Photosynth Res DOI 10.1007/s11120-010-9588-y
REGULAR PAPER
Characterization of photosystem II heterogeneity in response to high salt stress in wheat leaves (Triticum aestivum) Pooja Mehta • Suleyman I. Allakhverdiev Anjana Jajoo
•
Received: 5 May 2010 / Accepted: 2 August 2010 Ó Springer Science+Business Media B.V. 2010
Abstract The effect of high salt stress on PS II heterogeneity was investigated in wheat (Triticum aestivum) leaves. On the basis of antenna size, PS II has been classified into three forms, i.e., a, b, and c centers while on the basis of electron transport properties of the reducing side of the reaction centers, two distinct forms of PS II have been suggested, i.e., QB reducing centers and QB nonreducing centers. The chlorophyll a (Chl a) fluorescence transients, which can quantify PS II behavior, were recorded using PEA to derive OJIP in vivo with high time resolution and further analyzed according to JIP test. Our results showed that with an increase in the salt concentration during growth, the number of QB non-reducing centers increased. In antenna size heterogeneity the number of b and c centers increased while the number of a centers decreased. A change in the energetic connectivity between the PS II units was also observed. Recovery studies showed that antenna heterogeneity was completely recovered from damage at 0.5 M NaCl concentration and partially recovered at 1 M NaCl concentration while reducing side heterogeneity showed no recovery at all after 0.5 M onwards.
P. Mehta A. Jajoo (&) School of Life Science, Devi Ahilya University, Indore 452017, MP, India e-mail:
[email protected] S. I. Allakhverdiev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, Moscow 127276, Russia S. I. Allakhverdiev Institute of Basic Biological Problems, Puschino, Moscow Region 142290, Russia
Keywords Photosystem II Heterogeneity High salt stress Antenna size Abbreviations ABS Absorption Chl Chlorophyll DCMU 3-(3,4-Dichlorophenyl)-1,1-dimethylurea ETo Electron transport flux beyond QA FR Fluorescence rise FI Fluorescence induction curve RCs Reaction centers TRo Energy trapping flux by PS II centers
Introduction PS II is a multisubunit integral membrane protein complex used by higher plants and cyanobacteria to catalyze water oxidation and plastoquinone reduction (Boekema et al. 2000). The reaction center of PS II consist of D1–D2 proteins, which contain accessory Chl on D1 branch as primary electron donor (Groot et al. 2005; Holzwarth et al. 2006), the secondary electron donor P680, Yz, and YD (tyrosine), the intermediatory electron acceptor Pheophytin (Pheo) and two plastoquinone electron acceptor QA and QB along with an associated non-heme iron. PS II is a lightdependent water-plastoquinone oxidoreductase enzyme that uses light energy to oxidize water and is mainly located in the appressed grana stacks (Carpentier et al. 2005; Allakhverdiev et al. 2008). PS II has been found to be more heterogeneous than other components such as PS I and Cyt b6f in various aspects and differs in its structure and function both. This
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diverse nature of PS II is known as PS II heterogeneity. The fluorescence rise measured with DCMU treated plant material cannot be described by a single exponential increase (Doschek and Kok 1972). The biphasic fluorescence induction kinetics observed upon illumination of higher plant chloroplast suspended in the presence of herbicides (DCMU) was used for a description of one type of PS II heterogeneity, the PS II antenna heterogeneity (Melis and Homann 1975, 1976). Two main aspects of PS II heterogeneity have been studied widely: antenna heterogeneity and reducing side heterogeneity. Antenna heterogeneity is related to the antenna size as well as to the energetic connectivity between PS II units. By using kinetic analysis of fluorescence induction curve of DCMU poisoned chloroplast, PS II has been resolved into three components of different antenna sizes, i.e., a, a-s, and b (Hsu et al. 1989) and lately renamed to PS II a, PS II b, and PS II c (Strasser 1981; Strasser and Greppin 1981; Melis 1985; Hsu and Lee 1991), respectively, while Sinclair and Spence (1990) demonstrated four types of PS II, i.e., a, b, U, and d. PS II a are mainly located in the grana region of thylakoid membranes, have a large light harvesting antenna and show the possibility of excited states transfer between PS II units which displays a sigmoidal fluorescence rise when measured with DCMU. On the other hand PS II b are mainly located in stromal region of thylakoid membranes, have 2.5 times smaller light harvesting antenna and show impossibility of the excited states transfer between PS IIs displays in the form of an exponential fluorescence rise when measured with DCMU. Smaller antenna size in PS II b fraction has been ascribed to the absence of peripheral LHC II in PS II. The intrinsic trapping and fluorescence property of a and b centers are considered to be similar (Melis 1991). The antenna size of PS II c is the smallest amongst all. PS II a and PS II b both are photochemically competent and are able to transfer electron from QA to QB (Thielen and Van Gorkom 1981; Lavergne 1982; Melis 1985; Graan and Ort 1986; Ghirardi and Melis 1988; Greene et al. 1988; Guenther et al. 1988). According to the concept of connectivity (also called grouping) closed PS II reaction centers (RC) may transfer their excitation energy to open neighboring PS II units that results in sigmoidal fluorescence rise instead of exponential rise (Lavergne and Trissl 1995; Joliot and Joliot 1964; Joliot et al. 1973; Strasser et al. 2004). It was suggested that the three populations of PS II units (a, b, and c) are different in their connectivity properties, i.e., the a-centers are supposed to be grouped, whereas the two others are not, and the trapping efficiency of the c-centers is thought to be lowest. Based on the electron transport properties on the reducing side of the reaction centers, PS II in green plants occurs in two distinct forms: centers with efficient electron transport from QA to QB are known as QB reducing type,
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while centers that are photochemically competent but unable to transfer electron from QA to QB are known as QB non-reducing type (Graan and Ort 1986). In such centers QA can only be reoxidized by a back reaction with the donor side of PS II. QB reducing centers are active centers while QB non-reducing centers are inactive centers. Using fluorescence transients, the measurement of reducing side heterogeneity has been done in two ways: (i) by measuring height of the plateau (Fpl) in the presence of DCMU under low light intensity (Tomek et al. 2001), (ii) by double hit method where two fluorescence transients were induced by two subsequent pulses (Strasser et al. 2004). Various stress condition like high temperature, high salt, etc., adversely affect photosynthetic efficiency, particularly at the donor side and acceptor side of Photosystem II (Mathur et al. 2010; Mehta et al. 2010). Extent and nature of PS II heterogeneity may vary under different physiological conditions, i.e., high salt stress, temperature stress, etc. High salt stress is one of the major environmental factors that limit the plant productivity. Salt stress leads to reduction in the growth of the plant, which is associated with a decrease in the rates of photosynthesis. Many crop species are sensitive to high concentration of salt with negative impact on the crop production. There are many studies about the effects of salt stress on fluorescence induction kinetics (Mehta et al. 2010), however, investigation of change in PS II heterogeneity in response to high salt stress has not yet been studied. In the present work we have determined the effect of high salt stress on antenna and reducing side heterogeneity of PS II in wheat. Since most of the changes obtained in the heterogeneity of PS II were found to be reversible, we have proposed that alteration in the antenna size and reducing side heterogeneity of PS II may be a temporary adaptive mechanism exhibited by PS II to tolerate stress condition in the initial stages.
Materials and methods Plant material: wheat (Triticum aestivum) Lok-1 cultivar of wheat was used for experiments. Wheat seeds were allowed to germinate and then transferred to petriplates containing Knop solution with a photosynthetically active photon flux density (PPFD) of 300 l mol m-2 s-1, 20°C and a photoperiod of 16/8 h light/dark. High salt treatment High salt stress in the form of NaCl concentrations, i.e., 0.1, 0.2, 0.3, 0.4, 0.5, and 1 M NaCl was given to the seedlings gradually. For gradual stress, treatment of 0.1 M NaCl was given in steps to the seedlings after every 48 h
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from day one when it was transferred on nutrient medium (Knop solution) till when the concentration reached to 1 M. Measurement of fluorescence induction kinetics The chlorophyll a (Chl a) fluorescence induction kinetics was measured at room temperature using a Plant Efficiency Analyzer (PEA, Hansatech, King’s Lynn, Norfolk, England). The fluorescence measurements were performed two inches away from the tip and base, i.e., in the middle portion on the abaxial surface of the leaves. Thirty measurements were taken for each treatment. Excitation light of 650 nm (peak wavelength) from array of three light— emitting diodes is focused on the surface of the leaf to provide a homogenous illumination. Light intensity reaching the leaf was 3000 l mol m-2 s-1 which was sufficient to generate maximal fluorescence for all the treatments. The fluorescence signal is received by the sensor head during recording and is digitized in the control unit using a fast digital converter. Energy pipeline model was deduced using the Biolyzer HP 3 software (the chlorophyll fluorescence analyzing program by Bioenergetics Laboratory, University of Geneva, Switzerland). Determination of reducing side heterogeneities The double hit method was followed for the calculation of QB reducing and QB non-reducing centers (Strasser and Tsimilli-Michael 1998; Strasser et al. 2004). In this method two fluorescence transients were induced by two subsequent pulses (each of 1 s duration). The first pulse (denoted as 1st hit) was conducted after a dark period long enough to ensure the reopening of all reaction centers, followed by a second pulse (2nd hit). The duration of the dark interval between two hits is 500 ms (Fig. 1). Fv ¼ Fm Fo,
Fv ¼ Fm Fo
where Fv: variable fluorescence of 1st hit, Fm: maximal fluorescence of 1st hit, Fv*: variable fluorescence of 2nd hit, Fm*: maximal fluorescence of 2nd hit, Fo: minimal fluorescence of 1st hit, Fo* minimal fluorescence of 2nd hit. QB non-reducing centers were calculated by the following equation. VoðBoÞ ¼ ½ðFv=FmÞ ðFv =Fm Þ=ðFv=FmÞ where Bo = relative amount of QB non-reducing PS II centers (Strasser and Tsimilli-Michael 1998). The relative amounts of QB non-reducing center have been shown to vary with light intensity as suggested in Tomek et al. (2001), however, in this work, we have used high light intensity (3000 l mol m-2 s-1) for carrying out experiments in vivo. The advantage of the high light intensity is that the Fm can be clearly distinguished (To´th
Fig. 1 A representative fluorescence induction curve (log time scale) obtained from double hit method (as described in ‘‘Materials and methods’’ section). Fluorescence measurement was induced by two subsequent pulses (each of 1 s). The first pulse (denoted as 1st hit) was conducted after a dark period long enough to ensure the reopening of all reaction centers, followed by a second pulse (2nd hit). The duration of the dark interval between two hits was 500 ms. The graphs have time axis in logarithmic scale
and Strasser 2005). Similar light intensity has been used for control and salt stressed plants and so it was possible to measure relative changes in QB non-reducing centers. Determination of antenna heterogeneity For calculation of antenna heterogeneity, DCMU poisoning method (Strasser 1981; Hsu et al. 1989) was used. The method is as follows: wheat plants were put in darkness for *1 h before the DCMU treatment, and then pairs of leaves were placed into small trays (without detaching them from the plant) filled with 100 ml DCMU solution overnight and in complete darkness (the DCMU concentration was 200 lM, and the solution contained 1% ethanol, which was used to dissolve the DCMU). Following the treatment, leaves were removed from the DCMU solution (still not detached and in darkness), wiped and left in the air for *1 h to avoid possible effects of anaerobiosis. DCMU keeps QA in its reduced state during the measurements and does not reflect the photochemical reactions (Lazar et al. 2001). Determination of a, b, and c centers: Alpha (a), beta (b), and gamma (c) centers were calculated from the complementary area (CA) growth curve (Melis 1985). The CA is an area between the curve of fluorescence induction and line determining the level of the maximal fluorescence intensity Fm (Lazar 1999). Kinetics of
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complementary area of the dark adapted sample was fitted with three exponentials phases (corresponding to a, b, and c). Based on the lifetimes (s) of each of the fraction, their contribution to the total amplitude (A) of the kinetics of complementary area was calculated and has been indicated as percentage of a, b, and c centers (Strasser 1981; Hsu et al. 1989). It has been suggested that in the presence of DCMU, the kinetics of QA accumulation may be obtained by integrating the kinetics of complementary area. The complementary area is fitted by exponentials only and thus considers measurements of only energetically separated PS II units under salt stress.
Results and discussion Polyphasic chlorophyll a fluorescence transient was measured to evaluate the effects of high salt stress on the photochemical efficiency of PS II. The OJIP transient represents the successive reduction of electron transport pool of PS II (Govindjee 1995). The intensity of fluorescence in the OJIP transient decreased with increase in NaCl concentration, as shown in Fig. 2. An increase in salt
concentration causes a significant decrease in the minimal fluorescence (Fo), variable fluorescence (Fv), and maximal fluorescence (Fm). A decrease in the fluorescence yield of leaves can be attributed to an inhibition of electron flow at oxidizing site of PS II (Lu and Vonshak 2002). The decrease in Fm and fluorescence at J, I, P may be due to two reasons, first by inhibition of electron transport at the donor side of the PS II which results in the accumulation of P680? (Govindjee 1995; Neubauer and Schreiber 1987) and second due to a decrease in the pool size of QA. These chlorophyll a fluorescence transient curves measured in the absence (Fig. 2a) and presence of DCMU (Fig. 2b) were further used to evaluate the effect of high salt stress on reducing side and antenna size heterogeneity of Photosystem II. Effect of high salt stress on reducing side heterogeneity To study reducing side heterogeneity of PS II, relative amount of QB reducing and QB non-reducing centers were measured from the fluorescence rise (FR) curve as described in material and methods. The amount of QB nonreducing centers was increased in salt stressed leaves. In control leaves, the QB non-reducing centers were found to be 14% (Table 1) which became 32% in 0.5 M salt treatment. To study recovery process, the salt stressed leaves were kept in distilled water for 24 h and then fluorescence was measured. Leaves treated with 0.5 M NaCl showed no recovery, the number of QB non-reducing centers remained almost the same as in the 0.5 M NaCl treated leaves (Table 1). This result suggests that the damage at the reducing side of PS II was permanent. Effects of high salt stress on antenna heterogeneity The kinetics of complementary area of DCMU treated fluorescence induction curve was calculated by the equation R B ¼ ðFm FtÞdt , where B is the double normalized (between 0 and 1) kinetics of complementary area (Strasser Table 1 Relative changes in QB non-reducing and QB reducing centers in response to high salt stress in wheat leaves % of QB non-reducing centers
% of QB reducing centers
Control
14 ± 1
86 ± 4
0.1
15 ± 2
85 ± 3
0.2
21 ± 1
79 ± 2
0.3
23 ± 2
77 ± 3
0.4
25 ± 1
75 ± 2
0.5
32 ± 2
68 ± 3
Recovery
32 ± 2
68 ± 3
NaCl concentration (M)
Fig. 2 The OJIP Chl a fluorescence transient curve (log time scale) in wheat leaves exposed to various concentration of NaCl for 1 h dark. The graphs have time axis in logarithmic scale
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Experiment was repeated 5 times
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et al. 2000; Murata et al. 1966; Malkin and Kok 1966) and the B kinetics of the first light pulse were fitted with three exponentials that correspond to three different types of PS II centers namely PS II a, b, and c. They were further analyzed and later assigned as PS II a, b, and c centers on the basis of their life times. As is evident from Fig. 3, the lifetime of the fastest a component was 0.37 ms and contributed 70% of the total amplitude. The beta component was about 3.8-fold slower (life time *1.44 ms) and it was responsible for 26% of the total amplitude. The gamma component was very slow with lifetime of 9.14 ms and small, being only 4% of the total amplitude in control leaves. The changes in percentage of a, b, and c components with different salt concentrations are shown in Fig. 3. With increase in salt concentration the percentage of a centers decreased while that of b and c centers increased. The number of c centers has increased more as compared to b centers with increase in the salt concentration. The relative ratio of a:b:c centers in control leaves was 70:26:4 while it became 38:36:26 in salt stressed leaves (1 M NaCl). Recovery for antenna heterogeneity was also studied. It was observed that in antenna size heterogeneity the recovery of 0.5 M NaCl treatment was equal to control while in case of 1 M NaCl treatment recovery has been occurred but not exactly equal to the control. After recovery in 0.5 and 1 M NaCl stressed plant, the relative proportions of a:b:c centers became 70:26:4 and 66:29:5. These results indicate that the damage caused due to high salt stress in antenna size heterogeneity was temporary and
largely reversible, suggesting that the a, b, and c centers were interconvertible. It has been shown that the relative variable fluorescence [(Ft - Fo)/(Fm - Fo)] is not only directly proportional to the number of closed RCs, but it is linearly related to the rate at which centers close (Bennoun and Li 1973). This may be explained by the connectivity of PS II units. PS IIb were characterized by an exponential rise, of the time course of complementary area (CA) whereas PS IIa showed a non-exponential (sigmoidal) rise (Melis and Homann 1976). The exponential shape of this rise for PS IIb was suggested to reflect mutual energetic separation of these PS II. On the other hand, the non-exponential fluorescence rise of PS IIa is generally believed to reflect energetic connectivity between these PS IIs as originally suggested by Joliot and Joliot (1964). The fluorescence rise (FR) curves measured with DCMU and high salt-treated wheat leaves are shown in Fig. 4. The curves are presented by means of relative variable fluorescence (rFvt), which is defined as (Ft - Fo)/(Fm - Fo), where Fo, Fm, and F(t) are the minimal and maximal measured fluorescence intensity at time t, respectively (Lazar et al. 2001). With increase in NaCl concentration sigmoidicity of the curve decreased indicating that high salt stress reduces the connectivity between the PS II units. These results also suggest that the alpha component (sigmoidal phase) of chlorophyll a fluorescence induction curve decreased and beta component (exponential phase) increased. A loss in connectivity also
Fig. 3 Complementary area curves (linear time scale) showing percentage of alpha, beta, and gamma centers in control and salt-treated wheat leaves
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resulting in the reduction of QA. An increase in this ratio indicates that all the QA has been reduced but it is not able to oxidize back due to stress, i.e., the reoxidation of QA is inhibited so that QA cannot transfer electrons efficiently to QB. DIo/RC represents the ratio of the total dissipation of untrapped excitation energy from all RCs with respect to the number of active RCs. Dissipation may occurs as heat, fluorescence and energy transfer to other systems. It is influenced by the ratios of active/inactive RCs. The ratio of total dissipation to the amount of active RCs increased (DIo/RC) due to the high dissipation of the active RCs. These ratios conclusively describe that the number of inactive centers have increased due to high salt stress in wheat leaves.
Fig. 4 Time courses of the DCMU-FR (log time scale) curves measured by PEA (plant efficiency analyzer) in wheat leaves treated with different salt concentration (0.1–1 M NaCl) to measure connectivity between antenna molecules. The curve presented in term of the rFv (t) and start from 10 ls (Fo) and finish at 10 ms. The graphs have time axis in logarithmic scale
indicates that the fraction of closed RCs, i.e., QB nonreducing centers has also increased (Strasser and TsimilliMichael 1998). The antenna and reducing side heterogeneity were studied by energy pipeline models of the photosynthetic apparatus (Kru¨ger et al. 1997; Strasser 1987; Strasser et al. 2000) and specific energy fluxes were calculated. ABS/RC demonstrates average antenna size and expresses the total absorption of PS II antenna chlorophylls divided by the number of active (in the sense of QA reducing) reaction centers. Therefore, the antenna of inactivated reaction centers are mathematically added to the antenna of the active reaction centers. TRo/RC refers only to the active (QA to QA ) centers (Force et al. 2003). As a result of high salt stress, the flux ratios ABS/RC, TRo/RC, and DIo/RC increased (Table 2). The ratio of ABS/RC increased due to inactivation of some active RCs. TRo/RC represents the maximal rate by which an exciton is trapped by the RC
Table 2 Changes in the energy flux ratio in response to high salt stress in wheat leaves NaCl concentration (M) ABS/RC
TRo/RC
DIo/RC
0
3.23 ± 0.02 2.54 ± 0.01
0.69 ± 0.01
0.1
3.38 ± 0.03 2.65 ± 0.03
0.72 ± 0.01
0.2
3.5 ± 0.03 2.67 ± 0.02
0.86 ± 0.01
0.3
3.7 ± 0.03 2.69 ± 0.02
1.13 ± 0.01
0.4
3.9 ± 0.02
2.7 ± 0.03
1.5 ± 0.01
0.5
4.3 ± 0.04
2.8 ± 0.02
1.66 ± 0.02
1.0
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26.25 ± 0.12 3.12 ± 0.03 23.12 ± 0.09
Conclusion From these results we conclude that increase in salt concentration caused an alteration in both the types of PS II heterogeneity. An increase in salt concentration caused an increase in the relative amounts of QB non-reducing centers as well as a change in the relative amounts of a, b, and c centers. Change in response to salt stress led to the conversion of the active a centers into inactive b and c centers. It was observed that the change in reducing side heterogeneity could not be recovered while that of antenna size was recovered. Changes in heterogeneity of PS II seem to be an adaptive mechanism of plants to face harsh environmental conditions. The structure and function of PS II is manipulated temporarily under high salt stress in the form of change in heterogeneity. Acknowledgments PM thanks Council of Scientific and Industrial Research (CSIR), India for the Senior Research Fellowship [09/301/ (0019)09/EMR-I]. Project (INT/ILTP/B-6.27) to AJ by Department of Science and Technology (DST), New Delhi, India is thankfully acknowledged. This work was financially supported, in part, by grants from the Russian Foundation for Basic Research (08-04-00241; 0904-91219-CT). We are also thankful to Prof. Reto J. Strasser for gifting Biolyzer HP 3 Software.
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