JXB Advance Access originally published online on May 8, 2007
Journal of Experimental Botany 2007 58(8):2133-2143; doi:10.1093/jxb/erm067
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© 2007 The Author(s).
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details)
RESEARCH PAPER |
Response of photosynthetic apparatus to moderate high temperature in contrasting wheat cultivars at different oxygen concentrations
1Institute of Plant Physiology and Genetics, National Academy of Sciences of Ukraine, 31/17 Vasylkivska St., Kyiv 03022, Ukraine
2Plant Research Unit, Division of Environmental and Applied Biology, University of Dundee at SCRI, Invergowrie, Dundee DD2 5DA, Scotland, UK
* To whom correspondence should be addressed. E-mail: h.g.jones{at}dundee.ac.uk
Received 27 October 2006; Revised 13 February 2007 Accepted 7 March 2007
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Abstract |
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The photosynthetic responses to moderately high temperatures (38 °C, imposed at 21% or 2% O2 in air and 1500 µmol m–2 s–1) were compared in wheat (Triticum aestivum L.) cultivars grown in northern regions of Ukraine and expected to be relatively sensitive to high temperatures (‘North’ cultivars) and in cultivars grown in southern regions and expected to be relatively heat-tolerant (‘South’ cultivars). Heating intact leaves in 21% O2 for 1 h decreased CO2 assimilation by c. 63% in ‘North’ cultivars and only c. 32% in ‘South’ cultivars, with a decrease in PSII activity being observed in only one of the ‘North’ cultivars. Carboxylation efficiency was decreased by about 2.7-fold in ‘North’ cultivars with no significant effect in ‘South’ cultivars. The maximum rates of carboxylation by Rubisco in vivo, Vcmax, estimated from Farquhar's model, increased more than 2-fold in ‘South’ cultivars and remained unchanged in ‘North’ cultivars while the maximum rate of RuBP regeneration, Jmax, decreased by 53% and 21% in ‘North’ and ‘South’ cultivars, respectively. Where the heat treatment was imposed in 2% O2 this increased (as compared with treatment at 21% O2) the inhibitory effect on CO2 assimilation in tolerant cultivars, but decreased it in sensitive ones. The results suggested that differences in tolerance of moderately high temperatures in wheat relate to the stability of the Rubisco function and to RuBP regeneration activity rather than to the effects on PSII activity or stomatal control.
Key words: Heat-tolerance, high temperature, photosynthetic limitation, photosystem II, Triticum aestivum L
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Introduction |
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High temperature is a common stress for plants, restricting their growth and productivity in many regions (Boyer, 1982). Models of global climate change predict a further 1.5–5.5 °C warming for this century as a result of the increased atmospheric concentrations of CO2 and other trace gases (Houghton et al., 2001). Extreme high-temperature events are also anticipated to increase greatly in frequency (Wagner, 1996), thus plants are increasingly likely to be limited by high-temperature stress so an understanding of the mechanisms involved will be critical for the breeding of more tolerant genotypes.
In C3 plants, increasing leaf temperature above the growth temperature generally results in reduced photosynthesis (Berry and Björkman, 1980). This is partly a consequence of enhanced oxygenase activity of Rubisco due to the lower CO2/O2 specificity of Rubisco (Jordan and Ogren, 1984) and the increase in the O2/CO2 solubility ratio (Ku and Edwards, 1977). In the field, high temperatures are often accompanied by water deficits and stomatal closure with a consequent reduction in CO2 availability and more intense photorespiratory loss of CO2 and C cycling through the glycolate pathway (Cornic, 1994).
Moderately high temperatures (35–40 °C) can directly damage the photosynthetic apparatus through effects on light energy capture, photosystem II- and photosystem I-mediated electron transfer, and Calvin cycle activity (Berry and Bjorkman, 1980; Baker, 1991; Sharkey, 2005), with the oxygen-evolving complex on the donor side of PSII being especially susceptible (Yamane et al., 1998). In many cases, however, such PSII inhibition was not observed with treatments (usually <40 °C) that have inhibited CO2 fixation (Law and Crafts-Brandner, 1999; Sharkey, 2005).
High temperature may also lead to physical separation of LHCII from the PSII core complex; this is usually detected as an increase in the basal fluorescence, Fo, (Schreiber and Berry, 1977; Pastenes and Horton, 1999) and altered energy distribution in favour of PSI (Pastenes and Horton, 1996). Heat-induced stimulation of cyclic electron transport around PSI may account for increases in 
pH-related non-photochemical quenching (Pastenes and Horton, 1996; Bukhov et al., 1998) and the maintenance of high ATP contents under high temperature despite increased thylakoid membrane leakiness (Bukhov et al., 1999; Schrader et al., 2004).
Several reports (Kobza and Edwards, 1987; Law and Crafts-Brandner, 1999) have suggested that Rubisco deactivation may be more important than altered thylakoid function in decreasing CO2 assimilation under high temperatures and may underlie species differences. Rubisco activase has been shown to be extremely heat labile (Eckardt and Portis, 1997; Salvucci et al., 2001) and the activation state of Rubisco has been proposed as the primary constraint on photosynthesis at moderately high temperatures (Crafts-Brandner and Salvucci, 2000; Salvucci and Crafts-Brandner, 2004a). According to this hypothesis, the decrease in PSII activity under high temperature may be a consequence of photoinhibitory down-regulation of the electron transport chain and not to direct heat-induced damage. However, some recent publications have provided evidence arguing against a leading role of Rubisco activase in the limitation to photosynthesis at supraoptimal temperatures, regarding Rubisco deactivation as a regulated response to limitation in one of the processes contributing to the rate of RuBP regeneration (Wise et al., 2004; Cen and Sage, 2005).
Under photoinhibitory conditions, damage to photosynthesis could be strongly affected by oxygen, although reports concerning the role of O2 in the effects of excessive light on the photosynthetic apparatus are contradictory (Krause and Cornic, 1987; van Wijk and Krause, 1991; Wingler et al., 2000; Ort and Baker, 2002). These contradictions probably occur because O2 diminishes the extent of photoinhibition by the dissipation of energy through the photorespiratory carbon oxidation cycle and the Mehler reaction (Osmond and Grace, 1995; Ort and Baker, 2002). However, direct electron flow to O2 in the Mehler reaction, or that linked to PSII activity, produce the active oxygen species (AOS) that can inflict damage to the photosynthetic apparatus (Foyer and Noctor, 2000).
The objective of this study was to define the mechanisms involved in the differential temperature tolerance of winter wheat cultivars in response to short-term moderate temperature increases that might occur frequently in the field. Chlorophyll fluorescence and gas-exchange measurements were used to investigate and compare the photosynthetic responses to moderately high temperatures in cultivars expected to differ in their heat tolerance. In order to dissect the protective mechanisms in differentially adapted cultivars, the responses under 21% and 2% O2 were also compared.
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Plant materials
The seeds of four winter wheat cultivars (Triticum aestivum L.), Poliska 87, Myronivska 33, Obriy, and Odeska 66, were collected from the Institute of Plant Physiology and Genetics of the National Academy of Science of Ukraine (Kyiv). Poliska 87 and Myronivska 33 were recommended for growth in northern regions of Ukraine (‘North’ cultivars) and were expected to be relatively sensitive to heat while Obriy and Odeska 66 were recommended for growth in southern regions (‘South’ cultivars) and were therefore expected to be relatively heat-tolerant. The germinated seeds were planted in 12.5 cm pots filled with peat- and loam-based compost (F2, Levington, Horticulture Ltd, Ipswich, UK) and grown in a temperature-controlled greenhouse at day/night temperature of 24/19 °C. Natural light was supplemented with high-pressure sodium lamps that gave a photosynthetic photon flux density (PPFD) of 200 (morning and evening) to 1000 (sunny midday) µmol m–2 s–1 at the plant height. The plants were watered regularly and soil moisture was controlled by returning to a standard weight. The pairs of cultivars were expected to differ in tolerance but it had been revealed previously that they were more similar in morphological and developmental parameters, Poliska 87/Obriy and Myronivska 33/Odeska 66 (e.g. leaves of the second of these pairs expanded 2–3 d earlier and were 0.6 mm wider), were planted staggered once a week. A recently fully expanded 4th or 5th leaf was used in all experiments, and the number of replicate plants is indicated for each figure.
Gas exchange measurement and treatments
Rates of CO2 assimilation and stomatal conductance were measured using a portable photosynthesis system CIRAS-1 (PP Systems, Hitchin, UK). The mid-part of a leaf was sealed into the leaf chamber and allowed to equilibrate in air containing 21% O2, 350 µmol mol–1 CO2 and 70% relative humidity (RH) at 25 °C and a PPFD of 1500 µmol m–2 s–1 (control conditions). When steady-state CO2 assimilation rate and stomatal conductance were attained, the light-response (A/Q) at 350 µmol mol–1 CO2 or the CO2-response (A/Ci) at PPFD of 1500 µmol m–2 s–1 of CO2 assimilation was measured. As leaf gas exchange was again equilibrated to PPFD of 1500 µmol m–2 s–1 and 350 µmol mol–1 CO2 with 21% or 2% O2, leaf temperature was increased to 38 °C within about 3 min and maintained at this level (±1 °C) for 1 h using the internal heater of the photosynthesis system. CO2 assimilation rate and stomatal conductance were measured during heat treatment every 2 min. Leaf temperature was estimated using the leaf energy balance method. Air containing 2% O2 was produced by mixing air with pure N2 using a bank of mass flow controllers FC 260 (Tylan Gen. Ltd., UK). O2 concentration in the gas mixture was tested using galvanic oxygen sensors (KE25, Figaro Engineering Inc., Osaka, Japan). Light- or CO2-response of treated leaves was measured at 38 °C and 21% O2 immediately after 1 h of heating or as steady-state gas exchange was reached after switching O2 concentration from 2% to 21%. At each irradiance and CO2 concentration, steady-state rates of CO2 exchange were recorded and Ci was calculated by CIRAS-1 software. When test leaves were kept at the initial control conditions for 3 h after reaching steady state there were no significant changes in any of the CO2-exchange parameters for all cultivars (data not shown).
Chlorophyll fluorescence measurement
Chlorophyll fluorescence was measured using a modulated fluorimeter (Hansatech FMS1, King's Lynn, UK) simultaneously with measurements of the light-response of CO2 assimilation in the Parkinson gas-exchange chamber. The parameters of PSII photochemistry in light-adapted leaves were routinely measured using a standard protocol. A saturating pulse of white actinic light having a PPFD of approximately10 000 µmol m–2 s–1 was given to obtain 
; the light-adapted initial fluorescence, 
was acquired by switching the actinic light off and applying a 5 s pulse of weak far-red light (735 nm). The actual quantum efficiency of PSII in the light (
PSII), photochemical quenching (qP) and excitation trapping efficiency of PSII (maximal quantum efficiency in the light) (
) were calculated by Hansatech FMS1 software as defined by Genty et al. (1989).
Estimation of the CO2 exchange parameters from the A/Ci responses
Key characteristics of the CO2 exchange were derived from the A/Ci responses using ‘Photosyn Assistant Ver. 1.1.2’ (Parsons and Ogston, 1999; Dundee Scientific, Dundee, UK). This application fits parameters by minimizing the sum of squares. To obtain the A/Ci response, the CO2 concentration (Ca) was initially set to 350 µmol mol–1 and then sequentially to 260, 180, and 65 µmol mol–1. After that Ca was returned to 350 µmol mol–1 and the CO2 assimilation rate was measured at increased Ca, 560, 800, and 1000 µmol mol–1. The rate of respiration in the light (RL: comprising mainly photorespiration), and carboxylation efficiency (CE) were estimated by linear regression from the initial part of the A/Ci curve (Laisk, 1977; Parsons et al., 1997). The maximum rates of carboxylation by Rubisco (Vcmax) and electron transport used in regeneration of RuBP (Jmax) and the rate of triose phosphate utilization (TPU) were calculated from the Farquhar model (Farquhar et al., 1980) according to Harley et al. (1992) and Wullschleger (1993). These estimates assumed negligible mesophyll diffusive resistance to sites of CO2 fixation so may have somewhat underestimated Vcmax (von Caemmerer, 2000). Attempts to estimate mesophyll conductance (gm) were not made because of uncertainties in the alternative sink activities, although it is worth noting that values of gm for wheat are likely to have a small effect on the decline in CO2 concentrations between intercellular space and carboxylation sites (Ethier and Livingston, 2004).
Statistical analysis
Simple one-way or two-way analysis of variance and other statistical tests were conducted using Minitab for Windows 12.1 (Minitab Inc., State College, PA, USA). Comparisons were tested using Fisher's least significant difference (LSD); probabilities of less than 0.05 were considered significant.
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Time-course of CO2 assimilation rate, stomatal conductance, and internal CO2 concentration during high temperature treatment
Increasing the leaf temperature to 38 °C at 21% O2 in air and PPFD of 1500 µmol m–2 s–1 resulted in a greater decrease in CO2 assimilation rate over a period of 10–15 min in ‘North’ cultivars than in ‘South’ cultivars (Fig. 1a). After the initial decline, rates stabilized with the inhibition being substantially greater in the ‘North’, or sensitive, cultivars than in the ‘South’, or tolerant, cultivars. At the end of high temperature treatment, the CO2 assimilation activity was inhibited by 60–66% in sensitive cultivars and 27–38% in tolerant ones. These differences and changes in CO2 assimilation rate during treatment overall were not related to changes in stomatal conductance (gs) or intercellular CO2 concentration (Ci) (Fig. 1b, c). Although gs at the end of treatment appeared to be somewhat inhibited in most genotypes, no decrease in Ci was observed. In fact analysis of variance for the interaction between origin and temperature showed that Ci values after the heat treatment increased significantly (P <0.05) in ‘North’, but not in ‘South’, cultivars. None of these responses could be attributable to drifts in control rates as CO2-exchange parameters in all cultivars did not alter significantly over 3 h at control conditions.
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Effects of high-temperature stress on the light responses of CO2 assimilation and PSII photochemistry
Light-response curves of CO2 assimilation, chlorophyll fluorescence characteristics, and of electron transport through PSII (Genty et al., 1989), were measured on the same leaf at 25 °C before treatment (control) and at 38 °C after heating for 1 h. Left and right panels in Fig. 2 compare two pairs of cultivars contrasting in their thermotolerance, but which are similar in morphological and developmental features.
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The photosynthetic characteristics measured before treatment were essentially similar in all cultivars. The heat-induced reduction in CO2 assimilation rate was observed at all PPFD with the response in ‘South’ cultivars being substantially smaller than in ‘North’ cultivars (Fig. 2a). The most pronounced effects of high temperature on fluorescence parameters were detected under low irradiances (Fig. 2b, c, d). The decrease in
PSII at low and moderate light was, on average, slightly greater for the ‘North’ cultivars (36%) than for ‘South’ cultivars (22%). In contrast to the results for CO2 assimilation, no differences in PSII between control and heat-treated leaves were found at high light except for Poliska 87. PSII is a product of two other fluorescence parameters, qP and (Genty et al., 1989), which responded differently in ‘North’ and ‘South’ cultivars. Photochemical quenching declined by a rather similar extent in stressed leaves of both groups of cultivars, while the decrease in was greater in ‘North’ cultivars with Poliska 87 exhibiting the largest decrease in (about 20% under both the lowest and the highest light levels).
Oxygen dependence of heat-stress effect on photosynthesis
In order to assess the effects of oxygen-dependent processes on the response of photosynthesis to moderate heat-stress, the effects of treatments at high temperature (38 °C) under either 2% O2 in air or in 21% O2 were compared. Measurements were made under both treatment O2 concentration (Fig. 3) and at 21% O2 (Fig. 4) so that heat-induced damage could be assessed in the absence of confounding by photorespiration. Before treatment, all cultivars responded similarly to low O2 concentration with steady-state CO2 assimilation rate increasing by 42–44% and PSII largely unaffected (Table 1). Low O2 concentration, however, affected the photosynthesis response to high temperature differently for ‘North’ and ‘South’ cultivars. The primary decline in CO2 assimilation and its inhibition at the end of heating under low O2 were consistently smaller for ‘North’ cultivars but larger for ‘South’ as compared with the corresponding effect of high temperature under 21% O2 (Fig. 3). The differential effects of O2 on the decrease in CO2 assimilation rate induced by treatment at high temperature were statistically significant for all cultivars for comparisons at the same O2 concentration (21%) (Fig. 4a).
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These results could not be explained by changes in gs and Ci as those were rather higher in leaves treated at 2% O2 for all cultivars (data not shown). The oxygen effect on heat-stress response of
PSII (Fig. 4b) did not correlate well with changes in CO2 assimilation.
Effect of high temperature on CO2 response of photosynthesis: analysis of biochemical limitation on CO2 assimilation
CO2 response curves were measured under 21% O2 for control leaves at 25 °C before treatment and at 38 °C; the effect of exposure to 2% O2 while being heated was studied for one ‘North’ cultivar, Myronivska 33, and one ‘South’ cultivar, Odeska 66 as these showed the larger differential response to high temperature stress (Fig. 5). The variables Vcmax, Jmax, RL, and CE were estimated by analysis of the A/Ci curves (Fig. 6) using the ‘Photosyn Assistant’ software (Parsons and Ogston, 1999).
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High temperature treatment of leaves at 21% O2 decreased the maximum observed values of assimilation rate (Amax) on average by 52% and 24% in ‘North’ and ‘South’ cultivars, respectively (Fig. 5). Furthermore, the initial slope of the A/Ci curve (CE) declined 2.6–2.9-fold in stressed leaves of ‘North’ cultivars while it was not substantially affected for ‘South’ cultivars (Fig. 6a). The larger heat-induced inhibition of photosynthesis under 2% O2 in Odeska 66 was accompanied by greater decreases in CO2 assimilation at both high and low CO2 (Fig. 5). Heat-induced changes in RL were not statistically significant for every cultivar (Fig. 6b), but analysis of variance on the relative changes for the interaction between origin and temperature showed a significant difference (P <0.05) between ‘North’ and ‘South’ cultivars. This result fits predictions from the Farquhar model (Sharkey, 1988) (data not shown).
Similar to the reduction of Amax in heated leaves, Jmax decreased by 53% and 21% in ‘North’ and ‘South’ cultivars, respectively, although the changes for the latter were not statistically significant (Fig. 6d). By contrast, the calculated Vcmax increased at high temperature by a factor of more than 2 in ‘South’ cultivars and remained unchanged in ‘North’ cultivars (Fig. 6c). Low oxygen concentration during heating exacerbated significantly the decrease in Jmax and prevented the increase in Vcmax for Odeska 66. In Myronivska 33, heating at low O2 rather mitigated the decrease in Jmax and resulted in higher Vcmax.
The changes in both Jmax and Vcmax, caused by heating independently of O2 concentration, correlated well with the observed reductions in CO2 assimilation rate (Fig. 7b). Despite the differences in temperature response of Vcmax and Jmax between cultivars, the strong correlation between these parameters observed at 25 °C (R2=0.851) remained at 38 °C (R2=0.910, including data from low-O2-treated leaves) (Fig. 7a). Values of ratio of Jmax/Vcmax at 25 °C ranged from 2.23 to 2.53, but declined at 38 °C by factors of more than 2 and varied from about 0.76 to 1.14.
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The Farquhar model functions fitted to A/Ci curves are shown on Fig. 8. A possible limitation of CO2 assimilation by triose phosphate use efficiency (Harley and Sharkey, 1991) was suggested only in some cases at the highest Ci (data not presented). The high temperature treatment did not change the balance between Rubisco- and RuBP-dependent limitations of photosynthesis in ‘North’ cultivars. However, in leaves of ‘South’ cultivars treated at 21% O2, the modelled RuBP-dependent function described the observed data in the whole range of Ci much better than in the control indicating an increased role of RuBP regeneration in photosynthesis limitation. When the ‘South’ cultivar Odeska 66 was treated under 2% O2, however, Rubisco limitation became dominant at the operating Ci.
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In our experiments, CO2 assimilation rate decreased and then stabilized after 20–30 min of heat treatment, remaining virtually stable at least for 3 h (data not shown). This allowed us to investigate Ci and light dependencies of photosynthesis under nearly steady-state conditions. Such behaviour of the photosynthetic apparatus under heat stress is not common (Pastenes and Horton, 1999; O Stasik and HG Jones, unpublished data).
As expected, the cultivars grown in southern regions of Ukraine appeared to be more thermo-tolerant than ones grown in the North. Although Monneveux et al. (2003) attributed high temperature inhibition of assimilation in the field to decreased stomatal conductance, in our experiment stomata did not significantly affect CO2 assimilation. Insignificant effects of stomatal conductance have also been reported in other studies (Law and Crafts-Brandner, 1999; Bunce, 2000) where water vapour pressure deficits during heat treatment were kept low.
The differences in heat-induced inhibition of photosynthesis between cultivars also could not be explained by different responses of RL (Fig. 6b). In fact, the respiratory CO2 losses in the light under high temperature appeared to be rather higher (hence contributing more to the decrease in CO2 assimilation) in more tolerant ‘South’ cultivars than in ‘North’ ones. Although a decrease in gm could, in principle, inhibit photosynthesis, the similar relative heat-induced reductions in CO2 assimilation (Fig. 5) at ambient CO2 concentration and at high CO2 (where influences of photorespiration and gm are less important) suggest that this was not a significant factor in our experiments.
Data in Fig. 2 show that the reductions in CO2 assimilation due to moderate high temperature treatment under high light were not brought about by the decrease in PSII activity in leaves of Myronivska 33, Obriy, and Odeska 66, although such an effect could not be entirely ruled out in Poliska 87. Indeed the PSII activity under high light remained largely unchanged by heat treatment; although the decrease in PSII under low irradiance suggests some heat-induced damage to or down-regulation of linear electron transport in all cultivars related to reductions in both qP and in , with the latter being particularly inhibited in the ‘North’ cultivars (Fig. 2). The results imply, however, that the observed differences in PSII activity response were more likely to be a result of reduced carbon assimilation, than their cause.
Since the changes in respiratory processes could not fully account for the decline in net CO2 assimilation rate in treated leaves, differences in heat-responses of PSII and of CO2 assimilation suggested a significant increase in activity of alternative sinks for electron transport particularly in Myronivska 33. The direct reduction of oxygen from the acceptor side of PSI (water–water cycle) seems to be most probable and an important alternative sink (Osmond and Grace, 1995; Asada, 1999; Ort and Baker, 2002).
Analysis of the heat-induced changes in the A/Ci responses indicated that the greater inhibition of photosynthesis in ‘North’ cultivars under high light was attributable to their greater decrease in actual carboxylation rate in vivo (Fig. 6). The major difference between the ‘North’ and the ‘South’ cultivars was that Vcmax increased substantially with temperature in the more tolerant ‘South’ cultivars, but not in the ‘North’ cultivars (Fig. 6c).
In higher plants, Rubisco has been found to be very stable at high temperatures (Eckardt and Portis, 1997) with the carboxylation activity of the fully activated enzyme, Vcmax, in vitro increasing up to 50 °C (Salvucci and Crafts-Brandner, 2004a), although in vivo optima are commonly between 35 °C and 41 °C (Bernacchi et al., 2001; Medlyn et al., 2002, and references therein). In our experiments, the lack of a high-temperature-induced increase in Vcmax in ‘North’ cultivars most probably reflected a decline in Rubisco activation, while the corresponding increase in ‘South’ cultivars indicated the maintenance of a relatively high Rubisco activation state, possibly related to differences in activity of Rubisco activase (Crafts-Brandner and Salvucci, 2000; Portis, 2003, and references therein). It has recently been shown that Rubisco activase in wheat comprises three isoforms whose expression varies under heat stress that may be related to photosynthesis acclimation (Law and Crafts-Brandner, 2001; Portis, 2003). Salvucci and Crafts-Brandner (2004b) reported that activase in plant species endemic to cold regions is more sensitive to high temperature than activase in species from warm regions.
The high temperature treatment reinforced RuBP-limitation to photosynthesis in the ‘South’ cultivars (Fig. 8) and significantly decreased the maximum rate of electron transport used in RuBP regeneration (Jmax) in ‘North’ cultivars (Fig. 6d), despite the lack of any major inhibition in PSII activity. Although this discrepancy could be explained by the enhanced activity of alternative electron sink(s) and/or increased PSI activity at the expense of stromal reductants (Schrader et al., 2004) the causal sequence is not yet clear.
The use of differing O2 concentrations provides further information on the likely mechanisms involved in high temperature inhibition of photosynthesis. Lowering the O2 concentration from 21% to 2% strongly inhibits photorespiration and this peculiarity is often employed to investigate the role of photorespiration in stress responses (Powles, 1984; Wingler et al., 2000), however, this can also affect direct electron flow to oxygen from PSI or PSII (Asada, 1999; Foyer and Noctor, 2000).
In our experiments, the response of CO2 assimilation rate to lowering of the O2 concentration to 2% at the optimal temperature, 25 °C, was similar in all cultivars studied (Table 1), while PSII was largely unaffected. This suggested a similar relationship between photosynthesis and photorespiration (or other O2-dependent processes) in all cultivars. The reduced electron demand from photorespiration at low O2 was probably compensated by the increase in CO2 assimilation maintaining previous PSII levels. Interestingly, the effect of oxygen on the photosynthesis response to high temperature was very different in ‘South’ and ‘North’ cultivars (Figs 3, 4). Heat-induced damage to CO2 assimilation was enhanced by non-photorespiratory conditions in ‘South’ cultivars, but decreased in ‘North’ ones. Low oxygen appeared to be protective for the sensitive cultivars and damaging for the more heat-tolerant cultivars. These effects could not be fully explained in terms of down-regulation of PSII caused by the lack of electron sink since changes in PSII activity did not entirely coincide with those in CO2 assimilation (Fig. 4).
The detrimental effect of normal O2 and the high probability of increased Mehler reaction in ‘North’ cultivars suggested that an inability to cope with oxidative stress could be an important component of the damage observed in both ‘North’ cultivars under high temperature conditions at normal oxygen (van Wijk and Krause, 1991). PSII and PSI are usually considered as primary targets of oxidative damage under excessive light (Foyer and Noctor, 2000). The increase in Vcmax in Myronivska 33 while the leaf was heated at 2% O2, suggested that another potential aspect of the greater photosynthetic inhibition under photorespiratory conditions in these cultivars might be Rubisco inactivation by glyoxylate (Campbell and Ogren, 1990; Hausler et al., 1996; Wingler et al., 1997).
The contrasting and damaging response to lowered O2 concentration in the more tolerant ‘South’ cultivar Odeska 66 appeared to be related to specific changes in both Vcmax and Jmax (Fig. 6). However, alteration in the Rubisco-dependent function in leaves heated at low oxygen was larger than in the RuBP-dependent function and photosynthesis at the operating Ci was solely Rubisco-limited (Fig. 8). Therefore, the bigger inhibition of CO2 assimilation caused by high temperature at 2% O2 in relatively heat-tolerant cultivars was most probably attributed to a larger decrease in the Rubisco activation state. Such a decline in the Rubisco activation produced by low O2 concentration under high light conditions has been reported for various C3 species (Schnyder et al., 1984; Sharkey et al., 1986; Kobza and Edwards, 1987; Crafts-Brandner and Salvucci, 2000).
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Conclusions |
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The results strongly indicate that differences in tolerance of CO2 assimilation in wheat cultivars to moderately high temperatures can be attributed mainly to the stability of the Rubisco catalytic function and to RuBP regeneration rather than to the effects on stomata or PSII activity. It is likely that the differences in the responses of Rubisco activity observed between cultivars were related to Rubisco activation state and the large heat-induced decrease in carboxylation activity was the most notable distinction of relatively sensitive cultivars. By contrast, Rubisco in the leaves of relatively tolerant cultivars heated under photorespiratory conditions appeared to remain well activated, and photosynthesis in that case appeared to be limited by RuBP regeneration. Further information on the mechanisms underlying differential sensitivity to heat is provided by the differential response to oxygen, with oxygen-dependent processes contributing to heat-induced damage to photosynthesis in sensitive cultivars but preventing it in tolerant cultivars. The detrimental effects of O2 may relate to oxidative damage to linear electron transport and/or to down-regulation of Calvin cycle enzymes, while the protective role of oxygen in tolerant cultivars could, in part, be ascribed to sustaining electron transport through PSII, and partly to maintaining Rubisco activity. Such a protective effect of O2 obviously also took place in sensitive cultivars, but negative effects of oxidative stress appeared to outweigh this benefit.
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References |
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