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

  • Kumud B. Mishra
  • 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

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Supplementary material 1 (PDF 806 KB)


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Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Kumud B. Mishra
    • 1
    • 2
  • 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

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