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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
  • 182 Downloads

Abstract

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.

Keywords

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 

Abbreviations

A

CO2 assimilation rate

AC

Cold acclimated

Agross

Gross CO2 assimilation rate

Amax

Maximum CO2 assimilation rate under saturating light

Chl a

Chlorophyll a

ChlF

Chlorophyll a fluorescence

DCMU (also called diuron)

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

Fm

Maximum fluorescence intensity during actinic light exposure

F′′m(t)

Maximum fluorescence intensity during dark-relaxation

F683

Fluorescence emission band, with a maximum at 683 nm

F735

Fluorescence emission band, with a maximum at 735 nm

Fm

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

FO

Minimum fluorescence when QA is fully oxidized

FP

Fluorescence intensity at the P level

FM1

Fluorescence intensity at peak M1

FM2

Fluorescence intensity at peak M2

FT

Terminal steady-state fluorescence

Fv

Maximum variable ChlF (Fm − FO)

Fv/Fm

Equivalent to maximum quantum yield of PSII photochemistry

IS60

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

IT50

Induction time required to reach 50% of Amax

k (k− 1)

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

LHCs

Light-harvesting complexes

M1, M2

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

MV

Methyl viologen

NAC

Non-acclimated

NPQ

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

PQ

Plastoquinone

PSI

Photosystem I

PSII

Photosystem II

QA, QB

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

RFD

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

RuBP

Ribulose-1,5-bisphosphate

SMT

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

tFp

Time required to reach P (FP) level

tM1

Time required to reach M1 level of ChlF transient

tM2

Time required to reach M2 level of ChlF transient

t50

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

ΔpH 

pH difference across the thylakoid membrane

Φf,d

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

ΦNPQ

Quantum yield of “regulated” non-photochemical quenching

ΦPSII

Quantum yield of PSII photochemistry

ΦqE

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

ΦqI

Quantum yield of photoinhibition (I) quenching of Chl fluorescence

ΦqT

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

Notes

Acknowledgements

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)

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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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