Figures
Abstract
Background
The electron transport chain, Rubisco and stomatal conductance are important in photosynthesis. Little is known about their combined responses to heat treatment at different temperatures and following recovery in grapevines (Vitis spp.) which are often grown in climates with high temperatures.
Methodology/Findings
The electron transport function of photosystem II, the activation state of Rubisco and the influence of stomatal behavior were investigated in grapevine leaves during heat treatments and following recovery. High temperature treatments included 35, 40 and 45°C, with 25°C as the control and recovery temperature. Heat treatment at 35°C did not significantly (P>0.05) inhibit net photosynthetic rate (Pn). However, with treatments at 40 and 45°C, Pn was decreased, accompanied by an increase in substomatal CO2 concentration (Ci), decreases in stomatal conductance (gs) and the activation state of Rubisco, and inhibition of the donor side and the reaction center of PSII. The acceptor side of PSII was inhibited at 45°C but not at 40°C. When grape leaves recovered following heat treatment, Pn, gs and the activation state of Rubisco also increased, and the donor side and the reaction center of PSII recovered. The increase in Pn during the recovery period following the second 45°C stress was slower than that following the 40°C stress, and these increases corresponded to the donor side of PSII and the activation state of Rubisco.
Conclusions
Heat treatment at 35°C did not significantly (P>0.05) influence photosynthesis. The decrease of Pn in grape leaves exposed to more severe heat stress (40 or 45°C) was mainly attributed to three factors: the activation state of Rubisco, the donor side and the reaction center of PSII. However, the increase of Pn in grape leaves following heat stress was also associated with a stomatal response. The acceptor side of PSII in grape leaves was responsive but less sensitive to heat stress.
Citation: Luo H-B, Ma L, Xi H-F, Duan W, Li S-H, Loescher W, et al. (2011) Photosynthetic Responses to Heat Treatments at Different Temperatures and following Recovery in Grapevine (Vitis amurensis L.) Leaves. PLoS ONE 6(8): e23033. https://doi.org/10.1371/journal.pone.0023033
Editor: Hany A. El-Shemy, Cairo University, Egypt
Received: March 2, 2011; Accepted: July 4, 2011; Published: August 26, 2011
Copyright: © 2011 Luo et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by the National Natural Science Foundation of China (No. 30771758) and the Knowledge Innovation Program of the Chinese Academy of Sciences (No. KSCX2-EW-J-1). No additional external funding was received for this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
High temperature negatively affects plant growth and survival and hence crop yield. Photosynthesis is known to be one of the most heat-sensitive processes, and it can be inhibited by high temperature before other symptoms of stress are detected [1], [2]. Inhibition of photosynthesis by heat stress has long been attributed to an impairment of electron transport activity, especially the inhibition of photosystem II (PSII) activity [3], [4]. Heat stress not only damages the oxygen-evolving complex of PSII [5], [6], but also impairs electron transfer within the PSII reaction centres [7], [8], [9] and downstream of PSII. Some authors [10], [11] have suggested that the initial site of the inhibition is associated with a Calvin cycle reaction, especially inactivation of Rubisco [12], [13], [14], [15]. However, for different species, the specific effects of heat stress maybe different.
Worldwide, grape has become one of the most productive and important specialty crops. In many production regions, the maximum midday air temperature can reach more than 40°C, which is especially critical at berry ripening. Some researchers suggested the optimum temperature for photosynthesis is between 25°C and 35°C for some grape cultivars [16], [17]. Temperatures above 35°C generally reduce photosynthesis in grape leaves. Climate change may produce more frequent high temperature conditions close to the current northern limit of grape cultivation [18]. Extreme temperatures may therefore endanger berry quality and economic returns [19]. Although there are many reports dealing with the influence of heat stress to photosynthesis in grape leaves [20], [21], [22], [23], a very limited number of papers consider the combined response of the components of PSII, Rubisco and stomatal conductance to heat stress [24], [25]. Recently, Kadir [24] and Kadir et al. [25] determined the response of Vitis species to high temperature under controlled environmental conditions through chlorophyll fluorescence measurements such as Fv/Fm, Fv and Fo. It is not known if inhibition of grape photosynthesis by heat stress is caused by an impairment of electron transport or Rubisco activity. Moreover, the effect of heat on the donor side, acceptor side, reaction center, and on energy partitioning of PSII in grapevine is not clear. In contrast, studies about effects of low temperatures on photosynthetic performance of grape leaves from electron transport and energy partitioning are relatively abundant [23], [26], [27]. In addition, recovery from heat stress is an important factor of heat tolerance in plants. Plants, including grapevine, may be most likely to experience heat stress around midday, and relatively normal temperatures otherwise. Thus, plants may be exposed to a heat stress – recovery – heat stress – recovery cycle. However, less information is available on the plant behavior under the heat-stress recovery compared with under heat stress. In the past, attention usually was focused on the plant's direct response to stress. Consequently, more definitive studies on the plant traits for heat tolerance must be conducted to understand the mechanism of the recovery from heat. These results may help develop modern and acceptable technologies to increase and stabilize berry yield and qualities.
Inhibition of PSII leads to a decrease in variable chlorophyll fluorescence. Thus, in vivo chlorophyll fluorescence may be used to detect changes in the photosynthetic apparatus [28], [29]. Strasser et al. have developed a method for the analysis of the kinetics of fast fluorescence increases since the non-destructive measurements can be done with a high resolution of 10 µs [30]. All oxygenic photosynthetic materials investigated so far show a polyphasic fluorescence rise consisting of a sequence of phases, denoted as O, J, I, and P (OJIP test). With this test, it is possible to calculate several phenomenological and biophysical expressions of PSII. The kinetics of OJIP are considered to be determined by changes in the redox state of QA, but at the same time, the OJIP transient reflects the reduction of the photosynthetic electron transport chain [31]. The OJIP test has been a powerful tool for the in vivo investigation of the behavior of PSII function including energy absorption, trapping, and electron transport [30], [32], [33].
In the present study, gas exchange parameters, chlorophyll fluorescence parameters and the activity state of Rubisco in grape leaves during high temperature (35, 40 or 45°C) treatments and following recovery (stress-recovery-stress-recovery) were investigated. Our objective was to determine the importance of electron transport, Rubisco and stomatal factors to maintain photosynthesis and the sensitivity of components of the photosynthetic apparatus in grape leaves under high temperature stress and during recovery.
Results
Net photosynthesis rate (Pn), substomatal CO2 concentration (Ci) and stomatal conductance (gs)
At normal growth conditions of 25°C, Pn, Ci and gs of grape leaves did not change during the experiment (over the 3 days of the growth period monitored). Heat stresses at 35°C at two times did not significantly (P>0.05) influence Pn, Ci and gs of grape leaves compared with the control (at 25°C). A decline of Pn and gs after 40 and 45°C treatments was observed, accompanied with a Ci increase. Heat stress at 45°C had stronger negative impact on Pn and gs than 40°C and recovered more slowly. On the fourth day of recovery (Day 6) after the second heat stress, Pn, Ci and gs of plants that had received a 40°C treatment recovered to the control levels, but those exposed to 45°C were still exhibiting an effect of heat stress (Fig. 1).
25°C: normal growth and recovery temperature; 35, 40 and 45°C: high temperature treatments. Each value represents the mean ± S.E. of four replicates. At the same time point, the numerical values with different letters are significantly different (P<0.05) according to Duncan's multiple comparison.
Donor side, reaction centre and acceptor side of PSII and PSI
It has been shown that heat stress can induce a rapid rise in the OJIP polyphasic fluorescence transients. This phase, occurring at around 300 µs and labeled K, is caused by an inhibition of the oxygen evolving complex (OEC). The amplitude of step K can therefore be used as a specific indicator of damage to PSII donor side [26]. Fig. 2 shows the changes in the amplitude in the K step expressed as the ratio WK. Compared with the control (25°C), heat stress at 35°C did not alter WK of grape leaves. After the first heat treatment of 40°C or 45°C for 5 h, WK of grape leaves increased steeply, and WK was higher at 45°C than at 40°C. During the following recovery (on Day 2), WK values of these treatments were similar to the control level. However, they rapidly increased again after the second heat stress. On the first day of recovery (Day 3), they declined to some extent, but WK of the 45°C treatment was bigger than that of the 40°C treatment. On the fourth day of recovery (Day 6), WK of the 40°C and 45°C treatments recovered to the control level.
Wk = (Fk−Fo)/(Fj−Fo); RCQA = φPo×(Vj/Mo)×(ABS/CS). The definition of these parameters is shown in detail in Table 2. 25°C: normal growth and recovery temperature; 35, 40 and 45°C: high temperature treatments. Each value represents the mean ± S.E. of four replicates. At the same time point, the numerical values with different letters are significantly different (P<0.05) according to Duncan's multiple comparison.
RCQA shows the density of the of QA-reducing PSII reaction centers. Fig. 2 demonstrates that heat stress at 35°C did not influence the RCQA during the experiment. The first (on Day 1) and second (on Day 2) stresses of 40°C or 45°C significantly (P<0.05) reduced the RCQA. The RCQA values of the two treatments returned to control values during the first recovery. After the second stress, RCQA values of the two treatments basically reached the level of controls during recovery of the first day.
Fig. 3 demonstrates the changes in maximum quantum yield for primary photochemistry (φPo), the quantum yield for electron transport (φEo), the probability that a trapped exciton moves an electron into the electron transport chain beyond QA− (ψEo), the quantum yield for dissipated energy (φDIo) in grape leaves during high temperature stress and recovery. Heat stress at 35°C did not significantly (P>0.05) alter φPo, φEo, ψEo and φDIo in grape leaves. φPo significantly declined while φDIo was enhanced at the end of first and second heat stress of 40°C and 45°C. However, at the same time, φEo and ψEo showed no change at 40°C, but decreased at 45°C compared with the control. φPo decreased and φDIo rose at 40°C less than at 45°C at the first stress. However, φPo and φDIo at 40°C was similar to those at 45°C at the second stress. After both stress periods, these parameters recovered to control levels by the first day (Day 2 and Day 3) of recovery.
25°C: normal growth and recovery temperature; 35, 40 and 45°C: high temperature treatments. Each value represents the mean ± S.E. of four replicates. At the same time point, the numerical values with different letters are significantly different (P<0.05) according to Duncan's multiple comparison.
δRo expresses the redox state of PSI, i.e., the efficiency with which an electron from PQ through PS I to reduce PS I end electron acceptors. Heat stress at 35°C and 40°C did not change the δRo in grape leaves, but the δRo at 45°C rose significantly (P<0.05). However, these parameters recovered to control levels in the first day of recovery (Fig. 4).
25°C: normal growth and recovery temperature; 35, 40 and 45°C: high temperature treatments. Each value represents the mean ± S.E. of four replicates. At the same time point, the numerical values with different letters are significantly different (P<0.05) according to Duncan's multiple comparison.
PSII efficiency and excitation energy dissipation
PSII efficiency and excitation energy dissipation in grape leaves was examined by modulated fluorescence techniques. Fig. 5 shows that heat stress at 35°C had no effect on the actual PSII efficiency (ΦPSII), photochemical quenching coefficient (qp), as well as non-photochemical quenching (NPQ). Heat stress at 40 and 45°C led to a sharp decrease of ΦPSII and qp, and a striking increase of NPQ. After the first 40°C stress, NPQ, ΦPSII and qp recovered to the control levels the following day (Day 2). With a 1 d recovery after the second 40°C stress, ΦPSII slowly rose while NPQ declined to some extent, but qp reached the control level. On the fourth day of recovery (Day 6), NPQ, ΦPSII and qp had recovered to control levels. With the 45°C stress, NPQ, ΦPSII and qp changed more dramatically, and recovered more slowly after the second stress although they had recovered to the control levels after the first stress.
25°C: normal growth and recovery temperature; 35, 40 and 45°C: high temperature treatments. Each value represents the mean ± S.E. of four replicates. At the same time point, the numerical values with different letters are significantly different (P<0.05) according to Duncan's multiple comparison.
The activation state of Rubisco
As shown in Fig. 6, heat stress at 35°C had no influence on the activation state of Rubisco in grape leaves compared with 25°C. When the grape leaves were exposed to 40 or 45°C the first time, the Rubisco activation state declined significantly (P<0.05), and 45°C led to the bigger decline. However, after 1 d of recovery, the Rubisco activation state recovered to the control level. When these grape leaves were exposed to 40 or 45°C a second time, the Rubisco activation state declined more than after the first stress, with 45°C resulting in a sharper decrease. On the first day during the second recovery (Day 3), the Rubisco activation state of both treatments had not recovered to the control level although the 40°C treatment recovered more rapidly than the 45°C treatment. On Day 6, the Rubisco activation state of both the 40°C and 45°C treatments reached the control level.
25°C: normal growth and recovery temperature; 35, 40 and 45°C: high temperature treatments. Each value represents the mean ± S.E. of four replicates. At the same time point, the numerical values with different letters are significantly different (P<0.05) according to Duncan's multiple comparison.
Discussion
The step limiting photosynthesis at high temperatures has been debated recently. One proposed limitation is heat-induced deactivation of Rubisco [12], [13], [34], [35]. The other proposed limitation is impairment of the entire electron transport chain [36], [37], [38], [39]. In fact, different high temperatures may have different effects. This study clearly shows that Pn was not limited at 35°C in grape leaves, but it was limited at 40°C and 45°C. This result is similar to views that the optimum temperature for photosynthesis is between 25 and 35°C for some grape leaves [16], [17]. When the grape leaves were stressed at 40°C or 45°C, Pn and the activation state of Rubisco were markedly reduced while Ci increased, indicating that the inhibition of photosynthesis is non-stomatal and associated with Rubisco (Fig. 1 and 6). The reduction of Pn increase proportionally with the increasing of treatment temperature. However, when the grape leaves had recovered from heat stress, the increase of Pn was accompanied by increases of gs and the activation state of Rubisco, indicating that Pn recovery was also associated with stomatal factors and the activation state of Rubisco (Fig. 1 and 6). Recent studies with cotton, wheat, tobacco, and maize have confirmed earlier observations that Rubisco is deactivated markedly in response to moderate heat stress [12], [13], [14], [40], [41]. However, heat stress at 35°C did not significantly (P>0.05) influence the activation state of Rubisco in grape leaves, which is similar to the effect on Pn (Fig. 6). It has been shown that the inhibition of Rubisco activation by moderately elevated temperatures up to 40°C was fully reversible after the heated leaves were incubated at 22.5°C for 15 min [34], [42]. In the present study, Rubisco following treatment at 40°C recovered more rapidly than when treated at 45°C.
The decrease of Pn under heat stress and increase of Pn during recovery was also associated with electron transport capacity. Figs. 2, 3, 4, and 5 show that the PSII and PSI were damaged. In addition, the relationship between Pn and electron transport chain was dependent on temperature. Sage and Kubien [43] thought that it has been difficult to pinpoint specific limiting steps that control the temperature response of electron transport chain. However, the OJIP test may be used to demonstrate the limiting steps of electron transport of photosynthesis [44]. At present, the mechanism causing the decline in the electron transport rate above the thermal optimum remains uncertain. Inactivation of the oxygen-evolving complex (OEC) is implicated as a cause of heat–induced reduction in electron transport capacity, particularly at high temperatures (above 38°C in potato and above 40°C in spinach) [3], [6]. However, at moderately warm temperatures, this lesion is probably not significant, as leaves can readily alter PSII properties to reduce heat sensitivity of the OEC [3]. The present results showed that 35°C did not result in damage to OEC. Heat stress can influence the PSII reaction center, and the density of RCQA may reflect the density of QA-reducing PSII reaction centers [45]. In the present study, during the heat stress at 40 or 45°C and the following recoveries, changing trends of WK and RCQA values almost corresponded to that of Pn (Fig. 2). This indicated that heat stress and recovery influenced Pn partially via the donor side (the oxygen-evolving complex) and reaction center of PSII. Moreover, the higher stress temperature led to a slower recovery of Pn.
In these experiments, φPo declined and φDIo increased at 40°C or 45°C. However, after 1 d of recovery, they returned to control levels. Interestingly, ψEo and φEo significantly (P<0.05) decreased in grape leaves at 45°C but 40°C had almost no influence on φEo and ψEo (Fig. 3). φDIo demonstrates the quantum yield for dissipated energy. In this study, heat stress at 40 or 45°C increased φDIo. However, φDIo recovered to control levels after some time. In addition, δRo represents the efficiency with which an electron can move from PQ through PSI to the PSI end electron acceptor. The differential response of the δRo suggests that the redox state of PQ-pool was affected by the heat stress at 45°C but not 40°C (Fig. 4).
The efficiency of PSII under steady-state irradiance (ΦPSII) was closely related to the Pn [46]. In this study, under heat stress at 40°C or 45°C ΦPSII and qp decreased while NPQ increased. This suggests more energy was partitioned to heat dissipation and less energy was used in CO2 fixation under heat stress at both temperatures. However, the influence at 40°C was less than that at 45°C. After the second recovery, ΦPSII at 40°C increased more rapidly accompanied by an increase of qp and a decline of NPQ than that at 45°C. A NPQ increase of PSII is widely observed at temperatures where electron transport capacity slows with rising temperature [34], [36], which corresponds to the change in φDIo.
Conclusions
Heat treatment at 35°C did not significantly (P<0.05) influence grapevine photosynthesis. The decrease of Pn in grape leaves exposed to heat stress (40 or 45°C) was mainly attributed to the activation state of Rubisco and the donor side and the reaction center of PSII. However, the increase of Pn in grape leaves following heat stress was also associated with a stomatal responsec. The acceptor side of PSII in grape leaves was responsive but less sensitive to heat stress.
Materials and Methods
Plant materials and treatments
One-year old ‘Zuoyouhong’ grapevines (Vitis amurensis L.) were planted in pots, then grown in a greenhouse at 70–80% relative humidity, 25/18°C day/night cycle, with the maximum photosynthetically active radiation at about 1,000 µmol photons m2 s−1.
The progress of the experiment is shown in Table 1. Grapevines with identical growth (10 leaves) were acclimated for two days in a controlled environment room (70–80% relative humidity, 25/18°C day/night cycle and 800 µmol m2 s−1) and divided into four groups. On the following day (the first day of the experiment, Day 1), chlorophyll fluorescence and gas exchange parameters were analyzed at 9:30 h for all plants. Then, one group of grapevines was kept at 25°C in this controlled environment room. The other three groups were treated at 35, 40 or 45°C, respectively, in controlled environment rooms (except for temperature, the other conditions were the same as the 25°C room) until 14:30 h, when the relative photosynthesis parameters were then rapidly measured. The stressed grapevines were then allowed to recover at 25°C, with the other conditions the same as before heat treatments. On day 2, the same parameters were measured at 9:30 h, then the grapevines were stressed a second time until 14:30 h, when the relative photosynthesis parameters were then rapidly measured. The treated plants were again allowed to recover at 25°C as above. Chlorophyll florescence and gas exchange parameters were measured at 9:30 h on Day 3 and Day 6 during the following four days of recovery. All of the above measurements were made on the sixth leaf from the top of each plant. The experiment process is in Table 1. Four replications were made with leaves from different grape plants.
Analysis of photosynthetic gas exchange parameters
Photosynthetic gas exchange was analyzed with a Li-Cor 6400 portable photosynthesis system (Li-Cor Inc., Lincoln, NE, USA) which can control photosynthesis by means of photon flux density (PPFD), leaf temperature and CO2 concentration in the cuvette. Net photosynthetic rate (Pn), stomatal conductance (gs) and substomatal CO2 concentration (Ci) were determined at a concentration of ambient CO2 (360 µmol mol−1) , a PPFD of 800 µmol photons m−2 s−1, a 6 cm2 leaf area, a 500 µmol s−1 flow speed and at the treatment temperature.
Chlorophyll fluorescence quenching analysis
Chlorophyll fluorescence was measured with a FM-2 Pulse-modulated Fluorometer (Hansatech Instruments Ltd., King's Lynn, Norfolk, UK ). The maximal fluorescence level in the dark-adapted state (Fm) were measured by a 0.8 s saturating pulse at 8000 µmol m−2 s−1 after 15 min of dark adaptation. When measuring the induction, the actinic light (610 µmol photons m−2 s−1) was provided for 20 s by the FMS-2 light source. The steady-state fluorescence (Fs) was thereafter recorded and a second 0.8 s saturating light of 8000 µmol photons m−2 s−1 was provided to determine the maximum fluorescence in the light-adapted state (Fm′). The actinic light was then turned off and the minimal fluorescence in the light-adapted state (Fo′) was determined by illumination with 3 s of far red light. The following parameters were then calculated: (1) efficiency of excitation energy captured by open PSII reaction centers, Fv′/Fm′ = (Fm′−Fo′)/Fm′; (2) the photochemical quenching coefficient, qp = (Fm′−Fs)/(Fm′−Fo′); (3) the actual PSII efficiency, ΦPSII = (Fm′−Fs)/Fm′; and (4) non-photochemical quenching, NPQ = Fm/Fm′−1 [47].
Measurement of the polyphasic rise of chlorophyll a fluorescence (O-J-I-P)
The so-called OJIP-test was employed to analyze each chlorophyll a fluorescence transient by a Plant Efficiency Analyzer (Hansatech Instruments Ltd., King's Lynn, Norfolk, UK) which could provide information on photochemical activity of PSII and status of the plastoquinone pool [48]. The transients were induced by red light of about 3000 µmol photons m−2 s−1 provided by an array of six light emitting diodes (peak 650 nm). The fluorescence signals were recorded within a time span from 10 µs to 1 s with a data acquisition rate of 10 µs for the first 2 ms and every 1 ms thereafter. The fluorescence signal at 50 µs was considered as a true Fo. The following data from the original measurements were used: maximal fluorescence intensity (Fm); fluorescence intensity at 300 µs (Fk) [required for calculation of the initial slope (Mo) of the relative variable fluorescence (V) kinetics and Wk]; and the fluorescence intensity at 2 ms (the J-step) denoted as Fj, the fluorescence intensity at 30 ms (the I-step) denoted as Fi. Terms and formulae are as follows: relative variable fluorescence intensity, Vt = (Ft−Fo)/(Fm−Fo); a parameter which represent the damage to oxygen evolving complex (OEC), Wk = (Fk−Fo)/(Fj−Fo); approximated initial slope of the fluorescence transient, Mo = 4(Fk−Fo)/(Fm−Fo); probability that a trapped exciton moves an electron into the electron transport chain beyond QA−, ψEo = ETo/TRo = (Fm−Fj)/(Fm−Fo); maximum quantum yield of primary photochemistry at t = 0, φPo = TRo/ABS = Fv/Fm; quantum yield for electron transport (at t = 0), φEo = ETo/ABS = (Fm−Fj)/Fm; quantum yield at t = 0 for energy dissipation,φDIo = DIo/ABS = Fo/Fm; the density of QA-reducing reaction centers, RCQA = φPo×(Vj/Mo)×(ABS/CS); and the efficiency with which an electron can move from PQ through PSI to the PSI end electron acceptors, δRo = (1−Vi)/( 1−Vj). From OJIP transients, the extracted parameters led to the calculation and derivation of a range of new parameters (Table 2).
Extraction and assay of Ribulose-1,5-bisphosphate carboxylase/ oxygenase (Rubisco, EC4.1.1.39)
Leaves disks (1 cm2 each) were taken, then frozen in liquid nitrogen, and stored at −80°C until assay. Rubisco was extracted according to Chen and Cheng [49]. Three frozen leaves disks were ground with a pre-cooled mortar with 1.5 ml extraction buffer containing 50 mM Hepes-KOH (pH 7.5), 10 mM MgCl2, 2 mM EDTA, 10 mM dithiothreitol (DDT), 1% (v/v) Triton X-100, 1% (w/v) bovine serum albumin (BSA), 10% (v/v) glycerol, 0.5 mM phenylmethylsulfonyl fluoride (PMSF), and 5% (w/v) insoluble polyvinylpolypyrrolidone (PVPP). The extract was centrifuged at 13,000×g for 5 min in an Eppendorf microcentrifuge at 2°C, and the supernatant was used immediately for enzyme assays.
For Rubisco initial activity, a 50 µl sample extract was added to a semimicrocuvette containing 900 µl of an assay solution, immediately followed by adding 50 µl 0.5 mM RuBP, mixing well. The change of absorbance at 340 nm was monitored for 40 s. For Rubisco total activity , 50 µl 0.5 mM RuBP was added 15 min after a sample extract was combined with assay solution to activate all the Rubisco. Rubisco activation state was calculated as the ratio of initial activity to total activity [49], [50].
Author Contributions
Conceived and designed the experiments: LJW SHL. Performed the experiments: HBL LM HFX JFW. Analyzed the data: LJW WD. Contributed reagents/materials/analysis tools: SHL LJW. Wrote the paper: LJW HBL WL.
References
- 1. Berry JA, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol Plant Mol Bio 31: 491–543.
- 2.
Quinn PJ, Williams WP (1985) Environmentally induced changes in chloroplast membranes and their effects on photosynthetic function. In: Barber J, Baker NR, editors. Photosynthetic mechanisms and the environment. Amsterdam: Elsevier Science Publishers, Biomedical Division. pp. 1–47.
- 3. Havaux M (1993) Rapid photosynthetic adaptation to heat stress triggered in potato leaves by moderately elevated temperatures. Plant Cell Environ 16: 461–467.
- 4. Murakami Y, Tsuyama M, Kobayashi Y, Kodama H, Iba K (2000) Trienoic fatty acids and plant tolerance of high temperature. Science 287: 476–479.
- 5. Nash D, Miyao M, Murata N (1985) Heat inactivation of oxygen evolution in photosystem II particles and its acceleration by chloride depletion and exogenous manganese. Biochim Biophys Acta 807: 127–133.
- 6. Enami I, Tomo T, Kitamura M, Katoh S (1994) Immobilization of the three extrinsic proteins in spinach oxygen-evolving photosystem II membranes: roles of the proteins in stabilization of binding of Mn and Ca2+. Biochim Biophys Acta 1185: 75–80.
- 7. Bukhov NG, Sabat SC, Mohanty P (1990) Analysis of chlorophyll a fluorescence changes in weak light in heat treated Amaranthus chloroplasts. Photosynth Res 23: 81–87.
- 8. Pospíil P, Tyystjärvi E (1999) Molecular mechanism of high temperature-induced inhibition of acceptor side of photosystem II. Photosynth Res 32: 55–66.
- 9. Kouil R, Lazár D, Ilík P, Skotnica J, Krch ák P, et al. (2004) High temperature-induced chlorophyll fluorescence rise in plants at 40–50°C: experimental and theoretical approach. Photosynth Res 81: 49–66.
- 10. Jones R, Hoegh-Guldberg O, Larkum AWL, Schreiber U (1998) Temperature induced bleaching of corals begins with impairment of dark metabolism in zooxanthellae. Plant Cell Environ 21: 1219–1230.
- 11. Bukhov NG, Dzhibladze TG (2002) The effect of high temperatures on the photosynthetic activity of intact barley leaves at low and high irradiance. Russ J Plant Physiol 49: 332–335.
- 12. Law RD, Crafts-Brandner SJ (1999) Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/ oxygenase. Plant Physiol 120: 173–181.
- 13. Crafts-Brandner SJ, Law RD (2000) Effect of heat stress on the inhibition and recovery of ribulose-1,5-bisphosphate carboxylase/oxygenase activation state. Planta 212: 67–74.
- 14. Crafts-Brandner SJ, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc Natl Acad Sci USA 97: 13430–13435.
- 15. Spreitzer RJ, Salvucci ME (2002) Rubisco.: interactions, associations and the possibilities of a better enzyme. Annu Rev Plant Biol 53: 449–475.
- 16.
Mullins MG, Bouquet A, Williams LE (1992) Biology of the grapevine. Cambridge: Cambridge University Press. 43 p.
- 17. Schultz HR (2000) Climate change and viticulture: A European perspective on climatology, carbon dioxide and UV-B effects. Aust J Grape Wine Res 6: 2–12.
- 18. Van Leeuwen C, Friant P, Chone X, Tregoat O, Koundouras S, et al. (2004) The influence of climate, soil and cultivar on terroir. Am J Enol Viticult 55: 207–217.
- 19.
Schultz HR (2007) Climate change and world viticulture. Cost Action 858 Workshop: Vineyard under environmental constraints: adaptations to climate change. Abiotic stress ecophysiology and grape functional genomics. Poland: University of Lodz.
- 20. Sepúlveda G, Kliewer WM (1986) Stomatal response of three grapevine cultivars (Vitis vinifera L.) to high temperature. Am J Enol Vitic 37: 44–52.
- 21. Matsui S, Ryugo K, Kliewer WM (1986) Growth inhibition of Thompson Seedless and Napa Gamay berries by heat stress and its partial reversibility by applications of growth regulators. Am J Enol Viticult 37: 67–71.
- 22. Lakso AN, Kliewer WM (1978) The influence of temperature on malic acid metabolism in grape berries. II. Temperature responses of net dark CO2 fixation and malic acid pools. Am J Enol Viticult 29: 145–149.
- 23. Ferrini F, Mattii GB, Nicese FP (1995) Effect of temperature on key physiological responses of grapevine leaf. Am J Enol Viticul 46: 375–379.
- 24. Kadir S (2006) Thermostability of photosynthesis of V. aestivalis and V. vinifera. J Am Soc Horticul Sci 131: 476–483.
- 25. Kadir S, Von Weihe M, Kassim AK (2007) Photochemical efficiency and recovery of photosystem II in grapes after exposure to sudden and gradual heat stress. J Am Soc Horticul Sci 132: 764–769.
- 26. Hendrickson L, Ball MC, Osmond CB, Furbank RT, Chow WS (2003) Assessment of photoprotection mechanisms of grapevines at low temperature. Funct Plant Biol 30: 631–642.
- 27. Hendrickson L, Ball MC, Wood JT, Chow WS, Furbank RT (2004) Low temperature effects on photosynthesis and growth of grapevine. Plant Cell Environ 27: 795–809.
- 28. Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22: 131–160.
- 29. Strasser BJ (1997) Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients. Photosynth Res 52: 147–155.
- 30.
Strasser RJ, Srivatava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P, editors. Probing photosynthesis: mechanism, regulation and adaptation. Bristol: Taylor and Francis. pp. 445–483.
- 31. Lin ZH, Chen LS, Chen RB, Zhang FZ, Jiang HX, et al. (2009) CO2 assimilation, ribulose -1,5 -bisphosphate carboxylase/oxygenase, carbohydrates and photosynthetic electron transport probed by the JIP-test of tea leaves in response to phosphorus supply. BMC Plant Bio 9: 43.
- 32. Srivastava A, Guisse B, Greppin H, Strasser RJ (1997) Regulation of antenna structure and electron transport in photosystem II of Pisum sativum under elevated temperature probed by the fast polyphasic chlorophyll a fluorescence transient: OKJIP. Biochim Biophys Acta 1320: 95–106.
- 33.
Strasser RJ, Srivatava A, Tsimilli-Michael M (1999) Screening the vitality and photosynthetic activity of plants by fluorescence transient. In: Behl RK, Punia MS, Lather BPS, editors. Crop improvement for food security. India: AAARM. pp. 72–115.
- 34. Salvucci ME, Crafts-Brandner SJ (2004) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant 120: 179–186.
- 35. Kurek I, Chang TK, Bertain SM, Madrigal A, Liu L, et al. (2007) Enhanced thermostability of Arabidopsis rubisco activase improves photosynthesis and growth rates under moderate heat stress. Plant Cell 19: 3230–3241.
- 36. Schrader SM, Wise RR, Wacholtz WF, Ort DR, Sharkey TD (2004) Thylakoid membrane responses to moderately high leaf temperature in Pima cotton. Plant Cell Environ 27: 725–736.
- 37. Wise RR, Olson AJ, Schrader SM, Sharkey TD (2004) Electron transport is the functional limitation of photosynthesis in field-grown Pima cotton plants at high temperature. Plant Cell Environ 25: 717–724.
- 38. Cen YP, Sage RF (2005) The regulation of rubisco activity in response to variation in temperature and atmospheric CO2 partial pressure in sweet potato. Plant Physiol 139: 979–990.
- 39. Makino A, Sage RF (2007) Temperature response of photosynthesis in transgenic rice transformed with ‘sense’ or ‘antisense’ rbcS. Plant Cell Physiol 48: 1472–1483.
- 40. Weis ER (1981) Heat-inactivation of the Calvin cycle: a possible mechanism of the temperature regulation of photosynthesis. Planta 151: 33–39.
- 41. Kobza J, Edwards GE (1987) Influences of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiol 83: 69–74.
- 42. Feller U, Crafts-Brandner SJ, Salvucci ME (1998) Moderately high temperature inhibits ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase-mediated activation of Rubisco. Plant Physiol 116: 539–546.
- 43. Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30: 1086–1106.
- 44. Wang LJ, Fan L, Loescher W, Duan W, Liu GJ, et al. (2010) Salicylic acid alleviates decreases in photosynthesis under heat stress and accelerates recovery in grapevine leaves. BMC Plant Biol 10: 34.
- 45. Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transients in plants and cyanobacteria. Photochem Photobiol 61: 32–42.
- 46. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87–92.
- 47. Demmig-Adams B, Winter K (1986) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiol Plant 98: 253–264.
- 48. Strauss AJ, Kruger GHJ, Strasser RJ, Van Heerden PDR (2006) Ranking of dark chilling tolerance in soybean genotypes probed by the chlorophyll a fluorescence transient O-J-I-P. Environ Exp Bot 56: 147–157.
- 49. Chen LS, Cheng L (2003) Carbon assimilation and carbohydrate metabolism of ‘Concord’ grape (Vitis labrusca L.) leaves in response to nitrogen supply. J Am Soc Horticul Sci 128: 754–760.
- 50. Cheng LL, Fuchigami LH (2000) Rubisco activation state decreases with increasing nitrogen content in apple leaves. J Exp Bot 51: 1687–1694.