The spectra A,B were normalized to the area of under the spectrum, and the arithmetic differences C,D between them were calculated. The presented spectra are representative of 3—5 independent experiments. The difference spectrum for thylakoids from dark-chilling pea leaves — minus — control showed a slight increase in the emission at around and nm accompanied by a simultaneous decrease of fluorescence around nm.
The subsequent photo-activation of leaves led to a partial recovery to the values observed in control conditions Figure 3C. The intensities of these bands decreased upon photo-activation, which suggested a partial recovery of CP complexes organization during photo-activation.
However, the difference spectrum calculated from the emission spectra for thylakoids isolated from the photo-activated and dark-chilled leaves revealed a positive band around nm, indicating the formation of LHCII aggregates Figure 3D. The FTIR spectroscopy is a useful method to analyze the relationships between lipids and proteins, as well as the changes in the protein secondary structure.
The relative ratio of these band intensities, in spectrum normalized at cm —1 , reflects the relative lipid to protein ratio Szalontai et al. Figure 4. C Presents the difference spectrum between pea and bean control spectra. Lower panels show the difference spectra between control and stressed thylakoids for pea D and bean E , respectively.
The presented spectra are representative of 3 independent experiments. The difference FTIR spectrum for thylakoids of dark-chilled pea leaves dark-chilled — minus — control showed a slight decrease in the band assigned to lipids and in the band corresponding to the interactions between neighboring membrane proteins.
Subsequent photo-activation of leaves did not change the pattern of the difference spectra photo-activated — minus — control Figure 4D. The positive band around cm —1 was observed for both thylakoids isolated from chilled and subsequent photo-activated leaves Figure 4E , suggesting noticeable changes in lamellar interactions between proteins. Figure 5. Profiles of the main four classes of lipids extracted from thylakoids isolated from pea A and bean B control red , dark-chilled blue and subsequent photo-activation orange leaves.
Lower panels present the double bond index DBI for corresponding lipid classes of pea C and bean D thylakoids. The double-bond index DBI indicates the average number of double bonds in the fatty acid chains of a lipid molecular species; higher values of DBI correspond to the increase in membrane fluidity Zheng et al.
Furthermore, the relative content of the high melting point PG and molecular species was almost five times higher in bean than in pea thylakoids Supplementary Table 2.
The average acyl chain length ACL is the second indicator of the physical properties of the membrane — longer chains of fatty acids are related to lower fluidity of membrane Zheng et al. After the dark-chilling treatment, the relative content of galactolipids and the ratio of lipid classes changed significantly in bean thylakoids only Figures 5A,B.
The photo-activation did not significantly influence the lipid composition of both species thylakoid membranes compared with dark-chilling conditions Figures 5A,B. Carotenoids play different roles in the thylakoid membranes they can i participate in photochemical reactions and dissipate the excess of light energy, ii effectively quench the free radicals and iii modify the fluidity of the lipid phase Domonkos et al.
Therefore, the determination of the carotenoid composition is important in assessing the physical properties of thylakoid membranes. The content of the main carotenoids in control samples was significantly different in thylakoids from pea and bean leaves. The relative content of neoxanthin was similar in both species, whereas the violaxanthin was slightly more abundant in pea thylakoids. The content of zeaxanthin and antheraxanthin did not exceed 0.
Figure 6. Carotenoid compositions of pea A and bean B thylakoids isolated from control red , dark-chilled blue and subsequent photo-activation orange leaves. The photo-activation of leaves of both species did not change the proportion of carotenoids in comparison with data obtained for dark-chilled leaves Figures 6A,B. The protein patterns of the thylakoid membrane fractions isolated from control, dark-chilled and photo-activated pea and bean leaves were analyzed using SDS-PAGE and fluorescence staining.
In pea, there were no significant qualitative and quantitative changes in protein abundance in dark-chilled and photo-activated samples Figure 7A , left panel. In contrast, in bean, dark-chilling induced multiple changes in the protein pattern of the thylakoid membranes Figure 7B , left panel, arrowheads.
Figure 7. Changes of thylakoid protein and phospho-protein composition after dark-chilling and photo-activation in pea and bean plants. The quantitative analysis of selected phospho-proteins of pea C and bean D thylakoids. In pea, dark-chilling induced a significant decrease in D1, D2, Lhcb1, and Lhcb2 phosphorylation and a slight increase of CP43 phosphorylation Figure 7C compared with control conditions. Such a change in thylakoid protein phosphorylation was typical for the thylakoids isolated from plants directly after the night period.
In contrast, in bean, the dark-chilling induced 4-fold increase in the phosphorylation of LHCII major antenna proteins and 1. In both species, photo-activation of dark-chilled caused the return of protein phosphorylation status to the values of control samples Figures 7C,D.
Details of the thylakoid network structure were analyzed using both CLSM, reveling the distribution of grana stacks and their organization within the whole chloroplast Figure 8A , as well as TEM showing the detailed structure of stacked grana and unstacked stroma thylakoids Figures 8B—D.
Figure 8. Structural changes of thylakoid network after dark-chilling and photo-activation in pea and bean plants. The images of intact chloroplasts visualized by confocal microscopy; red fluorescence spots roughly correspond to grana size and their position inside the chloroplast A.
Electron micrographs of mesophyll chloroplasts B and grana enlargement showing changes in thylakoid network regularity and fluctuation in stacking repeat distance SRD C. Therefore, the spot distribution corresponds to the position of grana stacks in the chloroplast Rumak et al.
In pea, large and well-distinguished spots were registered as opposed to smaller and more blurry fluorescence discs present in bean chloroplasts Figure 8A. Such differences were even more profound after the dark-chilling treatment showing a disorganized thylakoid network in bean plants. In the case of pea, no significant changes in general features of the thylakoid network structure were registered Figure 8A. In both species, photo-activation did not change the chloroplast fluorescence image significantly compared to the one registered after dark-chilling Figure 8A.
More structural details were revealed by electron microscopy analysis of fixed leaf samples Figures 8B,C. Chloroplast cross-sections of control samples showed a significant difference in grana distribution between both analyzed species. Moreover, the disturbance in such regular arrangement was visible, with multiple shifts of grana stacks position. After the dark-chilling treatment, swelling of the chloroplast stroma was registered in both examined species. After the photo-activation stroma swelling was visible in bean chloroplasts only Figure 8B.
Low temperature did not affect the pea thylakoid network organization visible at the level of the whole chloroplast section, while in bean, the thylakoid network disorganization proceeded continuously after dark-chilling and photo-activation Figure 8B. One of the important ultrastructural grana features is the degree of thylakoid stacking, expressed by stacking repeat distance SRD , defined as the distance between adjacent partition gaps in the stacks Kirchhoff et al.
In control plants, no significant differences in the SRD value around 19—20 nm were registered between both analyzed species Figure 8D. Dark-chilling treatment induced a substantial decrease in the SRD value 15—16 nm both in pea and bean. Although photo-activation caused an increase in the SRD value in both species, full recovery of grana stacking SRD around 19 nm was observed in pea grana only. In the case of bean, only partial SRD increase was observed, reaching values of around 17 nm.
The diversity of the chloroplast membrane network structure organized into stacked, marginal and unstacked regions is generally explained by the presence of a lateral heterogeneity of CP complexes and in consequence, different steric and physicochemical interaction between membranes Jia et al.
The role of the lipid phase and lipid-protein interactions in the determination of the thylakoid structure is less explained Garab et al.
Moreover, the relationship between the stress-induced changes in the thylakoid structure and the changes in their protein or lipid composition, as well as the arrangement of the CP complexes is unclear. Since the lipid composition of thylakoids, especially the degree of thylakoid lipids desaturation, is related to plant sensitivity to chilling Kenchanmane Raju et al.
We have analyzed the two plant species belonging to two separate groups due to their different responses to chilling conditions and revealing different thylakoid network structures. The observations with the use of TEM and CLSM showed that chloroplasts in pea contain larger stacked areas than in bean, in which the stacked regions are less distinguished Figure 8.
It was established before that observed ultrastructural differences between both species depend on the diversity of the thylakoid protein composition and arrangement, and in consequence, in different protein-protein interactions Rumak et al. The observed differences in the thylakoid structure and the arrangement of the CP complexes might be, moreover, partially explained by the particular lipid composition and lipid-protein interactions of the thylakoid membrane matrix of CT pea and CS bean plants analyzed in this study.
However, the sum of these anionic lipids is similar in both analyzed species Figure 5 and Supplementary Table 2. Such results are in line with studies on lipid deficient plants pointing to the importance of the maintenance of the sum of the anionic lipids in thylakoid network formation and fitness Yu and Benning, ; Kobayashi et al. Another factor influencing thylakoid membrane fluidity is the degree of thylakoid lipid desaturation. Polyunsaturated fatty acids building acyl chain of galacto- and phospholipids stabilize the liquid-crystalline phase of the membrane.
Moreover, the and PG molecules are high-melting-point molecular species which, under the in vitro conditions, undergo the liquid-crystalline to gel phase transition at room temperature i. This effect is not directly observed in the thylakoid membranes because of the predominant abundance of desaturated lipids.
However, the positive correlation between the amount of these PG species and sensitivity to low-temperature was found in a wide variety of plants and transgenic lines Szalontai et al. These data indicate higher fluidity of the thylakoid membranes in CT pea compared with CS bean and agree with the observation that the higher desaturation level of lipids is correlated with the higher resistance to chilling Los et al.
The lower value of the ACL of the total lipid pool correlates with the higher fluidity of the thylakoid membranes Zheng et al. Chloroplast lipid metabolism involves the activity of many types of deacylating enzymes Matos and Pham-Thi, Significantly higher activity of galactolipase in CS than in CT species was reported previously Kaniuga, The galactolipase isolated from bean chloroplasts had almost ten times higher activity compared with pea one Gemel and Kaniuga, , and these activities were associated with two-times higher accumulation of FFA registered in bean chloroplasts Gemel and Kaniuga, ; Garstka et al.
The accumulated FFA might influence the structure of thylakoids, however, the FFA undergo enzymatic and non-enzymatic peroxidation, which might decrease its detergent-like effect Garstka et al. Free hydrophobic carotenoids, not bound to proteins, are embedded in membranes and can modify the physical properties of the lipid bilayer. Xanthophylls that contain polar groups at the two ends of the molecule and are positioned across the bilayer, cause the rigidification of membranes.
Apart from the lipids forming the thylakoid membrane matrix, lipids are bound inside the protein scaffold of supercomplexes playing an important role in the stabilization of their structure and maintaining their photochemical functions Jones, ; Domonkos et al. Such an ordered phase is probably larger than the bulk phase which contains lipids with higher fluidity Azadi Chegeni et al. Therefore, it might be possible that maintaining the optimal fluidity of thylakoids depends more on lipid-protein interactions than lipid composition alone.
The relationship between the supramolecular membrane structure and the photochemical reactions can be analyzed by temperature dependencies of Chl a fluorescence emission measured in F 0 or steady-state Wentworth et al. The breakpoint in the linear temperature-dependent plot indicates the changes in the interactions between CP complexes due to a temperature-induced structural transformation.
The temperature-dependent plot of Chl fluorescence for thylakoids isolated from control pea and bean leaves differ in the number of breakpoints; two and three phases of the fluorescence decrease in pea and bean, respectively Figures 2A,D.
The second and the third phase of the fluorescence decrease in bean revealed a similar slope as analogous phases for pea Supplementary Table 1 , indicating the similar interactions needed for the rearrangement of CP complexes. The temperature-dependent changes in the fluorescence decrease arise from small changes in the conformation of CP complexes.
Such changes may comprise alterations in the hydrogen and van der Waals interactions induced both by protein-protein and lipid-protein interactions. The breakpoint of the temperature-dependent plot might be correlated with a transition temperature of the lipid phase Kovacs et al. Our data Figure 2 showed that fluidity of bean thylakoid membranes is lower than in pea what indicates that at low temperatures, the possibility of gel phase formation is higher in bean thylakoids.
Therefore, we propose that the one-breakpoint plot for pea thylakoids might be attributed to the phase transition between liquid-crystalline and disorder phases, whereas the two-breakpoint plot for bean thylakoids is related to the transition from gel-phase to liquid-crystalline and further to disorder phase Los et al.
Species-dependent regulation of the thylakoid membrane fluidity is considered as an evolutionary adaptation mechanism to cope with high or low-temperature stress Zheng et al. The efficiency of photochemical reactions, among different factors, is regulated by the mobility of the electron transport chain components in the lateral plane of thylakoid membranes.
To maintain appropriate transport within the lipid matrix in low temperatures its fluidity has to be preserved.
Under dark-chilling and subsequent photo-activation at moderate light both in pea and bean, there is no decrease of the chlorophyll amount, no changes in Chl a to Chl b ratio Garstka et al. These data indicate that CP complexes are not degraded under applied experimental conditions.
However, data obtained by mild-denaturing electrophoresis Garstka et al. Therefore, the lack of significant changes in the photochemical parameters and the course of the fluorescence induction curves Figure 1 can be directly related to the stable behavior of pea supercomplexes under dark-chilling and subsequent photo-activation Figures 3 , 4.
Moreover, the presence of phosphorylated LHCII pool causes the increase of the negative charge of the stromal side of the thylakoid membrane, which changes the balance between the attractive and repulsion forces between neighboring CP complexes, and therefore alters their supramolecular organization Puthiyaveetil et al. Furthermore, only the partial recovery of the bean photochemical activity after photo-activation Figure 1 can be related to incomplete restoration of the native structure of CP complexes Figures 3 , 4 manifested mainly by the appearance of the aggregated LHCII Figure 3.
However, in pea, the overall fluidity of thylakoid membranes remains similar to the control conditions, which is visible in the same course of the temperature-dependent plots for the control and dark-chilling plants Figures 2A—C and Supplementary Table 1.
Probably, the high level of lipid desaturation in control pea Figure 5C retains the optimal fluidity at low temperatures and prevents the loss of the CP complexes functionality in dark-chilled plants Figure 1.
In contrast, the substantial changes in lipid composition are observed after dark-chilling of bean leaves. In various plant species, the long-term cold-adaptation includes a decrease in the MGDG level, probably because lower level of the MGDG stabilizes the membrane bilayer phase at low temperatures Zheng et al. Simultaneously, the rigidity of membranes induced by low-temperature is alleviated by the increase in the DBI index and a decrease in the ACL index Zheng et al.
It was previously proposed that the thylakoid lipids of the CT plants remain in the liquid-crystalline phase whereas thylakoids in the CS species enter the gel phase at chilling temperatures, mainly due to different levels of lipid desaturation Szalontai et al. The level of lipid saturation is related to the activity of desaturases and transferases regulated directly or non-directly by factors connected with the C-repeat binding factor signaling pathway Thomashow, ; Kenchanmane Raju et al.
In thylakoids isolated from dark-chilled bean leaves the DBI and ACL indexes are maintained at the same level as in control thylakoids Figure 5 and Supplementary Table 2 , which exclude activation of typical long-term adaptation processes during low-temperature treatment in bean.
Dark-chilling-induced changes in bean thylakoids, in lipid composition in particular, substantially alters the membrane properties, which is reflected by a drastic change in the course of the temperature-dependent plot; the three-phase plot is converted to a single-phase one Figures 2D,E. The temperature-dependent plot without breakpoint indicates impairment of the lipid-protein interactions or lack of lipid phase transition in the measured temperature range.
It is probably related to the detergent-like effect caused by the accumulation of FFA in thylakoids, which is typical for CS plants under dark-chilling stress Kaniuga, Under these conditions, the FFA level in bean thylakoids increases two times and remains unchanged in pea Garstka et al.
Such variable response is correlated with higher activity of galactolipase in bean than in pea plants Gemel and Kaniuga, Photo-activation of dark-chilled leaves of CS plants results in a decrease of FFA to the level observed in control plants Garstka and Kaniuga, ; Kaniuga, probably due to the increase of peroxidative reactions Garstka et al.
This effect might be a reason why in photo-activated bean thylakoids we observed the restoration of the three-phase temperature-dependent plot with breakpoints characteristic for the control thylakoids Figures 2D,F without significant changes in the ratios of lipids and carotenoids Figures 5 , 6. Moreover, changes in membrane properties of bean thylakoids during dark-chilling and photo-activation explain the reversible association of stromal proteins Rubisco and PcLOXA lipoxygenase Figure 7 ; Mazur et al.
In contrast to pea, dark-chilling induces significant alternation in the lipid phase, thylakoid protein phosphorylation status, and arrangement of CP complexes in bean Figures 3 , 5 , 7 which result in increased disorganization of the thylakoid network visible at the ultrastructural level Figure 8. The photo-activation of bean leaves considerably restores the physical properties of membranes Figure 2 and partially the structure and photochemical activity of CP complexes Figures 1 , 3 , 7.
However, the disorganized arrangement of the thylakoid network is still visible Figure 8. Such a specific supramolecular thylakoid structure in combination with the aggregation of LHCII induced by photo-activation Figures 3 , 4 makes a return to initial thylakoids organization difficult. The SRD value, which is one of the parameters describing the extent of grana stacking, decreases in dark-chilled pea thylakoids which is correlated with a decrease of LHCII phosphorylation Figures 7 , 8.
This indicates that there is no simple correlation between grana stacking and LHCII phosphorylation level in dark-chilling conditions. Under dark-chilling conditions, the bean thylakoid network comprises multiple small grana connected via many stroma lamellae Figures 8B,C ; Rumak et al.
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