Skip to main content
SpringerLink
Log in

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

  • Original Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

A :

CO2 assimilation rate

AC:

Cold acclimated

A gross :

Gross CO2 assimilation rate

A max :

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

F′m :

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

F m :

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

F O :

Minimum fluorescence when QA is fully oxidized

F P :

Fluorescence intensity at the P level

F M 1 :

Fluorescence intensity at peak M1

F M 2 :

Fluorescence intensity at peak M2

F T :

Terminal steady-state fluorescence

F v :

Maximum variable ChlF (Fm − FO)

F v/F m :

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

Q A, Q B :

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

R FD :

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)

t Fp :

Time required to reach P (FP) level

t M1 :

Time required to reach M1 level of ChlF transient

t M2 :

Time required to reach M2 level of ChlF transient

t 50 :

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)

References

  • 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 72:75–84

    Article  CAS  PubMed  Google Scholar 

  • 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 357:151–158

    Article  CAS  Google Scholar 

  • 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):4149–4154

    Article  CAS  PubMed  Google Scholar 

  • 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 137:263–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):1363–1371

    Article  CAS  PubMed  Google Scholar 

  • Allen JF (2003) State transitions—a question of balance. Science 299:1530–1532

    Article  CAS  PubMed  Google Scholar 

  • Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42

    Article  CAS  PubMed  Google Scholar 

  • 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 84:173–180

    Article  CAS  PubMed  Google Scholar 

  • 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 1019:269–275

    Article  CAS  Google Scholar 

  • Asada K (1999) The water–water cycle in chloroplasts: scavenging of activeoxygens and dissipation of excess photons. Annu Rev Plant Physiol PlantMol Biol 50:601–639

    Article  CAS  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  CAS  PubMed  Google Scholar 

  • Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621

    Article  CAS  PubMed  Google Scholar 

  • 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):1992–1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):183–198

    Article  CAS  PubMed  Google Scholar 

  • Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physol 31:491–543

    Article  Google Scholar 

  • 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 635:542–551

    Article  CAS  PubMed  Google Scholar 

  • 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 765:275–281

    Article  CAS  Google Scholar 

  • 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 548:128–138

    Article  CAS  PubMed  Google Scholar 

  • 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 591:198–202

    Article  CAS  PubMed  Google Scholar 

  • 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):1–9

    Article  CAS  PubMed  Google Scholar 

  • 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)

  • 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):16475–16480

    Article  PubMed  Google Scholar 

  • Chazdon RL, Pearcy RW (1986) Photosynthetic response to light variation in rainforest species. II Carbon gain and photosynthetic efficiency during lightflecks. Oecologia 69:524–531

    Article  PubMed  Google Scholar 

  • 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 124:253–265

    Article  CAS  PubMed  Google Scholar 

  • 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 101:15243–15248

    Article  CAS  PubMed  Google Scholar 

  • Crosatti C, Rizza F, Badeck FW, Mazzucotelli E, Cattivelli L (2013) Harden the chloroplast to protect the Plant. Physiol Plant 147:55–63

    Article  CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Adams WW (2000) Harvesting sunlight safely. Nature 403:371–374

    Article  CAS  PubMed  Google Scholar 

  • 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, Dordrecht

  • Ehlert B, Hincha DK (2008) Chlorophyll fluorescence imaging accurately quantifies freezing damage and cold acclimation responses in Arabidopsis leaves. Plant Methods 4:12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):775–781

    Article  CAS  PubMed  Google Scholar 

  • Ensminger I, Busch F, Huner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44

    Article  CAS  Google Scholar 

  • Fork DC, Satoh K (1986) The control by state transitions of the distribution of excitation energy in photosynthesis. Annu Rev Plant Physiol 37:335–361

    Article  CAS  Google Scholar 

  • 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 1556:239–246

    Article  CAS  PubMed  Google Scholar 

  • Franklin KA. Whitelam GC (2007) Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat Genet 39:1410–1413

    Article  CAS  PubMed  Google Scholar 

  • 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 104:207–213

    Article  CAS  Google Scholar 

  • 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 990:87–92

    Article  CAS  Google Scholar 

  • 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):869–893

    Article  CAS  Google Scholar 

  • Govindjee (1995) Sixty three years since Kautsky—Chlorophyll a fluorescence. Aust J Plant Physiol 22(2):131–160

    CAS  Google Scholar 

  • 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 29:425–434

    Article  CAS  Google Scholar 

  • Govindjee, Yang L (1966) Structure of the red fluorescence band in chloroplasts. J Gen Physiol 49:763–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Govindjee, Amesz J, Fork DC (eds) (1986) Light emission by plants and bacteria. Academic Press, New York

    Google Scholar 

  • 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 1797:525–530

    Article  CAS  PubMed  Google Scholar 

  • 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):e0127200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guy CL (1990) Cold acclimation and freezing stress tolerance: Role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 4:187–223

    Article  Google Scholar 

  • 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 31:1725–1733

    Article  CAS  PubMed  Google Scholar 

  • Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK (2006) Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol 142:98–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 148:113–120

    Article  Google Scholar 

  • Hendrickson L, Furbank RT, Chow WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res 82:73–81

    Article  CAS  PubMed  Google Scholar 

  • 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 57:291–302

    Article  CAS  PubMed  Google Scholar 

  • 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 226:90–120

    Article  CAS  PubMed  Google Scholar 

  • Horton P (2012) Optimization of light harvesting and photoprotection: molecular mechanisms and physiological consequences. Phil Trans R Soc B 367:3455–3465

    Article  CAS  PubMed  Google Scholar 

  • 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 11:20

    Article  PubMed  PubMed Central  Google Scholar 

  • Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230

    Article  Google Scholar 

  • Joliot P, Johnson GN (2011) Regulation of cyclic and linear electron flow in higher plants. Proc Natl Acad Sci USA 108:13317–13322

    Article  PubMed  Google Scholar 

  • Joliot P, Joliot A (2002) Cyclic electron transfer in plant leaf. Proc Natl Acad Sci USA 99(15):10209–10214

    Article  CAS  PubMed  Google Scholar 

  • Joliot P, Joliot A (2006) Cyclic electron flow in C3 plants. Biochim Biophys Acta 1757:362–368

    Article  CAS  PubMed  Google Scholar 

  • 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 114:69–96

    Article  CAS  PubMed  Google Scholar 

  • Kaňa R, Govindjee (2016) Role of ions in the regulation of light-harvesting. Front Plant Sci 7:1849

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 1817:1237–1247

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.3390/plants6030032

    Article  PubMed  PubMed Central  Google Scholar 

  • Knaupp M, Mishra KB, Nedbal L, Heyer AG (2011) Evidence for a role of raffinose in stabilizing photosystem II during freeze-thaw cycles. Planta 234:477–486

    Article  CAS  PubMed  Google Scholar 

  • 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 125:219–231

    Article  CAS  PubMed  Google Scholar 

  • Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78

    Article  CAS  Google Scholar 

  • 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 79:209–218

    Article  CAS  PubMed  Google Scholar 

  • Lamb JJ, Rokke G, Hohmann-Marriott MF (2018) Chlorophyll fluorescence emission spectroscopy of oxygenic organisms at 77 K. Photosynthetica 56(1):105–124

    Article  CAS  Google Scholar 

  • Lazár D (1999) Chlorophyll a fluorescence induction. Biochim Biophys Acta 1412:1–28

    Article  PubMed  Google Scholar 

  • Lazár D (2015) Parameters of photosynthetic energy partitioning. J Plant Physiol 175:131–147

    Article  CAS  PubMed  Google Scholar 

  • 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 191–221

    Google Scholar 

  • 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):2671–2683

    Article  CAS  Google Scholar 

  • 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 60:2987–3004

    Article  CAS  PubMed  Google Scholar 

  • 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):54–65

    Article  Google Scholar 

  • Martindale W, Leegood RC (1997) Acclimation of photosynthesis to low temperature in Spinacia oleracea L.II. Effects of nitrogen supply. J Exp Bot 48:1873–1880

    Article  CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • 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 6:301–310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mishra A, Heyer AG, Mishra KB (2014) Chlorophyll fluorescence emission can screen cold tolerance of cold acclimated Arabidopsis thaliana accessions. Plant Methods 10:38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):99–111

    Article  Google Scholar 

  • Mishra KB, Mishra A, Klem K, Govindjee (2016a) Plant phenotyping: A perspective. Indian J Plant Physiol 21(4):514–527

    Article  Google Scholar 

  • 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 12:46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohanty P, Govindjee (1974) The slow decline and subsequent rise of chlorophyll fluorescence transients in intact algal cells. Plant Biochem J 1:78–106

    CAS  Google Scholar 

  • Mohanty P, Papageorgiou GC, Govindjee (1971) Fluorescence induction in the red alga Porphyridium cruentum. Photochem Photobiol 14:667–682

    Article  CAS  Google Scholar 

  • 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 94:217–224

    Article  CAS  PubMed  Google Scholar 

  • Müller P, Li XP, Niyogi K (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 9:1–21

    Article  CAS  Google Scholar 

  • Murchie EH, Niyogi KK (2011) Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 155:86–92

    Article  CAS  PubMed  Google Scholar 

  • 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 67–87

    Google Scholar 

  • Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis? Curr Opin Plant Biol 5:193–198

    Article  CAS  Google Scholar 

  • 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):8529–8536

    Article  CAS  PubMed  Google Scholar 

  • 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 55:1195–1205

    Article  CAS  PubMed  Google Scholar 

  • Pandey JK, Gopal R (2012) Dimethoate-induced slow S to M chlorophyll a fluorescence transient in wheat plants. Photosynthetica 50:630–634

    Article  CAS  Google Scholar 

  • Papageorgiou GC, Govindjee (1968a) Light-induced changes in the fluorescence yield of chlorophyll a in vivo I. Anacystis nidulans. Biophys J 8:1299–1315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papageorgiou GC, Govindjee (1968b) Light-induced changes in the fluorescence yield of chlorophyll a in vivo. II. Chlorella pyrenoidosa. Biophys J 8:1316–1328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papageorgiou GC, Govindjee (eds) (2004) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in Photosynthesis and Respiration, vol 19. Springer, Dordrecht

    Google Scholar 

  • Papageorgiou GC, Govindjee (2011) Photosynthesis II fluorescence: slow changes-scaling from the past. J Photochem Photobiol B 104:258–270

    Article  CAS  PubMed  Google Scholar 

  • 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 94:275–290

    Article  CAS  PubMed  Google Scholar 

  • 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 1363:95–99

    Article  PubMed  Google Scholar 

  • Roháček K (2010) Method for resolution and quantification of components of the non-photochemical quenching (qN). Photosynth Res 105:101–113

    Article  CAS  PubMed  Google Scholar 

  • 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: 978-81-308-0104-9

  • 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 450:575–578

    Article  CAS  PubMed  Google Scholar 

  • Sage RF, Kubien DS (2007) The temperature response of C-3 and C-4 photosynthesis. Plant Cell Environ 30:1086–1106

    Article  CAS  PubMed  Google Scholar 

  • 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):2144–2151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 201:18–26

    Article  CAS  Google Scholar 

  • 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 13:1250–1257

    Article  PubMed  PubMed Central  Google Scholar 

  • Seaton GGR, Walker DA (1990) Chlorophyll fluorescence as a measure of photosynthetic carbon assimilation. Proc Royal Soc: Biol Sci 242(1303):29–35

    Article  Google Scholar 

  • Shikanai T (2007) Cyclic electron transport around photosystem I:genetic approaches. Annu Rev Plant Biol 58:199–217

    Article  CAS  PubMed  Google Scholar 

  • 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 237:513–519

    Article  CAS  PubMed  Google Scholar 

  • Sivak MN, Heber U, Walker DA (1985b) Chlorophyll a fluorescence and light-scattering displayed be leaves during induction of photosynthesis. Planta 163:419–423

    Article  CAS  PubMed  Google Scholar 

  • Smallwood M, Bowles DJ (2002) Plants in a cold climate. Philos Trans Roy Soc B 357:831–846

    Article  CAS  Google Scholar 

  • 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 104:236–257

    Article  CAS  Google Scholar 

  • Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: A personal perspective of the thermal phase, the J-I-P rise. Photosynth Res 113:15–61

    Article  CAS  PubMed  Google Scholar 

  • Stirbet A, Govindjee (2016) The slow phase of chlorophyll a fluorescence induction in silico: Origin of the S-M fluorescence rise. Photosynth Res 130:193–213

    Article  CAS  PubMed  Google Scholar 

  • 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):86–104

    Article  CAS  Google Scholar 

  • 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 119:1387–1397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strasser RJ, Srivastava A, Govindjee (1995a) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42

    Article  CAS  Google Scholar 

  • Strasser RJ, Srivastava A, Govindjee (1995b) Polyphasic chlorophyll a fluorescence transient in plants and cynobecteria. Photochem Photobiol 61:32–42

    Article  CAS  Google Scholar 

  • 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):77–83

    Article  CAS  Google Scholar 

  • Thomashow MF (2010) Molecular basis of plant cold acclimation: insight gained from studying the CBF cold response pathway 1. Plant Physiol 154:571–577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tóth SZ, Schansker G, Strasser RJ (2007) A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient. Photosynth Res 93:193–203

    Article  CAS  PubMed  Google Scholar 

  • Triantaphylidès C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14(4):219–228

    Article  CAS  PubMed  Google Scholar 

  • Tyystjärvi E (2013) Photoinhibition of photosystem II. Int Rev Cell Mol Biol 300:243–303

    Article  CAS  PubMed  Google Scholar 

  • 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 93:2213–2218

    Article  PubMed  Google Scholar 

  • 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 28:1189–1197

    Article  CAS  PubMed  Google Scholar 

  • Walker DA (1981) Secondary fluorescence kinetics of spinach leaves in relation to the onset of photosynthetic carbon assimilation. Planta 153:273–278

    Article  CAS  PubMed  Google Scholar 

  • Walters RG, Horton P (1991) Resolution of components of non-photochemical chlorophyll fluorescence quenching in barley leaves. Photosynth Res 27:121–133

    Article  CAS  PubMed  Google Scholar 

  • Walters RG, Ruban AV, Horton P (1996) Identification of proton-active residues in a higher plant light-harvesting complex. Proc Natl Acad Sci USA 93:14204–14209

    Article  CAS  PubMed  Google Scholar 

  • Wanner LA, Junttila O (1999) Cold-induced freezing tolerance in Arabidopsis. Plant Physiol 120:391–399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 19:17–25

    CAS  Google Scholar 

  • Yun JG, Hayashi T, Yazawa S, Yasuda Y, Katoh T (1997) Degradation of photosynthetic activity of Saintpaulia leaf by sudden temperature drop. Plant Sci 127:25–38

    Article  CAS  Google Scholar 

  • Zhang S, Scheller HV (2002) Photoinhibition of Photosystem I at chilling temperature and subsequent recovery in Arabidopsis thaliana. Plant Cell Physiol 45:1595–1602

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Global Change Research Institute, Czech Academy of Sciences, Bělidla 986/4a, 603 00, Brno, Czech Republic

    Kumud B. Mishra, Anamika Mishra, Jiří Kubásek & Otmar Urban

  2. Department of Experimental Biology, Masaryk University, Kamenice 5, 625 00, Brno, Czech Republic

    Kumud B. Mishra

  3. Department of Plant Biotechnology, Institute of Biomaterials and Biomolecular Systems, University of Stuttgart, Pfaffenwaldring 57, 70567, Stuttgart, Germany

    Arnd G. Heyer

  4. Department of Plant Biology, Department of Biochemistry and Center for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Govindjee

Authors
  1. Kumud B. Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anamika Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiří Kubásek
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Otmar Urban
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Arnd G. Heyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Govindjee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kumud B. Mishra.

Additional information

Five of us (KBM, AM, JK, OU, and AGH) pay tribute to three pioneers of Photosynthesis Research, Agepati S. Raghavendra (carbon reactions, specifically for C4 photosynthesis), William A. Cramer (bioenergetics, specifically for biochemistry and biophysics of cytochromes), and Govindjee (primary photochemistry and electron transport, specifically for the unique role of bicarbonate in Photosystem II; also a co-author of this manuscript), for their contributions and commendable leadership in photosynthesis research.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 806 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mishra, K.B., Mishra, A., Kubásek, J. et al. Low temperature induced modulation of photosynthetic induction in non-acclimated and cold-acclimated Arabidopsis thaliana: chlorophyll a fluorescence and gas-exchange measurements. Photosynth Res 139, 123–143 (2019). https://doi.org/10.1007/s11120-018-0588-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-018-0588-7

Keywords

Search

Navigation