Gao H.-Y. et al.: Development of photosystems 2 and 1 during leaf growth in grapevine seedlings probed by leaf chlorophyll a fluorescence transient and 820 nm transmission in vivo.–Photosynthetica 44: 454–463, 2006.CrossRefGoogle Scholar
  61. Jiang H.-X., Chen L.-S., Zheng J.-G. et al.: Aluminum-induced effects on Photosystem II photochemistry in citrus leaves assessed by the chlorophyll a fluorescence transient.–Tree Physiol. 28: 1863–1871, 2008.PubMedCrossRefGoogle Scholar
  62. Jiang H.-X., Tang N., Zheng J.-G. et al.: Antagonistic actions of boron against inhibitory effects of aluminum toxicity on growth, CO2 assimilation, ribulose-1,5-bisphosphate carboxylase/ oxygenase, and photosynthetic electron transport probed by the JIP-test, of Citrus grandis seedlings.–BMC Plant Biol. 9: 102, 2009.PubMedPubMedCentralCrossRefGoogle Scholar
  63. Joshi M.K., Mohanty P.: Chlorophyll a fluorescence as a probe of heavy metal ion toxicity in plants.–In: Papageorgiou G.C., {ieGovindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Vol. 19. Pp. 637–661. Springer, Dordrecht 2004.CrossRefGoogle Scholar
  64. Kalaji H.M., Carpentier R., Allakhverdiev S.I. et al.: Fluorescence parameters as early indicators of light stress in barley.–J. Photoch. Photobio. B 112: 1–6, 2012.CrossRefGoogle Scholar
  65. 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, 2016.CrossRefGoogle Scholar
  66. Kalaji H.M., Oukarroum A., Alexandrov V. et al.: Identification of nutrient deficiency in maize and tomato plants by in vivo chlorophyll a fluorescence measurements.–Plant Physiol. Biochem. 81: 16–25, 2014b.PubMedCrossRefGoogle Scholar
  67. Kalaji H.M., Schansker G., Brestic M. et al.: Frequently asked questions about chlorophyll fluorescence, the sequel.–Photosynth. Res. 132: 13–66, 2017a.PubMedCrossRefGoogle Scholar
  68. Kalaji H.M., Schansker G., Ladle R.J. et al.: Frequently asked questions about chlorophyll fluorescence: practical issues.–Photosynth. Res. 122: 121–158, 2014a.PubMedPubMedCentralCrossRefGoogle Scholar
  69. Kalaji M.H., Goltsev V.N., Żuk-Gołaszewska K. et al.: Chlorophyll Fluorescence: Understanding Crop Performance–Basics and Applications. Pp. 222. CRC Press, Boca Raton 2017b.CrossRefGoogle Scholar
  70. Kale R., Hebert A.E., Frankel L.K. et al.: Amino acid oxidation of the D1 and D2 proteins by oxygen radicals during photoinhibition of Photosystem II.–Proc. Natl. Acad. Sci. USA 114: 2988–2993, 2017.PubMedCrossRefGoogle Scholar
  71. Kaňa R., Govindjee: Role of ions in the regulation of light harvesting.–Front. Plant Sci. 7: 1849, 2016.PubMedPubMedCentralCrossRefGoogle Scholar
  72. Kouřil R., Lazár D, Lee H. et al.: Moderately elevated temperature eliminates resistance of rice plants with enhanced expression of glutathione reductase to intensive photooxidative stress.–Photosynthetica 41: 571–578, 2003.CrossRefGoogle Scholar
  73. Krause G.H., Weis E.: Chlorophyll fluorescence and photosynthesis: the basics.–Annu. Rev. Plant Phys. 42: 313–349, 1991.CrossRefGoogle Scholar
  74. Kromdijk J., Głowacka K., Leonelli L. et al.: Improving photosynthesis and crop productivity by accelerating recovery from photoprotection.–Science 354: 857–861, 2016.PubMedCrossRefGoogle Scholar
  75. Lazár D., Ilík P., Nauš J.: An appearance of K-peak in fluorescence induction depends on the acclimation of barley leaves to higher temperatures.–J. Lumin. 72-74: 595–596, 1997.CrossRefGoogle Scholar
  76. Lazár D., Ilík P.: 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, 1997.CrossRefGoogle Scholar
  77. Lazár D., Nauš J.: Statistical properties of chlorophyll fluorescence induction parameters.–Photosynthetica 35: 121–127, 1998.CrossRefGoogle Scholar
  78. Lazár D., Pospíšil P., Nauš J.: Decrease of fluorescence intensity after the K step in chlorophyll a fluorescence induction is suppressed by electron acceptors and donors to photosystem 2.–Photosynthetica 37: 255–265, 1999.CrossRefGoogle Scholar
  79. Lazár D., Schansker G.: Models of chlorophyll a fluorescence transients.–In: Laisk A., Nedbal A.L., Govindjee (ed.): Photosynthesis in Silico: Understanding Complexity from Molecules to Ecosystems. Advances in Photosynthesis and Respiration. Vol. 29. Pp. 85–123. Springer,DordrechtGoogle Scholar
  80. Lazár D.: Chlorophyll a fluorescence induction.–Biochim. Biophys. Acta 1412: 1–28, 1999.PubMedCrossRefGoogle Scholar
  81. 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.PubMedCrossRefGoogle Scholar
  82. 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.CrossRefGoogle Scholar
  83. Lazár D.: Parameters of photosynthetic energy partitioning.–J. Plant Physiol. 175: 131–147, 2015.PubMedCrossRefGoogle Scholar
  84. Lazár D.: Simulations show that a small part of variable chlorophyll a fluorescence originates in photosystem I and contributes to overall fluorescence rise.–J. Theor. Biol. 335: 249–264, 2013.PubMedCrossRefGoogle Scholar
  85. Lazár D.: The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light.–Funct. Plant Biol. 33: 9–30, 2006.CrossRefGoogle Scholar
  86. Ley A.C., Mauzerall D.C.: Absolute absorption cross-sections for photosystem II and the minimum quantum requirement of photosynthesis in Chlorella vulgaris.–Biochim. Biophys. Acta 680: 95–106, 1982.CrossRefGoogle Scholar
  87. Liang Y., Chen H., Tang M.J. et al.: Responses of Jatropha curcas seedlings to cold stress: photosynthesis-related proteins and chlorophyll fluorescence characteristics.–Physiol. Plantarum 131: 508–517, 2007.CrossRefGoogle Scholar
  88. Lichtenthaler H.K., Buschmann C., Rinderle U. et al.: Application of chlorophyll fluorescence in ecophysiology.–Radiat. Environ. Biophys. 25: 297–308, 1986.PubMedCrossRefGoogle Scholar
  89. Liu Q.D., Zhu Y.R., Tao H.L. et al.: Damage of PSII during senescence of Spirodela polyrrhiza explants under long-day conditions and its prevention by 6-benzyladenine.–J. Plant Res. 119: 145–152, 2006.PubMedCrossRefGoogle Scholar
  90. Makino A.: Rubisco and nitrogen relationships in rice: Leaf photosynthesis and plant growth.–Soil Sci. Plant Nutr. 49: 317–327, 2003.CrossRefGoogle Scholar
  91. Marschner H.: Mineral Nutrition of Higher Plants, 2nd ed. Academic Press, London 1995.Google Scholar
  92. Mathur S., Jajoo A., Mehta P. et al.: Analysis of elevated temperature-induced inhibition of photosystem II using chlorophyll a fluorescence induction kinetics in wheat leaves (Triticum aestivum).–Plant Biol. 13: 1–6, 2011.PubMedCrossRefGoogle Scholar
  93. McGrath J.M., Beztelberger A.M., Wang S. et al.: An analysis of ozone damage to historical maize and soybean yields in the United States.–Proc. Natl. Acad. Sci. USA 112: 14390–14395, 2015.PubMedCrossRefGoogle Scholar
  94. Mehta P., Jajoo A., Mathur S. et al.: Chlorophyll a fluorescence study revealing effects of high salt stress on Photosystem II in wheat leaves.–Plant Physiol. Biochem. 48: 16–20, 2010.PubMedCrossRefGoogle Scholar
  95. Meroni M., Rossini M., Guanter L. et al.: Remote sensing of solar-induced chlorophyll fluorescence: Review of methods and applications.–Remote Sens. Environ. 113: 2037–2051, 2009.CrossRefGoogle Scholar
  96. Mishra K.B., Mishra A., Klem K. et al.: Plant phenotyping: a perspective.–Ind. J. Plant Physiol. 21: 514–527, 2016a.CrossRefGoogle Scholar
  97. Mishra K.B., Mishra A., Novotná K. et al.: Chlorophyll a fluorescence, under half of the adaptive growth-irradiance, for high-throughput sensing of leaf-water deficit in Arabidopsis thaliana accessions.–Plant Methods 12: 46, 2016b.PubMedPubMedCentralCrossRefGoogle Scholar
  98. Misra A.N. Srivastava A., Strasser R.J.: Utilization of fast chlorophyll a fluorescence technique in assessing the salt/ion sensitivity of mung bean and Brassica seedlings.–J. Plant Physiol. 158: 1173–1181, 2001.CrossRefGoogle Scholar
  99. Morales F., Abadía A., Abadía J.: Photoinhibition and photoprotection under nutrient deficiencies, drought and salinity.–In: Demmig-Adams B., Adams III W.W., Mattoo A.K. (ed.): Photoprotection, Photoinhibition, Gene Regulation, and Environment. Pp. 65–85. Springer Science+Business Media B.V. Dordrecht 2008.Google Scholar
  100. Moya I., Cerovic Z.G.: Remote sensing of chlorophyll fluorescence: instrumentation and analysis.–In: Papageorgiou G.C., {ieGovidjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Pp. 429–445. Springer, Dordrecht 2004.CrossRefGoogle Scholar
  101. Müller P., Li X.P., Niyogi K.K.: Non-photochemical quenching. A response to excess light energy.–Plant Physiol. 125: 1558–1566, 2001.PubMedPubMedCentralCrossRefGoogle Scholar
  102. Munday J.C. Jr., Govindjee: Light-induced changes in the fluorescence yield of chlorophyll a in vivo. III. The dip and the peak in the fluorescence transient of Chlorella pyrenoidosa.–Biophys. J. 9: 1–21, 1969a.PubMedPubMedCentralCrossRefGoogle Scholar
  103. Munday J.C. Jr., Govindjee: Light-induced changes in the fluorescence yield of chlorophyll a in vivo. IV. The effect of preillumination on the fluorescence transient of Chlorella pyrenoidosa.–Biophys. J. 9: 22–35, 1969b.PubMedPubMedCentralCrossRefGoogle Scholar
  104. Munns R., Tester M.: Mechanisms of salinity tolerance.–Annu. Rev. Plant Biol. 59: 651–681, 2008.PubMedCrossRefGoogle Scholar
  105. Murata N., Takahashi S., Nishiyama Y. et al.: Photoinhibition of photosystem II under environmental stress.–Biochim. Biophys. Acta 1767: 414–421, 2007.PubMedCrossRefGoogle Scholar
  106. Murchie E.H., Lawson T.: Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications.–J. Exp. Bot. 64: 3983–3998, 2013.PubMedCrossRefGoogle Scholar
  107. Nagajyoti P.C., Lee K.D., Sreekanth T.V.M.: Heavy metals, occurrence and toxicity for plants: a review.–Environ. Chem. Lett. 8: 199–216, 2010.CrossRefGoogle Scholar
  108. Nash D., Miyao M., Murata N.: Heat inactivation of oxygen evolution in photosystem II particles and its acceleration by chloride depletion and exogenous manganese.–Biochim. Biophys. Acta 807: 127–133, 1985.CrossRefGoogle Scholar
  109. Nauš J., Kuropatwa R., Klinkovský T. et al.: Heat injury of barley leaves detected by the chlorophyll fluorescence temperature curve.–Biochim. Biophys. Acta 1101: 359–362, 1992.CrossRefGoogle Scholar
  110. Nernst W.H.: [Kinetics of solids: theory of difussion.]–Z. Phys. Chem. 3: 613–637, 1888. [In German]Google Scholar
  111. Niinemets U.: A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance.–Ecol. Res. 25: 693–714, 2010.CrossRefGoogle Scholar
  112. Nikiforou C., Manetas Y.: Inherent nitrogen deficiency in Pistacia lentiscus preferentially affects photosystem I: a seasonal field study.–Funct. Plant Biol. 38: 848–855, 2011.CrossRefGoogle Scholar
  113. Nilkens M., Kress E., Lambrev P. et al.: Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis.–Biochim. Biophys. Acta 1797: 466–475, 2010.PubMedCrossRefGoogle Scholar
  114. Oukarroum A., El Madidi S., Schansker G. et al.: Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering.–Environ. Exp. Bot. 60: 438–446, 2007.CrossRefGoogle Scholar
  115. Oukarroum A., El Madidi S., Strasser R.J.: Differential heat sensitivity index in barley cultivars (Hordeum vulgare L.) monitored by chlorophyll a fluorescence OKJIP.–Plant Physiol. Biochem. 105: 102–108, 2016.PubMedCrossRefGoogle Scholar
  116. Oukarroum A., Strasser R.J., van Staden J.: Phenotyping of dark and light adapted barley plants by the fast chlorophyll a fluorescence rise OJIP.–S. Afr. J. Bot. 70: 277–283, 2004.CrossRefGoogle Scholar
  117. Pan X., Chen X., Zhang D. et al.: Effect of Chromium(VI) on photosystem II activity and heterogeneity of Synechocystis sp. (Cyanophyta): studied with in vivo chlorophyll fluorescence tests.–J. Phycol. 45: 386–394, 2009.PubMedCrossRefGoogle Scholar
  118. Paoletti E., Bussotti F., Della Rocca G. et al.: Fluorescence transient in ozonated Mediterranean shrubs.–Phyton 44: 121–131, 2004.Google Scholar
  119. Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration, Vol. 19. Pp. 820. Springer, Dordrecht 2004.Google Scholar
  120. Papageorgiou G.C., Govindjee: Photosystem II fluorescence: slow changes - scaling from the past.–J. Photochem. Photobiol. B. 104: 258–270, 2011PubMedCrossRefGoogle Scholar
  121. Papageorgiou G.C., Tsimilli-Michael M., Stamatakis K.: The fast and slow kinetics of chlorophyll a fluorescence induction in plants, algae and cyanobacteria: a viewpoint.–Photosynth. Res. 94: 275–290, 2007.PubMedCrossRefGoogle Scholar
  122. Pareek A., Sopory S.K., Bohnert H.K. et al. (ed.): Abiotic Stress Adaptation in Plants: Physiological, Molecular and Genomic Foundation. Pp. 526, Springer, Dordrecht 2010.Google Scholar
  123. Parida A.K., Das A.B.: Salt tolerance and salinity effects on plants: A review.–Ecotoxicol. Environ. Safe. 60: 324–349, 2005.CrossRefGoogle Scholar
  124. Prakash J.S.S., Srivastava A., Strasser R.J. et al.: Senescence induced alterations in the photosystem II functions of Cucumis sativus cotyledons: probing of senescence driven alterations of photosystem II by chlorophyll a fluorescence induction O-J-IP transients.–Indian J. Biochem. Biophys. 40: 160–168, 2003.PubMedGoogle Scholar
  125. Rapacz M., Sasal M., Kalaji H.M. et al.: Is the OJIP test a reliable indicator of winter hardiness and freezing tolerance of common wheat and triticale under variable winter environments?–PLoS ONE 10: e0134820, 2015b.PubMedPubMedCentralCrossRefGoogle Scholar
  126. Rapacz M., Sasal M., Wójcik-Jagła M.: Direct and indirect measurements of freezing tolerance: advantages and limitations.–Acta Physiol. Plant. 37: 157–173, 2015a.CrossRefGoogle Scholar
  127. Rapacz M., Woźniczka A.: A selection tool for freezing tolerance in common wheat using the fast chlorophyll a fluorescence transient.–Plant Breeding 128: 227–234, 2009.CrossRefGoogle Scholar
  128. Rapacz M.: Chlorophyll a fluorescence transient during freezing and recovery in winter wheat.–Photosynthetica 45: 409–418, 2007.CrossRefGoogle Scholar
  129. Schansker G., Tóth S.Z., Holzwarth A.R. et al.: Chlorophyll a fluorescence: beyond the limits of the QA-model.–Photosynth. Res. 120: 43–58, 2014.PubMedCrossRefGoogle Scholar
  130. Schansker G., Tóth S.Z., Kovács L. et al.: Evidence for a fluorescence yield change driven by a light induced conformational change within photosystem II during the fast chlorophyll a fluorescence rise.–Biochim. Biophys. Acta 1807: 1032–1043, 2011.PubMedCrossRefGoogle Scholar
  131. Schreiber U., Berry J.A.: Heat-induced changes of chlorophyll fluorescence in intact leaves correlated with damage of photosynthetic apparatus.–Planta 136: 233–238, 1977.PubMedCrossRefGoogle Scholar
  132. Serbin S.P., Dillaway D.N., Kruger.E.L. et al.: Leaf optical properties reflect variation in photosynthetic metabolism and its sensitivity to temperature.–J. Exp. Bot. 63: 489–502, 2012.PubMedCrossRefGoogle Scholar
  133. Shabnam N., Sharmila P., Govindjee et al.: Differential response of floating and submerged leaves of long leaf pondweed to silver ions.–Front. Plant Sci. 8: 1052, 2017.PubMedPubMedCentralCrossRefGoogle Scholar
  134. Srivastava A, Govindjee, Strasser R.J.: Greening of peas: parallel measurements on 77 K emission spectra, OJIP chlorophyll a fluorescence transient, period four oscillation of the initial fluorescence level, delayed light emission, and P700.–Photosynthetica 37: 365–392, 1999.CrossRefGoogle Scholar
  135. Srivastava A., Guissé B., Greppin H. et al.: Regulation of antenna structure and electron transport in PSII of Pisum sativum under elevated temperature probed by the fast polyphasic chlorophyll a fluorescence transient OKJIP.–Biochim. Biophys. Acta 1320: 95–106, 1997.CrossRefGoogle Scholar
  136. Stauffer P.H.: Flux flummoxed: A proposal for consistent usage.–Ground Water 44: 125–128, 2006.PubMedCrossRefGoogle Scholar
  137. Stefanov D., Petkova V., Denev I.D.: Screening for heat tolerance in common bean (Phaseolus vulgaris L.) lines and cultivars using JIP-test.–Sci. Hortic.-Amsterdam 128: 1–6, 2011.CrossRefGoogle Scholar
  138. Stirbet A., Govindjee, Strasser B.J. et al.: Chlorophyll a fluorescence induction in higher plants: Modelling and numerical simulation.–J. Theor. Biol. 193: 131–151, 1998.CrossRefGoogle Scholar
  139. 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.PubMedCrossRefGoogle Scholar
  140. 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. Photochem. Photobiol. B 104: 236–257, 2011.PubMedCrossRefGoogle Scholar
  141. Stirbet A., Riznichenko G.Yu., Rubin A.B. et al.: Modeling chlorophyll a fluorescence transient: relation to photosynthesis.–Biochemistry-Moscow 79: 291–323, 2014.PubMedCrossRefGoogle Scholar
  142. 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.Google Scholar
  143. Strasser B.J.: Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients.–Photosynth. Res. 52: 147–155, 1997.CrossRefGoogle Scholar
  144. Strasser R.J., Srivastava A., Govindjee: Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria.–Photochem. Photobiol. 61: 32–42, 1995.CrossRefGoogle Scholar
  145. Strasser R.J., Srivastava A., Tsimilli-Michael M.: Screening the vitality and photosynthetic activity of plants by fluorescence transient.–In: Behl R.K., Punia M.S., Lather B.P.S. (ed.): Crop Improvement for Food Security. Pp. 72–115. SSARM, Hisar, India 1999.Google Scholar
  146. Strasser R.J., Tsimilli-Michael M., Dangre D. et al.: 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: Varma A., Oelmüler R. (ed.): Advanced Techniques in Soil Microbiology. Soil Biology. Pp. 319–341. Springer, Berlin 2007.CrossRefGoogle Scholar
  147. Strasser R.J., Tsimilli-Michael M., Srivastava A.: Analysis of the chlorophyll a fluorescence transient.–In: Papageorgiou G.C., {ieGovindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis, Advances in Photosynthesis and Respiration, Vol. 19. Pp. 321–362. Springer, Dordrecht 2004.CrossRefGoogle Scholar
  148. Strasser R.J., Tsimilli-Michael M., Srivastava A.: The fluorescence transient as a tool to characterize and screen photosynthetic samples.–In: Yunus M., Pathre U., Mohanty P. (ed.): Probing Photosynthesis: Mechanisms, Regulation and Adaptation. Pp. 443–480. Taylor & Francis, London 2000.Google Scholar
  149. Strasser R.J.: The grouping model of plant photosynthesis.–In: Akoyunoglou G., Argyroudi-Akoyunoglou J.H. (ed.): Chloroplast Development. Pp. 513–538. Elsevier Biomedical, Amsterdam 1978.Google Scholar
  150. Strauss A.J., Krüger G.H.J., Strasser R.J. et al.: Ranking of dark chilling tolerance in soybean genotypes probed by the chlorophyll a fluorescence transient O-J-I-P.–Environ. Exp. Bot. 56: 147–157, 2006.CrossRefGoogle Scholar
  151. Sudhir P., Murthy S.D.S.: Effects of salt stress on basic processes of photosynthesis.–Photosynthetica 42: 481–486, 2004.CrossRefGoogle Scholar
  152. Toepel J., Gilbert M., Wilhelm C.: Can chlorophyll a in-vivo fluorescence be used for quantification of carbon-based primary production in absolute terms?–Arch. Hydrobiol. 160: 515–526, 2004.CrossRefGoogle Scholar
  153. Tsimilli-Michael M., Eggenberg P., Biro B. et al.: Synergistic and antagonistic effects of arbuscular mycorrhizal fungi and Azospirillum and Rhizobium nitrogen-fixers on the photosynthetic activity of alfalfa, probed by the polyphasic chlorophyll a fluorescence transient O-J-I-P.–Appl. Soil Ecol. 15: 169–182, 2000.CrossRefGoogle Scholar
  154. Tsimilli-Michael M., Pêcheux M., Strasser R.J.: Vitality and stress adaptation of the symbionts of coral reef and temperate foraminifers probed in hospite by the fluorescence kinetics OJ-I-P.–Arch. Sci. Genève 51: 1–36, 1998.Google Scholar
  155. Tsimilli-Michael M., Strasser R.J.: In vivo assessment of plants’ vitality: applications in detecting and evaluating the impact of mycorrhization on host plants.–In: Varma A. (ed.): Mycorrhiza: State of the Art. Genetics and Molecular Biology, Eco-Function, Biotechnology, Eco-Physiology, Structure and Systematics, 3rd ed. Pp. 679–703. Springer, Dordrecht 2008.CrossRefGoogle Scholar
  156. van Heerden P.D.R., Strasser R.J., Krüger G.H.J.: Reduction of dark chilling stress in N2-fixing soybean by nitrate as indicated by chlorophyll a fluorescence kinetics.–Physiol. Plantarum 121: 239–249, 2004b.CrossRefGoogle Scholar
  157. van Heerden P.D.R., Tsimilli-Michael M., Krüger G.H.J. et al.: Dark chilling effects on soybean genotypes during vegetative development: Parallel studies of CO2 assimilation, chlorophyll a fluorescence kinetics O-J-I-P and nitrogen fixation.–Physiol. Plantarum 117: 476–491, 2003.CrossRefGoogle Scholar
  158. van Heerden P.D.R., Viljoen M.M., DeVilliers M. et al.: Limitation of photosynthetic carbon metabolism by dark chilling in temperate and tropical soybean genotypes.–Plant Physiol. Biochem. 42: 117–124, 2004a.PubMedCrossRefGoogle Scholar
  159. van Straten G., van Thoor B., van Willegenburg L.G. et al: A ‘big leaf, big fruit, big substrate’ model for experiments on receding horizon optimal control of nutrient supply to greenhouse tomato.–Acta Hortic. 718: 147–155, 2006.CrossRefGoogle Scholar
  160. Volgusheva A., Yakovleva O.V., Kukarskikh G.P. et al.: Performance index in assessing the physiological state of trees in urban ecosystems.–Biophysics 56: 90–95, 2011.CrossRefGoogle Scholar
  161. Wang X.Y., Xu X.M., Cui J.: The importance of blue light for leaf area expansion, development of photosynthetic apparatus, and chloroplast ultrastructure of Cucumis sativus grown under weak light.–Photosynthetica 53: 213–222, 2015.CrossRefGoogle Scholar
  162. Wong D., Govindjee: Effects of lead ions on photosystem I in isolated chloroplasts: Studies on the reaction center P700.–Photosynthetica 10: 241–254, 1976.Google Scholar
  163. Yan K., Chen P., Shao H. et al.: Responses of photosynthesis and photosystem II to higher temperature and salt stress in sorghum.–J. Agron. Crop Sci. 198: 218–226, 2012.CrossRefGoogle Scholar
  164. Yusuf M.A., Kumar D., Rajwanshi R. et al.: Overexpression of gamma-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: Physiological and chlorophyll fluorescence measurements.–Biochim. Biophys. Acta 1797: 1428–1438, 2010.PubMedCrossRefGoogle Scholar
  165. Yusuf M.A., Sarin N.B.: Antioxidant value addition in human diets: genetic transformation of Brassica juncea with γ-TMT gene for increased α-tocopherol content.–Transgenic Res. 16: 109–113, 2007.PubMedCrossRefGoogle Scholar
  166. 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.PubMedCrossRefGoogle Scholar
  167. Zubek S., Stojakowska A., Anielska T. et al.: Arbuscular mycorrhizal fungi alter thymol derivative contents of Inula ensifolia L.–Mycorrhiza 20: 497–504, 2010.PubMedCrossRefGoogle Scholar
  168. Živčák M., Olšovská K., Slamka P. et al.: Measurements of chlorophyll fluorescence in different leaf positions may detect nitrogen deficiency in wheat.–Zemdirbyste-Agriculture 101: 437–443, 2014.CrossRefGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  1. 1.Newport NewsUSA
  2. 2.Department of Biophysics, Center of the Region Haná for Biotechnological and Agricultural Research, Faculty of SciencePalacký UniversityOlomoucCzech Republic
  3. 3.Carl R. Woese Institute for Genomic BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  4. 4.Department of Biochemistry, Department of Plant Biology, and Center of Biophysics and Quantitative BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA

Personalised recommendations