Photosynthesis Research

, Volume 139, Issue 1–3, pp 123–143 | Cite as

Low temperature induced modulation of photosynthetic induction in non-acclimated and cold-acclimated Arabidopsis thaliana: chlorophyll a fluorescence and gas-exchange measurements

  • Kumud B. MishraEmail author
  • Anamika Mishra
  • Jiří Kubásek
  • Otmar Urban
  • Arnd G. Heyer
  • Govindjee
Original Article


Cold acclimation modifies the photosynthetic machinery and enables plants to survive at sub-zero temperatures, whereas in warm habitats, many species suffer even at non-freezing temperatures. We have measured chlorophyll a fluorescence (ChlF) and CO2 assimilation to investigate the effects of cold acclimation, and of low temperatures, on a cold-sensitive Arabidopsis thaliana accession C24. Upon excitation with low intensity (40 µmol photons m− 2 s− 1) ~ 620 nm light, slow (minute range) ChlF transients, at ~ 22 °C, showed two waves in the SMT phase (S, semi steady-state; M, maximum; T, terminal steady-state), whereas CO2 assimilation showed a linear increase with time. Low-temperature treatment (down to − 1.5 °C) strongly modulated the SMT phase and stimulated a peak in the CO2 assimilation induction curve. We show that the SMT phase, at ~ 22 °C, was abolished when measured under high actinic irradiance, or when 3-(3, 4-dichlorophenyl)-1, 1- dimethylurea (DCMU, an inhibitor of electron flow) or methyl viologen (MV, a Photosystem I (PSI) electron acceptor) was added to the system. Our data suggest that stimulation of the SMT wave, at low temperatures, has multiple reasons, which may include changes in both photochemical and biochemical reactions leading to modulations in non-photochemical quenching (NPQ) of the excited state of Chl, “state transitions,” as well as changes in the rate of cyclic electron flow through PSI. Further, we suggest that cold acclimation, in accession C24, promotes “state transition” and protects photosystems by preventing high excitation pressure during low-temperature exposure.


Low-temperature effect Cold acclimation Chlorophyll fluorescence transients Slow SMT fluorescence phase Gas-exchange measurements State transition 3-(3, 4-dichlorophenyl)-1, 1- dimethylurea Methyl viologen 



CO2 assimilation rate


Cold acclimated


Gross CO2 assimilation rate


Maximum CO2 assimilation rate under saturating light

Chl a

Chlorophyll a


Chlorophyll a fluorescence

DCMU (also called diuron)

3-(3, 4-dichlorophenyl)-1, 1- dimethylurea


Maximum fluorescence intensity during actinic light exposure


Maximum fluorescence intensity during dark-relaxation


Fluorescence emission band, with a maximum at 683 nm


Fluorescence emission band, with a maximum at 735 nm


Maximum fluorescence when the (plasto) quinone QA is fully reduced


Minimum fluorescence when QA is fully oxidized


Fluorescence intensity at the P level


Fluorescence intensity at peak M1


Fluorescence intensity at peak M2


Terminal steady-state fluorescence


Maximum variable ChlF (Fm − FO)


Equivalent to maximum quantum yield of PSII photochemistry


Induction state of A at 60 s after illumination, expressed as a percent of Amax


Induction time required to reach 50% of Amax

k (k− 1)

Rate constant (inverse of rate constant) [of the P-to-S phase]


Light-harvesting complexes

M1, M2

First and second maxima after peak P (FP) in the SMT phase of ChlF transient


Methyl viologen




Non-photochemical quenching (of the excited state of Chl a)




Photosystem I


Photosystem II


The first and the second (plasto) quinone acceptors of electrons in the reaction center of PSII


Fluorescence decrease ratio defined as FD/FT, where FD = FP − FT




Slow phase of chlorophyll a fluorescence transient (where S is semi steady-state, M is a maximum and T is terminal steady-state)


Time required to reach P (FP) level


Time required to reach M1 level of ChlF transient


Time required to reach M2 level of ChlF transient


Time required for 50% decline from P (FP) to the S level


pH difference across the thylakoid membrane


Quantum yield of “constitutive” thermal dissipation (d) and fluorescence (f)


Quantum yield of “regulated” non-photochemical quenching


Quantum yield of PSII photochemistry


Quantum yield of “fast” energy (E) dependent quenching


Quantum yield of photoinhibition (I) quenching of Chl fluorescence


Quantum yield of state-transition (T) quenching of Chl fluorescence, during State I (high fluorescence) to State II (low fluorescence)



This work was supported by the Ministry of Education, Youth and Sports of the Czech Republic within the National Sustainability Program I (NPU I), grant number LO1415. The infrastructure used within this research was supported by the project CzeCOS Proces (CZ.02.1.01/0.0/0.0/16_013/0001609). We thank Radek Kaňa (Institute of Microbiology, ASCR, Třeboň, CZ) for providing us the fluorometer used for measuring the 77 K spectra. Govindjee thanks the Schools of Integrative Biology and Molecular and Cell Biology of the University of Illinois at Urbana-Champaign for their support. We are grateful to George C. Papageorgiou for critical reading of an earlier draft of this paper, and for his valuable comments.

Supplementary material

11120_2018_588_MOESM1_ESM.pdf (805 kb)
Supplementary material 1 (PDF 806 KB)


  1. Agati G, Cerovic ZG, Moya I (2000) The effect of decreasing temperature up to chilling values on the in vivo F685/F735 chlorophyll fluorescence ratio in Phaseolus vulgaris and Pisum sativum: the role of the photosystem I contribution to the 735 nm fluorescence band. Photochem Photobiol 72:75–84Google Scholar
  2. Ahn TK, Avenson TJ, Peers G, Li Z, Dall’Osto L, Bassi R, Niyogi KK, Fleming GR (2009) Investigating energy partitioning during photosynthesis using an expanded quantum yield convention. Chem Phys 357:151–158Google Scholar
  3. Allakhverdiev SI, Klimov VV, Carpentier R (1997) Evidence for the involvement of cyclic electron transport in the protection of photosystem II against photoinhibition: influence of a new phenolic compound. Biochemistry 36(14):4149–4154Google Scholar
  4. Allakhverdiev SI, Nishiyama Y, Takahashi S, Miyairi S, Suzuki I, Murata N (2005) Systematic analysis of the relation of electron transport and ATP synthesis to the photodamage and repair of photosystem II in synechocystis. Plant Physiol 137:263–273Google Scholar
  5. Allakhverdiev SI, Los DA, Mohanty P, Nishiyama Y, Murata N (2007) Glycinebetaine alleviates the inhibitory effect of moderate heat stress on the repair of photosystem II during photoinhibition. Biochim Biophys Acta 1767(12):1363–1371Google Scholar
  6. Allen JF (2003) State transitions—a question of balance. Science 299:1530–1532Google Scholar
  7. Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42Google Scholar
  8. Andrizhiyevskaya EG, Chojnicka A, Bautista JA, Diner BA, van Grondelle R, Dekker JP (2005) Origin of the F685 and F695 fluorescence in Photosystem II. Photosynth Res 84:173–180Google Scholar
  9. Aro EM, Hundal T, Carlberg I, Andersson B (1990) In vitro studies on light-induced inhibition of photosystem-II and DI-protein degradation at low-temperatures. Biochim Biophys Acta 1019:269–275Google Scholar
  10. Asada K (1999) The water–water cycle in chloroplasts: scavenging of activeoxygens and dissipation of excess photons. Annu Rev Plant Physiol PlantMol Biol 50:601–639Google Scholar
  11. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113Google Scholar
  12. Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621Google Scholar
  13. Bernacchi CJ, Portis AR, Nakano H, Caemmerer SV, Long SP (2002) Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiol 130(4):1992–1998Google Scholar
  14. Bernát G, Steinbach G, Kaňa R, Govindjee, Misra AN, Prášil O (2018) On the origin of the slow M–T chlorophyll a fluorescence decline in cyanobacteria: interplay of short-term light-responses. Photosynth Res 136(2):183–198Google Scholar
  15. Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physol 31:491–543Google Scholar
  16. Bradbury M, Baker NR (1981) Analysis of the slow phases of the in vivo chlorophyll fluorescence induction curve. Changes in the redox state of Photosystem II electron acceptors and fluorescence emission from Photosystem I and II. Biochim Biophys Acta 635:542–551Google Scholar
  17. Bradbury M, Baker NR (1984) A quantitative determination of photochemical and non-photochemical quenching during the slow phase of the chlorophyll fluorescence induction curve of bean leaves. Biochim Biophys Acta 765:275–281Google Scholar
  18. Briantais JM, Vernotte C, Picaud M, Krause GH (1979) A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim Biophys Acta 548:128–138Google Scholar
  19. Briantais JM, Vernotte C, Picaud M, Krause GH (1980) Chlorophyll fluorescence as a probe for the determination of the photo-induced proton gradient in isolated chloroplasts. Biochim Biophys Acta 591:198–202Google Scholar
  20. Buchanan BB (1991) Regulation of CO2 assimilation in oxygenic photosynthesis: the ferredoxin/thioredoxin system. Perspective on its discovery, present status, and future development. Arch Biochem Biophys 288(1):1–9Google Scholar
  21. Cailly AL, Rizza F, Genty B, Harbinson J (1996) Fate of excitation at PSII in leaves, the non-photochemical side. Plant Physiol Biochem (Special Issue): 86 (abstract)Google Scholar
  22. Catalá R, Medina J, Salinas J (2011) Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proc Natl Acad Sci USA 108(39):16475–16480Google Scholar
  23. Chazdon RL, Pearcy RW (1986) Photosynthetic response to light variation in rainforest species. II Carbon gain and photosynthetic efficiency during lightflecks. Oecologia 69:524–531Google Scholar
  24. Chen J, Kell A, Acharya K, Kupitz C, Fromme P, Jankowiak R (2015) Critical assessment of the emission spectra of various photosystem II core complexes. Photosynth Res 124:253–265Google Scholar
  25. Cook D, Fowler S, Fiehn O, Thomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci USA 101:15243–15248Google Scholar
  26. Crosatti C, Rizza F, Badeck FW, Mazzucotelli E, Cattivelli L (2013) Harden the chloroplast to protect the Plant. Physiol Plant 147:55–63Google Scholar
  27. Demmig-Adams B, Adams WW (2000) Harvesting sunlight safely. Nature 403:371–374Google Scholar
  28. Demmig-Adams B, Grab G, Adams III WW, Govindjee (eds) (2014) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. In: series: advances in photosynthesis and respiration, vol 40. Springer, DordrechtGoogle Scholar
  29. Ehlert B, Hincha DK (2008) Chlorophyll fluorescence imaging accurately quantifies freezing damage and cold acclimation responses in Arabidopsis leaves. Plant Methods 4:12Google Scholar
  30. Endo T, Kawase D, Sato F (2005) Stromal over-reduction by high-light stress as measured by decreases in P700 oxidation by far-red light and its physiological relevance. Plant Cell Physiol 46(5):775–781Google Scholar
  31. Ensminger I, Busch F, Huner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44Google Scholar
  32. Fork DC, Satoh K (1986) The control by state transitions of the distribution of excitation energy in photosynthesis. Annu Rev Plant Physiol 37:335–361Google Scholar
  33. Franck F, Juneau P, Popovic R (2002) Resolution of the photosystem I and photosystem II contributions to chlorophyll fluorescence of intact leaves at room temperature. Biochim Biophys Acta 1556:239–246Google Scholar
  34. Franklin KA. Whitelam GC (2007) Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat Genet 39:1410–1413Google Scholar
  35. Furbank RT, Walker DA (1986) Chlorophyll a fluorescence as a quantitative probe of photosynthesis: Effects of Co2 concentration during gas transients on chlorophyll fluorescence in spinach leaves. New Phytol 104:207–213Google Scholar
  36. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92Google Scholar
  37. Goltsev VN, Kalaji HM, Paunov M, Bąba W, Horaczek T, Mojski J, Kociel H, Allakhverdieve SI (2016) Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic Apparatus. Russ J Plant Physiol 63(6):869–893Google Scholar
  38. Govindjee (1995) Sixty three years since Kautsky—Chlorophyll a fluorescence. Aust J Plant Physiol 22(2):131–160Google Scholar
  39. Govindjee, Spilotro P (2002) An Arabidopsis thaliana mutant, altered in the γ-sub-unit of ATP synthase, has a different pattern of intensity-dependent changes in non-photochemical quenching and kinetics of the P-to-S fluorescence decay. Funct Plant Biol 29:425–434Google Scholar
  40. Govindjee, Yang L (1966) Structure of the red fluorescence band in chloroplasts. J Gen Physiol 49:763–780Google Scholar
  41. Govindjee, Amesz J, Fork DC (eds) (1986) Light emission by plants and bacteria. Academic Press, New YorkGoogle Scholar
  42. Guadagno CR, Virzo De Santo A, D’Ambrosio N (2010) A revised energy partitioningapproach to assess the yields of non-photochemical quenching components. Biochim Biophys Acta 1797:525–530Google Scholar
  43. Gururani MA, Venkatesh J, Ganesan M, Strasser RJ, Han Y, Kim JI, Lee HY, Song PS (2015) In vivo assessment of cold tolerance through chlorophyll a fluorescence in transgenic Zoysiagrass expressing mutant phytochrome A. PLoS ONE 10(5):e0127200Google Scholar
  44. Guy CL (1990) Cold acclimation and freezing stress tolerance: Role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 4:187–223Google Scholar
  45. Hacker J, Spindelbock JP, Neuner G (2008) Mesophyll freezing and effects of freeze dehydration visualized by simultaneous measurement of IDTA and differential imaging chlorophyll fluorescence. Plant Cell Environ 31:1725–1733Google Scholar
  46. Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK (2006) Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol 142:98–112Google Scholar
  47. Hasdai M, Weiss B, Levi A, Samach A, Porat R (2006) Differential responses of Arabidopsis ecotypes to cold, chilling and freezing temperatures. Ann Appl Biol 148:113–120Google Scholar
  48. Hendrickson L, Furbank RT, Chow WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res 82:73–81Google Scholar
  49. Hikosaka K, Ishikawa K, Borjigidai A, Muller O, Onoda Y (2006) Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rates. J Exp Bot 57:291–302Google Scholar
  50. Holub O, Seufferheld MJ, Gohlke C, Govindjee, Heiss GJ, Clegg RM (2007) Fluorescence lifetime imaging microscopy of Chlamydomonas reinhardtii: non-photochemical quenching mutants and the effect of photosynthetic inhibitors on the slow chlorophyll fluorescence transient. J Microsc 226:90–120Google Scholar
  51. Horton P (2012) Optimization of light harvesting and photoprotection: molecular mechanisms and physiological consequences. Phil Trans R Soc B 367:3455–3465Google Scholar
  52. Humplík JF, Lazár D, Fürst T, Husičková A, Hýbl M, Spíchal L (2015) Automated integrative high-throughput phenotyping of plant shoots: a case study of the cold-tolerance of pea (Pisum sativum L.). Plant Methods 11:20Google Scholar
  53. Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230Google Scholar
  54. Joliot P, Johnson GN (2011) Regulation of cyclic and linear electron flow in higher plants. Proc Natl Acad Sci USA 108:13317–13322Google Scholar
  55. Joliot P, Joliot A (2002) Cyclic electron transfer in plant leaf. Proc Natl Acad Sci USA 99(15):10209–10214Google Scholar
  56. Joliot P, Joliot A (2006) Cyclic electron flow in C3 plants. Biochim Biophys Acta 1757:362–368Google Scholar
  57. Kalaji HM, Goltsev V, Bosa K, Allakhverdiev SI, Strasser RJ, Govindjee (2012) Experimental in vivo measurements of light emission in plants: A perspective dedicated to David Walker. Photosynth Res 114:69–96Google Scholar
  58. Kaňa R, Govindjee (2016) Role of ions in the regulation of light-harvesting. Front Plant Sci 7:1849Google Scholar
  59. Kaňa R, Kotabová E, Komárek O, Šedivá B, Papageorgiou GC, Govindjee, Prášil O (2012) The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. Biochim Biophys Acta 1817:1237–1247Google Scholar
  60. Khanal N, Bray G, Grisnich A, Moffatt B, Gray G (2017) Differential mechanisms of photosynthetic acclimation to light and low temperature in Arabidopsis and the extremophile Eutrema salsugineum. Plants. Google Scholar
  61. Knaupp M, Mishra KB, Nedbal L, Heyer AG (2011) Evidence for a role of raffinose in stabilizing photosystem II during freeze-thaw cycles. Planta 234:477–486Google Scholar
  62. Kodru S, Malavath T, Devadasu E, Nellaepalli S, Subramanyam R, Govindjee (2015) The slow S to M rise of chlorophyII a fluorescence induction reflects transition from state 2 to state 1 in the green alga Chlamydomonas reinhardtii. Photosynth Res 125:219–231Google Scholar
  63. Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78Google Scholar
  64. Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218Google Scholar
  65. Lamb JJ, Rokke G, Hohmann-Marriott MF (2018) Chlorophyll fluorescence emission spectroscopy of oxygenic organisms at 77 K. Photosynthetica 56(1):105–124Google Scholar
  66. Lazár D (1999) Chlorophyll a fluorescence induction. Biochim Biophys Acta 1412:1–28Google Scholar
  67. Lazár D (2015) Parameters of photosynthetic energy partitioning. J Plant Physiol 175:131–147Google Scholar
  68. Leegood RC, Edwards GE (1996) Carbon metabolism and photorespiration: temperature dependence in relation to other environmental factors. In: Baker NR (ed) Photosynthesis and the environment. Kluwer Academic Publishers, Dordrecht, pp 191–221Google Scholar
  69. Lukas V, Mishra A, Mishra KB, Hajslova J (2013) Mass spectrometry-based metabolomic fingerprinting for screening cold tolerance in Arabidopsis thaliana accessions. Anal Bioanal Chem 405(8):2671–2683Google Scholar
  70. Malenovský Z, Mishra KB, Zemek F, Rascher U, Nedbal L (2009) Scientific and technical challenges in remote sensing of plant canopy reflectance and fluorescence. J Exp Bot 60:2987–3004Google Scholar
  71. Marečková M, Barták M (2016) Effects of short-term low temperature stress on chlorophyll fluorescence transients in Antarctic lichen species. Czech Polar Reports 6(1):54–65Google Scholar
  72. Martindale W, Leegood RC (1997) Acclimation of photosynthesis to low temperature in Spinacia oleracea L.II. Effects of nitrogen supply. J Exp Bot 48:1873–1880Google Scholar
  73. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668Google Scholar
  74. Mishra A, Mishra KB, Höermiller II, Heyer AG, Nedbal L (2011) Chlorophyll fluorescence emission as a reporter on cold tolerance in Arabidopsis thaliana accessions. Plant Signal Behav 6:301–310Google Scholar
  75. Mishra A, Heyer AG, Mishra KB (2014) Chlorophyll fluorescence emission can screen cold tolerance of cold acclimated Arabidopsis thaliana accessions. Plant Methods 10:38Google Scholar
  76. Mishra A, Hájek J, Tuháčková T, Barták M, Mishra KB (2015) Features of chlorophyll fluorescence transients can be used to investigate low temperature induced effects on photosystem II of algal lichens from polar regions. Czech Polar Reports 5(1):99–111Google Scholar
  77. Mishra KB, Mishra A, Klem K, Govindjee (2016a) Plant phenotyping: A perspective. Indian J Plant Physiol 21(4):514–527Google Scholar
  78. Mishra KB, Mishra A, Novotná K, Rapantová B, Hodaňová P, Urban O, Klem K (2016b) Chlorophyll a fluorescence, under half of the adaptive growth-irradiance, for high-throughput sensing of leaf-water deficit in Arabidopsis thaliana accessions. Plant Methods 12:46Google Scholar
  79. Mohanty P, Govindjee (1974) The slow decline and subsequent rise of chlorophyll fluorescence transients in intact algal cells. Plant Biochem J 1:78–106Google Scholar
  80. Mohanty P, Papageorgiou GC, Govindjee (1971) Fluorescence induction in the red alga Porphyridium cruentum. Photochem Photobiol 14:667–682Google Scholar
  81. Mohanty P, Suleyman IA, Murata N (2007) Application of low temperatures during photoinhibition allows characterization of individual steps in photodamage and the repair of photosystem II. Photosynth Res 94:217–224Google Scholar
  82. Müller P, Li XP, Niyogi K (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566Google Scholar
  83. Munday JC, Govindjee (1969) Light-induced changes in the fluorescence yield of chlorophyll a in vivo: III. The dip and peak in the fluorescence transient of Chlorella pyrenoidosa. Biophys 9:1–21Google Scholar
  84. Murchie EH, Niyogi KK (2011) Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 155:86–92Google Scholar
  85. Öquist G, Greer DH, Ögren E (1987) Light stress at low temperature. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Topics in Photosynthesis. Elsevier, Amsterdam, pp 67–87Google Scholar
  86. Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis? Curr Opin Plant Biol 5:193–198Google Scholar
  87. Ort DR, Merchant SS, Alric J, Barkan A, Blankenshiph RE et al (2015) Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc Natl Acad Sci USA 112(28):8529–8536Google Scholar
  88. Oxborough K (2004) Imaging of chlorophyll a fluorescence: theoretical and practical aspects of an emerging technique for the monitoring of photosynthetic performance. J Exp Bot 55:1195–1205Google Scholar
  89. Pandey JK, Gopal R (2012) Dimethoate-induced slow S to M chlorophyll a fluorescence transient in wheat plants. Photosynthetica 50:630–634Google Scholar
  90. Papageorgiou GC, Govindjee (1968a) Light-induced changes in the fluorescence yield of chlorophyll a in vivo I. Anacystis nidulans. Biophys J 8:1299–1315Google Scholar
  91. Papageorgiou GC, Govindjee (1968b) Light-induced changes in the fluorescence yield of chlorophyll a in vivo. II. Chlorella pyrenoidosa. Biophys J 8:1316–1328Google Scholar
  92. Papageorgiou GC, Govindjee (eds) (2004) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in Photosynthesis and Respiration, vol 19. Springer, DordrechtGoogle Scholar
  93. Papageorgiou GC, Govindjee (2011) Photosynthesis II fluorescence: slow changes-scaling from the past. J Photochem Photobiol B 104:258–270Google Scholar
  94. Papageorgiou GC, Tsimilli-Michael M, Stamatakis K (2007) The fast and slow kinetics of chlorophyll a fluorescence induction in plants, algae and cyanobacteria: A viewpoint. Photosynth Res 94:275–290Google Scholar
  95. Pospíšil P, Skotnica J, Nauš J (1998) Low and high temperature dependence of minimum F-O and maximum F-M chlorophyll fluorescence in vivo. Biochim Biophys Acta 1363:95–99Google Scholar
  96. Roháček K (2010) Method for resolution and quantification of components of the non-photochemical quenching (qN). Photosynth Res 105:101–113Google Scholar
  97. Roháček K, Soukupova J, Bartak M (2008) Chlorophyll fluorescence: A wonderful tool to study plant physiology and plant stress. Plant Cell Compartments– Selected Topics, Editor: Benoit Schoefs. Chapter 3: 41–104. Research Signpost, Trivandrum, India. ISBN: 978-81-308-0104-9Google Scholar
  98. Ruban AV, Berera R, Ilioaia C, Van Stokkum IH, Kennis JT, Pascal AA, Van Amerongen H, Robert B, Horton P, Van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–578Google Scholar
  99. Sage RF, Kubien DS (2007) The temperature response of C-3 and C-4 photosynthesis. Plant Cell Environ 30:1086–1106Google Scholar
  100. Sane PV, Ivanov AG, Hurry V, Huner NP, Oquist G (2003) Changes in the redox potential of primary and secondary electron-accepting quinones in photosystem II confer increased resistance to photoinhibition in low-temperature-acclimated Arabidopsis. Plant Physiol 132(4):2144–2151Google Scholar
  101. Savitch LV, Gray GR, Huner NPA (1997) Feedback-limited photosynthesis and regulation of sucrose-starch accumulation during cold acclimation and low temperattre stress in a spring and winter wheat. Planta 201:18–26Google Scholar
  102. Schmid KJ, Sorensen TR, Stracke R, Torjek O, Altmann T, Mitchell-Olds T, Weisshaar B (2003) Large-scale identification and analysis of genome-wide single-nucleotide polymorphisms for mapping in Arabidopsis thaliana. Genome Res 13:1250–1257Google Scholar
  103. Seaton GGR, Walker DA (1990) Chlorophyll fluorescence as a measure of photosynthetic carbon assimilation. Proc Royal Soc: Biol Sci 242(1303):29–35Google Scholar
  104. Shikanai T (2007) Cyclic electron transport around photosystem I:genetic approaches. Annu Rev Plant Biol 58:199–217Google Scholar
  105. Sivak MN, Dietz J-J, Heber U, Walker DA (1985a) The relationship between light-scattering and chlorophyll a fluorescence during oscillation in photosynthesis carbon assimilation. Arch Biochem Biophys 237:513–519Google Scholar
  106. Sivak MN, Heber U, Walker DA (1985b) Chlorophyll a fluorescence and light-scattering displayed be leaves during induction of photosynthesis. Planta 163:419–423Google Scholar
  107. Smallwood M, Bowles DJ (2002) Plants in a cold climate. Philos Trans Roy Soc B 357:831–846Google Scholar
  108. Stirbet A, Govindjee (2011) 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: Biol 104:236–257Google Scholar
  109. Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: A personal perspective of the thermal phase, the J-I-P rise. Photosynth Res 113:15–61Google Scholar
  110. Stirbet A, Govindjee (2016) The slow phase of chlorophyll a fluorescence induction in silico: Origin of the S-M fluorescence rise. Photosynth Res 130:193–213Google Scholar
  111. Stirbet A, Lazár D, Kromdijk G (2018) Chlorophyll a fluorescence induction: Can just a one-second measurement be used to quantify abiotic stress responses? Photosynthetica 56(1):86–104Google Scholar
  112. Strand Å, Hurry V, Henkes S, Huner N, Gustafsson P, Gardeström P, Stitt M (1999) Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin Cycle and in the sucrose-biosynthesis pathway. Plant Physiol 119:1387–1397Google Scholar
  113. Strasser RJ, Srivastava A, Govindjee (1995a) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42Google Scholar
  114. Strasser RJ, Srivastava A, Govindjee (1995b) Polyphasic chlorophyll a fluorescence transient in plants and cynobecteria. Photochem Photobiol 61:32–42Google Scholar
  115. Telfer A, Nicolson J, Barber J (1976) Cation control of chloroplast structure and chlorophyll afluorescence yield and its relevance to the intact chloroplast. FEBS Lett 65(1):77–83Google Scholar
  116. Thomashow MF (2010) Molecular basis of plant cold acclimation: insight gained from studying the CBF cold response pathway 1. Plant Physiol 154:571–577Google Scholar
  117. Tóth SZ, Schansker G, Strasser RJ (2007) A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient. Photosynth Res 93:193–203Google Scholar
  118. Triantaphylidès C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14(4):219–228Google Scholar
  119. Tyystjärvi E (2013) Photoinhibition of photosystem II. Int Rev Cell Mol Biol 300:243–303Google Scholar
  120. Tyystjärvi E, Aro E-M (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc Natl Acad Sci USA 93:2213–2218Google Scholar
  121. Urban O, Sprtova M, Kosvancova M, Tomaskova I, Lichtenthaler HK, Marek MV (2008) Comparison of photosynthetic induction and transient limitations during the induction phase in young and mature leaves from three poplar clones. Tree Physiol 28:1189–1197Google Scholar
  122. Walker DA (1981) Secondary fluorescence kinetics of spinach leaves in relation to the onset of photosynthetic carbon assimilation. Planta 153:273–278Google Scholar
  123. Walters RG, Horton P (1991) Resolution of components of non-photochemical chlorophyll fluorescence quenching in barley leaves. Photosynth Res 27:121–133Google Scholar
  124. Walters RG, Ruban AV, Horton P (1996) Identification of proton-active residues in a higher plant light-harvesting complex. Proc Natl Acad Sci USA 93:14204–14209Google Scholar
  125. Wanner LA, Junttila O (1999) Cold-induced freezing tolerance in Arabidopsis. Plant Physiol 120:391–399Google Scholar
  126. Yamagishi A, Satoh K, Katoh S (1978) Fluorescence induction in chloroplasts isolated from the green alga Bryopsis maxima. III. A fluorescence transient indicating proton gradient across the thylakoid membrane. Plant Cell Physiol 19:17–25Google Scholar
  127. Yun JG, Hayashi T, Yazawa S, Yasuda Y, Katoh T (1997) Degradation of photosynthetic activity of Saintpaulia leaf by sudden temperature drop. Plant Sci 127:25–38Google Scholar
  128. Zhang S, Scheller HV (2002) Photoinhibition of Photosystem I at chilling temperature and subsequent recovery in Arabidopsis thaliana. Plant Cell Physiol 45:1595–1602Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Kumud B. Mishra
    • 1
    • 2
    Email author
  • Anamika Mishra
    • 1
  • Jiří Kubásek
    • 1
  • Otmar Urban
    • 1
  • Arnd G. Heyer
    • 3
  • Govindjee
    • 4
  1. 1.Global Change Research InstituteCzech Academy of SciencesBrnoCzech Republic
  2. 2.Department of Experimental BiologyMasaryk UniversityBrnoCzech Republic
  3. 3.Department of Plant Biotechnology, Institute of Biomaterials and Biomolecular SystemsUniversity of StuttgartStuttgartGermany
  4. 4.Department of Plant Biology, Department of Biochemistry and Center for Biophysics and Quantitative BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA

Personalised recommendations