Skip to main content
Log in

Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants

  • Minireview
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Cold acclimation requires adjustment to a combination of light and low temperature, conditions which are potentially photoinhibitory. The photosynthetic response of plants to low temperature is dependent upon time of exposure and the developmental history of the leaves. Exposure of fully expanded leaves of winter cereals to short-term, low temperature shiftsinhibits whereas low temperature growthstimulates electron transport capacity and carbon assimilation. However, the photosynthetic response to low temperature is clearly species and cultivar dependent. Winter annuals and algae which actively grow and develop at low temperature and moderate irradiance acquire a resistance to irradiance 5- to 6-fold higher than their growth irradiance. Resistance to short-term photoinhibition (hours) in winter cereals is a reflection of the increased capacity to keep QA oxidized under high light conditions and low temperature. This is due to an increased capacity for photosynthesis. These characteristics reflect photosynthetic acclimation to low growth temperature and can be used to predict the freezing tolerance of cereals. It is proposed that the enhanced photosynthetic capacity reflects an increased flux of fixed carbon through to sucrose in source tissue as a consequence of the combined effects of increased storage of carbohydrate as fructans in the vacuole of leaf mesophyll cells and an enhanced export to the crown due to its increased sink activity. Long-term exposure (months) of cereals to low temperature photoinhibition indicates that this reduction of photochemical efficiency of PS II represents a stable, long-term down regulation of PS II to match the energy requirements for CO2 fixation. Thus, photoinhibition in vivo should be viewed as the capacity of plants to adjust photosynthetically to the prevailing environmental conditions rather than a process which necessarily results in damage or injury to plants. Not all cold tolerant, herbaceous annuals use the same mechanism to acquire resistance to photoinhibition. In contrast to annuals and algae, overwintering evergreens become dormant during the cold hardening period and generally remain susceptible to photoinhibition. It is concluded that the photosynthetic response to low temperatures and susceptibility to photoinhibition are consequences of the overwintering strategy of the plant species.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

Asc:

ascorbate

BQ:

benzoquinone

CAP:

chloramphenicol

DAD:

diaminodurene

DCPIP:

dichlorophenolindophenol

DHA:

dehydroascorbate

DHQ:

dihydroduroquinone

DPH:

diphenylhexatriene

EPR:

electron spin resonance

FBP:

fructose bisphosphate

FBPase:

fructose-1,6-bisphosphatase

F-2,6-BP:

fructose-2,6-bisphosphate

FO :

minimum fluorescence with all PS II traps open in dark adapted leaves

FM :

maximum fluorescence with all PS II traps closed in dark adapted leaves

FV :

variable fluorescence (FV=FM−FO)

FO :

minimum fluorescence when all traps are open in light adapted leaves

FM :

maximum fluorescence when all traps are closed in light adapted leaves

FV :

variable fluorescence in light adapted leaves (FV =FM −FO )

H:

cold hardened state

HL:

high-light (1200 μmol m-2s-1) grown plants

LD:

plants grown with a 16 h photoperiod

LHC IIb:

oligomeric form of the light harvesting complex of PS II

LT50 :

freezing temperature at which 50% of the plants die

MDA:

monodehydroascorbate

MV:

methylviologen

NH:

nonhardened state

PCR:

photosynthetic carbon reduction cycle

PGA:

phosphoglycerate

PQ:

plastoquinone

PSmax:

maximum, light saturated rates of photosynthesis

qP :

photochemical quenching parameter

qN :

nonphotochemical quenching parameter

φPS II :

yield of PS II electron transport

(QA)ox :

oxidized form of the primary, stable electron acceptor for PS II

(QA)red :

reduced form of the primary, stable electron acceptor for PS II

RuBP:

ribulose-1,5-bisphosphate

SD:

plants grown with an 8 h photoperiod

SOD:

superoxide dismutase

SPS:

sucrose phosphate synthase

SUC-P:

sucrose phosphate

TMPD:

tetramethylphenylenediamine

TP:

triose phosphate

References

  • Andersson G (1944) Gas exchange and frost hardening studies in winter cereals. Ph.D. Thesis, University of Lund.

  • Andersson B and Styring S (1991) Photosystem II: Molecular organization, function and acclimation. In: Krogmann (ed) Current Topics in Bioenergetics, Vol 16, pp 1–81. Academic Press, New York.

    Google Scholar 

  • Aro EM, Tyystjärvi E and Nurmi A (1990) Temperature-dependent changes in the Photosystem II heterogeneity of attached leaves under high light. Physiol Plant 79: 585–592.

    Google Scholar 

  • Bailey KJ and Walker DA (1992) Changes in fluorescence quenching brought about by feeding dithiothereitol to illuminated leaves. Plant Physiol 99: 124–129.

    Google Scholar 

  • Baker NR (1991) A possible role for Photosystem II in environmental perturbations of photosynthesis, Physiol Plant 81: 563–570.

    Google Scholar 

  • Baker NR, Long SP and Ort DR (1988) Photosynthesis and temperature with particular reference to the effects of quantum yield. In: Long SP and Woodward FI (eds) Plants and Temperature, pp 347–375. Cambridge University Press, Cambridge.

    Google Scholar 

  • Barber J and Andersson B (1992) Too much of a good thing: Light can be bad for photosynthesis. Trends Biochem Sci 17: 61–66.

    Google Scholar 

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

    Google Scholar 

  • Blum A (1985) Breeding crop varieties for stress environments. CRC Crit Rev Plant Sci 2: 199–238.

    Google Scholar 

  • Boese SR and Huner NPA (1990) Effect of growth temperature and temperature shifts on spinach leaf morphology and photosynthesis. Plant Physiol 94: 1830–1836.

    Google Scholar 

  • Boese SR and Huner NPA (1992) Developmental history affects the susceptibility of spinach leaves to in vivo low temperature photoinhibition. Plant Physiol 99: 1141–1145.

    Google Scholar 

  • Bolhar-Nordenkampf HR and Lechner EG (1988) Temperature and light dependent modifications of chlorophyll fluorescence kinetics in spruce needles during winter. Photosynth Res 18: 287–298.

    Google Scholar 

  • Briantais J-M, Ducruet J-M, Hodges M and Krause GH (1992) The effects of low temperature acclimation and photoinhibitory treatments on Photosystem 2 studied by thermoluminescence and fluorescence decay kinetics. Biochim Biophys Acta 31: 1–10.

    Google Scholar 

  • Cadieux C, Sarhan F and Perras M (1988) Osmotic adjustment and photosynthetic electron transport response to cold hardening in winter and spring wheat. Plant Physiol Biochem 26: 313–322.

    Google Scholar 

  • Chen HH and Li PH (1982) Potato cold acclimation. In: Li PH and Sakai A (ed) Plant Cold Hardiness and Freezing Stress, Vol 2, pp 5–22. Academic Press, New York.

    Google Scholar 

  • Chow WS, Osmond CB and Huang LK (1989) Photosystem II function and herbicide binding sites during photoinhibition of spinach chloroplasts in vivo and in vitro. Photosynth Res 21: 17–26.

    Google Scholar 

  • Collier DE and Cummins WR (1990) The effects of low growth and measurement temperature on the respiratory properties of five temperate species. Ann Bot 65: 533–538.

    Google Scholar 

  • Cornic G and Louason G (1980) The effects of O2 on net photosynthesis at low temperature (5°C). Plant Cell Environ 3: 149–157.

    Google Scholar 

  • Crespi MD, Zabaleta EJ, Pontis HG and Salerno GL (1991) Sucrose synthase expression during cold acclimation in wheat. Plant Physiol 96: 887–891.

    Google Scholar 

  • DeLucia EH and Smith WK (1987) Air and soil temperature limitations on photosynthesis in Engelmann spruce during summer. Can J For Res 17: 527–533.

    Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020: 1–24.

    Google Scholar 

  • Dexter ST (1933) Effects of several environmental factors on the hardening of plants. Plant Physiol 8: 123–139.

    Google Scholar 

  • Falk S (1991) Photoinhibition and recovery of photosynthesis in the green algaChlamydomonas reinhardtii, Dangeard. Ph.D. Thesis, University of Umeå.

  • Falk S and Samuelsson G (1992) Recovery of photosynthesis and Photosystem II fluorescence inChalmydomonas reinhardtii after exposure to three levels of high light. Physiol Plant 85: 61–68.

    Google Scholar 

  • Falk S, Samuelsson G and Öquist G (1990) Temperature-dependent photoinhibition and recovery of photosynthesis in the green algaChlamydomonas reinhardtii acclimated to 12 and 27°C. Physiol Plant 78: 173–180.

    Google Scholar 

  • Falk S, Leverenz JW, Samuelsson G and Öquist G (1992) Changes in Photosystem II fluorescence inChlamydomonas reinhardtii exposed to increasing levels of irradiance in relationship to the photosynthetic response to light. Photosynth Res 31: 151–160.

    Google Scholar 

  • Farrar JF (1988) Temperature and the partitioning and translocation of carbon. In: Long SP and Woodward FI (eds) Plants and Temperature, pp 203–235. Society for Experimental Biology, Cambridge, UK.

    Google Scholar 

  • Foyer C, Furbank R, Harbinson J and Horton P (1990) The mechanisms contributing to photosynthetic control of electron transport by carbon assimilation in leaves. Photosynth Res 25: 83–100.

    Google Scholar 

  • Fowler DB and Carles RJ (1979) Growth, development and cold tolerance of fall acclimated cereal grains. Crop Sci 19: 915–922.

    Google Scholar 

  • Fowler DB, Dvorak J and Gusta LV (1977) Comparative cold hardiness of severalTriticum species andSecale cereale L. Crop Sci 17: 941–943.

    Google Scholar 

  • Franklin LA, Leavasseur G, Osmond CB, Henley WJ and Ramus J (1992) Two components of the onset and recovery during photoinhibition ofUlva rotundata. Plants 186: 399–408.

    Google Scholar 

  • Genty B, Harbinson J, Briantais J-M and Baker NR (1989) The relationship between non-photochemical quenching of chlorophyll fluorescence and the rate of Photosystem 2 photochemistry in leaves. Photosynth Res 25: 249–257.

    Google Scholar 

  • Goldschmidt E and Huber SC (1992) Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose and hexose sugars. Plant Physiol 99: 1443–1448.

    Google Scholar 

  • Gong H and Nilsen S (1989) Effect of temperature on photoinhibition of photosynthesis, recovery and turnover of the 32 kD chloroplast protein inLemna gibba. J Plant Physiol 135: 9–14.

    Google Scholar 

  • Grace J (1988) Temperature as a determinant of plant productivity. In: Long SP and Woodward FI (eds) Plants and Temperature, pp 91–107. Cambridge University Press, Cambridge.

    Google Scholar 

  • Graham D and Patterson BD (1982) Responses of plants to low, non-freezing temperatures: Proteins, metabolism and acclimation. Ann Rev Plant Physiol 33: 347–372.

    Google Scholar 

  • Greer DH, Berry JA and Björkman O (1986) Photoinhibition of photosynthesis in intact bean leaves: Role of light and temperature and requirement of chloroplast-protein synthesis during recovery. Planta 168: 253–260.

    Google Scholar 

  • Greer DH, Ottander C and Öquist G (1991) Photoinhibition and recovery of photosynthesis in intact barley leaves. Physiol Plant 81: 203–210.

    Google Scholar 

  • Griffith M, Elfman B and Camm EL (1984) Accumulation of plastoquinone A during low temperature growth of winter rye. Plant Physiol 74: 727–729.

    Google Scholar 

  • Groom QJ and Baker NR (1992) Analysis of light-induced depressions of photosynthesis in leaves of a wheat crop during winter. Plant Physiol 100: 1217–1223.

    Google Scholar 

  • Groom QJ, Baker NR and Long SP (1991) Photoinhibition of holly (Ilex aquifolium) in the field during the winter. Physiol Plant 83: 585–590.

    Google Scholar 

  • Guenther JE and Melis A (1990a) The physiological significance of Photosystem II heterogeneity in chloroplasts. Photosynth Res 23: 105–109.

    Google Scholar 

  • Guenther JE and Melis A (1990b) Dynamics of Photosystem II heterogeneity inDunaliella salina (green alga). Photosynth Res 23: 195–203.

    Google Scholar 

  • Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Ann Rev Plant Physiol Mol Biol 41: 187–223.

    Google Scholar 

  • Guy C, Huber JAL and Huber SC (1992) Sucrose phosphate synthase and sucrose accumulation at low temperature. Plant Physiol 100: 502–508.

    Google Scholar 

  • Hällgren JE, Lundmark T and Strand M (1990) Photosynthesis of Scots pine in the field after night frosts during summer. Plant Physiol Biochem 28: 437–445.

    Google Scholar 

  • Havaux M, Greppin H and Strasser RJ (1991) Functioning of Photosystems I and II in pea leaves exposed to heat stress in the presence or absence of light. Planta 186: 88–98.

    Google Scholar 

  • Holaday AS, Martindale W, Alred R, Brooks AL and Leegood RC (1992) Changes in activities of enzymes of carbon metabolism in leaves during exposure of plants to low temperature. Plant Physiol 98: 1105–1114.

    Google Scholar 

  • Huner NPA (1985) Acclimation of winter rye to cold hardening temperatures results in an increased capacity for photosynthetic electron transport. Can J Bot 63: 506–511.

    Google Scholar 

  • Huner NPA and Macdowall FDH (1979) The effects of low temperature acclimation of winter rye on the catalytic properties of its ribulose bisphosphate carboxylase-oxygenase. Can J Biochem 57: 1036–1041.

    Google Scholar 

  • Huner NPA and Reynolds TL (1989) Low growth temperature-induced increase in light saturated PS I electron transport is cation dependent. Plant Physiol 91: 1308–1316.

    Google Scholar 

  • Huner NPA, Migus W and Tolenaar M (1986) Leaf CO2 exchange rates in winter rye grown at cold-hardening and nonhardening temperatures. Can J Plant Sci 66: 443–452.

    Google Scholar 

  • Huner NPA, Krol M, Williams JP, Maissan E, Low PS, Roberts D and Thompson JE (1987) Low temperature development induces a specific decrease in trans-Δ3-hexadecenoic acid content which influences LHC II organization. Plant Physiol 84: 12–18.

    Google Scholar 

  • Huner NPA, Krol M, Williams JP and Maissan E (1988) Overwintering periwinkle (Vinca minor L.) exhibits increased Photosystem I activity. Plant Physiol 87: 721–726.

    Google Scholar 

  • Hurry VM (1991) Characterization of the photosynthetic responses of spring and winter wheat to growth at coldhardening temperatures. Ph.D. Thesis, University of Western Ontario.

  • Hurry VM and Huner NPA (1991) Low growth temperature affects a differential inhibition of photosynthesis in spring and winter wheat. Plant Physiol 96: 491–497.

    Google Scholar 

  • Hurry VM and Huner NPA (1992) Effect of cold hardening on sensitivity of winter and spring wheat leaves to short-term photoinhibition and recovery of photosynthesis. Plant Physiol 100: 1283–1290.

    Google Scholar 

  • Hurry VM, Krol M, Öquist G and Huner NPA (1992) Effect of long-term photoinhibition on growth and photosynthesis of cold hardened spring and winter wheat. Planta 188: 369–375.

    Google Scholar 

  • Hurry VM, Gardeström P and Öquist G (1993) Reduced sensitivity to photoinhibition following frost-hardening of winter rye is due to increased phosphate availability: Planta (in press).

  • Joliffe PA and Tregunna EB (1973) Environmental regulation of the oxygen effect on apparent photosynthesis in wheat. Can J Bot 51: 841–853.

    Google Scholar 

  • Kirilovsky DL, Vernotte C and Etienne A-L (1990) Protection from photoinhibition by low temperature inSynechocystis 6714 and inChlamydomonas reinhardtii: Detection of an intermediary state. Biochem 29: 8100–8106.

    Google Scholar 

  • Kobza J and Edwards GE (1987) Influences of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiol 83: 69–74.

    Google Scholar 

  • Krause GH (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol Plant 74: 566–574.

    Google Scholar 

  • Krause GH and Weis E (1991) Chlorophyll fluorescence and photosynthesis: The basics. Ann Rev Plant Physiol Plant Mol Biol 42: 313–394.

    Google Scholar 

  • Krol M and Huner NPA (1985) Growth and development at cold hardening temperatures. Pigment and benzoquinone accumulation in winter rye. Can J Bot 63: 716–721.

    Google Scholar 

  • Krol M, Griffith M and Huner NPA (1984) An appropriate physiological control for environmental temperature studies: Comparative growth kinetics for winter rye. Can J Bot 62: 1062–1068.

    Google Scholar 

  • Krol M, Huner NPA and MacIntosh A (1988) Chloroplast biogenesis at cold hardening temperatures. Development of Photosystem I and Photosystem II activities in relation to pigment accumulation. Photosynth Res 14: 97–112.

    Google Scholar 

  • Kyle DJ (1987) The biochemical basis for photoinhibition of Photosystem II. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Photoinhibition. Topics in Photosynthesis, Vol 9, pp 197–226. Elsevier, Amsterdam.

    Google Scholar 

  • Labate CA and Leegood RC (1988) Limitation of photosynthesis by changes in temperature. Factors affecting the response of carbon dioxide assimilation to temperature in barley leaves. Planta 173: 519–527.

    Google Scholar 

  • Labate CA and Leegood RC (1989) The influence low temperature on respiration and contents of phosphorylated intermediates in darkened barley leaves. Plant Physiol 91: 905–910.

    Google Scholar 

  • Labate CA, Adcock MD and Leegood RC (1990) Effects of temperature on the regulation of photosynthetic carbon assimilation in leaves and barley. Planta 181: 547–554.

    Google Scholar 

  • Lapointe L and Huner NPA (1992) Photoinhibition of isolated mesophyll cells from cold hardened and nonhardened winter rye. Plant Cell Environ (in press).

  • Lapointe L, Huner NPA, Carpentier R and Ottander C (1991) Resistance to low temperature photoinhibition is not associated with isolated thylakoid membranes of winter rye. Plant Physiol 97: 804–810.

    Google Scholar 

  • Lawrence T, Cooper JP and Breese EL (1973) Cold tolerance and winter hardiness inLolium perenne. II. Influence of light and temperature during growth and hardening. J Agric Sci 80: 341–348.

    Google Scholar 

  • Leegood RC (1985) Regulation of photosynthetic CO2-pathway enzymes by light and other factors. Photosynth Res 6: 247–259.

    Google Scholar 

  • Leegood RC and Furbank RT (1986) Stimulation of photosynthesis by 2% O2 at low temperatures is restored by phosphate. Planta 168: 84–93.

    Google Scholar 

  • Leverenz JW and Öquist G (1987) Quantum yields of photosynthesis at temperatures between-2°C and 35°C in a cold tolerant C3 plant (Pinus sylvestris) during the course of one year. Plant Cell Environ 10: 287–295.

    Google Scholar 

  • Levitt J (1980) Responses of Plants to Environmental Stress, Vol 1 (2nd ed). Academic Press, New York, 497 pp.

    Google Scholar 

  • Long SP and Woodward FI (1988) Plants and Temperature. Cambridge University Press, Cambridge, 415 pp.

    Google Scholar 

  • Lundmark T and Hällgren J-E (1988) Effects of frost on shaded and exposed spruce and pine needles planted in the field. Can J Forestry Res 10: 1197–1201.

    Google Scholar 

  • Macdowall FDH (1974) Growth kinetics of Marquis wheat. VI. Genetic dependence and winter hardening. Can J Bot 52: 151–157.

    Google Scholar 

  • Mächler F, Schnyder H and Nösberger J (1984) Influence of inorganic phosphate on photosynthesis of wheat chloroplasts. I. Photosynthesis and assimilate export at 5°C and 25°C. J Exp Bot 35: 481–487.

    Google Scholar 

  • Maciejewska U, Tomczyk J and Kacperska-Palacz A (1984) Effects of cold on CO2 exchange in winter rape leaves. Physiol Plant 62: 315–320.

    Google Scholar 

  • Mattoo AK, Marder JB and Edelmann M (1989) Dynamics of the Photosystem II reaction center. Cell 56: 241–246.

    Google Scholar 

  • Martin B, Martensson O and Öquist G (1978) Seasonal effects on photosynthetic electron transport and fluorescence properties in isolated chloroplasts ofPinus sylvestris. Physiol Plant 44: 102–109.

    Google Scholar 

  • Mawson BT, Svoboda J and Cummins RW (1986) Thermal acclimation of photosynthesis by the Arctic plantSaxifraga cernua. Can J Bot 64: 71–76.

    Google Scholar 

  • McNulty AK and Cummins WR (1987) The relationship between respiration and temperature in leaves of the Arctic plantSaxifraga cernua. Plant Cell Environ 10: 319–325.

    Google Scholar 

  • Neale PJ and Melis A (1990) Activation of a reserve pool of Photosystem II inChlamydomonas reinhardtii counteracts photoinhibition, Plant Physiol 92: 1196–1204.

    Google Scholar 

  • Newsted WJ, Chibbar RN and Georges F (1991) Effect of low temperature stress on the expression of sucrose synthetase in spring and winter wheat plants. Development of a monoclonal antibody against wheat germ sucrose synthetase. Biochem Cell Biol 69: 36–41.

    Google Scholar 

  • Oberhuber W and Bauer H (1991) Photoinhibition of photosynthesis under natural conditions in ivy (Hedera helix L.) growing in an understory of deciduous trees. Planta 185: 545–553.

    Google Scholar 

  • Ögren E and Rosenqvist E (1992) On the significance of photoinhibition of photosynthesis in the field and its generality among species. Photosynth Res 33: 63–71.

    Google Scholar 

  • Ögren E and Sjöström M (1990) Estimation of the effect of photoinhibition on the carbon gain in leaves of a willow canopy. Planta 181: 560–567.

    Google Scholar 

  • Okada K, Satoh K and Katoh S (1991) Chloramphenicol is an inhibitor of photosynthesis. FEBS Lett 295: 155–158.

    Google Scholar 

  • Öquist G and Huner NPA (1991) Effects of cold acclimation on the susceptibility of photosynthesis to photoinhibition in Scots pine and in winter and spring cereals: A fluorescence analysis. Func Ecol 5: 91–100.

    Google Scholar 

  • Öquist G and Huner NPA (1992) Cold-hardening induced resistance to photoinhibition in winter rye is dependent upon an increased capacity for photosynthesis. Planta 189: 150–156.

    Google Scholar 

  • Öquist G and Malmberg G (1989) Light and temperature dependent inhibition of photosynthesis in frost-hardened and unhardened seedlingsof pine. Photosynth Res 20: 261–277.

    Google Scholar 

  • Öquist G and Martin B (1986) Cold Climates. In: Baker NR, Long SP (eds) Photosynthesis in Contrasting Environments, Vol 7, pp 237–293. Elsevier, New York.

    Google Scholar 

  • Öquist G and Ögren E (1985) Effects of winter stress on photosynthetic electron transport and energy distribution between the two photosystems of pine as assayed by chlorophyll fluorescence kinetics. Photosynth Res 7: 19–30.

    Google Scholar 

  • Öquist G, Brunes L, Hällgren J-E, Gezelius K Hallén M and Malmberg G (1980) Effects of artificial frost hardening and winter stress on net photosynthesis, photosynthetic electron transport and RuBP carboxylase activity in seedlings ofPinus sylvestris. Physiol Plant 48: 526–531.

    Google Scholar 

  • Öquist G, Ögren E and Greer DH (1987) Light stress at low temperatures. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Photoinhibition. Topics in Photosynthesis, Vol 9, pp 67–88. Elsevier, Amsterdam.

    Google Scholar 

  • Öquist G, Hurry VM and Huner NPA (1993) Low temperature effects on photosynthesis and correlation with freezing tolerance in spring and winter cultivars of wheat and rye. Plant Physiol 101: 245–250.

    Google Scholar 

  • Ottander C and Öquist G (1991) Recovery of photosynthesis in winter-stressed Scots pine. Plant Cell Environ 14: 345–349.

    Google Scholar 

  • Ottander C, Hundal T, Andersson B, Huner NPA and Öquist G (1992) On the susceptibility of photosynthesis to photo-inhibition at low temperature in barley leaves. Photosynth Res 35: 191–200.

    Google Scholar 

  • Paul MJ, Lawlor DW and Driscoll SP (1990) The effect of temperature on photosynthesis and carbon fluxes in sunflower and rape. J Exp Bot 41: 547–555.

    Google Scholar 

  • Paul MJ, Driscoll SP and Lawlor DW (1992) Sink-regulation of photosynthesis in relation to temperature in sunflower and rape. J Exp Bot 43: 147–153.

    Google Scholar 

  • Pollock CJ and Chatterton NJ (1988) Fructans. In: Priess J (ed) The Biochemistry of Plants, Carbohydrates, Vol 14, pp 109–140. Academic Press, New York.

    Google Scholar 

  • Pollock CJ and Lloyd EJ (1987) The effect of low growth temperature upon starch, sucrose and fructan synthesis in leaves. Ann Bot 60: 231–235.

    Google Scholar 

  • Pollock C, Lloyd EJ, Stoddart JL and Thomas H (1983) Growth, photosynthesis and assimilate partitioning inLolium temulentum exposed to chilling temperatures. Physiol Plant 59: 257–262.

    Google Scholar 

  • Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Ann Rev Plant Physiol 35: 15–44.

    Google Scholar 

  • Prosser CL (1986) Adaptational Biology. Molecules to Organisms, J. Wiley and Sons, New York, 784 pp.

    Google Scholar 

  • Raven JA and Samuelsson G (1986) Repair of photoinhibitory damage inAnacystis nidulans 625 (Synechococcus 6301): Relation to catalytic capacity for and energy supply to, protein synthesis and implication for μmax and efficiency of light limited growth. New Phytol 103: 625–643.

    Google Scholar 

  • Reynolds TR and Huner NPA (1990) Effect of preincubation temperature on in vitro light saturated Photosystem I activity in thylakoids isolated from cold hardened and non-hardened rye. Plant Physiol 93: 319–324.

    Google Scholar 

  • Rütten D and Santarius KA (1992) Aged-related differences in frost sensitivity of the photosynthetic apparatus of twoPlagiomnium species. Planta 187: 224–229.

    Google Scholar 

  • Schöner S and Krause GH (1990) Protective systems against oxygen species in spinach: Response to cold acclimation in excess light. Planta 180: 383–389.

    Google Scholar 

  • Schnyder H, Mächler F and Nösberger J (1986) Regeneration of ribulose-1,5-bisphosphate and ribulose-1,5-bisphosphate carboxylase/oxygenase activity associated with lack of oxygen inhibition of photosynthesis at low temperature. J Exp Bot 37: 1170–1179.

    Google Scholar 

  • Senser M and Beck E (1977) On the mechanism of frost injury and frost hardening of spruce chloroplasts. Planta 137: 195–201.

    Google Scholar 

  • Sharkey TD (1985a) Photosynthesis in intact leaves of C3 plants: Physics, physiology and rate limitations. Bot Rev 51: 53–105.

    Google Scholar 

  • Sharkey TD (1985b) O2-insensitive photosynthesis in C3 plants. Its occurrence and a possible explanation. Plant Physiol 78: 71–75.

    Google Scholar 

  • Sharkey TD, Stitt M, Heinke D, Gerhardt R, Raschke K and Heldt HW (1986) Limitations of photosynthesis by carbon metabolism. II. O2-insensitive CO2 uptake results from limitation of triose phosphate utilization. Plant Physiol 81: 1123–1129.

    Google Scholar 

  • Somersalo S and Krause GH (1989) Photoinhibition at chilling temperatures. Fluorescence characteristics of unhardened and cold acclimated spinach leaves. Planta 177: 409–416.

    Google Scholar 

  • Somersalo S and Krause GH (1990) Reversible photoinhibition of unhardened and cold acclimated spinach leaves at chilling temperatures. Planta 180: 181–187.

    Google Scholar 

  • Steponkus PL (1984) Role of the plasma membrane in freezing injury and cold acclimation. Ann Rev Plant Physiol 35: 543–584.

    Google Scholar 

  • Steponkus PL and Lanphear FO (1968) The role of light in cold acclimation ofHedera helix L. var. Thorndale. Plant Physiol 43: 151–156.

    Google Scholar 

  • Stitt M (1986) Limitation of photosynthesis by metabolism I. Evidence for excess electron capacity in leaves carrying out photosynthesis in saturating light and CO2. Plant Physiol 81: 1115–1122.

    Google Scholar 

  • Stitt M and Grosse H (1988) Interactions between sucrose synthesis and CO2 fixation IV. Temperature-dependent adjustment of the relation between sucrose synthesis and CO2 fixation. J Plant Physiol 133: 392–400.

    Google Scholar 

  • Stitt M, Huber S and Kerr P (1987) Control of photosynthetic sucrose formation. In: Hatch MD and Boardman NK (eds) The Biochemistry of Plants, Photosynthesis, Vol 10, pp 327–409. Academic Press Inc, New York.

    Google Scholar 

  • Strand M and Öquist G (1985) Inhibition of photosynthesis by freezing temperatures and high light levels in cold acclimated seedlings of Scots pine (Pinus sylvestris). I. Effects on the light limited and light saturated rates of CO2 assimilation. Physiol Plant 64: 425–430.

    Google Scholar 

  • Strand M and Öquist G (1988) Effects of frost hardening, dehardening and freezing stress on in vivo fluorescence of seedlings of Scots pine (Pinus sylvestris L.) Plant Cell Environ 11: 231–238.

    Google Scholar 

  • Thomas PG, Quinn PJ and Williams WP (1986) The origin of Photosystem-I-mediated electron transport stimulation in heat stressed chloroplasts. Planta 167: 133–139.

    Google Scholar 

  • Tyystjärvi A and Aro EM (1990) Temperature-dependent changes in Photosystem II heterogeneity support a cycle of Photosystem II during photoinhibition. Photosynth Res 26: 109–117.

    Google Scholar 

  • van Wijk KJ (1992) Photoinhibition of photosynthesis in higher plants. From Photosystem II particle to intact leaf. Ph.D. Thesis, Rijksuniversiteit Groningen.

  • van Wijk KJ and Krause GH (1991) O2-dependence of photoinhibition at low temperature in intact protoplasts ofValerianella locusta L. Planta 186: 135–142.

    Google Scholar 

  • Vasil'yev IM (1956) Wintering of Plants. American Inst. of Biological Sciences. Roger and Roger Inc, Washington, 300 pp.

    Google Scholar 

  • Vogelmann TC, Bornmann JF and Josserand S (1989) Photosynthetic light gradients and spectral regime within leaves ofMedicago sativa. Phil Trans Soc Lond B 323: 411–421.

    Google Scholar 

  • Weis E and Berry JA (1987) Quantum efficiency of Photosystem II in relation to ‘energy’-dependent quenching of chlorophyll fluorescence. Biochim Biophys Acta 894: 198–207.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huner, N.P.A., Öquist, G., Hurry, V.M. et al. Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res 37, 19–39 (1993). https://doi.org/10.1007/BF02185436

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02185436

Key words

Navigation