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First published online March 28, 2008; 10.1104/pp.108.117598 Plant Physiology 147:402-414 (2008) © 2008 American Society of Plant Biologists OPEN ACCESS ARTICLE
Increased Air Temperature during Simulated Autumn Conditions Impairs Photosynthetic Electron Transport between Photosystem II and Photosystem I1,[OA]Department of Biology and the BIOTRON, University of Western Ontario, London, Ontario, Canada N6A 5B7 (F.B., N.P.A.H., I.E.); Institute of Chemistry and Dynamics of the Geosphere ICG-II, Phytosphere, Research Center Jülich, 52425 Juelich, Germany (F.B.); and Department of Forest Ecology, Forest Research Institute Baden-Wuerttemberg, 79100 Freiburg, Germany (I.E.)
Changes in temperature and daylength trigger physiological and seasonal developmental processes that enable evergreen trees of the boreal forest to withstand severe winter conditions. Climate change is expected to increase the autumn air temperature in the northern latitudes, while the natural decreasing photoperiod remains unaffected. As shown previously, an increase in autumn air temperature inhibits CO2 assimilation, with a concomitant increased capacity for zeaxanthin-independent dissipation of energy exceeding the photochemical capacity in Pinus banksiana. In this study, we tested our previous model of antenna quenching and tested a limitation in intersystem electron transport in plants exposed to elevated autumn air temperatures. Using a factorial design, we dissected the effects of temperature and photoperiod on the function as well as the stoichiometry of the major components of the photosynthetic electron transport chain in P. banksiana. Natural summer conditions (16-h photoperiod/22°C) and late autumn conditions (8-h photoperiod/7°C) were compared with a treatment of autumn photoperiod with increased air temperature (SD/HT: 8-h photoperiod/22°C) and a treatment with summer photoperiod and autumn temperature (16-h photoperiod/7°C). Exposure to SD/HT resulted in an inhibition of the effective quantum yield associated with a decreased photosystem II/photosystem I stoichiometry coupled with decreased levels of Rubisco. Our data indicate that a greater capacity to keep the primary electron donor of photosystem I (P700) oxidized in plants exposed to SD/HT compared with the summer control may be attributed to a reduced rate of electron transport from the cytochrome b6f complex to photosystem I. Photoprotection under increased autumn air temperature conditions appears to be consistent with zeaxanthin-independent antenna quenching through light-harvesting complex II aggregation and a decreased efficiency in energy transfer from the antenna to the photosystem II core. We suggest that models that predict the effect of climate change on the productivity of boreal forests must take into account the interactive effects of photoperiod and elevated temperatures.
Cold hardening in conifers is a physiological process that includes the cessation of growth and long-term changes in metabolism. In evergreen trees of the boreal forest, this process is triggered by short days and potentiated by low temperature (Weiser, 1970  ; Christersson, 1978; Bigras et al., 2001; Li et al., 2002; Beck et al., 2004; Puhakainen et al., 2004). One of the major challenges for overwintering evergreen conifers like Pinus banksiana is balancing the photosynthetic electron transport rate with the rate of consumption of reductant by metabolism (Busch et al., 2007). This is especially important since evergreen conifers retain a substantial amount of chlorophyll throughout the winter and hence continue to absorb light, while at the same time the short photoperiod-, low temperature-induced, down-regulated metabolism is not able to utilize the absorbed energy. Light capture and energy utilization are regulated in a coordinated manner to prevent oxidative damage to the photosynthetic apparatus. Energy balance, defined as photostasis (Öquist and Huner, 2003), is achieved by reorganization of the photosynthetic machinery, including changes in antenna size and organization, adjustments of protein and chlorophyll concentrations, and a range of alternative energy dissipation pathways (Demmig-Adams et al., 1996; Asada, 1999; Öquist and Huner, 2003; Ensminger et al., 2004, 2006; Horton et al., 2005; Sveshnikov et al., 2006; Rumeau et al., 2007).
Under conditions in which more light energy is absorbed than can be utilized, an increase in nonradiative dissipation can be observed as nonphotochemical quenching of chlorophyll fluorescence (NPQ). NPQ is linked to the deepoxidation of violaxanthin to zeaxanthin via the xanthophyll cycle (Demmig-Adams et al., 1996
Not all of the energy absorbed in excess is dissipated in the antenna. Electrons in excess are also used by photorespiration (Wingler et al., 2000
The northern latitudes, habitat of tundra and boreal forests, have experienced a dramatic increase in surface air temperature over the past decades, with increases observed especially in the winter, and this trend is expected to continue (ACIA, 2005
Effects of Photoperiod and Temperature on the Polypeptide Composition of the Photosynthetic Apparatus
Regardless of photoperiod, Lhcb1 levels in LD/HT and SD/HT plants were about 50% lower than in plants exposed to either LD/LT or SD/LT (Fig. 1A
), which is consistent with previous results (Busch et al., 2007
Effects of Photoperiod and Temperature on Photosynthetic Pigments
To test the validity of the quenching mechanism in the model proposed by Busch et al. (2007)
The total size of the xanthophyll cycle pigment pool exhibited only minimal changes between treatments and was only dependent on photoperiod, not on temperature (Fig. 2B). Therefore, decreased levels of DEPS also indicate decreased total amounts of zeaxanthin, as the overall amount of xanthophyll cycle pigments did not increase. In SD/HT- and SD/LT-exposed plants, the pool size was 13% less than in LD/HT plants. LD/LT plants, which showed the highest DEPS, had 23% more xanthophyll cycle pigments than the summer control and about 40% more than the short-day treatments (Fig. 2B). β-Carotene levels were equivalent in the summer and autumn controls (Fig. 2C). However, under SD/HT conditions, we observed about 50% higher levels of β-carotene than in either the summer or autumn control treatments as well as in plants exposed to LD/LT conditions.
PSII Function To examine this in more detail, we assessed the effects of growth regime on the fluorescence induction curves. In all four treatments, fluorescence yield (Fs) initially increased when the light was turned on and subsequently decreased to steady-state levels (Fig. 3 ). In the autumn control as well as in plants exposed to LD/LT, changes in the fluorescence yield were minimal and Fs reached initial minimal fluorescence (F0) levels within about 1 min. These results are consistent with those of Fv/Fm. Consistent with the Fv/Fm data, both summer control (LD/HT) and SD/HT plants exhibited significant increases in Fs upon exposure to actinic light. However, Fs was rapidly quenched within the first minute to levels that were lower than F0. The extent of this quenching appeared to be greater in plants exposed to SD/HT conditions than in the summer control (LD/HT). This effect was reversible when the light was switched off. After turning off the actinic light, a very rapid recovery of Fs close to F0 levels within minutes was observed in SD/HT plants but not in any other treatment. This rate of recovery of Fs was enhanced by applying far-red (FR) light (Fig. 3, inset).
Since there appeared to be a considerable effect of both growth temperature and photoperiod on fluorescence quenching, we examined the effects of growth regime on the light response curves for fluorescence quenching parameters, the redox state of PSII, as well as the effective quantum yield of PSII (Fig. 4 ). Plants grown at low temperature exhibited a significantly lower amount of NPQ than plants grown at high temperature, irrespective of photoperiod (Fig. 4A). At light intensities up to 800 µmol photons m–2 s–1, NPQ was slightly higher in SD/HT than in LD/HT plants. Under low to moderate light intensities, NPQ responded more strongly to an increase in light intensity in SD/HT than in LD/HT plants (Fig. 4A) and thus showed a 1.55-fold maximum quantum efficiency for NPQ (LD/HT, 8.5 ± 1.5 x 10–3 NPQ per µmol photons m–2 s–1; SD/HT, 13.2 ± 2.4 x 10–3), determined as the initial slope of the light saturation curve for NPQ. In plants treated with low temperature, maximum quantum efficiency of NPQ was reduced by 6- to 9-fold irrespective of photoperiod (LD/LT, 1.7 ± 0.1 x 10–3 NPQ per µmol photons m–2 s–1; SD/LT, 1.5 ± 0.3 x 10–3). These trends were confirmed by assessing antenna quenching measured as q0 (Fig. 4B). Excitation pressure (1 – qP), a measure of the reduction state of PSII reaction centers, was lowest in the summer control (LD/HT) and highest in the autumn control (SD/LT) and in plants exposed to LD/LT (Fig. 4C). Over the whole range of light intensities tested, SD/HT plants showed a 1 – qP higher than the summer control but lower than the autumn control. Thus, although low temperature had the greatest effect on excitation pressure, combining summer temperatures with a short photoperiod significantly increased the proportion of closed PSII reaction centers. Figure 4D depicts the effective quantum yield of PSII (Fv'/Fm'). Summer control (LD/HT) plants showed the highest yield across all light intensities. In the autumn control (SD/LT) as well as in LD/LT plants, Fv'/Fm' was substantially decreased. However, changing only the photoperiod from LD/HT to SD/HT caused a decrease in Fv'/Fm' to about half of the summer control value (Fig. 4D).
PSI Function
The summer control (LD/HT) showed the shortest half-time for P700+ reduction after the FR light source was turned off (Fig. 5B). The half-time of the autumn control (SD/LT) was 61% higher, which is an indication of lower PSI cyclic electron transport (Maxwell and Biggins, 1976 ), compared with the summer control (LD/HT). Under SD/HT, we observed an increase in the half-time of P700+ reduction by 91% relative to LD/HT. The slowest P700+ reduction was detected in LD/LT, with an increase of 182% compared with LD/HT. Clearly, exposure to both low temperature and a short photoperiod increased the half-time for dark reduction of P700+ relative to summer control plants. We found a clear temperature dependence in the pool size of electrons in the intersystem electron transport chain (e–/P700), calculated as the area ratio of multiple-turnover to single-turnover flash (Fig. 5C). The intersystem electron pool size in the summer control (LD/HT) was about twice as large as that of either the autumn control or plants exposed to LD/LT. Plants exposed to SD/HT conditions exhibited a pool size similar to that of the summer control.
Changes in the PSII and PSI polypeptide content (Fig. 1, B and C) were also reflected in the 77 K fluorescence emission spectra (Fig. 6A
). Shown are the averages of eight spectra for each treatment for all four treatments. Average spectra illustrate the emission obtained between 650 and 800 nm when excited at 436 nm, normalized to the emission of 685 nm. As expected, fluorescence maxima were detected at 685, 694, and 731 nm in the summer control (LD/HT; Fig. 6A, solid line), the first two representing emissions from the PSII core and the last from PSI (Krause and Weis, 1991
In addition, the difference spectra between the autumn and summer controls (SD/LT – LD/HT) indicated a distinct peak at 676 nm (Fig. 6B). A similar peak at 676 nm was observed in the difference spectra between plants exposed to LD/LT and the summer control (LD/LT – LD/HT). Thus, exposure of P. banksiana to low temperature appears to cause a blue shift in the PSI emission at 731 nm (Fig. 6A) and enhanced fluorescence emission at 676 nm (Fig. 6B). Although exposure of plants to SD/HT caused a minimal blue shift in the PSI emission band at 731 nm, this did result in enhanced emission at 676 nm relative to the summer control, as observed in plants exposed to low temperature (Fig. 6B).
Exposure to SD/HT Conditions Alters the Structure and Composition of the Photosynthetic Apparatus, Causing Inhibition of Photosynthetic Electron Transport
P. banksiana is an important species in boreal evergreen forests. Global climate change measurements over the past decades indicate that the average surface air temperature has increased significantly, and this warming trend is predicted to continue (ACIA, 2005
Where is the site of limitation in photosynthetic electron transport in plants grown in SD/HT conditions? The site of limitation is not k1 (Fig. 7
), since the quenching in the light (Fig. 3) and considerable 1 – qP (Fig. 4C) indicate a buildup of a proton gradient due to PQ reduction, and there were no significant differences in either Fv/Fm or intersystem electron pool size (e–/P700; Fig. 5C) in SD/HT plants compared with summer control plants (LD/HT). Assuming that Cyt b6f is evenly distributed throughout grana and stroma (Albertsson, 2001
LHCII Trimerization Facilitates Zeaxanthin-Independent Quenching of Excess Energy
The xanthophyll cycle generally plays a major role in the photoprotection of plants, and thermal dissipation of excess energy under high light is facilitated by zeaxanthin and antheraxanthin in the antenna of PSII (Adams et al., 2004
Figure 2A shows that plants exposed to SD/HT have by far the lowest DEPS, yet the xanthophyll cycle is fully functional in all four treatments. Whereas in the two low-temperature treatments the xanthophyll pool is largely deepoxidized even in the dark, the two high-temperature treatments exhibit this behavior only under high irradiance. The lower DEPS in SD/HT compared with LD/HT plants is not due to a larger total pool size of the xanthophyll cycle pigments, as can be seen in Figure 2B. Despite the low DEPS, antenna quenching, which should be mediated by zeaxanthin present in the antenna system, was highest in SD/HT (Fig. 4B). Thus, we propose that exposure of plants to SD/HT induces a higher aggregation state of LHCII, which constitutively quenches excess energy through a zeaxanthin-independent mechanism (Busch et al., 2007
In addition, under increasing light intensities, violaxanthin is increasingly converted to zeaxanthin, which provides additional photoprotection via zeaxanthin-dependent NPQ. This mechanism seems to be essential especially for LD/LT, which has the highest DEPS across all light intensities as well as the largest xanthophyll pool, providing constitutive quenching. It is generally accepted that a higher amount of zeaxanthin, most efficiently bound to oligomeric LHCII (Johnson et al., 2007
Changes in 77 K fluorescence emission characteristics of the long-wavelength peak were observed, and a shift of the emission maximum from 731 nm (LD/HT and SD/HT) to 723 nm (SD/LT) and 713 nm (LD/LT) was detected. Although it has been shown that this could be due to changes in the LHCI composition (Bossmann et al., 1997
Plants employ a multiple-step regulation to balance the electron flow with the required rate of ATP and NADPH production under changing environmental conditions. These include D1 turnover, state transitions, NPQ, xanthophyll cycle, chlororespiration, Mehler reaction, cyclic electron flow, and reactive oxygen species production (Scheibe et al., 2005
In summary, we have shown that the inhibition of CO2 assimilation in P. banksiana associated with exposure to elevated temperatures during a short, autumn photoperiod is a consequence of an inhibition of photosynthetic electron transport associated with a decreased PSII/PSI stoichiometry coupled with decreased levels of Rubisco. Furthermore, the results presented are consistent with the model for zeaxanthin-independent antenna quenching presented previously (Busch et al., 2007 ). A major component of photoprotection under a short, autumn photoperiod appears to be antenna quenching through zeaxanthin-independent LHCII aggregation to balance light absorption with a decreased capacity for energy utilization through CO2 assimilation. In P. banksiana, elevated temperatures and a short, autumn photoperiod interact to affect the structure and function of the photosynthetic apparatus, which leads to an inhibition of CO2 assimilation. The results from our experiments using seedlings grown in controlled environments with a relatively large difference in air temperature do not allow any quantitative prediction of how entire boreal forest stands might be affected by the projected increase of autumn air temperature of 4°C to 7°C by 2100 (ACIA, 2005; IPCC, 2007). However, the experiment clearly demonstrates the significance of warm autumn temperatures on the cold-hardening process in conifers that warrant further investigation (e.g. under manipulated field conditions). A net CO2 loss in response to autumn warming was recently observed in the field in northern ecosystems, and the underlying mechanisms and processes have yet to be explained (Piao et al., 2008). Models that predict the effects of climate change on conifers of the boreal forests mostly fail to take into account the interactive effects of increased temperatures and short photoperiod (Heimann and Reichstein, 2008). We suggest that the understanding of such an interaction is of critical importance for future modeling of the response of boreal forests of the northern hemisphere to global warming.
Plant Material and Growth Conditions One-year-old rooted Pinus banksiana (Jack pine) seedlings were obtained from a local nursery (Somerville Seedlings) and planted in a mixture of ProMix (Premier Horticulture) and low-nutrient mineral sand (1:2, v/v). The plants were kept outside underneath a light shelter for 2 years. In the third year, the plants were transferred to controlled environments in late summer 2006 (Conviron growth chambers). Eight 3-year-old plants per treatment were exposed for 4 weeks to either 22°C/18°C (day/night) with a photoperiod of 16 h (LD/HT; representing summer), 22°C/18°C with an 8-h photoperiod (SD/HT; warm autumn conditions), 7°C/5°C with a 16-h photoperiod (LD/LT; cold summer conditions), and 7°C/5°C with an 8-h photoperiod (SD/LT; representing late autumn). The photosynthetic photon flux density was set to 500 µmol photons m–2 s–1 for all four treatments. Although these light intensity and quality values may not accurately reflect field conditions, a factorial design with temperature and photoperiod as the only two variables allows for a qualitative analysis of the effect of increased autumn air temperature on evergreen conifers.
For protein extraction, needles were ground to a fine powder in liquid nitrogen. The proteins were extracted as described in detail previously (Busch et al., 2007
Needles of plants of all treatments were detached around noon, when plants had already been exposed to growth light for 4 h. They were then put on trays with their bottom covered with wet filter paper and exposed to 100, 200, 400, 800, and 1,500 µmol photons m–2 s–1. After 2 h of exposure to the respective light intensities, the samples were frozen in liquid nitrogen and stored at –80°C until further analysis. In addition, one set of samples was taken in the morning before the light was turned on to get dark-adapted samples. Needles were ground to a fine powder in liquid nitrogen, and pigments were extracted for 2 h in the dark on ice in 100% acetone buffered with NaHCO3. The pigment extracts were separated by HPLC as described (Busch et al., 2007
Chlorophyll a fluorescence was measured with a PAM 2100 chlorophyll fluorometer (Heinz Walz). F0 and Fm (maximum fluorescence) were determined in the morning at the end of the dark period. F0' (minimal fluorescence immediately after illumination), Fm' (maximum fluorescence under actinic light), and Ft (transient fluorescence) were recorded after steady-state fluorescence was achieved, usually within a 3-min illumination period. Optimum quantum efficiency of PSII was calculated as Fv/Fm = (Fm – F0)/Fm, and the effective quantum yield of PSII in the light was calculated as Fv'/Fm' = (Fm' – Ft)/Fm' (Genty et al., 1989 To assess the relaxation of F0 quenching, the plants were dark adapted for 20 min with a dark leaf clip and subsequently exposed to 650 µmol photons m–2 s–1 for 4.5 min. The postillumination relaxation of chlorophyll fluorescence was followed at the F0' level after switching off the actinic light with and without simultaneously applying FR light.
The redox state of P700 was determined in vivo using a PAM-101 modulated chlorophyll fluorometer (Heinz Walz) equipped with an ED-P700DW detector following the procedure of Schreiber et al. (1988)
Low-temperature (77 K) chlorophyll fluorescence emission spectra were collected using a PTI QM-7/2006 spectrofluorometer (Photon Technology International) equipped with a double monochromator, R928P red-sensitive photomultiplier tube (Hamamatsu Photonics) and a liquid nitrogen device. Thylakoid membranes suspended in a buffer containing 35 mM Tricine (pH 7.8), 0.3 M sorbitol, 7 mM NaCl, and 3.5 mM MgCl2 were dark adapted for 30 min and frozen in the presence of 30% glycerol before the measurements. The chlorophyll concentration was 5 µg mL–1. Corrected fluorescence emission spectra were excited at 436 nm and recorded from 650 to 800 nm using a slit width of 2.5 nm for both excitation and emission. All fluorescence spectra were additionally corrected by subtracting the medium blank.
The effects of daylength and temperature on photosynthetic properties were statistically analyzed by two-way ANOVA at P < 0.05 using SPSS version 14.0. All significant differences mentioned in the text and the figures refer to the two-way ANOVA results.
We are grateful to Dr. P.E. Jensen (Royal Veterinary and Agricultural University, Copenhagen) for providing the PSI antibody. We thank Marc Possmayer (University of Western Ontario, London, Canada) for assisting with the data collection. Received February 9, 2008; accepted March 18, 2008; published March 28, 2008.
1 This work was supported by a Marie-Curie Fellowship of the European Union (PhysConFor, contract no. MOIF–CT–2004-002476) to I.E. and by grants from the Natural Sciences and Engineering Research Council of Canada and the Canada Foundation for Innovation to N.P.A.H.  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Ingo Ensminger (ingo.ensminger{at}ctp.uni-freiburg.de).
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.108.117598 * Corresponding author; e-mail ingo.ensminger{at}ctp.uni-freiburg.de.
ACIA (2005) Arctic Climate Impact Assessment. Cambridge University Press, Cambridge, UK Adams WW, Zarter CR, Ebbert V, Demmig-Adams B (2004) Photoprotective strategies of overwintering evergreens. Bioscience 54: 41–49[CrossRef][Web of Science] Albertsson PA (2001) A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci 6: 349–354[CrossRef][Web of Science][Medline] Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50: 601–639[CrossRef][Web of Science] Asada K (2000) The water-water cycle as alternative photon and electron sinks. Philos Trans R Soc Lond B Biol Sci 355: 1419–1430 Asada K, Heber U, Schreiber U (1993) Electron flow to the intersystem chain from stromal components and cyclic electron flow in maize chloroplasts, as detected in intact leaves by monitoring redox change of P700 and chlorophyll fluorescence. Plant Cell Physiol 34: 39–50 Beck EH, Heim R, Hansen J (2004) Plant resistance to cold stress: mechanisms and environmental signals triggering frost hardening and dehardening. J Biosci 29: 449–459[CrossRef][Web of Science][Medline] Becker B, Holtgrefe S, Jung S, Wunrau C, Kandlbinder A, Baier M, Dietz KJ, Backhausen JE, Scheibe R (2006) Influence of the photoperiod on redox regulation and stress responses in Arabidopsis thaliana L. (Heynh.) plants under long- and short-day conditions. Planta 224: 380–393[CrossRef][Web of Science][Medline] Bigras FJ, Ryyppö A, Lindström A, Stattin E (2001) Cold acclimation and deacclimation of shoots and roots of conifer seedlings. In FJ Bigras, SJ Colombo, eds, Conifer Cold Hardiness. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 57–88 Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbency changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25: 173–185[CrossRef][Web of Science] Bossmann B, Knoetzel J, Jansson S (1997) Screening of chlorina mutants of barley (Hordeum vulgare L.) with antibodies against light-harvesting proteins of PS I and PS II: absence of specific antenna proteins. Photosynth Res 52: 127–136[CrossRef][Web of Science] Busch F, Hüner NPA, Ensminger I (2007) Increased air temperature during simulated autumn conditions does not increase photosynthetic carbon gain but affects the dissipation of excess energy in seedlings of the evergreen conifer Jack pine. Plant Physiol 143: 1242–1251 Cantrell A, McGarvey DJ, Truscott TG, Rancan F, Bohm F (2003) Singlet oxygen quenching by dietary carotenoids in a model membrane environment. Arch Biochem Biophys 412: 47–54[CrossRef][Web of Science][Medline] Carol P, Stevenson D, Bisanz C, Breitenbach J, Sandmann G, Mache R, Coupland G, Kuntz M (1999) Mutations in the Arabidopsis gene immutans cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell 11: 57–68 Christersson L (1978) The influence of photoperiod and temperature on the development of frost hardiness in seedlings of Pinus silvestris and Picea abies. Physiol Plant 44: 288–294[CrossRef] Cruz JA, Salbilla BA, Kanazawa A, Kramer DM (2001) Inhibition of plastocyanin to P700+ electron transfer in Chlamydomonas reinhardtii by hyperosmotic stress. Plant Physiol 127: 1167–1179 Demmig-Adams B, Adams WW (2002) Antioxidants in photosynthesis and human nutrition. Science 298: 2149–2153 Demmig-Adams B, Gilmore AM, Adams WW (1996) Carotenoids 3. In vivo functions of carotenoids in higher plants. FASEB J 10: 403–412[Abstract] Desquilbet TE, Duval JC, Robert B, Houmard J, Thomas JC (2003) In the unicellular red alga Rhodella violacea iron deficiency induces an accumulation of uncoupled LHC. Plant Cell Physiol 44: 1141–1151 Ensminger I, Busch F, Hüner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126: 28–44[CrossRef] Ensminger I, Schmidt L, Lloyd J (2008) Soil temperature and intermittent frost modulate the rate of recovery of photosynthesis in Scots pine under simulated spring conditions. New Phytol 177: 428–442[Web of Science][Medline] Ensminger I, Sveshnikov D, Campbell DA, Funk C, Jansson S, Lloyd J, Shibistova O, Öquist G (2004) Intermittent low temperatures constrain spring recovery of photosynthesis in boreal Scots pine forests. Glob Change Biol 10: 995–1008[CrossRef] Gaspar L, Sarvari E, Morales F, Szigeti Z (2006) Presence of ‘PSI free’ LHCI and monomeric LHCII and subsequent effects on fluorescence characteristics in lincomycin treated maize. Planta 223: 1047–1057[CrossRef][Web of Science][Medline] 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 Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218: 107–114[CrossRef][Web of Science][Medline] Haehnel W (1984) Photosynthetic electron transport in higher plants. Annu Rev Plant Physiol Plant Mol Biol 35: 659–693[CrossRef][Web of Science] Heimann M, Reichstein M (2008) Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451: 289–292[CrossRef][Medline] Horton P, Wentworth M, Ruban A (2005) Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching. FEBS Lett 579: 4201–4206[CrossRef][Web of Science][Medline] Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3: 224–230[CrossRef][Web of Science] IPCC (2007) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK Ivanov AG, Morgan RM, Gray GR, Velitchkova MY, Huner NPA (1998) Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. FEBS Lett 430: 288–292[CrossRef][Web of Science][Medline] Johnson MP, Havaux M, Triantaphylides C, Ksas B, Pascal AA, Robert B, Davison PA, Ruban AV, Horton P (2007) Elevated zeaxanthin bound to oligomeric LHCII enhances the resistance of Arabidopsis to photooxidative stress by a lipid-protective, antioxidant mechanism. J Biol Chem 282: 22605–22618 Kirchhoff H, Schöttler MA, Maurer J, Weis E (2004) Plastocyanin redox kinetics in spinach chloroplasts: evidence for disequilibrium in the high potential chain. Biochim Biophys Acta 1659: 63–72[Medline] Klimov SV (2003) Cold hardening of plants is a result of maintenance of an increased photosynthesis/respiration ratio at low temperatures. Biol Bull 30: 48–52[CrossRef] Klughammer C, Schreiber U (1991) Analysis of light-induced absorbency changes in the near-infrared spectral region. 1. Characterization of various components in isolated chloroplasts. Z Naturforsch [C] 46: 233–244 Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42: 313–349[CrossRef][Web of Science] Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56: 337–346 Li CY, Puhakainen T, Welling A, Vihera-Aarnio A, Ernstsen A, Junttila O, Heino P, Pavla ET (2002) Cold acclimation in silver birch (Betula pendula). Development of freezing tolerance in different tissues and climatic ecotypes. Physiol Plant 116: 478–488[CrossRef] Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265–275 Maxwell PC, Biggins J (1976) Role of cyclic electron transport in photosynthesis as measured by the photoinduced turnover of P700 in vivo. Biochemistry 15: 3975–3981[CrossRef][Web of Science][Medline] Moseley JL, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S, Hippler M (2002) Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO J 21: 6709–6720[CrossRef][Web of Science][Medline] Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching : a response to excess light energy. Plant Physiol 125: 1558–1566 Öquist G, Huner NPA (2003) Photosynthesis of overwintering evergreen plants. Annu Rev Plant Biol 54: 329–355[CrossRef][Medline] Peltier G, Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53: 523–550[CrossRef][Medline] Piao SL, Ciais P, Friedlingstein P, Peylin P, Reichstein M, Luyssaert S, Margolis H, Fang JY, Barr A, Chen AP, et al (2008) Net carbon dioxide losses of northern ecosystems in response to autumn warming. Nature 451: 49–53[CrossRef][Medline] Puhakainen T, Li CY, Boije-Malm M, Kangasjarvi J, Heino P, Palva ET (2004) Short-day potentiation of low temperature-induced gene expression of a C-repeat-binding factor-controlled gene during cold acclimation in silver birch. Plant Physiol 136: 4299–4307 Queval G, Issakidis-Bourguet E, Hoeberichts FA, Vandorpe M, Gakiere B, Vanacker H, Miginiac-Maslow M, Van Breusegem F, Noctor G (2007) Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression, and define photoperiod as a crucial factor in the regulation of H2O2-induced cell death. Plant J 52: 640–657[CrossRef][Web of Science][Medline] Quiles MJ (2006) Stimulation of chlororespiration by heat and high light intensity in oat plants. Plant Cell Environ 29: 1463–1470[CrossRef][Medline] Rees D, Noctor GD, Horton P (1990) The effect of high-energy-state excitation quenching on maximum and dark level chlorophyll fluorescence yield. Photosynth Res 25: 199–211[CrossRef][Web of Science] Rosso D, Ivanov AG, Fu A, Geisler-Lee J, Hendrickson L, Geisler M, Stewart G, Krol M, Hurry V, Rodermel SR, et al (2006) IMMUTANS does not act as a stress-induced safety valve in the protection of the photosynthetic apparatus of Arabidopsis during steady-state photosynthesis. Plant Physiol 142: 574–585 Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ 30: 1041–1051[CrossRef][Medline] Saxe H, Cannell MGR, Johnsen B, Ryan MG, Vourlitis G (2001) Tree and forest functioning in response to global warming. New Phytol 149: 369–399[CrossRef][Web of Science] Scheibe R, Backhausen JE, Emmerlich V, Holtgrefe S (2005) Strategies to maintain redox homeostasis during photosynthesis under changing conditions. J Exp Bot 56: 1481–1489 Schöttler MA, Kirchhoff H, Weis E (2004) The role of plastocyanin in the adjustment of the photosynthetic electron transport to the carbon metabolism in tobacco. Plant Physiol 136: 4265–4274 Schreiber U, Bilger W (1987) Rapid assessment of stress effects on plant leaves by chlorophyll fluorescence measurements. In JD Tenhunen, FM Catarino, OL Lange, WC Oechel, eds, Plant Response to Stress: Functional Analysis in Mediterranean Ecosystems, Vol 15. NATO Advanced Science Institute Series, Berlin, pp 27–53 Schreiber U, Klughammer C, Neubauer C (1988) Measuring P700 absorbance changes around 830 nm with a new type of pulse-modulation system. Z Naturforsch [C] 43: 686–698 Shahbazi M, Gilbert M, Labouré A, Kuntz M (2007) The dual role of the plastid terminal oxidase (PTOX) in tomato. Plant Physiol 145: 691–702 Slot M, Wirth C, Schumacher J, Mohren GMJ, Shibistova O, Lloyd J, Ensminger I (2005) Regeneration patterns in boreal Scots pine glades linked to cold-induced photoinhibition. Tree Physiol 25: 1139–1150 Streb P, Josse EM, Gallouet E, Baptist F, Kuntz M, Cornic G (2005) Evidence for alternative electron sinks to photosynthetic carbon assimilation in the high mountain plant species Ranunculus glacialis. Plant Cell Environ 28: 1123–1135[CrossRef] Sveshnikov D, Ensminger I, Ivanov AG, Campbell D, Lloyd J, Funk C, Hüner NPA, Öquist G (2006) Excitation energy partitioning and quenching during cold acclimation in Scots pine. Tree Physiol 26: 325–336[Web of Science][Medline] Telfer A (2005) Too much light? How beta-carotene protects the photosystem II reaction centre. Photochem Photobiol Sci 4: 950–956[CrossRef][Web of Science][Medline] Vandorssen RJ, Plijter JJ, Dekker JP, Denouden A, Amesz J, Vangorkom HJ (1987) Spectroscopic properties of chloroplast grana membranes and of the core of photosystem-II. Biochim Biophys Acta 890: 134–143 Wakasugi T, Tsudzuki J, Ito S, Nakashima K, Tsudzuki T, Sugiura M (1994) Loss of all Ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proc Natl Acad Sci USA 91: 9794–9798 Weiser CJ (1970) Cold resistance and injury in woody plants: Knowledge of hardy plant adaptations to freezing stress may help us to reduce winter damage. Science 169: 1269–1278 Wentworth M, Ruban AV, Horton P (2004) The functional significance of the monomeric and trimeric states of the photosystem II light harvesting complexes. Biochemistry 43: 501–509[CrossRef][Web of Science][Medline] White A, Cannell MGR, Friend AD (2000) The high-latitude terrestrial carbon sink: a model analysis. Glob Change Biol 6: 227–245[CrossRef] Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond B Biol Sci 355: 1517–1529 Zhang H, Goodman HM, Jansson S (1997) Antisense inhibition of the photosystem I antenna protein Lhca4 in Arabidopsis thaliana. Plant Physiol 115: 1525–1531[Abstract] Related articles in Plant Physiol.:
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, 
, and * indicate significant differences due to daylength, temperature, and their interactive effect, respectively. One symbol, P < 0.05; two symbols, P < 0.01; three symbols, P < 0.001.
A820/A820), than the summer control (LD/HT; 
max = 715 nm, 10 W m–2; Schott filter RG 715) was provided by the 101 FR light source. Multiple-turnover (50 ms) and single-turnover (half-peak width, 14 µs) saturating flashes were applied with the Walz XMT-103 power unit and the Walz XST-103 control unit. The redox state of P700 was measured on detached needles as the 
