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RESEARCH PAPER |
Effect of cold acclimation on the photosynthetic performance of two ecotypes of Colobanthus quitensis (Kunth) Bartl.
1Departamento de Botánica, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Correo 3, Concepción, Chile
2Department of Biology and The Biotron, University of Western Ontario, London, Ontario, Canada N6A 5B7
* To whom correspondence should be addressed. E-mail: lebravo{at}udec.cl
Received 27 April 2007; Revised 31 July 2007 Accepted 6 August 2007
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Abstract |
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The effects of cold acclimation of two ecotypes (Antarctic and Andes) of Colobanthus quitensis (Kunth) Bartl. Caryophyllaceae on their photosynthetic characteristics and performance under high light (HL) were compared. Non-acclimated plants of the Antarctic ecotype exhibited a higher (34%) maximal rate of photosynthesis than the Andes ecotype. In cold-acclimated plants the light compensation point was increased. Dark respiration was significantly increased during the exposure to 4 °C in both ecotypes. Cold-acclimated Antarctic plants showed higher
PSII and qP compared with the Andes ecotype. In addition, the Antarctic ecotype exhibited higher heat dissipation (NPQ), especially in the cold-acclimated state, which was mainly associated with the fast relaxing component of non-photochemical quenching (NPQF). By contrast, the Andes ecotype exhibited a lower NPQF and a significant increase in the slowly relaxing component (NPQs) at low temperature and HL, indicating higher sensitivity to low temperature-induced photoinhibition. Although the xanthophyll cycle was fully operational in both ecotypes, cold-acclimated Antarctic plants exposed to HL exhibited higher epoxidation state of the xanthophyll cycle pigments (EPS) compared with the cold-acclimated Andes ecotype. Thus, the photosynthetic apparatus of the Antarctic ecotype operates more efficiently than that of the Andes one, under a combination of low temperature and HL. The ecotype differences are discussed in relation to the different climatic conditions of the two Colobanthus. Key words: Antarctic plants, heat dissipation, low temperature, non-photochemical quenching, photoinhibition, photosynthesis
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Introduction |
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Excess irradiance may be harmful for plants that are unable to balance the absorbed/utilized energy ratio (Huner et al., 1998). This may be even worse when plants are exposed simultaneously to high light and low temperatures which decrease carbon and other enzymatic assimilation processes, creating a greater imbalance because light absorption is largely temperature insensitive (Huner et al., 1998). However, cold acclimation decreases susceptibility to photoinhibition (Krause, 1994) by causing several metabolic alterations and producing changes at the chloroplast level that may restore the energy balance. A widely accepted hypothesis is that cold acclimation may improve the ability of plants to maintain metabolism at low temperature by keeping QA, the primary quinone electron acceptor, more oxidized (Huner et al., 1998; Melis, 1999). Other plants use different strategies. For instance, cold-acclimated Pinus contorta L. partially loses PSII reaction centres, reduces needle chlorophyll per unit area, and reduces its daily carbon gain (Savitch et al., 2002). All these changes are accompanied by an increased and sustained capacity for heat dissipation through non-photochemical quenching. It is also known that xanthophyll levels increase during cold acclimation and the half-time to develop qE decreases (Krause, 1994). All these cold acclimation-induced changes may help to restore the energy balance and hence reduce the incidence of low-temperature-induced photodamage.
Colobanthus quitensis (Kunth) Bartl. Caryophyllaceae extends from the Maritime Antarctic and along the Andes Mountains to Ecuador, with one site in Mexico (Lewis Smith, 2003). It usually grows above 2500 masl in the Andes Mountains. The Antarctic C. quitensis plants have been described as morphologically and physiologically adapted to succeed in these cold environments (Mantovani and Vieira, 2000; Perez-Torrez et al., 2004). For instance, its photosynthetic machinery is well adapted to low temperature (Xiong et al., 1999, 2000). The photosynthetic responses of a C. quitensis population from the Andes of Central Chile have been recently studied in the field (Casanova-Katny et al., 2006) and ecotypic differentiation of the Antarctic and Andes populations has been proposed (Gianoli et al., 2004; Sierra-Almeida et al., 2007).
Antarctic and Andean environments can differ significantly in solar radiation and temperature during the summer. PFD in the Antarctic summer can go up to 1500 µmol photons m–2 s–1 on sunny days; however, sunny days are infrequent, accounting for less than 20% in summer (Xiong et al., 1999; Xiong and Day, 2001). Average temperature in the Antarctic summer is about 3 °C (Alberdi et al., 2002). In the Andes mountains, PFD in summer is frequently as high as 2500 µmol photons m–2 s–1 and the average temperature at 2600 masl is about 13 °C (Cavieres and Arroyo, 1999). These differences in PFD and temperature regime during the growing season could have resulted in selection for altered plasticity of the photosynthetic apparatus to cope with high light and low temperature in Andes and Antarctic ecotypes, respectively. In order to test this hypothesis, the two ecotypes of C. quitensis described above (Gianoli et al., 2004) were grown, one from Antarctica (sea level) and the other from the Andes (2700 masl), under the same controlled laboratory conditions. The purpose of this study was to assess the effect of cold acclimation on the capacity of these ecotypes of C. quitensis to cope with excess irradiance and low temperature-induced photoinhibition.
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Plant material
Antarctic plants of C. quitensis were collected on King George Island, Maritime Antarctic (sea level; 62°10' S; 58°29’ W) and transported to the laboratory. Plants of C. quitensis, ecotype Andes were collected on the slopes of Cerro La Parva (2650 masl; 33°19' S; 70°17' W). Both ecotypes were reproduced vegetatively in plastic pots, using a soil:peat mixture (3:1 v/v) and maintained at 13–15 °C in a growth chamber (Forma Scientific Inc.) with a photon flux density (PFD) of 120±20 µmol photons m–2 s–1 at the top of the canopy and a 16/8 h light/dark period. The light source consisted of cool-white fluorescent tubes F40CW (General Electric). Plants were fertilized with Phostrogen® (Solaris) using 0.2 g l–1 once every two weeks. One group of both Antarctic and Andes plants was cold-acclimated at 4 °C for 21 d. This treatment reduced the LT50 from –7 °C to –10 °C and from –7 °C to –14.5 °C in Andes and Antarctic ecotypes, respectively (Gianoli et al., 2004). Mature pre-existing leaves were sampled for each analysis.
Photoinhibitory treatment
Cold-acclimated and non-acclimated plants were subjected to high light treatment (HL) 1600±50 µmol photons m–2 s–1 and low light treatment (LL) 120±20 µmol m–2 s–1 both at low temperature (4 °C) for 2 h. Low and high PFD were provided by 1000 W halogen lamps. Pigment composition was monitored at the end of each treatment.
Net photosynthesis
Photosynthetic oxygen evolution was measured in detached leaves with a gas phase oxygen electrode unit, using an Oxylab and an oxygen electrode chamber (Model LD2/3 Hansatech Instruments Ltd., King's Lynn, Norfolk, UK). Measurements were performed at either 4 °C and/or 15 °C under saturating CO2 and irradiances over the range of 0–800 µmol m–2 s–1 given by an array of red light-emitting diodes, (Model LH36/2R, Hansatech Instruments Ltd., King's Lynn, Norfolk, UK). Detached leaves were adapted for 10 min to each temperature. Quantum yield of oxygen evolution (
), maximum rate of net photosynthesis (Pnmax), and light compensation point (LCP) were determined on the bases of incident light measured with the quantum sensor (QSRED, Hansatech).
Fluorescence measurements
C. quitensis, possess narrow and short leaves, especially the Antarctic ecotype. This makes the fluorescence measurements in attached leaves difficult to perform. For this reason, in order to conduct measurements in the same way for both ecotypes, fully developed detached leaves from control and HL-treated cold-acclimated and non-acclimated plants were aligned parallel and immobilized using transparent tape and then dark-adapted for 30 min using the instrument leaf-clips to obtain open PSII centres to ensure maximum photochemical efficiency. Chlorophyll fluorescence recordings and calculations were performed by a pulse-amplitude modulated fluorimeter (FMS 2, Hansatech, Instruments Ltd., Norfolk, UK) according to Schreiber et al. (1986). The fibre-optic and its adapter were fixed to a ring located over the clip at about 10 mm from the sample and the different light pulses (see below) were applied following the standard routines programmed within the instrument. Minimal fluorescence (Fo) with all PSII reaction centres in the open state was determined by applying a weak modulated light (0.4 µmol m–2 s–1). Maximal fluorescence (Fm) with all PSII reaction centres in the closed state was induced by a 0.8 s saturating pulse of white light (9000 µmol m–2 s–1). After 10 s, the actinic light was turned on and the same saturating pulse described previously was applied every 20 s, until steady-state photosynthesis was reached in order to obtain Fs and 
. Finally, 
was measured after turning the actinic light off and applying a 2 s far red light pulse. Definitions of fluorescence parameters (qP, 
, and PSII) were used as described by van Kooten and Snel (1990), Non-photochemical quenching (NPQ) was calculated according to Walters and Horton (1991) Fluorescence measurements were performed at different actinic light intensities which was controlled by the light source of the FMS 2 apparatus and applied through an optic fibre. Light intensity at the leaf surface was calibrated using a LI-250 light meter (Li-Cor).
Determination of NPQ components
The components of non-photochemical quenching (NPQ) were determined at 4 °C and 15 °C in leaves of cold-acclimated and non-acclimated plants from both the Antarctic and Andes ecotypes of C. quitensis. NPQ was resolved into slow (NPQs) and fast (NPQF) components (equivalent to qI and qE, respectively) essentially as described by Walters and Horton (1991) by analysing the kinetics of Fm recovery after actinic light has been turned off. NPQs=(Fm–Fmr)/Fmr and NPQF=(Fm–)–(Fm–Fmr). Fmr (the value of Fm that would have been attained if only slowly relaxing quenching had been present) was obtained by extrapolation in a semi-logarithmic plot of maximum fluorescence yield versus time of data points recorded toward the end of the relaxation back to the time where the actinic light was removed.
Pigments
C. quitensis leaves were cut and placed immediately in a cold mortar. A tip of spatula (approximately 1 mg) of CaCO3 was added before grinding in 100% (v/v) acetone at 4 °C under dim light. The supernatant was filtered through a 0.22 µm syringe filter and samples were stored at –80 °C until analysed. Pigments were separated and quantified by HPLC analysis as described previously (Ivanov et al., 1995) with some modifications. The HPLC system consisted of the Beckman System Gold programmable solvent module 126, a diode array detector module 168 (Beckman Instruments, San Ramon, California, USA), CSC-Spherisorb ODS-1 reverse-phase column (5 µm particle size, 25x0.46 cm ID) with an Upchurch Perisorb A guard column (both columns from Chromatographic Specialties Inc., Concord, Ontario, Canada). Pigments were eluted isocratically for 6 min with acetonitrile:methanol:0.1 M TRIS–HCl (pH 8.0), (72:8:3.5, by vol.), followed by a 2 min linear gradient to 100% methanol:hexane (4:1, v/v), which continued isocratically for 4 min with a flow rate of 2 ml min–1. Absorbance was monitored at 440 nm. Retention times and response factors of Chl a, Chl b, lutein, and β-carotene were determined by injection of known amounts of pure standards purchased from Sigma (St Louis, MO, USA). The retention times of zeaxanthin, antheraxanthin, violaxanthin and neoxanthin were determined by using pigments purified by thin-layer chromatography as described by Diaz et al. (1990). Epoxidation state (EPS) of the pigments pool was estimated as: EPS=(0.5A+V)/(V+A+Z), where A is antheraxanthin, V is violaxanthin, and Z is zeaxanthin.
Statistics
Differences in parameters extracted from light response curves of net photosynthesis were statistically evaluated using three-way ANOVA (level of significance was P <0.05) using growth condition, ecotype, and measurement temperature as factors. Fluorescence parameters and pigment contents were statistically evaluated using three-way ANOVA (level of significance was P <0.05) with growth condition, ecotype, and light intensity as factors. Tukey post-hoc tests were used to identify those means with significant differences. Statistical analyses were performed using SigmaStat 3.1 (Systat Software, Inc. Richmond CA, USA).
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Net photosynthesis
Light response curves of net photosynthesis (Pn) were performed in cold-acclimated and non-acclimated plants of both Antarctic and Andes ecotypes (Fig. 1). Pn was measured at 4 °C and 15 °C (Table 1). The Antarctic ecotype a exhibited higher maximum rate of net photosynthesis (Pnmax) value than the Andes ecotype, regardless of the measuring and/or growth temperature. The highest net photosynthesis was registered in non-acclimated Antarctic plants exposed to 15 °C, reaching 8.95 µmol O2 m–2 s–1. Cold acclimation did not significantly affect Pnmax of either ecotype (P >0.05) (Table 1). However, measuring temperature had a significant and differential effect on Pn and higher Pnmax values were observed at 15 °C than at 4 °C. This effect depended on the ecotype and the increase of Pnmax in cold-acclimated Andes plants exposed to 15 °C was 51%, with respect to 4 °C, while in the Antarctic plants this increase was significantly higher (73%) (Table 1). This clearly implies an increased capacity for photosynthesis in the cold-acclimated Antarctic ecotype.
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Cold acclimation significantly increased LCP in both ecotypes (Table 1), which is associated with an increase in dark respiration observed in cold-acclimated plants. At either temperature, LCP was higher in the Andes ecotype, except in non-acclimated plants exposed to 15 °C, where the Andes ecotype exhibited a lower LCP (7 µmol photons m–2 s–1) than the Antarctic ecotype (13 µmol photons m–2 s–1). Low measuring temperature increased LCP in both ecotypes independently of growth temperature, with the exception observed in the non-acclimated Antarctic ecotype which exhibited non-significant statistical differences between LCP at 4 °C and 15 °C. The effect of cold acclimation on
depends on the ecotype and measuring temperatures. The was higher in non-acclimated plants of the Andes ecotype at 15 °C and it was reduced upon cold acclimation. On the other hand, the Antarctic ecotype exhibited a tendency to increase upon cold acclimation at both measuring temperatures, although no statistically significant differences (P >0.05) were observed in this ecotype (Table 1).
Effect of light and growth temperature on steady state fluorescence yield
Light response curves of quantum yield of PSII (PSII), in the Andes and Antarctic ecotypes of C. quitensis under non-acclimated and cold-acclimated conditions, showed a decline of PSII with increasing PFD (Fig. 2A). Under cold-acclimated conditions, the Antarctic ecotype exhibited a significantly higher (P <0.05) quantum yield of PSII, compared with the Andes plants, except at the highest PFD (Fig. 2A). Under non-acclimated conditions, the Andes ecotype showed a slower decrease of PSII than the Antarctic ecotype from 200 to 700 µmol photons m–2 s–1 of PFD (Fig. 2B). The Antarctic ecotype also had a higher proportion of open reaction centres measured as Fv'/Fm' in the cold-acclimated state (Fig. 2C), while it showed no mayor differences with the Antarctic ecotype under non-acclimated conditions (Fig. 2D).
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Cold-acclimated Antarctic plants demonstrated significantly higher (P <0.05) photochemical quenching (qP) compared with the Andes ecotype (Fig. 2E). The opposite effect was observed under non-acclimated conditions, where the Andes ecotype had higher values of qP than the Antarctic one in the range of 200–800 µmol photons m–2 s–1 (Fig. 2F).
Growth and measuring temperature and light effects on NPQ components
NPQ and its fast and slow relaxation components were studied in both ecotypes of C. quitensis under cold-acclimated and non-acclimated conditions at different PFD and at two different temperatures, 15 °C and 4 °C, which are the optimum temperature for photosynthesis and the temperature used for cold acclimation, respectively. In general, cold-acclimated plants exhibited higher NPQ values at lower PFD than non-acclimated ones when measured at 15 °C (Fig. 3B), while no major differences were observed at 4 °C (Fig. 3A). Cold-acclimated Antarctic plants exposed to the 15 °C measuring temperature exhibited the highest capacity for NPQ, reaching values over 5.0 at high PFD (Fig. 3A). Non-acclimated leaves of both C. quitensis ecotypes exposed to the low measuring temperature (4 °C) showed a greater capacity for NPQ at lower actinic light and a lower increase with increasing the light intensity than at 15 °C, reaching similar NPQ values at high PFD under both growth temperature regimes (Fig. 3B).
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The fast relaxing component of the non-photochemical quenching (NPQF), which is associated with the energy-dependent NPQ (qE), reached the highest values at the 15 °C measuring temperature, being higher in the Antarctic ecotype at both measuring and growth temperatures at PFDs higher than 600 µmol photons m–2 s–1 (Fig. 3C, D). The cold-acclimated Andes ecotype measured at 4 °C exhibited little NPQF, which was saturated at the lowest light intensity of about 100 µmol photons m–2 s–1. In non-acclimated plants, NPQF was lower when measured at 4 °C than at 15 °C (Fig. 3D) and was similar to that of cold-acclimated plants of the Antarctic ecotype measured at 4 °C. Cold-acclimated plants exhibited minimal differences in NPQs regardless of the measuring temperature (Fig. 3E). No significant differences in NPQs were observed between the two non-acclimated ecotypes measured at 15 °C, compared with cold-acclimated plants (Fig. 3F). By contrast, there was a significantly higher NPQs in both ecotypes when the measuring temperature was 4 °C, with respect to 15 °C. The highest NPQ values were observed in non-acclimated Andes plants at high PFD (Fig. 3F).
Pigments and xanthophyll cycle under photoinhibitory conditions
Chlorophylls and carotenoids were measured in non-inhibited control (LL) and photoinhibited (HL) at 4 °C leaves of both Antarctic and Andes ecotypes of C. quitensis under non-acclimated and cold-acclimated growth conditions. In general, plants of the Andes ecotype showed lower total chlorophyll (Chl a+b) and carotenoid contents than the Antarctic ecotype independently of light and temperature treatments (Table 2). Cold-acclimated plants of both ecotypes also exhibited lower chlorophyll and carotenoid contents, the lowest content of pigments being observed in HL-treated cold-acclimated Andean plants, which also showed the lowest Chl/Car ratio (Table 2). Chl a/Chl b ratios were similar for both ecotypes in all treatments. Cold-acclimated and non-acclimated plants of both ecotypes showed an increase of chlorophylls and carotenoids under HL compared with LL treatment, and this increase was smaller in cold-acclimated plants (Table 2). This effect was not observed for the total pool of xanthophyll cycle pigments (VAZ). On the contrary, significantly higher levels of the VAZ pool (P <0.05) were observed in either cold-acclimated or non-acclimated C. quitensis plants of both ecotypes under HL conditions. The highest VAZ content was observed in the non-acclimated HL-treated Antarctic ecotype (Fig. 4). These results clearly indicate that some de novo synthesis of xanthophyll cycle pigments occurs during the HL treatments in both ecotypes, especially in non-acclimated plants. The epoxidation state (EPS) of the xanthophyll pool, which represents the inverse of the efficiency of violaxanthin conversion to zeaxanthin via antheraxanthin (Demmig-Adams and Adams III, 1996) was about 0.9 for both ecotypes at LL with no significant effect of cold-acclimation (Fig. 4). As expected, HL treatment caused a significant decrease in EPS reaching, in both non-acclimated ecotypes and in cold-acclimated Andes plants, values around 0.4 (Fig. 4B). Interestingly, cold-acclimated Antarctic plants showed a significantly (P <0.05) higher EPS (0.62) corresponding to less efficient conversion of violaxanthin to zeaxanthin under HL exposure than non-acclimated ones (Fig. 4).
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Concomitant with earlier studies, net O2 evolution measured in laboratory-grown C. quitensis plants was higher in the Antarctic ecotype compared with the Andes one (Table 1) and the values for Pnmax were similar to those observed in field experiments. For instance, Amax values of 8 µmol CO2 m–2 s–1 have been reported in the Antarctic plants (Xiong et al., 1999), while lower net photosynthesis (5.0 µmol CO2 m–2 s–1) was measured in plants from the Andes under field conditions (Casanova-Katny et al., 2006). It has been suggested that the moderately higher rate of net photosynthesis in the Antarctic ecotype may be associated with the thicker leaves of this ecotype (Gianoli et al., 2004). This is consistent with the higher chlorophyll content in the Antarctic ecotype on fresh weight bases (Table 2) and the lack of significant differences between the Antarctic and Andes ecotypes when net photosynthesis was expressed on chlorophyll bases (data not shown). The higher net photosynthesis and lower LCP at low temperature demonstrates the ability of the Antarctic ecotype to maximize its photosynthetic performance, which optimizes the energy allocated for growth and reproduction in a short period with favourable temperature and very unstable light supply for photosynthesis (Xiong and Day, 2001). It is interesting to note that in cold-acclimated plants of C. quitensis dark respiration was enhanced (Table 1). This confirms a previous observation of CO2 uptake in the cold-acclimated Antarctic ecotype of C. quitensis measured at low temperature (Pérez-Torres et al., 2006). The increase in dark respiration caused by cold-acclimation may be associated with the ability of this species to survive several months covered by snow. In fact, it has been shown that, in over-wintering winter wheat, the activity of respiratory enzymes is increased during the autumn to maintain the adenylate energy charge (Sagisaka et al., 1991). Lower growth temperature exacerbates the alternative oxidase pathway (Vanlerberghe and McIntosh, 1992). Overexpression of alternative oxidase has been shown to alleviate oxidative stress in transgenic A. thaliana under low temperature (Sugie et al., 2006). Furthermore, it has recently been reported that up-regulation of mitochondrial alternative oxidase occurs concomitantly with chloroplast over-reduction by excess light in A. thaliana (Yoshida et al., 2007). These authors suggest that the alternative pathway can dissipate the excess reducing equivalents, which are transported from the chloroplasts, and serve in efficient photosynthesis. It is not yet clear whether this increased dark respiration in cold-acclimated C. quitensis is due to alternative oxidase up-regulation.
Steady-state fluorescence yield and fluorescence quenching analyses demonstrated that the photosynthetic apparatus of both non-acclimated C. quitensis ecotypes responded similarly to light intensity. However, cold acclimation induced differential responses of PSII photochemical performance measured as PSII, , and qP in these two ecotypes. Overall, growth at low temperature (cold acclimation) increased photochemical performance of the Antarctic ecotype showing higher values of PSII, , and qP, while PSII photochemistry in cold-acclimated Andes plants was slightly suppressed (Fig. 2A–F).
In both ecotypes, heat dissipation of absorbed excess light energy (NPQ) was mostly associated with the fast relaxing component, or NPQF (Fig. 3) related to the 
pH- and zeaxanthin-dependent energy quenching (qE) within the LHCII antenna (Walters and Horton, 1991; Xu et al., 2000). Cold acclimation significantly modified the xanthophyll cycle activity in the Antarctic ecotype where a higher EPS was observed during exposure to HL (Fig. 4) as compared to non-acclimated plants and the Andes ecotype at both growth conditions. This unexpected result is quite intriguing, because the cold-acclimated Antarctic ecotype exhibited the highest NPQ and almost 90% of it was associated with NPQF (Fig. 3C, E). One possible explanation would be a greater contribution of an additional quenching process independent of zeaxanthin-mediated NPQ. The existence of such an additional quenching mechanism is consistent with earlier observations that significant levels of NPQ can occur independent of zeaxanthin (Hurry et al., 1997; Demmig-Adams et al., 1999) and cannot be accounted for by antenna quenching (Kramer, 2004). It has been proposed recently that dissipation of excess light energy via PSII reaction centre quenching might serve as such an additional quenching mechanism in cold-acclimated plants when the enzymatic conversion of violaxanthin to zeaxanthin within the xanthophyll cycle is thermodynamically restricted by low temperatures (Ivanov et al., 2003). Indeed, reaction centre quenching of excess light was suggested to play a substantial role in supplementing the antenna-based NPQ in cold-acclimated Scots pine (Ivanov et al., 2002) and cold-hardened Arabidopsis (Sane et al., 2003) and barley plants (Ivanov et al., 2006). Alternatively, the apparent uncoupling of NPQ from the EPS levels observed in the cold-acclimated Antarctic ecotype could also be due to the fact that only a few molecules of zeaxanthin are required for a fully active heat dissipation mechanism (Bukhov et al., 2001). Another interesting observation is that both ecotypes exposed to low temperature (4 °C), regardless of their acclimation state, exhibited higher values of NPQF even at very low PFD compared with plants exposed or acclimated to 15 °C (Fig. 3C, D). At very low PFD, electron transport rates would be too low to create and sustain a stable pH within the magnitude required for the conversion of violaxanthin to zeaxanthin. In addition, no zeaxanthin and/or antheraxantin are present in neither ecotype at low PFD (Fig. 4). Considering these two facts, it appears plausible to suggest that under very low light intensities non-radiative energy dissipation within PSII reaction centres may be induced prior to the detection of antenna quenching as proposed earlier (Finazzi et al., 2004).
Moreover, decreased photosynthetic capacity and increased dark respiration was observed in cold-acclimated ecotypes (Table 1). The enhanced rate of dark respiration has been reported earlier in cold-hardened plants such as cereals (Hurry et al., 1995) and conifers (Krivosheeva et al., 1996). It has been suggested that enhanced dark respiration, coupled to an enhanced activity of NADP-malate dehydrogenase, may contribute electrons for non-photochemical reduction of PQ (Savitch et al., 2000). This implies that low temperature may favour a light-independent process that can maintain a trans-thylakoid proton gradient at low light, possibly chlororespiration (Field et al., 1998). It has been suggested that the contribution of the chlororespiratory electron flux involving the NDH-complex and PTOX to total electron flow in the chloroplast and its photoprotective role as an alternative electron sink is rather limited under optimal growth conditions (Ort and Baker, 2002; Rosso et al., 2006). However, chlororespiration has been demonstrated to play an important photoprotective role in the high alpine plant species Ranunculus glacialis acclimated to low temperature (Streb et al., 2005). Furthermore, up-regulation of PTOX and the chloroplast NDH-complex have been reported in oat plants subjected to heat and high light stresses (Quiles, 2006). These data support the role of chlororespiration as an alternative electron sink in alleviating over-reduction of the PQ pool under unfavourable environmental conditions, which might be important for C. quitensis plants acclimated to the harsh environment of the Andes and Antarctica.
The increased contribution of the slow relaxing component (NPQs) of NPQ, which corresponds to photoinhibitory damage of PSII (Walters and Horton, 1991) in non-acclimated plants of both ecotypes exposed to 4 °C and high light compared to cold-acclimated plants (Fig. 3E, F), indicates that growth at low temperatures stabilizes the photosynthetic apparatus. The highest NPQs values were observed in non-acclimated Andes plants exposed to 4 °C and high light. This indicates that this ecotype is more susceptible to low temperature induced photoinhibition of PSII. In the field, under clear sky days the Andes ecotype is often under high irradiances (2500 µmol photons m–2 s–1), where temperature close to the soil can approach to 25 °C. Conversely, the Antarctic ecotype rarely experiences 1500 µmol photons m–2 s–1 and air temperature close to the soil is near 10 °C in snow free areas of the Maritime Antarctic. Therefore, the Andes ecotype is prepared to cope with high irradiances at relatively high temperatures, whereas the Antarctic ecotype can withstand low temperature and high irradiances better than the Andes one. Furthermore, freezing resistance of these ecotypes is consistent with the behaviour of their photosynthetic machineries. While the Antarctic ecotype is more freezing tolerant, reaching an LT50 of about –15 °C after 21 d of cold acclimation, the Andes ecotype only reaches an LT50 of –10 °C after the same acclimation time (Gianoli et al., 2004). It is suggested here that different selective pressure imposed by constant low temperature, shorter growing season, and a variable and sometimes limited light resource in the Antarctic relative to the Andes (Xiong et al., 1999; Xiong and Day, 2001) have genetically conditioned the Antarctic ecotype to an improved disposition for cold acclimation and, in this state, to maximize its photosynthetic performance.
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Acknowledgements |
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The authors gratefully thank Fondecyt 1010899 and DI 205.111.042–1S for funding. LA Bravo thanks MECESUP UCO-9906 for supporting a research stay in London, ON, Canada. N Huner is grateful for the support of NSERC.
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Abbreviations |
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A, antheraxanthin; EPS, epoxidation state of the xanthophyll cycle pigments; Fo, instantaneous (dark) chlorophyll fluorescence at open PSII centres in dark-adapted samples; Fm, maximal fluorescence at closed PSII centres; Fv, variable fluorescence; HL, high light intensity; LCP, light compensation point; LL, low light intensity; NPQ, non-photochemical quenching; NPQF, NPQs, fast and slow relaxing component of the NPQ; respectively; Pnmax, maximum rate of net photosynthesis;
PSII, quantum yield of PSII; O2, quantum yield of oxygen evolution; qE, energy-dependent quenching of chlorophyll fluorescence; qI, photoinhibitory quenching; qP, photochemical quenching; Rd, dark respiration; VAZ, pool of the xanthophyll cycle pigments; V, violaxanthin; Z, zeaxanthin. |
References |
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