Journal of Experimental Botany, Vol. 51, No. 346, pp. 911-917,
May 2000
© 2000 Oxford University Press
Role of light in the response of PSII photochemistry to salt stress in the cyanobacterium Spirulina platensis
Department of Biology, Hong Kong Baptist University, Kowloon Tong, Hong Kong
Received 1 November 1999; Accepted 12 January 2000
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Abstract |
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The role of light in the effect of salt stress on PSII photochemistry in the cyanobacterium Spirulina platensis grown at 50 µmol m-2 s-1 was investigated. The time-course of changes in PSII photochemistry in response to high salinity (0.8 M NaCl) incubated in the dark and at 30, 50 and 100 µmol m-2 s-1 was composed of two phases. The first phase, which was independent of light, was characterized by a rapid decrease (20–50%) in the maximal efficiency of PSII photochemistry (Fv/Fm), the efficiency of excitation energy capture by open PSII reaction centres (
/
), photochemical quenching (qP), and the quantum yield of PSII electron transport (
PSII) in the first 15 min, followed by a recovery of up to about 86–92% of their initial levels after 4 h of incubation. The second phase took place after 4 h, in which a further decline in the above parameters occurred only in the light but not in the dark, reaching levels as low as 32–56% of their initial levels after 12 h. Moreover, the higher incubation light intensity, the greater the decrease in the above parameters. At the same time, QB-non-reducing PSII reaction centres increased significantly in the first 15 min and then recovered to the initial level during the first phase, but increased again in the light in the second phase. Photosynthetic oxygen evolution activity decreased sharply by 70% in the first 5 min, and then kept largely constant until 12 h. The changes in oxygen evolution activity were independent of light intensity during both phases. Key words: Chlorophyll fluorescence, light effect, PSII photochemistry, salt stress, Spirulina platensis, cyanobacterium.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Photosynthesis of algae is inhibited by salt stress (review: Kirst, 1990
). Such an inhibition seems to be associated with a decrease in PSII activity. In the green alga Dunaliella tertiolecta, a decrease in PSII activity induced by salt stress was associated with state-2 transition (Gilmour et al., 1984, 1985). This has been confirmed (Endo et al, 1995) and it was also suggested that the inhibition of quantum yield of PSII electron transport in salt-stressed Chlamydomonas reihardtii is related to the state-2 transition. In the red alga Porphyra perforata, it has been demonstrated that a decrease in PSII activity induced by salt stress was due to the decrease in excitation energy reaching PSII reaction centres and damage to the oxidizing side of PSII (Satoh et al., 1983). In cyanobacteria, it has been suggested that the state-2 transition and a decrease in the content of PSII reaction centres may be responsible for the decreased PSII activity in salt-stressed cells (Schubert and Hagemann, 1990; Schubert et al., 1993), whereas it has been shown that salt stress has no effect on PSII activity when Synechocystis cells are exposed to high salinity (0.55 M NaCl) (Jeanjean et al., 1993). Thus, it is still a matter of uncertainty about how salt stress affects PSII photochemistry in algae. Previous studies on the effects of salt stress on PSII in algae were normally carried out by exposing the cells to salt stress and simultaneously incubating them under the original growth light condition. It is possible that the changes in PSII activity observed before may not result from salt stress itself but from the interaction of salt stress and light, which are defined poorly in previous studies reporting the changes in PSII activity.
In this study, the changes in PSII photochemistry in the cyanobacterium Spirulina platensis exposed to different salt concentrations and incubated either in the dark or under different light intensity have been examined in detail. The results reveal that the response of PSII photochemistry in S. platensis cells to salinity consisted of two distinct phases. The first phase, which was independent of light, was characterized by a rapid decrease in PSII activity followed by a subsequent recovery. In the second phase, a progressive decrease in PSII activity was observed only in the light and, the higher the incubation light intensity, the greater the decrease in PSII activity.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Cell culture
Spirulina platensis M2 was grown in Zarouk's medium, containing 200 mM sodium bicarbonate (Vonshak et al., 1982
) at photon flux density (PPFD) of 50 µmol m-2 s-1 provided by fluorescent lamps at 35 °C.
Salt stress and light treatments
Exponentially grown cells were harvested and resuspended in a fresh medium containing different concentrations of NaCl (0.2, 0.4, 0.6, and 0.8 M exclusive of 0.017 M NaCl already present in the medium) and incubated at 35 °C for 12 h with three light treatments: at PPFD of 30, 50 and 100 µmol m-2 s-1, or in the dark.
Photosynthetic oxygen evolution activity
Light-saturated photosynthetic oxygen evolution activity was measured at 35 °C using a Clarke-type electrode. Cells were harvested and resuspended in fresh medium containing the same NaCl concentration as that to which cells were adapted. Measuring light intensity was 900 µmol m-2 s-1 using a 100 W halogen lamp.
Measurements of chlorophyll and phycocyanin
Chlorophyll was determined according to Bennet and Bogorad (Bennet and Bogorad, 1973). The absorbance of phycocyanin was measured spectrophotometerically at 620 nm and its concentration was then calculated from the specific absorption coefficient E1%=73 (Boussiba and Richmond, 1979).
Fluorescence quenching analysis
Chlorophyll fluorescence quenching analysis was carried out at room temperature with a portable fluorometer (PAM-2000, Walz, Effeltrich, Germany). The fluorometer was connected to a computer with data acquisition software (DA-2000, Walz).
The procedure follows in general that which was developed for cyanobacteria (Campbell et al., 1998). After the cells were dark-adapted for 10 min, the minimal fluorescence level in the dark-adapted state (
) was measured by the measuring modulated light which was sufficiently low (0.1 µmol m-2 s-1) not to induce any significant variable fluorescence. A 0.8 s flash of saturating white light (8000 µmol m-2 s-1) was then given to determine the maximal fluorescence in the dark-adapted state, Fm(dark). The white actinic light (50 µmol m-2 s-1) was then turned on. The steady-state fluorescence, Fs, was reached within 2.5 min and a saturating light flash was given again to determine the maximal fluorescence in the light-adapted state, . In the dark, cyanobacteria are normally in state-2, with high non-photochemical quenching and low PSII fluorescence, since the PQ pool is reduced by respiratory electron transport. When illuminated, they rapidly shift to state-1, with lower non-photochemical quenching and increased PSII fluorescence (Öquist et al., 1995). The reversion of the dark-adapted cells to state-1 can be promoted by far-red illumination which is preferentially absorbed by photosystem I (PSI). The minimal fluorescence level in the light-adapted state, , was, therefore, measured by briefly interrupting the actinic light and illuminating the cells with far-red light for 3 s (5 µmol m-2 s-1). Since a single, high-intensity flash produces a Fm value, i.e. Fm(dark), in dark-adapted Spirulina cells that is 10–15% lower than the true Fm due mainly to the state transition (Öquist et al., 1995), the true maximal fluorescence was measured in the presence of 10 µM 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) to allow non-photochemical quenching to collapse after the steady-state fluorescence was achieved.
Using both light and dark fluorescence parameters, the following was calculated: (1) the maximum efficiency of PSII photochemistry in the dark-adapted state, Fv/Fm, (2) the photochemical quenching coefficient, qP=(
-Fs)/-
), which measures the proportion of open PSII reaction centres (van Kooten and Snel, 1990), (3) the efficiency of excitation energy capture by open PSII reaction centres, 
/=(-/, (4) the actual quantum yield of PSII electron transport in the light-adapted state, PSII=(–Fs)/, which was equal to the product of qP and / as defined previously (Genty et al., 1989). Therefore, PSII depends on the degree of the closed PSII reaction centres and the efficiency of excitation energy capture in PSII. Here, fluorescence nomenclature was according to van Kooten and Snel (van Kooten and Snel, 1990).
Kautsky fluorescence induction curve
Kautsky fluorescence induction curve was measured by PAM-2000 in the dark-adapted samples suddenly illuminated with moderate white light (20 µmol m-2 s-1) at a sampling rate of 1 ms point-1. In order to avoid an incomplete reoxidation of the plastoquinone pool in the dark, which could result in an increase in fluorescence level at phase I, the dark-adapted samples were illuminated with 3 s far-red light prior to the measurements of the fluorescence induction kinetics.
All samples were dark-adapted for 10 min before chlorophyll fluorescence was determined.
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Results |
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In order to study the effect of light on the responses of PSII photochemistry in Spirulina cells to salt stress, the cultures grown at 50 µmol photons m-2 s-1 were exposed to the different concentrations of NaCl (0–0.8 M) and incubated under three different PPFDs, i.e. 30 (<the original growth light intensity), 50 (=the original growth light intensity), 100 (>the original growth light intensity) µmol photons m-2 s-1 or in the dark.
Figure 1 shows the time-course of the maximal efficiency of PSII photochemistry (Fv/Fm) in response to 0.8 M NaCl. Addition of 0.8 M NaCl to a Spirulina culture incubated in the light resulted in an immediate decrease in Fv/Fm of about 35% in the first 15 min, followed by a partial recovery to about 91% of the original level after 4 h of incubation. Light intensity had no significant effect on the response of Fv/Fm to salt stress during the first 4 h. Four hours after the addition of 0.8 M NaCl, another decline in Fv/Fm was observed. Moreover, this decrease in Fv/Fm increased with the increase in light intensity. For example, Fv/Fm decreased by 14, 30 and 45% in the cells incubated at 30, 50 and 100 µmol m-2 s-1, respectively, after 12 h.
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) and at 30 (
), 50 (
) and 100 (
) µmol m-2 s-1. The true maximal fluorescence Fm was measured in the presence of 10 µM DCMU to allow non-photochemical quenching to collapse because of the state transition which may lower PSII fluorescence in cyanobacteria. The samples were dark-adapted for 10 min prior to fluorescence measurements. Values are mean±SE (n=3).The response pattern of Fv/Fm in cells incubated in the dark to 0.8 M NaCl was similar to that in cells incubated in the light in the first 4 h. Fv/Fm decreased rapidly by 35% in the first 15 min, and recovered subsequently to 92% of its initial level after 4 h of incubation. Nevertheless, the second decline in Fv/Fm occurring in the light was not observed after 4 h in the dark (Fig. 1
).
The time-courses of the efficiency of excitation energy capture by open PSII reaction centres (/), photochemical quenching (qP), and the quantum yield of PSII electron transport (PSII) in response to 0.8 M NaCl are shown in Fig. 2. Their response patterns in the dark and the light were similar to those of Fv/Fm. During the first 4 h, /, qP and PSII decreased by 40%, 20% and 50% in the first 15 min, followed by a partial recovery to around 92, 93 and 86% of their original values, respectively, after 4 h of incubation. The changes in these three parameters were also independent of light conditions. After 4 h from the beginning of the salt treatment, a second decline in these parameters was observed only in the light and this decline increased with the increase of light intensity.
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The time-course of the changes in the rapid fluorescence induction kinetics (Kautsky curve) in response to 0.8 M NaCl was further investigated. When the dark-adapted S. platensis cells are illuminated suddenly with low light, a typical Kautsky curve is observed, which displays a rapid rise of chlorophyll fluorescence from the minimal level (O) to an intermediate level (I) followed by a very fast rise to the maximum level (P) (curve a in Fig. 3A
) and this induction kinetics was similar to that of higher plants, such as wheat leaves (Lu and Zhang, 1999). The O–I phase has been attributed to QA reduction in QB-non-reducing PSII reaction centres, in which the electron transfer from 
to QB is inhibited. The amplitude of O–I can thus be considered as an indicator of electron transport from to QB (Chylla and Whitmarsh, 1989; Cao and Govindjee, 1990; Krause and Weis, 1991).
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Figure 3A
shows that an obvious increase in phase I was observed after the culture had been exposed for 12 h to 0.8 M NaCl and incubated at 100 µmol m-2 s-1. Figure 3B demonstrates the time-course of the changes in the amplitude of O–I in response to 0.8 M NaCl. Addition of 0.8 M NaCl caused a rapid increase in the amplitude of O–I in the first 15 min, thereafter, it showed a recovery to the original value in about 4 h. The data also show that the change in the amplitude of O–I in the first 4 h was independent of light. After 4 h, the amplitude of O–I increased significantly with the increase in light intensity, but was maintained in the dark.
The above results indicate that the response of PSII photochemistry to salinity stress in S. platensis cells consisted of two distinct phases. The first phase took place in the first 4 h of exposure to salinity. A transient decrease of Fv/Fm, /
, qP, PSII, or a rapid increase in the amplitude of O–I followed by subsequent recovery as observed regardless of light conditions, suggesting that this phase is independent of light. The second phase proceeded after the first 4 h of salt stress. The changes in PSII photochemistry during this phase are light-dependent, suggesting that photoinhibition was induced by salt stress. It should be noted that the two-phase responses of the fluorescence parameters to salinity were observed only when S. platensis cells were exposed to high salinity. When salinity was lower than 0.4 M NaCl, the first phase could not be observed and the changes in PSII photochemistry occurred only during the second phase.
The time-course of light-saturated photosynthetic activity was further investigated in response to salt stress (Fig. 4). The addition of 0.8 M NaCl caused an immediate inhibition of photosynthetic activity. After 15 min exposure to salt shock, the oxygen evolution decreased sharply to about 30% of the initial values in both light- and dark-incubated cells. Thereafter, photosynthetic activity partially recovered to 37% of their initial values in both light- and dark-incubated cells in about 4 h. Photosynthetic activity then remained constant in both light- and dark-incubated cells. The changes in photosynthetic activity in the whole course were independent of light condition.
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The time-course of the changes in the chlorophyll and phycocyanin contents was also followed (Fig. 5
). The chlorophyll content decreased slightly by 6% in the first 4 h irrespective of light condition. After 4 h it decreased significantly with the increase light intensity, but remained unchanged in the dark (Fig. 5A). Phycocyanin content decreased sharply by 60% in the first 2 h and thereafter remained constant. The changes in phycocyanin content during whole course were not affected by light conditions (Fig. 5B).
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To confirm that the changes in PSII photochemistry in the second phase, i.e. after 4 h from the beginning of a salt treatment, were due to photoinhibition induced by salt stress, the effects of different incubation light intensity on PSII photochemistry were evaluated after the cells were exposed to different salt concentrations for 12 h.
Figure 6 shows the changes in Fv/Fm in response to salt stress incubated either in the light, at 30, 50 and 100 µmol photons m-2 s-1 or in the dark for 12 h. It demonstrates that the cells exposed to salt stress in the dark exhibited no significant loss in Fv/Fm. On the other hand, the cells incubated in the light during their exposure to salt stress showed a drastic decline in Fv/Fm. Moreover, the higher the incubation light intensity, the greater the decrease in Fv/Fm.
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Similarly, salt stress induced no significant decrease in
/, qP, and PSII in the dark but a considerable decrease in /, qP, and PSII was observed when the cells were incubated in the light. The culture incubated at the lower PPFDs exhibited a smaller decrease in /, qP, and PSII than incubated at the higher PPFDs (Fig. 7).
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Figure 8
shows the changes in the amplitude of O–I determined from the Kautsky curves. The culture, which was exposed to salt stress and incubated in the dark, did not show a big change in the amplitude of O–I, while there was a significant increase in the amplitude of O–I when the culture was incubated in the light. Similar to the changes in Fv/Fm, /, qP, and PSII, the higher the incubation light intensity, the greater the increase in the amplitude of O–I.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The changes in the fluorescence parameters during the time-course of salt stress reveal that the response of PSII photochemistry in S. platensis cells to salinity consisted of two distinct phases. In the first phase, a rapid decrease in Fv/Fm,
/, qP, PSII and a rapid increase in the amplitude of O–I combined by a subsequent recovery occurred in the light and in the dark. Changes in these parameters during this phase were not affected by light intensity (Figs 1–3). These results suggest that the changes in fluorescence parameters during this phase were independent of light. In the second phase, a progressive decrease in Fv/Fm, /, qP, PSII, as well as a continuous increase in the amplitude of O–I were observed only in the light. Moreover, the higher the incubation light intensity, the greater the changes in these fluorescence parameters, indicating that a photoinhibitory stress was induced in this phase as a result of the salinity stress (Figs 1–3, 6–8). These results clearly demonstrate that during the second phase, salt stress per se has little direct effect on PSII photochemistry, but that light plays a crucial role in the effect of salt stress on PSII photochemistry in Spirulina cells. The changes in PSII photochemistry induced by salt stress in this phase obviously arise not from salt stress itself, but rather from the interaction of salt stress and light. However, the changes in PSII photochemistry during the first phase are apparently induced only by salt stress and is a largely reversible process. The immediate inhibition of PSII photochemistry after expose to salt stress can be explained by an immediate increase in the cellular sodium content (Ehrenfeld and Cousin, 1984; Reed et al., 1985), while the subsequent recovery of PSII photochemistry may be due to the rapid extrusion of sodium from the cells (Molitor et al., 1986) which is probably associated with the sodium–proton antiporter (Blumwald et al., 1984; Padan and Schuldiner, 1994). These results indicate the complexity of the response of PSII photochemistry to salt stress in Spirulina cells.
The results show that light-saturated photosynthetic oxygen evolution activity was much more inhibited than PSII photochemistry (Figs 1, 4). Light-saturated photosynthetic oxygen evolution activity decreased by 70% in the first 15 min and this decrease was largely irreversible. More importantly, such an inhibition was independent of light intensity and a similar inhibition was also observed in the dark during both the first and the second phases. However, the changes in PSII photochemistry during the first phase were almost reversible, and salt stress had no significant effect on PSII photochemistry in the dark during the second phase. These results indicate that the photosynthetic dark-reaction processes (i.e. CO2 assimilation process) rather than PSII photochemistry is the primary damage site by salt stress and that the CO2 assimilation process is highly sensitive to salt stress.
CO2 assimilation acts as a major sink for the reducing equivalents (ATP and NADPH) generated by the primary photochemical reactions. Substantially inhibited CO2 assimilation processes by salt stress suggest that the photosynthetically-generated energy equivalents ATP and NADPH would be in excess of what was required for the decreased CO2 assimilation. Salt stress could potentially lead to an increased susceptibility to photoinhibitory damage to the PSII apparatus even at low irradiance if excess excitation energy could not be dissipated safely (Powles, 1984). In cyanobacteria, excess excitation energy is mainly dissipated by shifting the excitation flow from the phycobilisome to photosystem I through a state transition (quist et al., 1995; Campbell et al., 1996, 1998), unlike in higher plants, where excess excitation energy can be mainly dissipated by energy-dependent quenching mechanisms (Demmig-Adams and Adams, 1992). During the first phase, the significant loss of phycocyanin (major antenna pigment in cyanobacteria) and small loss of chlorophyll accompanied by the significant inhibition of photosynthetic CO2 assimilation capacity suggests that the cells may down-regulate their light-harvesting capacity to acclimate their low carbon metabolic capacity. During the second phase, it seems that although salt stress induced a substantial decrease in phycocyanin which would decrease the absorption of excitation energy (Fig. 5B), the existing mechanism of excess excitation energy dissipation by the state transition in Spirulina cells under salt stress is not enough to prevent the PSII apparatus from photodamage. This is because the decrease in PSII photochemical efficiency was observed even at relatively low light (30 µmol m-2 s-1) (Figs 1, 6) and loss of chlorophyll increased with an increase in light intensity (Fig. 5A). The decline in PSII photochemical efficiency and the loss of chlorophyll during this phase suggest that photodamage was occurring to the photosynthetic apparatus.
During both phases, the decrease in the quantum yield of PSII electron transport (PSII) observed in this study was due to a decrease in both photochemical quenching (qP) and the efficiency of excitation energy capture (/) (Figs 2, 7).
Small differences between the extent of the decreased / and the decreased Fv/Fm (Figs 6, 7A) suggest the decrease in / was mainly due to a decrease in Fv/Fm, but also possibly due to slowly relaxing fluorescence quenching. The decrease in Fv/Fm was accompanied by a substantial increase in the proportion of the QB-non-reducing PSII reaction centres (Fig. 8). This may suggest that the decreased Fv/Fm was a result of the increased proportion of the inactivated PSII reaction centres.
The decrease in qP may indicate an increase in the proportion of the reduced state of QA (Dietz et al., 1985; Genty et al., 1989). How could the interaction of salt stress and light induce an increase in the proportion of the reduced state of QA? The results of this study showed a substantial increase in the proportion of the QB-non-reducing PSII reaction centres during two phases. It has been shown that the key characteristic of the QB-non-reducing PSII reaction centres is an inability to transfer electrons from QA to QB (Chylla and Whitmarsh, 1989; Cao and Govindjee, 1990). It is evident that a blocking of electron transfer from QA to QB will inevitably result in an accumulation of reduced QA and thereby a decrease in qP.
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Acknowledgments |
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Financial support by FRG (Faculty Research Grant) of the Hong Kong Baptist University and the Croucher Foundation is gratefully acknowledged.
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Notes |
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1 To whom correspondence should be addressed. Fax: +852 2339 5995. E-mail:jzhang{at}net1.hkbu.edu.hk
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Abbreviations |
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Fo, minimal fluorescence level in the dark-adapted state;
, minimal fluorescence level in light-adapted state; Fm, maximal fluorescence level in dark-adapted state; , maximal fluorescence level in light-adapted state; Fv, maximum variable fluorescence level in the dark-adapted state; , maximum variable fluorescence level in the light-adapted state; Fs, steady-state fluorescence level at qP>0; Fv/Fm, maximal efficiency of PSII photochemistry; PSII, quantum yield of PSII electron transport; /, efficiency of excitation energy capture by open PSII reaction centres; QA, primary quinone electron acceptor of PSII; QB, secondary quinone electron acceptor of PSII; qP, photochemical quenching coefficient.. |
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