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RESEARCH PAPER |
Temperature dependency of bark photosynthesis in beech (Fagus sylvatica L.) and birch (Betula pendula Roth.) trees
Institute of Applied Botany, University of Duisburg-Essen, D-45117 Essen, Germany
* To whom correspondence should be addressed. E-mail: hardy.pfanz{at}uni-essen.de
Received 13 June 2007; Revised 25 October 2007 Accepted 29 October 2007
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Abstract |
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Temperature dependencies of stem dark respiration (Rd) and light-driven bark photosynthesis (Amax) of two temperate tree species (Fagus sylvatica and Betula pendula) were investigated to estimate their probable influence on stem carbon balance. Stem Rd was found to increase exponentially with increasing temperatures, whereas Amax levelled off or decreased at the highest temperatures chosen (35–40 °C). Accordingly, a linear relationship between respiratory and assimilatory metabolism was only found at moderate temperatures (10–30 °C) and the relationship between stem Rd and Amax clearly departed from linearity at chilling (5 °C) and at high temperatures (35–40 °C). As a result, the proportional internal C-refixation rate also decreased non-linearly with increasing temperature. Temperature response of photosystem II (PSII) photochemistry was also assessed. Bark photochemical yield (
F/Fm') followed the same temperature pattern as bark CO2 assimilation. Maximum quantum yield of PSII (Fv/Fm) decreased drastically at freezing temperatures (–5 °C), while from 30 to 40 °C only a marginal decrease in Fv/Fm was found. In in situ measurements during winter months, bark photosynthesis was found to be strongly reduced. Low temperature stress induced an active down-regulation of PSII efficiency as well as damage to PSII due to photoinhibition. All in all, the benefit of bark photosynthesis was negatively affected by low (<5 °C) as well as high temperatures (>30 °C). As the carbon balance of tree stems is defined by the difference between photosynthethic carbon gain and respiratory carbon loss, this might have important implications for accurate modelling of stem carbon balance. Key words: Beech, birch, CO2 exchange, fluorescence, stem photosynthesis, stem respiration, temperature response
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Introduction |
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Temperature may affect productivity of forest trees by altering the balance between photosynthesis and respiration, because these processes respond differently to temperature changes (Maier et al., 1998). As temperature is the driving force behind most physiological processes that occur in a plant (Kramer and Kozlowski, 1979), changes in temperature may also have markedly different effects on the physiological processes that contribute to stem carbon balance, namely stem respiration and bark photosynthesis. Stem respiration makes an important contribution to total ecosystem respiration. In a beech forest in France, it was estimated that the annual CO2 efflux from aboveground woody tissues consumed 26% of the annual gross primary production (Damesin et al., 2002). In a tropical savanna ecosystem Cernusak et al. (2006) estimated the annual aboveground woody tissue CO2 efflux to be 275 g C m–2 ground year–1, or
13% of the annual gross primary production. Therefore, stem respiration is regarded as an important factor in the regulation of forest productivity and carbon storage (Ryan et al., 1997). A recent study by Cavalleri et al. (2006) further underlined the large contribution of small diameter woody tissue CO2 efflux to total plant respiration. For a tropical forest they found that small diameter stems (<10 cm), only 15% of total woody biomass, accounted for 70% of total woody tissue CO2 efflux from the forest. In young stems, a non-negligible part of the respired CO2 is directly re-assimilated in the assimilatory bark tissues during illumination, a process that has been termed ‘CO2 refixation’ or, alternatively, ‘bark photosynthesis’ (Foote and Schaedle, 1978; Sprugel and Benecke, 1991). Bark photosynthesis allows young stems to compensate for 60–90% of their respiratory carbon loss (Wittmann et al., 2001; Pfanz et al., 2002) and equals growth respiration on an annual basis (Damesin, 2003). For young beech trees, Gansert (1994) found annual bark photosynthetic rates of 24%. Kharouk et al. (1995) estimated the average bark input to whole tree C balance of Populus tremula as 10–15% during the mid-summer vegetative period. Thus, besides stem respiration, bark photosynthesis is an important and often overlooked component of stem and even tree carbon balance. All published carbon gain models use a temperature response function (Harley and Tenhunen, 1991; Leuning, 1997; Dreyer et al., 2001). Nevertheless, despite numerous studies that have shown the temperature response of stem respiration (Maier et al., 1998; Stockfors, 2000; Zha et al., 2004), only few studies (Cernusak and Marshall, 2000) have produced data sets for temperature dependency of bark photosynthesis, although both processes are clearly correlated with each other (Cernusak and Marshall, 2000; Aschan et al., 2001; Wittmann et al., 2005). Furthermore, the temperature response of bark photosynthesis among different tree species has not been compared. This would enhance our ability to predict individual tree function and competition between different tree species under changing environmental conditions.
Therefore, the objectives of this study were: (i) to examine the short-term temperature dependency of CO2 gas exchange [separated into dark respiratory (Rd) and photosynthetic fluxes (Amax)] as well as photosystem II (PSII) quantum yield (F/Fm') in stems of two temperate tree species (Fagus sylvatica and Betula pendula) under controlled environmental conditions; (ii) to examine whether F/Fm' in stems and leaves of both species responds similarly to changes in temperature; and (iii) to investigate the temperature dependency of Rd, Amax, and F/Fm' in stems under field conditions in order to estimate possible acclimation effects.
Studies indicate that different species originating from different habitats may have developed genotypic adjustments to their evolutionary temperature environment (Berry and Björkman, 1981; Read, 1990; Niinemets et al., 1999). To assess the extent to which temperature responses of stem Rd and Amax depend on species-specific attributes reflecting evolutionary adaptation to species temperature environment, experiments were conducted on two deciduous trees (F. sylvatica and B. pendula), which clearly differ in temperature and light requirements/preferences and successional status. Both F. sylvatica and B. pendula are widely distributed in Europe, but F. sylvatica is less frost-tolerant than B. pendula (Otto, 1994); the native range of B. pendula extends further north than that of F. sylvatica. With regard to the successional status, F. sylvatica is a shade-tolerant climax species growing in dense stands. Betula pendula is a pioneer tree abundant in northern Europe. Pioneer trees typically require gaps or clearings to establish a new generation of seedlings that are exposed to high irradiances, which support fast growth but also give rise to the danger of photoinhibition (Robakowski, 2005). In contrast, late-successional species germinate and undergo early development in the shade of forest canopies, often under extremely low irradiance (Küppers et al., 1996). Thus, the question was also asked of whether these species-specific attributes alter Amax, Rd, and F/Fm' versus T response curves.
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Materials and methods |
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Plant material
Laboratory and field experiments were performed during early summer (June) on 6-year-old beech (F. sylvatica L.) and birch trees (B. pendula Roth.), that were grown outside in plastic containers under sufficient nutrition (Einheitserde Typ T, Balster, Germany) and water supply, realized by periodic fertilization with Osmocote (Bayer, Germany) and daily irrigation. The plants were exposed to ambient temperatures. Mean monthly temperature recorded in June at the weather station Essen Schuir (Essen, Germany), located
1500 m from the growing side of the plants, was 19.9 °C.
Temperature treatment
For controlled environment observations, potted trees were transferred to the laboratory and were placed intact into a large climate chamber (4.46 mx4.83 mx2.95 m; PVP GmbH, Willich, Germany), which allows full control of temperature, relative humidity, and light intensity. Plants were left to acclimate for 1 d under the following conditions: air temperature, 20 °C; relative humidity, 50%; and PAR, 600/0 µmol m–2 s–1 (day/night). Day and night lengths were 15 h and 9 h, respectively. Thereafter, air temperature was set to the desired value (–5, 5, 10, 15, 20, 25, 30, 35, 40, and 43 °C) while relative humidity and PAR were kept constant. All measurements were made as follows: chamber temperatures were set to a constant value and the trees were left to temperature-adapt for at least 60 min. Then the gas exchange and fluorescence parameters were measured on the middle of the length of two intact stems (1–2 years old; stem diameters ranged from 1.1 cm to 2.0 cm) of each tree (n=5). In all cases, measurements were performed inside the climate chamber on stems/leaves from the outer sun-crown at a height of 1.5 m and the whole plant was exposed to the measurement temperature during this period. This procedure avoided bias due to leaf/stem portion versus whole-plant temperature control during measurement (Atkin et al., 2000; Griffin et al., 2002).
As acclimation processes may affect the temperature responses of photosynthesis (and respiration), for each temperature step a new set of trees (n=5) was collected from the field. Although acclimation can be rapid, for example acclimation occurred within 2 d of a temperature change in some species (Billings et al., 1971; Atkin et al., 2000), time to full acclimation has been reported to be of the order of 10 d or longer (Bolstad et al., 2003). These periods are substantially longer than those used in the present experiments.
CO2 gas exchange measurements
Laboratory measurements:
For gas exchange measurements 7 cm long portions of 1- to 2-year-old stems were enclosed in a transparent, stem cuvette allowing simultaneous measurements of CO2 exchange by infrared gas analysis. The gas exchange system operates with full control of CO2 concentrations, incident light intensity, air temperature, and relative humidity inside the cuvette. Stem temperature was measured with a thermocouple attached to the outer stem surface. Light was supplied by an Osram Power Star HQI-R lamp only to the upper part of the stem; comparable with natural conditions. The stem segment was exposed to a flow of 400 ml min–1 of air. CO2 gas exchange between the stem and the air was measured with a differential infrared gas analyser (Li 6400; Li-Cor, Lincoln, NE, USA) under constant microclimatic conditions (relative humidity 50%; constant temperature) and ambient CO2 (360 ppm). Both the climate chamber and the temperature-controlled cuvette of the gas exchange system were set to equal values during measurements.
Stem net CO2 flux may be considered as the sum of three terms: stem or woody tissue respiration (+flux), bark photosynthesis (–flux), and CO2 dissolved in the xylem sap (+flux, if diffusing out, –flux, if transported away) (Cernusak and Marshall, 2000; Pfanz et al., 2002; McGuire and Teskey, 2004; Bowman et al., 2005; Cavalleri et al., 2006). Yet, when stem CO2 efflux before and after cutting of young beech and birch stems was measured (for a total of 4 h) under laboratory conditions, no significant differences were found (data not shown). If CO2 dissolved in the xylem sap mainly contributed to stem CO2 efflux, a change in efflux rates should have occurred. Furthermore, longitudinal fluxes of respiratory CO2 in the transpiration stream were minimized by keeping relative humidity constant, while changing temperature. Thus, the assumption is made that observed CO2 efflux rates in the dark are equivalent to stem respiratory CO2 production rates. In young stems, live sapwood respiration rates are small in comparison with respiration of cambial, cortical, and phloem cells (Linder and Troeng, 1980; Matyssek and Schulze, 1988). The high surface to volume ratio further minimizes the contribution of sapwood xylem parenchyma cell respiration, thus the rate of dark CO2 efflux is expected to reflect primarily cambial/cortical (phloem included) respiration (Levy and Jarvis, 1998; Cavalleri et al., 2006; Wittmann et al., 2006). Secondly, the assumption is made that the contribution of CO2 dissolved in the xylem sap is minimized under the measurement conditions applied (constant relative humidity), so that maximum bark photosynthesis (Amax) is equivalent to:
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Relative CO2 refixation as a percentage of the dark respiration rate was estimated as follows:
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Field measurements:
Daily courses of CO2 gas exchange were monitored on 6-year-old potted birch trees (see Plant material), which were exposed for the whole year to ambient temperatures. Seasonal patterns of stem Rd and Amax were determined from diurnal (daytime) assays made during the summer vegetative period (August) but also during winter (January). CO2 gas exchange between the stem and the air was measured with a differential infrared gas analyser (Li 6400; Li-Cor). Stem temperature was measured with a thermocouple attached to the outer stem surface. PAR was monitored in the chamber near the stem plane using a miniature GaAsP sensor. For measurements of bark photosynthesis, a transparent stem cuvette was used. For respiratory measurements, cuvettes were surrounded with aluminium foil. Bark photosynthesis at a given time was calculated according to Equation 1 as the absolute value of the difference between CO2 efflux in the dark (Rd) and under illumination with ambient light (Ramb).
Fluorescence measurements
Temperature response measurements:
Fluorescence measurements were made under ambient CO2 and constant microclimatic conditions (relative humidity: 50%; 600 µmol photons m–2 s–1) by means of a pulse amplitude-modulated fluorometer (PAM-2000; Walz, Effeltrich, Germany), equipped with a 2030-B leaf clip holder, featuring an integrated micro-quantum sensor and a thermocouple. The 0.8 s saturation pulse intensity was set to 10 000 µmol m–2 s–1, an intensity that was found to be always saturating. To determine accurately the fluorescence signal of a cylindrical stem, a piece of non-fluorescing black paper with a rectangular 3 mmx10 mm window was attached on the clip. During the measurements this window was orientated along the stem axis; thus only photon exchange between the plane, central part of the stem and the instrument is considered. The outer bark temperature of the investigated stems was measured by the thermocouple of the clip holder directly attached to the stem surface; all temperatures reported are thus stem surface temperatures (±0.5 °C).
All measurements were made as follows: trees were left to dark-adapt for at least 60 min. After determination of maximum quantum yield in dark-adapted material (Fv/Fm), the effective quantum yield (F/Fm') of PSII was measured on two stems (1–2 years old) and adjacent, fully developed leaves of each tree (n=5) under an actinic light intensity of 600 µmol photons m–2 s–1. As determined in preliminary experiments, 600 µmol photons m–2 s–1 are saturating for leaf and bark photosynthesis. These results corresponded to observations in a number of tree species (Fagus crenata, Quercus acutissima, Han and Suzaki, 1981; Populus tremuloides, Foote and Schaedle, 1976; Acer rubrum, Coe and McLaughlin, 1980; F. sylvatica, Populus tremula, Wittmann et al., 2001; B. pendula, Wittmann et al., 2006); in all these species bark photosynthesis saturated between 200 and 500 µmol PAR m–2 s–1. Chlorophyll fluorescence parameters, maximum quantum yield (Fv/Fm), and effective quantum yield (F/Fm') of PSII were calculated according to Schreiber et al. (1994) and Genty et al. (1989).
Light response measurements:
Additionally, instant light response curves of the effective quantum yield (F/Fm') of PSII under freezing (–5 °C), chilling (5 °C), and warm temperatures (20 °C) were obtained using the PAR curve program of the PAM. After determination of maximum quantum yield in dark-adapted material (60 min), a 5 min pre-irradiation period at moderate irradiance (120 µmol photons m–2 s–1) provided a stationary fluorescence level of the samples. Then the ‘actinic light’ intensity was decreased to 60 µmol photons m–2 s–1 for 5 min, before a saturation pulse was applied to obtain the effective quantum yield (F/Fm') of PSII. Within the following 20 min, irradiance was increased stepwise with irradiation periods of 2 min and subsequent saturation pulses until 1250 µmol photons m–2 s–1 was reached.
Data analysis
Non-linear least-square regression was used to fit temperature dependencies of bark photosynthesis (Amax) by (see also Harley et al., 1992; Niinemets et al., 1999):
 | (3) |
Ha (kJ mol–1) is an activation energy, Hd (kJ mol–1) is a deactivation energy, S (kJ K–1mol–1) is an entropy term, T (K) is leaf temperature, and R (0.008314 kJ mol–1 K–1) the gas constant. The whole temperature data set for Amax was fitted to Equation 3. To simplify the fitting procedure and make comparison of temperature responses easier, the entropy term S was held constant at 0.385 kJ K–1 mol–1. A similar approach is described in Harley et al. (1992). Equation 3 provided a function closely fitting the data, and r2 of the non-linear regressions was always >0.99 (cf. Fig. 1 for the fits).
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The temperature dependence of dark respiration rates (Rd) is described by the Arrhenius equation:
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Ha (kJ mol–1) is the activation energy, and R (0.008314 kJ mol–1 K–1) the gas constant. The whole temperature data set for Rd was fitted to Equation 4. The Arrhenius equation gave excellent fits to the data with a minimum r2 of 0.99 (cf. Fig. 1 for the fitted curves). Yet, the parameters c and Ha of Equation 4 are not fitted independently, thus making it difficult to compare the changes in the shape of the temperature response curves. To eliminate the autocorrelation, the stem respiration data were standardized with respect to the respiration rate measured at 20 °C as in Harley and Baldocchi (1995). Given that the standardized rate, 
, is equal to:
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c is eliminated, and for each standardized rate i, an estimate of Ha independent of c was found as:
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Further, the whole standardized stem respiration data was fitted to Equation 5 and the coefficient Ha (±SE) for the regression model was computed.
As in carbon balance models, respiration rates are often expressed in terms of Q10, temperature response of dark respiration was additionally described by respiration–temperature response functions of the form (see also Bolstad et al., 2003):
 | (7) |
and Q10 are estimated coefficients. The Q10 may be interpreted as the ratio of respiration measured over a 10 °C span (see also Tjoelker et al., 1999; Turnbull et al., 2001; Bolstad et al., 2003). The whole temperature data set for Rd was fitted to Equation 7 and the coefficient Q10 (±SE) for the regression model was computed. Equation 7 provided a function fitting the whole stem respiration data just as well as Equation 4, and r2 of the non-linear regressions was always >0.99 (P <0.0001). For statistical data analysis, the SigmaPlot 2001 software (SPSS Inc., Chicago, IL, USA) was used. The significance of differences between sets of data was checked by Student's t-tests. To visualize and plot the curve that best describes the shape and behaviour of the data (‘curve fitting’) the ‘regression wizard’ of the program was used. The coefficient of determination, a measure of how well the regression model describes the data, is given in the figures.
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Temperature response of Rd and Amax
The temperature response of stem dark respiration of F. sylvatica and B. pendula revealed a typical exponential relationship (Fig. 1). Regression-based estimates of
Ha (activation energy) were 45±0.82 kJ mol–1 for beech and 43±0.36 kJ mol–1 for birch trees. Regression-based estimates of Q10 gave a value of 1.75±0.01 for beech and 1.87±0.08 for birch stems. In contrast, an exponential increase in light-saturated bark photosynthesis (Amax) with temperature was only found from 5 °C to 25 °C, while at higher temperatures saturation or even inhibition (40 °C) of photosynthesis was obtained (Fig. 1). Thus, the percentage of dark-respired CO2 that was refixed within the bark chlorenchyma (=relative refixation) declined with increasing temperature (Fig. 1c, d).
At a common reference temperature of 20 °C, stem Rd and Amax were closely related to each other (Fig. 2). The slope of the relationship between the two parameters was 0.68 for birch and 0.83 for beech stems. This suggests that the photosynthetic bark chlorenchyma reduced dark respiration rates under saturating illumination up to 68% or 83%, respectively. The relationship between stem Rd and Amax was clearly temperature dependent (Fig. 3).
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At moderate values between 10 °C and 25 °C a linear relationship [birch, r2=0.98; beech, r2=0.91; f(x)=0.5x] between both physiological processes was observed. If additionally freezing (–5 °C), chilling (5 °C), and high temperatures (35–40 °C) were considered (Fig. 3), this relationship clearly departs from a simple linear function [f(x)=ax]. Consequently, the data set was expressed most appropriately by a non-linear equation closely fitting the data (r2 of the non-linear regressions was always >0.99; cf. Fig. 3 for the fits). Furthermore, species differences in temperature response of bark photosynthesis were recorded. Estimates of the temperature coefficients
Hd (deactivation energy) and Ha (activation energy) differed significantly (Table 1). A complete list of parameters used to describe the temperature dependence of Amax is shown in Table 1.
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Daily courses of Rd and Amax
To compare short- and long-term temperature responses, the diurnal and seasonal patterns of Rd and Amax were additionally monitored in the field. Typical daily courses of bark photosynthesis during the summer vegetative period (Fig. 4a, c) and the winter period (Fig. 4b, d) showed that Amax clearly followed the daily temperature and PAR course during the summer months (Fig. 4c, e), reaching photosynthetic rates of up to 4 µmol CO2 m–2 s–1, while the values were almost zero during the winter months (Fig. 4d, f). Even when illumination increased stem surface temperatures from below zero to values of
10 °C for up to 6 h (12:00–18:00; Fig. 4b, d), bark photosynthesis did not return to summer values.
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Temperature response of PSII photochemistry
Differences between leaves and stems in the temperature response of PSII quantum yield were also assessed. Light-adapted photochemical yield of stems (
F/Fm'; Fig. 5) followed a similar temperature pattern to Amax (Fig. 1). Yet, a clear difference with respect to leaves was found as the temperature optimum of F/Fm' (Topt) was 34 °C in stems and 28 °C in leaves of birch (for beech 36 °C and 30 °C, respectively). Besides the difference in Topt, it was evident that at high temperatures (>35 °C) the reduction in effective quantum yield of PSII was clearly higher in leaves than in stems (Fig. 5). Accordingly, stems showed a broader thermal optimum range and the decline in the curve was comparatively flat (Fig. 5).
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Compared with CO2 assimilation (Fig. 1) and light-adapted photochemical yield (Fig. 5), the maximum quantum yield of PSII (Fv/Fm) of stems and leaves was relatively insensitive to temperature changes (Table 2). Between 5 °C and 30 °C no significant differences in Fv/Fm were found (Table 2). In contrast, freezing temperatures (–5 °C) resulted in a steep decrease in maximum quantum yield of PSII of leaves and stems. High temperatures (40 °C) led only to a marginal decrease in Fv/Fm, while a significant decrease occurred in leaves (Table 2). To follow up the influence of low temperatures on bark photosynthesis, the light response of
F/Fm' at warm (20 °C), chilling (5 °C), and freezing (–5 °C) temperatures was also determined (Fig. 6). In both species a steep decline in F/Fm' at 5 °C and –5 °C was observed.
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Temperature response of Rd and Amax
Because photosynthesis (Amax) and respiration (Rd) are temperature sensitive, a change in temperature results in an immediate alteration in the rate of Rd and Amax, with the extent of that alteration being determined by the temperature coefficient of each process (Atkin et al., 2007). Temperature response of stem Rd revealed a typical exponential relationship, with regression-based estimates of Q10 that confirm observations in other woody species in which Q10 values of stem dark respiration were between 1.6 and 2.3 (Sprugel and Benecke, 1991: 2–2.3; Damesin et al., 2002: 1.6–2.1; Edwards et al., 2002: 1.9–2.1). Regression-based estimates of
Ha (activation energy) were within the range of published values for Rd (Reddig and Gries, 1999). Temperature response of bark photosynthesis was similar to that generally found in leaves (Kramer and Kozlowski, 1979; Larcher, 2001). At a common reference temperature of 20 °C and saturating illumination, photosynthetic bark chlorenchyma reduced dark respiration rates by 68% or 83%, respectively (Fig. 2). These results are in good agreement with previous studies in which light-saturated bark photosynthesis was found to compensate for 60–90% of the respiratory carbon loss of young stems (Sprugel and Benecke, 1991; Cernusak and Marshall, 2000; Aschan et al., 2001; Wittmann et al., 2001, 2005; Pfanz et al., 2002). Thus, bark photosynthesis clearly supports stem carbon balance at moderate temperatures. However, while stem dark respiration was found to increase exponentially with increasing temperatures, bark photosynthesis levelled off or decreased at high temperatures (35–40 °C). As a result, the proportion of carbon that is refixed also declined dramatically as the temperature increases (Fig. 1). Accordingly, a linear relationship between respiratory and assimilatory metabolism was only found at moderate temperatures (10–30 °C). This confirms findings by Cernusak and Marshall (2000), Aschan et al. (2001), and Wittmann et al. (2007), who reported a linear relationship between stem Rd and Amax at 20 °C for Pinus monticola, Populus tremula, and B. pendula stems. Rd and photosynthesis are interdependent, with Rd relying on photosynthate as substrate, whereas photosynthesis depends on Rd for the carbon skeletons and for the ATP required for sucrose synthesis plus repair of photosynthetic proteins (Krömer, 1995; Atkin et al., 2000, 2007; Padmasree et al., 2002). Consequently, Rd and Amax cannot diverge indefinitely, and homeostasis of Rd/Amax is often assumed (Gifford, 2003). Yet, at high (
35 °C) and low (<5 °C) temperatures this relationship departed from linearity in stems (Fig. 3). This indicates that temperature sensitivity of Amax differs from that of Rd under these conditions, with the result that Rd/Amax is altered. One reason for this alteration may be that photosynthesis is particularly sensitive to the rate of utilization or export of its products. If this is low (e.g. with reduced sink strength or at low temperatures which limit respiration) the rate of photosynthesis may become restricted by ‘feedback inhibition’ (see Stitt et al., 1987). Woodwell (1990) and Ryan et al. (1996) found that the Rd/Amax ratio increased with elevated temperature in leaves. According to Dewar et al. (1999), this reflects the transient dynamics of the plant pools (e.g. the non-structural carbohydrate and protein pools), in which the turnover rates of labile C and starch are more temperature sensitive than photosynthesis. Consequently, an imbalance between the underlying C fluxes with increasing temperature is maintained. Similar reasons may also explain why increases in temperature stimulated stem Rd more than Amax. There may be several physiological reasons for the species-specific differences in temperature response of Amax, but those reasons are difficult to assess, because of the variety of contributing processes. In leaves, the cause may originate from intrinsic differences in Rubisco activase activity (Crafts-Brandner and Salvucci, 2000) or part of the specific temperature responses may be related to the thermal properties of the processes contributing to CO2 diffusion and transport into the chloroplast (Dreyer et al., 2001). Nevertheless, addressing those reasons in stems will require further investigation before it can be wholly understood.
Temperature response of PSII photochemistry
The relationship between quantum yield of PSII and quantum yield for CO2 assimilation has been well documented (Cheng et al., 2001). Linear relationships have been reported in many species (Krall and Edwards, 1990, 1991; Cornic and Ghashghaie, 1991; Genty et al., 1992; Maxwell et al., 1998) and it appears that this relationship is conserved, as it holds across species (Seaton and Walker, 1990) and is not affected by water stress or elevated CO2 (Cornic and Ghashghaie, 1991; Habash et al., 1995). Based on this relationship, T versus F/Fm' curves of leaves and stems were examined. Bark photochemical yield (F/Fm') followed the same temperature pattern as bark CO2 assimilation, which reflects a functional linkage between photochemistry and photosynthetic carbon reduction of stems. However, compared with F/Fm', the maximum quantum yield of PSII (Fv/Fm) of stems and leaves was relatively insensitive to temperature changes. Between 5 °C and 30 °C no significant differences in Fv/Fm were found (Table 2), indicating a well-functioning PSII over a broad range of temperatures. Manetas and Pfanz (2005) found comparable Fv/Fm values for both species at room temperature. However, at freezing temperatures, maximum quantum yield of PSII (Fv/Fm) of leaves and stems decreased drastically (–5 °C, Table 2). It is suggested that the observed drop in Fv/Fm reflects an active down-regulation of Fv/Fm to avoid low temperature stress. However, damage to PSII also cannot be excluded. According to Solhaug and Haugen (1998), maximum quantum yield of PSII in bark of P. tremula was considerably reduced during winter. Since the reduction in Fv/Fm partly depended on sun exposure and on phellem thickness, they concluded that photoinhibition must be partly responsible for the low Fv/Fm. The steep decline in the light response curves of F/Fm' at 5 °C and –5 °C reflects the increasing stress resulting from low temperatures as the light level is increased (Fig. 6). Under low temperature, increased levels of photoinhibition (even under moderate light levels) in leaves have been attributed to several factors, including the reduced utilization of excitation energy in carbon metabolism. This leads to an increased proportion of reduced QA (primary quinone acceptor; the first electron acceptor of PSII) in the steady state, which results in an increase in excess excitation energy. Rates of repair via D1 protein turnover can be severely reduced as well (Krause, 1994). Furthermore, Fv/Fm of stems and leaves declined at high temperatures (40 °C; Table 2). PSII is well known to be sensitive to high temperatures, and it is often cited as the most heat-sensitive component of photosynthesis in temperate species (Berry and Björkman, 1980; Havaux, 1992). Therefore, it is likely that damage to PSII contributed to the inhibiton of leaf and bark photosynthesis at these temperatures (Fig. 5).
Differences in optimum temperature for photosynthesis
Comparison of T versus F/Fm' curves of leaves and stems revealed that optimal bark photosynthesis occurred at higher temperatures than leaf photosynthesis (Fig. 5). C4 plants have a higher temperature optimum for photosynthesis than C3 plants due to the operation of a CO2-concentrating system that inhibits Rubisco oxygenase activity (Berry and Björkman, 1980; Edwards and Walker, 1983; Badger and Pfanz, 1995). Thus, it is assumed that the comparably higher temperature optimum of stems may hint at a C3–C4 intermediate pathway of carbon fixation in the stem chlorenchyma, as recently reported by Hibberd and Quick (2002) for herbaceous plants. Phosphoenolpyruvate (PEP) carboxylase in tree stems was found at 10–23 times higher levels than in leaves of C3 plants (Höll, 1973, 1974; Berveiller and Damesin, 2005). Compared with Rubisco, PEP carboxylase is heat stable; Rubisco activase is actually the heat-labile component of C3 photosynthetic reactions (Rubisco between 20 °C and 25 °C; PEP carboxylase is optimally active at 37 °C). The suggestion of C3–C4 intermediacy should also show up in the carbon isotope discrimination of photosynthetic stems. Indeed, Cernusak et al. (2001) did observe a departure from the discrimination expected for C3 photosynthesis at high refixation rates in bark chlorenchyma of P. monticola. Another important aspect is the high CO2 concentration in the refixing bark tissues. In young stems of B. pendula, suppression of photorespiration was attributed to high bark CO2 concentrations (618–1548 µmol CO2 mol–1; Wittmann et al., 2006). These values are up to seven times higher than those generally reported for C3 (240 µmol CO2 mol–1) or C4 (200 µmol CO2 mol–1) leaves (Von Willert et al., 1995). In leaves of C3 plants elevated CO2 concentrations led to a suppression of photorespiration as well as a shift of the photosynthetic optimum to higher temperatures (Acock and Allen, 1985; Long, 1991; Bowes, 1993). Furthermore, the greater heat capacity of stems may contribute to the observed differences in temperature optimum, but addressing those reasons in stems will require further investigation before it can be wholly understood. Several studies also demonstrated lower optimum temperatures in species evolutionarily adapted to cooler environments (Berry and Björkman, 1980; Hällgren and Öquist, 1990). Betula pendula, the range of which extends further north than that of F. sylvatica, is a pioneer tree that typically requires gaps or clearings to establish a new generation of seedlings that are exposed to high irradiances. Yet, optimum temperatures for photosynthesis of birch leaves and stems were always somehow lower than those of beech trees. Across a wide range of species, foliar frost resistance and optimum temperatures for photosynthesis are inversely correlated (Read and Hope, 1989), and it seems that species are unable to optimize the performance in either hot or cold environments. Thus, irrespective of differences between leaf and stem temperature optimum for photosynthesis, the species-specific differences in optimum temperature of bark photosynthesis may also manifest evolutionary adaptation to temperature environment. Niinemets et al. (1999) reported similar results for leaves of Tilia cordata and P. tremula.
Daily courses of bark photosynthesis in the field
In situ measurements on field-grown plants were generally consistent with those made on plants in the chamber studies. Bark photosynthesis clearly followed the daily temperature and PAR course during the summer months (mean monthly temperature recorded in August was 21.5 °C), but values were strongly inhibited during the winter months (mean monthly temperature recorded in January was 2.6 °C). Several authors suggested that branches of deciduous trees might be able to photosynthesize even during the leafless period and that bark photosynthesis is an important factor in the ability of deciduous trees to survive in areas with long cold winters (Pearson and Lawrence, 1958; Strain and Johnson, 1963; Perry, 1971; Foote and Schaedle, 1976; Parker, 1978; Pilarski, 2002). The present results call this assumption into question. Foote and Schaedle (1976) found similar seasonal patterns of bark photosynthesis on 5- to 7-year-old aspen stems. Furthermore, Larcher and Nagele (1992) conclusively demonstrated that the photosynthetic capacity of 3- to 7-year-old stems of F. sylvatica is lowered in winter, and that short-term rewarming treatments cannot restore it to summer values. In contrast, the maximum quantum yield of PSII in bark chlorenchyma of Scots pine twigs, measured as Fv/Fm, was shown to be well preserved during winter, while Fv/Fm of Scots pine needles was severely reduced (Ivanov et al., 2005). In leaves and needles of evergreen woody plants, winter depression of photosynthesis has been considered to be associated with after-effects of freezing (Larcher, 1981; Öquist, 1983), with changes in chloroplast structure and molecular composition during winter (Senser et al., 1975), and with processes of cold adaptation and photoinhibition (Strand and Öquist, 1988). Similar processes might in pars or in toto also explain the observed winter depression of bark photosynthesis in stems of F. sylvatica and B. pendula. Furthermore, it is well known that from autum to winter the levels of soluble carbohydrate in stem tissues of trees increase (Sakai and Larcher, 1987). The outcome of this is that besides osmotic effects on photosynthetic activity, the high sugar accumulation in the chloroplasts leads to a potent feedback inhibition of photosynthesis (Foyer, 1988). Electron microscopic studies by Sagisaka et al. (1990) further revealed that major cytological changes in the cortical cells of deciduous trees began to occur in early September in conjunction with the metabolic transition from the growing to the wintering stage.
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
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This study showed that the benefit of bark photosynthesis is negatively affected by low (<5 °C) as well as high temperatures (>30 °C). The carbon balance of trees is defined by the difference between photosynthetic carbon assimilation and the expenditure of fixed C by respiration; it is therefore obvious that any shift in this balance reduces the efficiency of stems/trees to convert photosynthetically reduced C into new biomass. Temperatures above 30 °C lead to a sustained imbalance between stem dark respiration and bark photosynthesis, because bark photosynthesis declines at high temperatures, while respiration increases exponentially. Consequently, the proportion of carbon that is refixed also declines dramatically as temperature increases and a higher amount of CO2 is lost to the atmosphere. Even though it is difficult to extrapolate from young saplings to mature trees, and from short-term temperature change to long-term acclimation, the possible implications for forest carbon balance with increasing global temperatures are thought-provoking. During winter, both gas exchange and fluorescence measurements clearly indicated a reduction of stem carbon assimilation. Thus, carbon acquisition capacity of stems may be limited in winter by low temperatures (<5 °C) due to a drop in Fv/Fm and in summer by high temperatures (>30 °C). First evidence also suggests species-specific differences in temperature response of bark photosynthesis due to evolutionary adaptation to the temperature environment. Nevertheless, in the face of carbon balance, bark photosynthesis could be important during the winter even if its values are low, because respiration values are also low during this period. Furthermore, the present data suggest an important role for bark photosynthesis by woody trees in maintaining a favourable carbon balance during the late autumn and early spring, when leaf photosynthesis of deciduous trees is decreasing or non-existent, and stems are exposed to rather low temperatures (
5–10°C).
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Acknowledgements |
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We would like to thank Gudrun Friesewinkel, Sabine Kühr, and Christa Kosch for technical assistance. Warm thanks also to Dr Sabine Begall, Dipl. Umweltwiss. Sabine Flohr, and Janne Mombour. Dr Francesco Loreto (CNR-Roma) is gratefully acknowledged for helpful discussions.
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