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Cold acclimation and photoinhibition of photosynthesis in Scots pine

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Abstract

Cold acclimation of Scots pine did not affect the susceptibility of photosynthesis to photoinhibition. Cold acclimation did however cause a suppression of the rate of CO2 uptake, and at given light and temperature conditions a larger fraction of the photosystem II reaction centres were closed in cold-acclimated than in nonacclimated pine. Therefore, when assayed at the level of photosystem II reaction centres, i.e. in relation to the degree of photosystem closure, cold acclimation caused a significant increase in resistance to photoinhibition; at given levels of photosystem II closure the resistance to photoinhibition was higher after cold acclimation. This was particularly evident in measurements at 20° C. The amounts and activities of the majority of analyzed active oxygen scavengers were higher after cold acclimation. We suggest that this increase in protective enzymes and compounds, particularly Superoxide dismutase, ascorbate peroxidase, glutathione reductase and ascorbate of the chloroplasts, enables Scots pine to avoid excessive photoinhibition of photosynthesis despite partial suppression of photosynthesis upon cold acclimation. An increased capacity for light-induced de-epoxidation of violaxanthin to zeaxanthin upon cold acclimation may also be of significance.

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Abbreviations

APX:

ascorbate peroxidase

DHA:

dehydroascorbate

DHAR:

dehydroascorbate reductase

Fm:

maximal fluorescence when all reaction centres are closed

Fv/Fm:

maximum photochemical yield of PSII

GR:

glutathione reductase

GSH:

reduced glutathione

Je:

rate of photosynthetic electron transport

MDAR:

monodehydroascorbate reductase

qN :

nonphotochemical quenching of fluorescence

qP :

photochemical quenching of fluorescence

SOD:

superoxide dismutase

References

  • Anderson J, Chevone B, Hess J (1991) Seasonal variation in the antioxidant system of Eastern white pine needles. Evidence for thermal dependence. Plant Physiol 98:501–508

    Google Scholar 

  • Asada K, Badger MR (1984) Photoreduction of 18O2 and H2 18O2 with concomitant evolution of 16O2 in intact spinach chloroplasts: Evidence for scavenging of hydrogen peroxide by peroxidase. Plant Cell Physiol 25:1169–1179

    Google Scholar 

  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Topics in photosynthesis. Photoinhibition, vol 9. Elsevier, Amsterdam, pp 227–287

    Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    Google Scholar 

  • Bilger W, Schreiber U (1986) Energy-dependent quenching of dark-level chlorophyll fluorescence in intact leaves. Photosynth Res 10:303–308

    Google Scholar 

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

    Google Scholar 

  • Britton G (1985) General carotenoid methods. Methods Enzymol 11:113–148

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams III WW (1991) Light, photosynthesis and the xanthophyll cycle. In: Pelland EJ, Steffen KL (eds) Current topics of plant physiology. Active oxygen/oxidative stress and plant metabolism, vol 6. Am Soc Plant Physiologist, Rockville, Md., USA, pp 171–179

    Google Scholar 

  • Demmig-Adams B, Adams III WW, Logan BA, Verhoeven AS (1995) Xanthophyll cycle-dependent energy dissipation and flexible photosystem II efficiency in plants acclimated to light stress. Aust J Plant Physiol 22:249–260

    Google Scholar 

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

    Google Scholar 

  • Foyer CH, Lelandais M, Edvards AE, Mullineaux PM (1991) The role of ascorbate in plants, interactions with photosynthesis, and regulatory significance. In: Pell EJ, Steffen KL (eds) Current topics in plant physiology. Active oxygen/oxidative stress and plant metabolism, vol 6. Am Soc Plant Physiologists, Rockville, Md, USA, pp 131–144

    Google Scholar 

  • Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    CAS  Google Scholar 

  • Gillham DJ, Dodge AD (1986) Hydrogen peroxide scavening systems within pea chloroplasts. Planta 167:246–251

    Google Scholar 

  • Havaux M, Strasser RJ, Greppin H (1991) A theoretical and experimental analysis of the qP and qN coefficients of chlorophyll fluorescence quenching and their relation to photochemical and nonphotochemical events. Photosynth Res 27:41–55

    Google Scholar 

  • Horton P, Ruban AV, Walters RG (1994) Regulation of light harvesting in green plants. Induction of nonphotochemical quenching of chlorophyll fluorescence. Plant Physiol 106:415–420

    Google Scholar 

  • Hurry VM, 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, Gardeström P, Öquist G (1993) Reduced sensitivity to photoinhibition following frost-hardening of winter rye is due to increased phosphate availability. Planta 190:484–490

    Google Scholar 

  • Idle DB, Proctor CW (1983) An integrating sphere leaf chamber. Plant Cell Environ 6:437–439

    Google Scholar 

  • Karpinski S, Wingsle G, Karpinski B, Hällgren J-E (1993) Molecular responses to photooxidative stress in Pinus sylvestris (L.) II. Differential expression of CuZn-superoxide dismutases and glutathione reductase. Plant Physiol 103:1385–1391

    Google Scholar 

  • Koroleva OY, Brüggemann W, Krause GH (1994) Photoinhibition, xantophyll cycle and in vivo chlorophyll fluorescence quenching of chilling-tolerant Oxyria digyna and chilling-sensitive Zea mays. Physiol Plant 92:577–584

    Google Scholar 

  • Leverenz JW (1987) Chlorophyll content and the light response curve of shade-adapted conifer needles. Physiol Plant 71:20–29

    Google Scholar 

  • Leverenz JW, Falk S, Pilström C-M, Samuelsson G (1990) The effects of photoinhibition on the photosynthetic light response curve of green plant cells (Chlamydomonas reinhardtii). Planta 182:161–168

    Google Scholar 

  • Loreto F, Harley PC, Marco GD, Sharkey TD (1992) Estimation of mesophyll conductance to CO2 flux by three different methods. Plant Physiol 98:1437–1443

    Google Scholar 

  • Markgraf T, Berry J (1990) Measurement of photochemical and non-photochemical quenching: correction of turnover of PSII during steady-state photosynthesis: In: Baltscheffsky M (ed) Current research in photosynthesis, vol IV. Kluwer Academic Publishers, Dordrecht, pp 279–282

    Google Scholar 

  • Nakagawara S, Sagisaka S (1984) Increase in enzyme activities related to ascorbate metabolism during cold acclimation in poplar twigs. Plant Cell Physiol 25:899–906

    Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    Google Scholar 

  • Neubauer C, Yamamoto HY (1992) Mehler-peroxidase reaction mediates zeaxanthin formation and zeaxanthin-related fluorescence quenching in intact chloroplasts. Plant Physiol 99:1354–1361

    Google Scholar 

  • Ögren E (1991) Prediction of photoinhibition of photosynthesis from measurements of fluorescence quenching components. Planta 184:538–544

    Google Scholar 

  • Ögren E, 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 

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

    Google Scholar 

  • Öquist G, Huner NPA (1993) Cold-hardening-induced resistance to photoinhibition of photosynthesis in winter rye is dependent upon an increased capacity for photosynthesis. Planta 189:150–156

    Google Scholar 

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

    Google Scholar 

  • Öquist G, Strand M (1986) Effects of frost hardening on photosynthetic quantum yield, chlorophyll organization, and energy distribution between the two photosystems in Scots pine. Can J Bot 64:748–753

    Google Scholar 

  • Oquist G, Brunes L, Hällgren J-E, Gezelius K, Hallén M, Malm-berg G (1980) Effects of artifical frost hardening and winter stress on net photosynthesis, photosynthetic electron transport and RuBP carboxylase in seedlings of Pinus silvestris. Physiol Plant 48:526–531

    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. Photoinhibition, vol 9. Elsevier, Amsterdam, pp 67–87

    Google Scholar 

  • Öquist G, Chow WS, Anderson JM (1992) Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosynthesis. Planta 186:450–460

    Google Scholar 

  • Öquist G, Hurry VM, Huner NPA (1993a) 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 

  • Öquist G, Hurry VM, Huner NPA (1993b) The temperature dependence of the redox state of QA and susceptibility of photosynthesis to photoinhibition. Plant Physiol Biochem 31:683–691

    Google Scholar 

  • Osmond CB, Grace SC (1995) Perspectives on photoinhibition and photorespiration in the field: the quintessential inefficiencies of the light and dark reactions photosynthesis. J Exp Bot 46:1351–1362

    CAS  Google Scholar 

  • Osmond CB, Ramus J, Leavavasseur G, Franklin LA, Henley WJ (1993) Fluorescence quenching during photosynthesis and photoinhibition of Ulva rotundata Blid. Planta 190:97–106

    Google Scholar 

  • Ottander C, Hundal T, Andersson B, Huner NPA, Öquist G (1993) Photosystem II reaction centres stay intact during low temperature photoinhibition. Photosynth Res 35:191–200

    Google Scholar 

  • Ottander C, Campbell D, Öquist G (1995) Seasonal changes in photosystem II organization and pigment composition in Pinus sylvestris. Planta 197:176–183

    CAS  Google Scholar 

  • Polle A, Rennenberg H (1994) Photooxidative stress in trees. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defense systems in plants. CRC Press, Boca Raton, Ann Arbor, London Tokyo, pp 199–218

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Schreiber U, Neubauer C (1990) O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth Res 25:279–293

    Google Scholar 

  • Schröder WP, Åkerlund H-E (1990) Hydrogen peroxide production in photosystem II preparations. In: Baltscheffsky M (ed) Current research in photosynthesis, vol 1. Kluwer Academic Publishers, Dordrecht, pp 901–904

    Google Scholar 

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

    Google Scholar 

  • Siefermann-Harms D (1988) High-performance liquid chromatography of chloroplast pigments. One step separation of carotene and xanthophyll isomers, chlorophylls and pheophytins. J Chromatogr 448:411–416

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Thayer SS, Björkman O (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynth Res 23:331–343

    Google Scholar 

  • Thile A, Schirwitz K, Winter K, Krause GH (1996) Increased xanthophyll cycle activity and reduced D1 protein inactivation related to photoinhibition in two plant systems acclimated to excess light. Plant Sci 115:237–250

    Google Scholar 

  • van Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387

    Google Scholar 

  • van nKooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150

    Google Scholar 

  • Vass I, Styring S, Hundal T, Koivuniemi A, Aro E-M, Andersson B (1992) Reversible and irreversible intermediates during photoinhibition of photosystem II. Stable reduced QA species promote chlorophyll triplet formation. Proc Nat Acad Sci USA 89:1408–1412

    Google Scholar 

  • Vogelman TC, Martin G (1993) The functional significance of palisade tissue: penetration of directional versus diffuse light. Plant Cell Environ 18:65–72

    Google Scholar 

  • Wingsle G, Sandberg G, Hällgren J-E (1989) Determination of glutathione in Scots pine needles by high-performance liquid chromatography as its monobromobimane derivative. J Chromatogr 479:335–344

    Google Scholar 

  • Wingsle G, Gardeström P, Hällgren J-E, Karpinski S (1991) Isolation, purification, subcellular localization of isozymes of superoxide dismutase from Scots pine (Pinus sylvestris L.) needles. Plant Physiol 95:21–28

    Google Scholar 

  • Wise RR, Naylor AW (1987) Chilling-enhanded photooxidation. Evidence for the role of singlet oxygen and superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiol 83:278–282

    Google Scholar 

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Author notes

  1. Sylvain L. Dube

    Present address: Horticulture Research Center, University Lavai, G1K 7P4, Québec, Canada

Authors and Affiliations

  1. Department of Plant Physiology, University of Umeå, S-901 87, Umeå, Sweden

    Christina Ottander & Gunnar Öquist

  2. Department of Biophysics, Ural Forest Technology Institute, 620032, Ekaterinburg, Russia

    Alla Krivosheeva

  3. Institute of Applied Ecology, Academia Sinica, P.O. Box 417, 110015, Shenyang, China

    Da-Li Tao

  4. Department of Forest Genetics and Plant Physiology, Faculty of Forestry, Swedish University of Agricultural Sciences, S-901 83, Umeå, Sweden

    Gunnar Wingsle

  5. Department of Plant Physiology, University of Lund, S-220 27, Lund, Sweden

    Sylvain L. Dube

Authors
  1. Alla Krivosheeva
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  2. Da-Li Tao
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  3. Christina Ottander
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  4. Gunnar Wingsle
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  5. Sylvain L. Dube
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  6. Gunnar Öquist
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Corresponding author

Correspondence to Gunnar Öquist.

Additional information

This work was supported by the Swedish Natural Science Research Council and the National Natural Science Foundation of China.

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Krivosheeva, A., Tao, DL., Ottander, C. et al. Cold acclimation and photoinhibition of photosynthesis in Scots pine. Planta 200, 296–305 (1996). https://doi.org/10.1007/BF00200296

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